The Microbial Ecology of Dental Caries

G. H. W. Bowden

To cite this article: ​G. H. W. Bowden (2000) The Microbial Ecology of Dental
Caries, Microbial Ecology in Health and Disease, 12:3, 138-148, DOI:
10.1080/089106000750051819

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REVIEW ARTICLE

The Microbial Ecology of Dental Caries

G. H. W. Bowden

From the Department of Oral Biology, Faculty of Dentistry, University of Manitoba, 780 Bannatyne Avenue, Winnipeg,
Manitoba, Canada R3E 0W2

Correspondence to: George Bowden, Department of Oral Biology, Faculty of Dentistry, 780 Bannatyne Avenue,

Winnipeg, Manitoba, Canada R3E 0W2. Tel: ​+​1 204 789 3595; E-mail: george​–​bowden@umanitoba.ca

Microbial Ecology in Health and Disease 2000; 12: 138–148

The microbial ecology of caries is complex and incorporates mechanisms common to the natural colonization of the host and to plaque
accumulation at sites that do not develop caries lesions. It is not simply accumulation of plaque in the oral cavity but also the ecology of oral
bacteria among the host population and the ecology of organisms in the lesion. In these three habitats odontopathogens and other oral bacteria can
undergo genotypic change, which may produce phenotypes more virulent or better able to survive specific evironments. Adaptation and response to
stress will also enhance bacterial survival and selection. Therefore, in these habitats diversity is generated and this, coupled with adaptation,
provides strains that are selected to be best suited to specific environments, including cariogenic environments. In this way odontopathogens may
be selected and become more numerous among hosts in a population. The most common ecological mechanism associated with caries is bacterial
succession, and dominance of the plaque community by mutans streptococci. However caries is the outcome of interactions within the plaque
community, host physiology, diet, fluoride, pH and the nature of the tooth enamel, and dominance by mutans streptococci does not always produce
a lesion. Caries can be reduced by bacteria that degrade lactate or produce base from urea and salivary peptides, while other bacteria, including a
group of ‘low pH’ streptococci could lower the pH of plaque, and produce enamel demineralization. In addition, the plaque biofilm not only serves
as a habitat but includes in its structure a fluid phase (plaque fluid) and a matrix that have a direct influence on the physiology of plaque bacteria
and the formation of a lesion. Given the complexity of the microbial ecology of caries even with the elimination of mutans streptococci caries
would most likely persist, albeit at a significantly reduced level. ​Key words​: biofilms, caries, microbial ecology, mutans streptococci, plaque fluid.
some extent by limiting studies to a selected stage or
quence of stages in the ‘life cycle’ of a specific bacterial
INTRODUCTION rain, a species, or a bacterial community. This approach has
een taken with oral microbial ecology, where study is usually
Microbial ecology describes the interaction between mi- ade of the stages of plaque accumulation, the biology of
croorganisms and the structural, physical and biological pecific bacteria or selected microhabitats, and plaque
components of their habitats and infectious diseases provide hysiology. However, studies of the ecology of oral bacteria in
examples of the impact of ecology of specific organisms on aries have not been limited to their activities in the mouth. A
their host populations of plants or humans and other animals. le for the human host population as a reservoir for mutans
Moreover, disease promotes responses from the host, changing reptococci (6) has been considered in relation to transmission
the ecology between the host and the bacteria, influencing the mong hosts (7–9) and in approaches to prevent caries in
well-being and activities of the host population (1). Examples umans (10, 11). Also, studies of antibiotic resistance and
of the responses of host populations that affect microbial pecific genes of indi- vidual strains of oral bacteria have
ecology include vaccina- tion, to reduce the ability of bacteria vealed evidence for transfer of genetic characters that
to colonize the host and delivery of fluoride in water and nhances their diversity (12–15). Furthermore, the ecology of
dental products that modifies bacterial metabolism and reduces aries includes not only the processes that cause destruction of
the incidence of caries. Considering microbial ecology and its namel but also those that promote bacterial invasion of
outcomes, at the level of infectious disease with a specific entine. Clearly, the microbial ecology of caries involves at
pathogen (2–5) makes it clear that complex mechanisms are ast three easily recognizable areas, 1. Bacterial ecology
in- volved and assessing their function in nature is a difficult mong the host population, 2. The ecology of the plaque
task. This problem is made more complex when, as is the case ommu- nity, 3. The ecology of the community within the
with dental caries, odontopathogens are usually com- ponents sion. Figure 1 shows the relationships between areas 1 and 2,
of the resident flora of the host, unlike many other overtly hich determine the composition and contribute to the
pathogenic bacteria. icrobial diversity of the oral flora of an individual host.
Analysis of microbial ecology has been simplified to

© Taylor & Francis 2000. ISSN 0891-060X ​Microbial Ecology in Health and Disease
There are several reviews and book chapters that discuss the
microbial ecology of caries (16–20). Consequently, this review
will try to emphasize and discuss areas that are problematic
and those that require more study.
THE COMPLEXITY OF ORAL MICROBIAL
ECOLOGY AND CARIES
A problem in understanding microbial ecology of caries is that
many of the events that leadecology
The microbial to theofdevelopment
dental caries ​1of
39a caries
lesion are common to those associated with healthy enamel. In
human nursing caries ​S.​ ​mutans c​ an predomi- nate at sites that
develop a white spot and those that do not. This can occur
even at adjacent susceptible sites in the same individual (21).
Similarly, van Ruyen et al. (22) have shown no significant
difference between the numbers of ‘low pH isolates’ from
white spot lesions and normal enamel in subjects with caries.
Explanations for such ob- servations include suggestions for
local environmental dif- ferences and ecological mechanisms
that could modify the microflora to reduce its cariogenic
potential (17, 19, 20, 23). The significance of the presence of
 mutans strepto- cocci, diet and dietary sucrose, fluoride, poor
oral hygiene and host antibodies on caries ​in ​6​i​6​o ​is well
accepted. However, some other factors that may be involved
such as 1.Complex interactions among cells within the dental
plaque biofilm (24), 2. Novel expression of genes during
biofilm formation (25, 26), 3.Stress responses by oral bacteria
(27), and 4. The ability of bacteria to modify local
environments (23, 28) may often be supported predomi- nately
by findings ​in ​6​itro.​ Confirmation of their roles in caries in
animals or preferably in humans, is an important topic for
research in oral microbiology. ​In ​6​itro s​ tudy of mechanisms is
essential to aid in developing strategies for prevention and
control of caries however, the true value of
any strategy has to be confirmed ​in 6​ ​i6
​ ​o ​and preferably in
humans.
A second significant point is that although many
aspects of the caries process are common among hosts they
may be influenced by factors that reflect the individuality of a
person and their microflora. The common processes in- clude
adhesion, co-aggregation, growth and survival, which are basic
to bacterial colonization of the mouth (29–32). However,
genetic variation among hosts, their habits and immunological
history (e.g. disease, vaccina- tion), together with the variety
of habitats in a given mouth, and the diversity among strains of
Fig​. ​1​. The stages involved in colonization of infants by oral bacteria from the host population and the factors that contribute to the diversity among
the bacterial populations within the oral cavity and the plaque biofilm.
G​. ​140 ​H​. ​W.​ ​Bowden Fig.​ ​2​. Stages in the accumulation of dental plaque, including the factors that contribute towards the metabolic activities of
the plaque biofilm that determine the outcomes of oral microbial ecology in caries.
physiologically based nutrients, oral bacteria receive an erratic
input of variable substrate from the hosts’ diet, an important
factor in caries risk (37). Apart from the nutri- tional
components of saliva there are molecules that en- hance
colonization and those that have an adverse effect on oral
bacteria (38–43). Saliva also acts as a buffer, modifying plaque
pecies of oral bacteria that colonize a host are unique to a
erson. Therefore, while general observations can be made of
icrobial ecology and the development of a carious lesion it
as to be recognized that host specific factors also influence
e process.
IGNIFICANT FACTORS IN THE MICROBIAL
COLOGY OF CARIES
efore discussing microbial ecology and caries some of the
omponents and factors shown in Figures 1 and 2 should be
scussed. The final outcome of the interaction among these
fferent factors and processes at a specific site on the
entition determines the formation, or not, of a caries lesion.
he habitat
he oral cavity provides an excellent environment for the
rowth and survival of bacteria. Although saliva is not a
omplete nutrient for all oral bacteria some species or
onsortia of species utilize it as a substrate (30, 33–36). Other
ral nutrients arise from gingival crevicular fluid and
esquamated mucosal cells. Also, in addition to these
pH and reduced salivary flow, xerosto- mia and the variation
in salivary flow over different tooth surfaces can influence the
formation of a caries lesion (44–46). In addition fluoride,
which can dramatically influ- ence the carbohydrate
metabolism of bacteria is a signifi- cant component of both
saliva and plaque. Fluoride delivery has proved to be one of
the most important anticariogenic strategies available, and its
 action is based on modification of the ecology of bacteria and
interaction with enamel and tooth root (47).
The hard (enamel and tooth root) and soft (mucosal)
tissue surfaces in the mouth provide a variety of microhab-
itats with distinctly different structural and environmental
parameters. In particular, the non-shedding surface of enamel
allows the accumulation of a biofilm that provides a protected
habitat with a variety of niches that support a wide range of
bacterial genera and species (48, 49). The plaque biofilm is an
essential factor in the aetiology of
caries. The interactions among the bacteria in dental plaque
together with the variations in nutrient, buffer, fluoride,
concentrations of various ions and pH in the biofilm determine
the formation of a caries lesion.
In addition to forming the substratum for dental
plaque accumulation enamel and tooth root are the tissues that
are destroyed during the formation of a caries lesion. The
composition of enamel varies among teeth and even over the
surfaces of a single tooth. These variations include the degree
of mineralization and also the fluoride content (50, 51).
Significantly, the composition of enamel is a determi- nant in
its susceptibility to demineralization and conse- quently
variation in enamel at a site can influence the development of
caries lesions (52).
Bacteria associated with caries in humans
These bacteria are opportunistic pathogens, found com- monly
as members of the resident flora of persons without caries and
expressing their pathogenicity only under spe- cific
environmental conditions. ​Streptococcus mutans ​and
Streptococcus sobrinus​, two species of the ‘mutans strepto-
cocci’ are the most significant in human caries (16, 19, 53) and
studies of the microbial ecology of caries have been directed
principally at these species (21, 54–56). There is
also a strong association between ​Lactobacillus s​ pp. and caries
but little is known of the relative significance of the different
species.
It has been apparent for years that other genera and
species of oral bacteria can either be associated with caries in
humans, or cause caries in experimental animals (17, 22,
57–59). In particular, although ​S.​ ​mutans ​and ​S​. ​sobrinus ​are
the principal agents of enamel caries, a wider range of
organisms is proposed as opportunist pathogens in root surface
caries. Generally the organisms other than mutans streptococci
and ​Lactobacillus ​associated with caries fall into
Streptococcus a​ nd ​Actinomyces.​
Actinomyces odontolyticus,​ originally isolated from
caries lesions (60), colonizes infants before eruption of teeth
(61). An association between this species and pro- gressing
incipient interproximal caries lesions in humans has also been
shown (62). Some root caries lesions are dominated by
Actinomyces naeslundii a​ nd it has been suggested that strains
of this species could play a patho- genic role in this disease
(63–66) and recently, ​A​. ​israelii a​ nd ​A​. ​gerencseriae h​ ave also
been shown to be present in high numbers in root caries
lesions (67). Schu ̈pbach et al., (65) demonstrated the
complexity of the bacterial commu- nity associated with root
caries and most importantly, they correlated the microflora to
the state of lesions in extracted teeth (66).
The other significant ​Streptococcus ​species involved in
caries includes ​Streptococcus mitis (​ 58, 63) and a group of
‘low pH’ aciduric streptococci (68). Recently, these, and other
‘low pH’ isolates (possibly ​Bifidobacterium ​and ​Acti​-
nomyces​) have been isolated from white spot lesions in
humans (22).
In contrast to bacteria that lower plaque pH there are
others including ​Veillonella a​ nd ​Actinomyces t​ hat degrade
lactic acid, thereby increasing plaque pH and reducing its
cariogenicity. This proposed anti-caries mechanism has been
shown to be effective with ​Veillonella b​ oth ​in ​6​itro a​ nd in an
animal model (69–71). A second bacterial process promoting
an increase in plaque pH is the produc- tion of base from urea
and the arginine containing pep- tides in saliva (31, 72). Oral
streptococci and actinomyces can be protected in low pH
environments by expression of urease (26, 73, 74). Recently,
studies with recombinant strains of ​S.​ ​mutans i​ n experimental
animals have shown that urease production by strains
contributed to reduction of caries (75). Also, support for this
‘anticariogenic’ effect comes from studies of plaque pH ​in
6​itro a​ nd ​in ​6​i6
​ ​o ​(76, 77) and from patients with chronic renal
failure, who have high levels of salivary urea and show a
reduction in caries (78).
​ ​ersity among strains of species of oral bacteria
Di6
The microbial ecology of dental caries 1
​ 41
Although bacterial populations in oral microbial ecology are
often studied at the level of species, it is well accepted that
phenotypic characteristics among strains of bacterial
pecies can vary. Differences in phenotype may be impor- tant
caries if specific variants within the plaque commu- nity at
calized sites on the dentition were ‘more cariogenic’ or, in
ontrast, strains had increased capacities to degrade lactate or
roduce base from urea and salivary peptides, reducing the
ariogenicity of plaque. In addition, changes in the phenotypes
plaque could influence bacte- rial selection and survival (31,
9) and the overall (commu- nal) activities of the plaque
ommunity (see below). In the past variations among strains of
species were identified by biochemical, physiological and
ntigenic differences. Analysis of variation in their enzyme
rofiles or their genomic DNA (31) has identified more
cently individual strains (clones). The DNA typing methods
ave been valuable in showing the transmission and
persistence of clones of oral species within and among their
host popula- tion and the diversity among clones of a species
in a habitat (8, 79, 80).
Variations in the genome of daughter compared to
parent cells can originate from mutation, transposition and
recombination and also integration of DNA from other
bacteria (79, 81). Therefore, the genome of strains within oral
species may differ, resulting in a species population composed
of clonal variants (31, 80, 82, 83). Commensal bacteria,
including oral opportunistic pathogens usually, but not always,
show more genetic diversity than overt pathogens and very
often several different clonal variants will colonize a single
host (31, 79). Interestingly, from the aspect of colonization of
a host population clones of oral species can have a specific
association with a limited group of hosts (84, 85). Although
there are data on clonal diversity within oral species there is
relatively little on any relationship between such variation and
the phenotype or virulence of strains of oral opportunistic
odontopathogens (31).
In addition to generation of diversity through
changes in their genomic DNA strains of species of oral
bacteria colonizing a mouth may be influenced by ‘clonal
replace- ment’. In ‘clonal replacement’ new clones replace the
exist- ing clones in a habitat and contribute to strain diversity
(79). ‘Clonal replacement’ may be more common on mu- cosal
surfaces where cells are shed, compared to the dental plaque
biofilm, which provides a retentive and protected habitat.
Adaptation by oral bacteria to en​6​ironmental parameters
Apart from ecological advantages provided to oral bacte- ria
arising through changes in their genome they will also adapt
(phenotypic adaptation) and respond to environ- mental stress
in order to survive. Generally, adaptive and stress response
mechanisms such as tolerance of acid, starvation, oxygen,
fluoride and expression of urease (26, 27, 31, 72, 73) that are
common among strains of a species can be regarded as having
evolved to assist bacteria to survive stresses common to their
habitats (86). Phenotypic
G​. ​H​. ​W.​ ​Bowden ​142
adaptation is usually transient and expressed only during stress
(31). However, stable adaptation to tolerate xylitol by ​S.​
mutans h​ as been shown ​in ​6​i6 ​ ​o a​ nd although xylitol will
hysical changes seen in enamel (95) during the formation of a
normally inhibit the growth of ​S.​ ​mutans,​ xylitol tolerant
strains are selected when ​S​. ​mutans i​ s grown ​in ​6​itro o​ n
een used ​in 6​ ​itro ​to show the importance of such coatings in
another carbohydrate (glucose) in the presence of xylitol (87).
aries lesion formation and also, their interaction with different
An important feature of adaptation and survival of
bacterial cells in sub-optimal growth environments (e.g. low
pH, heat, starvation), is expression of a range of ‘stress
xtracellular matrix and a fluid that bathes both cells and
proteins’ (88–90). These proteins that promote the survival of
the cells in adverse conditions are the subjects of extensive
research. Relatively little is known of stress proteins in oral
bacteria, although information is accumu- lating (27).
Significant to the current discussion is that adaptation or
response to stresses varies among different oral species and
among strains of a species, including odontopathogens (91).
Responses by bacteria will also include the production
of different signaling molecules that influence the activities of
the cells within the population (92). Signaling molecules
include peptide pheromones that promote competence and cell
density dependent peptides in Gram positive and ​N​-acyl
homoserine lactones in Gram negative cells (24). These latter
density dependent molecules are responsible for ‘quorum
sensing’ in bacterial populations, promoting expression of
genes when the population has reached a specific cell density.
In one case a molecule that seems to act in a ‘quorum sensing’
manner has been demonstrated in an ​in situ m ​ odel of dental
plaque (93).
The biofilm mode of growth
Dental plaque is a complex biofilm community where bacterial
populations exist as separated micro-colonies in
physiologically diverse environments. Biofilm cells exhibit
different characteristics from the same cells growing in
suspended culture (24). Together with demonstration of the
unique characteristics of biofilm cells has come the
recognition that bacteria in a biofilm can form a commu- nity
where the spatially distributed populations may inter- act (24).
Caldwell and his colleagues have described the concept and
implications of bacteria growing as communi- ties (94). The
activities of a community (communality) are distinct from
those of a simple mixture of the same bacte- rial populations
and the community life style provides advantages compared to
those of the component popula- tions. The range of habitats for
colonization can be ex- tended, resistance to stress and host
defenses will increase, and cooperative degradation of
complex substrates can take place (24). However, it is
important to recognize that the presence of an organism in a
biofilm does not necessar- ily mean that it is part of a
community. Some bacterial populations could be present in
their defined area of the biofilm, physiologically isolated from
other populations, without interaction.
The composition of the plaque biofilm community is
rectly related to the process of formation of a caries lesion.
lso, the presence of a biofilm is important in governing the
sion. Gelatine gels and biofilms of ​Streptococcus s​ pp. have
ns (96–99).
Biofilms consist of three physical components, cells,
atrix. Although the knowledge of the bacterial popula- tions
plaque is far from complete over 300 taxa have been
described. Relatively little is known of the composi- tion of
the extracellular matrix of plaque ​in ​6​i​6​o ​(100) but given its
relationship to the formation of lesions, the composition of the
matrix and factors controlling its com- position and production
would seem to be an important area for research. However,
there are ​in 6 ​ ​itro s​ tudies of the structure and impact of
bacterial polysaccharides on diffu- sion and demineralization
(101–104). The fluid component of plaque, plaque fluid, plays
a significant role in caries and microbial ecology. This fluid
can be regarded as the ‘planktonic phase’ of dental plaque and
as such its compo- sition reflects not only the outcome of the
physiological and metabolic activities of the plaque microflora
but also the result of the dynamic interaction between these
activi- ties and tooth enamel. Importantly, differences in
compo- sition have been shown between plaque fluid from
samples of plaque from caries free and caries active persons
after sucrose rinses. Margolis & Moreno (105) discuss various
aspects of plaque fluid, including variation in composition and
the relationships between plaque fluid and demineral- ization
and remineralization of enamel. Although methods are
available to analyze the composition of plaque fluid from
single tooth surfaces (106–108) relatively few studies (97, 98)
have been made of plaque fluid from mixed or single culture ​in
6​itro b​ iofilms. Information on the influ- ence that the
composition of this fluid has on the physiol- ogy of biofilm
cells and vice versa, would be very valuable. In particular, the
potassium levels in plaque fluid are higher than those in saliva
and extracellular potassium levels influence bacterial
metabolism (109–113). Plaque fluid also probably acts as a
‘carrier’ for substrates, the endproducts of bacterial
metabolism and the signal molecules that mediate interaction
between bacterial cells. It seems most likely that the channels
that run through the plaque biofilm (114) are conduits for
plaque fluid.
The foregoing has emphasized some of the aspects
of microbial ecology that contribute to the complexity of the
biology of dental plaque and factors that can influence its
cariogenicity. Despite this potential complexity, caries re-
mains a common problem in humans, suggesting that the
occurrence of one or more combinations of factors neces- sary
to produce a lesion is also common. It is possible that among
these factors are those that may play a greater role
than others. Given a normal resident flora, which would
include odontopathogens, one can consider diet to be one such
dominant factor (37). However, even under dietary conditions
that favour caries identical bacterial succession may only
produce a lesion on one of two adjacent suscep- tible sites in
the same person (21).
MICROBIAL EVENTS LEADING TO THE
FORMATION OF A CARIES LESION
dhesion and coaggregation
wide variety of oral bacteria will have colonized the
ucosal surfaces of the oral cavity of infants prior to their
cquisition of ​S​. ​mutans a​ nd ​S.​ ​sobrinus​. Therefore, mu- tans
reptococci adhering to the newly erupted non-shed- ding
urfaces of teeth do so in competition with a wide variety of
tablished oral bacteria (29). Bacteriocin pro- duction is one
echanism that promotes colonization of ​S​. ​mutans ​in the
resence of other bacteria (117) and detailed analyses of these
olecules has been made (120).
Plaque accumulation is a dynamic process and central to the
microbiology of caries is the concept that the plaque
community responds to autogenic (internal) and allogenic
(external) stimuli that modify the parameters of the niches
available for bacterial populations (16, 48). The changing
niches and interactions (24) result in sequential selection of
component populations (succession) within the community of
bacteria that develops to be in balance with its environ- ment
(climax community). Figure 2 shows the stages of
accumulation of dental plaque together with the factors
described above that can influence the ecology of the
microflora during the formation of a climax community, and
also the possible outcomes of such accumulation.
Two processes that are not mutually exclusive and may
be perhaps two stages of the same process can describe the
microbial ecology of caries. The most obvious, well de-
scribed and easily understood is bacterial succession in an
environment (e.g. high carbohydrate, low salivary flow)
leading to local dominance by mutans streptococci, fol- lowed
by enamel demineralization and cavitation, that often involves
Lactobacillus ​(16–20). This process proba- bly accounts for
the majority of caries lesions in humans. The second process
involves different species of bacteria (22, 58, 59, 65, 66) and
perhaps, the communal activities of plaque. It is more
speculative, with less evidence to sup- port it, compared to
dominance by mutans streptococci. Both of these processes are
illustrated in Figure 2 and discussed below.
Dominance by mutans streptococci
Theinmicrobial
The risk of caries childrenecology of dentalby
is influenced the 1​ oral
caries 43 health
status and attitudes of their care-givers (115), al- though
isolation frequencies of odontopathogens in chil- dren may be
independent of their socio-economic background (116). The
ease of transmission and coloniza- tion of infants and children
by mutans streptococci could be regarded as the earliest stage
in the process leading to dominance of plaque by these
bacteria. Factors influencing the transmission, oral
colonization, caries risk and survival of ​S.​ ​mutans ​among its
hosts have been described (6, 7, 10, 11, 117, 118). Clones of ​S.​
mutans ​vary in virulence (119) and selection or generation of
 more virulent clones of ​S​. ​mutans w ​ ithin the host population
could also influence the process of dominance by this species.
A second mechanism for adhesion of bacteria to the
dentition is by interaction with previously adherent bacte- ria,
through a process described as co-aggregation (32).
Co-aggregation of ​S​. ​mutans w ​ ith ​Actinomyces h​ as been
shown ​in 6 ​ ​itro (​ 121) and ​Veillonella a​ nd ​S​. ​mutans c​ oag-
gregate ​in ​6​i​6​o (​ 122).
Growth and response to the en​6​ironment
Although co-aggregation is significant it is only one of the
mechanisms that determines the composition of dental plaque.
Two other factors, the growth of bacterial cells in plaque (30),
and the survival of strains that cannot grow (31, 79), also play
important roles. There is a close associ- ation between diet and
caries that identifies carbohydrate and acid production by
plaque as significant risk factors for caries (19, 22, 37, 123).
Dominance by ​S​. ​mutans ​or ​S​. ​sobrinus i​ n areas of the plaque
biofilm indicates that a strain or strains of these species occupy
a favourable niche with available carbohydrate and a low pH
(16, 23). It is the latter parameter that has featured
predominantly in explaining the etiology of caries. The
relationship between the ‘resting pH’ of plaque, the
characteristics of the Stephan Curve including the lowest pH
level reached and the time of recovery to the resting pH, are all
related to caries risk (123). Selection of aciduric bacteria in
plaque environments of low pH remains the central and funda-
mental concept in the microbial ecology of caries.
An unanswered question is whether ​S.​ ​mutans ​is
always responsible for the reduction in pH that gives it an
ecolog- ical advantage in plaque. Other organisms such as the
‘low pH’ group (22, 124) may initially lower the pH of the
local plaque environment and thereby promote dominance by
mutans streptococci. Some ​in 6 ​ ​itro ​data support a role for
other organisms in lowering the pH of communities of oral
bacteria sufficiently to decalcify enamel or promote domi-
nance by mutans streptococci (121). Studies in humans using a
banding model also suggested that early enamel
decalcification, presumably resulting from low pH could occur
in the absence of ​S.​ ​mutans ​(57). However, in this study
colonization by mutans streptococci was more com- mon as
the bands were left on the teeth for longer periods, suggesting
that the early non-mutans organisms produced an environment
conducive to colonization by mutans streptococci (125).
Recently Van Ruyven et al. (22) have
G.​ ​H​. ​W​. ​Bowden 1
​ 44
proposed a model for succession in caries that takes into
account carbohydrate intake, ‘low pH’ groups of bacteria and
redominant species in lesions suggests that the process of
mutans streptococci. In any event, there is substantial evidence
that succession in a suitable environment leads to local
pecies involved. Again it is assumed that such succession to
dominance by mutans streptococci that is associated with
formation of a caries lesion.
As stated above, it is less easy to explain why under
apparently identical conditions, even in a child at high caries
risk, ​S.​ ​mutans ​dominance at an adjacent susceptible site does
not always lead to caries (21). In this case, although the
environment promoted dominance by the organism,
demineralization did not occur. As we have seen above and in
Figure 2 a variety of complex factors may be involved in
determining the formation of a lesion and more data are
available on some than others: 1. The time of exposure to a
‘cariogenic’ plaque may be too short, 2. Salivary flow and
fluoride levels at each site might be different, 3. The
composition and fluoride content of the enamel at the sites
may vary, 4. The local community or individual bacterial
populations may increase the plaque pH at the ‘resistant’ site,
5. Strains of mutans streptococci at the two sites may vary in
virulence, 6. The plaque fluid within the biofilm at the
resistant site can provide a different environment for the
biofilm community and influ- ence demineralization, 7.The
sites may receive differing levels of carbohydrate, 8. The
populations of mutans strep- tococci may be in different spatial
relationships to the enamel surface, 9. Unknown chemical
mediators that mod- ify the physiology of ​S.​ ​mutans ​may be
present in plaque at the ‘resistant’ site.
Although there is a plethora of factors and interactions
that can influence dominance by ​S.​ ​mutans l​ eading to the
formation of a caries lesion it is possible that at some point this
organism may be released from any constraints of the
community. A dominant microcolony might become
independent of the other populations in the community and
‘control’ its own environment (126). This would mean that
essentially in a limited area the population could be acting in a
manner similar to cells in a biofilm in mono-as- sociated
gnotobiotic animals. The release of such a micro- colony from
any ‘community control’ may encourage lesion formation.
Finally, a point worth noting is that mutans strepto-
cocci, like other oral bacteria can, in all probability, survive in
the plaque biofilm in the absence of an immedi- ately available
niche (31). These cells could take advantage of any change in
the environment that provided a suitable niche and then move
to dominance in the community.
THE INVOLVEMENT OF BACTERIA OTHER THAN
MUTANS STREPTOCOCCI IN CARIES
The results from several studies (see above) suggest that other
bacteria can also become dominant in plaque com- munity and
be associated with demineralization and for-
ation of a caries lesion. The common finding of a
lection, succession and dominance is independent of the
dominance is based on selection in an environment of low pH.
However, there is some evidence that the pH associated with
root surface lesions may not necessarily be any lower than that
of plaque on normal enamel (127). Also, early lesions of root
caries seem to favour ​Actino-​ ​myces ​(65), which are generally
less acid tolerant compared to mutans streptococci (125, 128).
Consequently, although acid selection may operate, it may be
less stringent in some cases and favour bacteria that while
being less aciduric than mutans streptococci are still able to
destroy tissue. Also, it is known that other species and strains
may be as aciduric as mutans streptococci (22).
We lack evidence for caries being the result of the
collaborative activities of a community (communality), as we
usually tend to find dominance by a particular strain. However
it could be argued that communality is responsi- ble for all
caries lesions. The formation of a lesion is the end result of a
temporal process involving the bacterial community and also
the physiology of the host. Certainly, other organisms and
interactions (i.e. communality) are invoked for reducing the
cariogenicity of plaque. However, as mentioned previously,
the failure of these anti-cario- genic interactions and the loss of
‘communality’, which promotes isolated activity by a specific
odontopathogen could promote caries.
The microbial ecology of the lesion
Bacteria decalcify enamel and tooth root and may follow
protein in the enamel, and invade dentine via the tubules (95).
It is well accepted that the microflora of lesions in teeth and
tooth roots is extremely complex and may vary at different
sites (65, 125, 129). Although decalcification is a major factor
involved in the initiation of enamel and root caries,
degradation of dentine probably involves pro- teolysis (130).
Also, specific receptors allow ​Lactobacillus t​ o localize to
exposed dentine, via collagen receptors (131) and similar
molecules may be present on other bacteria. The results of
Schu ̈pbach et al. (66) are particularly signifi- cant when the
possibility of succession in caries lesions is addressed. These
authors found different species to be predominant in the flora
of lesions of different severity, suggesting that succession
could occur during lesion for- mation. They present a detailed
and logical discussion of the microbiology of caries lesions
based on their careful sampling and extensive analysis of the
microflora.
The populations in the lesion community may also
be spatially distributed in a manner similar to those in a
biofilm. Therefore, one could suggest that a range of niches
and microhabitats could equally well exist within a lesion.
Spatial distribution could be one explanation of the finding of
the same patterns of distribution of ribotypes of
A.​ ​naeslundii,​ in samples from enamel, root and caries lesions
of individuals (80), although in one case they have been shown
to have different phenotypes (79). The empha- sis that has
been placed on the mechanisms involved in the initiation of
caries lesions in enamel is easily understood in terms of
designing strategies to prevent caries. However, the microbial
ecology of the stages of dentine destruction presents an equally
fascinating area for study.
CONCLUSIONS
The microbial ecology of caries includes the biology of oral
bacteria within three related habitats 1.The host population, 2.
The oral cavity of individuals and 3. The caries lesion. The
distribution of odontopathogens among the host population
influences the colonization of infants and children. Caries in
an individual is characterized by a series of interactions and
succession within the plaque biofilm as the populations
respond to environmental changes and succession probably
also occurs in the lesion. The population interactions are
complex and apart from the commonly known mutualism,
competition etc. involve stress responses, adaptation, variation
in gene expression, genetic variation and probably ‘quorum
sensing’. All of these can result in selection of bacteria,
including odonto- pathogens best suited to the environment,
which in some cases is conducive to caries. Modulation of the
microbial ecology of caries using relatively simple approaches
such as oral hygiene, diet control and fluoride are very
effective. Perhaps that is because they modulate the oral
bacterial community so that the bacteria cannot adapt, (oral
hy- giene), or control a significant parameter (diet) or adapta-
tion reduces the cariogenicity of odontopathogens (fluoride).
Other approaches to modulate the flora and control caries e.g.
antibacterials (132), immune mecha- nisms (133), replacement
therapy (134) are attractive and more sophisticated in concept
and delivery. However, in general these approaches are
directed at mutans strepto- cocci and although their use would
make significant reduc- tions in caries, they may not eliminate
the disease. As we have seen, oral microbial ecology is
complex and other, somewhat forgotten bacteria, could assume
the role of mutans streptococci in caries.
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