Periodontal Microbiology in Latin America

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Periodontal microbiology in Latin America

ARTICLE in PERIODONTOLOGY 2000 FEBRUARY 2015
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Retrieved on: 28 July 2015
Periodontology 2000, Vol. 67, 2015, 5886

Printed in Singapore. All rights reserved
2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
PERIODONTOLOGY 2000
Periodontal microbiology in
Latin America
A D O L F O C O N T R E R A S , S A N D R A M. M O R E N O , A D R I A N A J A R A M I L L O , M E L I S S A
P E L A E Z , A N D R E S D U Q U E , J A V I E R E. B O T E R O & J R G E N S L O T S
Periodontal diseases affect a large proportion of the

worlds population and are considered an important
health issue in developed and developing countries
(150). The subgingival microbiota involved in the
onset and progression of periodontal disease has
been a major research topic for more than 40 years
(13, 48, 177, 181, 182, 190, 199). The latest research
based upon sequencing of the 16S rRNA gene has
identied 8001,000 bacterial and Archaea oral species, representing 19,000 phylotypes, and many of
the organisms are unculturable (96, 112, 149, 152,
207). In spite of the sizeable microbial diversity,
only about 50 bacterial species are closely related to
periodontal breakdown (35, 190). Evidence for bacterial specicity in periodontitis comes from culture
studies on microbial occurrence in health and disease and on virulence factors in in vitro and in vivo
study models. However, a major portion of the periodontal microbiota remains incompletely characterized, and the virulence and the immunobiology of
the newly identied bacteria are essentially unknown.
Bacteria that are present in elevated proportions in
disease-active periodontitis are designated major
pathogens or red complex bacteria; they include Aggregatibacter actinomycetemcomitans (formerly Actinobacillus actinomycetemcomitans), Porphyromonas
gingivalis, Tannerella forsythia and Treponema denticola (190). Other species may also contribute to periodontal destruction, such as Prevotella intermedia,
Prevotella nigrescens, Campylobacter rectus, Campylobacter gracilis, Parvimonas micra, Eubacterium species, Dialister pneumosintes and Dialister invisus. A
diverse group of gram-negative enteric rods, including Pseudomonas and Acinetobacter, beta-hemolytic
Streptococcus, Staphylococcus and Candida can also
inhabit periodontitis lesions (15, 27, 113, 177, 178),
and human viruses have been linked to severe types
of periodontal disease (40, 173) and peri-implantitis
58
(100). Alpha-hemolytic streptococci and actinomyces

species, bacteria possessing little or no periodontopathic potential, predominate in periodontal health
and after successful periodontal therapy (35, 122,
182). The periodontopathic signicance is not known
for the newly described bacteria Filifactor alocis,
Pseudoramibacter alactolyticus, Selenomonas noxia,
TM7 species, Deferribacter species, Solobacterium
moorei, Bacteriodetes species OT 272, Desulfobulbus
species OT 041, Shuttleworthia satelles, Granulicatella
adiacens, Mogibacterium timidum, Megasphaera species, Catonella species, Synergistes species cluster II,
Brevundimonas diminuta and Sphaerocytophaga
species (111).
The maintenance of a stable periodontium
depends on obtaining a balance between benecial
and pathogenic bacterial species and between protective and destructive host immune responses (13, 54).
Microbial dysbiosis refers to an alteration of this equilibrium and represents an important concept in the
understanding of the etiopathogenesis of periodontal
disease. A herpesviral infection of the periodontium
can upset local immunity and give rise to upgrowth of
bacterial pathogens and subsequently destructive
periodontal disease (172). Members of bacterial species/phylotypes can exhibit considerable genetic variations, and whole genomes of multiple strains of a
given species may only share about two-thirds of the
genetic material (60, 162, 192). Genetic variability
may explain why some phylogenetic lineages of bacterial species are closely associated with disease,
whereas other phylotypes of the same species can
persist in a host without causing notable disease (140,
166). A bacterial species, according to this concept,
can be view as a group of heterogeneous, but related,
microbial clones that demonstrate varying degrees of
pathogenic potential (49, 58, 92, 99, 110, 187). A
recent study proposed that genetic variations within
the oral microbiome can inuence the outcome of

periodontal treatment (165).
A major challenge in studying periodontal microbiology is the complexity that exists among individuals
in terms of socio-economic status, oral hygiene practices and other environmental determinants of periodontopathogenicity (78, 157). Difculties in
periodontal research even extend into such basic
concepts as denition and classication of periodontal diseases (10, 175). Nonetheless, with recent
advances in molecular diagnostics, it is hoped that
the more complete picture of the periodontal microbiota can lead to a better understanding of the initiation and progression of periodontitis and to more
cost-effective approaches to therapy.
This review focuses on studies from the past
20 years that have addressed the microbial composition of periodontitis in Latin America. We performed
a systematic search of periodontal microbiological
studies from Central and South America, using the
following databases: MEDLINE, LILACS (Latin America and Caribbean Literature in Health Science) and
BBO (Brazilian Library of Dentistry). The search keywords, in English, Portuguese or Spanish, were periodontal microbiology, chronic periodontal disease
microbiology, aggressive periodontitis microbiology, gingivitis microbiology and oral health microbiology. Other relevant publications were also
included when appropriate. All 22 countries in Central and South America were incorporated in the literature search.
Methodological issues
The prevalence of periodontal disease and specic
periodontal microbes in Latin America can be
difcult to assess due to variability in study design,
uncertain clinical diagnoses and vague criteria for
case selection (62, 145, 148). However, despite these
obstacles, it seems clear that a high proportion of
individuals in Latin America and in other developing
parts of the world exhibit particularly severe types of
periodontal disease (150). The occurrence of severe
periodontal disease is related to environmental factors, such as oral hygiene habits, socio-economic status and lack of access to proper therapy, and to
biological determinants, including genetic susceptibility, microbial composition and immunocompromising diseases/conditions.
A wide range of methodologies have been used in
the search for periodontal pathogens. Microbiological
methods in current use are microbial culture, ELISA,
immunouorescence, DNADNA hybridization, endpoint PCR, real-time PCR and next-generation

sequencing techniques (147). The new molecularbased diagnostic methods are capable of detecting
minute amounts of specic microorganisms. However, in the context of periodontal disease, only
pathogens that exceed a certain critical threshold
may be relevant for disease initiation and progression. This realization complicates the interpretation
of purely qualitative data obtained by exquisitely sensitive microbiological techniques.
Microbial sampling
Securing a representative sample of the disease-associated microbiota can be challenging, especially
when sampling deep periodontal pockets (30, 105).
The need for a large representative sample is particularly important when using microbiological techniques with high detection thresholds, such as
culture (176) and DNADNA checkerboard analysis
(183, 184), and is relevant to a lesser degree when
using technologies with low detection thresholds,
such as PCR (5, 30, 87).
The validity of a microbiological examination
depends also on the number of periodontal sites that
are sampled and the method of sampling (208). Periodontal pocket sampling by paper points seems to
yield more pathogens than sampling by curettes
(156). Saliva samples are easier to collect than subgingival samples (196), and the levels of periodontopathic microbes in saliva can potentially be used to screen
for the presence of periodontitis (163, 179). However,
the salivary level of an organism may not correlate
well with its subgingival level in individual patients
and thus may not always provide an accurate assessment of the periodontal disease status.
Microbial identication methods

Culture-based identication has a long tradition in
periodontal microbiology (171, 177). In contrast to
the other techniques described below, the recovery
by culture depends on the composition of the sample
transport medium and the length of the transport
time. The culture methods have gradually been
enhanced by the introduction of more procient
anaerobic handling and incubation procedures and
by improvements of nonselective and selective culture media. However, as culture-based techniques
depend heavily on the skills of the laboratory personnel and on equipment-related factors, as well as on
the methods employed for microbial identication,
59
Contreras et al.
culture results can differ signicantly among laboratories, even when using similar techniques (94, 109).
Moreover, results from recent molecular studies show
that more than 50% of the organisms in dental plaque
are nonculturable, despite using culture techniques
considered optimal by current standards (152).
The ELISA technique is probably the most commonly used immunological technique in periodontal
research. The ELISA technique has demonstrated the
presence of elevated levels of antibodies against specic pathogens in patients with advanced periodontitis (33). The uorescence in situ hybridization (FISH)
technology uses confocal microscopy and uorescence-labeled species-specic antibodies to study
biolms. There is some expectation of using the FISH
technology on subgingival samples to study difcultto-grow bacteria, microbial interdependency and biolm development (79).
The checkerboard hybridization technique uses
full-length genomic DNA as diagnostic probes (183,
184). The original version of the checkerboard technique included a panel of 40 microbial species, which
was later expanded to 80 species. The method has
been employed to study periodontal microbiology in
geographically and ethnically diverse populations (34,
68, 86, 206, 207). Although the specicity of some of
the genomic probes may be questioned, especially for
closely related species, the method can provide semiquantitative results of the target species, which is
unaffected by sample transport conditions, although
a prolonged storage time of plaque samples may
affect the outcome (109). Better standardization of
the checkerboard technique among laboratories
would provide more comparable results. The checkerboard technique used in a microarray format may
have a role in the study of bacterial virulence genes
(35).
Molecular diagnostics implies technologies that
measure nucleic acids (DNA and/or RNA) for clinical
applications. Molecular diagnostic technics are rapidly moving beyond the need for highly sophisticated
reference laboratories to low-resource and moderately complex laboratory settings. The PCR technology for nucleic acid testing can provide high
diagnostic specicity and sensitivity, and highly
reproducible results (5, 23, 31, 66). However, proper
primer design and amplication conditions are critical for data quality. PCR diagnostics may be used
independently of traditional culture-based methods
or complementing culture. Traditional PCR identies
the presence or absence of a microorganism, and
real-time PCR provides quantitative results (112). PCR
is widely used in periodontal microbiology to identify
60
specic microorganisms and their virulence traits (12,

64, 67, 88, 161). Loop mediated isothermal amplication (LAMP) is a point-of-care assay, which may be
used to screen for periodontal pathogens in large geographic areas and populations (124).
High-throughput genomic sequencing techniques,
such as pyrosequencing and illumina-sequencing, are
the latest developments in oral and medical microbiology. These next-generation DNA-sequencing technologies are cost-effective and can rapidly analyze
entire genomes with the resolution of a single-base
precision. The techniques enhance the possibilities of
addressing a variety of questions about the composition, structure and function of complex microbial
communities and their interaction with the host (34,
111, 124, 134, 145). The slightly older microarray technology, coupled with advanced computer-based data
analysis, may be used to study intricate bacteriahost
relationships (35, 147, 152), but does not have the
superior technical performance and cost advantage
of next-generation sequencing technologies. In the
foreseeable future, novel diagnostic tools will be able
to test simultaneously for both microbial and host
variables and provide better insights into the determinants of health and disease. The new diagnostic
methods may help to identify periodontal disease
activity, microbial composition and early inammatory changes, including connective tissue metabolites, as well as the response to periodontal therapy at
both the microbial and the host level.
Periodontal microbiology in Latin

America
Studies of periodontal microbiology in Latin America
have employed culture, ELISA, checkerboard DNA
DNA hybridization, conventional PCR and, more
recently, real-time PCR for bacterial and viral identication (23).
Brazil
Brazil is the leading Latin American country in
research on periodontal microbiology, and A. actinomycetemcomitans in severe periodontal disease has
been a particularly important topic of study (4245,
93, 97, 104, 194, 201) (Table 1). The prevalence of
A. actinomycetemcomitans in aggressive periodontitis
was found to range between 67% and 80%, with the
majority of isolates belonging to biotype X (7, 194). In
chronic periodontitis, the prevalence of A. actinomycetemcomitans periodontitis was 18% with a predomi-
Table 1. Studies on the subgingival microbiota in Brazil

Study type and Author/Year
Findings
Prevalence of Aggregatibacter actinomycetemcomitans

Aggressive periodontitis
Avila-Campos et al. (1995) (7)
77% with predominance of biotype X in 30 subjects with periodontitis
Tinoco et al. (1997) (194)
80% prevalence in adolescents, 39.5% in their family members, 35.3% in the

adolescents parents and 43.9% in their siblings
Chronic periodontitis
Cultures showed a signicant association between

A. actinomycetemcomitans and periodontitis, along with Tannerella
forsythia and Prevotella intermedia
Malheiros et al. (2004) (125)
18% prevalence with a predominance of biotype II
Jardim et al. (2006) (104)
68% prevalence in chronic periodontitis
Leukotoxic Aggregatibacter actinomycetemcomitans strains

Guazeli-Amin et al. (2000) (84)
Both leukotoxic and nonleukotoxic strains of A. actinomycetemcomitans can

be isolated from localized juvenile periodontitis and from patients with
AIDS/necrotizing ulcerative periodontitis, but A. actinomycetemcomitans
with high leukotoxic activity is more frequent in localized juvenile
periodontitis than in patients with AIDS/necrotizing ulcerative periodontitis
Rosalem-Junior et al. (2006) (161)
Deletion of a 530-bp sequence in the leukotoxin gene was observed in 16

(57.1%) of the 28 patients with generalized advanced periodontitis who were
positive for A. actinomycetemcomitans. The deletion was not detected in
individuals with periodontal health
Cortelli et al. (2005) (42)
A higher prevalence of leukotoxic strains of A. actinomycetemcomitans was

detected in Brazilian subjects with aggressive periodontitis and with the
deepest pockets (>6 mm)
Cortelli et al. (2003) (45)
There was a signicant correlation between highly leukotoxic

A. actinomycetemcomitans and aggressive periodontitis (v2 = 22.06).
However, a signicant correlation was not detected when analyzing
separate periodontal variables as pocket depth (v2 = 0.73),
plaque index (v2 = 0.35) and bleeding index (v2 = 0.09)
Gaetti-Jardim et al. (2008) (74)
Only one of 50 samples from Brazilian patients with periodontitis harbored

highly leukotoxic A. actinomycetemcomitans. Biotype II was the most
prevalent, and no correlation between biotypes and leukotoxic activity was
observed
Vieira et al. (2009) (202)
In Indians from the Umutina Reservation, Mato Grosso, all

A. actinomycetemcomitans strains were grouped as non-JP2 clones based on
the absence of a 530-bp deletion in the leukotoxin promoter gene
Studies on the red complex bacteria: Porphyromonas gingivalis, T. forsythia and Treponema denticola
Gaetti-Jardim et al. (1998) (75)
A higher frequency of red complex bacteria was found in patients with

periodontitis. Black-pigmented bacteria and Fusobacterium spp. were
common. An association was found between T. forsythia and P. gingivalis
Rodrigues et al. (1999) (158)
156 isolates of black-pigmented bacteria were recovered from 30 Brazilian

subjects. The most predominant bacteria were P. intermedia/Prevotella
nigrescens (93.9%), P. gingivalis (12.1%) and Prevotella spp. (6.1%)
Shibli et al. (2008) (167)
The microbiota of peri-implant disease revealed higher total colony counts

than in peri-implant healthy sites. Porphyromonas gingivalis, T. denticola and
T. forsythia were present in supra- and submucosal sites of peri-implantitis
Fernandes et al. (2010) (71)
Porphyromonas gingivalis and T. forsythia were more prevalent on the tongue

than on the cheek. Diverse niches of the oral cavity can harbor periodontopathic
bacteria
61
Contreras et al.
Table 1. (Continued)
Findings
Ide et al. (2000) (97)
66 Xingu Indians with periodontitis harbored P. gingivalis (53%),

Campylobacter rectus (31%), T. forsythia (25%), P. intermedia
(22%), A. actinomycetemcomitans (17%), T. denticola (17%) and Eikenella
corrodens (14%). Forty-nine Xingu Indians with gingivitis were positive for
P. gingivalis (20%), A. actinomycetemcomitans (10%) and E. corrodens (2%)
Missailidis et al. (2004) (136)
Porphyromonas gingivalis occurred in 89.4% of patients with periodontal attachment

loss, in 30% of patients with gingivitis and in 8.0% of healthy subjects. The most
prevalent P. gingivalis genotypes in patients with periodontitis were mAII
and mAIb. Genotype V was not detected in any of the samples and
genotype IV was the most common in patients with gingivitis
Teixeira et al. (2009) (189)
An association was found between P. gingivalis mAIV and disease severity

in smokers with chronic periodontitis
Trevilatto et al. (2002) (195)
Actinobacillus actinomycetemcomitans, P. gingivalis, T. forsythia and

T. denticola were detected in a family with aggressive periodontitis
Heller et al. (2012) (93)
Actinomyces gerensceriae, Actinomyces israelii, Eubacterium nodatum and

Propionibacterium acnes showed signicantly higher counts in generalized
aggressive periodontitis, whereas Capnocytophaga ochracea, Fusobacterium
periodonticum, Staphylococcus aureus and Veillonella parvula
predominated in patients with chronic periodontitis (adjusted P < 0.001)
da Silva-Boghossian et al. (2011) (52) Putative periodontal pathogens and nonoral bacteria, alone, or in association
with classical periodontopathogens, were strongly associated with
periodontitis
Bonifacio et al. (2011) (16)
A high frequency of periodontal pathogens was associated with the severity

of periodontal disease (P. gingivalis, T. forsythia,
A. actinomycetemcomitans, C. rectus and P. intermedia)
Periodontitis and systemic diseases

Human immunodeciency virus
Goncalves et al. (2004) (80)
The subgingival microbiota of HIV-positive patients with chronic

periodontitis included a high prevalence of the classical periodontal
pathogens present in non-HIV-infected individuals
Ramos et al. (2012) (155)
Tannerella forsythia was a prevalent periodontal species in HIV-positive patients.

E. corrodens, Dialister pneumosintes, Streptococcus intermedius and
C. rectus were also recovered from periodontal lesions of HIV-positive
patients
Diabetes mellitus
da Cruz et al. (2008) (51)
Diabetic and nondiabetic patients did not differ signicantly in microbial

composition (P. gingivalis, T. forsythia and A. actinomycetemcomitans)
Cardiovascular disease
Marcelino et al. (2010) (126)
A signicant association was found between the presence of P. gingivalis and

atheromas
Romito et al. (2004) (160)
In patients with heart transplants, subgingival samples yielded a prevalence

of 93% for P. intermedia, 66% for Fusobacterium nucleatum , 66% for
Parvimonas micra and 30% for C. rectus
Studies on other bacteria

Gebara et al. (2004) (77)
62
Helicobacter pylori was found in the saliva of three (10%) patients, in the
supragingival plaque in six (20%) patients and in the subgingival plaque in
eight (26.6%) patients. However, the organism was not recovered from the
dorsum of the tongue of any patient. The presence of H. pylori was similar
in patients with gingivitis and chronic periodontitis
Findings
Silva et al. (2010) (168)
Helicobacter pylori was detected in supragingival plaque, but not in subgingival

plaque, of individuals with periodontal disease and upper gastric diseases
Oliveira et al. (1998) (146)
Fusobacterium bacteriocins were found in periodontally diseased and healthy

subjects
Loberto et al. (2004) (117)
Staphylococcus spp. were recovered from subgingival sites of patients with

chronic periodontitis
Haffajee et al. (2004) (86)
Actinomyces naeslundii had a prevalence of 8.4% of genospecies 1 and 7.2%

of genospecies 2
Goncalves et al. (2007) (81)
Periodontal patients yielded Enterobacter cloacae (43.75%), Serratia

marcescens (31.25%), Klebsiella pneumoniae (6.25%), Enterobacter aerogenes
(6.25%), Pantoea agglomerans (6.25%) and Citrobacter freundii (6.25%)
Ferraro et al. (2007) (72)
Dialister pneumosintes was positively associated with periodontitis
Faveri et al. (2008) (67)
Selenomonas spp. and Streptococcus spp. were associated with generalized

aggressive periodontitis
Faveri et al. (2011) (66)
Peri-implantitis sites showed a signicantly higher prevalence of Archaea

than did peri-implant healthy sites and natural teeth
Matarazzo et al. (2011) (132)
The levels and proportions of Archaea were higher in generalized aggressive

periodontitis than in periodontal health. The predominant species was
Methanobrevibacter oralis
Souto et al. (2006) (185)
Predominant species in 600 subgingival samples from 14 subjects with

chronic periodontitis included Corynebacterium diphtheriae, Enterococcus
faecalis, S. aureus and Escherichia coli
Souto et al. (2008) (186)
Enterococcus faecalis was detected signicantly more often in saliva (40.5%) and in
subgingival samples (47.8%) of patients with periodontitis compared with
controls (14.6% and 17.1%, respectively)
Bacterial resistance studies

The minimal inhibitory concentration of mercuric chloride was 4 lg/ml
Feres et al. (2002) (70)
Metronidazole-resistant microorganisms: A. naeslundii 1, Streptococcus

constellatus, A. naeslundii 2, Streptococcus mitis, Streptococcus oralis,
Actinomyces odontolyticus and Streptococcus sanguis
Amoxicillin-resistant microorganisms: S. constellatus, P. nigrescens,
Eubacterium saburreum, A. naeslundii 1, Streptococcus oralis, Prevotella
melaninogenica and P. intermedia
Rodrigues et al. (2004) (159)
Tetracycline-resistant microorganisms: Streptococcus spp., V. parvula,

P. micra, P. intermedia, Gemella morbillorum and
A. actinomycetemcomitans
Clinical trials
Matarazzo et al. (2008) (131)
Evaluated the clinical and microbiological effects of scaling and root planing
alone or in combination with metronidazole (N = 15) or with
metronidazole + amoxicillin (N = 14) in smokers with chronic periodontitis.
The scaling and root planing + metronidazole + amoxicillin therapy
showed signicant reductions in the mean counts and proportions of
T. forsythia, P. gingivalis and T. denticola, and the considerable increase in
proportions of non-periodontopathic species
Feres et al. (2009) (69)
The clinical and microbiological effects were assessed of scaling and root
planing, alone, or combined with mechanical (professional plaque control)
or chemical (chlorhexidine rinsing) treatment of supragingival plaque in 60
patients with chronic periodontitis. Overall, the chlorhexidine rinse
treatment showed a signicant reduction in the proportions of red and
orange bacterial complexes
63
Contreras et al.
Findings
Haas et al. (2012) (85)
Azithromycin was ineffective in lowering the subgingival levels of important

putative periodontal pathogens in young subjects with aggressive
periodontitis compared with placebo
Novaes et al. (2012) (144)
Antimicrobial photodynamic therapy associated with scaling and root

planing may be benecial for the nonsurgical treatment of aggressive
periodontitis
nance of biotype II (125). Leukotoxic strains of A. actinomycetemcomitans (JP2 clone, serotype b) were a
common nding in aggressive periodontitis in South
America, with a particularly high prevalence in Brazil
(84, 161). Cortelli et al. (42) found a higher occurrence
of A. actinomycetemcomitans and of highly leukotoxic
strains in Brazil than in other South American countries, and linked highly leukotoxic strains to a greater
loss of periodontal attachment compared with minimally leukotoxic strains. Another study by Cortelli
et al. (45) recovered the highly leukotoxic genotype
from young subjects with aggressive periodontitis
and suggested a role for A. actinomycetemcomitans
leukotoxic strains in the development of the disease, and possibly also in chronic periodontitis (74).
Cortelli et al. (43, 44) proposed that the presence, in
saliva, of leukotoxic strains of A. actinomycetemcomitans was a useful marker of aggressive periodontitis
in children and adolescents. The association of the
JP2 clone with aggressive periodontitis has also been
documented outside Latin America (73, 8992, 111).
In a 2-year prospective study in Morocco, Haubek et
al. (91) found that adolescents, who were initially
free of periodontitis but harbored the JP2 clone, had
a signicantly higher relative risk (18.0; 95% CI: 7.8
41.2) for developing destructive periodontal disease
than did individuals infected with other types of
bacteria (3.0; 95% CI 1.37.1). Aggregatibacter actinomycetemcomitans serotype c demonstrates low pathogenicity compared with the JP2 clone (serotype b),
and individuals from Asia with little or no periodontal disease harbor predominantly strains of the c
serotype (90, 188, 193).
The highly leukotoxic JP2 clone seems to be particularly prominent in individuals of African descent,
which may account, in part, for the observed high
level of aggressive periodontitis in African-Americans
and in black Latin-American people (39, 4345). Different levels of the population with African ancestry
may explain the different prevalence of A. actinomycetemcomitans and of the JP2 clonal type in Brazil
(many people of African descent) (4345) and Chile
(few people of African descent) (76, 120). The
64
A. actinomycetemcomitans leukotoxin may directly

destroy polymorphonuclear leukocytes or may interact with host genetic-susceptibility factors (13, 54,
110, 118). The leukotoxin may be a particularly potent
virulence factor in young individuals, who may not
yet have developed effective immunity against the
organism (92, 134, 142). However, individuals colonized by A. actinomycetemcomitans clones other than
the JP2 clonal type can also develop periodontitis (6,
44, 74, 89, 137). Subgingival A. actinomycetemcomitans was detected in 26% of subjects with chronic
periodontitis from the Umutina Indian Reservation at
the Mato Grosso region of Brazil, and none of the
A. actinomycetemcomitans isolates was of the leukotoxic phenotype (202).
The cytolethal-distending toxin is another potential
virulence factor of A. actinomycetemcomitans. In a
study of 40 clinical isolates from Brazil, Kenya, Japan
and Sweden (64), the three cdt genes (ABC) were
detected in 34 of the 40 strains. One strain from
Kenya did not possess cdtA or cdtB genes and
expressed no toxic activity (64). Quantitative differences in cytotoxicity exist among cdt gene-containing
strains, but no clear relationship has been found
between cytolethal-distending toxin activity and
periodontal disease status.
The red complex of bacteria (P. gingivalis, T. forsythia and T. denticola) (181) is found at elevated levels
in Latin American patients with periodontitis (75, 76,
158) and peri-implantitis (167). Specically, black-pigmented bacteria of the Porphyromonas and Prevotella
species were detected in subjects with periodontitis
(58%), gingivitis (37%) and healthy periodontium
(15%) (42). Orange complex pathogens, such as Fusobacterium species (201), and other groups of bacteria,
such as Staphylococcus aureus (and even yeasts) may
also contribute to chronic periodontitis (27, 117).
Dental implants can harbor relatively unique bacteria, but may also share the microbiota of periodontitis
(71, 167). Faveri et al. (65) suggested that tongue dorsum acts as a reservoir for periodontopathic bacteria
and may be a source of microbial transmission and
recolonization of periodontal sites. Feres et al. (69)
recommended chlorhexidine oral rinse, along with

scaling and root planning, to reduce periodontal
pathogens in patients with periodontal disease.
Recent ndings from Argentina point to sodium
hypochlorite (dilute bleach) oral rinse as an effective
means of controlling dental biolm and gingival
inammation (57). The low-cost bleach therapy could
strengthen periodontal health efforts in poor rural
and urban areas with limited access to professional
dental care (174).
Most studies on periodontal microbiology in Latin
America have focused on the red complex of bacteria,
with a particular emphasis on P. gingivalis. This
microorganism is a major pathogen of chronic periodontitis and can also be involved in aggressive periodontitis (76, 113). Its average prevalence is 89% in
periodontitis patients, 30% in gingivitis patients and
8% in periodontally healthy subjects (136). Porphyromonas gingivalis strains that possess a vast array of
potent virulence factors are linked to severe periodontal disease, whereas P. gingivalis strains of reduced
pathogenicity may be associated with minimal disease.
The genetic polymorphism of the mA gene, which
encodes the subunit of P. gingivalis mbriae, has
attracted signicant research interest because of the
importance of mbriae in adherence to host tissues
(3). Six genetic types of mA (I, Ib, II, III, IV and V) have
been identied. Among these, type II, followed by type
IV, predominated in periodontitis patients from Japan,
China, Europe and a multiethnic population in Brazil,
whereas mAI strains predominantly inhabited
healthy carriers (2, 3, 12, 136, 139, 198, 209). The most
prevalent genotype in smokers was mAIV, and that
genotype was associated with clinical attachment loss
and deep pocket depths. FimAIV was detected in
69.6% of infected periodontal sites with no difference
between shallow and deep pockets (189).
Six capsular serotypes have been identied in the
P. gingivalis species, but a signicant proportion of
P. gingivalis isolates express little or no capsular
material. All six capsular serotypes of P. gingivalis,
except K1, were found in an Indonesian population,
but no particular serotype was related to the extent of
periodontal attachment loss (200). Likewise, studies in
the USA showed that antibody responses to all six serotypes were common in both chronic and aggressive
periodontitis (26). Virtually all (96%) subgingival isolates of P. gingivalis from an ethnically homogeneous
Swedish population were phenotypically homogeneous in biochemical tests, enzyme prole and antibiotic susceptibility, and belonged to somatic antigen
serotype A (53). To our knowledge, there are no reports
from Latin America on P. gingivalis capsular serotypes.
The periodontal microbiota of special patient categories has been studied in Brazil. Tannerella forsythia
was a prevalent periodontal species in HIV-positive
patients, and Eikenella corrodens, D. pneumosintes,
Streptococcus intermedius and C. rectus were also
common periodontal isolates from patients with HIV/
AIDS (80, 83, 155). Patients with diabetes mellitus
showed a periodontal microbiota that resembled that
of non-diabetic individuals (51). Enterococcus faecalis
was recovered from 42% of patients with periodontitis, and species of the Enterobacteriaceae family, such
as Enterobacter cloacae, Klebsiella pneumoniae, Serratia marcescens, Enterobacter aerogenes and Escherichia coli, and even Archaea organisms, may also inhabit
periodontitis lesions (15, 52, 66, 81, 115, 132, 185,
186). The presence of nonoral bacteria in periodontal
sites may be related to immunosuppression, malnutrition, poor sanitary conditions, or an indiscriminate
use of antibiotics.
Studies from Brazil have examined the microbial
relationship between periodontal disease and systemic
diseases. Helicobacter pylori, which is involved in gastric ulcer and gastric cancer, can be recovered from
saliva and from supragingival and subgingival plaque,
suggesting that the oral cavity can serve as a reservoir
for the organism (77, 168). Atheromatous plaque
obtained from coronary arteries of periodontitis
patients may contain periodontopathic bacterial DNA
(126, 160). Periodontitis patients with inammatory
bowel disease (Crohns disease) harbored higher levels
of periodontopathic bacteria than did control subjects
(25). It may be that the interaction between periodontal and systemic diseases is a two-way street that can
give rise to, respectively, nonoral and oral pathosis.
Bacterial resistance to antimicrobial agents has
been studied in Brazil. Avila-Campos et al. (7, 8)
showed that A. actinomycetemcomitans was sensitive
to mercuric chloride with a minimum inhibitory concentration of 4 mg/ml. Feres et al. (70) and Rodrigues
et al. (159) evaluated the resistance of periodontal
bacteria to metronidazole, amoxicillin and tetracycline. Actinomyces naeslundii type 2, Streptococcus
mitis, Actinomyces odontolyticus and Streptococcus
sanguinis were resistant to metronidazole. Prevotella
nigrescens, Eubacterium saburreum, Prevotella melaninogenica and P. intermedia were resistant to
amoxicillin. Actinomyces naeslundii type 1, Streptococcus constellatus and Streptococcus oralis were
resistant to both metronidazole and amoxicillin. Species that were resistant to amoxicillin were also resistant to tetracycline.
Clinical trials performed to compare different periodontal treatments have been conducted in Brazil.
65
Contreras et al.
Matarazzo et al. (131) studied the clinical and microbiological effects of scaling and root planing, used
alone or in combination with metronidazole, or in a
combined
metronidazole+amoxicillin
therapy.
Patients treated with scaling and root planing
together with the two antibiotics experienced a
reduction in the red and orange complexes of pathogens (131). A clinical trial by Novaes et al. (144) suggested that a combination of photodynamic therapy
and scaling and root planing constituted a promising
new approach to the nonsurgical treatment of aggressive periodontitis.
Colombia
The rst studies on periodontal infections in Colombia were performed by Jimenez and coworkers in
1975 and 1993, and reviewed in 2005 (106108)
(Table 2). These authors found that necrotizing ulcerative gingivitis was a precursor to noma (cancrum
oris), and that low socio-economic status, acute herpetic gingivostomatitis, measles, leukemia, malnutrition and poor oral hygiene were associated with
noma. Pathogenetic synergy between the major periodontal pathogens T. denticola and P. gingivalis, in
combination with cytomegalovirus, may also contribute to the development of necrotizing oral diseases
(37, 170, 172).
The microbiota of chronic and aggressive periodontitis has been a major research emphasis in
Colombia. Botero et al. (18) detected P. gingivalis,
T. forsythia and E. corrodens in higher proportions in
aggressive than in chronic periodontitis or in periodontal health (P < 0.05). Gram-negative enteric rods
were frequent inhabitants of periodontitis lesions
and, in particular, of aggressive periodontitis lesions
(P < 0.01) (18). Martinez-Pabon et al. (130) determined that T. denticola was closely related to chronic
periodontitis (P < 0.05), and they were able to identify
the organism in patients saliva (129). A study in
Bogota found that chronic and aggressive periodontitis lesions were associated with a high prevalence of
P. gingivalis, T. forsythia, P. intermedia/P. nigrescens,
C. rectus, Fusobacterium species and E. corrodens,
and a relatively low prevalence of P. micra, A. actinomycetemcomitans, D. pneumosintes and gram-negative enteric rods (133). A multicenter study of
periodontitis patients in the ve largest Colombian
cities found a high prevalence of P. gingivalis (72%),
T. forsythia (59%), C. rectus (58%), A. actinomycetemcomitans (24%) and gram-negative enteric rods (35%)
(113). Aggregatibacter actinomycetemcomitans was
increased in aggressive periodontitis compared to
66
chronic periodontitis (113). Tannerella forsythia,

C. rectus and E. corrodens had a relatively low
presence in periodontitis patients in the WestPacic and Central regions of Colombia, and
gram-negative enteric rods occurrred with increased
frequency in the Central region of Colombia
(P < 0.05) (113). Another study recovered P. gingivalis
and gram-negative enteric rods from subjects with
chronic periodontitis at frequencies of 67% and 26%,
respectively, and found the organisms to correlate
positively with increased probing depth, clinical
attachment loss and bleeding on probing (P < 0.001)
(4). However, a longitudinal study of untreated
periodontitis found that the gram-negative enteric
rods were not consistantly observed in many subjects
throughout a 1-month study period, indicating that
gram-negative enteric rods are frequently transient
microorganisms in subgingival sites (128). Apart from
the enteric rods, other unusual microorganisms can
also inhabit periodontal pockets, perhaps as superinfecting or transient occupants (15, 128).
The periodontal microbiota of special patient categories has also been an important research topic in
Colombia. In HIV-infected patients, Botero et al. (17)
detected a higher frequency of periodontopathic bacteria in HIV-negative periodontitis patients than in
HIV-positive periodontitis patients and in periodontally healthy subjects (P < 0.05), but HIV-positive
patients harbored higher levels of superinfecting
microorganisms, including Pseudomonas aeruginosa,
E. cloacae and K. pneumoniae (P < 0.05). Castrillon
et al. (32) studied the periodontal microbiota of diabetic patients. The red complex microorganisms
(P. gingivalis, T. forsythia and T. denticola) were
detected at a lower frequency in patients with diabetes, but A. actinomycetemcomitans occurred at an elevated level in diabetic patients (P < 0.05) (32).
Porphyromonas gingivalis was associated with periodontitis in nondiabetic patients (P < 0.05), and
A. actinomycetemcomitans was associated with periodontitis in diabetic patients (P < 0.05) (32). Contreras et al. (38) studied the periodontal microbiota in
women with pre-eclampsia and periodontitis. Most
patients with pre-eclampsia had chronic periodontitis
(odds ratio = 3.0; 95% condence interval: 1.914.87;
P < 0.001), and P. gingivalis, T. forsythia and E. corrodens were more prevalent in pre-eclamptic subjects
than in control subjects (P < 0.01).
A variety of special dental conditions has been studied in Colombia. Botero et al. (21) found that implants
with peri-implantitis harbored more P. gingivalis, P. intermedia/P. nigrescens and gram-negative
enteric rods than did control implants (P < 0.05) (21).
Table 2. Studies on the subgingival microbiota in Colombia

Author
Year Subjects
Technique
Findings
Jimenez & Baer

(106)
1975 28 patients with acute

necrotizing ulcerative
gingivitis
Clinical
evaluation
Acute necrotizing ulcerative gingivitis occurred

only in children from low socio-economic
groups and was associated with poor oral
hygiene and malnutrition. In the case of noma,
previous infection with a virus or an intestinal
parasite appeared to be important predisposing
factors
Jimenez et al.
(108)
2005 29 patients with necrotizing

ulcerative gingivitis, 7 with
necrotizing ulcerative
periodontitis and 9 with
noma
Clinical
evaluation
Malnutrition and poor oral hygiene favored

progression of the necrotic gingival lesion into
deeper periodontal tissue and other structures
of the oral cavity or of the facial tissues. The
population presented predisposing and/or
contributing factors such as acute herpetic
gingivostomatitis, measles and leukemia.
Necrotizing ulcerative gingivitis may progress to
ulcerative necrotizing stomatitis, necrotizing
ulcerative periodontitis and, nally, to noma
Botero et al. (18) 2007 68 patients with chronic

Microbiological There was a higher frequency of Porphyromonas
periodontitis, 12 with
culture, PCR
gingivalis, Tannerella forsythia and Eikenella
aggressive periodontitis and
corrodens in patients with aggressive
30 healthy subjects
periodontitis than in those with chronic
periodontitis and with healthy periodontium
(P < 0.05). Gram-negative enteric rods were more
frequent in patients with aggressive periodontitis
(P < 0.01)
Martinez-Pabon 2008 37 patients with chronic
PCR
et al. (130)
28 healthy subjects
The prevalence of Treponema denticola in

patients with chronic periodontitis was
signicantly higher than in periodontally
healthy subjects and in those with aggressive
periodontitis (P < 0.05)
Martinez-Pabon 2010 97 patients with chronic

PCR
et al. (129)
periodontitis and 51 healthy
subjects
Salivary carriage of T. denticola may be a risk

indicator for chronic periodontitis
Mayorga-Fayad
et al. (133)
Microbiological Parvimonas micra, Aggregatibacter

2007 84 patients with chronic
culture
actinomycetemcomitans, Dialister pneumosintes
and enteric rods (mostly Klebsielleae spp.)
were recovered. P. gingivalis was isolated
40 healthy subjects
more frequently than A. actinomycetemcomitans
from patients with aggressive
periodontitis
Lafaurie et al.
(113)
PCR
137 healthy subjects
Ardila et al. (4)

periodontitis
Frequency in periodontitis: P. gingivalis, 71.5%;

T. forsythia, 58.5%; Campylobacter rectus,
57.5%; A. actinomycetemcomitans, 23.6%; and
enteric rods, 34.5%. Porphyromonas gingivalis,
T. forsythia and C. rectus were the most prevalent
periodontopathic microorganisms in periodontitis
patients from large Colombian cities
Microbiological Porphyromonas gingivalis and gram-negative

culture
enteric rods correlated positively with probing
depth, clinical attachment level and bleeding on
probing (P < 0.0001)
67
Contreras et al.
Author
Year Subjects
Technique
Findings
Castrillon et al.
(32)
2013 60 patients with diabetes

mellitus and 62 nondiabetic
patients
PCR
The red complex microorganisms occurred at a

lower rate in patients with diabetes. The
detection rate of A. actinomycetemcomitans was
higher in patients with diabetes and
periodontitis than in systemically healthy
patients without periodontitis (P < 0.05).
Porphyromonas gingivalis was associated with
periodontitis in nondiabetic patients (P < 0.05)
Botero et al.
(21)
2005 16 implants with signs of

pocketing, 12 neighboring
teeth and 11 nonneighboring teeth, in 11
patients
Signicant correlations were found between

Clinical,
implants and neighboring teeth for gramradiographic
and anaerobic negative enteric rods (P = 0.023), and between
implants and non-neighboring teeth for
culture study
P. gingivalis (P = 0.042). The frequency of
detection of gram-negative enteric rods (75%)
and Prevotella intermedia/Prevotella nigrescens
(25%) was higher in peri-implant lesions
(P < 0.05). Porphyromonas gingivalis comprised
1.4% of total isolates in peri-implant lesions
Jaramillo et al.
(101)
2005 60 periodontal abscesses from Microbiological Periodontal abscesses showed Fusobacterium

54 patients with chronic
culture
spp. (75%), P. intermedia/P. nigrescens (60%),
periodontitis
P. gingivalis (51%) and
A. actinomycetemcomitans (30%). None of the
bacteria tested presented resistance to
azithromycin. An intermediate resistance was
found for tetracycline in two of 14 isolates of
P. intermedia/P. nigrescens and in three of four
isolates of A. actinomycetemcomitans. One of 11
isolates of P. gingivalis was resistant to
metronidazole. One isolate of
A. actinomycetemcomitans and two isolates of
P. intermedia/P. nigrescens were resistant to
amoxicillin
Jaramillo et al.
(102)
2013 192 patients with aggressive

periodontitis and 256 with
moderate periodontitis
PCR
Elevated levels of high-density lipoprotein (HDL)

and triglyceride were present in patients with
periodontitis. Serum IgG1 against P. gingivalis
was associated with HDL-35. Serum IgG1
against T. forsythia was associated with
triglyceride and serum IgG2.
Aggregatibacter actinomycetemcomitans
correlated with levels of HDL and HDL-35.
The presence of IgG1 against P. gingivalis and
A. actinomycetemcomitans correlated with
reduced HDL levels
Moreno et al.
(139)

gingivitis and 25 healthy
subjects
PCR
No difference among study groups was detected

in the distribution of the P. gingivalis mA
genotype. An association was found among
P. gingivalis, T. denticola and T. forsythia in
patients with periodontitis
Jaramillo et al. (101) studied the microbiology of periodontal abscesses and found a high prevalence of
Fusobacterium species (75%), P. intermedia/P. nigrescens (60%), P. gingivalis (51%) and A. actinomycetemcomitans (30%). Naranjo et al. (141) studied changes
in the periodontal microbiota following orthodontic
68
treatment. Orthodontic bracket placement caused

an increase in plaque index, gingival index and bleeding on probing (P < 0.05), and an increase in P. gingivalis, P. intermedia/P. nigrescens, T. forsythia, and
Fusobacterium species compared with controls
(P < 0.01). Superinfecting E. cloacae, Klebsiella oxytoca,
K. pneumoniae and Serratia marcescens were also

detected after bracket placement (141).
The systemic impact of periodontal disease was
studied by Lafaurie et al. (114), who evaluated the frequency of subgingival anaerobic and facultative bacteria in the bloodstream following scaling and root
planing of patients with severe generalized periodontitis. Eighty-one per cent of peripheral blood samples
were positive for bacteria immediately after scaling,
and the periodontopathic microorganisms most frequently identied were P. gingivalis and P. micra,
and organisms less often isolated were Campylobacter
species, E. corrodens, T. forsythia, Fusobacterium species and P. intermedia. In a similar study, Castillo
et al. (31) identied bacteria in peripheral blood after
scaling and root planing in 55% of periodontitis
patients; P. gingivalis and A. actinomycetemcomitans
were the periodontal pathogens most frequently
identied. Jaramillo et al. (102) studied the relationship between untreated periodontal disease and
low-grade systemic inammation and blood lipid
alteration. A high IgG1 level against P. gingivalis and
A. actinomycetemcomitans may correlate with a
reduced level of the anti-atherogenic high-density
lipoprotein (102).
Moreno et al. (139), in a recent study of P. gingivalis mA genotypes, found no differences in genotype
distribution among chronic periodontitis, gingivitis
and healthy periodontium. Microbial antibiotic resistance was determined by Jaramillo et al. (103) in isolates from patients with aggressive periodontitis and
chronic periodontitis and from periodontally healthy
subjects. Aggregatibacter actinomycetemcomitans was
resistant to metronidazole, amoxicillin and clindamycin, and P. intermedia/nigrescens and Enterobacteriaceae species were resistant to amoxicillin (103).
Finally, Ramirez et al. (154) found an increased level
of important cardiovascular markers and red complex
bacteria in patients with severe and moderate chronic
periodontitis.
Chile
Lopez et al. (121) studied the microbiota of chronic
periodontitis in Chilean patients using the checkerboard DNADNA hybridization technique (Table 3).
The main ndings were high proportions of the red
complex bacteria P. gingivalis, T. forsythia, and T. denticola, and variable levels of the periodontopathic
microorganisms C. rectus, F. nucleatum, P. micros and
Treponema socranskii (121). A study of aggressive
periodontitis found a low prevalence of Actinomyces
species, which are considered commensal organisms
in the subgingival area (119). Gajardo et al. (76)

determined the predominant periodontopathic
bacteria to be P. gingivalis, C. rectus, E. corrodens,
P. micra and Capnocytophaga species. Silva et al.
(169) compared the occurrence of A. actinomycetemcomitans, P. gingivalis and T. forsythia in progressive
and stable periodontitis, and found a higher percentage of P. gingivalis in disease-active sites (18%) than
in disease-inactive sites (2%).
Lopez et al. (123) studied the consortia of microorganisms associated with periodontitis in different
stages of the disease. Prevotella nigrescens, P. intermedia, P. gingivalis and T. forsythia were present at
high levels in subjects with periodontitis. One cluster
of organisms included T. forsythia, C. rectus, P. gingivalis, P. intermedia, P. nigrescens, P. micra and
T. denticola. Another cluster of organisms contained
Actinomyces oris, Capnocytophaga ochracea, E. corrodens, S. intermedius, S. noxia, S. oralis, S. sanguinis
and Veillonella parvula. Fusobacterium nucleatum
was assigned to both clusters. The personal cluster of
periodontal bacteria may be an important determinant of the outcome of periodontal therapy (165).
Lopez et al. (122) also evaluated the clinical and
microbiological effects of treating periodontitis
solely with metronidazole plus amoxicillin. They
found a marked reduction in the mean counts of
the red complex bacteria P. gingivalis, T. forsythia
and T. denticola for up to 12 months post-treatment
in both the antibiotic-treated group and the scaled
control group. Actinomyces counts increased
signicantly post-treatment. The authors made the
interesting observation that the antibiotic therapy
and periodontal scaling and root planing led to
similar improvements in clinical and microbiological
variables (122).
Mexico
The subgingival microbiota has been described in
patients from Mexico using the checkerboard DNA
DNA hybridization technique (Table 4). Consistent
with other studies, periodontitis patients presented
higher quantities of P. gingivalis, T. denticola, T. forsythia and A. actinomycetemcomitans than did periodontally healthy subjects (1, 206). No signicant
differences were observed in the detection level of 40
test species between generalized aggressive periodontitis and generalized chronic periodontitis. The bacterial species that were associated with periodontitis
were also detected in periodontally healthy subjects
(205, 206). Another study detected subgingival P. intermedia in 89%, and subgingival P. gingivalis in 58%,
69
Contreras et al.
Table 3. Studies on the subgingival microbiota in Chile

Author
Year Subjects
Technique
Findings
Lopez
Checkerboard DNADNA
et al. (121)
periodontitis from Chile and hybridization
the USA
Red complex and other periodontopathic

microorganisms such as Campylobacter
rectus, Fusobacterium nucleatum,
Parvimonas micra and Treponema
socranskii, as well as yellow complex
bacteria, were signicantly elevated in
Chilean subjects, whereas Actinomyces
spp. were higher in US subjects
Gajardo
2005 36 patients with aggressive
et al. (76)
periodontitis from Chile
Microbiological culture
Campylobacter rectus, Porphyromonas

gingivalis, Eikenella corrodens, P. micra
and Capnocytophaga spp. were predominant
in aggressive periodontitis lesions, but
only C. rectus was statistically associated
with periodontitis
Silva
et al. (169)
periodontitis from Chile
ELISA, anaerobe
microbiological culture
Higher RANKL, interleukin-1beta and

matrix metalloproteinase-13 activity
levels were observed in disease-active
sites (P 0.05). The proportion of
P. gingivalis, Aggregatibacter
actinomycetemcomitans and Tannerella
forsythia, and the number of CD4+ T cells,
were higher in disease-active than in
inactive periodontal sites
Lopez
et al. (122)
periodontitis
Clinical trial, Checkerboard Metronidazole plus amoxicillin or scaling

DNADNA hybridization
and root planing were given to patients
with periodontitis harboring high
percentages of Streptococcus gordonii,
A. actinomycetemcomitans, Eubacterium
nodatum, Fusobacterium periodonticum,
P. gingivalis, Treponema denticola and
T. socranskii. At 12 months posttreatment, changes in clinical and
microbiological parameters were similar
in subjects receiving systemic antibiotics
or scaling and root planing
Haffajee
2004 300 subjects from the USA,
et al. (86)
Sweden, Brazil and Chile
(total number of
samples=6036)
Checkerboard DNADNA
hybridization
70
Porphyromonas gingivalis, comprised adjusted

means of 7.5, 11.9, 1.6 and 6.6% of the
microbiota in subjects from Brazil, Chile,
Sweden and USA (P < 0.001), and mean
proportions of T. denticola were 6.7, 4.2,
0.8 and 2.3, respectively (P < 0.001).
Tannerella forsythia mean proportions
ranged from 6.2 to 8.5% and did not differ
signicantly among countries.
Actinomyces naeslundii genospecies 1
and 2 (8.4% and 7.2% respectively) and
Prevotella intermedia (6.5%) were
prominent species in Brazil; Prevotella
melaninogenica (6.4%) and Neisseria
mucosa (5.3%) were prominent in Chile;
A. naeslundii genospecies 2 (8.4%),
Capnocytophaga gingivalis (7.1%) and
P. micra (5.0%) were prominent in
Sweden; A. naeslundii genospecies 2
(7.5%), Prevotella intermedia (6.8%) and
Capnocytophaga gingivalis (6.1%) were
prominent in the USA
Author
Year Subjects
Herrera
et al. (94)
periodontitis
Technique
Findings
Anaerobic microbiological Aggregatibacter actinomycetemcomitans

culture
(19.4%), Prevotella intermedia (19.4%),
Tannerella forsythia (16.2%), Capnocytophaga
spp. (13.5%), P. micra (29.7%), E. corrodens
(34.3%), P. gingivalis (83.8%), Fusobacterium
spp. (63.9%) and superinfecting enterics
(17.6%) were detected in chronic
periodontitis of Chilean patients
of patients with periodontitis and rheumatoid arthritis (127). The same microorganisms were detected by
PCR in synovial uid of subjects with periodontitis
and rheumatoid arthritis (74% and 42% respectively),
but not by culture (127). A study using a multiplexPCR protocol found P. gingivalis in subjects with
chronic periodontitis (37%) as well as with a normal
periodontium (24%) (56).
Davila-Perez et al. (55) studied the distribution of
P. gingivalis mA genotypes in type 2 diabetic
patients with periodontitis and in nondiabetic
patients with and without periodontitis. The diabetic
patients harbored manly the mAI, II and III genotypes, the nondiabetic patients harbored the mAI, Ib
and II genotypes, and the periodontally healthy subjects harbored the mAI genotype (55).
Various countries
The periodontal microbiota has also been studied
in Argentina, the Dominican Republic, Guatemala,
Haiti, Panama and Venezuela (Table 5). In Argentina, A. actinomycetemcomitans, red complex bacteria and superinfecting organisms were prevalent in
patients with periodontitis (11, 28, 46, 47, 59, 138,
197). Bazzano et al. (11) found that scaling and
root planing reduced the occurrence of P. gingivalis, T. forsythia and T. denticola in deep periodontal
pockets and that no further loss of clinical attachment was observed for 12 months in 79% of the
treated sites. In the Dominican Republic, gram-negative enteric rods were prevalent in untreated periodontal sites (178). In Guatemala, Pomes et al.
(151) identied A. actinomycetemcomitans, yeast
and Entamoeba gingivalis as risk indicators of adolescent periodontitis. A high prevalence of A. actinomycetemcomitans was also demonstrated in
black Panamanian patients with localized juvenile
periodontitis (61). Two studies from Venezuela
described periodontal pathogens in patients with
gastritis and HIV infection (14, 24).
A few studies have compared the periodontal microbiota among different countries in Latin America
and abroad. Haffejee et al. (86), using checkerboard
DNADNA hybridization, found elevated levels of
P. gingivalis and T. denticola in Brazil and Chile compared with Sweden and the USA. Samples from Chileans of low socio-economic status harbored relatively
high proportions of Streptococcus gordonii, A. actinomycetemcomitans, Eubacterium nodatum, Fusobacterium periodonticum, P. gingivalis, T. denticola and
T. socranskii, and low percentages of A. naeslundii
and C. gracilis (86).
Herrera et al. (94) studied the microbiota of
patients with chronic periodontitis in Colombia, Chile
and Spain. Patients from Colombia revealed greater
severity of periodontitis, signicantly higher total bacterial colony counts, and increased levels of P. gingivalis and gram-negative enteric rods. Chilean
patients showed a high prevalence of P. micra and
E. corrodens and relatively low percentages of A. actinomycetemcomitans, P. intermedia, T. forsythia and
Capnocytophaga species. Spanish patients exhibited
increased levels of P. intermedia and did not yield
gram-negative enteric rods. The study suggested that
differences exist in the periodontopathic microbiota
of subjects in these three countries.
Aggressive periodontitis in adolescents (i.e. patients
with localized juvenile periodontitis) has been related
to A. actinomycetemcomitans and P. gingivalis. The
classic type of localized juvenile periodontitis starts at
the onset of puberty and involves rst molars and
incisors and exhibits very little dental plaque and virtually no gingivitis. This type of disease typically
harbors A. actinomycetemcomitans at a prevalence of
73100% (180). Another type of localized juvenile periodontitis shows the characteristic rst molar-incisor
tissue destruction, but also manifests distinct plaque
accumulation and gingivitis and tends to appear in
slightly older patients. This type of disease has been
studied in Jamaica (135) and Colombia (18, 22, 113)
and is predominated by P. gingivalis, which may
71
Contreras et al.
Table 4. Studies on the subgingival microbiota in Mexico

Author
Year Subjects
Technique
Almaguer-Flores
et al. (1)

periodontitis; 23 healthy
subjects
Checkerboard The presence of bacterial DNA for

DNADNA
Porphyromonas gingivalis, Tannerella
hybridization forsythia, Treponema denticola and
Aggregatibacter actinomycetemcomitans was
signicantly higher in subjects with chronic
periodontitis. Lower proportions of
Actinomyces spp. and microorganisms
included in the yellow complex were found
in patients with chronic periodontitis than
in healthy subjects
Ximenez-Fyvie
et al. (205)
2006 19 patients with generalized

aggressive periodontitis; 39
patients with generalized
chronic periodontitis; 19
healthy subjects
Checkerboard Patients with generalized aggressive

DNADNA
periodontitis and patients with generalized
hybridization chronic periodontitis harbored signicantly
higher levels of P. gingivalis, T. forsythia and
Prevotella nigrescens than did healthy
subjects. No signicant differences in any of
40 microbial species were detected between
untreated generalized aggressive
periodontitis and untreated generalized
Ximenez-Fyvie
et al. (206)

subjects
Checkerboard No signicant differences were detected in

DNADNA
the percentage of carriers of any of the
hybridization species tested. The proportions of
P. gingivalis, T. forsythia and red complex
species (P. gingivalis, T. forsythia and
T. denticola) were also signicantly higher in
patients with periodontitis
Martinez-Martinez
et al. (127)

periodontitis and
rheumatoid arthritis
PCR
De La Garza-Ramos 2008 65 patients with chronic

et al. (56)
subjects
Davila-Perez
et al. (55)
Subgingival plaque and synovial uid yielded

Prevotella intermedia (89.4% and 73.6%,
respectively) and P. gingivalis (57.8% and
42.1%, respectively). Culture did not show
any bacterial growth
Multiplex-PCR In untreated patients with periodontitis, 37%

yielded P. gingivalis, 17% yielded
Streptococcus intermedius, and 24.5%
yielded both species. Porphyromonas gingivalis
was detected in 23.5% of healthy volunteers,
whereas Streptococcus intermedius was not
detected in healthy individuals
PCR
2007 25 healthy subjects; 25
patients with chronic
periodontitis; 25 patients
with type 2 diabetes mellitus
and chronic periodontitis
occur as a superinfection or independently of an

A. actinomycetemcomitans infection. Studies in Chile
of patients with localized juvenile periodontitis
yielded A. actinomycetemcomitans at prevalences of
3944%, but also P. gingivalis and P. intermedia at
relatively high levels (119, 120).
72
Findings
Porphyromonas gingivalis genotypes were

analyzed. In healthy subjects, type I mA
was the most frequently detected individual
genotype (40%). In subjects with periodontitis,
the most frequently detected individual mA
genotype was Ib (20%). In periodontitis
patients with type 2 diabetes mellitus, the
most frequently detected genotypes were
types I and III mA (20%)
Human viruses and periodontal disease

Herpesviruses and other human viruses are often
acquired in childhood and can be identied in the
oral cavity of most adult individuals (Table 6). Herpesviruses employ various strategies to interact with
, Hait and Venezuela

Table 5. Studies on the subgingival microbiota in Argentina, Guatemala, Panama
Country and Author Year Subjects
Technique
Findings
Argentina
Canigia
et al. (28)
1999 45 patients with

Microbiological In 138 periodontitis sites, the most prevalent species

culture
were Prevotella intermedia/Prevotella nigrescens
(77%), followed by Aggregatibacter
actinomycetemcomitans (44%) and Parvimonas micra
(39%). Porphyromonas gingivalis was detected in 26%
of the sites, and was associated with a greater depth
of periodontal pockets. Healthy periodontal sites
yielded mainly viridans streptococci and
Neisseria spp. and the previously mentioned
species were not detected
Cuesta
et al. (46)

periodontal disease
Microbiological The prevalence of Staphylococcus spp. was 42.7% in

culture
periodontal pockets and 69.5% in the oral mucosa,
and the prevalence of Candida spp. was 25.6% in
periodontal pockets and 42.7% in the oral mucosa.
The coexistence of these species was 13.4% in
Staphylococcus aureus occurred in 13.4% of the
Candida albicans was detected in 76.2% of the
periodontal pockets and in 63% of oral mucosa
Cuesta
et al. (47)

periodontitis and
gingivitis
Microbiological Staphylococcus aureus was found in 10.8% (n = 11) of

culture and
periodontal pockets and in 19.6% (n = 20) of the
PCR
oral mucosa. This species may behave as
an opportunistic pathogen that can colonize
the gingival sulcus, nding an ecological niche
that provides optimal conditions for infection
Monetti
et al. (138)
2012 Six patients with

gingivitis, 7 with mild
chronic periodontitis,
23 with moderate
and 7 with severe
periodontitis
PCR
Prevotella denticola + P. intermedia (P = 0.04) and

P. intermedia + Tannerella forsythia (P = 0.02) were
associated with the presence of tumor necrosis
factor-alpha mRNA in 20% and 25% of subjects,
respectively. Porphyromonas gingivalis +
A. actinomycetemcomitans and
A. actinomycetemcomitans + T. forsythia were
associated with severe periodontal disease and
clinical attachment loss, respectively. The association
between the presence of P. intermedia and expression
levels of tumor necrosis factor-alpha was signicant
(P = 0.05)
Bazzano
et al. (11)
2012 44 sites from 11

patients with chronic
periodontitis
PCR
Porphyromonas gingivalis, T. forsythia and

Treponema denticola occurred at baseline in
66%, 55% and 41%, respectively, of the
test sites. Deep pockets correlated with T. forsythiaTreponema denticola (6.8 mm) and T. forsythiaT. denticola-P. intermedia (7 mm)
Usin
et al. (197)
2013 150 pregnant women
PCR
A high prevalence of P. gingivalis was found in

pregnant women, especially in combination with
T. forsythia and T. denticola. Older age was a risk
factor for moderate periodontitis (odds ratio = 4.92,
95% condence interval = 1.121.3, P = 0.0328). In
pregnant women, the presence of P. gingivalis was
found to increase the risk for showing a clinical
attachment level >5 mm and for moderate
periodontitis
73
Contreras et al.
Technique
Findings
Dominican Republic
Slots
et al. (178)

periodontitis
Microbiological Direct microscopic examination revealed that cocci

culture
and nonmotile organisms made up 85% of the total
organisms and spirochetes as little as 3%.
Nonselective culture showed gram-negative
organisms to constitute 53% of total isolates.
Fusobacterium nucleatum averaged 15%, blackpigmented anaerobes 7% and Parvimonas micra
10% of the cultivable microora. Enteric rods and
acinetobacter species were recovered from
16 patients and comprised 23% of the cultivable
ora. The most common enteric species were
Enterobacter cloacae, Klebsiella oxytoca and 7
other species
Dowset
et al. (59)
2002 114 subjects

from 45 families
Checkerboard Streptococcus sanguis, Actinomyces naeslundii

DNADNA
genospecies 2 and Fusobacterium nucleatum were
hybridization signicantly more common in deep periodontal
pockets, and A. naeslundii and P. micra were
signicantly more common in healthy periodontal
sites. Aggregatibacter actinomycetemcomitans was
not detected in any sample
Pomes
et al. (151)
2000 62 subjects, 1115 years Different tests

of age
for each pair
of sites
The prevalence of BANA-positive test results (red

bacteria indicator) was 77%, of
A. actinomycetemcomitans was 47%, of yeasts was
43% and of Entamoeba gingivalis was 21%. The risk
for severe gingival inammation and/or increased
probing depth was 1.5 and 5.2 times higher with a
positive BANA test or A. actinomycetemcomitans test.
No associations were found for yeasts and
E. gingivalis
2011 104 Haitian

adolescents
Quantitative
PCR
The frequency of Streptococcus mutans was 67.3% in

supragingival plaque samples, and
A. actinomycetemcomitans had a frequency of 85.1%
in subgingival plaque samples
Eisenmann
et al. (61)

localized juvenile
periodontitis and 10
with gingivitis
Microbiological Aggregatibacter actinomycetemcomitans was present

culture
in all localized juvenile periodontitis lesions studied
and was, on average, recovered in hundred-fold
higher numbers from localized juvenile
periodontitis lesions than from gingivitis lesions.
Capnocytophaga was only recovered in
approximately threefold higher numbers from
localized juvenile periodontitis than from gingivitis
Wiebe
et al. (204)
2003 18 individuals with

Kindler syndrome
PCR
Guatemala
Haiti
Psoter
et al. (153)
Panama
74
Kindler syndrome periodontitis yielded a prevalence

of 54% for T. denticola, 46% for P. nigrescens, 31% for
Dialister pneumosintes, 31% for P. gingivalis, 23%
for A. actinomycetemcomitans and 15% for
T. forsythia
Technique
Findings
Venezuela
Berroteran
et al. (14)
2002 32 patients with chronic PCR

gastritis and 20
healthy subjects
Helicobacter pylori was detected in antral samples

from 24 (75%) of 32 patients with chronic gastritis.
Helicobacter pylori was also detected in dental
plaque samples of 12 (37.5%) of the 32 patients.
Seven patients with chronic gastritis yielded
H. pylori in both antral and dental plaque samples.
There was no positive relationship between
H. pylori and periodontal parameters
Brito
et al. (24)
2008 32 HIV-positive and 16 PCR

HIV-negative patients
The mean values of plaque index, gingival index and

clinical attachment loss were similar for HIV-infected
patients undergoing or not receiving HAART therapy.
Linear gingival erythema was observed in HIVinfected patients, and necrotizing ulcerative
periodontitis occurred only in HIV-positive patients
without HAART therapy. Prevotella intermedia was
the most frequently recovered microorganism.
Porphyromonas gingivalis was observed only in one
(5%) HIV-positive patient receiving HAART therapy.
The periodontal indexes were not related with the
CD4+ count or viral load
Escalona
et al. (63)
2011 20 HIV-positive patients PCR

with periodontal
disease and 7 HIVnegative patients with
periodontal disease
Human papillomaviruses were detected in 46% of

HIV-positive patients under therapy. The
CD4 cell counts in the human papillomaviruspositive patients were not signicantly different from
those in the human papillomavirus-negative group.
Genotypes 6 and 11 were observed in the human
papillomavirus-positive samples, of which 4 (66.6%)
of six presented a co-infection with both types.
No signicant differences in the periodontal
conditions were observed between
patients with human papillomavirus + HIV infection
compared with patients infected with HIV only.
Papillomaviruses were detected only in the gingival
crevicular uid of HIV-positive patients under
HAART, independently of the periodontal condition
and subvert host defenses to ensure their continued

existence and propagation (173). Herpesvirus infections vary considerably in severity, which can range
from subclinical infection to encephalitis and cancer,
including carcinoma, lymphoma and sarcoma (179).
Genomes of herpes simplex virus type 1, human cytomegalovirus and EpsteinBarr virus have been
detected in periodontal pockets (22, 23, 40, 83), saliva
(179) and gingival immune cells (36, 41, 98), and the
three herpesviruses have been associated with
chronic periodontitis (22, 40), aggressive periodontitis
(203), acute necrotizing ulcerative gingivitis (37) and
periodontal abscesses (50, 164). Herpesviruses can
occasionally be present at low levels in healthy periodontal sites (22, 23, 82, 179).
In Colombia, Botero et al. (23) cultured cytomegalovirus from the gingival crevicular uid of patients
with periodontitis, but with a lower yield than that

obtained by molecular identication. Cytomegalovirus
was detected in patients with periodontitis (53%) and
in periodontally healthy subjects (18%) (P < 0.05),
and cytomegalovirus-positive sites showed a higher
occurrence of major periodontopathic bacteria and
more loss of periodontal attachment compared with
cytomegalovirus-negative sites (22). Botero et al. (19)
studied the in vitro effect of human cytomegalovirus
infection on gingival broblast expression of collagen I and III and matrix metalloproteinases 1 and 2.
Gingival broblasts infected with human cytomegalovirus exhibited reduced expression of mRNA for
collagens I and III (P < 0.05), and up-regulation of
mRNA expression for matrix metalloproteinases 1
and 2 (P < 0.05). Botero et al. (19) also found higher
expression of mRNA for collagens I and III in biop-
75
76
Brazil
Grande
et al. 2008 (82)
50 HIV-positive patients with chronic
periodontitis and 50 HIV-negative control
patients
40 patients with chronic periodontitis
14 patients with chronic periodontitis and 3

healthy subjects
Brazil
Colombia
Botero
et al. 2008 (19)
20 patients with chronic periodontitis, 10

patients with aggressive periodontitis and
22 healthy subjects
Imbronito
et al. 2008 (98)
Colombia
Botero
et al. 2007 (22)
37 patients with chronic periodontitis, 7

patients with aggressive periodontitis and 24
healthy subjects
30 patients with aggressive periodontitis
Colombia
Botero
et al. 2008 (23)
Number of subjects
Watanabe
Brazil
et al. 2007 (203)
Country
Author/year
Table 6. Subgingival detection of mammalian viruses in Latin America
Subgingival plaque:
HIV+: 72%
HIV : 48%
Saliva:
HIV+: 62%
HIV : 40%
Blood:
HIV+: 18%
HIV : 24%
Subgingival plaque: 45%

Saliva: 37.5%
Blood: 25%
Periodontitis sites: 57%

Gingivitis sites: 30%
EpsteinBarr virus-1
Virus
Subgingival plaque:
HIV+: 82%
HIV : 80%
Saliva:
HIV+: 72%
HIV : 80%
Blood:
HIV+: 68%
HIV : 84%
Subgingival plaque: 82.5%

Saliva: 75%
Blood: 82.5%
Prevalence: 6%
Gingival biopsies from human

cytomegalovirus-positive
individuals with periodontitis had
higher expression of mRNA for
collagens I and III compared with
biopsies from human
cytomegalovirus-negative
individuals
Chronic periodontitis: 60%

Aggressive periodontitis: 40%
Healthy patients: 18.1%
Periodontitis:
PCR: 79.5%
Real-time PCR: 47.7%
Culture: 2.3%
Healthy subjects:
PCR: 25%
Real-time PCR: 4.1%, Culture: 0%
Human cytomegalovirus
Subgingival plaque:
HIV+: 6%
HIV : 16%
Saliva:
HIV+: 18%
HIV : 24%
Blood:
HIV+: 6%
HIV : 8%
Herpes simplex virus type 1
Contreras et al.
46 patients with chronic periodontitis and

type 2 diabetes
Brazil
Venezuela 20 HIV-positive patients with chronic

periodontitis, 7 HIV-negative patients with
chronic periodontitis and 7 HIV-negative
subjects with healthy periodontium
Casarin
et al. 2010 (29)
Escalona
et al. 2011 (63)
27 HIV-positive patients with chronic

periodontitis and 23 HIV-positive patients
with gingivitis
50 patients with chronic periodontitis and 50

healthy subjects
Brazil
Grande
et al. 2011 (83)
Number of subjects
Nishiyama
Brazil
et al. 2008 (143)
Country
Author/year
Subgingival plaque:
Periodontitis: 3.7%
Gingivitis: 8.7%
Saliva:
Periodontitis: 14.8%
Gingivitis: 17.4%
Blood:
Periodontitis: 0%
Gingivitis: 13%
Subgingival plaque:
Periodontitis: 74%
Gingivitis: 91.3%
Saliva:
Gingivitis: 65.2%
Blood:
Gingivitis: 60%
Chronic periodontitis: 3.4%

Healthy periodontium: 0%
Herpes simplex virus type 1
Human cytomegalovirus
Glycemic control did not inuence

A higher frequency of
the frequency of human
EpsteinBarr virus in
cytomegalovirus
shallow periodontal
pockets of patients with
poorly controlled diabetes
Subgingival plaque:
Gingivitis: 78.3%
Saliva:
Gingivitis: 52.2%
Blood:
Periodontitis: 22%
Gingivitis: 13%
EpsteinBarr virus-1
Virus
77
Contreras et al.
sies from cytomegalovirus-positive individuals with

periodontitis than in biopsies from cytomegalovirusnegative patients with periodontitis. The ability of
cytomegalovirus to upregulate the expression of
mRNA for collagens and metalloproteinases may
contribute to the development of periodontitis.
Other pathways by which herpesviruses may cause
periodontitis include direct cytopathic effects on
broblasts, keratinocytes and other types of cells
(19, 20, 40, 83) and synergistic pathogenetic interactions with periodontopathic bacteria (22, 172, 179).
In Brazil, Watanabe et al. (203) detected Epstein
Barr virus-1 in 57% of sites with aggressive periodontitis and in 30% of sites with gingivitis; the relative risk
for periodontitis was 3.05 with a condence interval
of 1.436.47. Cytomegalovirus was found in 6% of the
study individuals (203). Imbronito et al. (98) identied EpsteinBarr virus-1 in 45% of chronic periodontitis samples, 38% of salivary samples and 25% of
peripheral blood samples. Cytomegalovirus was
detected in 82% of the periodontitis and blood samples and in 75% of the saliva samples (98). Grande
et al. (82), in a study of HIV-infected subjects, found
cytomegalovirus in 82% of periodontitis sites of HIVpositive and in 80% of periodontitis sites of HIV-negative patients, and EpsteinBarr virus-1 in 72% of periodontitis sites of HIV-positive and in 48% of
periodontitis sites of HIV-negative patients. In
another study of HIV, Grande et al. (83) detected
cytomegalovirus and EpsteinBarr virus-1 in, respectively, 74% and 70% of periodontitis samples, in 77%
and 81% of salivary samples, and in 74% and 22% of
peripheral blood samples. Herpes simplex-1 virus
occurred with a frequency of 4% in periodontitis samples and 15% in salivary samples, and was not
detected in blood samples (83). Nishiyama et al. (143)
also found a low occurrence (3%) of herpes simplex-1
virus in periodontitis lesions. Casarin et al. (29) studied the relationship between herpesviruses and periodontal status in patients with type 2 diabetes and
found EpsteinBarr virus in 81% of shallow periodontal sites of patients with poor glycemic control and in
43% of shallow periodontal sites of patients with good
glycemic
control
(P = 0.05).
Cytomegalovirus
occurred in 3343% of shallow periodontal sites, with
no preference for poorly controlled diabetes (29). The
elevated prevalence of herpesviruses in periodontal
sites of patients with type 2 diabetes may partly
explain the elevated risk of these patients for developing periodontitis.
Human viruses other than herpesviruses can also
reside in the periodontium. Escalona et al. (63) in
Venezuela studied the presence of human papilloma-
78
virus in periodontal pocket samples of HIV-infected

patients. Papillomavirus was detected in 46% of HIVpositive patients receiving anti-retroviral treatment,
but was not found in HIV-seronegative patients (63).
Horewicz et al. (95) did not detect the oncogenic papillomavirus type 16 in samples from chronic periodontitis, gingivitis or healthy periodontium. Lins
et al. (116) found that individuals orally infected with
the human T-lymphotropic virus type I were more
affected by periodontitis than were noninfected
controls.
The future of periodontal

microbiology in Latin America
A healthy periodontium is important for overall oral
health, but the increasing evidence that periodontitis
also can have systemic consequences raises treatment of periodontal disease to a new level of importance (38, 102, 154, 197). Periodontal disease has a
global distribution, but is particularly prevalent and
severe in low-income individuals. Many periodontitis
patients of Central and South America do not receive
adequate periodontal therapy because of economic
and social constrains and a scarcity of affordable dental services. There is a need to nd safe and effective
methods to control periodontal infections in Latin
American populations with limited access to professional dental care.
Knowledge of the periodontal microbiota is critical
for implementing a successful periodontal therapy.
Periodontal therapy aims to control periodontopathic
microorganisms by means of mechanical pocket
debridement, periodontal pocket irrigation with
potent antiseptics, treatment of advanced disease
with systemic antibiotics and attention to proper selfcare. The worldwide increase in antibiotic-resistant
bacteria and the high costs of new, effective antibiotics have created interest in the use of inexpensive
antiseptics to combat periodontal infections. Antiseptics are broad-spectrum microbicidal agents that are
applied topically onto living tissue to prevent or treat
clinical infections caused by bacteria, yeasts and
viruses (174, 175). Unlike antibiotics, antiseptics
destroy periodontal bacteria and viruses in a nondiscriminative manner and can cover the entire spectrum of traditional periodontal pathogens, gramnegative enteric rods and superinfecting organisms
(190, 191). Low-cost periodontal therapy, based predominantly on antiseptic agents, may help to meet
the unmet treatment needs of large impoverished
populations in Latin America (57, 174, 175).
Although research in periodontal microbiology is

steadily increasing in Central and South America,
several research issues in periodontology remain
unresolved and merit attention. It is critical to establish a clear denition of periodontal diseases and
proper periodontal diagnoses to make studies comparable. Studies that compare the microbiology of
periodontal disease in various socio-economic groups
have yet to be undertaken in most Latin American
countries. Microbiological risk factors for periodontal
disease and effective periodontal treatments remain
to be identied for immunocompromised and noncompromised patients. And nally, the growing realization that periodontal infections may give rise to
systemic illness, perhaps especially in immunocompromised individuals, ought to be a high-priority
research topic. Signicant progress in molecular
microbiology has made such studies possible, even in
low-budget laboratories. Continued research in periodontal microbiology is poised to generate discoveries that can form the basis for more effective
approaches to the prevention and treatment of
destructive periodontal disease in Latin America.
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Periodontal microbiology in Latin America

Universidad del Valle (Colombia)

Pontificia Universidad Javeriana - Cali

95 PUBLICATIONS 2,104 CITATIONS

Javier Enrique Botero

Universidad del Valle (Colombia)

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24 PUBLICATIONS 289 CITATIONS

Available from: Adriana Jaramillo

Periodontology 2000, Vol. 67, 2015, 5886

Periodontal diseases affect a large proportion of the

(100). Alpha-hemolytic streptococci and actinomyces

Periodontal microbiology in Latin America

the oral microbiome can inuence the outcome of

immunouorescence, DNADNA hybridization, endpoint PCR, real-time PCR and next-generation

Microbial identication methods

specic microorganisms and their virulence traits (12,

Periodontal microbiology in Latin

Periodontal microbiology in Latin America

Table 1. Studies on the subgingival microbiota in Brazil

Prevalence of Aggregatibacter actinomycetemcomitans

77% with predominance of biotype X in 30 subjects with periodontitis

Tinoco et al. (1997) (194)

80% prevalence in adolescents, 39.5% in their family members, 35.3% in the

Cultures showed a signicant association between

Malheiros et al. (2004) (125)

18% prevalence with a predominance of biotype II

Jardim et al. (2006) (104)

68% prevalence in chronic periodontitis

Leukotoxic Aggregatibacter actinomycetemcomitans strains

Both leukotoxic and nonleukotoxic strains of A. actinomycetemcomitans can

Rosalem-Junior et al. (2006) (161)

Deletion of a 530-bp sequence in the leukotoxin gene was observed in 16

Cortelli et al. (2005) (42)

A higher prevalence of leukotoxic strains of A. actinomycetemcomitans was

Cortelli et al. (2003) (45)

There was a signicant correlation between highly leukotoxic

Gaetti-Jardim et al. (2008) (74)

Only one of 50 samples from Brazilian patients with periodontitis harbored

Vieira et al. (2009) (202)

In Indians from the Umutina Reservation, Mato Grosso, all

A higher frequency of red complex bacteria was found in patients with

Rodrigues et al. (1999) (158)

156 isolates of black-pigmented bacteria were recovered from 30 Brazilian

Shibli et al. (2008) (167)

The microbiota of peri-implant disease revealed higher total colony counts

Fernandes et al. (2010) (71)

Porphyromonas gingivalis and T. forsythia were more prevalent on the tongue

Ide et al. (2000) (97)

66 Xingu Indians with periodontitis harbored P. gingivalis (53%),

Missailidis et al. (2004) (136)

Porphyromonas gingivalis occurred in 89.4% of patients with periodontal attachment

Teixeira et al. (2009) (189)

An association was found between P. gingivalis mAIV and disease severity

Trevilatto et al. (2002) (195)

Actinobacillus actinomycetemcomitans, P. gingivalis, T. forsythia and

Heller et al. (2012) (93)

Actinomyces gerensceriae, Actinomyces israelii, Eubacterium nodatum and

A high frequency of periodontal pathogens was associated with the severity

Periodontitis and systemic diseases

The subgingival microbiota of HIV-positive patients with chronic

Ramos et al. (2012) (155)

Tannerella forsythia was a prevalent periodontal species in HIV-positive patients.