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


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14 Magnusson and Lindhe

loss of 2.46 m m (range: 1.56 to 3.90 mm), Jeffcoat et a111 have designed an electronic
indicating that in some patients a considerable periodontal probe that can automatically detect
loss of attachment is n e e d e d to determine pro- the cemento-enameljunction. TheJeffcoat probe
gression of disease with a high level of probability. provided highly reproducible measurements in
Magnusson et aP also investigated the repro- 10 h u m a n subjects with attachment loss ranging
ducibility of attachment level measurements us- between 0.5 and 7.5 m m who were measured 10
ing the Florida Probe. With the use of fixed times for 2 weeks. ~2 The overall mean SD of the
reference points on custom-made acrylic stents, repeated measurements was + 0.17 ram.
a high level of agreement was achieved for Two other electronic probes, the Toronto
attachment level measurements made by differ- Probe 13 and the Florida Disk Probe 14 have been
ent examiners (mean SD = +_0.28 mm) or by a designed to measure changes in attachment level
single examiner during different visits (mean using the occlusal surface or the incisal edge as a
SD = +-0.33 mm). The highest agreement be- reference point. The Toronto Probe works on
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 constant air pressure and measures attachment
achieved when the measurements were per- level from the occlusal surface. In a study of
f o r m e d at the same visit, even t h o u g h the mea- duplicate measurements in nine subjects, it was
f o u n d that 82% of the measurements were within
surements were performed by two different exam-
1 m m difference. The SD for all teeth was +_0.46.
iners. It is significant that by using the tolerance
The Florida Disk Probe was used independently
method, Magnusson et al 5 established that the
by Low et aP 4 and Osborn et a115 to assess
Florida Probe was more sensitive in detecting a
reproducibility of repeated measurements. Both
true attachment loss than was the standard
studies resulted in highly reproducible measure-
periodontal probe. For the 10 subjects, the SD
ments with low standard deviations between
varied from +-0.25 to 0.33 mm, with an average
replicate m e a s u r e m e n t s (mean SD = +0.26
of +_0.28 mm. With the standard manual probe,
and +0.18 m m respectively). This probe does
Haffajee et al 4 reported an average of -+0.82 mm,
not require a prefabricated stent.
with a range of -+0.52 to 1.30 mm. Using three
Gerlach et a116 described repeatability of con-
SD as a threshold for attachment loss, the aver-
trolled pressure relative attachment level mea-
age threshold in the Magnusson study 5 would be
surements collected in a multicenter clinical trial
0.84 ram, compared with 2.46 m m tor Haffajee 4
setting. Relative attachment level measurements
et al. Thus, it seems that progressive periodontal
were recorded for 213 patients by five different
disease could be detected earlier by the constant-
examiners at three study centers. For each pa-
force electronic probe.
tient, measurements were recorded from four
Several reports indicate that measurements of periodontally involved posterior teeth. Duplicate
deeper pockets are difficult. 6+ In the study by attachment level measurements were collected
Haffajee et al 4 subjects were classified as having at baseline, and after 3 and 6 months from each
advanced periodontal disease; the Magnusson selected site. A total of 2,453 duplicate measure-
study 5 dealt with subjects having minimal-to-early ments were collected during the study. O f these,
disease. However, when the Florida Probe was 215 (8.8%) pairs differed by more than 1.0 mm.
used in subjects with severe periodontal disease, Overall, the mean SD of replicate measurements
the SD was f o u n d to be of the same magnitude or was -+0.29 mm. The repeatability shown in this
lower in that group of subjects. Yang et al 1° study supports use of controlled pressure prob-
studied different probing designs to investigate ing to evaluate changes in periodontitis in multi-
the reproducibility of the Florida Probe. The center studies.
maximum probing error was found to be approxi- Electronic probes seem to be superior to
mately +_0.3 mm, which is considerably smaller manual probes. In the studies described previ-
than that f o u n d in most previous studies. The ously, the range of overall SD for repeated
errors associated with the periodontal condition measurements of individual sites in different
and probing effect were also estimated. The subjects was +_0.17 to +_0.32 ram. Regarding the
variance c o m p o n e n t s obtained here can be used ability to detect significant attachment level
for determining the sample size in controlled changes, this is an improvement over earlier
clinical studies. findings.
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Current Concepts in Diagnosis and Treatment 15

Probing a t t a c h m e n t level is currently the gold tion radiography is higher than that previously
standard for detecting active disease at a site, but r e p o r t e d using periodontal probing, and that
changes in a t t a c h m e n t level are not always easy the p r o p o r t i o n of sites losing b o n e is greater
to interpret because of the limitation of p r o b i n g than the p r o p o r t i o n gaining bone. However, the
in assessing the histological a t t a c h m e n t level. clinical significance of a change in b o n e density
Short-time changes, both loss and gain, may only is not clear. We must keep in m i n d that changes
reflect fluctuation in collagen content accompa- in alveolar b o n e may not correlate with changes
nied by changes in inflammatory status and may in the true a t t a c h m e n t level or with measure-
not indicate real a t t a c h m e n t changes. Watts 17 ments of the clinical a t t a c h m e n t level. Nonethe-
suggested that it is also possible that despite o u r less, in a periodontal patient, sites that show
best efforts, these changes might also represent evidence of b o n e loss must be considered to have
errors in p r o b e p l a c e m e n t or angulation. If been active sites at some time during the time
a t t a c h m e n t loss is confirmed at a later time, interval the radiographs were taken, especially
however, it probably represents a true loss, indica- when they correlate with loss of attachment.
tive of active and progressive periodontal dis-
ease.
Microbiology
Overwhelming data support the role of specific
Computer-assisted Subtraction bacteria in the cause of periodontal diseases. A
Radiography classical association is the one between localized
Over the past years the technique of subtraction juvenile periodontitis and ActinobaciUus actinomy-
radiography has been refined. More sensitive cetemcomitans.24-'~° Several other potential peri-
a n d objective m e t h o d s for analyzing radio- odontal pathogens have b e e n described primar-
graphs 1~21 and perhaps a better opportunity to ily in association with adult chronic periodontal
c o m p a r e changes in a t t a c h m e n t with changes in disease. Species of note include mainly gram-
b o n e density are offered. H a u s m a n n et al zl negative anaerobic bacteria: Bacteroidesforsythus,
m o n i t o r e d crestal interdental b o n e in 15 un- Campylobacter rectus, Eubacterium spp, EikeneUa
treated patients with periodontitis for a 6-month corrodens, Fusobacterium nucleatum, Peptostreptococ-
period. Nine percent of the sites exhibited b o n e cus micros, Porphyromonas gingivalis, Prevotella inter-
loss, whereas 4% exhibited b o n e gain. T h e inves- media, Selenomonas spp and spirochetes have been
tigators suggested that the findings were consis- strongly associated with diseased sites. 3a-3s How-
tent with the theory of exacerbation and remis- ever, Streptococcus intermedius has also b e e n identi-
sion at crestal alveolar b o n e sites in untreated fied in forms of refractory periodontal d i s e a s e 9
periodontitis patients. However, in this study This condition was described by the American
there was no attempt to correlate the findings to Academy of Periodontology as a disease that
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. continues to progress with loss of connective
Few attempts have b e e n m a d e to correlate tissue a t t a c h m e n t and bone despite appropriate
b o n e loss with changes in attachment. Deas et periodontal therapy. Traditionally, bacteria have
a122 c o m p a r e d the frequency of a t t a c h m e n t loss b e e n cultured and identified on selective and
in 21 subjects with periodontitis at baseline and nonselective m e d i a but also microscopic tech-
at 3, 6, and 9 months. They r e p o r t e d changes in niques have b e e n used to identify morphotypes.
b o n e density in 53% of sites at 3 months, 56% at Recently, DNA probes have been developed to
6 months, and 62% at 9 months. With 88% to detect the presence of putative pathogens. 4°42
92% of attachment level measurements reproduc- Several of these probes are commercially avail-
ible within 1.0 m m , the frequency of a t t a c h m e n t able and some can be used chair-side for rapid
level changes was 19% at 3 months, 25% at 6 identification.
months, and 32% at 9 months. Cogen et a123 T h e presence of a potential p a t h o g e n must
subtracted radiographs taken at baseline, 3 always be regarded as a risk factor and not as a
months, and 6 months and reported that of the disease indicator. Patients with refractory peri-
sites examined, 23% were losing b o n e and 3% odontal disease have often had previous antibi-
were gaining bone. This suggests that the preva- otic therapy resulting in the d e v e l o p m e n t of
lence of active b o n e loss r e p o r t e d using subtrac- antibiotic resistance and in these cases it seems
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16 Magnusson and Lindhe

advisable to base continued antibacterial therapy and quantification of these substances may pro-
on microbial susceptibility. 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-
Antimicrobial Approach to the eling or destruction have been studied. These
Treatment of Periodontal Diseases include collagenase, [3-glucuronidase ([3-G), aryl-
Conventional periodontal therapy, including scal- sulfatase (AS), and L-aspartate aminotransferase
ing, root planing, and possibly periodontal sur- (AST).
gery, is still the therapy of choice and is very Villela et a151 studied collagenolytic activity in
successful provided that the patient adheres to a crevicular fluid from subjects with chronic adult
regular maintenance schedule. However, in some periodontitis, localized juvenile periodontitis,
forms of disease, antimicrobial therapy is appro- gingivitis, and from healthy control subjects.
priate as an adjunct to conventional therapy (for Among subjects, collagenase activity increased
review4a,44). In patients with adult periodontitis with severity of disease. Among sites, significant
administration of systemic antibiotics without correlation was found between crevicular fluid
mechanical treatment has shown little promise. activity and pocket depth in chronic adult peri-
The use of systemic tetracycline in the treat- odontitis and in localized juvenile periodontitis,
m e n t of juvenile periodontitis is well docu- but not in gingivitis.
m e n t e d and has been proven effective in sup- Birkedal-Hansen et a152 reported that neither
pressing subgingival A actinomycetemcomitans. 26 In
gingival crevicular fluid flow nor collagenolytic
patients with refractory periodontal disease sub-
activity are good indicators or predictors of bone
gingival plaque exhibits a high percentage of
loss. On the other hand, Ciancio et a153suggested
microorganisms with resistance, especially against
that gingival crevicular fluid collagenolytic activ-
tetracycline. Therefore, Magnusson et aP 9 se-
ity may be of diagnostic value in periodontal
lected antibiotics, based on susceptibility testing,
disease, however, they did not monitor attach-
as an adjunct to treat patients with refractory
m e n t level changes. It is clear that further investi-
periodontal disease. The results were consider-
gation is n e e d e d to establish if collagenase levels
ably better than those obtained in a placebo
control group. can be used as indicators of progressive periodon-
Recently, research has focused on local antibi- tal disease.
otic therapy to achieve a high local drug concen- Lamster et a154 evaluated crevicular fluid for
tration and to avoid side effects observed with collagenase, [3-G, and AST during development
systemic administration. Favorable results have of experimental gingivitis in humans. They found
been described with the local delivery of tetracy- that after 4 weeks the absolute a m o u n t of active
cline (25%) impregnated ethylene vinyl acetate collagenase had increased 550% in interproxi-
fibers, 45,46 the application of tetracycline (2%) in mal areas. For interproximal sites the increase in
a lipid gel, 47 and the application of metronida- [3-G activity was 180% and for AS 240%. Thus,
zole (25%) in lipid gel. 4s these enzyme levels correlated positively with
The use of lower-than-normal doses of tetracy- increased gingival inflammation, although in-
cline to treat periodontal disease has been inves- creases in specific enzyme levels lagged slightly
tigated by Rifkin et al. 49 They showed that the behind increases in gingival index. H a r p e r et a155
treatment was effective in preventing attachment evaluated lysosomal [3-G and AS and cytoplasmic
loss in adult periodontitis patients. Low doses of lactate dehydrogenase (LDH) enzyme activity
tetracycline effectively inhibit pathologically ex- and the composition of subgingival plaque flora
cessive collagenase activity in gingival tissue. 5° in patients with adult periodontitis. [3-G levels
correlated significantly with populations of spiro-
chetes, P intermedius, Pgingivalis, and total lactose-
Gingival Crevicular Fluid negative black-pigmenting Bacteroides (BPB). LDH
Analysis of GCF shows a n u m b e r of enzymes, activity showed a significant positive correlation
metabolic byproducts, serum proteins, and other with levels of B gingivalis and total lactose-
substances related to the inflammatory process, negative BPBs. AS levels correlated significantly
tissue degradation, and cell death. Identification with B gingivalis only. In these studies no at-
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Current Concepts in Diagnosis and Treatment 17

tempts were m a d e to correlate increases in levels concept of local therapy has been approached. 7°
of these enzymes to changes in attachment. In a 6-month controlled study, the effect on b o n e
AST is an intracellular enzyme that is released height was evaluated for three different regi-
and can be detected in crevicular fluid as a result mens: ketorolac rinse (0.1%) with placebo cap-
of cell death. Chambers et a156and Persson et aP 7 sule twice daily (BID); flurbiprofen capsule (50
have shown that AST m e a s u r e m e n t s correlate mg) with placebo rinse BID; or placebo capsule
with gingival inflammation and seem to differen- and placebo rinse BID. Significant b o n e loss was
tiate sites with spontaneously occurring gingivitis observed in the placebo group but not in the
in steady states, from sites with active gingival flurbiprofen or ketorolac rinse groups. Data
inflammation. In a longitudinal study, Crawford indicate that topical application of ketorolac may
et a158 showed that elevated levels of AST in be beneficial in the t r e a t m e n t of adult periodon-
gingival crevice samples exhibited a strong corre- tal disease.
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- Smoking
struction in humans. T h e r e is a clear association
between the levels present within the periodon- Smoking seems to be an i m p o r t a n t risk factor for
tal tissues and crevicular fluid and the state of periodontal diseases and for the refractory f o r m
periodontal health. 57-61When considering gingi- in particular. Magnusson et a171 and McFarlane
vitis, adult periodontitis, and juvenile periodonti- et a172 r e p o r t e d that in two groups of 21 and 31
tis, crevicular fluid levels are low or nondetect- refractory patients, 19 and 28, respectively had a
able in health, and are elevated markedly with history of smoking. Smoking has also b e e n con-
increased disease severity. Extremely high levels sidered a major risk in adult chronic periodontal
of prostaglandin E2 are present at periodontal disease. 7~-7~ Smoking has a negative impact on
sites with active loss of attachment. In sites that healing after both nonsurgical and surgical peri-
are in remission or showing no loss, low concen- odontal therapy. 79,s° It has also b e e n suggested
trations are found. It can be concluded that high that smoking is associated with increased risk of
levels of prostaglandin Ez constitute a significant subgingival infection and that smoking may
active disease indicator and that a diagnostic kit modulate the periodontal flora, sl
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- Immunization
leukins and cytokines that could contribute to Experiments using vaccination against specific
tissue destruction in periodontal disease has periodontal pathogens have b e e n p e r f o r m e d by
increased interest in cre~icular fluid levels of several research groups with the main goal of
these mediators. 62,63
eliminating existing pathogens and preventing
subsequent colonization and growth. McArthur
et al s2 described the modulation of colonization
Anti-inflammatory Approach to the
by black-pigmented bacteria in squirrel monkeys
Treatment of Periodontal Diseases
by immunization with P gingivalis. Ebersole et
Over the last years, considerable interest has al a3 r e p o r t e d that P gingivalis immunization sig-
been focused on the use of nonsteroid anti- nificantly reduced the e m e r g e n c e of this species
inflammatory drugs to modulate the host re- during disease progression in ligature-induced
sponse and research has shown that such com- disease in Macacafascicularis. However, immuni-
pounds can retard b o n e loss. Controlled studies zation with P intermedia had minimal effect on
have n o t e d this effect in adult and refractory the subgingival plaque in this primate. Persson et
periodontal disease using systemic flurbiprofen al s4 r e p o r t e d that antibody titer and m a x i m u m
therapy and in rapidly progressive periodontal percentage of P gingivalis in M fascicularis were
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- inversely correlated, indicating that a h u m o r a l
dium therapy. 64-68 i m m u n e response may be effective in reducing P
Because of the c o n c e r n of side effects with the gingivalis overgrowth. Although these animal
use of systemic therapy 69 of these drugs, the experiments look promising, it is n o t reasonable
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18 Magnusson and Lindhe

to assume that i m m u n i z a t i o n in humans will be the diagnosis of periodontal bone lesions. Oral Surg
used in the foreseeable future. Oral Med Oral Patho11983;55:208-213.
19. Gr6ndahl K, Gr6ndahl H-G, Webber RL. Influence of
variations in projection geometry on detectability of
periodontal bone lesions. A comparison between subtrac-
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Current Concepts in Diagnosis and Treatment 19

35. van WinkelhoffAJ, van Steenbergen TJM, de GraaffJ, et gingivitis and from healthy control subjects. J Periodont
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