Periodontology 2000, Vol.
53, 2010, 12–27
Printed in Singapore. All rights reserved
Comparison of the clinical
features of chronic and
aggressive periodontitis
G A R Y C. A R M I T A G E & M A R Y P. C U L L I N A N
Historical perspective
In the late 1800s, what is now known as chronic
periodontitis was clinically characterized as a slowly
progressive destruction of the periodontium due to
the accumulation of Ôlime depositsÕ on the teeth (21),
or Ôcalcic inflammation of the peridental membraneÕ
secondary to deposits of ÔsalivaryÕ and ⁄ or ÔserumalÕ
calculus (13). The calcified deposits were considered
to be mechanical irritants that led to gingival reces-
sion and a generalized or even pattern of bone loss
(13, 21). Throughout most of the 20th century, this
form of periodontitis has been considered an
inflammatory disease associated with local irritants
and the formation of dental plaque (biofilms) on
tooth surfaces (4). This concept prevails today.
What is now known as Ôgeneralized aggressive
periodontitisÕ was not clearly described until the lat-
ter part of the 20th century. However, G.V. Black used
the terms Ôphagedenic pericementitisÕ and Ôchronic
suppurative pericementitisÕ to describe patients who
suffered from a rapid destruction of alveolar bone
(14). In the past three decades, authors have used a
variety of terms for cases in which there is general-
ized severe periodontal destruction in young
patients, including Ôgeneralized juvenileÕ (16, 94),
Ôrapidly progressiveÕ (46, 64), or simply ÔsevereÕ
periodontitis (18). In most respects, the disease
clinically resembles chronic periodontitis except the
affected individuals are much younger and the rate of
progression is assumed to be rapid since there is
extensive periodontal damage in a young person.
Current views regarding the major characteristics
of localized aggressive periodontitis have been con-
siderably influenced by historical perspectives of the
disease. In a series of papers from 1920 to 1928,
12
 2010 John Wiley & Sons A/S
PERIODONTOLOGY 2000
Bernard Gottlieb of the University of Vienna School
of Medicine described an unusual form of peri-
odontal disease that primarily affected some or all of
the permanent incisors and first molars of young
individuals (29–33). Based on certain histological
observations such as thin cementum on extracted
teeth from affected sites, he believed that the disease
was due to defective deposition of cementum or
ÔcementopathiaÕ (32–34). Gottlieb applied the princi-
ples of classical pathology as they were practiced in
the 1920s, which stated that all human non-neo-
plastic diseases could be classified as either inflam-
matory or non-inflammatory (4). Since his adolescent
patients did not exhibit the intense gingival inflam-
mation ordinarily seen in other patients (i.e. adults)
with periodontitis, he believed that the disease was a
non-inflammatory or degenerative condition. It was
claimed that initial stages of the disease were not
associated with local irritants such as dental plaque
or calculus, and therefore the disease was subse-
quently referred to as Ôdiffuse atrophy of the alveolar
boneÕ or ÔperiodontosisÕ (34, 63). According to this
hypothesis, the alveolar bone degenerated and the
teeth drifted apart or migrated without the formation
of periodontal pockets (90). Since it was thought that
continuous deposition of cementum was required in
order to prevent the apical migration of epithelium
along the root surface, pockets formed at sites that
were supposedly afflicted with cementopathia. As a
secondary phenomenon, once a pocket formed, it
became susceptible to colonization by oral bacteria
and was Ô…a potential trap for accumulating deposits
from salivaÕ (63). In the final stage of the disease,
bacterial toxins and other irritants eventually caused
some inflammation, which contributed to additional
loss of bone and connective tissue attachment to the
 Comparison of the clinical features of chronic and aggressive periodontitis
tooth. Therefore, it was believed that periodontal
inflammation was often observed in cases of peri-
odontosis, but only after non-inflammatory degen-
eration of the alveolar bone and impairment of
cementum deposition established conditions that
promoted pocket formation.
Scientific proof for this hypothetical series of
events could not be provided, and, at the 1966 World
Workshop in Periodontics, it was concluded that
there is little to no evidence for the existence of non-
inflammatory degenerative periodontal disease. It
was the consensus of the group of experts at the
workshop Ô…that the term periodontosis is ambigu-
ous and that the term should be eliminated from
periodontal nomenclatureÕ (86). Nevertheless, the
group also acknowledged the possible existence of a
form of periodontitis in adolescents and young adults
that was clinically different from the common Ôadult
periodontitisÕ found in older individuals (86).
In 1971, Paul Baer wrote a paper in which he sug-
gested that the term ÔperiodontosisÕ be retained (10).
He also supplied a definition based on some of the
clinical features of the disease, which has not been
significantly modified in the past four decades (10):
ÔPeriodontosis is a disease of the periodontium
occurring in an otherwise healthy adolescent, which
is characterized by a rapid loss of alveolar bone about
more than one tooth of the permanent dentition.
There are two basic forms in which it occurs. In one
form of the disease, the only teeth affected are the
first molars and incisors. In the other, more gener-
alized form, it may affect most of the dentition. The
amount of destruction manifested is not commen-
surate with the amount of local irritants present.Õ
He also indicated that the disease appeared to have
its onset in the circumpubertal period (i.e. between
the ages of 11 and 13 years), was more common in
females than males, and had a familial background.
Furthermore, he stated that, in a few patients, the
disease may be self-limiting as Ô…the loss of alveolar
bone may progress only to a certain point, and then
may remain stationary for many yearsÕ (10).
In the late 1970s and early 1980s, the idea that the
disease may be due to degeneration of cementum, or
any other components of the periodontium, was laid
to rest when it was shown that the condition was an
infection (49, 61, 62, 81, 94, 96) that could be effec-
tively treated by therapy based on excellent plaque
control (95). These findings were of major clinical
importance since infections were considered treat-
able, whereas degenerative diseases were deemed
beyond the scope of conventional therapeutic ap-
proaches. As a reflection of this changing opinion
regarding the etiology of the disease, Ôjuvenile peri-
odontitisÕ replaced ÔperiodontosisÕ as the preferred
term for the condition (48, 49, 57, 70, 81, 94). How-
ever, all of the other characteristics of the disease
listed by Baer in 1971 (10) have been retained. In the
1999 classification system, the name of the disease
was changed to localized aggressive periodontitis (3,
45).
Shared clinical features
In a general way, chronic and aggressive periodontitis
share many clinical features, but the specific details
of the shared features are not necessarily identical in
both forms of the disease. Nevertheless, it is well
established that they are both complex infections that
occur in susceptible hosts and are caused by biofilms
that form on tooth surfaces (37, 47, 66, 83, 96, 99). In
both cases, the disease-producing biofilms comprise
microorganisms that are components of the indige-
nous (normal) oral microbiota (7). In addition, host
inflammatory ⁄ immune reactions to the presence of
the biofilms are primarily responsible for the loss of
periodontal attachment and alveolar bone supporting
the teeth (26, 27, 78). Anti-infective treatment is
usually effective in the management of both chronic
and aggressive forms of periodontitis (23). The
eventual outcome of untreated disease is tooth loss.
One of the shared clinical characteristics of chronic
and aggressive periodontitis is that affected individ-
uals have no known medical or general health con-
ditions that might contribute to development of their
periodontitis. According to the 1999 classification (3),
if an individual has a systemic disease that can pro-
foundly modify the initiation and clinical course of
periodontal infections, the resulting periodontitis
should be classified as Ôperiodontitis as a manifesta-
tion of systemic diseaseÕ. Examples include severe
cases of plaque-induced periodontitis associated
with immunosuppression acquired via chemother-
apy (41), viral infection (44, 67) or any other means,
and inherited defects in neutrophil function (19, 20,
68, 87, 98), as well as other syndromic perturbations
in host–parasite interactions (1, 11, 17, 22, 24, 38, 39,
71, 73, 97). Therefore, individuals with significant and
powerful modifiers of the innate and adaptive
immune responses should not be classified as having
either chronic or aggressive periodontitis. The term
Ôperiodontitis as a manifestation of systemic diseaseÕ
should only be used when the systemic disease pro-
foundly impairs the ability of the host to cope with
the bacterial challenge associated with periodontitis.
13
Armitage & Cullinan
Exacerbation of the periodontal infection becomes so
marked that any existing periodontitis is transformed
into a clinically different entity. For example, an
uncomplicated case of chronic periodontitis super-
imposed on a patient with severe neutropenia be-
comes a periodontal infection with a significantly
modified clinical course. Effective treatment of such a
systemically modified infection requires a different
strategy than would be routinely used for a medically
healthy individual with chronic periodontitis.
This raises the interesting question ÔAt what point
does a modifier of host immune responses become so
important that the periodontitis becomes a manifes-
tation of that modifier?Õ. There is no simple answer to
this question. In a patient with severe chronic perio-
dontitis who also has poorly controlled type 2 diabe-
tes mellitus, there are excellent data to show that the
systemic disease (i.e. diabetes) significantly modifies
the course of the periodontal infection (35, 69, 84, 89).
It can be argued that the periodontal disease in such a
patient could properly be categorized as any of the
following: (i) diabetes-associated chronic periodonti-
tis, (ii) periodontitis as a manifestation of systemic
disease, or (iii) diabetes-associated periodontitis. In
the last two categories, omission of the term ÔchronicÕ
implies that the periodontitis has become a different
entity than a routine and relatively uncomplicated
form of slowly progressing periodontal disease. In this
case, for all practical purposes, it does not matter
what the condition is called so long as it is recognized
that medical management of the systemic disease is
an important component of successful treatment of
the periodontal infection. A similar situation exists in
heavy cigarette smokers whose longstanding habit is
clearly a powerful modifier of the severity of perio-
dontal infections (43, 72). Should a longtime heavy
smoker with severe chronic periodontitis be catego-
rized as having: (i) chronic periodontitis in a smoker,
(ii) smoking-associated chronic periodontitis, or
simply (iii) smoking-associated periodontitis? Again,
in clinical practice, it does not matter what the con-
dition is called so long as it is recognized that the
treatment of the periodontal infection should
include recommendation or inclusion of a program
of smoking cessation.
Classification systems versus
diagnoses
Classification systems and diagnoses often serve
different functions when multifactorial diseases or
conditions are under consideration. Such diseases
14
are usually associated with complex combinations of
incompletely understood risk factors and etiological
agents. Simple cause-and-effect dual-purpose clas-
sification and diagnostic statements (e.g. strepto-
coccal sore throat) are not possible because of an
insufficient understanding of the etiopathogenesis of
the disease. Classification systems for these types of
diseases are useful in studying disease patterns and
types in large populations of patients. They can
provide a framework for studying the epidemiology,
etiology and treatment outcomes for a given group
of similar diseases (6). Such systems can serve as a
starting point for considering a diagnosis for a given
patient, but are ill-suited for direct and rigid appli-
cation to individuals. Indeed, one of the main
objections to the 1999 classification has been from
those who have found it difficult to apply the system
to individual patients and have therefore advocated
a nominalistic or descriptive approach to the clas-
sification of periodontitis (9, 59, 91, 92). Van der
Velden (93) has stated that it would be worthless to
group periodontal diseases on the basis of their
probable causes since Ô…the causal web for perio-
dontitis is so complex and involves so many differ-
ent constellations that a classification based on
etiology is effectively precludedÕ. Part of the problem
for those who have resisted acceptance of the 1999
system is that they have attempted to use a classi-
fication scheme to generate clinical diagnoses for
individual patients. As mentioned above, any exist-
ing classification system for periodontal infections
cannot be simply applied to generate diagnoses for
patients with these types of multifactorial diseases.
Such systems are not intended to be rigidly and
inflexibly used to generate a diagnosis for an indi-
vidual patient. The best these systems can do is
to serve as a first step in generating a clinically
meaningful diagnosis for an individual.
A diagnosis is a summary statement of the clini-
cianÕs best estimate regarding the disease or condi-
tion detected in a given patient. It is derived from a
thorough analysis of all information collected during
a review of relevant data from medical ⁄ dental his-
tories, the results of diagnostic tests, and findings
from a careful clinical examination (5, 6). Most
importantly, a diagnosis should be a short and con-
cise statement that conveys an idea or mental picture
of what disease or condition is present in a specific
patient. It is extremely valuable in communication
with colleagues and provides a basis for thinking
about appropriate treatment approaches. For a vari-
ety of practical reasons, such as categorizing a dis-
ease for third-party payment purposes, it should be
 Comparison of the clinical features of chronic and aggressive periodontitis
possible to fit the diagnosis assigned to a specific
patient somewhere into a currently recognized or
widely used classification system. The fit of the
diagnosis into the classification system does not have
to be precise, somewhere in the general vicinity is
usually sufficient. Clinicians should avoid rigid
application of disease-category definitions of classi-
fication systems in arriving at a diagnosis. For
example, arguments among clinicians about whether
the patient has chronic or aggressive periodontitis are
pointless, especially if the proposed treatment is
going to be the same.
This flexibility is not possible for clinician scien-
tists who intend to carefully study the epidemiology,
etiology or treatment for a well-defined group of
periodontal infections. Prior to performing their
study, the investigators should use or adopt a clas-
sification system that can be reproducibly applied to
a study population. For example, if epidemiologists
intend to study the prevalence of severe generalized
aggressive periodontitis in a given population, they
must first agree upon an acceptable Ôcase definitionÕ
for the disease. Such a case definition must be able
to clearly distinguish individuals without overlap
with other disease categories. If a new anti-infective
treatment for generalized severe chronic periodon-
titis is going to be tested, investigators must agree
on the disease criteria (i.e. inclusion ⁄ exclusion cri-
teria) for potential study volunteers prior to starting
the study. Disease category definitions found in
classification systems can be extremely important in
planning most types of clinical studies. In these
situations, arguments among scientists about whe-
ther a potential study volunteer has chronic or
aggressive periodontitis are very important. Their
decision will influence how the results of the
investigation will be interpreted. For example, the
presence of severe disease does not necessarily
mean that the condition should be classified as
aggressive periodontitis. The case definition of
aggressive periodontitis needs to include as many of
the primary features as possible to discriminate
sufficiently between a severe case of chronic peri-
odontitis and aggressive periodontitis. Unfortu-
nately, at the current time, there is no universal
agreement among researchers as to the optimal or
best case definitions for studies of periodontal dis-
eases (25, 56, 74). In addition, no existing or pro-
posed classification system is able to provide precise
guidelines for selecting an optimal case definition.
This problem has been around for a long time and
will not be resolved anytime soon. Fortunately, the
case definition problem is not a major issue in the
management of specific patients in clinical practice,
as the diagnosis is tailor-made for the individual.
Significant clinical differences
between chronic and aggressive
periodontitis
Although similar in many general or overall respects,
it has been suggested that chronic and aggressive
forms of periodontitis have a number of significant
clinical differences including: (i) age of onset (i.e.
detection), (ii) rates of progression, (iii) patterns of
destruction, (iv) clinical signs of inflammation and (v)
relative abundance of plaque and calculus. Indeed,
combinations of these clinical differences are the
primary basis for placing affected individuals into
one of the three major categories of periodontitis (i.e.
chronic periodontitis, localized aggressive periodon-
titis and generalized aggressive periodontitis).
Localized and generalized chronic periodontitis are
usually considered to be two clinical expressions of
the same disease. In both cases, there are similar
signs of inflammation (e.g. redness, swelling, bleed-
ing on probing) associated with moderate to heavy
deposits of plaque and calculus. They also share slow
rates of progression, affect similar populations (e.g.
age range, gender), and are associated with similar
genetic and environmental risk factors. Except for a
general tendency to exhibit bilateral symmetry (60),
no consistent pattern of destruction is usually ob-
served. In addition, there do not appear to be any
noticeable differences in the subgingival microbiota
(7) or histopathological features (82) between local-
ized and generalized forms of the disease.
In contrast, localized and generalized aggressive
periodontitis can be considered to be different dis-
eases. In localized aggressive periodontitis, especially
in its early stages, there are often only minimal signs
of clinical inflammation associated with a thin and
unimpressive biofilm on the affected tooth surfaces
(10). Fig. 1 shows a 17-year-old Hispanic female with
localized aggressive periodontitis on the mesial sur-
face of a mandibular first molar. There was only mild
inflammation, no detectable supragingival or sub-
gingival dental calculus, and the lesion was associ-
ated with a relatively thin biofilm. Fig. 2 shows the
appearance of a 15-year-old white male with gener-
alized aggressive periodontitis affecting most of the
permanent dentition. There were very heavy deposits
of plaque and calculus and extremely intense
gingival inflammation. Although there are extensive
15
Armitage & Cullinan
A in both conditions, with the only difference being the
B
Fig. 1. (A) Clinical appearance of the mandibular right
gingiva in a 17-year-old Hispanic female with localized
aggressive periodontitis. The mesial surface of the first
molar had a probing depth of 8 mm, with 7 mm of clinical
attachment loss. There was some bleeding on probing
immediately after the site was examined. Note that there
are no heavy deposits of supragingival dental plaque. (B)
Radiograph of the site shown in (A).
differences between the clinical appearance of the
patients shown in Figs 1 and 2, this striking contrast
is not always found when comparing the two dis-
eases. In some instances, the levels of inflammation
and amounts of plaque are approximately the same
A B
Fig. 2. (A) Clinical appearance of the gingival tissues in a
15-year-old white male with generalized aggressive perio-
dontitis. Note the intense gingival inflammation and heavy
deposits of plaque and calculus. Compare with the patient
16
number of affected teeth or pattern of damage (i.e.
localized to incisors and molars versus generalized
involvement). However, the two forms of aggressive
periodontitis appear to be associated with somewhat
different bacterial profiles in the subgingival micro-
biota (7) and have separate genetic risk factors (79).
Age of onset
The age of onset, or age at the time of detection, is an
important feature that has traditionally been used to
help place patients in either the aggressive or chronic
periodontitis category. The 1999 classification rec-
ommended deletion of age-dependent terms such as
ÔadultÕ and ÔjuvenileÕ periodontitis since age is not an
appropriate descriptor for use in diagnostic catego-
ries (3). There was considerable uncertainty about
setting arbitrary upper age limits for certain forms of
periodontitis. For example, it was not clear what
criteria should be used to distinguish between an
adult and a juvenile. Should one use legal definitions
for the age ranges of an adult versus juvenile, or
should an attempt be made to develop a more
biologically based definition? Therefore, the age-
dependent categories were eliminated from the
classification.
Nevertheless, age is still an important characteristic
that can be useful in differentiating between chronic
and aggressive forms of periodontitis. Given similar
amounts of periodontal damage (i.e. probing depths,
attachment loss, alveolar bone resorption), people
with aggressive periodontitis are significantly youn-
ger than individuals with chronic periodontitis. The
age difference is a general feature that can be useful
in preliminarily deciding whether a patient has
chronic or aggressive periodontitis. However, there is
shown in Fig. 1. (B) Representative radiographs showing
examples of the massive bone loss that was present on
virtually all teeth.
 Comparison of the clinical features of chronic and aggressive periodontitis
no fixed or arbitrary upper age limit that can be used
for this purpose. It is a mistake to rigidly adhere to an
arbitrary age when deciding whether a patient has
chronic or aggressive periodontitis. It is pointless for
clinicians to argue about what is the best cut-off age
to distinguish between aggressive and chronic perio-
dontitis (e.g. should it be 30 or 35 years?). In fact, the
diagnostic label is unimportant as the treatment of a
30-year-old patient with severe periodontitis will
probably be the same regardless of what the disease
is called. However, for research purposes and
depending on the research question, it may well be
reasonable to include age limits in case definitions to
reduce heterogeneity within study groups and to
ensure that there is no overlap in disease categories.
Rates of progression
The rate at which loss of supporting periodontal tis-
sues occurs has long been considered an important
characteristic by which chronic and aggressive forms
of periodontitis can be clinically distinguished.
Chronic periodontitis has traditionally been viewed
as a slowly progressing disease, whereas aggressive
forms of periodontitis progress at a rapid rate (10).
Baer estimated that the loss of attachment in
aggressive periodontitis patients progressed three or
four times faster than in cases of chronic periodon-
titis (10).
Figures 3 and 4 show the progression of chronic
periodontitis in posterior regions of the mandible
over a 9-year period in a white male who was 51 years
of age at baseline. Periodontal treatment during this
A B
C D
observation period was provided by the general
dentist, and included scaling and root planing at
baseline followed by coronal polishing (Ôoral pro-
phylaxisÕ) once a year. Appropriate periodontal
maintenance therapy was not provided. The average
annual rate of progression was approximately
0.25 mm at affected sites.
Rates of progression of various forms of perio-
dontitis are difficult to study in a formal or organized
way since there are many factors that influence how
rapidly periodontal tissues are destroyed. Progression
of periodontal diseases is affected by the effective-
ness of oral hygiene habits, access to dental care,
genetically controlled susceptibility to periodontal
infections, certain systemic diseases (e.g. diabetes
mellitus) and other powerful host-response modifiers
(e.g. smoking). Several longitudinal studies have
demonstrated that there is a tendency for increased
progression of periodontitis with age (2, 8, 52, 65, 77).
In the few studies that have been performed on the
natural history of progression of chronic periodon-
titis, the disease was found to progress at a full-
mouth average rate of approximately 0.2 mm ⁄
year (15, 50, 52, 53, 65, 88). On a population basis,
untreated chronic periodontitis progresses slowly
over time, and the 0.2 mm ⁄ year rate appears to be
applicable to sites without prior attachment loss as
well as to those with advanced disease at the initial
examination (50).
In contrast, there are forms of periodontitis with
faster rates of progression. In a longitudinal study of
Sri Lankan workers on a tea plantation, one group
of individuals lost, on a full-mouth basis, an average
Fig. 3. Progression of bone loss over
a 9-year period in a patient with
chronic periodontitis without fol-
low-up periodontal maintenance
care. No maintenance care was gi-
ven after an initial subgingival scal-
ing at the baseline visit. (A) Age
51 years at baseline prior to sub-
gingival scaling by a general dentist.
(B) Age 51 years, immediately after
scaling. (C) Age 56 years; note the
additional loss of bone on the distal
surface of the first molar. (D) Age
60 years; note the additional loss of
bone.
17
Armitage & Cullinan
A B
C
of 0.46 mm ⁄ year (53). This group was referred to as
Ôrapidly progressiveÕ, and would probably be classi-
fied as generalized aggressive periodontitis using the
current system of nomenclature. However, in a lon-
gitudinal assessment of young individuals with
localized aggressive periodontitis (n = 40) or gener-
alized aggressive periodontitis (n = 48), it was found
that the average full-mouth rate of attachment loss
was only 0.06 mm ⁄ year (36). The reasons for this
difference are unclear, but many of the patients in the
latter study received some form of periodontal ther-
apy. Further, use of full-mouth averages probably
had a diluting effect, especially in the case of local-
ized aggressive periodontitis where the majority of
sites are unaffected and show no attachment loss.
The most compelling argument indicating that
aggressive periodontitis progresses at a rapid rate
comes from case series and epidemiological reports
showing extensive periodontal damage at some sites
in adolescents and young adults (10, 18, 49, 57, 76).
Fig. 5 shows the relatively rapid progression of
untreated localized aggressive periodontitis over an
8-year period in a white female who was 12 years of
age at baseline. At affected sites, the annual rate of
progression was approximately 1–2 mm. The radio-
graphs were taken in the early 1960s and were re-
trieved from old dental records. The patient was
regularly seen by her general dentist, who assigned
her a diagnosis of ÔperiodontosisÕ. She was provided
with oral prophylaxis at 6-month intervals. Her den-
tist believed that she had a degenerative periodontal
disease that would not respond to anti-infective
therapy. This is an excellent example of how a diag-
18
Fig. 4. Progression of bone loss over
a 9-year period in a patient with
chronic periodontitis without fol-
low-up periodontal maintenance
care. This is the same patient as
shown in Fig. 3. (A) Age 51 years,
immediately after subgingival scal-
ing. (B) Age 56 years; note the addi-
tional bone loss. (C) Age 60 years;
note the additional bone loss
including the furcation area of the
first molar.
nostic label (i.e. periodontosis) led her dentist to
believe that her disease was untreatable. Most den-
tists trained prior to 1960 were taught that the disease
would not respond to conventional therapy.
There is a long-standing clinical impression that
the rate of disease progression slows down or stops
entirely in a small percentage of patients with local-
ized aggressive periodontitis (10, 45). Baer (10)
referred to this phenomenon as Ôburn outÕ of the
disease. A possible example of this apparent self-
limiting feature of the disease is shown in Fig. 6, in
which there was no radiographic evidence of pro-
gression of untreated localized aggressive periodon-
titis in a white female from the age of 12 to 16 years.
The patient was temporarily lost to follow-up and
received no periodontal therapy during the 4-year
period. Fig. 7 shows a 24-year-old African-American
female who had periodontal destruction localized to
all first molars and two mandibular incisors in a
pattern consistent with that observed in cases of
localized aggressive periodontitis. She had no history
of any periodontal therapy and her periodontal
tissues had minimal to no signs of clinical inflam-
mation. In these two cases, it is possible that the
periodontal disease had merely gone into remission
and could become active sometime in the future.
There are data suggesting that the progression of
periodontal diseases is an episodic phenomenon,
with alternating periods of exacerbation and remis-
sion (28). In a longitudinal study of patients with ei-
ther localized or generalized forms of aggressive
periodontitis, Gunsolley et al. (36) noted that the
localized form appeared to be a Ôstable disease in
 Comparison of the clinical features of chronic and aggressive periodontitis
A B
C D
E F
G 1960s. The patientÕs general dentist
most individualsÕ, whereas individuals with the gen-
eralized form continued to lose periodontal attach-
ment and teeth over time. Despite this observation, it
should not be assumed that all, or even most, cases of
localized aggressive periodontitis will be self-limiting.
Indeed, in the study by Gunsolley et al. (36), it was
found that two of the 42 patients initially diagnosed
with localized aggressive periodontitis were re-clas-
sified as having the generalized form of the disease at
the end of a 3-year observation period. This is con-
sistent with the conclusions of Hørmand & Frandsen
(40) and Saxén (75) who suggested, based on cross-
sectional data, that localized forms of the disease
become generalized with increasing age.
Fig. 8 shows radiographs of a 20-year-old white
female who had localized aggressive periodontitis
Fig. 5. Progression of bone loss over
an 8-year period in a white female
with untreated localized aggressive
periodontitis. Radiographs were re-
trieved from dental records from the
believed that the patient had an
untreatable degenerative disease
(i.e. ÔperiodontosisÕ). (A) Age 12 years
+ 2 months. (B) Age 13 years + 4
months. (C) Age 14 years + 1 month.
(D) Age 16 years + 1 month. (E) Age
18 years + 7 months. (F) Age 19
years + 5 months. (G) Age 20 years
+ 4 months.
that was not treated and appears to have spread to
the mandibular bicuspids and the cuspid on the
mandibular left side. It is of interest that the infection
on the mandibular right side does not appear to have
involved the bicuspids and cuspid. This is the same
patient who is shown in Fig. 5 whose periodontal
infection was mistakenly thought to be an untreat-
able degenerative disease (i.e. periodontosis) by her
general dentist in the 1960s. It is clear that the peri-
odontal infection is not limited to the permanent first
molars and incisors in this patient. At the present
time, it is not possible to predict when, or if, a peri-
odontal infection will go into remission or become
self-limiting. It must be assumed that localized
periodontal infections have the potential to spread to
adjacent teeth and must be treated accordingly.
19
Armitage & Cullinan
A B
C aggressive periodontitis over a
It is possible that instances where localized
aggressive periodontitis appears to spread to adjacent
teeth and acquire a generalized pattern of destruction
are due to the development of a new periodontal
infection rather than the spread of an existing one.
This possibility is supported by the observation of
multiple types of periodontitis in the same family (54,
58, 85) or in a single individual (80). This issue is
primarily of academic interest as it is likely that
treatment would be the same for a spreading infec-
tion or superimposition of a new infection on an old
one.
Patterns of destruction
In cases of chronic periodontitis, there is no consis-
tent pattern to the number and types of teeth in-
volved. The disease can be localized to a few teeth or
can affect the entire dentition. There is a slight ten-
dency for the destruction to exhibit bilateral sym-
metry (60), but there is no well-defined pattern in
most cases. In cases of generalized aggressive peri-
odontitis, most permanent teeth are usually affected.
There are no evidence-based criteria to determine
when a localized periodontal infection becomes
generalized. The 1999 classification (45) suggested
that the pattern of damage in generalized aggressive
periodontitis includes situations where there is
Ô…generalized interproximal attachment loss affect-
ing at least three permanent teeth other than first
molars and incisorsÕ. This is similar to the criteria
used by Burmeister et al. (18), who suggested that a
generalized pattern of destruction is present if there
20
Fig. 6. Possible example of self-
limiting of untreated localized
4-year period in a white female. (A)
Age 12 years, radiographic appear-
ance of bone loss on the distal of the
first molar. (B) Age 16 years, radio-
graphic appearance of the same site
4 years later. The patient was lost to
follow-up and had received no
periodontal therapy in the inter-
vening period. (C) Clinical appear-
ance at age 16 years.
is Ô…attachment loss on 8 or more teeth, at least 3 of
which were not first molars or incisorsÕ. These case
definitions may be useful for the purposes of epide-
miological investigations but they lose most of their
clinical utility in the diagnosis and management of an
individual patient. For example, if only eight teeth are
affected, most clinicians would characterize the
disease as a localized rather than a generalized
condition.
It was the consensus of the group at the 1999
Classification Workshop that the extent of the dis-
ease be considered localized if £ 30% of the sites (or
teeth) are affected, and generalized if > 30% of the
sites (or teeth) are involved (3). This suggestion was
not based on any data and was completely arbitrary.
The only reason for including a description of the
extent of the disease is to facilitate communication
among colleagues as to the general location of the
problem. For example, in written communications,
most clinicians simply state the diagnosis (e.g.
chronic periodontitis) followed by a list of the af-
fected teeth. When the list of the affected teeth be-
comes quite long, it is often easier to merely indicate
that the disease is generalized. The fallacy of rigidly
using the 30% cut-off point between localized and
generalized patterns of disease is nicely demon-
strated in a classic case of localized aggressive peri-
odontitis in which 12 teeth are affected (i.e. all
incisors and first molars). If such a patient has only
28 teeth, then 12 ⁄ 28 or 42.9% teeth have the dis-
ease. Therefore, if the 30% figure is rigidly applied,
some individuals with localized aggressive perio-
dontitis paradoxically have generalized disease!
 Comparison of the clinical features of chronic and aggressive periodontitis
A B
Fig. 7. Possible example of self-limiting of untreated
localized aggressive periodontitis in a 24-year-old African
American female. (A) Gingival tissues show no obvious
clinical signs of inflammation. (B) Healthy gingival tissues
on anterior palate. (C) Slight gingival inflammation with
visible supragingival calculus on the distal surface of the
mandibular left central incisor. (D) Radiographs of the
anterior teeth showing bone loss isolated to a few sites. (E)
Fig. 9 shows a classic case of localized aggressive
periodontitis in a 19-year-old white male in whom 12
permanent teeth were affected (i.e. all maxillary and
mandibular incisors and first molars). This pattern is
probably the exception rather than the rule (18). In
many cases, a subset of these teeth are affected, often
only including the first molars and a few incisors. In
the case series reported by Liljenberg & Lindhe (49),
of the eight patients with localized aggressive perio-
dontitis, the number of affected teeth per patient
C
Radiographically visible bone loss localized to all first
molars. (F) Clinical and radiographic appearance of the
mandibular right first molar. Note the absence of clinically
visible inflammation and supragingival plaque. There was
slight bleeding on probing of the mesial and distal inter-
proximal surfaces. Based on these findings, it is impossi-
ble to determine whether the disease is in remission or
progressing.
ranged from 3 to 6, whereas in the seven patients
with chronic periodontitis, the number ranged from
18 to 28. This is consistent with the observations of
other investigators who reported similar variations in
the patterns or numbers of affected teeth (12, 18, 40,
42, 76).
In some instances, the isolated periodontal damage
associated with localized aggressive periodontitis can
be mimicked by an infection around a retained root
fragment of a primary tooth. Fig. 10A shows a
21
Armitage & Cullinan
A B
C
radiograph from a 10-year-old female with a retained
root fragment of a carious primary tooth adjacent to
the mesial surface of a mandibular left permanent
first molar (i.e. tooth 19). Similar cases have been
reported in the literature (55). Bitewing radiographs
(Fig. 10B,C) show that the bone loss was only on the
left side, and that this patient had a severe problem
with multiple carious teeth. The root fragment was
most certainly heavily colonized by bacteria, which
presumably resulted in a biofilm-induced destruction
of the periodontal tissues on the permanent molar.
An appropriate working diagnosis for such a situation
might be: Ôsevere periodontitis on the mesial of tooth
19 associated with a retained root fragment of a pri-
mary molarÕ. In this case, it is unnecessary to include
any decision on the type of periodontitis (i.e. chronic
versus aggressive). It serves no purpose in the
management of the problem. Appropriate treatment
included removal of the root fragment and debride-
ment of the site.
The above case is a good example of the limitations
of any classification system when a diagnostic state-
ment for a specific patient is being generated.
22
Fig. 8. Radiographic appearance of
untreated localized aggressive perio-
dontitis in a 20-year-old white
female. This is the same patient as
shown in Fig. 5. (A) On the right
side, the periodontal infection has
apparently spread to the adjacent
teeth. (B) On the left side, there is no
radiographic evidence that the dis-
ease has affected the adjacent
bicuspids. (C) Radiographs showing
the pattern of bone loss in the entire
mandibular anterior region.
According to the 1999 classification system (3), the
patientÕs problem could be classified as a periodontal
abscess (associated with a root fragment) or a gingi-
val lesion (not otherwise specified). No clinically
useful purpose is served by forcing the patientÕs
problem into the existing matrix of a classification
system. Although not likely, the working diagnosis
might be wrong, and the patient may actually have
localized aggressive periodontitis isolated to the
mesial surface of a single molar.
Clinical signs of inflammation
One of the features of localized aggressive perio-
dontitis described originally was the relatively low
level of gingival inflammation (e.g. redness, swelling)
compared with other forms of periodontitis (10, 29–
33, 63). It was this observation that was partly
responsible for early authors concluding that the
condition was a degenerative non-inflammatory dis-
ease. In fact, most patients with the disease often
exhibit some clinical inflammation at affected sites,
such as bleeding upon gentle probing along with
 Comparison of the clinical features of chronic and aggressive periodontitis
A D
Fig. 9. Localized aggressive periodontitis in a 19-year-old
white male in whom all permanent incisors and first
molars were affected. There was no significant involve-
ment on any of the other teeth. (A) Facial view. (B) Palatal
view of maxilla showing slight inflammation (i.e. gingival
A
B
Fig. 10. (A) Radiograph showing periodontal damage on
the mesial surface of a mandibular first permanent molar
in a 10-year-old white male. The lesion resembles the
pattern of bone loss found in cases of localized aggressive
periodontitis. However, infection around a retained root
slight redness and swelling of the gingival margin
(Fig. 9B,C). Burmeister et al. (18) examined a popu-
lation of these patients and found that the gingival
index, gingival bleeding and suppuration scores at
sites with attachment loss were equally high in pa-
tients with localized or generalized forms of aggres-
sive periodontitis. Late in the disease, when there are
redness) around all incisors. (C) Lingual view of lower
anterior teeth showing gingival inflammation. (D) Re-
presentative radiographs showing massive bone loss
confined to first molars and incisors.
fragment from a primary tooth is the likely reason for the
bone loss. (B) Bitewing radiographs showing that bone
loss is only found at the site with the retained root.
Note the numerous carious lesions visible in the radio-
graphs.
very deep probing depths together with massive loss
of periodontal support, the clinical inflammation can
be quite marked (Fig. 11). In contrast, patients with
generalized aggressive or chronic forms of perio-
dontitis usually present with relatively intense gingi-
val inflammation (Figs. 2 and 12). The reasons for
these differences are not understood, but they are
23
Armitage & Cullinan
A B
C D
Fig. 12. Severe inflammation, marked gingival recession,
and heavy deposits of calculus in a 47-year-old white male
with chronic periodontitis.
probably related to the time of initial presentation
and hence amounts of microbial biomass that form
on tooth surfaces over time. In localized aggressive
periodontitis, the biofilms that form on tooth sur-
faces are often quite thin, but these deposits are
usually quite thick and abundant in the other forms
of periodontitis (51).
Plaque and calculus formation
In many patients with localized aggressive perio-
dontitis, there are only thin deposits of dental plaque
(i.e. biofilm), with little or no calculus (10, 49, 51).
However, sites affected by the disease are not bio-
film-free. Electron microscopic observations of teeth
extracted because of localized aggressive periodon-
titis revealed that root surfaces were covered with
thin deposits of gram-negative coccoid and filamen-
tous bacteria together with other microorganisms.
24
Fig. 11. Late signs of localized
aggressive periodontitis. Migration
and drifting of teeth with marked
gingival inflammation. (A) Facial
view of maxillary anteriors. Note the
diastema between the central and
lateral incisor. (B) Palatal view. (C)
Facial view of mandibular incisors.
One central incisor has been lost.
(D) Lingual view of the same site.
The microbiota on the root surfaces was described as
Ô…relatively sparse and simpleÕ (51). In contrast, teeth
with chronic periodontitis usually have very complex
and thick deposits of polymicrobial communities on
affected root surfaces (51). In addition, population
surveys of patients with localized aggressive perio-
dontitis have shown that there are clinically detect-
able biofilms at affected sites (18).
Summary and Conclusions
Overall, while most clinicians would agree that
aggressive forms of periodontitis exist as clinical
entities, the clinical distinction between chronic and
aggressive periodontitis (especially generalized) is
not clear cut. This may not be all that significant from
a treatment perspective, in so far as individualized
anti-infective therapies are effective for both forms of
the disease. However, from a research perspective, it
is essential that these diseases be clearly distin-
guished in order to gain a complete understanding of
their etiology and pathogenesis. The relative lack of
clinical inflammation often associated with the
localized molar-and-incisor form of aggressive peri-
odontitis has been commented on for almost
100 years, and it is generally accepted that this form
of the disease is associated with a thin biofilm, at
least in its early stages. In contrast, the presence of
clinical inflammation in generalized aggressive peri-
odontitis appears to be similar to that observed in
chronic periodontitis, and in this situation age of
onset and family history are important additional
criteria for either diagnosis or classification. It is also
generally recognized that chronic periodontitis may
subsequently be superimposed on both localized and
generalized forms of aggressive periodontitis. While
 Comparison of the clinical features of chronic and aggressive periodontitis
this may have little bearing on the treatment of such
cases, it could have an enormous impact on both the
design and interpretation of research studies, whe-
ther basic science or clinical. This highlights the
essential difference between a diagnosis and a clas-
sification, whereby a diagnosis is the clinicianÕs best
guess, leading on to a treatment plan, whereas a
classification does not allow such flexibility, requiring
non-overlapping case definitions for research pur-
poses if the underlying etiology of these diseases is
ever to be fully elucidated.
References
1. Alaluusua S, Kivitie-Kallio S, Wolf J, Haavio M-L, Asikainen
S, Pirinen S. Periodontal findings in Cohen syndrome
with chronic neutropenia. J Periodontol 1997: 68:
473–478.
2. Albandar JM, Rise J, Gjermo P, Johansen JR. Radiographic
quantification of alveolar bone level changes. A 2-year
longitudinal study in man. J Clin Periodontol 1986: 13:
195–200.
3. Armitage GC. Development of a classification system for
periodontal diseases and conditions. Ann Periodontol
1999: 4: 1–6.
4. Armitage GC. Classifying periodontal diseases – a long-
standing dilemma. Periodontol 2000 2002: 30: 9–23.
5. Armitage GC. Periodontal diagnoses and classification of
periodontal diseases. Periodontol 2000 2004: 34: 9–21.
6. Armitage GC. Diagnosis and classification of periodontal
diseases and conditions: current and future challenges. In:
Bartold PM, Ishikawa I, Zhang J, editors. A perspective of
periodontal-systemic relationships for the Asian Pacific
region. Adelaide, Australia: Asian Pacific Society of
Periodontology, 2008: 12–19.
7. Armitage GC. Comparison of the microbiological features
of chronic and aggressive periodontitis. Periodontol 2000
2010: 53: 70–88.
8. Axelsson P, Lindhe J. Effect of controlled oral hygiene
procedures on caries and periodontal disease in adults.
J Clin Periodontol 1981: 8: 239–248.
9. Baelum V, Lopez R. Defining and classifying periodontitis:
need for a paradigm shift? Eur J Oral Sci 2003: 111: 2–6.
10. Baer PN. The case for periodontosis as a clinical entity.
J Periodontol 1971: 42: 516–520.
11. Bailleul-Forestier I, Monod-Broca J, Benkerrou M, Mora F,
Picard B. Generalized periodontitis associated with Ché-
diak–Higashi syndrome. J Periodontol 2008: 79: 1263–
1270.
12. Benjamin SD, Baer PN. Familial patterns of advanced
alveolar bone loss in adolescence (periodontosis). Perio-
dontics 1967: 5: 82–88.
13. Black GV. Diseases of the peridental membrane having
their beginning at the margin of the gum. In: Litch WF,
editor. American system of dentistry, volume I. Philadel-
phia: Lea Brothers, 1886: 953–1079.
14. Black GV. Chronic suppurative pericementitis. A work on
special dental pathology, 1st edn. Chicago: Medico-Dental
Publishing Co., 1915: 158–184.
15. Brown LJ, Löe H. Prevalence, extent, severity and pro-
gression of periodontal disease. Periodontol 2000 1993: 2:
57–71.
16. Brown LJ, Albandar JM, Brunelle JA, Löe H. Early-onset
periodontitis: progression of attachment loss during
6 years. J Periodontol 1996: 67: 968–975.
17. Buduneli N, Baylas H, Aksu G, Kütükçüler N. Prepubertal
periodontitis associated with chronic granulomatous dis-
ease. J Clin Periodontol 2001: 28: 589–593.
18. Burmeister JA, Best AM, Palcanis KG, Caine FA, Ranney
RR. Localized juvenile periodontitis and generalized se-
vere periodontitis: clinical findings. J Clin Periodontol
1984: 11: 181–192.
19. Carlsson G, Wahlin Y-B, Johansson A, Olsson A, Eriksson
T, Claesson R, Hänström L, Henter J-I. Periodontal disease
in patients from the original Kostman family with severe
congenital neutropenia. J Periodontol 2006: 77: 744–751.
20. Dababneh R, Al-Wahadneh A, Hamadneh S, Khouri A,
Bissada NF. Periodontal manifestation of leukocyte adhe-
sion deficiency type I. J Periodontol 2008: 79: 764–768.
21. Davis CG. Gum and alveolar diseases. Dental Cosmos 1879:
21: 192–201.
22. Deas DE, Mackey SA, McDonnell HT. Systemic disease
and periodontitis: manifestations of neutrophil dysfunc-
tion. Periodontol 2000 2003: 32: 82–104.
23. Deas DE, Mealey BL. Response of chronic and aggressive
periodontitis to treatment. Periodontol 2000 2010: 53: 154–
166.
24. Delcourt-Debruyne EMC, Boutigny HRA, Hildebrand HF.
Features of severe periodontal disease in a teenager with
Chédiak–Higashi syndrome. J Periodontol 2000: 71: 816–
824.
25. Demmer RT, Papapanou PN. Epidemiologic patterns of
chronic and aggressive periodontitis. Periodontol 2000
2010: 53: 28–44.
26. Gemmell E, Yamazaki K, Seymour GJ. Destructive perio-
dontitis lesions are determined by the nature of the lym-
phocyte response. Crit Rev Oral Biol Med 2002: 13: 17–34.
27. Gemmell E, Seymour GJ. Immunoregulatory control of
Th1 ⁄ Th2 cytokine profiles in periodontal disease. Perio-
dontol 2000 2004: 35: 21–41.
28. Goodson JM, Tanner ACR, Haffajee AD, Sornberger GC,
Socransky SS. Patterns of progression and regression of
advanced destructive periodontal disease. J Clin Period-
ontol 1982: 9: 472–481.
29. Gottlieb B. Zur Aetiologie und Therapie der Alveolarpy-
orrhoe. Z Stomatol 1920: 18: 59–82.
30. Gottlieb B. Aetiologie und Prophylaxe der Zahnkaries.
Z Stomatol 1921: 19: 129–132.
31. Gottlieb B. Der Epithelansatz am Zahne. Dtsch Monatsschr
Zahnheilk 1921: 39: 142–147.
32. Gottlieb B. Die diffuse Atrophie des Alveoarknochens.
Weitere Beiträge zur Kenntnis des Alevolarschwundes und
dessen Wiedergutmachung durch Zementwachstum. Z
Stomatol 1923: 21: 195–201.
33. Gottlieb B. The formation of the pocket: diffuse atrophy of
alveolar bone. J Am Dent Assoc 1928: 15: 462–476.
34. Gottlieb B. The new concept of periodontoclasia. J Peri-
odontol 1946: 17: 7–23.
35. Graves DT, Liu R, Oates TW. Diabetes-enhanced inflam-
mation and apoptosis – impact on periodontal pathosis.
Periodontol 2000 2007: 45: 128–137.
25
Armitage & Cullinan
36. Gunsolley JC, Califano JV, Koertge TE, Burmeister JA,
Cooper LC, Schenkein HA. Longitudinal assessment
of early onset periodontitis. J Periodontol 1995: 66:
321–328.
37. Haffajee AD, Teles RP, Socransky SS. The effect of perio-
dontal therapy on the composition of the subgingival
microbiota. Periodontol 2000 2006: 42: 219–258.
38. Hamilton RE Jr, Giansanti JS. Chediak–Higashi syndrome.
Report of a case and review of the literature. Oral Surg
Oral Med Oral Pathol 1974: 37: 754–761.
39. Hart TC, Shapira L. Papillon–Lefèvre syndrome. Perio-
dontol 2000 1994: 6: 88–100.
40. Hørmand J, Frandsen A. Juvenile periodontitis. Localiza-
tion of bone loss in relation to age, sex, and teeth. J Clin
Periodontol 1979: 6: 407–416.
41. Hou G-L, Tsai CC. Oral manifestations of agranulocytosis
associated with methimazole therapy. J Periodontol 1988:
59: 244–248.
42. Kim KJ, Kim DK, Chung CP, Son S. Longitudinal moni-
toring for disease progression of localized juvenile perio-
dontitis. J Periodontol 1992: 63: 806–811.
43. Labriola A, Needleman I, Moles DR. Systematic review of
the effect of smoking on nonsurgical periodontal therapy.
Periodontol 2000 2005: 37: 124–137.
44. Lamster IB, Grbic JT, Bucklan RS, Mitchell-Lewis D,
Reynolds HS, Zambon JJ. Epidemiology and diagnosis of
HIV-associated periodontal diseases. Oral Dis 1997:
3(Suppl.): S141–S148.
45. Lang N, Bartold PM, Cullinan M, Jeffcoat M, Mombelli A,
Murakami S, Page R, Papapanou P, Tonetti M, Van Dyke T.
Consensus report – aggressive periodontitis. Ann Period-
ontol 1999: 4: 53.
46. Lavine WS, Maderzao EG, Stolman J, Ward PA, Cohen RB,
Greenblatt I, Robertson PB. Impaired neutrophil chemo-
taxis in patients with juvenile and rapidly progressive
periodontitis. J Periodontal Res 1979: 14: 10–19.
47. Ledder RG, Gilbert P, Huws SA, Arons L, Ashley MP, Hull
PS, McBain AJ. Molecular analysis of the subgingival
microbiota in health and disease. Appl Environ Microbiol
2007: 73: 516–523.
48. Lehner T, Wilton JMA, Ivanyi L, Manson JD. Immuno-
logical aspects of juvenile periodontitis (periodontosis).
J Periodontal Res 1974: 9: 261–272.
49. Liljenberg B, Lindhe J. Juvenile periodontitis. Some
microbiological, histopathological and clinical character-
istics. J Clin Periodontol 1980: 7: 48–61.
50. Lindhe J, Haffajee AD, Socransky SS. Progression of
periodontal disease in adults subjects in the absence of
periodontal therapy. J Clin Periodontol 1983: 10: 433–442.
51. Listgarten MA. Structure of the microbial flora associated
with periodontal health and disease in man. A light and
electron microscopic study. J Periodontol 1976: 47: 1–18.
52. Löe H, Anerud A, Boysen H, Smith M. The natural history
of periodontal disease in man. The rate of periodontal
destruction before 40 years of age. J Periodontol 1978: 49:
607–620.
53. Löe H, Anerud A, Boysen H, Morrison E. Natural history of
periodontal disease in man. Rapid, moderate and no loss
of attachment in Sri Lankan laborers 14 to 46 years. J Clin
Periodontol 1986: 13: 431–440.
54. Long JC, Nance WE, Waring P, Burmeister JA, Ranney RR.
Early onset periodontitis: a comparison and evaluation of
26
two proposed modes of inheritance. Genet Epidemiol
1987: 4: 13–24.
55. Mahan CJ, Hurt WC. Retained deciduous tooth fragments
and periodontal lesions: radiographic, clinical, and histo-
logic observations. Oral Surg Oral Med Oral Pathol 1973:
35: 708–714.
56. Manau C, Echeverria A, Agueda A, Guerrero A, Echeverria
JJ. Periodontal disease definition may determine the
association between periodontitis and pregnancy out-
come. J Clin Periodontol 2008: 35: 385–397.
57. Manson JD, Lehner T. Clinical features of juvenile perio-
dontitis (periodontosis). J Periodontol 1974: 45: 636–640.
58. Marazita ML, Burmeister JA, Gunsolley JC, Koertge TE,
Lake K, Schenkein HA. Evidence for autosomal dominant
inheritance and race-specific heterogeneity in early-onset
periodontitis. J Periodontol 1994: 65: 623–630.
59. Meyer J, Lallam-Laroye C, Dridi M. Aggressive periodontitis
– what exactly is it? J Clin Periodontol 2004: 31: 586–587.
60. Mombelli A, Meier C. On the symmetry of periodontal
disease. J Clin Periodontol 2001: 28: 741–745.
61. Newman MG, Socransky SS, Savitt ED, Propas DA, Craw-
ford A. Studies on the microbiology of periodontosis.
J Periodontol 1976: 47: 373–379.
62. Newman MG, Socramsky SS. Predominant cultivable
microbiota in periodontosis. J Periodontal Res 1977: 12:
120–128.
63. Orban B, Weinmann JP. Diffuse atrophy of the alveolar
bone (periodontosis). J Periodontol 1942: 13: 31–45.
64. Page RC, Altman LC, Ebersole JL, Vandesteen GE, Dahl-
berg WH, Williams BL, Osterberg SK. Rapidly progressive
periodontitis. A distinct clinical condition. J Periodontol
1983: 54: 197–209.
65. Papapanou PN, Wennström JL, Gröndahl K. A 10-year
retrospective study of periodontal disease progression.
J Clin Periodontol 1989: 16: 403–411.
66. Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN,
Levanos VA, Saharabudhe A, Dewhirst FE. Bacterial
diversity in human subgingival plaque. J Bacteriol 2001:
183: 3770–3783.
67. Paster BJ, Russell MK, Alpagot T, Lee AM, Boches SK,
Galvin JL, Dewhirst FE. Bacterial diversity in necrotizing
ulcerative periodontitis in HIV-positive subjects. Ann
Periodontol 2002: 7: 8–16.
68. Pernu HE, Pajari UH, Lanning M. The importance of regular
dental treatment in patients with cyclic neutropenia. Fol-
low-up of 2 cases. J Periodontol 1996: 67: 454–459.
69. Preshaw PM, Foster N, Taylor JJ. Cross-susceptibility
between periodontal disease and type 2 diabetes mellitus:
an immunobiological perspective. Periodontol 2000 2007:
45: 138–157.
70. Ranney RR. Pathogenesis of periodontal disease. In:
International Conference on Research in the Biology
of Periodontal Disease. Chicago: American Academy of
Periodontology, 1977: 223–300.
71. Reuland-Bosma W, van der Reijden WA, van Winkelhoff AJ.
Absence of a specific subgingival microflora in adults with
DownÕs syndrome. J Clin Periodontol 2001: 28: 1004–1008.
72. Rivera-Hidalgo F. Smoking and periodontal disease.
Periodontol 2000 2003: 32: 50–58.
73. Saglam F, Atamer T, Onan U, Soydinç M, Kiraç K. Infantile
genetic agranulocytosis (Kostmann type). A case report.
J Periodontol 1995: 66: 808–810.
 Comparison of the clinical features of chronic and aggressive periodontitis
74. Savage A, Eaton KA, Moles DR, Needleman I. A systematic
review of definitions of periodontitis and methods that
have been used to identify this disease. J Clin Periodontol
2009: 36: 458–467.
75. Saxén L. Heredity of juvenile periodontitis. J Clin Period-
ontol 1980: 7: 276–288.
76. Saxén L, Murtomaa H. Age-related expression of juvenile
periodontitis. J Clin Periodontol 1985: 12: 21–26.
77. Schätzle M, Löe H, Lang NP, Heitz-Mayfield LJA, Bürgin
W, Ånerud Å, Boysen H. Clinical course of chronic peri-
odontitis. III. Patterns, variations and risks of attachment
loss. J Clin Periodontol 2002: 30: 909–918.
78. Schenkein HA. Host responses in maintaining periodontal
health and determining periodontal disease. Periodontol
2000 2006: 40: 77–93.
79. Shapira L, Eizenberg S, Sela MN, Soskolne A, Brautbar H.
HLA A9 and B15 are associated with the generalized form,
but not the localized form, of early-onset periodontal
diseases. J Periodontol 1994: 65: 219–223.
80. Shapira L, Smidt A, Van Dyke TE, Barak V, Soskolne AW,
Brautbar C, Sela MN, Bimstein E. Sequential manifestation
of different forms of early-onset periodontitis. A case re-
port. J Periodontol 1994: 65: 631–635.
81. Slots J. The predominant cultivable organisms in juvenile
periodontitis. Scand J Dent Res 1976: 84: 1–10.
82. Smith M, Seymour GJ, Cullinan MP. Histopathological
features of chronic and aggressive periodontitis. Period-
ontol 2000 2010: 53: 45–54.
83. Socransky SS, Haffajee AD. Dental biofilms: difficult
therapeutic targets. Periodontol 2000 2002: 28: 12–55.
84. Soskolne WA, Klinger A. The relationship between peri-
odontal diseases and diabetes: an overview. Ann Period-
ontol 2001: 6: 91–98.
85. Spektor MD, Vandessteen GE, Page RC. Clinical studies of
one family manifesting rapidly progressive, juvenile and
prepubertal periodontitis. J Periodontol 1985: 56: 93–101.
86. Sprague WG, Löe H, Carranza F, Baer PN, Bradley RE,
Cattoni M, Ferrigno P, Gupta O, Landay M, Moser E,
Packer M, Parfitt G, Ruben M, Thilander H, Thomas BOA.
Committee report - periodontal pathology. In: Ramfjord
SP, Kerr DA, Ash MM editors. World Workshop in Perio-
dontics - 1966. Chicago: American Academy of Periodon-
tology, 1966: 123.
87. Stabholz A, Soskolne V, Machtei E, Or R, Soskolne A. Effect
of benign familial neutropenia on the periodontium of
Yemenite Jews. J Periodontol 1990: 61: 51–54.
88. Tanner ACR, Izard J. Tannerella forsythia, a periodontal
pathogen entering the genomic era. Periodontol 2000
2006: 42: 88–113.
89. Taylor GW. Bidirectional interrelationship between dia-
betes periodontal diseases: an epidemiologic perspective.
Ann Periodontol 2001: 6: 99–112.
90. Thoma KH, Goldman HM. Wandering and elongation of
the teeth, and pocket formation in parodontosis. J Am
Dent Assoc 1940: 27: 335–341.
91. van der Velden U. Diagnosis of periodontitis. J Clin
Periodontol 2000: 27: 960–961.
92. van der Velden U. Purpose and problems of periodontal
disease classification. Periodontol 2000 2005: 39: 13–21.
93. Van Dyke TE, Horoszewicz HO, Cianciola LJ, Genco RJ.
Neutrophil chemotaxis dysfunction in human periodon-
titis. Infect Immun 1980: 27: 124–132.
94. Waerhaug J. Subgingival plaque and loss of attachment in
periodontosis as observed in autopsy material. J Period-
ontol 1976: 47: 636–642.
95. Waerhaug J. Plaque control in the treatment of juvenile
periodontitis. J Clin Periodontol 1977: 4: 29–40.
96. Waerhaug J. Subgingival plaque and loss of attachment in
periodontosis as evaluated on extracted teeth. J Period-
ontol 1977: 48: 125–130.
97. Waldrop TC, Anderson DC, Hallmon WW, Schmalstieg FC,
Jacobs RL. Periodontal manifestations of the heritable
Mac-1, LFA-1, deficiency syndrome. Clinical, histopatho-
logic and molecular characteristics. J Periodontol 1987: 58:
400–416.
98. Zaromb A, Chamberlain D, Schoor R, Almas K, Blei F.
Periodontitis as a manifestation of chronic benign neu-
tropenia. J Periodontol 2006: 77: 1921–1926.
99. Zinsli Fritschi B, Albert-Kiszely A, Persson GR. Staphylo-
coccus aureus and other bacteria in untreated periodon-
titis. J Dent Res 2008: 87: 589–593.
27
Copyright of Periodontology 2000 is the property of Wiley-Blackwell and its content may not be copied or
emailed to multiple sites or posted to a listserv without the copyright holder's express written permission.
However, users may print, download, or email articles for individual use.