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Current Concepts in Diagnosis and

Treatment of Periodontitis
Ingvar Magnusson andJan Lindhe

This article describes some areas of periodontal research and current

opinions regarding detection of disease progression, as well as risk indica-
tors and risk factors associated with disease progression. Longitudinal
probing of periodontal attachment level is considered the gold standard for
detection of disease activity although there are problems with this concept.
Digital subtraction radiography can assist in the detection of minor changes
of alveolar bone height and density. Risk factors such as composition of
subgingival plaque and gingival crevicular fluid, as well as the effect of
smoking are discussed. Adjunctive treatment with both antibiotics and
nonsteroidal anti-inflammatory drugs, systemic or local, seems to be helpful
in some forms of disease, Immunization to prevent colonization of tooth
surfaces and pockets by periodontal pathogens does not seem to be feasible
in the near future. (Semin Orthod 1996;2:13-20.) Copyright © 1996 by W.B.
Saunders Company

ongitudinal probing of periodontal attach- cluded that the reproducibility of pocket d e p t h

L m e n t has b e e n and still is the gold standard
for the diagnosis of active disease or progression
of disease. Interesting questions arise: How repro-
ducible and exact are the measurements? Which
measured differences are clinically significant?
Efforts have focused on the i m p r o v e m e n t of
probing validity for earlier detection of disease
progression. Gibbs et al 1 developed the Florida
Probe system (Florida Probe Corporation, Gaines-
ville, FL) that combines the advantages of con-
stant probing force with precise electronic mea-
s u r e m e n t and c o m p u t e r storage of the data. T h e
Florida Probe eliminates the potential errors
associated with visual reading. T h e system, which
consists of a p r o b e handpiece, a digital readout,
a foot switch, c o m p u t e r interface, and computer,
was studied by Magnusson et al z and correlated
to standard p r o b e measurements. It was con-
From the Department of Oral Biology, College of Dentistry,
University of Flarida, Gainesville, bL; and the Department of
Periodontology, Faculty of Odontology, University of G6teborg,
G6teborg, Sweden.
Address correspondenceto Ingvar Magnusson, DDS, OdontDr,
Department of Oral Biology, College of Dentistry, University of
Florida, Gainesville,FL 32610-0275.
Copyright© 1996 by W.B. Saunders Company
1073-8746/96/0201-000355.00/0
measurements obtained with the electronic probe
was superior to the reproducibility of those
obtained with a standard probe. T h e r e was no
difference in time c o n s u m p t i o n between the two
methods; however, p r o b i n g data f r o m the elec-
tronic p r o b e are entered into the c o m p u t e r
automatically, eliminating the n e e d for an assis-
tant to record the measurements. A slightly
different electronic p r o b e using an optical en-
coder transduction e l e m e n t (Interprobe, Bausch
& Lomb, Tucker, GA) was c o m p a r e d with conven-
tional probing. 3 Reproducibility was somewhat
higher with the I n t e r p r o b e c o m p a r e d with con-
ventional probing.
To detect progression of periodontal disease
for a short period, Haffajee et al 4 r e c o m m e n d e d
the tolerance method, in which the difference
between replicate a t t a c h m e n t level measure-
ments is used to calculate a standard deviation
for all the m e a s u r e m e n t pairs m a d e in one
individual. The subject threshold for a t t a c h m e n t
loss in an individual site is defined as three
standard deviations of the m e a n differences
between all the paired measurements. For 22
subjects, s t a n d a r d deviation values varied
f r o m +0.52 to 1.30 ram, resulting in a m e a n
subject threshold for detection of a t t a c h m e n t

Seminars in Orthodontics, Vol 2, No 1 (March), 1996: pp 13-20 13

<< :,FJ,. ~ >>
14 Magnusson and Lindhe
loss of 2.46 m m (range: 1.56 to 3.90 mm),
indicating that in some patients a considerable
loss of attachment is n e e d e d to determine pro-
gression of disease with a high level of probability.
Magnusson et aP also investigated the repro-
ducibility of attachment level measurements us-
ing the Florida Probe. With the use of fixed
reference points on custom-made acrylic stents,
a high level of agreement was achieved for
attachment level measurements made by differ-
ent examiners (mean SD = +_0.28 mm) or by a
single examiner during different visits (mean
SD = +-0.33 mm). The highest agreement be-
tween a t t a c h m e n t level m e a s u r e m e n t s was
achieved when the measurements were per-
f o r m e d at the same visit, even t h o u g h the mea-
surements were performed by two different exam-
iners. It is significant that by using the tolerance
method, Magnusson et al 5 established that the
Florida Probe was more sensitive in detecting a
true attachment loss than was the standard
periodontal probe. For the 10 subjects, the SD
varied from +-0.25 to 0.33 mm, with an average
of +_0.28 mm. With the standard manual probe,
Haffajee et al 4 reported an average of -+0.82 mm,
with a range of -+0.52 to 1.30 mm. Using three
SD as a threshold for attachment loss, the aver-
age threshold in the Magnusson study 5 would be
0.84 ram, compared with 2.46 m m tor Haffajee 4
et al. Thus, it seems that progressive periodontal
disease could be detected earlier by the constant-
force electronic probe.
Several reports indicate that measurements of
deeper pockets are difficult. 6+ In the study by
Haffajee et al 4 subjects were classified as having
advanced periodontal disease; the Magnusson
study 5 dealt with subjects having minimal-to-early
disease. However, when the Florida Probe was
used in subjects with severe periodontal disease,
the SD was f o u n d to be of the same magnitude or
lower in that group of subjects. Yang et al 1°
studied different probing designs to investigate
the reproducibility of the Florida Probe. The
maximum probing error was found to be approxi-
mately +_0.3 mm, which is considerably smaller
than that f o u n d in most previous studies. The
errors associated with the periodontal condition
and probing effect were also estimated. The
variance c o m p o n e n t s obtained here can be used
for determining the sample size in controlled
clinical studies.
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Jeffcoat et a111 have designed an electronic
periodontal probe that can automatically detect
the cemento-enameljunction. TheJeffcoat probe
provided highly reproducible measurements in
10 h u m a n subjects with attachment loss ranging
between 0.5 and 7.5 m m who were measured 10
times for 2 weeks. ~2 The overall mean SD of the
repeated measurements was + 0.17 ram.
Two other electronic probes, the Toronto
Probe 13 and the Florida Disk Probe 14 have been
designed to measure changes in attachment level
using the occlusal surface or the incisal edge as a
reference point. The Toronto Probe works on
constant air pressure and measures attachment
level from the occlusal surface. In a study of
duplicate measurements in nine subjects, it was
f o u n d that 82% of the measurements were within
1 m m difference. The SD for all teeth was +_0.46.
The Florida Disk Probe was used independently
by Low et aP 4 and Osborn et a115 to assess
reproducibility of repeated measurements. Both
studies resulted in highly reproducible measure-
ments with low standard deviations between
replicate m e a s u r e m e n t s (mean SD = +0.26
and +0.18 m m respectively). This probe does
not require a prefabricated stent.
Gerlach et a116 described repeatability of con-
trolled pressure relative attachment level mea-
surements collected in a multicenter clinical trial
setting. Relative attachment level measurements
were recorded for 213 patients by five different
examiners at three study centers. For each pa-
tient, measurements were recorded from four
periodontally involved posterior teeth. Duplicate
attachment level measurements were collected
at baseline, and after 3 and 6 months from each
selected site. A total of 2,453 duplicate measure-
ments were collected during the study. O f these,
215 (8.8%) pairs differed by more than 1.0 mm.
Overall, the mean SD of replicate measurements
was -+0.29 mm. The repeatability shown in this
study supports use of controlled pressure prob-
ing to evaluate changes in periodontitis in multi-
center studies.
Electronic probes seem to be superior to
manual probes. In the studies described previ-
ously, the range of overall SD for repeated
measurements of individual sites in different
subjects was +_0.17 to +_0.32 ram. Regarding the
ability to detect significant attachment level
changes, this is an improvement over earlier
findings.
< < :"d-'J~- ?:- > >
Current Concepts in Diagnosis and Treatment
Probing a t t a c h m e n t level is currently the gold
standard for detecting active disease at a site, but
changes in a t t a c h m e n t level are not always easy
to interpret because of the limitation of p r o b i n g
in assessing the histological a t t a c h m e n t level.
Short-time changes, both loss and gain, may only
reflect fluctuation in collagen content accompa-
nied by changes in inflammatory status and may
not indicate real a t t a c h m e n t changes. Watts 17
suggested that it is also possible that despite o u r
best efforts, these changes might also represent
errors in p r o b e p l a c e m e n t or angulation. If
a t t a c h m e n t loss is confirmed at a later time,
however, it probably represents a true loss, indica-
tive of active and progressive periodontal dis-
ease.
Computer-assisted Subtraction
Radiography
Over the past years the technique of subtraction
radiography has been refined. More sensitive
a n d objective m e t h o d s for analyzing radio-
graphs 1~21 and perhaps a better opportunity to
c o m p a r e changes in a t t a c h m e n t with changes in
b o n e density are offered. H a u s m a n n et al zl
m o n i t o r e d crestal interdental b o n e in 15 un-
treated patients with periodontitis for a 6-month
period. Nine percent of the sites exhibited b o n e
loss, whereas 4% exhibited b o n e gain. T h e inves-
tigators suggested that the findings were consis-
tent with the theory of exacerbation and remis-
sion at crestal alveolar b o n e sites in untreated
periodontitis patients. However, in this study
there was no attempt to correlate the findings to
changes in m e a s u r e m e n t s of a t t a c h m e n t level.
Few attempts have b e e n m a d e to correlate
b o n e loss with changes in attachment. Deas et
a122 c o m p a r e d the frequency of a t t a c h m e n t loss
in 21 subjects with periodontitis at baseline and
at 3, 6, and 9 months. They r e p o r t e d changes in
b o n e density in 53% of sites at 3 months, 56% at
6 months, and 62% at 9 months. With 88% to
92% of attachment level measurements reproduc-
ible within 1.0 m m , the frequency of a t t a c h m e n t
level changes was 19% at 3 months, 25% at 6
months, and 32% at 9 months. Cogen et a123
subtracted radiographs taken at baseline, 3
months, and 6 months and reported that of the
sites examined, 23% were losing b o n e and 3%
were gaining bone. This suggests that the preva-
lence of active b o n e loss r e p o r t e d using subtrac-
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15
tion radiography is higher than that previously
r e p o r t e d using periodontal probing, and that
the p r o p o r t i o n of sites losing b o n e is greater
than the p r o p o r t i o n gaining bone. However, the
clinical significance of a change in b o n e density
is not clear. We must keep in m i n d that changes
in alveolar b o n e may not correlate with changes
in the true a t t a c h m e n t level or with measure-
ments of the clinical a t t a c h m e n t level. Nonethe-
less, in a periodontal patient, sites that show
evidence of b o n e loss must be considered to have
been active sites at some time during the time
interval the radiographs were taken, especially
when they correlate with loss of attachment.
Microbiology
Overwhelming data support the role of specific
bacteria in the cause of periodontal diseases. A
classical association is the one between localized
juvenile periodontitis and ActinobaciUus actinomy-
cetemcomitans.24-'~° Several other potential peri-
odontal pathogens have b e e n described primar-
ily in association with adult chronic periodontal
disease. Species of note include mainly gram-
negative anaerobic bacteria: Bacteroidesforsythus,
Campylobacter rectus, Eubacterium spp, EikeneUa
corrodens, Fusobacterium nucleatum, Peptostreptococ-
cus micros, Porphyromonas gingivalis, Prevotella inter-
media, Selenomonas spp and spirochetes have been
strongly associated with diseased sites. 3a-3s How-
ever, Streptococcus intermedius has also b e e n identi-
fied in forms of refractory periodontal d i s e a s e 9
This condition was described by the American
Academy of Periodontology as a disease that
continues to progress with loss of connective
tissue a t t a c h m e n t and bone despite appropriate
periodontal therapy. Traditionally, bacteria have
b e e n cultured and identified on selective and
nonselective m e d i a but also microscopic tech-
niques have b e e n used to identify morphotypes.
Recently, DNA probes have been developed to
detect the presence of putative pathogens. 4°42
Several of these probes are commercially avail-
able and some can be used chair-side for rapid
identification.
T h e presence of a potential p a t h o g e n must
always be regarded as a risk factor and not as a
disease indicator. Patients with refractory peri-
odontal disease have often had previous antibi-
otic therapy resulting in the d e v e l o p m e n t of
antibiotic resistance and in these cases it seems
<< ACJ~ e >>
16 Magnusson and Lindhe
advisable to base continued antibacterial therapy
on microbial susceptibility.
Antimicrobial Approach to the
Treatment of Periodontal Diseases
Conventional periodontal therapy, including scal-
ing, root planing, and possibly periodontal sur-
gery, is still the therapy of choice and is very
successful provided that the patient adheres to a
regular maintenance schedule. However, in some
forms of disease, antimicrobial therapy is appro-
priate as an adjunct to conventional therapy (for
review4a,44). In patients with adult periodontitis
administration of systemic antibiotics without
mechanical treatment has shown little promise.
The use of systemic tetracycline in the treat-
m e n t of juvenile periodontitis is well docu-
m e n t e d and has been proven effective in sup-
pressing subgingival A actinomycetemcomitans. 26 In
patients with refractory periodontal disease sub-
gingival plaque exhibits a high percentage of
microorganisms with resistance, especially against
tetracycline. Therefore, Magnusson et aP 9 se-
lected antibiotics, based on susceptibility testing,
as an adjunct to treat patients with refractory
periodontal disease. The results were consider-
ably better than those obtained in a placebo
control group.
Recently, research has focused on local antibi-
otic therapy to achieve a high local drug concen-
tration and to avoid side effects observed with
systemic administration. Favorable results have
been described with the local delivery of tetracy-
cline (25%) impregnated ethylene vinyl acetate
fibers, 45,46 the application of tetracycline (2%) in
a lipid gel, 47 and the application of metronida-
zole (25%) in lipid gel. 4s
The use of lower-than-normal doses of tetracy-
cline to treat periodontal disease has been inves-
tigated by Rifkin et al. 49 They showed that the
treatment was effective in preventing attachment
loss in adult periodontitis patients. Low doses of
tetracycline effectively inhibit pathologically ex-
cessive collagenase activity in gingival tissue. 5°
Gingival Crevicular Fluid
Analysis of GCF shows a n u m b e r of enzymes,
metabolic byproducts, serum proteins, and other
substances related to the inflammatory process,
tissue degradation, and cell death. Identification
H o m e [ T O C [ Index
and quantification of these substances may pro-
vide better understanding of both the dynamics
and metabolic stages of the periodontal tissues.
A n u m b e r of enzymes reflecting tissue remod-
eling or destruction have been studied. These
include collagenase, [3-glucuronidase ([3-G), aryl-
sulfatase (AS), and L-aspartate aminotransferase
(AST).
Villela et a151 studied collagenolytic activity in
crevicular fluid from subjects with chronic adult
periodontitis, localized juvenile periodontitis,
gingivitis, and from healthy control subjects.
Among subjects, collagenase activity increased
with severity of disease. Among sites, significant
correlation was found between crevicular fluid
activity and pocket depth in chronic adult peri-
odontitis and in localized juvenile periodontitis,
but not in gingivitis.
Birkedal-Hansen et a152 reported that neither
gingival crevicular fluid flow nor collagenolytic
activity are good indicators or predictors of bone
loss. On the other hand, Ciancio et a153suggested
that gingival crevicular fluid collagenolytic activ-
ity may be of diagnostic value in periodontal
disease, however, they did not monitor attach-
m e n t level changes. It is clear that further investi-
gation is n e e d e d to establish if collagenase levels
can be used as indicators of progressive periodon-
tal disease.
Lamster et a154 evaluated crevicular fluid for
collagenase, [3-G, and AST during development
of experimental gingivitis in humans. They found
that after 4 weeks the absolute a m o u n t of active
collagenase had increased 550% in interproxi-
mal areas. For interproximal sites the increase in
[3-G activity was 180% and for AS 240%. Thus,
these enzyme levels correlated positively with
increased gingival inflammation, although in-
creases in specific enzyme levels lagged slightly
behind increases in gingival index. H a r p e r et a155
evaluated lysosomal [3-G and AS and cytoplasmic
lactate dehydrogenase (LDH) enzyme activity
and the composition of subgingival plaque flora
in patients with adult periodontitis. [3-G levels
correlated significantly with populations of spiro-
chetes, P intermedius, Pgingivalis, and total lactose-
negative black-pigmenting Bacteroides (BPB). LDH
activity showed a significant positive correlation
with levels of B gingivalis and total lactose-
negative BPBs. AS levels correlated significantly
with B gingivalis only. In these studies no at-
<< AFJ,. a >>
Current Concepts in Diagnosis and Treatment
tempts were m a d e to correlate increases in levels
of these enzymes to changes in attachment.
AST is an intracellular enzyme that is released
and can be detected in crevicular fluid as a result
of cell death. Chambers et a156and Persson et aP 7
have shown that AST m e a s u r e m e n t s correlate
with gingival inflammation and seem to differen-
tiate sites with spontaneously occurring gingivitis
in steady states, from sites with active gingival
inflammation. In a longitudinal study, Crawford
et a158 showed that elevated levels of AST in
gingival crevice samples exhibited a strong corre-
lation with loss of attachment.
Prostaglandin E2 is r e p o r t e d to be a principal
biochemical mediator of periodontal tissue de-
struction in humans. T h e r e is a clear association
between the levels present within the periodon-
tal tissues and crevicular fluid and the state of
periodontal health. 57-61When considering gingi-
vitis, adult periodontitis, and juvenile periodonti-
tis, crevicular fluid levels are low or nondetect-
able in health, and are elevated markedly with
increased disease severity. Extremely high levels
of prostaglandin E2 are present at periodontal
sites with active loss of attachment. In sites that
are in remission or showing no loss, low concen-
trations are found. It can be concluded that high
levels of prostaglandin Ez constitute a significant
active disease indicator and that a diagnostic kit
assessing concentration could be a valuable tool.
A n u m b e r of soluble mediators are p r o d u c e d
by inflammatory cells. The identification ofinter-
leukins and cytokines that could contribute to
tissue destruction in periodontal disease has
increased interest in cre~icular fluid levels of
these mediators. 62,63
Anti-inflammatory Approach to the
Treatment of Periodontal Diseases
Over the last years, considerable interest has
been focused on the use of nonsteroid anti-
inflammatory drugs to modulate the host re-
sponse and research has shown that such com-
pounds can retard b o n e loss. Controlled studies
have n o t e d this effect in adult and refractory
periodontal disease using systemic flurbiprofen
therapy and in rapidly progressive periodontal
disease using n a p r o x e n or m e c l o t e n a m a t e so-
dium therapy. 64-68
Because of the c o n c e r n of side effects with the
use of systemic therapy 69 of these drugs, the
Home [ TOC [ Bndex
17
concept of local therapy has been approached. 7°
In a 6-month controlled study, the effect on b o n e
height was evaluated for three different regi-
mens: ketorolac rinse (0.1%) with placebo cap-
sule twice daily (BID); flurbiprofen capsule (50
mg) with placebo rinse BID; or placebo capsule
and placebo rinse BID. Significant b o n e loss was
observed in the placebo group but not in the
flurbiprofen or ketorolac rinse groups. Data
indicate that topical application of ketorolac may
be beneficial in the t r e a t m e n t of adult periodon-
tal disease.
Smoking
Smoking seems to be an i m p o r t a n t risk factor for
periodontal diseases and for the refractory f o r m
in particular. Magnusson et a171 and McFarlane
et a172 r e p o r t e d that in two groups of 21 and 31
refractory patients, 19 and 28, respectively had a
history of smoking. Smoking has also b e e n con-
sidered a major risk in adult chronic periodontal
disease. 7~-7~ Smoking has a negative impact on
healing after both nonsurgical and surgical peri-
odontal therapy. 79,s° It has also b e e n suggested
that smoking is associated with increased risk of
subgingival infection and that smoking may
modulate the periodontal flora, sl
Immunization
Experiments using vaccination against specific
periodontal pathogens have b e e n p e r f o r m e d by
several research groups with the main goal of
eliminating existing pathogens and preventing
subsequent colonization and growth. McArthur
et al s2 described the modulation of colonization
by black-pigmented bacteria in squirrel monkeys
by immunization with P gingivalis. Ebersole et
al a3 r e p o r t e d that P gingivalis immunization sig-
nificantly reduced the e m e r g e n c e of this species
during disease progression in ligature-induced
disease in Macacafascicularis. However, immuni-
zation with P intermedia had minimal effect on
the subgingival plaque in this primate. Persson et
al s4 r e p o r t e d that antibody titer and m a x i m u m
percentage of P gingivalis in M fascicularis were
inversely correlated, indicating that a h u m o r a l
i m m u n e response may be effective in reducing P
gingivalis overgrowth. Although these animal
experiments look promising, it is n o t reasonable
<< Ar'Jc e >>
18 Magnusson and Lindhe
to assume that i m m u n i z a t i o n in humans will be
used in the foreseeable future.
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