The concept of immunity in dental caries

I. General considerations

TV. Sims, Ph.D., P.D.S., M.R.C.Path., London, England

PATHOLOGY DEPARTMENT, ROYAL DENTAL HOSPITAL, UNIVERSITY OF LONDON

A precise definition of immunity is surprisingly difficult to formulate, a fact

which is obscured by the common use and abuse of the term. When considering
immunity to a unique disease, such as dental caries,1 even the cardinal features
of which are still subject to speculative controversy and obstinate confusion,
particular care is required. For an erudite discussion of immunity, the reader
is referred to the work of Wilson and Miles,2 who point out that, essentially,
immunit.y means resistance to a8particular diseasebut add that there are varying
degrees of immunity, ranging from complete susceptibility to absolute resistance.
Obviously, the magnitude of attack or the size of the dose of the disease-
producing agent is similarly variable. The observed clinical manifestations of a
disease are the outcome of the degree of exposure to the disease and the sub-
ject’s resistance to this attack. The important corollary is that immunity can
be measured only in t,erms of the size of the dose of the disease-producing agent
resisted and that the potency of the agent can be estimated only by measuring
the amount required to produce disease in a host of known or, more usually,
“average” resistance. It should already be clear that a person cannot be classedas
‘(caries immune” or “ca.ries prone” on the basis of the number of carious teeth
present without someknowledge of the degree of his exposure to caries-producing
condit,ions. The “caries-immune” subject may never have been exposed to the
disease and, if exposed to the same degree as the “caries-prone” person, might
have produced even more carious lesions. Nevertheless, these terms are used
frequently, and almost invariably without justification, in the dental literature.

NATURE OF THE ATTACK IN DENTAL CARIES

The disease-producing agent in dental caries is not simply the bacterial
aggregate on tooth surfaces known as dent,al plaque but dental plaque possessing
certain essential characteristics.3-5 The plaque must contain the necessary con-
670
Volume 30 Immunity in dental caries 671
Number 5

centration of la,ctic acid bacteria6 per given area of tooth surface so that, when
sugar is supplied, acid is produced so rapidly 1y7s* that, in spite of the various
forces opposing such a change,ll 9-12 dissolution of the underlying enamel occurs.
The intensity of attack would depend on the number of tooth surfaces covered
by plaque of this type, the actual degree of acidity produced, and the length of
time during which the plaques were producing and maintaining enamel-dis-
solving acid conditions. There are two requirements for the establishment of
a caries-producing situation: (1) a liberal supply of sugar to facilitate the
build-up of the carbohydrate-dependent lactic acid bacteria3J 5 and to supply
the essential substrate for acid production and (2) the absence of mechanical
forces which would remove or reduce the plaque, that is, a stagnation area.3f 4
Dental caries is absolutely precluded by the absence of sugar59 I3 or conditions
which prevent the formation of dental plaque. I4 It should be noted that plaque
capable of producing caries can form at sites where no lesion can result, as on
restorations or prostheses.4
Delineation of the disease-producing agent in dental caries is not simple and
requires careful thought, but a clear appreciation of its nature is an absolute
prerequisite to a discussion of caries immunity. Measuring the magnitude of the
caries attack presents formidable, and probably insoluble, problems. The only
methods at present available are the various caries-activity tesW5~ I6 which, as
a result of misuse and misunderstanding, have become a source of controversy
and confusion. An attempt to clarify the use and interpretation of lactobacillus
counts and Snyder tests has been presented elsewhere.4 At best, these tests pro-
vide only a crude index of caries activity at a particular time, but they are all
we have and, as discussed earlier, without some means of assessing the intensity
of the caries attack it is impossible to comment sensibly on caries immunity.

RESISTANCE TO DENTAL CARIES

The factors which oppose the occurrence of dental caries fall into two groups
-those which resist the accumulation of plaque and those which counter the
acid dissolution of ena.mel. The first category would embrace the morphology,
arrangement, a.nd occlusion of the teeth; attrition; natural cleansing by the
tongue, cheeks, and saliva; and the various methods of oral hygiene.*, l7 These
factors would probably preserve certain surfaces in the dentition from caries
throughout life, no matter how cariogenic the diet, but many surfaces are lost as
a result of caries originating in other parts of the teeth. A dentition consisting
of completely smooth, well-spaced teeth would probably prove inpervious to
dental caries. It must be clearly understood that freedom from caries in these
instances is due to the absence of plaque and not to some intrinsic resistance of
the teeth themselves. Should the natural cleansing be impeded by a clasp or
band, or by some more drastic alteration in the musculature or salivary secre-
tion, caries will supervene.
Because of normal biologic variation, the actual degree of acidity required
to cause destruction of the enamel varies from mouth to mouth. There are dif-
ferences in acid solubility of the enamel itselfs; differences in the concentrations
of calcium and phosphate ions in saliva and plaque, giving varying values for
672 hhs Oral Surg.
Norclnher, 1970

the “critical pH”l*; and diversity in other factors, such as buffering capacity.lS
Omitting fluoride from consideration, the fact is that, even in the happy circum-
stance in which all these factors a,re maximal with regard to resistance to dental
caries, t,hey are rea.dily overwhelmed by the acid-producing capacity of dental
plaque. Indeed, the most important limiting factor in dental caries is the acid
itself! The lactic acid bacteria produce almost as high a, degree of acidity in
the mouth71ly as they are capable of in any other environment? 20,21; t,heir acid
production is eventually halted by the inhibitory effect of the low pH that they
themselves have created. If streptococci and lactobacilli could produce an acidity
of pH 3.0, instead of their normal limit in the region of pH 4.0, the increase in
caries rate would be devastating.
Some factors (buffering capacity, for example), though usually regarded as
beneficial in opposing acid solution of enamel, are of questionable va1ue.l. Is
The main buffer in plaque is protein,18 and the bulk of the protein in plaque
is contributed by bacteria. Increasing the buffering capacity by increasing the
concentration of organisms is a dubious bargain .2z Although higher buffering
capacity means that more acid is required to1 effect a given fall in pH, more
acid will be produced because the bacteria are correspondingly less inhibited at
the higher pH values.z3 Finally, it is often forgot,tcn that buffers oppose changes
in hydrogen ion concentration in either direction. In highly bufferetl plaque,
although more acid is required to produce damaging pH levels, an equally larger
amount of base is needed to restore the pH to noninjurious values.
Enamel containing an optimum amount of fluoride is less acid soluble than
enamel containing smaller quantit.ies .OAlso, the fluoride ion almost certainly has
some direct effect on bacteriaz4 and possibly enhances resistance to caries in
other ways. 25 Persons whose dentitio’ns have been formed while they were con-
suming water containing the requisite amount of fluoride display a genuine en-
hanced immunity to dental caries.‘” The immunity is genuine because, in view
of the large groups of subjects involved in the fluoridation studies,z7 there is
no doubt that the fluoride groups, on the average, were exposed to a caries attack
similar to that of the control groups and displayed an increased resistance to it.
Such considerations do not apply to many other demonstrations of so-called
caries immunity. The various other ways of presenting fluoride ions to the
enamel would seemto be more correctly regarded as preventive therapeutics. A
similar distinction should be made between natural cleansing of the dentition
and the different methods of oral hygiene. In other words, immunity should re-
quire no conscious effort on the part of the individual or his dentist.

IMMUNITY TO DENTAL CARIES

Now that a(ttnck and resistance as they apply to dental caries have been
briefly defined, the rational use of the term immunity in relation to the disease
can be examined. An initial difficulty is that immunity to other diseasesmeans
immunity of the individual,2 whereas in the case of dental caries a sensible dis-
cussion of immunity requires consideration of discrete sites in the dentition.
Let us consider two hypothetic subjects who habitually consume a highly
Volume 30 Imnuuity iu dental caries 673
Number 5

cariogenic diet. In one, because of the complete absence of cleansing, caries has
occurred at every possible stagnation area in the dentition and each lesion has
been repaired with a faultless restoration. In the other, because of favorable
tooth structure, occlusion, and attrition as well as superlative oral cleansing,
plaque of the necessary characteristics has been unable to form and the dentition
is free of caries. Since both persons are apparently exposed to the disease by
virtue of their cariogenic diets and no caries or no further caries is occurring,
both may correctly be described as immune. It may seem odd to describe some-
one who has suffered the maximum ravages of a disease as immune, but this is
in keeping with usage of the term in reference to other diseases. Indeed, the
whole science of immunology stems from the observation of the ancients that
those who were afflicted with disease and survived were often immune to subse-
quent attacks. 28 Insusceptibility to caries in these two cases is, of course, for
quite different reasons, and a clear appreciation of this difference is crucial to
the understanding of immunity in dental caries. In one subject plaque is present
everywhere but, because it is located on restorations, caries cannot occur. In the
other subject there simply is no plaque. Plaque constitutes the attack in dental
caries, however, and thus the teeth of the caries-free person are not exhibiting
great resistance or immunity because they have not been exposed to attack. A
caries-activity test will confirm this. 4 The person with the ravaged dentition,
because of the masses of plaque, will have a very high lactobacillus count, and
the caries-free subject will have a very low count. Paradoxically, then, it is the
caries-prone subject who is truly immune for only his teeth are displaying
immunity to a bona fide caries attack.
The fact is that natural teeth that are not susceptible to the full brunt of
dental caries simply do not exist. The acid-producing capacity of plaque of
optimal proportions7, 8 is grossly in excess of that required to dissolve the most
acid-resistant enamel in the mo& favorable oral envir0nment.l’ g-12 Sound tooth
surfaces are those on which plaque of the necessary acid-producing capacity has
failed to form. As is well known, caries does not occur indiscriminately in the
dentition; on the contrary, various sites become carious in a fairly orderly
sequence.2gt 3o Sites where plaque forms readily become carious first; areas less
favorable to plaque accumulation become carious later and more gradually;
and where plaque is prevented from building up, the tooth surface remains
sound. The rapidity and final extent of the occurrence of dental caries
will depend on the diet and oral cleansing of each individual. Eventually, a state
that is usually intermediate between the two hypothetic extremes discussed
above is reached. Sites where caries-producing plaque has formed have been
restored or extracted, and the rest of the dentition remains sound. The caries
state becomes stable and the subject is immune to the degree of caries attack
posed by his particular combination of diet and oral cleansing or any less potent
combination. Any change for the worse in diet or cleansing will result in further
caries if sites where caiies can occur still remain.
The full benefits of fluoridation will’markedly retard the caries attack, slowing
the process where the attack is severe and preventing a lesion altogether where
674 Sims Oral Surg.
November, 1970

the attack is slight.2Gl 27 However, carious lesions still develop and the pattern
of occurrence is unaltered, depending, as before, on the degree of plaque ac-
cumulation. As before, the final extent of the disease will be contingent on the
individual diet and oral cleansing.

COMMON MISCONCEPTIONS REGARDING IMMUNITY TO DENTAL CARIES

Easily the most common error concerning immunity to dent,al caries,
whether in regard to a tooth surface, a tooth, a complete dentition, or the dental
status of a whole community, is the assumption that absence of disease is in-
dicative of immunity. A sound tooth surface is a surface which has not been
subjected to an adequate caries attack. A caries-free person is one whose diet and
oral cleansing preclude the formation of caries-producing plaque at any site in
the dentition. Those exceedingly rare, truly caries-immune persons who can
consume a cariogenic diet, practice no oral hygiene, and yet, remain caries-free
are examples not of insusceptibility to carious attack but of the impossibility of
establishing a carious attack. If the anatomy of the dentition and the natural
oral cleansing are such that there are effectually no stagnation areas, dental
plaque cannot form and there is no carious attack. Few readers of this article
will have suffered from rabies, but they are certainly not immune to the disease.
Absence of disease is not, in itself, evidence of immunity, and in the case of
dental caries it is hardly ever so.
The incidence of dental caries and most other diseases varies markedly in
different parts of the world. l, 31 Unfortunately, peoples with a low incidence of
dental caries are frequently described as “caries immune.” A cursory study of
the diets of these peoples shows that, at worst, they have been only moderately
exposed to dental caries; moreover, when they do adopt a. highly cariogenic
diet they cease to evince their “immunity.“l, 32 Undoubtedly, there are cliff er-
ences in caries susceptibility between the different peoples of the world, but
the existence and magnitude of these differences can be established only between
peoples exposed to comparable caries attacks. Why the fact that primitive bush-
men or Eskimos are free from dental caries should be thought to be of any more
significance than, say, the fact that Londoners are free from schistosomiasis is
inexplicable. A frivolous but revealing comparison is afforded by experimental
animals. Dental caries in rats, hamsters, and monkeys is confined to those
creatures housed in various institutes of dental research. In the wild these
animals are caries-free, but it would clearly be wrong to describe them as im-
mune. The long-standing and widesprea,d t,endency to describe caries-free persons
as immune has caused confused thinking and retarded progress.
Next, there is the matter of immunity to dental caries ascribable to age. As
already mentioned, after the passage of a long period of time the degree of
carious attack to which a person is subjected by virtue of his diet and oral
cleansing has completely manifested itself in carious lesions. The carious process
ceases or proceeds a.t an extremely slow rate because all the attacked sites have
been restored or extracted and the sound areas remain unattacked. This is an
immune state, but, unfortunately, the cessation of caries is often attributed to
enhanced resistance of the remaining intact surfaces, this property in some way
 Immunity in dental caries 675

being the consequence of age. As teeth age, they do take up ions and other sub-
stances from saliva which tend to make them more caries resistant,*~lO~ 33
but it would be a gross exaggeration to suggest that this alone explains the
“burning out” of the caries process with age. A tooth surface which is caries
free at a given age has obviously been in that state since eruption, and it
is plainly illogical to suggest that a property that it has been displaying
from the outset is due to age. Once again, the error arises from regard-
ing healthy teeth as resistant teeth, whereas they are merely insufficiently
attacked teeth.
The most serious misuse of the term immunity occurs in the type of study in
which subjects are separated into “caries-active” and “caries-immune” groups on
the basis of their DMF states. Care is taken to see that the groups are compa-
rable with regard to age and so forth, but the fundamental requirement that
both groups should have been subjected to a comparable caries attack is utterly
ignored. Although no attempt is made to assess diet and oral cleansing, it is as-
sumed and tacitly accepted by dentists in general that, because all the sub-
jects are drawn from the same community, institution, or college, they have
all been equally exposed to caries. Dental caries is not a disease like influenza;
because an individual is part of a community in which the disease is rife, it does
not follow that he has been equally exposed to attack. Diet and oral cleansing
are highly individual affairs, and the degree of exposure to dental caries differs
markedly from person to person. While it is all right to describe a large group
or a community as being subject to a certain average caries attack, the same
assumption with regard to caries-ravaged and caries-free persons selected from
that group is flagrantly invalid. Occasionally caries-activity tests are carried out
in these studies, and the results invariably reveal a gross difference in caries
attack in the two groups. These findings, however, do not deter the investigators
from proceeding to account for the difference in caries rate as being the conse-
quence of a lack or excess of some minor esoteric oral factor.
Errors of this type never occur in animal studies because care is taken to
ensure that, within normal biologic variation, all animals compared are sub-
jected to an equivalent caries attack. This makes the frequency with which these
mistakes are encountered in human studies even more remarkable, for not un-
commonly the same investigators are involved. It is a curious fact that while
dentists in general readily affirm that rampant caries is the result of a highly
cariogenic diet and poor oral hygiene, they seem to have the greatest difficulty
in accepting the idea that freedom from caries is achieved by a diet of low
cariogenicity a.nd good oral hygiene. There is an inexplicable predisposition to
attribute the absence of dental caries to almost anything other than the lack
of those factors which are known to cause the diseas,e.
People vary greatly in their standards of oral cleansing, the foods they eat,
and the frequency with which they eat them. Only when the particular combi-
nation of these factors fails to provide an adequate explanation of the caries
status of an individual is it logical to seek alternatives. Only when the caries
experience is irrefutably less than would be expected from the magnitude of
the caries attack is it legitimate to use the term immunity.
 676 Sims Oral Surg.
November, 1970

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1. Brislin, J. F., and Cox, G. J.: Survey of the Literature of Dental Caries, 1948-1960,
Pittsburgh, 1964, University of Pittsburgh Press.
2. Wilson, G. S., and Miles, A. A.: Topley and Wilson’s Principles of Bacteriology and
Immunity, ed. 5, London, 1964, Edward Arnold & Co., Ltd., vol. 2, pp. 1193-1203.
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4. Sims, W.: The Interpretation and Use of Snyder Tests and Lnctobacillus Counts, J.
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Nourished by Stomach Tube. 11. Acidogemc Properties and Selected Bacterial Com-
ponents of Plaques Material, Arch. Oral Biol. 12: 601, 1967.
6. Sharpe, M. E., Fryer, T. F., and Smith, D. G.: Identification of the Lactic Acid Bacteria.
In Gibbs, B. M., and Skinner, F. A. (editors) : Identification Methods for Microbiologists,
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7. Stephan, R. M.: Intra-oral Hydrogen-Ion Concentrations Associated With Dental
Caries Activity, J. Dent. Res. 23: 257, 1944.
8. Sims, W.: Measuremeut of the Rates of Acid Production of Surface Aggregates of
Lactobacilli, Streptococci and Some Other Oral Micro-organisms, Brit. Dent. J. 119:
22, 1965.
9. Brudevold, F., McCann, H. G., and Gron, P.: Caries Resistance as Related to the Chemistry
of Enamel. In Wolstenholme, G. E. W., and O’Connor, M. (editors) : Caries-Resistant
Teeth, London, 1965, J. & A. Churchill, Ltd. pp. 121-140.
10. Darling, A. I.: The Physical Features of Caries-Resistant Teeth. Zn Wolstenholme,
G. E. W., and O’Connor, M. (editors) : Caries-Resistant Teeth, London, 1965, J. & A.
Churchill, Ltd., pp. 149.161.
11. Jenkins, G. N.: Tho Equilibrium Between Plaque and Enamel in Rdatiou to Caries
Resistance. In Wolstenholme, G. E. W., and O’Connor, M. (editors) : Caries-Resistant
Teeth, London, 1965, J. & A. Churchill, Ltd., pp. 192.210.
12. Leung, S. W.: The Role of Saliva in Caries. In Wolstenholme, G. E. W., and O’Connor,
M. (editors) : Caries-Resistant Teeth, London, 1965, J. & A. Churchill, Ltd., pp. 266-283.
13. Kite, 0. W., Shaw, J. H., and Sognnaes, R. F.: Prevention of Experimental Tooth
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14. Orland, F. J., Blayney, J. R., Harrison, R.. W., Reyniers, J. A., Trexler, P. C., Wagner,
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of Experimental Dental Caries, J. Dent. R,es. 33: 147. 1954.
15. Snyder, M. L., Porter, D. R., Claycomb, C. K., and Sims, W.: Evaluation of Laboratory
Tests for the Estimation of Caries Activity, J. Amer. Dent. Ass. 65: 30, 19862.
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of Laboratory Tests for the Estimation of Caries Activity, Arch. Oral Biol. 8: 541, 1963.
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Disease, Northwest Dent. 45: 3, 1966.
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20. Florestano, H. J.: Acidogenic Properties of Certain Oral Micro-organisms, J. Dent. Res.
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22. Clement, A. J., Plotkin, R., and Fosdick, L. S.: The Formation of Lactic Acid in Dental
Plaques; Oral Conditions of Primitive Bushmen of the Western Kalahari Desert, J. Dent.
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23. Englander, H. R., Carter, W. J., and Fosdick, L. 8.: The Formation of Lactic Acid in
Dental Plaques. Caries Immune Individuals, J. Dent. Res. 35: 792, 1956.
24. Sims, W.: The Effect of Sodium Fluoride on the Rate of Acid Production of Surface
Aggregates of Streptococci and Lactobacilli, J. Demt. Res. 45: 915, 1966.
25. Simpson, W. J., and Castaldi, C. R,.: A Study of Crown Morphology of Newly-Erupted
First Permanent Molars in Wetaskiwin, Alberta (Optimum Fluoride) and Camrose,
Alberta (Low Fluoride), Odont. Rev. 20: 1, 1969.
26. Backer Dirks, 0.: The Relation Between the Fluoridation of Water and Dental Caries
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27. Blayney, J. R.., and Hill, I. N.: Fluorine and Dental Caries, J. Amer. Dent. Ass. (special
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28. Humphrey, J. H., and Whito, R. G. : Immunology for Students of Medicine, cd. 3, Oxford,
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29. Klein, H., and Palmer, C. E.: Studies on Dental Caries. XII. Comparison of the Caries
Volume 30 Immunity in dental caries 677
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Susceptibility of the Various Morphological Types of Permanent Teeth, J. Dent. Res.

20: 203, 1941.
30. Barr, J. H., Diodati, R. R., and Stephens, R. G.: Incidence of Caries at Different Loca-
tions on the Teeth, J. Dent. Res. 36: 536, 1957.
31. Finn, 5. B.: In. Survey of the Literature of Dental Caries, Publication 225, Washington,
D. C., 19582, National Academy of Science, National Research Council, p. 117.
32. Holloway, P. J., James, P. M. C., and Slack, G. L.: Dental Disease in the Inhabitants
of Tristan Da Cunha in 1962, Arch. Oral Biol. (special ORCA supplement) p. 337, 1963.
33. KGnig, K. G.: Caries Resistance in Experimental Animals. I?z Wolstenholme, G. E. W.,
and O’Connor, M. (editors) : Caries-Resistant Teeth, London, 1965, J. & A. Churchill,
Ltd., pp. 87-106.