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Classification of Periodontal Diseases: Where were we? Where are we now?


Where are we going?

Article  in  Dental update · January 2003


DOI: 10.12968/denu.2003.30.1.37 · Source: PubMed

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P E R I O D O N T OP LE OR G
I O
Y D O N T O L O G Y

Classification of Periodontal Diseases:


Where were we? Where are we now?
Where are we going?
M.R. MILWARD AND I.L.C. CHAPPLE

inflammatory in nature. That is to say


Abstract: This paper discusses the past, present and possible future classification of periodontal disease is the outcome of
periodontal diseases. It outlines the reasons for using a classification system from a
complex, and often unpredictable,
clinical perspective and provides a critical appraisal of the latest classification. The
major changes introduced in the 1999 system are discussed alongside the rationale interactions between microbial
behind the recommended nomenclature. complexes and the host’s inflammatory/
immune response. In some patients
Dent Update 2003; 30: 37-44 (such as juveniles) the dominant
determinant of disease development and
Clinical Relevance: This paper aims to provide the general dental practitioner
progression is the host response,
with a practical classification system for periodontal diseases, which is based upon the
new international nomenclature introduced in 1999. whereas in others (older subjects with
slowly progressive disease, for example)
the principal determinant is the longer
term accumulation of plaque. Whatever
the case, it is important to recognize
that, although 95% of the population
INTRODUCTION
A number of periodontal
classification schemes have been
proposed, modified and updated as
Classification systems are used for most
diseases and help clinicians to design
have gingival inflammation, only 8%
appear to be at risk of developing
periodontitis.1,2
knowledge of the pathobiology of appropriate therapeutic strategies,
periodontal diseases has improved. based on evidence from appropriately
Such changes can often confuse and conducted clinical trials. Periodontal A HISTORICAL
frustrate practitioners as they try to diseases are no exception. Classification PERSPECTIVE: WHERE
come to terms with new systems and to of periodontal disease helps in the WERE WE?
relate new nomenclature to the clinical development of frameworks to study the The first classification system for
diagnosis of their patients’ periodontal aetiology, pathogenesis and treatment periodontal disease was recorded in
problems. of diseases; in addition it provides the 1806, when Joseph Fox attempted to
This paper aims to appraise international healthcare community with classify ‘gum disease.’ Since then, a
classification systems in periodontology a way of communicating in a common number of different systems have been
by looking back at historical language. Classification systems also proposed (Table 1).
classifications and relating them to the provide practitioners with a scheme with The first classification scheme to be
most recent scheme, introduced in 1999. which to organize and execute treatment accepted by the American Academy of
It also aims to outline the problems strategies for individual patients. Periodontology (AAP) was that of
created by continually changing The ideal way to classify any disease Orban in 1942. In 1966, the AAP
nomenclature, and the rationale behind is to use the name of the aetiological convened a workshop to produce a new
the use of classification systems. agent. For example, tuberculosis is so system, which was further revised in
called because it is a monoinfection, in 1986. The classification that evolved
this case with the organism from these discussions categorized
M.R. Milward, BDS(Birm.), MFGDP(Eng.), MFDS
RCPS(Glasg.), IMLT, Clinical Lecturer in
Mycobacterium tuberculosis. However, periodontal diseases into a number of
Periodontology, and I.L.C. Chapple, BDS(Newc.), periodontal diseases cannot be key groups, with which most
FDS RCPS(Glasg.), PhD, Professor of classified according to their aetiology practitioners will be familiar:
Periodontology, Head of Unit, Birmingham Dental because they are complex diseases that
School. are polymicrobial and polyimmuno- l juvenile periodontitis (prepubertal,

Dental Update – January/February 2003 37


P E R I O D O N T O L O G Y

Year Body responsible Main points of classification presents at 36 years of age with severe
proposed generalized bone loss and is a non-
smoker with reasonable oral hygiene, he
1806 Joseph Fox First recorded classification of ‘gum disease’
or she would be classified as having
1942 Orban First classification recognized by the American Academy
of Periodontology ‘adult periodontitis’, when in fact the
1966 American Academy of Chronic marginal periodontitis disease is more likely to be early-onset
Periodontology periodontitis that has presented at a late
1977 American Academy of Juvenile periodontitis stage (Figure 1). The mis-classification
Periodontology of such a case may lead to inappropriate
1986 American Academy Prepubertal periodontitis management.
of Periodontology Localized juvenile
Generalized juvenile It is important to realize that the age of
Adult periodontitis presentation may be far removed from
Necrotizing ulcerative periodontitis the age of onset of a disease and
Refractory periodontitis
provides information only about its
1989 Nyman and Lindhe, in Periodontitis levis
their Textbook of Clinical Periodontitis gravis historical rate of progression, not about
Periodontology other risk factors (e.g. smoking, poor
1989 American Academy of Early-onset periodontitis oral hygiene) that may have been
Periodontology3 Periodontitis associated with systemic disease present. Furthermore, a diagnosis can
Refractory periodontitis
change throughout a patient’s life. For
1993 European Workshop Early-onset periodontitis
on Periodontics4 Adult periodontitis instance, localized early-onset (juvenile)
Necrotizing ulcerative periodontitis periodontitis can ‘burn out’ or resolve
1999 International Workshop See Boxes 1 and 2 after successful management. The
on Periodontal
Classification5
affected sites have attachment loss and
are anatomically more susceptible (e.g.
Table 1. The major landmarks in the classification of periodontal disease exposed furcations) to chronic
periodontal disease progression in the
future.
localized and generalized); periodontitis (along with rate of The other factors that were used in
l adult periodontitis; progression and the possibility of host the 1989 classification were:
l acute necrotizing ulcerative defence abnormalities), patients over 35
periodontitis; years being diagnosed with adult l rate of disease progression;
l refractory periodontitis. periodontitis and the younger cohort l presence/absence of systemic
with early-onset disease. This age cut- health;
A further workshop was convened by off, although a guide rather than a strict l local risk factors; and
the AAP in 1989,3 amending the rule, does introduce a number of l the patient’s response to therapy.
classification further into the scheme problems when attempting to design
that most practitioners in the UK use treatment regimens for specific To this end, the terms ‘refractory
today. conditions. For example, if a patient disease’, and ‘rapidly progressive
The main subclasses of periodontal
disease identified by the 1989 workshop
are:

l early-onset periodontitis (formally


prepubertal, juvenile and rapidly
progressive);
l adult periodontitis;
l periodontitis associated with
systemic disease;
l acute necrotizing ulcerative
periodontitis;
l refractory periodontitis.

This classification system is heavily


age dependent: a cut-off point of 35
years is used as one of the main Figure 1. Periapical radiographs of a 36-year-old patient, showing severe generalized bone loss.
category determinants for early-onset Diagnosis: ‘chronic adult periodontitis’ or ‘early-onset periodontitis’?

38 Dental Update – January/February 2003


P E R I O D O N T O L O G Y

periodontitis’ were used in this Dental plaque-induced gingival diseases Non-plaque-induced gingival lesions
classification. 1. Gingivitis associated with dental plaque 1. Gingival diseases of specific bacterial origin
In the 1989 system gingival diseases only a. Neisseria gonorrhoea-associated lesions
a. Without other local contributing b. Treponema pallidum-associated lesions
were not classified, and the implications factors c. streptococcal species-associated lesions
of systemic diseases on the periodontal b. With local contributing factors d. other
tissues were omitted. There was 2. Gingival diseases modified by systemic 2. Gingival diseases of viral origin
factors a. herpesvirus infections
considerable overlap of disease a. associated with the endocrine system 1 ) primary herpetic gingivostomatitis
categories, and the classification criteria 1 ) puberty-associated gingivitis 2 ) recurrent oral herpes
were considered unclear. 2 ) menstrual cycle-associated 3 ) varicella-zoster infections
gingivitis b. other
A European Workshop in 19934 3 ) pregnancy-associated 3. Gingival diseases of fungal origin
simplified the 1989 classification, a) gingivitis a. candidal infections
allowing clinicians to exercise more b ) pyogenic granuloma 1 ) generalized gingival candidosis
4 ) diabetes mellitus-associated b. linear gingival erythema
clinical judgement. This workshop gingivitis c. histoplasmosis
introduced a number of proposals, b. associated with blood dyscrasias d. other
which met with worldwide approval, but 1 ) leukaemia-associated gingivitis 4. Gingival lesions of genetic origin
2 ) other a. hereditary gingival fibromatosis
it was subsequently felt that these 3. Gingival diseases modified by medications b. other
proposals lacked sufficient detail to 1 ) drug-influenced gingival 5. Gingival manifestations of systemic
enable classification of the range of enlargements conditions
2 ) drug-influenced gingivitis a. mucocutaneous disorders
periodontal diseases that a practitioner a) oral contraceptive-associated 1 ) lichen planus
may need to treat. gingivitis 2 ) pemphigoid
Although the classifications of the b ) other 3 ) pemphigus vulgaris
4. Gingival diseases modified by malnutrition 4 ) erythema multiforme
1980s and 1990s represented progress a. ascorbic acid-deficiency gingivitis 5 ) lupus erythematosus
from the earlier schemes, they were not b. other 6 ) drug-induced
sufficiently comprehensive for the 7 ) other
b. allergic reactions
systems of dental care provision and 1 ) dental restorative materials
funding within the USA and some a) mercury
European countries. In such countries, b ) nickel
c) acrylic
where periodontal care is paid for by d ) other
insurance schemes, names/categories 2 ) reactions attributable to
were required for as many conditions as a) toothpastes/dentifrices
b ) mouthrinses/mouthwashes
possible to help insurers create ‘fee c) chewing gum additives
bands’ and ‘tick boxes’ for appropriate d ) foods and additives
remuneration. 3 ) other
6. Traumatic lesions (factitious, iatrogenic,
accidental)
a. chemical injury
THE PRESENT: WHERE ARE b. physical injury
WE NOW? c. thermal injury
7. Foreign body reactions
The AAP and European classification 8. Not otherwise specified (NOS)
schemes were further amended in 1999 Box 1. The 1999 International Workshop for the Classification of Gingival Diseases5
when The International Workshop for
Classification of Periodontal Diseases5
was convened to address a number of diseases on periodontal status were periodontal diseases is shown in Boxes
issues that were felt to be lacking in the expanded and more comprehensively 1 and 2. This is an extremely complex
1989 and 1993 classifications. defined. classification with over 100 disease
The following changes were l ‘Necrotizing periodontal diseases’ categories listed and, owing to its
implemented: were introduced to cover both complexity, it is unrealistic for general
‘necrotizing periodontitis’ and practitioners to use; thus, to allow ease
l Gingival disease category ‘necrotizing gingivitis’. of understanding and clinical
introduced. l ‘Periodontal abscess’ and application, in Figures 2 and 3 the
l ‘Adult periodontitis’ replaced by ‘periodontal-endodontic’ lesions classification has been simplified to the
‘chronic periodontitis’. were added. main subcategories of the 1999
l ‘Refractory disease’ category l A category for developmental or classification.6
removed. acquired lesions was introduced. This new classification system still
l ‘Early-onset periodontitis’ replaced has its critics, but it has addressed a
by ‘aggressive periodontitis’. The 1999 International Workshop number of important areas that were
l The implications of systemic classification for gingival and lacking in the 1989 system. The points

Dental Update – January/February 2003 39


P E R I O D O N T O L O G Y

A. Chronic periodontitis
discussed below have been commented
a. Localized on.
b. Generalized

B. Aggressive periodontitis ‘Aggressive Disease’ in place of


a. Localized
b. Generalized ‘Early-onset Periodontitis’
In the 1999 classification, ‘aggressive
C. Periodontitis as a manifestation of systemic diseases disease’ was defined as disease in
a. Associated with haematological disorders
1. Acquired neutropenia patients who were systemically healthy,
2. Leukaemias had rapid loss of attachment and
3. Other alveolar bone, and a high incidence of a
b. Associated with genetic disorders
1. Familial and cyclic neutropenia familial link.
2. Down’s syndrome The introduction of the term
3. Leukocyte adhesion deficiency syndromes ‘aggressive disease’ is useful as it
4. Papillon–Lefèvre syndrome
5. Chediak–Higashi syndrome addresses the clinical behaviour of the
6. Histiocytosis syndromes disease but avoids the controversial age
7. Glycogen storage disease barrier. Clearly, older subjects can
8. Infantile genetic agranulocytosis
9. Cohen syndrome experience episodes of more rapid
10. Ehlers–Danlos syndrome (Types IV and VIII) attachment loss; whilst this is rare it is
11. Hypophosphatasia embraced by the new system. However,
12. Other
c. Not otherwise specified (NOS) it is accepted that most patients falling
into this category will be less than 30
D. Necrotizing periodontal diseases years old.
a. Necrotizing ulcerative gingivitis (NUG)
b. Necrotizing ulcerative periodontitis (NUP) Localized Aggressive Disease
E. Abscesses of the periodontium l Onset around puberty.
a. Gingival abscess l First molar and incisor involvement.
b. Periodontal abscess
c. Pericoronal abscess
l Raised serum antibody response to
pathogens.
F. Periodontitis associated with endodontic lesions
Combined periodontic-endodontic lesions Generalized Aggressive Disease
l Usually affecting people under 30
G. Developmental or acquired deformities and conditions
a. Localized tooth-related factors that modify or predispose to plaque-induced gingival years of age, but does occur in
diseases/periodontitis older patients.
1. Tooth anatomic factors l Poor antibody response to
2. Dental restorations/appliances
3. Root fractures pathogens.
4. Cervical root resorption and cemental tears l Pronounced episodic nature of loss
b. Mucogingival deformities and conditions around teeth of attachment and alveolar bone.
1. Gingival/soft tissue recession
a. facial or lingual surfaces l Generalized interproximal
b. interproximal (papillary) attachment loss affecting at least
2. Lack of keratinized gingiva three permanent teeth (other than
3. Decreased vestibular depth
4. Aberrant fraenum/muscle position first molars and incisors).
5. Gingival excess
a. pseudopocket
b. inconsistent gingival margin ‘Chronic Periodontitis’ Instead
c. excessive gingival display
d. gingival enlargement of ‘Chronic Adult
6. Abnormal colour Periodontitis’
c. Mucogingival deformities and conditions on edentulous ridges
1. Vertical and/or horizontal ridge deficiency In the 1999 classification, ‘chronic
2. Lack of gingiva/keratinized tissue periodontitis’ was subdivided into
3. Gingival/soft tissue enlargement localized and generalized on the basis of
4. Aberrant fraenum/muscle position
5. Decreased vestibular depth the number of sites affected, localized
6. Abnormal colour being up to 30% of sites, and
d. Occlusal trauma generalized being more than 30% of
1. Primary occlusal trauma
2. Secondary occlusal trauma sites.
Clinical features and characteristics of
Box 2. The 1999 International Workshop for the Classification of Periodontal Diseases.5 chronic periodontitis are:

40 Dental Update – January/February 2003


P E R I O D O N T O L O G Y

that affect the re-occurrence of disease


(e.g. extent of previous disease,
anatomy, occlusal trauma, tooth type,
microflora, host response, smoking),
and the 1999 Workshop considered that
‘refractory disease’ was not a separate
disease entity, suggesting that any
periodontal disease could be termed
‘recurrent disease’ (‘recurrent
aggressive periodontitis’, ‘recurrent
chronic periodontitis’, etc.).

Subclassification of
‘Periodontal Disease as a
Manifestation of Systemic
Disease’
The term ‘ periodontitis associated with
systemic disease’ in the 1989
classification was largely carried over
Figure 2. Gingival diseases: A simplified version of the 1999 International Workshop.5 into the 1999 scheme under the title
‘periodontal disease as a manifestation
of systemic disease’. This is really
l Most prevalent in adults (but can suffer from slowly progressive misnamed, as the conditions listed are
occur in children and adolescents). attachment loss; hence chronic disease.7 strictly systemic diseases that affect
l Amount of destruction of the The loss of the age determinant is the periodontal tissues, or present
periodontium is consistent with the important in view of research within them, rather than periodontal
presence of local risk factors. demonstrating that patients younger than diseases arising de novo.
l Subgingival calculus is a frequent 35 can suffer with a chronic, slowly Diabetes mellitus has not been
finding. progressive periodontal disease.7 included in this subclass as it can
l Slow to moderate rate of modify all forms of periodontal disease,
progression (but can have periods and there is insufficient information to
of rapid attachment loss). Addition of a ‘Gingival conclude that there is a specific
l May be modified by systemic Disease’ Category diabetes mellitus-associated form of
disease. This is an important inclusion in the periodontitis. The same reasoning is
l Can be modified by factors such as new classification. This category is applied to smoking, which is therefore
smoking and stress. split into ‘plaque-induced’ and ‘non- also not included because it is
plaque-induced’ gingival diseases, considered a significant modifier of all
The severity of the disease can be although a number of conditions periodontal diseases.
described for the entire dentition or for causing non-plaque-induced disease
individual teeth or sites. As a general are not included. Also of note are the
guide the 1999 Workshop suggested so-called ‘modifying factors for plaque- Replacement of ‘ANUG’ and
that it could be categorized on the related disease’, which are in fact not ‘ANUP’ with ‘Necrotizing
basis of clinical attachment loss (CAL): modifying factors (for example, Vitamin Periodontal Diseases’
C deficiency and ‘drug-induced’ may The workshop agreed that ANUG and
l Slight: CAL 1–2 mm. be plaque independent). ANUP were clinically distinguishable
l Moderate: CAL 3–4 mm. disease entities, although they were
l Severe: CAL 5 mm or more. unsure whether they were two separate
Removal of ‘Refractory diseases or part of the same disease
Traditionally, the term ‘adult Disease’ as a Term process. It was concluded that there is
periodontitis’, used by previous Refractory disease can be defined by currently insufficient evidence to
classification systems, relates to patients the 1989 classification as continued warrant two separate categories and the
over the age of 35 years, and loss of attachment despite the term ‘necrotizing periodontal diseases’
approximately 16% of the population over provision of adequate treatment and was introduced.
this age will have disease.2 However, it is the patient maintaining a good level of However, the 1999 classification
important to note that adolescents also oral hygiene. There are many factors omitted ‘acute necrotizing stomatitis’,

42 Dental Update – January/February 2003


P E R I O D O N T O L O G Y

l strong family history, suggesting a


genetic association.

These factors in our view make the loss


of this particular term from the
international language of
periodontology a retrograde step.

Conclusions
On the whole, despite its limitations,
the 1999 system has attempted to
address periodontal disease
classification from an evidence-based
perspective, which is to be welcomed.
It seems unnecessarily complex, which
may dissuade practitioners from using
it; but no classification system is
perfect and all will change as our
knowledge increases. For example, the
patient shown in Figure 4 has no
pocketing over 4 mm, no bleeding on
probing and minimal mobility and,
although this patient has suffered from
periodontal disease in the past, this is
historical disease and no longer
currently active or progressing – the
patient was disease free at the time of
Figure 3. Periodontal diseases: A simplified version of the 1999 International Workshop.5
examination. There is no separate
category ‘historical/previous disease’
which would have been a useful alter susceptibility to disease rather for such a clinical case; if there were
inclusion. than being discrete disease entities. For the clinical diagnosis would be
example, primary occlusal trauma is a ‘recession and attachment loss due to
condition, whereas secondary occlusal historical chronic periodontitis’. This
Addition of ‘Periodontal–
trauma refers to the modification of the situation is not recognized within the
Endodontic Lesions’
persisting periodontitis by excessive 1999 classification, but if it were it
The 1989 classification did not include occlusal forces. would embrace the concept that
this group, and this was amended in disease may not be active at
1999 to include only one category: the presentation and therefore not in need
‘combined lesion’. This had been Removal of ‘Localized Juvenile of treatment, although the patient
recommended in an earlier publication8 Periodontitis’
and is welcomed because it implies a The removal of this diagnostic category
single treatment regimen based on the from the classification systems is
pathology present and not on the unfortunate because localized juvenile
aetiology of the lesion, which in this periodontitis is the most well defined of
case is irrelevant to its management.8 all periodontal diseases, with a large
body of research underpinning the
condition and with distinctive clinical
Addition of Category on
and microbiological features:
‘Developmental or Acquired
Deformities and Conditions’
l a strong association with
This category is difficult to interpret Acetomyces Figure 4. Clinical photograph of a patient with
and it seems inappropriate to include it actinomycetemcomitans; no pocketing above 4 mm, no bleeding on
in a classification of periodontal probing and minimal mobility. Clinical diagnosis is
l reduced chemotactic and recession due to ‘historic periodontal disease’, but
diseases as the conditions within this phagocytic activity of the host’s no classification for this exists in the 1999
group are modifying factors, which polymorphonuclear cells; classification.

Dental Update – January/February 2003 43


P E R I O D O N T O L O G Y

remains at risk of disease recurrence. to reflect these advances.


2000 1993; 2: 57–71.
The 1999 classification is now It should be remembered that all 2. Morris AJ, Steele J, White DA. The oral
recognized internationally, and is classification systems have their faults, cleanliness and periodontal health of UK
commonly cited in the literature. It is and this may always be the case for adults in 1998. Br Dent J 2001; 191: 186–192.
3. The American Academy of Periodontology.
therefore important to have a working periodontal diseases, owing to their Proceedings of the World Workshop in Clinical
knowledge of the classification and, multifactorial origin and varied natural Periodontics. Chicago: The American Academy
although in its current form it is too history. of Periodontology, 1989; 1/23–1/24.
complex for routine use in general dental The facility to study gene expression 4. Attstrom R, van der Velden U. Consensus
report (epidemiology). In: Lang NP, Karring T,
practice, the simplified version (Figures and the genetic factors underlying the eds. Proceedings of the First European Workshop
2 and 3) would be appropriate for differences in host response to on Periodontics, 1993. London: Quintessence,
routine clinical use. periodontal pathogens between patients 1994; pp.120–126.
may help inform the classification 5. 1999 International Workshop for the
Classification of Periodontal Diseases. Annals
systems of 2010–2020. However, as of Periodontol 1999; 4: 1–108.
THE FUTURE: WHERE ARE nothing is guaranteed, the systems of 6. Armitage GC. Development of a
WE GOING? the future are also likely to be classification system for periodontal diseases
Research into the aetiology and natural controversial, stimulate much debate, and conditions. Ann Periodontol 1999; 4: 1–6.
7. Clerehugh V, Worthington HV, Lennon MA,
history of the periodontal diseases is and require further modification. Chandler R. Site progression of loss of
moving forward rapidly. As we learn attachment over 5 years in 14-19 year old
more about the mechanisms underlying adolescents. J Clin Periodontol 1995; 22: 15–
21.
the aetiology and pathogenesis of R EFERENCES 8. Chapple ILC, Lumley PJ. The periodontal-
periodontal diseases the systems of 1. Brown LJ, Loe H. Prevalence, extent, severity and endodontic interface. Dent Update 1999; 26:
classification will have to be modified progression of periodontal disease. Periodontol 331–341.

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