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MONITORING OF SUBGINGIVAL
BACTEROIDES GINGIVALIS AND
ACTINOBACILL US ACTINOMYCE TEMCOMITANS
IN THE MANAGEMENT OF ADVANCED
PERIODONTITIS
L.A. CHRISTERSSON 1 *, B.G. ROSLING 2 , R.G. DUNFORD 1 , U.M.E. WIKESJO 1 ,
JJ. ZAMBON 1 , AND RJ. GENCO 1
Departments of Oral Biology and Periodontology, Periodontal Disease Clinical Research Center2, School
of Dental Medicine, State University of New York at Buffalo, Buffalo, New York 14214, U.S.A.; and
The Department of Periodontology, Public Dental Services2, Helsingborg, Sweden
Adv Dent Res 2(2):382-388, November, 1988
ABSTRACT
n a series of clinical trials involving 79 adult periodontitis patients, we evaluated the clinical and microbiological effects of H O , NaHCO , and a commercially available povidine solution, as adjuncts to
I
mechanical periodontal debridement. Each trial included a placebo as a control. The healing response was
2
2
3
monitored clinically by measurement of changes in probing attachment levels after treatment. The current
report includes data from single-rooted teeth only.
In general, healing in severely advanced periodontal lesions (initial pocket depth > 7 mm) was enhanced by
the use of the listed topical antimicrobial agents administered subgingivally during mechanical debridement.
Correlations were sought between changes in probing attachment levels 12 months after treatment, and the
presence of subgingival B. gingivalis and A. actinomycetemcomitans in the periodontal lesions. For a total of 428
lesions included in this report, B. gingivalis was detected in 53.1% of lesions showing probing attachment loss
(>1.5 mm), but in only 4.7% of lesions showing gain (> 1.5 mm). Either B. gingivalis or A. actinomycetemcomitans
was detected in 70.1% of the lesions showing loss and in only 4.8% of those showing gain. These studies
indicate the benefits of the adjunctive antimicrobial therapy described, and the usefulness of specific microbiological monitoring as an aid to clinical measurements in the evaluation of success or failure of treatment of
chronic adult periodontitis.
PERIODONTITIS: AN INFECTIOUS DISEASE
Studies performed several decades ago have clearly
defined the relationship between dental plaque and
the diseases gingivitis and periodontitis. More recent
studies have specifically indicated Gram-negative organisms as the principal micro-organisms involved in
their pathogenesis (Newman and Socransky, 1977;
Socransky, 1977; Slots, 1979; van Palenstein Helderman, 1981). For example, Bacteroides gingivalis has been
implicated as a key organism in severe forms of adult
Presented at the Sunstar Portside Symposium, November 14-15,
1986, Kobe, Japan
*To whom correspondence should be addressed
382
periodontitis (Tanner et al, 1979; Slots, 1982; Slots
and Genco, 1984), and is also reported to be predominant in isolated cases of juvenile periodontitis (Wilson et al., 1985). Actinobacillus actinomycetemcomitans
is generally recognized as the main infectious agent
in localized juvenile periodontitis (Slots et al., 1980;
Zambon et al., 1983; Mandell, 1984; Zambon, 1985)
and is also found in adult periodontitis patients (Slots
and Genco, 1984). Eikenella corrodens and Capnocyto-
phaga sp. are also prominent members of the subgingival flora in pockets of juvenile periodontitis patients
(Newman and Socransky, 1977; Mandell, 1984). Other
organisms often found in subgingival plaque samples
from periodontal lesions include Eubacterium, Haemophilus, Wolinella, Fusobacterium, and Selenomonas;
Vol. 2 No. 2
MONITORING OF B. gingivalis AND A. actinomycetemcomitans
however, their role in periodontal disease is as yet
not clear.
The concept that periodontal diseases may be caused
by specific micro-organisms — i.e., organisms not regularly found in the healthy gingival sulci and/or oral
cavity —suggests the possibilities of using these criteria in the monitoring of periodontal treatment (Genco
et al, 1986, 1988). Furthermore, recent studies have
reported on the development of methodologies which
will provide the technology for rapid assays useful
for this purpose (Bonta et al, 1985; Zambon et al.,
1985).
383
process over an extensive period of time related to
the initial severity of the disease (Badersten, 1984).
Regardless of the therapy employed, the outcome in
gain of attachment level is reported to be related to
the degree of plaque control and the trauma from the
technique involved. Furthermore, long-term evaluations of periodontal therapy have suggested that an
appropriate maintenance regime, controlling for reinfection, is more important than the regime used to
eliminate the initial periodontal infection (Lindhe and
Nyman, 1984).
MANAGEMENT OF PERIODONTAL
DISEASES AS INFECTIOUS DISEASES
ADJUNCTIVE ANTIMICROBIAL AGENTS
IN THE MANAGEMENT OF
THE PERIODONTAL INFECTION
Presently, the emphasis in periodontics is directed
toward three major goals: (1) treatment of the disease, i.e., elimination of the infection per se; (2) reconstruction of tooth support, i.e., regeneration of
lost periodontal tissues; and (3) maintenance of periodontal health.
Since periodontal diseases are primarily infections,
an anti-infectious approach is the main choice of therapy. Different ways to treat periodontitis have been
known for decades. Since complete knowledge of the
cause of disease is not available, clinical treatment
modalities have often been directed toward technical
solutions, such as pocket elimination and reshaping
of the diseased alveolar processes by osseous surgical
procedures. Today, it is reasonable to consider replacing these technical procedures with therapeutic
modalities which are directed to reduction, or elimination, of the infectious agents causing the disease.
The importance of plaque control measures and
mechanical debridement in various forms of surgical
and non-surgical periodontal therapy has been very
well-documented in clinical trials over the years
(Ramfjord et al, 1973,1975; Zamet, 1975; Lindhe and
Nyman, 1975,1984; Nyman et al, 1975,1977; Rosling
et al, 1976a, b; Waite, 1976; Knowles et al, 1979,1980;
Axelsson and Lindhe, 1981a, b; Badersten et al, 1981,
1984a, b; Hill et al, 1981; Pihlstrom et al, 1981, 1983;
Lindhe et al, 1982; Isidor et al, 1984). Results from
these studies clearly indicate that the progressive destruction of periodontal support can be arrested, regardless of the specific techniques used for subgingival
instrumentation. Also, these studies show that it is
possible to eliminate gingival inflammation and progressive periodontitis by combining periodontal therapy with a carefully exercised and supervised
maintenance program.
Numerous studies have shown the potential of
scaling and root planing procedures alone to resolve
even advanced periodontitis (Zamet, 1975; Waite, 1976;
Hill et al, 1981; Lindhe et al, 1982, 1984; Garrett,
1983; Rosling et al, 1983a, b; Badersten et al, 1984a;
Isidor et al, 1984). However, the healing following
non-surgical therapy is suggested to be a gradual
Since access to most of the infecting organisms in
periodontal disease can be accomplished through the
orifice of the periodontal pocket, application of antimicrobial agents locally into the periodontal pocket
represents a logical alternative for management of the
periodontal infection. Also, the use of antimicrobial
agents administered systemically or topically to enhance the result of mechanical subgingival debridement is clinically attractive. However, the potential
risk for uncontrolled adverse reactions and bacterial
drug resistance to antibiotics has to be considered
(Genco, 1981; Baker et al, 1985).
In order for the risks involved to be minimized,
antimicrobial agents with low toxicity and a broad
antimicrobial spectrum have been tested and found
to enhance the effects of mechanical subgingival debridement (Rosling et al, 1983a, b, 1985, 1986; Christersson et al, 1985a).
In the present report, we describe four clinical
treatment studies designed to evaluate the effects of
adjunctive topical antimicrobials on the changes in
clinical attachment level after periodontal therapy. The
patient groups included a total of 79 patients, 45 males
and 34 females, with an average age of 43 years (Table
1). All patients were systemically healthy and exhibited moderate to severe adult periodontitis. Periodontal examinations were performed at baseline, 6,
and 12 months postoperatively, by means of probing
pocket depth and probing attachment level (Rosling
et al, 1983a).
The clinical protocols were similar for all four studies and were designed to evaluate the effects of topical antimicrobial agents as adjuncts to scaling and
root planing procedures. Briefly, all patients received
three visits of oral hygiene instructions accompanied
by supragingival debridement and professional tooth
cleaning. Then, subgingival debridements were performed under local anesthesia, with the additional
delivery of a test compound or a placebo. The test
antimicrobial compounds were: (Study I) a povidine
solution (Jodopax®, Ferrosan, Malmo, Sweden) with
a final concentration of 0.05% active iodine; (Study
384
Adv Dent Res November 1988
CHRISTERSSON et al.
TABLE 1
NUMBER, AGE, AND GENDER OF ADULT
PERIODONTITIS PATIENTS INCLUDED IN FOUR
CLINICAL TREATMENT STUDIES
Study3
Gender Ratio
Number of
Subjects Mean Age Age Range (males/females)
19
18
18
24
44
41
44
44
28-61
32-61
29-65
33-56
12/7
II
III
IV
Total
79
43
28-65
45/34
I
a
8/10
11/7
14/10
Study I: Non-surgical treatment 4- topical iodine application.
Study II: Non-surgical treatment + topical baking soda
application.
Study III: Non-surgical treatment + topical hydrogen peroxide application.
Study IV: Non-surgical treatment + topical baking soda
and hydrogen peroxide application.
II) a baking soda "tooth powder" (NaHCO 3 , Church
& Dwight, Princeton, NJ); (Study III) a 3% hydrogen
peroxide solution (Swan® 3% H 2 O 2 , Cumberland,
Smyrna, TN); and (Study IV) a combination of baking
soda (ACO, Sundbyberg, Sweden) and hydrogen
peroxide (ACO, Sundbyberg, Sweden). The test compounds and respective placebos were, for all groups,
professionally administered at the time of subgingival
debridement. The iodine, hydrogen peroxide, and
saline (placebo) solutions were administered by connection of a pressurized tank to the cooling system
of the ultrasonic unit. The baking soda, the baking
soda + hydrogen peroxide mixture, and their corresponding placebos (calcium-diphosphate powder and
calcium-diphosphate + saline) were administered as
a "slurry" and applied directly into the gingival pockets at the time of subgingival debridement. These
compounds were also professionally applied at each
postoperative visit. In addition, the patients used their
respective compound at home as a substitute for regular toothpaste.
In this report, we will describe the overall results
of changes in probing attachment level and the correlation of these changes with subgingival B. gingivalis and A. actinomycetemcomitans to evaluate the
usefulness of microbiological tests in monitoring success or failure of therapy. Teeth included in this presentation were all non-surgically treated, with
subgingival debridement achieved by ultrasonic debridement alone (Odontoson®, Goof A/S, Ftyrsholm,
Denmark) in Studies I and III, and debridement with
hand instrument alone in Studies II and IV. Periodontal healing was ensured by biweekly professional tooth cleaning for the first three months
postoperatively (Rosling et al., 1983a).
The baseline values for the percent of pockets 5 mm
or greater on single-rooted teeth ranged from 27r.7%
to 49.6%. The average percent of these deeper pockets was lowered to between 2.3% and 17.4% at the
12-month examination (Table 2). Reduction in the
proportions of deeper pockets was approximately the
same in test as in placebo groups, indicating the ability of the non-surgical regimes to manage moderate
to severe periodontal disease. The clinical measurements also indicated a gain in the overall average
probing attachment level for all groups (data not
shown).
The proportions of periodontal lesions, which were
initially 7 mm or greater in pocket depth, that gained
probing attachment level were generally greater for
the test groups than for the placebo groups. In the
test groups, the proportions of deep sites gaining
probing attachment levels of 2 mm or more ranged
between 53% and 81%. The corresponding values for
the placebo groups were 39% and 55% (Table 3). Conversely, the placebo groups showed higher proportions of sites losing probing attachment level compared
with the test groups (Table 3). These results further
substantiate previous reports indicating that adjunctive antimicrobial therapy can result in an additional
gain in probing attachment level in deep pockets,
compared with that achievable with mechanical scaling and root planing alone.
BACTERIAL MONITORING AS A SPECIFIC
PARAMETER IN PERIODONTAL THERAPY
Studies have clearly indicated a strong relationship
between elimination of A. actinomycetemcomitans and
healing of periodontal defects in localized juvenile
periodontitis patients (Slots and Rosling, 1983; Christersson et al., 1985b, 1986; Kornman and Robertson,
1985; Mandell et al., 1986), and hence, therapy can be
directed toward elimination of A. actinomycetemcomitans. Studies on the effects of systemic antimicrobial
therapy alone further substantiate this concept
(Christersson et al., 1985c, 1986; Christersson, 1986).
Monitoring black-pigmented Bacteroides in adults has
revealed a relationship between recurrent or continuing periodontitis and detectable levels of B. gingivalis at examinations 12 months after therapy (Rosling
et al., 1983b, 1986; Slots et al., 1985).
The initially promising results from clinical studies
utilizing bacterial monitoring, and the development
of rapid microbiological techniques (Bonta et al., 1985;
Zambon et al., 1985), may represent the advent of a
new era in clinical periodontology.
For this presentation, we analyzed the results of specific microbiologic monitoring of periodontal healing in
the four studies. B. gingivalis and A. actinomycetemcom-
itans were assessed as specific indicators of success or
failure in treatment of individual deep lesions. The
presence or absence of B. gingivalis was analyzed for a
total of 428 subgingival plaque samples obtained 12
Vol. 2 No. 2
MONITORING OF B. gingivalis AND A. actinomycetemcomitans
385
TABLE 2
PERCENT OF MEASUREMENT SITES WITH A PROBING POCKET DEPTH > 5 mm AT BASELINE, 6-MONTH, AND
12-MONTH EXAMINATIONS
Study3
Group
Sites
Baseline (%)
6 Months (%)
12 Months (%)
I
test
placebo
test
placebo
test
placebo
test
placebo
510
480
516
526
962
935
546
504
42.2
36.7
27.7
48.7
34.8
28.1
48.0
49.6
2.7
5.8
5.2
5.3
5.3
2.3
11.0
17.3
7.2
5.6
6.4
6.1
14.3
16.7
17.4
13.3
II
III
IV
a
Study
Study
Study
Study
I: Non-surgical treatment + topical iodine application.
II: Non-surgical treatment + topical baking soda application.
III: Non-surgical treatment + topical hydrogen peroxide application.
IV: Non-surgical treatment + topical baking soda and hydrogen peroxide application.
TABLE 3
DISTRIBUTION (%) OF MEASUREMENT SITES RELATED TO CHANGES IN PROBING ATTACHMENT LEVEL AT
THE 12-MONTH EXAMINATION FOR SITES WITH INITIAL PROBING POCKET DEPTH > 7mm
Studva
Test Groups
Changes in Probing Attachment Level
(% sites)
>-2 mm
-1,0, + l m m
6
20
19
43
42
80
81
54
53
0
15
5
3
45
46
44
46
55
39
51
50
2
31
67
6
45
49
I
II
III
IV
0
0
Average(%)
a
Study
Study
Study
Study
> +2 mm
Placebo Groups
Changes in Probing Attachment Level
(% sites)
>-2 mm
-1,0, 4-lmm
>+2mm
r\
D
I: Non-surgical treatment -f topical iodine application.
II: Non-surgical treatment + topical baking soda application.
III: Non-surgical treatment + topical hydrogen peroxide application.
IV: Non-surgical treatment + topical baking soda and hydrogen peroxide application.
months after periodontal therapy for patients in Studies
I, II, III, and IV. The presence or absence of A. actinomycetemcomitans was analyzed for a total of 265 samples
from patients in Studies I, III, and IV. All subgingival
plaque samples were obtained with the paper-point
technique (Rosling et al, 1983a). Presence of B. gingivalis and A. actinomycetemcomitans was assessed by the
indirect immunofluorescence method (Bonta et al, 1985;
Zambon et al, 1985).
Overall, B. gingivalis was found in 15.2% of the
lesions, and A. actinomycetemcomitans in 11.7%, 12
months post-treatment (Table 4). Of the 428 lesions
monitored for B. gingivalis, 172 (40.2%) gained probing attachment level (> 1.5 mm) and 32 (7.5%) lost
attachment (> 1.5 mm) between baseline and the 12month examination. Of the 172 lesions which gained
attachment, eight (4.7%) were positive for B. gingivalis. In contrast, 17 (53.1%) out of the 32 lesions that
lost probing attachment level (> 1.5 mm) were pos-
itive for B. gingivalis. Forty (17.9%) of 224 periodontal
lesions which showed only small or no changes in
probing attachment level ( - 1 , ±0, + 1 mm) were
also positive for this micro-organism (Table 5).
The relationship between presence of A. actinomycetemcomitans and changes in probing attachment level is
presented in Table 6. It can be seen that three (2.9%)
of the 104 lesions that showed gain in probing attachment level (> 1.5 mm) harbored A. actinomycetemcomitans and, conversely, that seven (29.1%) of the 24 lesions
which lost attachment harbored the organism.
In conclusion, a high proportion of lesions losing
probing attachment level was found to harbor B. gingivalis and/or A. actinomycetemcomitans. The change in
probing attachment levels and the results of the microbiological monitoring were strongly correlated (p
< 0.001).
To illustrate the usefulness of a bacteriological "test",
the Fig. depicts the data from three of the four studies
386
Adv Dent Res November 1988
CHR1STERSS0N et al.
TABLE 4
NUMBER OF SUBGINGIVAL PLAQUE SAMPLES POSITIVE FOR B. gingivalis AND A. actinomycetemcomitans AT THE 12MONTH EXAMINATION IN FOUR CLINICAL TREATMENT STUDIES
Study 3
Number of
Samples
Number of Samples
Positive for
Number of Samples
Positive for
A. actinomycetemcomitansb
B. gingivalisb
(10.9)c
(12.3)
(14.0)
(24.2)
I
II
III
IV
73
163
93
99
8
20
13
24
Total
428
65 (15.2)
8 (10.9)
N.A.d
18 (19.4)
5 (5.1)
31 (11.7)c
a
Study I: Non-surgical treatment + topical iodine application.
Study II: Non-surgical treatment 4- topical baking soda application.
Study III: Non-surgical treatment + topical hydrogen peroxide application.
Study IV: Non-surgical treatment + topical baking soda and hydrogen peroxide application.
b
Determined by indirect immunofluorescence microscopy (Bonta et al, 1985; Zambon et ah, 1985).
c
Values within brackets describe percent of samples.
d
Not Available.
e
Value within brackets describe percent of samples positive out of 265 samples available.
TABLE 5
RELATIONSHIP BETWEEN PRESENCE OF
SUBGINGIVAL B. gingivalis AND CHANGE IN
PROBING ATTACHMENT LEVEL AT THE 12-MONTH
EXAMINATION
Number of Positive/Total Number Tested
Subgingival Plaque Samplesb by Change, Gain
( + ) , or Loss ( - ) in Probing Attachment Level
- 1.0 to
Study3
^ - 1.5 mm
+ 1.0 mm
^ + 1.5 mm
I
4/8
4/28
0/37
II
1/8
6/68
13/87
III
0/2
11/62
2/29
IV
12/14
12/47
0/38
17/32
40/224
8/172
a
Study I: Non-surgical treatment + topical iodine application.
Study II: Non-surgical treatment + topical baking soda
application.
Study III: Non-surgical treatment + topical hydrogen
peroxide application.
Study IV: Non-surgical treatment + topical baking soda
and hydrogen peroxide application.
b
Determined by indirect immunofluorescence microscopy
(Zambon et ah, 1985).
(265 monitored sites). The "test 7 ' using only B. gingivalis identified 66.7% of the lesions labeled "losers",
those periodontal lesions showing loss of 1.5 mm or
more as determined by probing attachment measurements. Only 1.9% of the "gamers", those lesions
showing an increase of 1.5 mm or more in probing
attachment level, showed presence of B. gingivalis
(Fig.). The g r o u p of l e s i o n s c o n s i d e r e d " u n changed", based upon measured change in average
TABLE 6
RELATIONSHIP BETWEEN PRESENCE OF
SUBGINGIVAL A. actinomycetemcomitans AND CHANGE
IN PROBING ATTACHMENT LEVEL AT THE
12-MONTH EXAMINATION
Number of Positive/Total Number Tested
Subgingival Plaque Samples13 by Change, Gain
( + ), or Loss ( - ) in Probing Attachment Level
- 1.0 to
Study 3
I
III
IV
^ - 1.5 mm
4/8
0/2
3/14
4- 1.0 mm
4/28
15/62
Z/47
^ + 1.5 mm
0/37
3/29
0/38
7/24
21/137
3/104
a
Study I: Non-surgical treatment 4- topical iodine application.
Study III: Non-surgical treatment + topical hydrogen
peroxide application.
Study IV: Non-surgical treatment 4- topical baking soda
and hydrogen peroxide application.
b
Determined by indirect immunofluorescence microscopy
(Bonta et al., 1985).
level of > - 1.5 mm to > + 1 . 5 mm over 12 months,
exhibited evidence of the presence of B. gingivalis in
19.7% of the lesions. The clinical and microbiological
evaluations were in "agreement" for 86% of the lesions.
The 14% of "disagreement" should not necessarily be
classified as "false" results; they may be interpreted as
an indication of the need for further therapy.
The "test" which includes the presence of either B.
gingivalis or A. actinomycetemcomitans gave similar re-
sults, however, with a slightly higher proportion
(70.1%) of the "losers" identified as microbiologically
positive. The use of additional marker organisms may
Vol. 2 No. 2
A.
e. gingivalis
"losers"
D
MONITORING OF B. gingivalis AND A. actinomycetemcomitans
387
REFERENCES
"unchanged"
B. gingivalisandlor
' A. actinomycetemcomitans
"unchanged"
Fig. —Results of the bacteriological "tests", applied to data obtained 12 months after treatment, for 265 monitored periodontal
lesions. The percent values indicate the proportion of lesions, within
each category, positive for respective organisms and/or combinations of organisms. "Losers" indicates lesions with an average loss
of >1.5 mm of probing attachment level, "unchanged" indicates
lesions with an average change of - 1 , 0, or +1 mm of probing
attachment level at the adjacent two interproximal measurement
sites, and "gainers" indicates lesions with an average gain of >1.5
mm of probing attachment level at the adjacent two interproximal
measurement sites.
increase the detection of sites undergoing, or being
at risk for, loss. Interestingly, the use of two suspected periodontopathogens did not markedly increase the proportion of "gainers" positive (4.8%) for
the test (Fig.) —further evidence of the usefulness of
bacteriological monitoring as a parameter in the management of periodontal disease.
Since periodontal disease is an infectious disease,
successful treatment regimes must be anti-infectious
in nature. Success in control and prevention will be
based on our understanding of the cause of the disease, as indicated by the results from our investigations. Furthermore, monitoring of the subgingival
microflora is likely to become useful in the management of periodontitis. Restorative procedures, whether
indicated by functional or esthetic needs, do not control the disease per se. Hence, they have to be recognized as separate entities unrelated to efforts directed
at controlling the infection.
ACKNOWLEDGMENTS
This study was supported in part by USPHS Research Grant DE04898 from the National Institute of
Dental Research, National Institutes of Health, Bethesda, MD 20892. The authors would also like to
express their sincere thanks to Mr. Homer Reynolds
for technical assistance, and to Ms. Phyllis Hill for
preparing the manuscript.
AXELSSON, P. and LINDHE, J. (1981a): Effect of Controlled Oral
Hygiene Procedures on Caries and Periodontal Disease in Adults
(Results After 6 Years), / Clin Periodontol 8: 239-248.
AXELSSON, P. and LINDHE, J. (1981b): The Significance of Maintenance Care in the Treatment of Periodontal Disease, / Clin
Periodontol 8: 281-294.
BADERSTEN, A. (1984): Nonsurgical Periodontal Therapy. Doctoral
Dissertation, University of Lund, Sweden.
BADERSTEN, A.; NILVEUS, R.; and EGELBERG, J. (1981): Effect
of Nonsurgical Periodontal Therapy, I. Moderately Advanced
Periodontitis, / Clin Periodontol 8: 57-72.
BADERSTEN, A.; NILVEUS, R.; and EGELBERG,). (1984a): Effect
of Nonsurgical Periodontal Therapy, II. Severely Advanced
Periodontitis, / Clin Periodontol 11: 63-76.
BADERSTEN, A.; NILVEUS, R.; and EGELBERG, J. (1984b): Effect
of Nonsurgical Periodontal Therapy, III. Single Versus Repeated
Instrumentation, / Clin Periodontol 11: 114-124.
BAKER, P.J.; EVANS, R.T.; SLOTS, ).; and GENCO, R.J. (1985):
Susceptibility of Human Oral Anaerobic Bacteria to Antibiotics
Suitable for Topical Use, / Clin Periodontol 12: 201-208
BONTA, C.Y.; ZAMBON, J.J.; GENCO, R.J.; and NEIDERS, M.E.
(1985): Rapid Identification of Periodontal Pathogens in Subgingival Plaque, Comparison of Indirect Immunofluorescence Microscopy with Bacterial Culture for Detection of Actinobacillus
actinomycetemcomitans, J Dent Res 64: 793-798.
CHRISTERSSON, L. (1986): Microbiologic Monitoring in the Treatment of Localized Juvenile Periodontitis (LJP), / Dent Res 65:
163, Abst. No. S4.
CHRISTERSSON, L.A.; BOTELHO, M.; WIKESJO, U.M.E.; BONTA,
Y.; and ZAMBON, JJ. (1985c): Suppression of A. actinomycetemcomitans Using Systemic Tetracycline, in Patients with Localized
juvenile Periodontitis, / Dent Res 64: 305, Abst. No. 1170.
CHRISTERSSON, L.A.; ROSLING, B.G.; ZAMBON, J.J.; and
GENCO, R.J. (1985a): Antimicrobial Treatment of Periodontal
Diseases, Predictability of Clinical Results, / Dent Res 64: 168,
Abst. No. S18.
CHRISTERSSON, L.; SLOTS, J.; ROSLING, B.; and GENCO, R.
(1985b): Microbiological and Clinical Effects of Surgical Treatment of Localized Juvenile Periodontitis, / Clin Periodontol 12:
465-476.
CHRISTERSSON, L.A.; ZAMBON, J.J.; WIKESJO, U.; ROSLING,
B.G.; DUNFORD, R.; and GENCO, R.J. (1986): The Effects of
Systemic Tetracycline Alone on Localized Juvenile Periodontitis,
{Dent Res 65: 805, Abst. No. 718.
GARRETT, J.S. (1983): Effects of Nonsurgical Periodontal Therapy
on Periodontitis in Humans, A Review, / Clin Periodontol 10:
515-523.
GENCO, R.J. (1981): Antibiotics in the Treatment of Human Periodontal Diseases, / Periodontol 52: 545-558.
GENCO, R.J.; ZAMBON, J.J.; and CHRISTERSSON, L.A. (1988):
The Origin of Periodontal Infections, Adv Dent Res 2: 245-259.
GENCO, R.J.; ZAMBON, J.J.; and CHRISTERSSON, L.A. (1986):
Use and Interpretation of Microbiological Assays in Periodontal
Diseases, Oral Microbiol Immunol 1: 73-79.
HILL, R.W.; RAMFJORD, S.P.; MORRISON, E.C.; APPLEBERRY,
E.A.; CAFFESSE, R.G.; KERRY, G.J.; and NISSLE, R.R. (1981):
Four Types of Periodontal Treatment Compared over Two Years,
/ Periodontol 52: 655-662.
ISIDOR, F.; KARRING, T.; and ATTSTROM, R. (1984): The Effect
of Root Planing as Compared to That of Surgical Treatment, /
Clin Periodontol 11: 669-681.
KNOWLES, J.; BURGETT, F.; MORRISON, E.; NISSLE, R.; and
RAMFJORD, S.P. (1980): Comparison of Results Following Three
388
CHR1STERSS0N
et al.
Modalities of Periodontal Therapy Related to Tooth Type and
Initial Pocket Depth, / Periodontol 7: 32-47.
KNOWLES, J.W.; BURGETT, F.G.; NISSLE, R.R.; SHICK, R.A.;
MORRISON, E.C.; and RAMFJORD, S.P. (1979): Results of Periodontal Treatment Related to Pocket Depth and Attachment
Levels, Eight Years, / Periodontol 50: 225-233.
KORNMAN, K.S. and ROBERTSON, P.B. (1985): Clinical and Microbiological Evaluation of Therapy for Juvenile Periodontitis, /
Periodontol 56: 443-446.
LINDHE, J. and NYMAN, S. (1975): The Effect of Plaque Control
and Surgical Pocket Elimination on the Establishment and Maintenance of Periodontal Health, A Longitudinal Study of Periodontal Therapy in Cases of Advanced Disease, / Clin Periodontol
9: 67-79.
LINDHE, J. and NYMAN, S. (1984): Long-term Maintenance of
Patients Treated for Advanced Periodontal Disease, / Clin Periodontol 11: 504-514.
LINDHE, J.; WESTFELT, E.; NYMAN, S.; SOCRANSKY, S.S.; and
HAFFAJEE, A.D. (1984): Long-term Effect of Surgical/Non-surgical Treatment of Periodontal Disease, / Clin Periodontol 11: 448-458.
LINDHE, J.; WESTFELT, E.; NYMAN, S.; SOCRANSKY, S.S.;
HEIJL, L.; and BRATTHALL, G. (1982): Healing Following Surgical/Non-surgical Treatment of Periodontal Disease, A Clinical
Study, / Clin Periodontol 9: 115-128.
MANDELL, R.L. (1984): A Longitudinal Microbiological Investigation of Actinobacillus actinomycetemcomitans and Eikenella corrodens in Juvenile Periodontitis, Infect Immun 45: 778-780.
MANDELL, R.L.; TRIPODI, L.S.; SAVITT, E.; GOODSON, J.M.;
and SOCRANSKY, S.S. (1986): The Effect of Treatment of Actinobacillus actinomycetemcomitans in Localized Juvenile Periodontitis, J Periodontol 57: 94-99.
NEWMAN, M.G. and SOCRANSKY, S.S. (1977): Predominant Cultivable Microbiota in Periodontitis, / Periodont Res 12: 120-128.
NYMAN, S.; LINDHE, J.; and ROSLING, B. (1977): Periodontal Surgery in Plaque-infected Dentitions, / Clin Periodontol 4: 240-249.
NYMAN, S.; ROSLING, B.; and LINDHE, J. (1975): Effect of
Professional Tooth Cleaning on Healing after Periodontal Surgery, / Clin Periodontol 2: 80-86.
PIHLSTROM, B.L.; McHUGH, R.B.; OLIPHANT, T.H.; and ORTIZ-CAMPOS, C. (1983): Comparison of Surgical/Non-surgical
Treatment of Periodontal Disease, A Review of Current Studies
and Additional Results After 6 V2 Years, / Clin Periodontol 10:
524-541.
PIHLSTROM, B.L.; ORTIZ-CAMPOS, C ; and McHUGH, R.B.
(1981): A Randomized Four-year Study of Periodontal Therapy,
/ Periodontol 52: 227-242.
RAMFJORD, S.P.; KNOWLES, J.W.; NISSLE, R.R.; BURGETT, F.G.;
and SHICK, R.A. (1975): Results Following Three Modalities of
Periodontal Therapy, / Periodontol 46: 522-526.
RAMFJORD, S.P.; KNOWLES, J.W.; NISSLE, R.R.; SHICK, R.A.;
and BURGETT, F.G. (1973): Longitudinal Study of Periodontal
Therapy, / Periodontol 44: 66-77.
ROSLING, B.G.; CHRISTERSSON, L.A.; SLOTS, J.; and GENCO,
R.J. (1985): Predictability of Topical and Subgingival Antimicrobial Therapy in the Management of Advanced Adult Periodontitis, / Dent Res 64: 360, Abst. No. 1672.
ROSLING, B.; NYMAN, S.; and LINDHE, J. (1976a): The Effect of
Systemic Plaque Control on Bone Regeneration in Infrabony
Pockets, / Clin Periodontol 3: 38-53.
ROSLING, B.; NYMAN, S.; LINDHE, J.; and JERN, B. (1976b):
The Healing Potential of the Periodontal Tissues Following Different Techniques of Periodontal Surgery in Plaque-free Dentitions, A 2-year Clinical Study, / Clin Periodontol 3: 233-250.
Adv Dent Res November 1988
ROSLING, B.G.; SLOTS, J.; CHRISTERSSON, L.A.; and GENCO,
R.J. (1983b): Microbiological and Clinical Effects of Conventional
Periodontal Therapy and Adjunctive Subgingival Iodine Irrigation, / Dent Res 62: 245, Abst. No. 688.
ROSLING, B.G.; SLOTS, J.; CHRISTERSSON, L.A.; GRONDAHL,
H.G.; and GENCO, R.J. (1986): Topical Antimicrobial Therapy
and Diagnosis of Subgingival Bacteria in the Management of
Periodontal Disease, / Clin Periodontol 13: 975-981.
ROSLING, B.; SLOTS, J.; WEBBER, R.L.; CHRISTERSSON, L.A.;
and GENCO, R.J. (1983a): Microbiological and Clinical Effects
of Topical Subgingival Antimicrobial Treatment on Human Periodontal Disease, / Clin Periodontol 10: 487-514.
SLOTS, J. (1979): Subgingival Microflora in Periodontal Disease, /
Clin Periodontol 6: 351-382.
SLOTS, J. (1982): Importance of Black-pigmented Bacteroides in Human Periodontal Disease. In: Host-Parasite Interactions in Periodontal Diseases, R.J. Genco and S.E. Mergenhagen, Eds.,
Washington, D.C.: American Society for Microbiology, pp. 27-45.
SLOTS, J.; EMRICH, L.; GENCO, R.J.; and ROSLING, B.G. (1985):
Relationship Between Some Subgingival Bacteria and Periodontal
Pocket Depth and Gain or Loss of Periodontal Attachment after
Treatment of Adult Periodontitis, / Clin Periodontol 12: 540-552.
SLOTS, J. and GENCO, R.J. (1984): Black-pigmented Bacteroides species, Capnocytophaga species and Actinobacillus actinomycetemcomitans in H u m a n Periodontal Disease: Virulence Factors in
Colonization, Survival, and Tissue Destruction, / Dent Res 63:412—
421.
SLOTS, J.; REYNOLDS, H.S.; and GENCO, R.J. (1980): Actinobacillus actinomycetemcomitans in Human Periodontal Disease, A
Cross-sectional Microbiological Examination, Infect Immun 29:
1013-1020.
SLOTS, J. and ROSLING, B.G. (1983): Suppression of the Periodontopathic Microflora in Localized Juvenile Periodontitis by
Systemic Tetracycline, / Clin Periodontol 10: 465-486.
SOCRANSKY, S.S. (1977): Microbiology of Periodontal Disease Present Status and Future Considerations, / Periodontol 48: 497-504.
TANNER, A.C.R.; HAFFER, C ; BRATTHALL, G.T.; VISCONTI,
R.A.; and SOCRANSKY, S.S. (1979): A Study of the Bacteria
Associated with Advancing Periodontitis in Man, / Clin Periodontol 6: 278-307.
van PALENSTEIN HELDERMAN, W.H. (1981): Microbial Etiology
of Periodontal Disease, / Clin Periodontol 8: 261-280.
WAITE, I.M. (1976): A Comparison Between Conventional Gingivectomy and a Nonsurgical Regime in the Treatment of Periodontitis, / Clin Periodontol 3: 173-185.
WILSON, M.E.; ZAMBON, J.J.; SUZUKI, J.B.; and GENCO, R.J.
(1985): Generalized Juvenile Periodontitis, Defective Neutrophil
Chemotaxis and Bacteroides gingivalis in a 13-Year-Old Female, /
Periodontol 56: 457-464.
ZAMBON, J.J. (1985): Actinobacillus actinomycetemcomitans in Human Periodontal Disease, / Clin Periodontol 12: 1-20.
ZAMBON, J.J.; CHRISTERSSON, L.A.; and SLOTS, J. (1983): Actinobacillus actinomycetemcomitans in Human Periodontal Disease:
Prevalence in Patient Groups and Distribution of Biotypes and
Serotypes within Families, / Periodontol 54: 707-711.
ZAMBON, J.J.; REYNOLDS, H.S.; CHEN, P.; and GENCO, R.J.
(1985): Rapid Identification of Periodontal Pathogens in Subgingival Dental Plaque. Comparison of Indirect Immunofluorescence Microscopy with Bacterial Culture for Detection of
Bacteroides gingivalis, J Periodontol 56 (Sp. Iss): 32-40.
ZAMET, J.S. (1975): A Comparative Clinical Study of Three Periodontal Surgical Techniques, / Clin Periodontol 2: 87-97.