Role of the Oral Microflora in Health
Philip D. Marsh
From the Research Division, Centre for Applied Microbiology & Research, Salisbury, SP4 0JG, and Division
of Oral Biology, Leeds Dental Institute, Leeds, LS2 9LU, UK
Phone: 44 (0)1980 612 287; Fax: 44 (0)1980 612 731; E-mail: firstname.lastname@example.org
Microbial Ecology in Health and Disease 2000; 12: 130–137
The mouth contains both distinct mucosal (lips, cheek, tongue, palate) and, uniquely, non-shedding surfaces (teeth) for microbial
colonisation. Each surface harbours a diverse but characteristic microflora, the composition and metabolism of which is dictated by the
biological properties of each site. The resident oral microflora develops in an orderly manner via waves of microbial succession (both
autogenic and allogenic). Pioneer species (many of which are sIgA protease-producing streptococci) colonise saliva-coated surfaces
through specific stereo-chemical, adhesin-receptor interactions. The metabolism of these organisms modifies local environmental
conditions, facilitating subsequent attachment and growth by later, and more fastidious, colonisers. Eventually, a stable biofilm
community develops, that plays an active role in (a) the normal development of the physiology of the habitat, and (b) the innate host
defences (colonisation resistance). Thus, when considering treatment options, clinicians should be aware of the need to maintain the
beneficial properties of the resident oral microflora. Key words: resident oral microflora, microbial succession, dental plaque, biofilm,
Far from having a passive relationship with the host,
recent research has confirmed earlier (and largely forgot-
ten) studies that demonstrated that the resident microflora
of animals and humans plays a positive role in the normal
development of the host. This resident microflora also
plays an active role in the maintenance of the healthy state
by contributing to the host defences and preventing coloni-
sation by exogenous microorganisms. Implicit in this state-
ment is that disease can be a consequence of disruption of
this resident microflora. A deeper understanding of the
relation between the host and its resident microflora may
lead to new strategies for the prevention of disease via the
active maintenance of a health-associated microflora.
It has been estimated that the human body is made up
of 1014cells of which only 10% are mammalian (1). The
remainder are the microorganisms that make up the resi-
dent microflora of the host. The composition of this
microflora varies at distinct habitats, but is relatively con-
sistent over time at each individual site among individuals.
The mouth is similar to other environmentally-exposed
sites in the body in having a characteristic (autochthonous)
and diverse microflora in health (Table I). Curiously, this
microflora consists of organisms with apparently contra-
dictory requirements; for example, facultative, micro-
aerophilic, capnophilic and obligately anaerobic species
(with either saccharolytic or asaccharolytic metabolic
lifestyles) are able to co-exist. Bacteria that are presently
unculturable can also be detected by molecular techniques
in samples from the mouth (2, 3).
The organisms making up the oral microflora are regu-
larly transferred to neighbouring habitats via saliva. Of
significance, however, only 29 out of ?500 microbial taxa
recovered from the mouth are cultivated from faecal sam-
ples, despite the continuous passage of these bacteria into
the gut (4), while oral bacteria do not establish on the skin
surface. Thus, the resident microflora is directly influenced
by the environmental conditions prevailing in a particular
habitat. Following on from this, the composition of the
resident oral microflora shows local variations in composi-
tion on distinct surfaces (e.g. tongue, cheek, teeth) due to
differences in key environmental conditions (see below).
The environmental factors that help define the mouth as a
microbial habitat will now be reviewed.
THE MOUTH AS A MICROBIAL HABITAT
As stated above, the mouth is not a homogeneous environ-
ment for microbial colonisation. Distinct habitats exist, for
example, the mucosal surfaces (such as the lips, cheek,
palate, and tongue) and teeth which, because of their
biological features, support the growth of a distinctive
microbial community (Table II).
The mouth is continuously bathed with saliva, and this
has a profound influence on the ecology of the mouth (5).
The mean pH of saliva is between pH 6.75–7.25, which
favours the growth of many microorganisms, and the ionic
composition of saliva promotes its buffering properties
and its ability to remineralise enamel. The major organic
constituents of saliva are proteins and glycoproteins, such
© Taylor & Francis 2000. ISSN 0891-060X
Microbial Ecology in Health and Disease
Role of the oral microflora in health
Principal bacterial genera found in the healthy oral ca?ity
Cocci Rods CocciRods
A number of other genera are isolated infrequently and/or in low
numbers in health, but increase markedly in disease (e.g. Acti-
(c) binding to the surface of bacteria to mask bacterial
antigens, thereby making the organism appear more host-
(d) aggregating microorganisms and thereby facilitating
their clearance from the mouth by swallowing; the flow of
saliva will also wash away weakly-adherent cells, and
(e) inhibiting the attachment and growth of some exoge-
nous microorganisms, via their role as components of the
The properties of some of the major habitats in the
mouth will change during the life of an individual. For
example, during the first few months of life the mouth
consists only of mucosal surfaces for microbial colonisa-
tion. Hard non-shedding surfaces appear with the develop-
ment of the primary dentition, providing a unique surface
in the body for microbial colonisation. The eruption of
teeth also generates another habitat, the gingival crevice
(where the tooth emerges from the gums), and an addi-
tional major nutrient source for that site (gingival crevicu-
lar fluid, GCF). Teeth allow the accumulation of large
masses of microorganisms (predominantly bacteria) and
their extracellular products (collectively, this is termed
dental plaque), especially at stagnant or retentive sites. In
contrast, elsewhere in the body, desquamation ensures that
the microbial load is relatively light on most mucosal
surfaces. In addition, ecological conditions within the
mouth will also be affected by the eruption and loss of
teeth, the insertion of prostheses such as dentures, and any
dental treatment including scaling, polishing and restora-
tions. Transient fluctuations in the stability of the oral
ecosystem may be induced by the frequency and type of
food ingested, periods of antibiotic therapy, and variations
in the composition and rate of flow of saliva. For example,
a side-effect of medication can be a reduction in saliva
flow, and this can predispose a site to caries. In old age,
the activity of the host defences can wane, and this might
explain the increased isolation of staphylococci and enter-
as amylase, mucin, immunoglobulins (mainly sIgA),
lysozyme, lactoferrin and sialoperoxidase. These influence
the oral microflora by:
(a) adsorbing to oral surfaces, especially teeth, to form a
conditioning film (the acquired pellicle) to which microor-
ganisms can attach. Adherence involves specific inter-
molecular interactions between adhesins on the surface of
the microorganism and receptors in the acquired pellicle.
Oral organisms are not distributed randomly but usually
display tissue tropisms, i.e. they selectively attach and
grow on certain surfaces (6, 7),
(b) acting as primary sources of nutrients (carbohydrates
and proteins) which foster the growth of the resident
microflora without inducing a damaging pH fall (8, 9),
Distinct microbial habitats within the healthy mouth
CommentsPredominant microbial groupsHabitat
Lips, palate, cheekstreptococci,
desquamation restricts biomass;
surfaces have distinct cell types;
Candida act as opportunistic pathogens; staphylococci may be present.
highly papillated surface—reservoir for anaerobesTonguestreptococci,
non-shedding surfaces—promote biofilm formation (dental plaque).
Distinct surfaces for colonisation (fissures, approximal, gingival crevice)
which support a characteristic flora due to their intrinsic biological prop-
erties. Teeth harbour the most diverse oral microbial communities.
P. D. Marsh
obacteria from the oral cavity of the elderly (10, 11). In
general, however, the composition of the microflora at a
site remains relatively constant over time (microbial
homeostasis) despite regular minor perturbations (12).
The health of the mouth is dependent on the integrity of
the mucosa (and enamel) which acts as a physical barrier
preventing penetration by microorganisms or antigens.
The host has a number of additional defence factors
present in oral secretions (saliva and GCF, see below)
which play an important role in maintaining the integrity
of these oral surfaces. As stated earlier, saliva contains
several anti-bacterial factors (5), including sIgA which can
reduce or prevent microbial colonisation of oral surfaces.
Antimicrobial peptides are present, including histidine-rich
polypeptides (histatins), and cystatins, which may control
the levels of yeasts, and a range of active proteins and
Serum components can reach the mouth via GCF (13).
The flow of GCF is relatively slow at healthy sites, but
increases during the inflammatory responses associated
with periodontal diseases. IgG is the predominant im-
munoglobulin in GCF; IgM and IgA are also present, as is
complement. GCF contains large numbers of viable neu-
trophils, as well as a minor number of lymphocytes and
monocytes. GCF can influence the ecology of the site by:
(a) removing weakly-adherent microbial cells,
(b) introducing additional components of the host de-
(c) acting as a novel source of nutrients for the resident
microorganisms. The growth of several fastidious obli-
gate anaerobes is dependent on haemin, which can be
derived from proteolysis of haemoglobin, haemopexin,
and transferrin, etc.
A brief summary of other environmental conditions
prevailing in the mouth is listed in Table III. Although
temperature remains relatively constant, it can increase in
the sub-gingival area during an inflammatory response if
plaque accumulates beyond levels compatible with health.
The local pH in dental plaque can fall rapidly to ca. pH
4.0–5.0 following the intake of fermentable dietary carbo-
hydrates, before returning to resting values (6.75–7.25).
Gradients in oxygen concentration and redox potential
develop over relatively short distances in plaque, which
enables the growth of large numbers of obligate anaerobes
recovered from the mouth (14).
DEVELOPMENT OF THE RESIDENT ORAL
The foetus in the womb is normally sterile. Acquisition of
the resident microflora of any surface depends on the
successive transmission of microorganisms to the site of
potential colonization. In the mouth, this is by passive
transfer from the mother, from organisms present in milk,
water (and eventually food), and the general environment,
although saliva is probably the main vehicle for transmis-
sion (15–18). Microorganisms such as lactobacilli and
candida may also be acquired transiently from the birth
canal. The mouth is highly selective for microorganisms
even during the first few days of life. Only a few of the
species common to the oral cavity of adults, and even less
of the large number of bacteria found in the environment,
are able to colonize the mouth of the newborn.
The first microorganisms to colonize are termed pioneer
species, and collectively they make up the pioneer micro-
bial community. In the mouth, the predominant pioneer
organisms are streptococci and in particular, S. sali?arius,
S. mitis and S. oralis (19, 20). Some pioneer streptococci
possess IgA1 protease activity (21), which may enable
producer and neighbouring organisms to evade the effects
of this key host defence factor that coats most oral sur-
faces. With time, the metabolic activity of the pioneer
community modifies the environment thereby providing
conditions suitable for colonization by a succession of
other populations. This may be by:
(a) changing the local Eh or pH,
(b) modifying or exposing new receptors on surfaces for
attachment (‘cryptitopes’; (22)), or
(c) generating novel nutrients, for example, as end prod-
ucts of metabolism (lactate, succinate, etc.) or as break-
Key en?ironmental factors affecting the growth of microorganisms in the healthy oral ca?ity (adapted from (14))
0–21% oxygen is abundant at mucosal surfaces; gradients exist in dental plaque enabling obligate
anaerobes to grow.
gradients exist in biofilms such as plaque; lowest value in gingival crevice.
pH plaque pH falls during dietary sugar metabolism. Sub-gingival plaque pH rises during inflamma-
peptides, proteins and glycoproteins in saliva and gingival crevicular fluid.
dietary sugars facilitate selection of acidogenic and acid-tolerating species in plaque; plaque pH
falls and demineralises enamel.
Role of the oral microflora in health
down products (peptides, haemin, etc.) which can be used
as primary nutrients by other organisms as part of a food
Microbial succession eventually leads to a stable situa-
tion with an increased species diversity (climax commu-
nity). The component species interact, and there is the
opportunity for a genuine division of labour; this may
involve chemical signalling among members of the com-
munity to co-ordinate gene expression (23, 24). This results
in participating organisms having a broader habitat range
(e.g. obligate anaerobes grow in an overtly aerobic habi-
tat), a more efficient metabolism (i.e. consortia are able to
more fully catabolise complex host macromolecules such
as mucin, against which the individual organisms have
only limited metabolic activity), and are more tolerant of
environmental stress and to antimicrobial action. A climax
community reflects a highly dynamic state; a change in the
environment can lead to a reaction from the microflora
resulting in an altered composition and metabolic activity,
and can also predispose a site to disease.
The oral cavity of the newborn contains only epithelial
surfaces for colonization. The pioneer populations consist
of mainly aerobic and facultatively anaerobic species. In a
study of 40 full-term babies, a range of streptococcal
species were recovered during the first three days of life,
and Streptococcus oralis, S. mitis biovar 1 and S. sali?arius
were the numerically dominant species (20). The diversity
of the pioneer oral community increases during the first
few months of life, and several species of Gram-negative
anaerobes appear. In a study of edentulous infants with a
mean age of 3 months (range: 1–7 months), Pre?otella
melaninogenica was the most frequently isolated anaerobe,
being recovered from 76% of infants (25). Other com-
monly isolated bacteria were Fusobacterium nucleatum,
Veillonella spp., and non-pigmented Pre?otella spp.. In
contrast, Capnocytophaga spp., P. loescheii and P. interme-
dia were recovered from 4–23% of infants, while E. corro-
dens and Wolinella succinogenes were only found in a
single mouth. The number of different anaerobes in the
same mouth varied from 0–7 species (25).
The same infants were followed longitudinally during
the eruption of the primary dentition (26). Gram-negative
anaerobic bacteria were isolated more commonly, and a
greater diversity of species were recovered from around the
gingival margin of the newly erupted teeth (mean age of
the infants=32 months) (26). Also, mutans streptococci
and S. sanguis appear in the mouth following tooth erup-
tion (27, 28). These findings confirm that a change in the
environment, such as the eruption of teeth, has a signifi-
cant ecological impact on the resident microflora.
Bacteriocin-typing and genotyping of strains have estab-
lished the vertical transmission of many oral bacteria (e.g.
S. sali?arius, mutans streptococci, Porphyromonas gingi-
?alis and Actinobacillus actinomycetemcomitans) from
mother to child (15–18). Generally, similar clonal types of
species are found within family groups, while different
patterns are usually observed between such groups. The
genotypes of mutans streptococci found in children ap-
peared identical to those of their mothers in 71% of 34
infant-mother pairs examined (29). No evidence of father-
infant (or father-mother) transmission of mutans strepto-
cocci was observed, although horizontal transmission of
some periodontal pathogens, such as P. gingi?alis, may
occur between spouses (17, 18).
During the first year of life, members of the genera
Neisseria, Veillonella, Actinomyces, Lactobacillus, and
Rothia are commonly isolated, particularly after tooth
eruption (30). Some of the genera (Porphyromonas and
Actinobacillus) associated with the aetiology of periodontal
disease have been cultivated from the plaque of infants
aged around 12 months, albeit infrequently and in low
numbers (31). This suggests that these diseases result from
a change to the balance of the components of the resident
microflora, presumably due to an alteration to the ecology
of the affected site.
The acquisition of some bacteria may occur optimally
only at certain ages. Studies of the transmission of mutans
streptococci to children have identified a specific ‘window
of infectivity’ at 19–31 months (median age: 26 months)
(32). This opens up the possibility of targeting preventive
strategies over this critical period to reduce the likelihood
of colonisation in the infant. Indeed, reducing the carriage
of mutans streptococci in mothers can reduce transmission
of these potentially cariogenic bacteria to their offspring,
and delay the onset of caries.
The development of a climax community at an oral site
can involve examples of both allogenic and autogenic
microbial succession. In allogenic succession, factors of
non-microbial origin are responsible for an altered pattern
of community development. For example, mutans strepto-
cocci and S. sanguis only appear in the mouth following
tooth eruption (19, 27, 28) or the insertion of artificial
devices such as acrylic obturators in children with cleft
palate. Community development is also influenced by mi-
crobial factors (autogenic succession). Examples include
(a) the lowering of the redox potential and consumption of
oxygen in plaque by pioneer species, thereby facilitating
colonisation by obligate anaerobes, (b) the development of
food chains and food webs, whereby the metabolic end
product of one organism becomes a primary nutrient
source for a second, and (c) the exposure of new receptors
on host macromolecules for bacterial adhesion by the
metabolism of the resident microflora (‘cryptitopes’; (22)).
EVASION OF THE HOST DEFENCES
One of the least understood phenomena is the ability of
the resident microflora to persist in the presence of a broad
range of specific and innate host defence factors. Some of
the proposed mechanisms that might explain this apparent
P. D. Marsh
Mechanisms by which oral bacteria may e?ade the host defences
oral bacteria bind host molecules to their
surface (‘stealth technology’).
bacterial epitopes resemble those of the
pioneer streptococci produce IgA1 protease;
other bacteria produce general proteases
that cleave other Ig’s and host defence
some species are immuno-modulatory, or
produce factors that instruct the host
defences to recognise them as ‘self’
(‘Commensal communism’, (35))
constant subtle antigenic changes; may
explain clonal turnover.
local conditions may be unsuitable for the
optimal functioning of the host defences.
adsorbed to clean tooth surfaces. The early colonisers
interact with, and adhere to, this conditioning film initially
via long range, non-specific physico-chemical interactions
followed by irreversible, short range stereo-chemical ad-
hesin-receptor interactions (6, 7, 37). Later colonisers bind
to already attached species by co-adhesion (38).
A range of habitats are associated with distinct tooth
surfaces, each of which are optimal for colonization and
growth by different microorganisms (Table V). Again, this
is due to the physical nature of the particular surface and
the resulting biological properties of the area. The areas
between adjacent teeth (approximal) and in the gingival
crevice afford protection from the normal removal forces,
such as mastication, salivary flow and oral hygiene prac-
tices. Both sites have a low redox potential (Eh) and, in
addition, the gingival crevice region is bathed in the nutri-
tionally-rich GCF, particularly during inflammation, and
so these areas are able to support a more diverse microbial
community including higher proportions of obligately
anaerobic bacteria. Pits and fissures of the biting (occlusal)
surfaces of the teeth also offer protection from some of
these environmental factors and, in addition, are also
susceptible to food impaction. Such protected areas are
associated with the largest microbial communities and, in
general, the most disease (see other chapters, this volume).
In contrast, smooth surfaces are more exposed to the
prevailing environmental conditions and, consequently, are
colonized by only limited numbers of organisms.
Plaque is an example of a biofilm (39, 40), and, while it
is found naturally in health, in disease there is a shift in the
composition of the plaque microflora away from the spe-
cies that predominate in health (see the other Chapters in
paradox in the context of the oral cavity are listed in Table
IV. Oral bacteria use salivary molecules as receptors when
they attach to a surface; the binding of such molecules will
also mask microbial antigens and make the cell appear
‘host-like’. Some clones of species such as S. mitis appear
to persist for long periods at a site whereas others appear
to be transient, and undergo replacement by distinct clones
(33, 34). Wide variations in the expression of carbohydrate
and protein antigens were found among different geno-
types of S. mitis biovar 1 within a family, suggesting that
this ‘clonal turnover’ might play a role as an ‘immune-eva-
sion’ mechanism for this species.
The resident oral microflora comprises a broad range of
gram-negative species (Table I) that contain potentially
inflammatory molecules such as LPS in their cell wall.
Although local inflammation is a hallmark of periodontal
diseases (see Liljemark, this volume), such a reaction by
the host is relatively uncommon. Recently, it has been
proposed that the resident microflora and mucosal tissues
exist in a balanced state due to active signalling between
the bacteria and the epithelial cells. This ‘cross-talk’ would
suppress inflammation and enable the microflora to grow
and enter a symbiotic relationship with the host (‘commen-
sal communism’, (35)), for example, the flora derives nutri-
ents from the host while also contributing to the host
defences (see later).
FORMATION OF DENTAL PLAQUE
Most studies have focussed on the development and prop-
erties of dental plaque, because of its role in caries and
periodontal diseases. The formation of dental plaque in-
volves an ordered colonization (microbial succession) by a
range of bacteria (36). Host and bacterial molecules are
The predominant bacteria found in dental plaque at three distinct
sites (adapted from (57))
BacteriumPercentage viable count (range)
saliva & diet,
saliva & GCF,
*An G+R, An G−R: obligately anaerobic Gram-positive and
anaerobic Gram-negative rods, respectively.
**+: detected occasionally.
Role of the oral microflora in health
Detrimental effects associated with the absence or suppression of the
resident microflora at a site. Adapted from (12)
thin intestinal walls
poorly developed villi
poor nutrient adsorption
reduced host defences
overgrowth by drug-resistant organisms
colonisation by exogenous species
1data based on germ-free animal studies.
2data based on the effects of antibiotics on the human microflora.
of pathogens such as Salmonella enteritidis from ca. 106to
as low as 10 cfu (48). In humans, the use of antibiotics is
associated with overgrowth in the gut by Clostridium
difficile leading to severe diarrhoea. In the mouth, antibi-
otic usage perturbs the resident microflora resulting in
overgrowth by drug-resistant, but previously minor, com-
ponents of the oral microflora (49), or colonisation by
exogenous and potentially pathogenic organisms, including
yeasts (1, 50).
These observations suggest that the resident microflora
of all sites in the body can influence the physiology of the
host and contribute to the innate host defences, by being a
barrier to exogenous species. This barrier effect is termed
‘colonisation resistance’ (51). The mechanisms involved in
colonisation resistance include competition for (a) nutri-
ents and (b) attachment sites. Natural selection has proba-
bly ensured that the most competitive and efficient strains
in terms of metabolism and colonisation are already mem-
bers of the oral resident microflora. In addition, colonisa-
tion resistance will be maintained by (c) the production of
inhibitory metabolites, and (d) the creation of unfa-
vourable environmental conditions for exogenous organ-
isms (48). Some strains of S. sali?arius strains produce a
bacteriocin (termed enocin or salivaricin) with activity
against Lancefield Group A streptococci (52). Bacteriocin
production by such strains in the pharynx may reduce or
prevent colonisation of the mouth by this pathogen. Simi-
larly, many oral bacteria produce other inhibitors such as
volatile fatty acids or hydrogen peroxide, or they change
local environmental conditions (e.g. pH or redox poten-
tial), which may exclude exogenous species and suppress
opportunistic pathogens. For example, the production of
hydrogen peroxide by members of the S. mitis-group can
suppress the growth in plaque of potential periodontal
pathogens, such as A. actinomycetemcomitans.
The arguments outlined above clearly demonstrate that the
resident oral microflora plays an active role in the normal
development of the mouth and in the maintenance of
health at a site. Clinicians need to be aware of the benefi-
cial properties of the resident microflora, and their treat-
ment strategies should be focussed on the control rather
than the elimination of these organisms, especially in
dental plaque. In the future, it may be feasible to target
treatment more specifically at particular ‘pathogens’ (e.g.
immunotherapy (53)), or more imaginative approaches
could be used to prevent disease. For example, it may be
possible to remove the environmental pressures that favour
the selection of the organisms associated with disease (54),
and ‘prebiotics’ (agents that encourage the growth of the
normal microflora) and ‘probiotics’ (the deliberate use of
organisms to restore colonisation resistance) may become
available. Such approaches are currently finding increasing
this volume; (41)). Bacteria growing on a surface as a
biofilm display an altered phenotype, and are also more
resistant to antimicrobial agents (42–44).
FUNCTIONS OF THE RESIDENT ORAL
MICROFLORA IN HEALTH
The presence of a resident microflora is not essential for
life, but is an important component if the host is to have
a normal existence. Information on the beneficial role of
the resident microbial flora has come from early studies
comparing the physiology of germ-free and conventional
laboratory animals, and from humans in whom the normal
flora has been disrupted by long-term administration of
antibiotics. Most studies have focused on the gut mi-
croflora but, in general, such findings are also relevant to
the mouth. The role played by the resident microflora is
one of the most poorly understood topics in microbiology,
and has been neglected for many years; further research
applying modern approaches to this area would be
The gut of germ-free animals is poorly developed, and
these animals may suffer from an enlarged caecum, poor
nutrient adsorption and from vitamin deficiencies; in addi-
tion, the development of the host defences is impaired
(Table VI) (45, 46). Also, components of the microflora
modify the differentiation programmes of intestinal epithe-
lial cell lineages at critical points during their morphogene-
sis. However, many of these anatomical and physiological
deficiencies can be reversed when these animals are
colonised by members of the resident microflora.
The presence of a resident microflora prevents disease
by reducing the chance of colonisation by exogenous spe-
cies. Thus, germ-free animals are highly susceptible to
disease, so that if they are introduced to a conventional
environment they suffer from diarrhoea and have a high
death rate (47). It has been determined experimentally that
the use of antibiotics can suppress the normal flora of the
digestive tract resulting in a reduction in the infective dose
P. D. Marsh
favour in those attempting to enhance the natural proper-
ties of the gut microflora (55). In this context, the outcome
of current clinical trials with bacteriocin-producing, non-
acidigenic but highly competitive strains of S. mutans
(replacement therapy) will be of great relevance (56).
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