Anaerobe (1999) 5, 221227

Article No. anae.1999.0204

ORAL MICROBIOLOGYAND RELATED INFECTIONS (FACULTY PRESENTATION)

Bacteriology of Most Frequent Oral Anaerobic

Infections
S. Piovano
School of Dentistry,
Maimonides University,
Buenos Aires, Argentina

Key Words: oral anaerobic

infections

The anaerobic infections most frequently found in the oral cavity are
gingivoperiodontal diseases and pulpal and periapical infections. Gingivitis
and adult periodontitis are the most frequent forms. In adult periodontitis
the subgingival microbiota are complex and there is a prevalence of
Porphyromonas gingivalis, Prevotella intermedia, Prevotella nigrescens, Actinobacillus actinomycetemcomitans, Bacteroides forsythus, Peptostreptococcus micros,
Campylobacter rectus, and species of Fusobacterium, Eikenella and Treponema.
The microflora associated with peri-implant infections are similar to the
microflora found in periodontal diseases, particularly in partially edentulous patients. Implant placement is therefore not recommended in patients
presenting with uncontrolled periodontal disease.
Likewise, there is a similarity between the genera identified in periodontal pockets and infected root canals, and in periapical infections.
However, some species are more prevalent than others in both infections.
The following were predominantly observed inside the root canals:
Prevotella intermedia, Prevotella nigrescens, Peptostreptococcus anaerobius,
Peptostreptococcus micros, Eubacterium lentum, Eubacterium alactolyticum and
Porphyromonas endodontalis, with strong associations among some species.
Pericoronaritis is another infection associated with anaerobic Gramnegative bacilli and treponeme. There are a great number of methods for
microbiological diagnosis, and treatment of some oral infections depends
on close interaction between the microbiologist and the dentist.
# 1999 Academic Press

Introduction
The oral cavity is the habitat of numerous microbial
species. It has been observed that 1 g of dental plaque
contains more than 1011 micro-organisms [1]. Many
indigenous flora are anaerobes and these microorganisms can be associated with oral infections and
be the origin of distant infections [19]. The most
frequent oral anaerobic infections include gingivoper10759964/99/030221 + 07 $30.00/0

iodontal diseases, pulpal and periapical infections,

peri-implantitis and pericoronarities.

Gingivoperiodontal Diseases
Gingivoperiodontal diseases, including gingivitis and
periodontitis, are caused by dental plaque, which is a
biofilm [10,11].
# 1999 Academic Press

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S. Piovano

Microbial species associated with gingivitis

Studies have demonstrated that the dental plaque
associated with gingivitis presents a high burden of
micro-organisms (104106) and an increase in anaerobic Gram-negative organisms (1550%) [10]. Culture
studies of the plaque near the marginal gum have
demonstrated a prevalence of Actinomyces species
[12].
Likewise, culture studies indicate that Fusobacterium
nucleatum, Prevotella intermedia, Campylobacter species
and Veillonella are frequently isolated from plaque
samples associated with gingivitis [12]. Spirochaetes
can be found mainly at the apical subgingival area.
Gingivitis can be worsened by steroid hormones. In
puberty, pregnancy and women taking oral contraceptives, it has been shown that gingival disease is
associated with an inadequate plaque control, worsened by steroid hormones that stimulate the growth
of Prevotella intermedia [1315].
Acute necrotizing ulcerative gingivitis is a destructive inflammatory disease associated with species of
Selenomonas, Porphyromonas, Prevotella, Fusobacterium
and Treponema [4,16]. The prevalent bacteria are
Prevotella intermedia and spirochaetes and Prevotella
intermedia represents between 8% and 15% of the
microbiota. Spirochaetes represent approximately
30% of the morphotypes that are present with
medium and large spirochaetes being prevalent.
Studies by Transmission Electron Microscopy have
shown the invasion of tissues by spirochetes [1719].
Microbial species associated with periodontitis
Adult periodontitis. An increase in the total microbial
burden (105108 micro-organisms) and high levels of
Porphyromonas gingivalis have been observed in adult
periodontitis [10]. Porphyromonas gingivalis, Bacteroides
forsythus and Actinobacillus actinomycetemcomitans
have been identified as causative agents, and not as
agents merely associated with disease [10]. The
micro-organisms specifically implied are Porphyromonas gingivalis, Bacteroides forsythus, P. intermedia, Prevotella nigrescens and Actinobacillus actinomycetemcomitans. A second group of micro-organisms include
F. nucleatum, Campylobacter rectus, Eikenella corrodens,
Eubacterium nodatum, Selenomonas noxia, Peptostreptococcus micros, Streptococcus intermedius and Treponema
denticola [2,2033].
Adult periodontitis is associated with a group of
bacteria and different microbial complexes have been
described from subgingival plaque samples [10,34,35].
Many transmission studies have demonstrated that
the same clonal types of P. gingivalis, A. actinomycetemcomitans and T. denticola can be found in members

of the family [3640]. Porphyromonas gingivalis, A.

actinomycetemcomitans and T. denticola penetrate the
gingival epithelium, and they have endotoxins, active
compounds and cytotoxic enzymes which act upon
the host [21,4144]. Spirochetes constitute 3756% of
the flora [19] and all morphogroups are detected with
a prevalance of small and medium spirochetes
[25,26,45]. The microflora are necessary to produce
and allow progression of disease, modulated by host
factors and lifestyle [33,46].

Rapidly progressing periodontitis. It affects young individuals and has a rapid evolution. Prevalent bacteria
in active sites are A. actinomycetemcomitans, P. gingivalis, P. intermedia, F. nucleatum, T. denticola, B. forsythus
and Campylobacter species [47].
Kamma et al. [47] have examined the microflora of
severe, moderate and minimal lesions in young adults
with rapidly progressing periodontitis, and have
observed microbial complexes associated with severe
and moderate lesions, while in small lesions species of
Antinomyces and Streptococcus, Capnocytophaga ochracea, Haemophilus segnis and Veillonella parvula were
identified.

Juvenile periodontitis. Juvenile periodontitis affects

adolescents and is characterized by a rapid destruction of periodontal tissues [4]. The major microorganism related to juvenile periodontitis is
A. actinomycetemcomitans [4,44,48]. A. actinomycetemcomitans has been considered as an agent of exogen
infection in periodontitis [31,44], in patients with
early-onset periodontitis and adult periodontitis it has
been frequently isolated from periodontal pockets and
other ecological niches of the oral cavity [44,48,49].
Epidemiological studies have shown that this microorganism can be transmitted by members of the
family [3639]. The introduction of the bacteria into
the oral cavity is facilitated by the presence of
frequent contacts and high inoculation doses [38].
Although A. actinomycetemcomitans is the major
species related to juvenile periodontitis, high rates of
P. gingivalis, Capnocytophaga, E. corrodens, F. nucleatum
and Eubacterium brachy have been observed.

Prepubertal periodontitis. The main features are a rapid

and severe destruction of deciduous teeth. In the
generalized form the patients have defects in polymorphonuclear neutrophils and macrophages [4].
They usually present with other infections as well as
periodontal lesions. The prevalent micro-organism is
A. actinomycetemcomitans frequently associated with

Frequent oral anaerobic infections

Capnocytophaga sputigena, P. intermedia and E. corrodens
[4].
Refractory periodontitis. The species identified in active
sites have been: P. gingivalis, A. actinomycetemcomitans,
F. nucleatum, P. micros, C. rectus, B. forsythus, P.
intermedia and E. corrodens. Some of these bacteria
were isolated inside the gingiva in samples from
biopsies of the active disease sites [50,51].
Periodontal abscess. There is a wide range of bacteria
present in abscesses, which can exist in the plaque
adhered to the tooth, or be free at the apical portions
or adhered to the soft wall of the pocket. The
prevailing micro-organisms are: P. micros, P. gingivalis,
Fusobacterium spp., Capnocytophaga spp., Actinomyces
spp. and species of oral streptococcus.
Periodontal microbiota and halitosis. Halitosis has frequently been associated with gingivoperiodontal
infection [52]. T. denticola, P. gingivalis, Veillonella
species and Fusobacterium have all been associated
with halitosis [53,54]. Halitosis can also be associated
with flora of the tongue and flora lower down the
gastro-intestinal tract. A direct relation between
halitosis, the tongue's covering, and subgingival
plaque has been observed [55].

Pulpal and Periapical Infections

Micro-organisms reach the pulp in various ways. The
most frequent are: fracture of dental tissues, as a result
of natural history of dental caries; or through tubules
of exposed dentine in the surface of root as a result of
fissures or radicular caries. Likewise, the pulp can be
infected by the microbial flora of the periodontal
pocket and by dental procedures [56].
When anaerobic Gram-negative bacilli are prevalent in an endodontic infection, they release lipopolysaccharides and a periapical periodontitis is
initialized at the periapex [5,5762]. Sundqvist [63]
analysed the microflora of root canals of teeth with
apical periodontitis according to the frequency of
occurrence and the analysis of association between
bacteria. Results have shown that the most frequent
species isolated was F. nucleatum, present in 45% of
the root canals. Likewise, P. intermedia, P. micros,
Peptostreptococcus anaerobius, Eubacterium alactolyticum,
Eubacterium lectum and Capnocytophaga rectus were
the prevalent species in this kind of infections.
F. nucleatum showed a positive association with
P. micros, Porphyromonas endodontalis, Selenomonas
sputigena and C. rectus. A positive association was
seen between P. intermedia and P. micros, P. anaerobius
and E. lectum, and E. alactolyticum and C. rectus.

223

Many authors have reported that the presence of

species of the genera Porphyromonas, Prevotella and
Peptostreptococcus are associated with an increase in
the incidence of clinical symptoms of pain and
sensitivity to pressure on the teeth [6371]. Acute
symptoms have been associated with Prevotella buccae,
P. intermedia, P. gingivalis, P. endodontalis and Peptostreptococcus magnus [66,67,71]. Conrads et al. [72]
analysed samples from nectrotic root canals using
PCR and have observed species of Actinomyces,
F. nucleatum, Streptococcus milleri and B. forsythus, the
latter having not been shown previously in endodontic samples. Nair Ramachandran et al. [73] examined
through microscopic studies the apex of endodontically treated teeth presenting a periapical lesion in the
radiography after a post-treatment period of 4 to 10
years. Extraradicular presence of bacteria and yeast
was observed in the teeth with infection following
endodontic therapy [62,73,74].
Gomes et al. [65] observed the presence of Prevotella,
Peptostreptococcus, Eubacterium and Propionibacterium
spp. in these refractory lesions. In periapical abscesses, 75% to 94% of the flora are anaerobes. Species
of Prevotella and Porphyromonas have frequently been
isolated. P. gingivalis, P. endodontalis and P. intermedia
are the prevalent species [68,75] and other Prevotella
species identified in abscesses are Prevotella oralis,
Prevotella oris, and Prevotella buccae [68,75].
P. anaerobius, P. micros, Peptostreptococcus prevotti and
P. magnus are the prevalent Peptostreptococcus species
[65]. Species of Veillonella, Eubacterium, Actinomyces
and Fusobacterium are frequently isolated [64,65].
`Viridans streptococci', facultative anaerobes, are
present in periapical infections associated with anaerobes [56]. Figure 1 shows the micro-organisms most
frequently isolated from endodontic infections.

Peri-implantitis
Various criteria originally used for the study of
periodontal diseases have been applied to implantology [29,76,77]. The sulcus of relatively healthy
implants with stable probing depth (35 mm for 1
year) has shown by MCO a prevalence of non-mobile
bacteria. Cocoid cells prevail in those sites (64.2%). In
culture, the microbiota are poor, dominated by
facultative anaerobic Gram-positive cocci [7883].
The microbial infection can lead to two different
clinical manifestations: (1) a lesion limited to inflammation of superficial soft tissues (mucositis); and (2) a
lesion comprising soft tissues and the marginal
portion of the implantbone interface (peri-implantitis) [77].
The presence of remnant teeth with any untreated
or badly controlled periodontal disease enhances

224

S. Piovano

Figure 1. Prevalent species in pulpal and periapical infections.

colonization of potentially peridontopathic bacteria in

the peri-implant area [84]. Differences in the microflora of implants of partially or totally edentulous
patients have been observed. Spirochetes have been
seen from samples of teeth and implants in partially
edentulous patients, but were not detected in implants from totally edentulous patients [81,85]. Apse
[85] noticed a higher prevalence of Gram-negative
black-pigmented anaerobic bacilli in partially edentulous patients compared with totally edentulous
patients.
George et al. [86] evaluated implants in partially
and totally edentulous patients with implants.
P. intermedia and P. gingivalis were observed in 39%
of partially edentulous patients and in 19% of totally
edentulous patients. In the implants harbouring one
of these micro-organisms an increased probing depth,
high tendency to bleeding and a higher level of
gingival fluid were recorded [86].
A long-term study clinically and microbiologically
examined peri-implant infections in totally edentu-

lous patients. High levels of anaerobes were detected

2 weeks after the implantation. Fusobacterium spp.
were first detected at day 42; spirochetes at day 120,
and during that period increased probing depth and
pus formation were observed [79].
Other micro-organisms such as F. nucleatum,
P. intermedia, Prevotella melaninogenica, P. micros,
Capnocytophaga and C. rectus have been associated
with development of peri-implantitis [78,79,87,88].
Likewise, it has been seen that the long-term
systemic use of antibiotics or immunosuppressors
longterm, can lead less prevalent micro-organisms to
play a major role in these infections. This happens
with Candida albicans, Pseudomonas aeruginosa, Klebsiella pneumoniae, Escherichia coli, Staphylococcus species,
and others [77,86].
The failure of an implant can be produced by a periimplant infection, enhanced oclusal forces, incorrect
surgical technique or systemic states affecting the
bone [76]. Rosenberg [76] stated indicators used to
determine the aetiology of implant failures due to

Frequent oral anaerobic infections

infections or oclusal trauma. The study of microbial
morphotypes by dark-field microscopy and cultures,
as well as clinical indicators, have shown that
infection and oclusal trauma respond differently.
Clinical indicators of infected sites behave in a similar
way as periodontitis and the examination of morphotypes led to high rates of spirochetes and mobile
bacilli [76]. The micro-organisms identified by culture
methods from failed implants due to infections have
been associated with periodontitis, while implant
failure due to oclusal trauma showed prevalence of
Streptococcus sanguis [76].
The diagnosis of peri-implantitis is made clinically
and radiographically. However, microbiological studies should be included to examine the associated
microbiota. It is now recognized that peri-implant
tissues behave in a way similar to periodontal tissues
when confronting microbial challenge, and therefore,
strict control of the microbiota surrounding the
implants is a determinant for long-term success.

Pericoronaritis
Pericoronaritis develops during eruption of teeth. Few
studies have examined the microflora associated with
pericoronaritis, although Gram-negative anaerobic
bacilli and treponemes are prevalent [89,90]. It has
also been observed that Treponema denticola is prevalent in pericoronaritis [89]. Transmission Electron
Microscopic studies have demonstrated that spirochetes can be found in almost all cases of chronic
pericoronaritis of the third inferior molar [91].

Oral Microora Associated with

Systemic Infections
The association of oral infections with infectious
endocarditis has been demonstrated [1,92,93]. Recently, periodontal disease has been associated as a
high-risk factor for coronal diseases, arteriosclerosis,
myocardial infarction, pneumonia, pre-term births
and low birth weight [3,7,9,94].

Conclusions
The oral cavity is characterized by harbouring
indigenous flora. The ability of micro-organisms to
colonize the different oral surfaces depends mainly on
their binding potential. Various environmental factors
and host factors are involved in the harbouring of
micro-organisms and microbial composition. Oral
infections are predominantly anaerobic. There is a
variety of microbiological diagnostic methods for oral

225

infections, the therapy of which depends on a close

relation between the clinician and the microbiologist.
Dentistry should assume this new challenge of team
work interaction in order to prevent and solve oral
and systemic infections.

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