Biotechnology & Biotechnological Equipment

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Microbiology of Periodontal Diseases. A Review

Christina Popova, Velitchka Dosseva-Panova & Vladimir Panov

To cite this article: Christina Popova, Velitchka Dosseva-Panova & Vladimir Panov (2013)
Microbiology of Periodontal Diseases. A Review, Biotechnology & Biotechnological Equipment,
27:3, 3754-3759, DOI: 10.5504/BBEQ.2013.0027

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MEDICAL BIOTECHNOLOGY
MICROBIOLOGY OF PERIODONTAL DISEASES. A REVIEW
Christina Popova1, Velitchka Dosseva-Panova1, Vladimir Panov2
1
Medical University of Sofia, Faculty of Dental Medicine, Sofia, Bulgaria
2
Medical University “Prof. Dr. P. Stoyanov”, Faculty of Dental Medicine, Varna, Bulgaria
Correspondence to: Velitchka Dosseva-Panova
E-mail: vdosseva@yahoo.com

ABSTRACT
Periodontal diseases are inflammatory and destructive diseases of the dentogingival complex associated with specific periodontal
pathogens inhabiting periodontal pockets. Periodontal diseases lead to damage of the periodontal tissues supporting the teeth
(bone and connective tissue) and affect the quality of life of the affected individuals: poor alimentation, tooth loss, social
and financial problems. Although it is generally considered that the disease has multifactorial etiology, data show that some
specific Gram-negative microorganisms in the subgingival plaque biofilm play a major role in the initiation and progression of
periodontitis. Porphyromonas gingivalis, Treponema denticola and Tannerella forsythia form a consortium in the subgingival
biofilm and are regarded as the principal periodontopathogenic bacteria. Other microorganisms that have been implicated as
predominant species in the disease process are: Aggregatibacter actinomycetemcomitans, Fusobacterium nucleatum, Prevotella
intermedia, Campylobacter rectus, Peptostreptococcus migros, Eikenella corrodens. In periodontitis, the initiation of the disease
is the colonization of the tissues by these pathogenic species. The next step is bacterial invasion or invasion by pathogenic
products into the periodontal tissues, interactions of bacteria or their substances with host cells, and this directly/indirectly
causes degradation of the periodontium, resulting in tissue destruction.

Biotechnol. & Biotechnol. Eq. 2013, 27(3), 3754-3759
Keywords: periodontal disease, periodontal pathogens,
microbial diagnosis of periodontitis
Introduction
It is well known that destructive periodontal diseases are
infections caused by bacteria that colonize the tooth surface,
gingival margin and subgingival environment. Multiple studies
in the last decades illustrate the unique infectious nature of
chronic periodontitis and aggressive periodontal diseases.
It has been demonstrated, however, that the initiation and
progression of the inflammatory and destructive periodontal
lesion is related not only to the presence of bacterial strains
pathogenic for the periodontium, but also to the lack or
minimal proportions of the beneficial microorganisms in a
susceptible host (3, 8, 14, 15, 24, 28). Periodontal diseases are
polymicrobial, multifactorial diseases, and there are many host
factors involved in determining the individual susceptibility
to disease. It is recognized that the relationship between
periodontal microbiota and the host is generally benign
but, when the specific bacterial species overgrows in the
subgingival spaces, this may cause periodontal inflammation
and destruction with attachment loss and bone loss.
It is important to underline that periodontal diseases appear
to be initiated by a relatively limited number of periodontal
pathogens in the complex dental biofilm (4, 5, 7, 8, 10, 15,
16, 17, 18, 22, 25, 28). The periodontal pathogens currently
known represent a small part of all of the 600 bacterial
species that can colonize dental surfaces over and below the
gingival margin and oral mucous membranes. Clinical and
3754
experimental evidences confirm that certain bacterial strains
in the periodontal environment can induce gingival tissue
inflammation and bone destruction. These bacterial strains
are defined as periodontal pathogens (16, 24). In the last
three decades, it has been generally accepted that periodontal
infections are polymicrobial (1, 5, 27). Only a small percentage
of the dental biofilm bacteria are defined as pathogenic for the
periodontal tissues. It is well documented that these bacteria,
even when present in very small quantities, possess the ability
to damage the periodontal structures.
Most of the periodontal pathogens are anaerobes but the
biofilm can also harbour facultative aerobes, capnophiles and
microaerophiles whose number depends on the environment in
the developed biofilm and periodontal pocket. Most periodontal
pathogens represent the true periodontal infection. Some
bacterial species in the periodontal environment that are part
of the commensal flora (Actinomyces, certain Streptococcus
and Staphylococcus spp.) can provoke opportunistic infections
in case of ecosystem disturbance. There is evidence that
detection of certain enterobacteria, viruses and Saccharomyces
spp. in the periodontal pockets could indicate superinfection
associated with a periodontal destructive process. It has
recently been generally recognized that periodontal diseases
are mixed infections.
Numerous investigations accentuate on the definition
of the subgingival flora which is most specific for a distinct
periodontal disease. Although results relate to the presence
of certain periodontopathogens with fixed periodontal status,
there is still no convincing evidence for the specificity of
bacterial species in different periodontal diseases (12, 26).
Biotechnol. & Biotechnol. Eq. 27/2013/3
 While localized periodontitis is strongly associated
with the presence of Actinobacillus (Haemophilus)
actinomycetemcomitans and Capnocytophagа and Eikenella
corrodens, for the major part of periodontal diseases there is
no correlation with a definite composition of the bacterial flora.
Criteria for identification of bacterial species as
periodontopathogens
There is considerable evidence that the bacterial biofilm is
the etiological agent in periodontal diseases. The scientific
evidence supports a polymicrobial etiology and the currently
prevailing view implicates minor constituents of the subgingival
microbial community as primary periodontopathogens.
According to the criteria proposed by Socransky and
Haffajee (23), a periodontal microorganism has to meet
some conditions to be considered a potential pathogen: to be
associated with the disease by means of increased number in
diseased patients and sites; to be reduced or eliminated after
treatment and, with the healing, to be capable of provoking
the destructive host response; to possess the capacity to cause
the disease in experimental animal models; to demonstrate
production of virulence factors known to cause periodontal
destruction.
To realize their pathogenic potential, bacterial species
should be able to colonize the subgingival area, to produce
virulence factors that directly (enzymes and toxins) or
indirectly (antigens and activators) lead to initiation of a
destructive inflammatory reaction in the individual and injury
of periodontal tissues (1, 2, 18). The virulence capacities of
bacteria depend on the production of certain factors for adhesion
such as adhesins, lectins, fimbriae and vesicles. Agents that
directly damage the periodontal tissues are proteases, alkali
and acid phosphatases produced by microorganisms, fatty and
organic acids, IgG- and IgA-proteases, chondroitinsulfatase
and toxic products (endotoxins, leukotoxin, mucopeptides of
the bacterial wall, end-products of metabolism such as H2S,
NH4, indole). Chairside tests can be used to determine the
bacterial biofilm pathogenicity on the basis of the proteolytic
activity of the dental plaque. Bacterial enzyme activity (BANA
hydrolysis) is used as a marker for the proteolytic activity of
the bacterial biofilm (11). This test is positive for T. forsythia,
T. denticola and P. gingivalis and reveals the high virulence
of the whole biofilm when these microorganisms are present.
Mobility is an essential virulent factor of certain pathogenic
bacteria and allows them to invade the epithelium and
connective tissue (spirochetes). Invasive properties have been
found for many microorganisms of the dental biofilm (14, 24):
1. Invasion into the epithelium: A. actinomycetemcomitans,
P. gingivalis, Tannerella forsythia, P. intermedia, F. nucleatum;
2. Invasion in the basal lamina with collagen type I and IV:
P. gingivalis, F. nucleatum;
3. Invasion into deep layers of the connective tissue:
spirochetes, Selenomonas spp., Campylobacter spp.
Biotechnol. & Biotechnol. Eq. 27/2013/3
Specific bacterial sequence has been illustrated in studies
on the development of the dental plaque. The domination of
the Gram-negative bacteria relatively to the Gram-positive
microorganisms in the process of biofilm development
corresponds to physiologic changes in the dental plaque. Early
colonizing streptococci and actinomycetes consume oxygen
and reduce the oxygen potential of the biofilm environment,
which favors the growth of anaerobic species. That is why,
the pathogenic bacteria dominating the mature plaque are
anaerobic and asaccharolytic.
Essential interbacterial relationships have been observed in
mature biofilms. Such relationships may affect the virulence
of certain species and, in general, of the entire biofilm. These
relations are categorized as positive or negative. Three types
of positive relationships are known (symbiosis): mutualism,
synergism, and commensalism. Mutualism is a symbiosis
in which the bacterial species have equal benefit from their
coexistence (Porphyromonas gingivalis and Treponema
denticola; T. forsythia and Fusobacterium nucleatum).
Synergism is the interbacterial relation when the pathogenic
potential of both species is superior to the sum of their individual
potentials (Porphyromonas gingivalis and Fusobacterium
nucleatum). Commensalism is a bacterial interaction that
favors one of the two species (Porphyromonas gingivalis and
Campylobacter rectus). Negative interactions between bacterial
species exist in the form of antagonism (Streptococcus mutans
and Aggregatibacter actinomycetemcomitans; Streptococcus
sanguis and Aggregatibacter actinomycetemcomitans) and
competitive relations (Porphyromonas gingivalis and Gram-
positive Actinomyces viscosus, Actinomyces naeslundii,
Actinomyces israelii, Streptococcus mutans, Streptococcus
mitis, Corynebacterium sp.).
The current knowledge about the dental biofilm
structure is that interbacterial interactions are facilitated
by a common circulatory system in the biofilm and the
established interbacterial exchange of metabolic products
in an environment that is limited in nutritive factors. Recent
data confirms that the bacteria in microcolonies of the biofilm,
under certain cellular density, communicate through exchange
of information (quorum sensing) by gene expression including
genes for antibiotic resistance (19). Interbacterial relationships
in the biofilm have the potential to influence the bacterial
community structure and to stimulate the growth of certain
species and inhibit the concurrent species. These interactions
can, to a great extent, determine and affect the relations
between the microorganisms and the host.
The pathogenicity of certain bacterial species in relation
to periodontal tissues is evaluated based on the classical
postulates of Koch, modified by Socransky (7) and based on
the following criteria:
• association with disease;
• treatment elimination, which means the influence of
successful therapy both on clinical parameters and on
3755
 the associated microbiota, and subsequent remission of
the disease;
• pathogenicity in animal models, which is the ability to
cause disease in experimental animals;
• induction of a host response by bacteria or bacterial
components gaining access into the underlying
periodontal tissues;
• production of virulence factors with direct and indirect
effect, which give bacteria a selective advantage to
destroy host tissues or evade host defenses.
According to published reports, Aggregatibacter
actinomycetemcomitans and Porphyromonas gingivalis (7) are
the two species classified as periodontal pathogens that fulfill
all of the criteria listed above. Other suspected periodontal
pathogens are: Treponema denticola, T. forsythia, Fusobacterium
nucleatum, Prevotella intermedia, Campylobacter rectus,
Eikenella corrodens, Peptostreptococcus micros, Selenomonas
sp.
Based on scientific evidence, Socransky and Haffajee
(22) classified the microorganisms in the bacterial complexes
depending on their presence in the biofilm and subgingival
area and their involvement in the pathogenesis of periodontal
diseases.
Table  1 presents the subgingival bacterial classification
in Socransky complexes, which are associated with different
periodontal status (9). Bacteria of the purple, yellow and green
complexes correspond to periodontal health, but bacteria of
the orange and red complexes and other not grouped ones are
suspected periodontopathogens.
TABLE 1
Subgingival bacterial classification in Socransky complexes
Bacterial species Complex
Actinomyces
Purple
Veillonella
Streptococcus: gordonii, intermedius,
Yellow
mitis, sanguis
Capnocytophaga
Green
E. corrodens
Campilobacter rectus
Fusobacterium nucleatum
Orange
P. micros
P. intermedia
T. forsythia
P. gingivalis Red
T. denticola
A. actinomycetemcomitans
Not grouped
Selenomonas
Table  2 indicates suspect periodontopathogens and their
association with periodontal diseases, the clinical response to
elimination, immune response and virulent factors (6).
3756
The most studied periodontopathogens in the last years
are: A. actinomycetemcomitans, T. forsythia, T. denticola, P.
gingivalis, P. intermedia, C. rectus and spirochetes. There is
substantial evidence proving that these bacteria are associated
and/or responsible for attachment loss, especially in aggressive
periodontitis (24).
Aggregatibacter actinomycetemcomitans is a small, short,
straight or curved rod with rounded ends that is nonmotile
and gram-negative and is strongly associated with destructive
periodontal lesions. It has five serotypes and many biotypes
based on differences in polysaccharide composition and can
be isolated in aggressive periodontitis and from active lesions
of the chronic periodontitis. This microorganism possesses
a great number of virulence factors, including leukotoxin
(forms pores in neutrophil granulocytes, monocytes, some
lymphocytes, which die due to the osmotic pressure),
collagenase (destruction of connective tissue), protease (able
to cleave IgG), endotoxin (lipopolysaccharide), fibroblast-
inhibition factor, factor inducing the bone resorption.
Porphyromonas gingivalis is a Gram-negative, nonmotile,
asaccarolytic rod-like obligate anaerobe which is related to
the initiation and progression of the periodontal destruction.
It possesses a capsule which protects against phagocytosis,
fimbriae (for adhesion) and vesicles, and produces a
number of virulence factors: proteases (for destruction of
immunoglobulins and the complement factors, and degradation
of host-cell collagenase inhibitors), collagenase, hemolysin
(heme-sequestering proteins), endotoxin, fatty acids, H2S,
NH4.
Tannerella forsythia (previously Bacteroides forsythus)
is a Gram-negative nonmotile rod-like obligate anaerobe
which is found in periodontal sites with active destruction as
well as with disease recurrence. This species produces some
proteolytic enzymes that can destroy immunoglobulins and
complement factors, and induces apoptotic cell death.
Prevotella intermedia is a short, round-ended nonmotile
gram-negative anaerobic pathogenic rod which is less virulent
and less proteolytic than P. gingivalis.
Treponema denticola is a Gram-negative motile anaerobe
related to periodontal lesions. It is found in patients with severe
periodontitis, rather than in patients with healthy periodontium
or gingivitis. This microorganism produces proteolytic
enzymes that can destroy immunoglobulins (IgA, IgM, IgG)
and complement factors.
Campylobacter rectus is a motile gram-negative anaerobic
short rod that produces leukotoxin.
According to Haffajee and Socransky (7), there is a
classification of the pathogenic bacteria according to the
strength of their relationship to periodontal disease: very
strong – A. actinomycetemcomitans, P. gingivalis; strong – T.
forsythia, P. intermedia, C. rectus, E. nodatum, Treponema
sp; moderate – S. intermedius, P. micros, P. nigrescens, E.
nucleatum, E. corrodens, Eubacterium sp.
Biotechnol. & Biotechnol. Eq. 27/2013/3

Suspect periodontopathogens and their association with periodontal diseases, clinical response to elimination, immune response
and virulent factors
Bacterial strain Association Elimination
A. actinomycetemcomitans +++ + +++
P. gingivalis +++ +++
P. intermedia ++ + +
T. forsythia ++ + +
T. denticola ++ +++
C. rectus ++ + ?
E. corrodens + +
P. micros + +
F. nucleatum + +
Selenomonas + ?
Microbiota in different periodontal diseases
Many different bacterial species live in the healthy gingival
sulcus and are present in different periodontal diseases. The
bacterial flora associated with healthy periodontal tissue
contains mainly Gram-positive microorganisms with a
dominance of Actinomyces and Streptococcus spp. Gram-
negative species and spirochetes may be also present in healthy
patients, although in low concentration. Most of the species
colonize several niches within the oral cavity and even in the
oropharyngeal area.
The studies on the relations between some specific
bacterial strains and periodontal diseases began in 1960
with the isolation of certain bacterial morphotypes from
healthy and diseased sites (14). The specificity of periodontal
microflora is strongly supported by the identification of
A. actinomycetemcomitans as a pathogen associated with
localized aggressive periodontitis (13, 21). Subsequent cross-
sectional and prolonged studies aimed to associate bacterial
species with health and disease. These investigations provide
enough evidence to relate a small group of periodontopathogens
with periodontitis and these bacteria have been defined as
key periopathogens: A. actinomycetemcomitans, Tannerella
forsythia and Porphyromonas gingivalis. They are strongly
related with the initiation of periodontal disease, disease
progression and unsuccessful periodontal therapy. Moderately
strong evidence has been accumulated for other bacteria
isolated from subgingival microbiota, including Prevotella
intermedia, Prevotella nigrescens, Campylobacter rectus,
Peptostreptococcus micros, Fusobacterium nucleatum,
Eubacterium nodatum and various spirochetes, such as
Treponema denticola, although their etiologic role is less
evident (14). Therefore periodontal disease may be regarded as
a polymicrobial infection (14).
The presence of periodontopathogens in the subgingival
flora is now considered as necessary but not sufficient to initiate
periodontal inflammation. The essential factor for the initiation
Biotechnol. & Biotechnol. Eq. 27/2013/3
TABLE 2
Immune response Virulent factors
leukotoxin, invasion
++ proteolytic, capsule
proteolytic
proteolytic
+ motile, proteolytic
motile, leukotoxin invasion
? -
+ proteolytic
+ proteolytic
? motile
and progression of periodontal disease is the increasing
of their proportions for effective damaging host response.
The currently accepted concept about the pathogenesis of
periodontitis considers three groups of factors that determine
whether active periodontitis will occur in a patient: 1) a
susceptible host, 2) presence of pathogenic species, 3) absence
or a small proportion of “beneficial” species. The significance
of the “beneficial” microorganisms in the disease progression
is currently intensely discussed. Some studies indicate that
in the subgingival flora there is balance between “beneficial”
and “pathogenic” species in inactive sites. This part of the
protection is probably due to the fact that certain species
control others through antagonistic bacterial interactions.
The importance of all identified periodontal bacteria in
different periodontal diseases is not well understood but it is
known that these bacteria can act in different ways: by passively
occupying the niches; by limiting the ability of a periodontal
pathogen to adhere to appropriate tissue surfaces; by enhancing
the vitality and growth of a pathogen; by enhancing the ability
of a pathogen to produce virulence factors; additionally, some
of the beneficial microorganisms can produce anti-periodontal
pathogen factors (Streptococcus sanguis produces hydrogen
peroxide – H2O2, which either directly or by host-enzyme
amplification can kill A. actinomycetemcomitans) (14).
There is epidemiological evidence that plaque-induced
gingivitis is a more prevalent periodontal disease, is more
commonly generalized, and is more severe in individuals with
poor oral hygiene. Development of this plaque-associated
gingival lesion has been largely investigated in a model system
of experimental gingivitis (4) and it has been found that
inflammatory features are related to emergence and growth of
Gram-negative rods and filaments in the dental biofilm, and
subsequently, of spirochetes and motile microorganisms. The
identified organisms are mainly Gram-negative, anaerobic
bacteria and include Streptococcus sanguis, S. mitis,
Fusobacterium spp., Actinomyces viscosus, and Veillonella
parvula. There is evidence that gingivitis-associated microflora
3757
is composed of approximately equal proportions of Gram-
positive (56 %) and Gram-negative (44 %) species; 59 % are
facultative anaerobes and 41  % obligate ones. Actinomyces
and Streptococcus species are dominant, and there is a very
small number of Gram-negative bacilli, obligate anaerobes
such as P. gingivalis and P. intermedia. Pregnancy-associated
gingivitis is accompanied by increase in steroid hormones
in the crevicular fluid and demonstrates modification in the
bacterial composition with a higher level of P. intermedia.
A number of experimental studies demonstrate that
the disease development can be rather related to selective
changes in the microbial composition of the dental plaque
than to additional plaque accumulation. Although individuals
may have stable gingival lesions for a long time, gingivitis
is recognized today as a precursor of chronic periodontitis.
Conceptually the progression of gingivitis to periodontitis may
be a result of bacterial composition shift (14).
Heterogenic subgingival flora has been found in chronic
periodontitis but the bacteria most cultivated in elevated
levels are P. gingivalis, T. forsythia, P. intermedia, C. rectus,
Eikenella corrodens, F. nucleatum, A. actinomycetemcomitans,
P. micros, Treponema denticola, and Eubacterium spp. Gram-
negative anaerobes and capnophiles are dominant; spirochetes
may be present. In the course of initiation and progression of
the inflammatory process, the subgingival bacteria increase
in numbers and invade the pocket epithelial cells and,
subsequently, the underlying tissues. It has been proven that
A. actinomycetemcomitans and P. gingivalis can invade the
gingival tissues and this fact is distinctive for the more severe
chronic periodontitis and aggressive periodontitis. Some
recent data demonstrate some herpes viruses present in the
periodontal pockets, e.g. Epstein-Barr virus-1 (EBV-1) and
human cytomegalovirus (HCMV) (14).
The microbiota in aggressive periodontitis is dominated
by Gram-negative capnophiles and anaerobic rods. In localized
aggressive periodontitis, A. actinomycetemcomitans is
constantly present; this microorganism may constitute up
to 90  % of the cultivable microflora but essential levels of
other microorganisms (Capnocytophaga, E. corrodens, P.
gingivalis) have been found in periodontal pockets. In other
forms of aggressive periodontitis, A. actinomycetemcomitans,
P. gingivalis, P. intermedia, C. rectus are dominant.
Нerpesviruses, including Epstein-Barr virus-1 (EBV-1) and
human cytomegalovirus (HCMV), can also be encountered.
A. actinomycetemcomitans is defined as a species typical for
localized juvenile periodontitis.
Refractory periodontitis microflora is associated
with the presence of F. nucleatum, P. intermedia, A.
actinomycetemcomitans, P. micros, and spirochetes, rather
than with P. gingivalis, T. forsythia and Candida spp. in the
dental biofilm (14).
Studies in the last few decades on the microflora of acute
periodontal diseases have secured the most solid evidence
about the periodontal infection specifics. A strong relation has
3758
been found between necrotic periodontal diseases and some
bacterial species. The microflora associated with necrotic-
ulcerative gingivitis and periodontitis contains Gram-negative
bacilli, obligate anaerobes such as F. nucleatum and P.
intermedia and spirochetes (Treponema spp. and Selenomonas
spp.).
Animal studies, cross-sectional and long-term investigations
in humans demonstrate that the microbiota associated with
peri-implant diseases (inflammatory process affecting the
peri-implant mucosa or all tissues around dental implants, with
supporting bone loss) is similar to that of periodontitis: with
a high proportion of anaerobic Gram-negative rods, motile
microorganisms and spirochetes. P. gingivalis, P. intermedia
and C. rectus are presented (20).
Conclusions
The key to successful periodontal therapy and maintenance
is elimination or reduction of pathogenic bacteria from
periodontal pockets and establishment of microbiota compatible
with periodontal health. On the other hand, the presence
of certain microorganisms in the periodontal pockets (P.
gingivalis, T. forsythia, P. intermedia, Treponema denticola, A.
actinomycetemcomitans, Candida spp.) allows the evolutional
potential of the periodontal disease to be estimated. Therefore,
the identification of subgingival pathogenic strains in gingivitis
and periodontitis could aid in the better differentiation of the
different periodontal diseases. That is why, it is important to
perform both qualitative and quantitative determination of
well-known periodontopathogens in the periodontal pockets.
In addition, prediction of the disease progression would allow
targeted preventive therapy.
Acknowledgements
This publication is part of a Grant project, scientific research,
Medical University of Sofia for 2012 (Agreement No. 1 of
17.07.2012).
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