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Cariology

Edwina Kidd Ole Fejerskov

Changing Concepts in Cariology:


Forty Years On
Abstract: The caries lesion is a sign or symptom resulting from numerous pH fluctuations in biofilms on teeth. The lesion may or may not
progress and lesion progression can be controlled, slowed down or arrested. Control of the biofilm is the treatment of caries, the most
important measure being to disturb the biofilm mechanically using a fluoride-containing toothpaste. The informed patient controls caries
and the role of the dental professional is to advise how this should be done. This is the non-operative treatment of caries and it is worthy
of payment. It should be mandatory as part of any operative treatment to ensure that the patient understands, and is able to perform,
adequate plaque control.
Clinical Relevance: It is very unfortunate that the current remuneration scheme (Unit of Dental Activity) in Health Service practice in
England and Wales prevents practitioners adopting a modern biological approach to caries control.
Dent Update 2013; 40: 277–286

Changing concepts in School when Ted Renson carried in his


cariology: forty years on baby, Dental Update, Volume 1, Number
1. It was a revelation to see such a
Forty years on, when afar and asunder
beautifully produced, colour illustrated
Parted are those who are reading today,
and readily understandable production.
When you look back, and forgetfully wonder
The cariology article in that first number
What you were like in your work and your play,
concerned the white spot lesion and was
Then, it may be, there will often come o’er you,
written by Leon Silverstone.1 The authors
Glimpses of past and some of it wrong,
of the current paper (EK and OF) met in
Visions of studies shall float them before you,
Leon’s laboratory (a euphemism for a
Echoes of teaching shall bear you along,
large cupboard) at the London Hospital at
What is new for the patient our hope to fulfil,
that time. One (EK) was a junior lecturer
Teeth unto death are chiefly our will.
at The London whose PhD Leon was Figure 1. Forty years on!
(With apologies to Edward Ernest Bowen
supervising; the other (OF), already a
and Harrow School.)
Professor of Oral Pathology in Denmark,
had recently been appointed to a chair in
A personal introduction Cariology and needed to change research The relevance of cariology
focus from soft to hard tissues. He was in Dental caries is ubiquitous − it
Edwina Kidd was in the staff
London to research aspects of fluorosis is omnipresent in all populations and is
room at the London Hospital Dental
and work with Leon, Newell Johnson and as old as mankind. The caries incidence
Ron Fearnhead. Having met in a long, rate varies extensively between and
thin cupboard, where communication within populations. With increasing
Edwina Kidd, BDS, FDS RCS(Eng), PhD, was inevitable, we subsequently worked age, signs and symptoms of dental
DSc, Emerita Professor of Cariology, together for 40 years (Figure 1). We now caries accumulate and, in most adult
King’s College, London, UK and Ole combine in this anniversary issue to take populations, the caries prevalence
Fejerskov, DDS, PhD, Dr Odont, a helicopter journey over contemporary approaches 100 percent. Prevention and
Professor of Anatomy, Faculty of Health Cariology, discussing aspects of the subject operative treatment of caries lesions, and
Sciences, University of Arhus, Denmark. as understood in 2013 and highlighting their sequelae, occupy the majority of the
changes in understanding from the 1970s. dental profession life-long around the
May 2013 DentalUpdate 277
Cariology

world and the cost of dental health care When GV Black published From these statements it is
is a major societal burden. The majority of his comprehensive textbook in 19084 he obvious that it is the informed patient
dental restorations are made because of emphasized that clinical diagnosis and that actually controls caries. So what then
dental caries. Caries and failed restorative treatment decisions should have a sound is the role of the dental professional? It
care are the main causes for tooth loss in biologic rationale. Although it became is to advise, so that all our patients are
all contemporary populations. appreciated by the middle of the 20th aware of the importance of good tooth-
Century that dentistry is a biomedical cleaning, appropriate use of fluoride and
specialty, the technical advances with a sensible diet. This is the non-operative
The current concept of caries high-speed drilling seemed to distort the treatment of caries. Note that the
and caries control true application of biological knowledge examination of the patient and giving
Dental caries is a dynamic in the optimal treatment of dental caries. appropriate advice are time-consuming,
process. It is a chemical dissolution Dental caries became synonymous with skilful and worthy of payment. However,
brought about by metabolic activity in ‘a cavity’ in the tooth and the automatic in the 1970s treatment (as opposed to
a microbial deposit (biofilm) covering a reaction was that the treatment should be prevention) of caries was by filling teeth,
tooth surface at any given time. Over time ‘drill and fill’. which is very unfortunate because fillings
the outcome of these fluctuations may In the growing field of caries mask the problem of poor plaque control
result in a disturbance of the equilibrium epidemiology, dental caries was recorded and the dentist takes responsibility away
between the tooth mineral and the as DMF teeth/surfaces where D stood from the patient. ‘You have decay, let
surroundings. Mineral loss, subsequent for Decay and decay meant a cavity. me treat it for you by cutting it away
lesion formation and possible cavity The knowledge about aetiology and and replacing with a filling’. Fillings are
formation in teeth, is a symptom of pathology of caries was often taught even claimed by some to be ‘secondary
imbalance in this dynamic process. in dental curricula in departments of prevention’ which is nonsense! For a while
The metabolism in the biofilm is an microbiology, pathology and physiology, fillings will appear to be successful, but
ubiquitous, natural process; part of having as well as in the growing disciplines if the real cause of the problem is not
teeth. However, its possible consequence, of the 50s and 60s of dental public addressed, caries will recur adjacent to
lesion formation and progression, can be health, departments of paediatrics and the filling. To place restorations without
controlled so that a clinically visible lesion preventive dentistry. However, the clinical addressing the reason the lesion has
never forms or an established lesion relevance of ‘cariology‘ to restorative formed in the first place is tantamount to
arrests.2 clinical departments was not emphasized repairing a fire damaged building without
The following points in all schools (The London being a notable extinguishing the flames. Fillings are a
encapsulate our current view of caries:3 exception!) and knowledge to be applied part of plaque control and important in
 Caries is ubiquitous; at the chairside was fragmented. To some the management of cavitated lesions, but
 It is a sign or symptom resulting from extent this was understandable because, they are not the most important aspect of
numerous pH fluctuations in biofilms in a clinical department, the students caries control.
on teeth. The resulting de- and re- were supposed to produce fillings and Forty years ago, in the United
mineralization of the tooth surface may crowns and bridges. Thus the appreciation Kingdom and Denmark, there were
result in the formation of a clinically of the need for concomitant disease departments of conservative, operative
detectable lesion (the sign/symptom); control as part of any long-term successful or restorative dentistry where, although
 These lesions may or may not progress; restorative treatment was limited, or non- the pathology of dental caries might
 Lesion progression can be controlled, existent. be taught, rewards were only given for
slowed down or arrested; fillings. Undergraduates had points quotas
 Everyone is at risk of lesion formation with points given for restorations. There
from cradle to grave; What constitutes treatment of were no similar rewards for non-operative
 Caries is the predominant cause of caries? treatments. Students would thus qualify
tooth loss in all ages. This question is incredibly in the UK tailor-made for a National
In the 1970s, it was suggested important. Since lesion formation and Health Service which also gave rewards
that caries could be prevented and progression can be controlled, control of for operative dentistry (fee per item of
the concept of caries control was not the biofilm is the treatment of caries. operative treatment) but not for the non-
emphasized. The distinction between the The most important control measure is operative caries control measures.
process in the biofilm and its reflection, to clean teeth regularly, and thus disturb It is now tempting to take a
the lesion in the tooth, was not made the biofilm mechanically, with a fluoride- sneaky look across the Atlantic where,
clear. Although it was realized that all ages containing toothpaste. If sugar intake is even today, there are few departments of
were susceptible to caries, prevention was high and frequent, the pH fluctuations in cariology and operative dentistry reigns
mainly taught in paediatric departments, the biofilm may result in overgrowth of supreme. This is of great importance to
and it was suggested that periodontal cariogenic micro-organisms, making lesion the young dentist who is emerging from
disease was the more important cause of formation and progression more likely.5 the dental school egg with debts of a
tooth loss in the elderly. Thus dietary advice may have a role to play. quarter of a million pounds. And before
278 DentalUpdate May 2013
Cariology

we get too smug about this, let us remind so that the patient can disturb/remove examined for lesion progression or arrest.
ourselves of what has just happened in most of the biofilm with a fluoride- Decisions, about activity
England and Wales to university fees, now containing toothpaste. Any lesion, at and cavitation, are inevitably best
£9000 per year in dental schools. Add any stage of progression, is arrestable by guesses. This is not a disaster because
to this living costs for five years and it is cleaning alone provided the pulp is not dentists should review patients and
obvious that this problem is ours already. irreparably damaged. This diagnosis is thus review the decisions. However,
best performed by a careful clinical-visual the opportunity for review should have
examination of clean, dry teeth. It was implications for decision-making. If a
Caries diagnosis realized that, while a sharp probe was lesion is suspected as active, it should
A diagnosis has been described useful to feel the surface of the lesion be treated non-operatively so as not to
as a mental resting place on the way to to detect roughness indicating activity, miss the opportunity to arrest the lesion.
a treatment decision. What in diagnosis the probe must be used gently. It is However, if a dentist is unsure whether
is relevant to that treatment decision as not a bayonet and rough use to test for an approximal lesion is cavitated, and
far as caries is concerned? The activity of ‘stickiness’ actually damages the surface therefore unsure whether a filling is
the lesion is of great importance (Figure of the lesion and encourages plaque required, the better decision is to institute
2). Lesions judged as active (by this we accumulation. non-operative treatment and reassess
mean if nothing changes, the lesion Radiographs are an aid rather than prescribe a restoration
will progress) require non-operative to diagnosis for approximal lesions. because this is an irrevocable decision. We
treatments and a review of the efficacy of However, while a radiograph gives some know from research started at the London
the treatment is to check that lesions do appreciation of lesion depth, a single Hospital by Richard Elderton in the early
not progress and appear to be arrested. radiograph cannot assess either activity 70s, that placement of a restoration
The other aspect of great relevance is or cavitation. It must also be remembered may start a cascade of restoration and
whether a cavity is present that traps that there may be false positive and re-restoration, each replacement resulting
plaque and precludes cleaning (Figure 3). negative findings on these two- in further tooth removal, until we simply
If the patient cannot access the plaque, dimensional shadows. Radiographs do run out of hard tissue and the tooth is
the lesion is almost bound to progress. not alone define the truth. A subsequent lost.7
These lesions must either be filled or picture, taken after a period of time with In the 1970s, there was no
perhaps made accessible to cleaning,6 a film holder and beam aiming device to appreciation of the relevance of lesion
ensure comparable geometry, should be activity to the treatment decision.
Approximal lesions tended to be treated
a operatively when they were just in
a dentine on radiograph − and in Denmark
even when confined to enamel.8 The
current threshold for operative treatment,
in contemporary low caries populations,
tends to be lesions that are well into
dentine because the less advanced lesions
are often not cavitated when opened.
These should be treated non-operatively
and thus given a chance to arrest
b following improved oral hygiene and
b fluoride application.
In the 1980s and 1990s,
there was a flurry of activity in the use of
machines to aid diagnosis, for example
electrical conductance measurements
and fluorescence techniques, such as
DIAGNOdent (KaVo, Biberach, Germany).
The idea was to take the subjectivity
out of the task as well as to diagnose
Figure 2. (a) Active, non-cavitated, occlusal demineralization at an earlier stage
lesion. The biofilm must be gently removed with Figure 3. (a) Active caries lesion with small cavity. so that non-operative caries control
the side of an explorer or toothbrush otherwise This is not cleansable and restoration is required measures could be instituted in a timely
this lesion will not be seen. (b) Arrested, non- to aid plaque control. (b) Arrested occlusal caries fashion. After considerable research
cavitated pit or fissure lesions often present as lesion. The undermined enamel margins have effort, and many publications, it was
darkly stained. Removal of any biofilm important fractured away and the cavity is cleansable. No
acknowledged that these machines can
to aid diagnosis. restoration needed to control caries.
only detect demineralization and not
280 DentalUpdate May 2013
Cariology

make judgements on what matters most, erupting premolar/molar, in particular, assessment will also guide appropriate
namely activity and cavitation. It was thus should be carefully cleaned by a parent, recall intervals. After much research, it
eventually concluded that a visual-tactile with the brush coming in at right angles can be stated that no single factor or
examination of clean, dry teeth, together to the arch (Figure 5). Occlusal lesions combination of biological factors will
with careful thought, were preferable to any can be prevented/controlled by careful accurately predict risk, on an individual
machine.9 cleaning over the eruption period, and patient basis, except the presence of early
Occlusal lesions have given fissure sealants are not required.10 non-cavitated lesions and a history of
particular food for thought. In the 1970s, it Unfortunately, the profession lesions and fillings.12 This makes a careful
was considered that the lesion formed in seems to have been very slow in adopting clinical visual-tactile diagnosis even more
the depth of the fissure and was difficult to a chart that allows the salient features of important. However, all our patients
see and impossible to access for thorough lesion activity and cavitation to be visually should be taught good oral hygiene with
cleaning. In the 1980s, dentists noticed recorded, although such a chart has been a fluoride-containing toothpaste and the
that they were missing quite advanced developed (Figure 6) and described in relevance of diet to caries. This is called
lesions on clinical examination but finding Dental Update!11 a whole population approach and is
large lesions in dentine on radiograph appropriate to any disease that potentially
(Figure 4). The term ‘hidden caries’ was occurs in everyone.
used to describe lesions missed on clinical Assessment of caries risk The one factor that will predict
examination but found on radiograph, Question: Who is at risk from increased risk is dramatically reduced
and fluoride was blamed for masking the lesion development? Answer: Everyone salivary flow (hyposalivation). Resting
diagnosis. It was subsequently shown that with teeth, from cradle to grave, because flow should be measured when this
the occlusal lesion forms at the entrance to the metabolism in the biofilm is a natural is suspected because, if the clinician’s
the fissure and it can be diagnosed visually, part of having teeth. In recent years, suspicion is confirmed, the patient is at
provided plaque is removed from the there has been much interest in whether risk of rapid lesion development. Frequent
fissure entrance. This was a very important this concept of risk assessment can be recall and strenuous effort will be required
finding because it implied that these lesions further refined so that caries control to control lesion progression in these
could be controlled by cleaning alone. The measures may be targeted appropriately types of patients. The management
before any lesions form. Caries risk majors on plaque control and fluoride
(Figure 7). These are some of the most
a
difficult patients to manage; those one
a worries about in the darker reaches of
the night.

Epidemiology
It was in the early 1980s that
data from around the developed world
showed a decline in caries prevalence and
incidence (rate of development). In UK,
b
decennial National Surveys have shown
this decline. In Denmark, all children
b enrolled in the school dental health
service were examined annually, resulting
in unique longitudinal data. Initially, the
caries decline caused some panic. If dental
caries was solved, what were dentists
to do? Several dental schools closed in
the developed world and, ironically, in
England the school that trained therapists
Figure 4. (a) The clinical picture shows a lesion was also closed. The dental profession
with a cavity in the central fossa. To see this, was climbing into the boat and pushing
the tooth must be clean and dry. The clinician Figure 5. (a) The occlusal surface of this first per- off. After a few years it was realized that
mistakenly diagnosed this lesion as arrested. (b) manent molar is at its most vulnerable during the the decline in caries prevalence and
However, the radiograph shows an extensive period from first eruption until it is in occlusion incidence, far from obviating the need
radiolucent lesion in dentine and a restoration (arrow points to erupting tooth). (b) Brushing the for dentists, actually might require more
is required. This makes the point that it is always occlusal surface of the erupting molar. The parent dental personnel because there are so
important to examine radiographs carefully. They assists, bringing the brush in at right angles to
many more teeth to look after. Why have
aid diagnosis. the arch.
there been changes in caries prevalence
May 2013 DentalUpdate 281
Cariology

fluids, delays lesion development and


progression and it does it at any age. The
fluoride does not have to be in water, it
can be in toothpaste, mouthwash, varnish,
gels. All systemic effects may result in
unnecessary development of dental
fluorosis14 but are not needed to obtain
maximum caries control. It should also be
appreciated that changing criteria for the
decision to restore has resulted in fewer
fillings and this has also played a major
role for the change in DMFT in many
countries.15

The role of diet


The evidence linking sugar
and caries is irrefutable, although there
is no linear relationship between daily
sugar consumption and caries experience
Figure 6. Chart with red (active) and blue (inactive) colours to indicate lesion activity. Lines and circles on a population basis. Unfortunately,
differentiate non-cavitated from cavitated lesions. there is less evidence that it is possible
to alter diets and persuade people to
eat differently. We only have to consider
the current obesity epidemic to realize
the difficulty. Caries decline occurs in
The reader may be interested to know most populations without a concomitant
that this was stressed in 1908 by GV Black decrease in sugar consumption (Figure 8).
when he wrote his Textbook of Operative Changes in socio-economic conditions,
Dentistry.4 Today, as in the 1970s, almost widespread use of fluorides, increased
all toothpastes contain fluoride and oral appreciation of the role of oral hygiene
hygiene is an ideal route for fluoride and changing restorative thresholds
application. have had a major impact on the caries
Figure 7. Cancer patient who has mastered
caries control subsequent to resection of the left situation. For this reason, our major
mandible and radiation therapy of the head and focus in caries control should move from
neck. The patient received regular professional
The role of fluoride diet to oral hygiene, with a fluoride-
tooth cleaning and topical fluoride therapy in So if fluoride explains much containing toothpaste. However, this does
conjunction with meticulous self-performed oral of this alteration, what is its mechanism not mean that we should ignore diet.
hygiene. of action? In the 1970s, it was thought All our patients should be aware of the
that, to be effective, fluoride had to be relationship of sugar to caries and dietary
incorporated into developing enamel and advice is still needed in those developing
and incidence? The likely explanation the fluoridated apatite so formed would several new lesions at any stage in life.
would seem to be the advent of fluoride, be more resistant to acid attack. Several It is especially important for those with
particularly in toothpaste. It should also be studies had shown the significant effect decreased salivary flow, where dietary
noted that caries distribution in populations of fluoridated water on dental caries, not advice is mandatory.
is now more and more skew and often least in the United States and Holland.
concentrated in socially deprived people, This concept of incorporation into enamel
to the extent that rampant caries in a child would basically mean that children, in When do we need fillings?
should make the dentist consider whether particular, would be the target group for As discussed earlier, from a
the child is seriously neglected. fluoride prevention. However, in 1981, purely cariological perspective, fillings
one of the cupboard companions (OF), should be considered a somewhat strange
together with two Danish colleagues, way of performing plaque control! Thus
The role of plaque control put together the evidence from research they are required when the patient cannot
Since the metabolism in the works around the world to show that clean plaque out of a hole in a tooth, for
biofilm is responsible for caries lesion the important mechanism of fluoride instance a cavitated occlusal (Figures
development, plaque control is the most was its topical effect.13 Fluoride, present 3a and 4) or an approximal surface. This
important part of non-operative treatment. at the point of acid attack in the oral means that many root caries lesions do
282 DentalUpdate May 2013
Cariology

c
Figure 8. The blue bars show the decline in caries experience (DMFT) in Denmark in 12-year-old chil-
dren between 1974 and 1997. This pattern is typical of developed countries. The red bars show the
sugar consumption (kg/individual/year over the same years). The decline in caries is not likely to be due
to changed sugar consumption because this has not changed.

1970s. Lesions, as seen in Figure 9, would


have been restored and this was not easy Figure 10. (a) Cervical lesions covered by plaque.
because suitable adhesive restorative (b) The same cavities 14 days later after removing
materials were in their infancy and even overhanging enamel and showing the patient
these cannot last forever.16 how to clean. The teeth were then brushed twice
In the 1970s, fissure sealants a day with a toothbrush and fluoride paste. At
were recently developed and were this stage, from a cariological point of view, these
applied to sound fissures to prevent lesions were stable but very ugly. For this reason,
b they were restored with composite (c). This was
lesion formation on molars and
taken immediately after removal of the rubber
premolars. Remember that the caries
dam and the teeth had dried out, which explains
prevalence was much higher in those a small colour difference that will disappear
years. However, the contemporary rapidly as the teeth rehydrate.
indications for sealants are much less.
Caries prevalence is reduced, it is unusual
to see occlusal lesions in premolars
There was a fee for scaling and polishing
and occlusal lesion formation can be
Figure 9. (a, b) There are 8 years between and one of us (EK) used this fee to cover
controlled by cleaning with fluoride
the two photographs. In (a) the root lesions preventive advice. In her hands money was
are active, plaque-covered and soft to gentle toothpaste. The contemporary indication
lost, but it did not haemorrhage.
probing. In (b) the lesions are arrested, hard and for sealants would be in patients who are
In 2006 the fee structure was
shiny. The non-operative treatment has involved not cleaning effectively, despite advice.
altered, with a new contract, and fees were
removal of a rim of unsupported enamel at the
divided into three bands. This system is
occlusal aspect of the lesion, and daily plaque Delivery of caries control still in operation and, in the opinion of
removal with fluoride toothpaste. The lesions are treatments in the NHS in one of the authors (EK), it is a problem and
not visible and do not need restoration. England and Wales should have been discontinued long ago.
When Dental Update was Non-operative treatments are part of Band
born practitioners were rewarded on 1 which comprises diagnosis, treatment
not require restoration because they can a fee per item of operative treatment planning and maintenance, attracting a
be arrested by plaque control and fluoride basis. There were no fees for preventive single Unit of Dental Activity (UDA), which
(Figure 9). Thus, unless appearance is a treatments, such as oral hygiene will represent about 15 minutes of surgery
problem (Figure 10), it is preferable to avoid instruction, fluoride application, diet time at best. For this fee the practitioner
restorations. This was not practised in the analysis and fissure sealant application. should carry out:
May 2013 DentalUpdate 285
Cariology

 History and examination; functioning dentition from cradle to grave. in relation to treatment of approximal
 Special tests such as radiographs; In the upcoming third edition of our mutual carious lesions. Caries Res 1982; 16:
 Diagnosis and treatment planning; textbook, we will soon document how 1−6.
 Agreeing the plan with the patient this goal is achievable today. Indeed, it has 9. Ricketts D. The eyes have it. How good
and gaining consent; been achievable for many years with the is DIAGNOdent at detecting caries?
 Scale and polish, if required; knowledge that we now have about the Evid Based Dent 2005; 6: 64−65.
 All non-operative treatments, oral nature of dental caries. 10. Ekstrand KR, Christiansen ME.
hygiene advice, fluoride advice and Outcomes of a non-operative
application if appropriate, diet analysis treatment program for children and
Acknowledgements
and advice. adolescents. Caries Res 2005; 39:
Figures 2, 3, 4, 7, 8, 9, 10
One of the authors is 455−457.
are reproduced with permission from:
on record asking advice from the 11. Page J, Kidd E. Practical suggestions
Dental Caries. The Disease and Its Clinical
Department of Health as to how this can for implementing caries control and
Management. Fejerskov O, Kidd E (eds).
be done for a single UDA11 but, as in the recall protocols for children and young
Oxford: Blackwell Munksgaard, 2008.
Walrus and the Carpenter,17 ‘answer came adults. Dent Update 2010; 37: 422−432.
The dentist who took each
there none’. Literary buffs will recall that 12. Hausen H. Caries prediction. In: Dental
photograph and cared for the patient
in the poem there could be no answer Caries. The Disease and Its Clinical
is acknowledged by a ‘signature’ on the
because the oysters were dead, they had Management. Fejerskov O, Kidd E (eds).
picture. This acknowledgement is important
all been eaten. Oxford: Blackwell Munksgaard, 2008:
because illustrations of this quality are
This combining of diagnosis pp527−541.
difficult to produce but invaluable teaching
and preventive treatment into a single 13. Fejerskov O, Thylstrup A, Larsen ML.
material.
band precludes the hygienist (the Rational use of fluorides in caries
preventive therapist) from working in the prevention. A concept based on
Health Service in many practices because possible cariostatic mechanisms. Acta
the dentist would then have to split the
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286 DentalUpdate May 2013