The Microbiology of Primary Dental Caries

Jason M. Tanzer, D.M.D., Ph. D., Jill Livingston, M.S., and Angela M. Thompson, B.S.

(Dedication. To Paul H. Keyes and Robert J. Fitzgerald whose pioneering work on dental caries in
experimental animals framed the issues and set the stage for focused consideration of the role of
microorganisms in human dental caries, and to the many investigators who have subsequently devoted much of
their professional lives to the clarification of the microbial causes of caries in humans.)

This review was conducted to evaluate the implication of certain microorganisms in the
causation of human tooth decay. It examines the evidence concerning bacterial species
identified in both early and current literature to be involved in tooth decay, whether
originally from wild animal, experimental animal and/or human data. It also examines the
source of this putative infection of humans. Attention is focused on the mutans streptococci,
the sanguinis streptococci, other streptococci, the enterococci, the lactobacilli, and certain
actinomycetes, all of which are resident in the human mouth.

There is an immense literature on this topic. Systematic search using MEDLINE and
EMBASE, from 1966 to 2000, retrieved 2730 unique English language citations. This
retrieval was achieved by requiring that the full-length papers deal with isolation and
identification (at some level) of bacteria from human subjects in the context of caries.
Studies of so-called secondary or recurrent caries have been excluded from this review (due
to time and space limitations), as have studies done either wholly in vitro, in experimental
animals, or with so-called in situ caries models. The literature search thus conducted,
nonetheless, failed to retrieve a few papers either known to the reviewers or identified from
the bibliographies of articles retrieved by the searches. Of the papers chosen for review, all
but 39 could be read from our library’s collection or obtained from another library for
detailed study. Only in the case of the brief Background section of this paper are scholarly
review papers and conceptual advances from human or a few experimental animal studies
cited, for the sake of economy of presentation.

The Current Review, thus, deals with studies of the microbial causes and associations with
dental caries in humans only, relying upon cross-sectional, case-control, longitudinal, and
experimental/interventional studies. It addresses tooth decay in young children having only
deciduous (primary) dentition, older children and adolescents having mixed and permanent
(secondary) dentitions, adults and seniors, whose secondary dentition often presents varying
degrees of root exposure. As such, patients and experimental subjects with incipient enamel
lesions (white spots) and established cavitations (cavities) of the tooth crowns and root
surface lesions are considered. (The authors acknowledge that their review may have missed
potentially important information contained in papers that were not available or, under the
charge for this review, not appropriate for review. They also express sincere apologies to the
authors of many excellent studies whose description space does not allow, although those
papers were considered and are cited in the evidence tables.)

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Extensive evidence tables accompany this review and should be considered as the full list of
cited literature and its summarization/evaluation. The tables are constructed according to the
questions posed (below) and categorized according to the microorganisms which were the
focus of the literature search. Individual papers, while retrieved in the search for one or
another microorganism, also reference the simultaneous study of other implicated
microorganisms in that same publication.

Background

Earlier studies had characterized the biological behaviors of the most strongly caries-
implicated microorganisms. The essentials of those behaviors are summarized below as
background:

Mutans streptococci colonize the host only after the first teeth erupt, and their preferential
colonization site is the teeth (1) (2); they are highly localized on the surfaces of the teeth and
their abundance in the plaque is highest over initial lesions (3) (4); their level of colonization
within the plaque is increased by sucrose consumption (5) (6); they synthesize certain macro-
molecules from sucrose that foster their attachment to the teeth (7) (8); they are rapid
producers of acid from simple carbohydrates, including sucrose, and are tolerant to low pH
(9) (10) and they are essentially always recovered on cultivation of initial and established
carious lesion sites (11) (12) (13). Interest in them grew after the demonstration of their
potency in induction and progression of carious lesions in a variety of experimental animals ,
including mono-infected gnotobiotes (14) (15). Their virulence expression is strongly
associated with consumption of carbohydrates, especially sucrose (16) (17). However, caries
does not occur in germ-free animals, no matter what their genetic background or their diet; it
is an infection.

Lactobacilli do not avidly colonize the teeth and may be transiently found in the mouth
before the teeth erupt; they preferentially colonize the dorsum of the tongue and are carried
into saliva by the sloughing of the tongue’s epithelium (18); their numbers in saliva appear to
be a reflection of the consumption of simple carbohydrates by the host (6) (19); they, too, are
highly acidogenic from carbohydrates and are acid tolerant (20). They are often cultured
from established carious lesions (21). Some lactobacilli are cariogenic in experimental
animals and their cariogenicity is dependent upon consumption of carbohydrate rich diets of
animals (22).

Non-mutans streptococci of several types, including the sanguinis (formerly sanguis) group
of organisms, and S. salivarius, are extremely abundant in the mouth; some are tooth surface
colonizers, some mucosal colonizers. Some are quite acidogenic from carbohydrates and are
acid tolerant (23) (9) (24). Less evidence exists of their virulence in experimental animals
than either the mutans streptococci or the lactobacilli.

Enterococci were the first bacteria shown experimentally to induce caries in gnotobiotic
animals (25). While carbohydrate users, acidogenic, and acid tolerant, they are not
frequently abundant in the human oral cavity (23) (9) (24).

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Actinomycetes are abundant in the human mouth and induce root surface caries in hamsters
and gnotobiotic rats (26). They are also carbohydrate users, but are not powerfully
acidogenic or acid tolerant.

Current Review

I. The association of specific bacteria with tooth decay (Table 1)

Question 1:

Are persons who have high levels of specific oral microorganisms at an increased or
decreased risk for developing carious lesions compared to persons who do not have high
levels of those same microorganisms? (The question, developed in PICO [population
interventions comparisons and outcomes] format, addresses the association of specific
bacteria with tooth decay.)

The search strategy developed to answer this question contained two primary concepts:
1) oral microorganisms and 2) carious lesions. For the concept of oral microorganisms,
five separate hedges of terms were created, one for each of the following groups of
bacteria -- mutans streptococci, lactobacilli, sanguinis (formerly sanguis) and other non-
mutans streptococci, enterococci, and actinomycetes. A sixth, very broad hedge, was
created to capture the concept of bacteria in general; the purpose of it was to retrieve
pertinent articles indexed under the broad terms--bacteria, streptococcus, or
enterococcus--but not under a specific microorganism.
The concept of carious lesions was represented in the searches by the caries hedge
developed for common use by all reviewers in this systematic review. A dental plaque
enhancement was added to the caries hedge to account for instances when pertinent
articles were indexed under the concept of dental plaque rather than dental caries or
carious lesions.
The oral microorganism and carious lesion hedges, as well as all other hedges used in this
review, were created with respect to possible term and conceptual variants, past
taxonomical references, misspellings, and indexing omissions and oversights.
The search was limited to human subjects and English language articles only.

Table 1. Summary of Search Retrieval on The Association of Specific Microorganisms and Dental Caries

Bacterial Group Total Total Interventional Longitudinal/ Case- Cross

Retrieved Selected Retrospective Control Sectional
Mutans 854 189 25 59 20 85
streptococci
Sanguinis/other 1245 16 1 2 2 11
streptococci
Enterococci 253 3 0 0 0 3
Lactobacilli 657 144 9 40 20 75
Actinomycetes 700 27 1 3 3 20

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The mutans streptococci

Randomized clinical trials

Twenty-five interventional studies which monitor the putative cariogenic flora and record
effects on caries scores are found in the literature of human caries. Several of these applied
extremely complex strategies [e.g. (27)] -- some focused on mitigation of the solubility of the
teeth with fluorides; some on repair or sealing of the teeth; some on diet management and/or
use of sugar substitutes and, thus, indirectly on changing the implicated tooth surface flora;
and some directly on the flora by mechanical plaque control and/or use of antiseptic agents.

Because the questions for the present review are more straight-forward (viz. what are the
bacterial determinants of caries and what is known of the transmission of those bacteria),
such multi-strategic studies confound interpretations of antibacterial effects with anti-tooth
demineralization effects. It is understandable that investigators wish to accept this problem,
because of the ethical need to offer patients at high risk the perceived best available
anticaries strategies. Nonetheless, multi-strategy approaches to experimental interventions
set a very high threshold for detection of effects of interventions on the flora and attribution
of anti-caries responses to them. Some notable studies are less confounded, however.

Partial suppression of mutans streptococci by topical chlorhexidine use and dietary

counseling in randomized to treatment (or control) Swedish children (28) inhibits mutans
streptococcal recoveries and carious lesion development during 3 years, while lactobacillus
titers in saliva are not detectably affected.

Study of primiparous mothers with 3-8 month-old infants in a Swedish community,

alternately assigned to treatment or control groups, was aimed at reduction of mutans
streptococcal salivary levels by sucrose avoidance counseling, professional tooth cleaning
(and topical fluoride application), oral hygiene instruction, and excavation of large carious
lesions if present, and, if test mothers had salivary mutans streptococcal levels that exceeded
a pre-set threshold, by treatment with topical chlorhexidine. This strategy increased the time
to colonization by mutans streptococci of their young children, time to caries experience of
those children, and the severity of caries experience of those children (29). There was no
significant difference in titers of salivary lactobacilli. Preventive strategies were
discontinued when children had become colonized. The study ran until children were 36
months old. Four years later (30), with the same children now 7 yr old, treated mothers had
lower mutans streptococci and lactobacilli than control mothers, and far lower percentages of
children of treated mothers carried mutans streptococci compared with children of control
mothers. The children of test mothers who were carriers also had lower levels of mutans
streptococci than those of the mutans carrier control mothers. 23% of children of test
mothers were caries free, compared to 9% of the children of control mothers, and total group
caries experience for test and control children were 5.2 vs 8.6 def, respectively.

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A similar strategy was used to treat 50-60 yr old Swedish patients of private dentists (31).
Two randomized groups of high and low risk patients (defined by salivary mutans, salivary
flow rate, and salivary buffer capacity) were assigned test protocol or served as controls who
were given standard care as deemed appropriate by their dentists. At year’s end, the treated
high risk group had lower caries increments and lower mutans and lactobacillus titers than
high risk controls, but there was no difference between the two low risk groups. The
intervention was discontinued. Four years later there was no difference in microbiological
parameters or caries increment between the former treated and untreated high risk and low
risk groups, and the one year differential benefits of the test intercession had been lost.

A 3 year study (32) of initially 12 yr old Swedish children, using an intervention of

chlorhexidine-impregnated dental floss treatment of approximal surfaces compared with
placebo-impregnated floss, and with no floss treatment resulted in about 50% reduction of
new DFS of the chlorhexidine-floss compared with the placebo-floss group, and about a 60%
reduction compared with the no floss group. Chlorhexidine impregnated floss effects were
about 42% better than placebo-floss. Salivary monitoring of bacteriology (rather than
approximal plaque monitoring) evidenced no differences among the groups, as could have
been expected.

A 3 year intensive program (33) focused on personalized education to avoid sucrose,

excavation of cavities, fluoride varnish application, professional tooth cleaning and oral
hygiene instruction. All study participants were randomized by school class and had group
instruction on sugar avoidance, tooth brushing, fluoride toothpaste use, and were provided
tooth brushes. The personalized program resulted in about a 6-fold decline of new DFS in
10-12 yr old Polish children and, after 3 years, significant reductions of mutans and
lactobacillus salivary counts.

A 2 year randomized 4 group study of 13 year old Swedish children (34) compared
supervised chlorhexidine gel treatment to fluoride varnish, topical FeAlF professional
application, and to untreated controls status with no intercession. The antibacterial treatment
resulted in about a 50% reduction of new DFS when compared with the untreated controls
and lesser, but still substantial and significant, DFS reductions compared with the fluoride
treated groups. There was a correlated reduction of salivary mutans streptococci in the
chlorhexidine group.

Finnish 10-12 year old children were randomized to either high content xylitol gum use or
not, during a first experimental phase (35). When two years later the controls were randomly
recruited for evaluation, some had begun the voluntary use of xylitol gum, i.e. a self imposed
cross-over. The approximal plaque mutans levels were lower in the xylitol users and the
continuous users of xylitol gum had lower decay scores 6 years after the beginning of their
xylitol use than did non-users. Mutans streptococci were lower at approximal sites that were
clinically and radiographically sound than at decayed sites.

The use of a xylitol chewing gum by Finnish mothers (36) (37) until their children were 3
years old was recently reported to inhibit the mutans streptococcal colonization of their

5
children and reduce the caries experience of those children during a 5 year period of
observation. Mothers were randomized to either xylitol gum use, chlorhexidine varnish, or
fluoride varnish applications. The children did not use the gum or receive varnish treatments.
The probability of being caries free was 70% for non-mutans-colonized children compared to
about 25% for mutans colonized ones at 5 years of age and the group mean dmf score for the
xylitol intercession cohort was 0.83, while those for the chlorhexidine and fluoride varnish
groups were 3.22 and 2.87, respectively.

Longitudinal and case-control studies

Seventy nine longitudinal (prospective and retrospective) and case control studies indicate an
important role of mutans streptococci in caries. They examined the relationship between
salivary titers or plaque relative abundance of mutans streptococci (and often simultaneously
quantified other implicated bacteria, especially lactobacilli, actinomycetes, and sanguinis
streptococci) as well as the inception, prevalence or incidence of carious lesions of various
surfaces of crowns or roots of teeth. Many studies have used randomized subjects, some
being dental or medical patients; some subjects were almost totally naïve dentally. Some
studies have used population samples and some compared cohorts of high or low caries
experience, fluoridated or non-fluoridated communities, diverse racial/ethnic groups, diverse
socioeconomic statuses, diverse methods to pay for dental health care, ambulatory and non-
ambulatory health status, and, of course, diverse ages. The longitudinal, case-control, and
cross sectional (not discussed here) studies come from all continents except Antarctica. A
few illustrative of the diverse study populations are cited here [(38) (39) (40) (41) (42) (43)
(44) (45) (46) (47) (48) (49) (50) (51) (52) (53) (54) (55) (19) (56) (57) (58) (59) (60) (61)
(62) (63) (64) (65)] and provide, overall, a remarkably consistent picture.

These (and cross-sectional) studies, with few exceptions, support a strong positive statistical
association of mutans streptococci with inception or incidence of carious lesions. They often
report concomitant positive associations with lactobacilli, especially if saliva, rather than
discrete plaque samples, had been monitored. When studied, they sometimes report negative
associations of sanguinis streptococci with mutans streptococci and with lesions. Some
suggest that S. sobrinus (the less common of the mutans streptococci, the more common one
being S. mutans) are favored in their ability to colonize the teeth by prior colonization of S.
mutans. There is suggestion of an association of S. sobrinus and lactobacilli.

While mutans streptococci can be found in the mouths of infants only after the teeth erupt,
they colonize the mouth much earlier when obturators are placed for cleft palate
management, again supporting the notion that mutans streptococci require solid non-
shedding surfaces as their preferred colonization site (66).

Often these studies (randomized clinical trial, longitudinal, and cross-sectional) gather data
on other variables of interest – socioeconomic status, sucrose consumption (usually as food
types or patterns of consumption), fluoride exposure, oral hygiene status, breast feeding or
close personal contact between mothers and their children and, especially, initial or baseline

6
caries status. Some studies ask the clinical examiners to predict the decay experience of the
study participants depending on the examiners’ beliefs.

Several of these studies focused on a related question, viz. the prediction of carious lesion
increments as a function of the sum total of many of the variables of interest to cariologists
and caries epidemiologists, rather than on the microbiological variables targeted for this
review. In such studies when predictive values were estimated and when multiple regression
models included other caries-associated variables (such as candy or soft drink consumption,
oral hygiene, SES and, especially, prior numbers of lesions), the amount of variance
explained by the bacteria of interest became predictably smaller. Prediction of the dependent
variable, caries score, by inclusion of the baseline caries score as an independent variable
appears inherently tautological in the context of explaining the causation of the disease (and
arguably a post hoc, ergo propter hoc problem).

Discernment of microbial etiology from several longitudinal (and cross-sectional) studies

was probably blunted by using salivary (or pooled plaque) monitoring of mutans streptococci
as a surrogate for monitoring small samples of plaque in areas of high caries risk, as the
knowledge of the biology of the mutans streptococci and expected locations of carious
lesions would have seemed to dictate.

Lactobacilli

Interventional trials

The concerns for confounding and ambiguity of interpretations in interventional clinical trials
stated above for the mutans streptococci are applicable to the lactobacilli as well. Several of
the randomized clinical trials which yielded data concerning the mutans streptococci also
evaluated changes in the lactobacilli. Generally they resulted in inconsistent evidence that
inception of carious lesions in children or adults were associated with lactobacillus titer
increases in saliva [ex. (67) (30) (31) (33) (34)].

Longitudinal and case-control studies

Longitudinal and case-control studies were perhaps more informative. Lactobacilli are late
colonizers of the mouth (68) (18) (1) (57) (4). Lactobacilli are recovered from carious
lesions, but they are later colonizers of those lesions than the mutans streptococci (43) (51)
(19). Some data suggest that they are favored in their ability to colonize by pre-existing
colonization by the mutans streptococci, especially S. sobrinus. These data thus indicate that
lactobacilli are not requisite for the development of lesions. Nonetheless, they may potently
contribute to the demineralization of the teeth once lesions are established on either crowns
or roots (43) (69) (70) (71) (72) (63) (73) (74). Little information is available concerning the
species of lactobacilli that colonize the human tongue and teeth. The many pertinent cross-
sectional studies will, similarly, not be described here, but their descriptions can be found in
the evidence tables.

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Non-mutans streptococci

Essentially no data support a causative role of sanguinis streptococci or S. salivarius in

human caries. In fact some data suggest an inverse relationship of the abundance of
sanguinis streptococci and the mutans streptococci, and that the sanguinis streptococci are
inversely related to lesion development [ex. (38) (40) (75) (76)].

Enterococci

No human data support a significant role of enterococci in the development of human carious
lesions or in their prevalence in the human mouth.

Actinomycetes

Actinomycetes are prevalent in the human mouth and are frequently found in association
with both carious and sound root surfaces, as well as sound crown surfaces. Evidence of
their role in root surface carious lesion induction, from interventional, longitudinal, case-
control and cross-sectional data, are variable and inconclusive. In fact, they sometimes
suggest actinomycetes are more reflective of non-cariogenic than cariogenic status, by
contrast with the mutans streptococci and the lactobacilli.

The source of infection by the cariogenic bacteria (Table 2)

Question 2:

Are persons who have undetectable levels of cariogenic flora more likely to acquire
them from persons who have high levels of cariogenic flora than from persons who have
low levels of cariogenic flora? (The question is developed in PICO format.)

The search strategy developed to answer this question contained two primary concepts:
1) oral microorganisms and 2) disease transmission.
For the concept of oral microorganisms, five separate hedges of terms were created, one
for each of the following groups of bacteria -- mutans streptococci, lactobacilli, sanguinis
and other non-mutans streptococci, enterococci, and actinomycetes. A sixth, very broad
hedge, was created to capture the concept of bacteria in general; the purpose of this was
to retrieve pertinent articles indexed under the broad terms--bacteria, streptococcus, or
enterococcus--but not under a specific microorganism.
The hedge for disease transmission took into account such variant concepts as infection;
transmission; communicable diseases; mother(s), and persons likely to transmit infection.
The search was limited to human subjects and English language articles only.

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 Table 2. Summary of Search Retrieval on The Transmission of Bacterial Species Implicated in Dental
Caries

Bacterial Group Total Total Molecular and Interventional Longitudinal/ Cross

Retrieved Selected genetic tracing: Case-Control Sectional
bacteriocin/mutacin/
phage
typing/endonuclease
mapping/ribotyping
Mutans 122 40 17 8 13 1
streptococci
Sanguinis/other 772 1 0 0 1 0
streptococci
Enterococci 129 0 - - - -
Lactobacilli 104 7 0 4 3 0
Actinomycetes 114 0 - - - -

Just as modern molecular and genetic methods are now widely used in forensic science, they
are now used to trace the spread of infection. They provide perhaps the strongest evidence of
the source of transmission of infection in the case of dental caries. That evidence will be
briefly abstracted here. Nonetheless, other evidence of the source of transmission of the
bacteria etiologically involved in caries, from experimental and longitudinal studies, is
consistent with the even more compelling genetic evidence. The convincing data on the
source of infection by cariogenic bacteria almost entirely pertain to the mutans streptococci.

Study of the mutans streptococci isolated from children and their parents/siblings/caretakers
by bacteriocin typing, phage typing, mutacin typing, endonuclease DNA mapping and
ribotyping establish that these bacteria are transmitted to humans early in their lives, after the
first teeth erupt, and that they originate mainly from their mothers, i.e. vertical, matrilineal
transmission [(77) (78) (79) (80) (81) (82) (83) (84) (85)]. Only two reports suggest
significant patrilineal transmission. While it is common for children to share more than one
genotype or bacteriocin type of mutans streptococci with their mothers, failure to detect all of
the types longitudinally among mother/child pairs suggests that some genotypes may be lost
with time. New genotypes not detected in mothers have also been reported to colonize
children during longitudinal studies, suggesting that additional and extra-familial
transmission sometimes occurs, perhaps from other caretakers.

Longitudinal study of children led to the proposal of a “window of infectivity” by mutans

streptococci (86), but that concept does not appear presently well-supported. Children
become colonized both before and after that “window” period (87) (66) (88) (89)]. Also, as
reported in essentially all of the studies of adults (cited above), virtually all dentate adults
appear to some degree colonized by mutans streptococci. Hence, there are likely to be other
events of transmission or, alternatively, the methods historically used to cultivate the mutans
streptococci may be of insufficient sensitivity to detect transmission which had in fact
occurred.

9
Interventional studies of transmission are clearly inhibited by the ethical impossibility of
exchanging children shortly after birth among mothers for foster-rearing. Nonetheless,
controlled experiments aimed at reducing the salivary levels of mutans streptococci and, thus,
altering the probability of transmission of mutans streptococci from mothers to their children
strongly support the concept that mother is the usual source of transmission of these bacteria
to her child (30) (90) (36).

There are few data on the source of transmission of lactobacilli to children. Despite the use
of very specific selective media for the cultivation of oral lactobacilli, speciation of
lactobacilli has been laborious and usually not done in a cariological context. As for the
mutans streptococci, speciation studies would not seem useful for tracing the transmission of
the oral lactobacilli; molecular/genetic marker tracing would seem more promising. Also,
literature search does not reveal studies of the genetics of the lactobacilli in the mouth,
vaginal, or GI tract of mothers and their children in the context of dental caries. While
lactobacilli can be found in the mouths of infants, they appear to be transient and not a
common feature of the oral cavity until after teeth erupt or after obturators are placed for cleft
palate management.

There is little information on the source of colonization of the mouth by sanguinis group
streptococci, enterococci, and actinomycetes. S. salivarius is long known to colonize the
mouth usually within a day of birth, suggesting mother’s oral or vaginal flora as the source.

Problems of methods and literature interpretation

Many questions inevitably arise concerning the methods and data handling in this area. Of
them, three perhaps warrant special note.

Benefits and shortcomings of salivary and plaque monitoring of the cariogenic flora.
Several studies have demonstrated, on a population basis, that the level (titer) of mutans
streptococci per ml saliva is a reflection of their levels on the teeth. Thus, saliva, rather than
dental plaque (the location of colonization by mutans streptococci), has been used as a
surrogate for plaque monitoring. Use of this strategy was attractive for the study of
potentially uncooperative young children. It also required virtually no equipment or thought
about where mutans streptococci colonize the teeth, compared with the careful taking of
small, localized plaque samples. Such sampling was also attractive because of the
assumption that saliva was the likely vehicle for transmission of mutans streptococci among
humans, an assumption shown subsequently to have strong support. To a probably
significant extent, the use of salivary monitoring systems was also driven by the availability
of commercial kits designed for salivary mutans monitoring. The method assumes that all
tooth sites are equally colonized and available for sampling.

Mutans streptococcal levels in mastication-stimulated saliva reflect something akin to a

pooled, averaged plaque, sampled from those tooth surfaces from which plaque is most likely
to be dislodged. Collection of stimulated saliva is commonly effected by chewing a piece of
paraffin, thereby partially disrupting the plaque, on the exposed-to-the-paraffin tooth

10
surfaces. Such saliva samples can be expected to bias data against the sampling of plaque
located in the fissures of the teeth, below the approximating contact areas, below the
maximal curvature of buccal and lingual surfaces of teeth, and on the root surfaces, viz. all of
the surfaces of the teeth most likely to decay and those most heavily colonized by mutans
streptococci. They would bias for the disproportionate sampling of plaque located on cusp
inclines and about one half to two thirds of the buccal and lingual surfaces of the teeth (viz.
the least likely surfaces of the teeth to decay), as can readily be observed by viewing the
impressions of the teeth made in chewed softened paraffin or chewing gum. Hence, the
sampling method fosters underestimation of the mutans streptococcal colonization levels on
the teeth and assumes that the teeth are uniformly blanketed with them. [As expected, if
prostheses that have not been disinfected are left in the mouth during chewing of paraffin,
saliva levels of prosthesis-dislodged plaque organisms are increased (see evidence table)].
The method also either assumes that patients would not brush their teeth before saliva
sampling or that brushing and, thus, plaque amount reduction before sampling, would have
no effect on the numbers of plaque bacteria available for dislodgment into saliva. It
furthermore assumes that there would be no effect of eating and brushing before sampling,
despite data (91) to the contrary. Most clinical studies have not standardized saliva
collection conditions, likely increasing variance of data.

It is, nonetheless, clear that for naïve subjects, especially young ones with all of their teeth,
there is a strong correlation between mutans streptococcal numbers/ml saliva and the
percentage of mutans streptococci in pooled (accessible) dental plaque. Saliva sampling has
served well in this context. Such correlations have notably been demonstrated with large
numbers of study participants, i.e. with populations. Salivary sampling is especially
convenient for field studies. It is less established, however, as evidence of individual patient
status, risk, results of treatment, or prognosis for individual management.

Salivary sampling has been done by several methods: the collection of pooled saliva from the
floor of the mouth with a cotton swab, with care not to mechanically disrupt the plaque; the
pressing of a stick or tongue blade, often called a “spatula”, against the dorsum of the tongue,
to obtain a saliva sample (there is no evidence that mutans streptococci have a differential
affinity for the tongue epithelium); the drooling of collected saliva, without stimulation, into
a collection vessel. All of these are usually referred to as “unstimulated” saliva samples. For
stimulated salivary samples, subjects are commonly supplied a masticatory stimulus, usually
a standardized piece of paraffin wax that at mouth temperature is easily chewed and serves to
dislodge some of the plaque from the accessible areas of the teeth. Saliva is then usually spat
into a collection vessel.

Salivary samples are, by various techniques, cultivated on so-called selective (actually,

differential) media for growth of mutans streptococci (or lactobacilli). Some kits have been
marketed to facilitate this. Alternatively, samples may be added to viability preserving
media (most commonly VMGII or RTF) or simply chilled or frozen for transport to a
laboratory where they are disaggregated and diluted to avoid confluent colony growth on
differential media. After incubation, some workers view these agar surfaces with the naked
eye, using manufacturer-supplied reference standards, with the assumption that all of the

11
mutans streptococci (or lactobacilli) in the sample, and only they, grow into visible colonies.
Other studies more carefully confirm that only mutans streptococci (or lactobacilli) are being
enumerated, but most of these do not exclude false negatives. That false negatives occur
commonly using the most popular of these culture media, and perhaps to various degrees
with all analogous culture media, is abundantly documented (not reviewed in this paper).
Results are reported in colony forming unit count/ml of saliva. For example, 1 x 106 cfu/ml,
is generally accepted as a high count for mutans streptococci. It should be recognized that if
non-selective media were used, total recoveries would be between 108 and 109 cfu/ml. Thus,
at most, mutans streptococci constitute less than 1% of the bacteria in saliva.

Plaque samples, by contrast, are collected either by scraping the surfaces of the dentition to
harvest all accessible plaque, thus pooling it and doubtless underestimating the levels of
colonization of the highly localized mutans streptococci (92) (93) (3) (94), or by taking tiny
amounts of plaque at selected areas of the teeth. Samples are plated usually on the same
differential media as used for salivary sampling, but are also plated on a non-selective
medium such as trypticase soy blood agar. Data by these methods are reported usually as the
% of total recoverable colony forming units which are mutans streptococci (or lactobacilli).
Such data are expected to be relatively unaffected by time-of-day, tooth brushing, and eating
artifacts; there is no evidence that any of these conditions differentially dislodge or fail to
dislodge bacterial components of the dental plaque. Plaque sampling by comparison with
salivary sampling requires good lighting and trained personnel to take samples, cultivate
them, and microscopically view plates for identification of characteristic colonial
morphologies, and at least semi-quantitate them. By such methods, it is not unusual to
recover more than 50% of the total flora over white spot lesions as mutans streptococci.

Lactobacillus monitoring using saliva has less uncertainty of interpretation than saliva
monitoring for mutans streptococci, probably because lactobacilli are mucosal colonizers, not
tooth colonizers (evidence table). Mucosal cells slough into the saliva, carrying their
adherent bacterial burden of lactobacilli (especially from the tongue). When lactobacilli are
recovered from the surfaces of teeth by plaque sampling, lactobacillus colonies may
substantially reflect salivary contamination of that tooth surface. Lactobacilli do not colonize
the mouth with stability until the caries process is underway (evidence tables) and acidogenic
conditions associated with the consumption of abundant carbohydrate are established.
Nonetheless, these bacteria may contribute significantly to lesion formation, especially in the
context of their advancement.

The medium most used for the selective enumeration of lactobacilli does not provide
speciation, and we know of no data on the possible loss of oral lactobacilli on it, thus leaving
open the possibility of significant false negative recoveries, both qualitatively with regard to
specific lactobacilli and quantitatively. Thus, a considerable information gap may exist re
the significance of lactobacilli in caries.

The role of sugar(s) in decay as it relates to the presumptive cariogenic flora.

Time did not allow the systematic review of the role of various sugars and sugar substitutes
in the context of the status of infection or colonization by the mutans streptococci and the

12
lactobacilli. The evidence tables for Question 1, however, abound with data to indicate that
for caries-active patients, sugar consumption, especially that of sucrose, may be very potently
cariogenic and is associated with the ecological emergence of the mutans streptococci and of
the lactobacilli, as was indicated by the old literature (reviewed by others). Surely, detection
of sucrose’s or other fermentable carbohydrate's effects on lesion formation may be
dampened in the setting of abundant exposure to fluorides, and the effect may consequently
be of less moment for some citizens of Western societies. Much of the US and most of the
world, however, do not have abundant exposure to fluorides. Some of those populations,
especially in the economically emerging nations, are increasingly exposed to sucrose (not
reviewed here). Cross-sectional analysis of impact on caries of various sugars is likely to be
less sharp in detecting their significance than randomized experimental studies that
manipulate sugar use. (Indeed, the most powerful interventional strategies described in the
present review of the role of bacteria in caries involve sucrose restriction or substitution.)
Similarly, analysis of sugar(s) use without regard to the pattern, frequency, duration and
quantity of exposure, or estimation of the time of exposure of the high risk areas of the teeth
to specific fermentable carbohydrate foods may mitigate detection of powerful effects on the
cariogenic flora and on the development of lesions. Two human genetic diseases that
mandate that patients consume essentially no sucrose, hereditary fructose intolerance and
intestinal sucrase deficiency, make clear its great impact on both colonization of the dentition
by cariogenic bacteria and development of lesions (95) (96).

Modeling strategies to predict lesion score increments, as distinct from estimation of the
impact of specific bacterial types in caries.
A number of studies understandably have sought to characterize caries risk by evaluation of
independent variables such as implicated bacteria, socioeconomic status, sugar intake,
specific food intakes, oral hygiene, fluoride exposure, etc. and existence of carious lesions,
whether cavitated or initial (white spot). Not surprisingly, the inclusion of the existence of
the disease’s result (carious lesions) as an independent variable in the multifactorial or
predictive analysis of the dependent variable, carious lesion score increment, has resulted in
the conclusion that the biggest predictor of lesions was preexisting caries lesions. Generally,
the more variables considered in regression equations, the smaller the impact of any one of
them. It would not seem that such an analysis is substantially different from using the
presence of gangrenous toes in diabetic patients as a predictor of occurrence of more
gangrenous toes. Use of carious lesions to predict that the patient will get carious lesions
appears tautological, true on its face.

Perhaps more appropriate issues would be either 1) the prediction of who among populations
of children (or adults) may develop carious lesions when they are essentially free of them, so
that disease preventive strategies may target those individuals and/or 2) the prediction of
management outcomes for people with existing lesions from the evaluation of
microbiological, dietary, fluoride, and/or salivary conditions. It is arguably dangerous and
wasteful to presume that real individual dental patients with carious lesions are at high risk
for more, when clinicians know that many carious lesions may have been formed years
previously and may not have advanced. For the clinician or dental educator to think

13
otherwise is to commit all patients with a history of decay (dmfs or DMFS) to endless
restorative therapies, to exalt restorative procedures over preventive ones.

Conclusions of Review

Evidence from the current review strongly supports a central role of the mutans group of
streptococci in the initiation of caries on the smooth surfaces and fissures of the crowns of
the teeth of adults and children, and suggest a potent etiologic role of them in the induction of
root surface caries also. Lactobacilli are also implicated as important contributory bacteria in
tooth decay, but their role in induction of lesions is not well supported. Evidence that other
streptococci, enterococci, or actinomycetes are prominent etiological agents of dental caries
in humans is equivocal at best. The mutans streptococci are spread vertically in the
population, mostly but not exclusively, from mothers to their children. These findings
suggest strategies for improvement of the dental health of both children and adults in the US
and in other countries.

Future Directions for Microbiological Clinical Caries Research

It would seem overdue that facile methods for the molecular detection of colonization of
tooth sites by mutans streptococci be established and validated. These methods should be
used to indicate individual patient and individual tooth site risk for lesions and, ideally,
should be executable in the dental office. They must be reimbursed by third-parties. They
should save enormous amounts presently expended for repeated restorative care.

Such development would also make more feasible the study of outcomes of individual
patient management, the compliance of patients with dietary advice, the assessment of
effects of antimicrobial treatments, the establishment of prognosis for further decay, and the
estimation of the probability of failure of restorative treatment. Such development and issue
focus would move the practice of restorative dentistry out of a fundamentally reparative
mode into a diagnosis-based, infection control-oriented, tooth surface-protective, and
selectively-restorative mode.

There is need for the development of more potent topical antimicrobial agents that target the
suppression of the mutans streptococci by topical treatment of the teeth. Although
chlorhexidine was once seen as a promising agent of this sort, and it has shown considerable
efficacy, its effects have been less than ideal and its potency at presently allowed
concentrations is marginal. There is considerable literature (not reviewed here) to suggest
other agents and avenues for such antibacterial therapies.

The reported effects of xylitol confections in the reduction of decay increments are notable.
Public health promotion of strategies to reduce the probability or level of colonization of
mothers and, perhaps, other caregivers, by mutans streptococci, whether based on use of
xylitol, restriction of certain sugars, excavation and filling of carious lesions, antiseptic
treatment, and/or other strategies are of great interest. The literature indicates that these
strategies can effect delay of cariogenic microbial infection of children and consequent

14
mitigation of their caries experience. It would seem appropriate for practitioners to use such
strategies to protect the dental health of children now, and for health research funding
agencies/industry to conduct large scale clinical trials to assess population dental health
improvement of children by treatment of their mothers and caretakers. Other caretakers
should include grandmothers and daycare personnel who increasingly participate in the
rearing of children in this time of growing parental obligations to the workplace.

Special attention should be given to secondary decay occurring at the junction of restorative
material and the enamel cavosurface. Abundant data (reviewed by others) indicate that a
very large part of practitioner time and patient money is spent re-filling previously filled
teeth. Although there is a literature on the bacterial correlates of secondary decay, it is
limited. The issue warrants substantial funding for longitudinal and interventional clinical
trials.

With the aging of Western societies and the increasing use of medications which compromise
salivary function (reviewed by others) tooth decay should be increasingly seen as not a
pediatric/adolescent disease but also as a disease of adults and the elderly, as demonstrated
by national survey data. Special interventional strategies accordingly need to be developed
to care for the aging.

Lastly, it is paramount that the term “dental caries” not be equated with “cavities” by dentists
and dental educators. The lesion is not the disease, but the effect of the disease. The disease
does not occur without infection by cariogenic bacteria. To prevent, detect, and manage
caries throughout life one must not be restrictively focused on the end result of the disease,
cavities.

Note:

References (97) to (313) are to papers which were also considered in this review, but for
which space did not allow discussion or individual citation in the text. They, as papers (1) to
(96), are presented in the Evidence Tables accompanying this paper.

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