New insights in understanding dental caries and periodontal disease: the avalanche model

doi:10.4236/health.2009.14042

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Vol.1, No.4, 263-268 (200

doi:10.4236/health.2009.14042

9) Health

Openly accessible at/HEAL H

New insights in understanding dental caries and

periodontal disease: the avalanche model

Peter Gaengler1, Ljubisa Markovic1, Dagmar Norden2, Rainer A. Jordan1

1Department of Operative and Preventive Dentistry, University of Witten/Herdecke, Witten, Germany; peter.gaengler@uni-wh.de

2Ordination, Rheinstraße 1826382 Wilhelmshaven, Germany

Received 12 October 2009; revised 10 November 2009; 13 November 2009.

ABSTRACT

Biology is based on evolution; therefore, eu-

cariotes like plants, animals and human beings

are living in harmony with their procariote an-

cestors. If this is obviously the normal way of

life, then pathobiology follows the same basic

principles. The highly complex harmony of the

living world may be disrupted, and a punctuated

disease starts which is different from the health

equilibrium. To reflect this biological archetype

on the main diseases in dentistry - caries and

periodontitis - the avalanche model is being

proposed based on scientific and clinical evi-

dence. This way of argumentation does influ-

ence the strategic planning of preventive and

curative programmes in dental research as well

as in daily practise.

Keywords: Dentistry; Dental Caries; Etiology;

Model; Pathology; Periodontal Disease

1. INTRODUCTION

The role of dental caries as a health related sociological

phenomenon goes back to the 10th millenium BC, at the

end of the last ice age, when raising temperatures in the

flood plains of the fertile crescent allowed the cultivation

of wild corn [1]. As a consequence, the fundamental

change from a nomadic hunting-gathering way of life to

settled farming and agriculture in man took place [2].

The development of the grinding stone was an important

milestone during the continuous process of refining food.

Consequently, the highly abrasive and fibre rich food of

the prehistoric population was being more and more

replaced by a soft diet consisting of pastries and pasta. In

the 2nd millennium BC, increasing incidence of dental

caries - though on a low level - inspired the creation of

the very first etiologic model for tooth decay in human

history: the concept of the tooth worm causing caries

and periodontal disease. Paleoantropologic examination

of skulls showed a low prevalence of dental caries (Pa-

ganelli C. Dental caries frequency in adult egyptian

mummies. Personal communication. Valdaora, 2006) less

than 10% [3] increasing up to 25% in medival times [3].

During the transatlantic slave trade and the beginning of

the industrial processing of cane sugar in North America

and Europe, dental caries prevalence went up to 50%

reaching a frequency of almost 100% in all industrialised

countries today [4]. Sociologically, the dramatic increase

and spread of dental caries in human society can be seen

as a consequence of civilisation and industrialisation in

food production. From a functional point of view, it

seems to be a consequence of the absence of masticatory

abrasion and tribological attrition caused by dramatic

changes in diet [5]. Thus, non-opened fissures and

proximal sites show the highest rates of affection, when

no longer exposed to abrasive and attritional wear. These

presumptions are supported by comparative odontology.

Extended occlusal wear far into the dentine core, a pulp

chamber becoming smaller by forming tertiary dentine

and the dentition drifting mesially by flattening the

proximal contacts were shown to be a natural pattern of

function in omnivorous dentitions, i.e. in dentitions of

wild living boars and primates showing hardly any tooth

decay [6]. The Witten Dental Caries study showed fur-

ther strong correlation between tooth wear and dental

caries experience in man [7]. Based on phylogenetic

findings, it is supposed that a thick enamel cover and a

spacious pulp lumen in omnivorous species represents

an equifinality - a common characteristic in open sys-

tems converging to a dynamic equilibrium - in which the

pulp is a spaceholder for replacement with tertiary den-

tine to compensate the decreasing thickness of enamel

and dentine caused by attrition and abrasion [8].

2. PUNCTUATED EQUILIBRIA AS A

BIOLOGIC PRINCIPLE

Clinical observations have shown that caries and perio-

dontal diseases have a chronic-cumulative character and

no continuous way of progression. They lead to the con-

P. Gaengler et al. / HEALTH 1 (2009) 263-268

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Figure 1. Biomineralisation consequences of the pathogenesis of dental caries diseases

according to the concept of progression and stagnation. Comparison of factors con-

tributing to either bursts of disease progression or to long-lasting periods of stagnation.

MC = stem cell; T = T lymphocyte; B = B lymphocyte; P = plasma cell; L = lympho-

cyte. [21]

cept of a destructive periodontal disease pathogenesis

with different types of progression showing characteris-

tic episodes of activity and inactivity [9]. Corresponding

dynamics in caries progression with episodes of demin-

eralisation and remineralisation have already been

pointed out since the 1960s [10,11]. Consequently,

knowledge from both cariology and periodontology was

then consolidated to one robust pathogenetic Concept of

Progression and Stagnation of Dental Caries and Perio-

dontitis noticing epidemiologic, historic, immunologic,

odontologic, physiologic and sociologic perceptions [12]

(Figures 1,2). The initial stages of the diseases,

pre-caries as the first detectable mineral deficite and

gingivitis are reversible and therefore, they are at least

partly underlying a principle of progression and remis-

sion. In dental caries, the highly complex “ion whip”

contributes to loss and uptake of calcium and phosphate

ions in enamel and exposed dentine and cementum. This

is a lifelong ongoing equilibrium, and bursts of prevail-

ing demineralisation activity with the consequence of

pre-caries and clinical caries lesions are rather occa-

sional episodes.

P. Gaengler et al. / HEALTH 1 (2009) 263-268

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Figure 2. Biomineralisation consequences of the pathogenesis of periodontal diseases according to the

concept of progression and stagnation. Comparison of factors contributing to either bursts of rapid

disease progression with periodontal pocket formation or to long-lasting periods of stagnation. T = T

lymphocyte; B = B lymphocyte. [21]

In periodontal diseases, there are alternating short

lasting activities of destruction (with localised immu-

nological breakdowns) and long-lasting episodes of

equilibria. From a structural biological point of view,

progression means loss of connective tissue and bacterial

penetration through the wall of leucocytes, stagnation

means replacement of connective tissue and build-up of

the wall of leucocytes.

Irregularity in biological behaviour as a principle has

already been discussed in evolutionary theories in the

1970s as an alternative to phyletic gradualism of Dar-

win’s theory of evolution, and it was later described as a

general biological principle [13,14]. Phyletic gradualism

proceeds on the assumption of long-term continuous

transformation of genetic material in the majority of a

population without basic episodes of stagnation. Palae-

ontological evidence for this stepwise transformation of

slightly different forms in a common evolutionary chain

could never be found. The conceptual basis for the al-

ternative theory of punctuated equilibria is based on this

assumptions: a) geographic isolation as a precondition

for a genetic process of transformation and b) a homoeo-

static equilibrium with rare and temporally compressed

changes in the gene pool alternating with long episodes

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Figure 3. Initial white spot lesion (teeth 43 and 45)

and brown spot lesion (tooth 47) in a young female pa-

tient, (a) start of non-invasive treatment with the daily

bioavailability of fluoride by F-containing dentifrice

and F tablets (1 mg p.d.), (b) clinical control over 5

years demonstrating reversals of the white spot lesions

in canine and premolar and decreased but stable molar

lesion. (courtesy of Dr. T. Lang, Witten, Germany).

Figure 4. Periodontal condition in a young HIV-

seropositive patient undergoing Highly-active Anti-

retroviral Therapy, (a) before periodontal treatment

with black triangles especially between incisors as a

result of chronic marginal periodontitis triggered by

necrotising ulcerative bursts, (b) 16 month after con-

servative treatment and a strict supportive periodontal

programme with a “creeping attachment”.

of stasis. The theory especially implies so-called punctu-

ated equilibria during the early stages of speciation,

while dramatic changes in the environmental conditions

are taking place. If this is indeed a general biological

principle, then one could try to apply this to pathobiol-

ogy. Punctuationalism applied to oral medicine, then,

also means, periodontal disease is a pathologic event in

limited dental sites and not in the entire dentition despite

the all-over presence of plaque; just like caries, that is

rarely seen as a generalised event but showing age-re-

lated peaks. In palaeontology, the postulation of favour-

able environmental conditions for punctuations is met by

geographic separation from the mother-species; in hu-

man life sciences by a locally different immunologic

host reactivity [15]. The concept of pulpal reaction [16]

in particular takes up the theory of biologic equilibria, as

it compares pattern of pulpal reactions on dental caries

progression with different functional periods of the den-

tition. The concept of a multifactorial disease [17] goes

even one step further assuming biofilms to be a physiol-

ogic phenomenon, and demineralisations to be a simple

reflection to multifactorial disturbances in a physiologic

balance between the natural biofilm and all (wet) smooth

surfaces. The dynamic character of dental caries and

periodontal diseases has recently emphazised in the

concept of cyclical progression [18]. Knowledge from

microbiology confirms this view, as only 10% of all cells

in human beings are mammalian; the vast amount are

procaryotes, mainly bacteria. In the oral cavity, more

than 20,000 genetically differentiable bacterial species

were recently analyzed. They usually diversify in several

clones, of which eventually one is pathogenic. As a re-

sult, many organic systems basically live in a state of

symbiosis or commensalism with their microorganisms

[19]. Recently, Mogens Kilian et al. suggested a scenario

that commensal streptococci gradually evolved from a

pathogen by genome reduction. Their study provided

insight into the evolutionary history that resulted in ge-

netically closely related streptococci with very high (S.

pneumoniae) or no pathogenic potential of commensal

species [20]. The comprehensive model of progression

and stagnation was extended by these realisations from

palaeontology and contemporary theories of evolution,

from cellular biology, microbiology, and cariology to

suggest the avalanche model of dental caries and perio-

dontal diseases:

“[Punctuated equilibrium means] for the main infec-

tious diseases in dentistry, caries and periodontitis, a

promotion of the concept of progression and stagnation,

when rapid punctuated bursts disrupt prolonged dormant

episodes of stagnation: the macroorganism, which is

otherwise living in balance with its microorganisms,

reacts with an acute burst of demineralisation and/or

inflammation - the episode of punctuation. This is an

avalanche model, where different punctuated episodes

(sun, snow, wind, hazardous snowboarder) initiate an

avalanche in an otherwise highly complex system” [21].

3. THE AVALANCHE CARIES

PROGRESSION MODEL

It would make sense to look at very few clinical exam-

ples to demonstrate the snowballing character of the

avalanche caries progression model. Despite a complex

variety of etiological components, the development of

white spot lesions per time and per tooth mainly on

smooth surfaces of dental enamel is well documented as

the only evident clinical risk factor for progression or

remission of subclinical pre-caries or initial caries into a

surface lesion. This is also reflected in modern caries

detection and assessment systems [22]. Otto Backer

Dirks clearly demonstrated in a rather simple way that

initial lesions may undergo remineralisation and, there-

fore, being arrested (10). This could be shown in longi-

tudinal studies assessing caries over an eight year period

[23]: even under highly controlled clinical conditions in-

cluding oral health education and bioavailability of topical

fluoride, one third of initial smooth surface caries lesions

were found to turn into superficial cavities (Figure 3).

As with avalanches in winter mountains it is hard to

say that a single factor of lesion progression is responsi-

ble for cavity formation, and it could easily be asked: is

the shift in bacterial activity due to quorum sensing re-

sponsible, is the change in host responses due to saliva

factors responsible, is temporary overload of low mo-

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267

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lecular carbohydrates responsible, is insufficient oral

hygiene responsible, or is any other factor causing pro-

gression responsible? It could also be looked at the in-

fluence of drug-induced hyposalivation as one of the

main factors of root caries progression in the elderly [24].

Seemingly, it is a well-known scenario in patients at-

tending for their routine dental check-ups to see indi-

viduals under antihypertensive and/or tranquilizing

medication to develop hidden approximal or root dentine

lesions within a very short time after decades of robust

caries inactivity. Is the causative factor just the hy-

posalivation when a change in food intake and oral hy-

giene within the last few months is rather unlikely? An-

other issue is the susceptibility to secondary caries in

teeth with long-term performing composite restorations

with obvious marginal leakage: eighteen years old fill-

ings were followed-up for another two years, and despite

slightly increasing surface deterioration no secondary

caries at the wide gaps was micromorphologically de-

tected [25]. Plaque control at these sites was rather poor,

alimentary regime stressed a slight cariogenic influence,

but the avalanche did not occur.

4. THE AVALANCHE PERIODONTAL

PROGRESSION MODEL

Per Axelsson, Birgitta Nyström and Jan Lindhe fol-

lowed-up 357 subjects maintained in a preventive pro-

gramme for 3, 6, 15 and finally 30 years [26]. The clini-

cal outcome clearly demonstrated: only 21 teeth were

lost due to progressive periodontitis or due to dental car-

ies, and it was evident that the exposure of patients to a

highly individualised maintenance programme in only

one private dental practice provided by the same dental

hygienist was mainly contributing to disease stagnation.

Undeniably, the influence of various factors may have

slowed down the progression of the disease, but man-

agement with a strict preventive programme retarded

tooth loss dramatically, and the avalanche in most cases

did not occur. On the other hand, it is also clinically and

microbiologically well documented that bacterial shift

due to systematic antibiotic treatment regimes may lead

to outbursts of deep pocket periodontal abscesses [27].

This is obviously the result of an overgrowth of antibi-

otic resistant anaerobic pathogens turning a long-lasting

stable periodontal disease into progressive deep pockets

rapidly. Risky snowboarding with antibiotics, though,

may be that fundamental change in environmental com-

mensalism condition to initiate a punctuated equilibrium.

Finally, the prevalence of oral manifestations in HIV-

seropositive showed necrotising ulcerative periodontitis,

erythematous candidiasis and oral hairy leucoplakia to

be significantly associated with the HI-viral load [28].

Again, only one factor - like the famous risky snow-

boarder – out of the complex host response was contrib-

uting to severe disease progression and an avalanche

(Figure 4).

5. CONCLUSIONS

Dentistry is a medical discipline. Therefore, biomedical

principles in their uniqueness in the living world should

be applied to dental problems and solutions. The mam-

malian life is mainly characterised by symbiosis and

harmony of our “own” (eucaryotic) cells and of the

neighborhood (procaryotic) cells, communicating to

each other by signal molecules until – the avalanche

goes down. This is a rare punctuated episode. And the

whole dental care armamentarium should be concen-

trated to these episodes. Rather often we do not know

what is the real cause for a given individual burst. Nev-

ertheless, our preventive programmes and treatment

strategies are powerful and effective bringing back the

harmony disrupted by the avalanche.

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