Professional Documents
Culture Documents
5, 1994, 52-65
Printed in Denmark All rights reserved
PERIODONTOLOGY 2000
ISSN 0906-6713
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teeth, which normally favor their retention. Lactobacillus does not reappear in the mouth until after
age 2, usually as Lactobacillus casei, the dominant
oral species.
Streptococcus sanguis, an organism that preferentially colonizes tooth surfaces, can be recovered
shortly after the teeth erupt (23). Streptococcus mutans, which favors the same ecological niche, was absent from the mouths of 91 predentate infants but
was detected in 9 of 40 infants with only erupted
primary incisors (9) and half of a group of 2-yearolds (57). It has been shown that, if mothers are
treated so as to reduce their levels of S. mutans, the
rate of transmission of S. mutans to their infants can
be reduced by as much as one-third (57).
Actinomyces naeslundii, a predominant species of
dental plaque, is recovered from 40% of young
children. Actinomyces uiscosus which is absent in infants, gradually increases in prevalence as the child
grows older, with half the children colonized by age
7 (36). Veillonella species follow a similar pattern of
increasing prevalence with increasing age (86).
Although most infants harbor a predominantly
gram-positive, facultative microbiota, anaerobes can
also be recovered (59), particularly after tooth
emergence. As many as 61% of children aged 5-7
years harbor black-pigmenting gram-negative anaerobes (7, 30, 41, 84), as well as spirochetes (30, 84,
90). The proportion of these organisms and other
strict anaerobes increases in adolescence and adulthood (106, 147) but may show a great deal of siteto-site variability (14),with local factors such as pH,
eH and assorted bacterial interactions playing an
important role (89). Some variability is also due to
such factors as the state of health of the dentition
(Table 1) and periodontal tissues (5, 6, 17, 31, 33),
the medical status of the patients (8, 18, 19, 43, 87)
and their racial origin (21,120).
With the loss of teeth in older adults, some ecological niches such as tooth surfaces and gingival
sulci that favor the retention of certain species are
lost. As these specialized environments disappear
there is a marked reduction, if not a complete elimination, of such species as Actinobacillus actino-
Table 1. Microbiology of the periodontal region: representative species in periodontal health and disease
Health
Juvenile periodontitis
Streptococcus sanguis
Actinobacillus actinomycetemcomitans
Streptococcus mitis
Other bacterial species (?)
Veillonella parvula
Actinomyces naeslundii
Rapidly progressive periodontitis
Actinomyces viscosus
Actinobacillus actinomycetemcomitans
Rothia dentocariosa
Porphyromonas gingivalis
Bacteroidesforsythus
Gingivitis
Campylobacter rectus
Actinomyces species
Eikenella corrodens
Streptococcus species
Veillonella species
Refractory periodontitis
Fasobacterium species
Actinobacillus actinomycetemcomitans
Treponema species
Porphyromonas gingivalis
Prevotella intermedia
Prevotella intermedia
Bacteroides forsythus
Adult periodontitis
Campylobacter rectus
Treponema species
Peptostreptococcus micros
Enteric rods
Prevo tella intermedia
Porphyromonas gingivalis
Candida species
Bacteroidesforsythus
Peptostreptococcus micros
Campylobacter rectus
Actinobaciltus actinomycetemcomitans
Eikenella corrodens
Fusobacterium species
Selenomonas species
Eubacterium species
The results of these and other investigations demonstrated that dental plaque is composed of a large
variety of bacterial morphotypes with some significant heterogeneity in the appearance of the microbial deposits. Because of the lack of standardization, it has been difficult to relate the findings from
one study to another. Furthermore, most of the
studies were not designed to investigate the dynamics of plaque formation at the cellular level but
rather to provide a cross-sectional view of plaque
structure in one or more subjects at a particular
point in time. However, in at least one study (791,
data were obtained that provided some new insight
into the process of dental plaque formation and
maturation. A related study also demonstrated that
detectable morphological differences could be observed among dental plaques from mouths with differing states of periodontal health (70). These studies
are reviewed in greater detail later.
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Early studies focused on differences in the composition of the microbiota associated with stable and
failing implants. The reports generally indicated that
healthy implants have a microbiota similar to that of
healthy teeth, while failing implants have a microbiota similar to that found around teeth with periodontitis (1, 91, 93, 110, 111, 117). It is likely, however, that around failing implants the composition
of the microbiota may be related to the nature of the
implant failure. Thus if a microbiota is found resembling that of adult periodontitis, the failure is probably infectious in nature (infectious peri-implantitis), since in failures due to traumatic injury
the microbiota is similar to that around stable implants or periodontally healthy teeth (114). These
dramatic differences between failures due to trauma
and failures due to infection presumably apply only
to cases that fall clearly either into one or the other
category. The possibility exists that an implant failure initially due to trauma may become secondarily
infected, with an accompanying shift in the composition of the microbiota. Resolving the infection may
not necessarily solve the primary clinical problem,
which is occlusal in nature.
It is noteworthy that spirochetes and Porphyrornonas gingiualis do not colonize healthy implants in
an edentulous mouth as readily as they do implants
in partially edentulous patients (92, 97, 105, 107).
The frequently reported absence of spirochetes
around healthy implants in edentulous mouths
coupled with their presence in low numbers around
healthy fixtures in dentulous patients suggests that
diseased teeth may serve as a source of infection for
dental implants (107). Should this be the case, controlling periodontal infections prior to implant
placement ought to improve the long-term survival
rate of dental implants.
Since a variety of materials are used in the manufacturing of dental implants, some studies have
examined the influence of materials on plaque formation in situ (46, 54, 96, 108, 109, 146). It appears
that materials can affect the rate of early plaque formation, that is, within the first few hours of exposing
the fresh surface to the intraoral environment. After
4 hours in the mouth, some differences were noted
in the rate of plaque formation on disks of assorted
materials, including titanium and hydroxyapatite,
that were glued to the gingiva. Quirynen et al. (108)
and Weerkamp et al. (146) observed a direct correlation between plaque accumulation on a variety of
substrates and increasing surface free energy. However, surface roughness emerged as a more important factor than surface free energy in promoting
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Fig. 1. One-day-old supragingival plaque on epoxy resin crown. The bacterial deposit (B) is attached to an electron-dense pellicle (P) which lines
the surface of the epoxy crown (E). X24,OOO; bar=l pm.
Fig. 2. One-week-old supragingival plaque on epoxy resin crown. The bulk
of this deposit consists of columnar colonies of coccoid bacteria (C) growing from the epon surface (E) outward. Some filamentous bacteria (F) have
colonized the plaque surface. x 1200.
Fig. 3. One-week-old supragingival plaque on epoxy crown. Three different
coccoid bacterial morphotypes (labelledA through C) have formed columnar microcolonies that compete for space as they grow away from the
crown surface (toward top of figure). X5400; bar=l pm.
56
Calculus
Mineralization of supragingival as well as subgingiVal plaque gives rise to calculus. Mineralization generally proceeds in an incremental pattern from the
Fig. 4. Mature supragingival plaque on enamel surface (E). The bulk of the
deposit consists of filamentous bacteria (F). Corncob formations ( C ) are visible on the surface. x 1000.
Fig. 5. Mature subgingival plaque in periodontitis pocket. Test-tube brush
formations (T) cut through their long axis are surrounded by a predominantly
motile, gram-negative microbiota (M), rich in spirochetes. X 1700.
Fig. 6. Wo-month-old subgingival plaque adjacent to epoxy resin crown. The
microbiota is composed of predominantly gram-negative, anaerobic bacteria,
including thin, gram-negative filaments (F) and spirochetes (S). X 7800; bar=
1 pm.
inner zones of the dental plaque outward. This pattern of mineralization may give rise to Liesegang
rings, concentric rings reflecting successive phases
of mineralization, which are particularly noticeable
in old calculus deposits. For a comprehensive review
of calculus formation, see Schroeder (121). As new
layers of plaque become mineralized from the
deeper layers outward, the layering pattern throughout the deposit becomes emphasized, giving the erroneous impression that the entire deposit grew by
apposition of bacteria on the surface of the underlying calculus. Although calculus may grow in an incremental fashion through the progressive mineral-
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Fig. 7. Wo-month-old subgingival plaque adjacent to epoxy resin crown. The majority of the bacteria in this field
consist of spirochetes (S) with their distinctive ultrastructure. X52,OOO; bar=0.5 km.
Fissure plaque
The microbial colonization of occlusal fissures is of
interest because of the relationship of the fissure
microbiota to the pathogenesis of dental caries. In
order to obtain a dynamic picture of the colonization
process in humans, Loe et al. (82) developed an artificial fissure made of Mylar foil, which they embedded in the occlusal surface of human mandibular
molars for periods of up to 2 months (55, 139, 142).
In the first week, the fissure first contained mostly
food debris, later replaced by gram-positive cocci,
mostly streptococci, short rods and yeast cells. Later,
lactobacilli appeared and increased in number with
time (136). Some filaments appeared after 3 weeks.
Some foci of mineralization were observed at about
the same time. After 2 months, the contents consisted mostly of gram-positive cocci and short rods,
many of which had undergone lysis, and some plant
wall material. No fusiform or spirillar forms were observed at any time (55, 139, 142).This type of plaque
did not exhibit the dynamic changes observed on
smooth tooth surfaces (139).
59
Listgarten
such a microbiota from developing, by regularly removing recently formed dental plaque, thereby interfering with its maturation and ability to provide a
hospitable environment for a number of periodontal pathogens.
Our improved understanding of the dynamic nature of plaque formation has helped clarify the biological basis underlying the effectiveness of plaque
control on the clinical status of the periodontal
structures. Even though mechanical and some forms
of chemical plaque control are nonspecific methods
of reducing plaque mass, they also affect the qualitative nature of dental plaque. This is accomplished
through regular interference with the normal plaque
maturation process, which leads to the establishment of an anaerobic environment favorable to the
proliferation of most periodontal pathogens. Of
course, there are exceptions to this general observation. One example is that of A. actinomycetemcomitans infections, which may persist despite repeated mechanical debridement. This may be due,
in part, to the ability of A. actinomyceterncornitans, a
facultative bacterium, to colonize the dentition without the prior establishment of an anaerobic environment. It has also been suggested that the persistence
of A. actinomycetemcomitans may be due to its ability to invade and persist within periodontal tissues
(25, 27). Similarly, other periodontal pathogens may
be able to survive mechanical debridement and lead
to the production of periodontal diseases that have
been described as refractory to standard treatment.
Some reports indicate that, in relatively shortterm studies, supragingival plaque control has no
detectable influence on established subgingival
plaque in deep pockets, that is, with probing depths
of 7 mm or greater (56, 75). However, studies that
included shallower pockets or extended for one or
more years suggest that supragingival plaque control
not only results in beneficial clinical improvement
but also affects the composition of subgingival
plaque (29, 88, 131). Yet, even in long-term studies,
pockets with probing depths of 7 mm or greater were
not significantly affected by supragingival plaque
control alone (29). The apparent discrepancy between these results may be due to the cumulative
influence of a relatively minor effect of supragingival
plaque control on the subgingival microbiota. Waerhaug (145) demonstrated that toothbrushing was
able to disrupt subgingival plaque up to 0.9 mm
from the gingival margin. This effect may not be sufficient to cause immediate changes in the composition of the subgingival plaque of deep pockets. In
time, however, the cumulative effect of brushing and
60
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