periodontal microbiology in latin america

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Periodontal microbiology inLatin AmericaADOLFO CONTRERAS, SANDRA M. MORENO, ADRIANA JARAMILLO, MELISSAPELAEZ, ANDRES DUQUE, JAVIER E. BOTERO & JRGEN SLOTS

Periodontal diseases affect a large proportion of theworlds population and are considered an importanthealth issue in developed and developing countries(150). The subgingival microbiota involved in theonset and progression of periodontal disease hasbeen a major research topic for more than 40 years(13, 48, 177, 181, 182, 190, 199). The latest researchbased upon sequencing of the 16S rRNA gene hasidentied 8001,000 bacterial and Archaea oral spe-cies, representing 19,000 phylotypes, and many ofthe organisms are unculturable (96, 112, 149, 152,207). In spite of the sizeable microbial diversity,only about 50 bacterial species are closely related toperiodontal breakdown (35, 190). Evidence for bac-terial specicity in periodontitis comes from culturestudies on microbial occurrence in health and dis-ease and on virulence factors in in vitro and in vivostudy models. However, a major portion of the peri-odontal microbiota remains incompletely character-ized, and the virulence and the immunobiology ofthe newly identied bacteria are essentially unknown.Bacteria that are present in elevated proportions in

disease-active periodontitis are designated majorpathogens or red complex bacteria; they include Ag-gregatibacter actinomycetemcomitans (formerly Acti-nobacillus actinomycetemcomitans), Porphyromonasgingivalis, Tannerella forsythia and Treponema denti-cola (190). Other species may also contribute to peri-odontal destruction, such as Prevotella intermedia,Prevotella nigrescens, Campylobacter rectus, Campylo-bacter gracilis, Parvimonas micra, Eubacterium spe-cies, Dialister pneumosintes and Dialister invisus. Adiverse group of gram-negative enteric rods, includ-ing Pseudomonas and Acinetobacter, beta-hemolyticStreptococcus, Staphylococcus and Candida can alsoinhabit periodontitis lesions (15, 27, 113, 177, 178),and human viruses have been linked to severe typesof periodontal disease (40, 173) and peri-implantitis

(100). Alpha-hemolytic streptococci and actinomycesspecies, bacteria possessing little or no periodonto-pathic potential, predominate in periodontal healthand after successful periodontal therapy (35, 122,182). The periodontopathic signicance is not knownfor the newly described bacteria Filifactor alocis,Pseudoramibacter alactolyticus, Selenomonas noxia,TM7 species, Deferribacter species, Solobacteriummoorei, Bacteriodetes species OT 272, Desulfobulbusspecies OT 041, Shuttleworthia satelles, Granulicatellaadiacens, Mogibacterium timidum, Megasphaera spe-cies, Catonella species, Synergistes species cluster II,Brevundimonas diminuta and Sphaerocytophagaspecies (111).The maintenance of a stable periodontium

depends on obtaining a balance between benecialand pathogenic bacterial species and between protec-tive and destructive host immune responses (13, 54).Microbial dysbiosis refers to an alteration of this equi-librium and represents an important concept in theunderstanding of the etiopathogenesis of periodontaldisease. A herpesviral infection of the periodontiumcan upset local immunity and give rise to upgrowth ofbacterial pathogens and subsequently destructiveperiodontal disease (172). Members of bacterial spe-cies/phylotypes can exhibit considerable genetic vari-ations, and whole genomes of multiple strains of agiven species may only share about two-thirds of thegenetic material (60, 162, 192). Genetic variabilitymay explain why some phylogenetic lineages of bac-terial species are closely associated with disease,whereas other phylotypes of the same species canpersist 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 ofpathogenic potential (49, 58, 92, 99, 110, 187). Arecent study proposed that genetic variations within

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Periodontology 2000, Vol. 67, 2015, 5886 2014 John Wiley & Sons A/S. Published by John Wiley & Sons LtdPrinted in Singapore. All rights reserved PERIODONTOLOGY 2000

the oral microbiome can inuence the outcome ofperiodontal treatment (165).A major challenge in studying periodontal microbi-

ology is the complexity that exists among individualsin terms of socio-economic status, oral hygiene prac-tices and other environmental determinants of peri-odontopathogenicity (78, 157). Difculties inperiodontal research even extend into such basicconcepts as denition and classication of periodon-tal diseases (10, 175). Nonetheless, with recentadvances in molecular diagnostics, it is hoped thatthe more complete picture of the periodontal micro-biota can lead to a better understanding of the initia-tion and progression of periodontitis and to morecost-effective approaches to therapy.This review focuses on studies from the past

20 years that have addressed the microbial composi-tion of periodontitis in Latin America. We performeda systematic search of periodontal microbiologicalstudies from Central and South America, using thefollowing databases: MEDLINE, LILACS (Latin Amer-ica and Caribbean Literature in Health Science) andBBO (Brazilian Library of Dentistry). The search key-words, in English, Portuguese or Spanish, were peri-odontal microbiology, chronic periodontal diseasemicrobiology, aggressive periodontitis microbiol-ogy, gingivitis microbiology and oral health micro-biology. Other relevant publications were alsoincluded when appropriate. All 22 countries in Cen-tral and South America were incorporated in the liter-ature search.

Methodological issues

The prevalence of periodontal disease and specicperiodontal microbes in Latin America can bedifcult to assess due to variability in study design,uncertain clinical diagnoses and vague criteria forcase selection (62, 145, 148). However, despite theseobstacles, it seems clear that a high proportion ofindividuals in Latin America and in other developingparts of the world exhibit particularly severe types ofperiodontal disease (150). The occurrence of severeperiodontal disease is related to environmental fac-tors, such as oral hygiene habits, socio-economic sta-tus and lack of access to proper therapy, and tobiological determinants, including genetic suscepti-bility, microbial composition and immunocompro-mising diseases/conditions.A wide range of methodologies have been used in

the search for periodontal pathogens. Microbiologicalmethods in current use are microbial culture, ELISA,

immunouorescence, DNADNA hybridization, end-point PCR, real-time PCR and next-generationsequencing techniques (147). The new molecular-based diagnostic methods are capable of detectingminute amounts of specic microorganisms. How-ever, in the context of periodontal disease, onlypathogens that exceed a certain critical thresholdmay be relevant for disease initiation and progres-sion. This realization complicates the interpretationof purely qualitative data obtained by exquisitely sen-sitive microbiological techniques.

Microbial sampling

Securing a representative sample of the disease-asso-ciated microbiota can be challenging, especiallywhen sampling deep periodontal pockets (30, 105).The need for a large representative sample is particu-larly important when using microbiological tech-niques with high detection thresholds, such asculture (176) and DNADNA checkerboard analysis(183, 184), and is relevant to a lesser degree whenusing 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 thatare sampled and the method of sampling (208). Peri-odontal pocket sampling by paper points seems toyield more pathogens than sampling by curettes(156). Saliva samples are easier to collect than subgin-gival samples (196), and the levels of periodontopath-ic microbes in saliva can potentially be used to screenfor the presence of periodontitis (163, 179). However,the salivary level of an organism may not correlatewell with its subgingival level in individual patientsand thus may not always provide an accurate assess-ment of the periodontal disease status.

Microbial identication methods

Culture-based identication has a long tradition inperiodontal microbiology (171, 177). In contrast tothe other techniques described below, the recoveryby culture depends on the composition of the sampletransport medium and the length of the transporttime. The culture methods have gradually beenenhanced by the introduction of more procientanaerobic handling and incubation procedures andby improvements of nonselective and selective cul-ture media. However, as culture-based techniquesdepend heavily on the skills of the laboratory person-nel and on equipment-related factors, as well as onthe methods employed for microbial identication,

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culture results can differ signicantly among labora-tories, even when using similar techniques (94, 109).Moreover, results from recent molecular studies showthat more than 50% of the organisms in dental plaqueare nonculturable, despite using culture techniquesconsidered optimal by current standards (152).The ELISA technique is probably the most com-

monly used immunological technique in periodontalresearch. The ELISA technique has demonstrated thepresence of elevated levels of antibodies against spe-cic pathogens in patients with advanced periodonti-tis (33). The uorescence in situ hybridization (FISH)technology uses confocal microscopy and uores-cence-labeled species-specic antibodies to studybiolms. There is some expectation of using the FISHtechnology on subgingival samples to study difcult-to-grow bacteria, microbial interdependency and bio-lm development (79).The checkerboard hybridization technique uses

full-length genomic DNA as diagnostic probes (183,184). The original version of the checkerboard tech-nique included a panel of 40 microbial species, whichwas later expanded to 80 species. The method hasbeen employed to study periodontal microbiology ingeographically and ethnically diverse populations (34,68, 86, 206, 207). Although the specicity of some ofthe genomic probes may be questioned, especially forclosely related species, the method can provide semi-quantitative results of the target species, which isunaffected by sample transport conditions, althougha prolonged storage time of plaque samples mayaffect the outcome (109). Better standardization ofthe checkerboard technique among laboratorieswould provide more comparable results. The check-erboard technique used in a microarray format mayhave a role in the study of bacterial virulence genes(35).Molecular diagnostics implies technologies that

measure nucleic acids (DNA and/or RNA) for clinicalapplications. Molecular diagnostic technics are rap-idly moving beyond the need for highly sophisticatedreference laboratories to low-resource and moder-ately complex laboratory settings. The PCR technol-ogy for nucleic acid testing can provide highdiagnostic specicity and sensitivity, and highlyreproducible results (5, 23, 31, 66). However, properprimer design and amplication conditions are criti-cal for data quality. PCR diagnostics may be usedindependently of traditional culture-based methodsor complementing culture. Traditional PCR identiesthe presence or absence of a microorganism, andreal-time PCR provides quantitative results (112). PCRis widely used in periodontal microbiology to identify

specic microorganisms and their virulence traits (12,64, 67, 88, 161). Loop mediated isothermal amplica-tion (LAMP) is a point-of-care assay, which may beused to screen for periodontal pathogens in large geo-graphic areas and populations (124).High-throughput genomic sequencing techniques,

such as pyrosequencing and illumina-sequencing, arethe latest developments in oral and medical microbi-ology. These next-generation DNA-sequencing tech-nologies are cost-effective and can rapidly analyzeentire genomes with the resolution of a single-baseprecision. The techniques enhance the possibilities ofaddressing a variety of questions about the composi-tion, structure and function of complex microbialcommunities and their interaction with the host (34,111, 124, 134, 145). The slightly older microarray tech-nology, coupled with advanced computer-based dataanalysis, may be used to study intricate bacteriahostrelationships (35, 147, 152), but does not have thesuperior technical performance and cost advantageof next-generation sequencing technologies. In theforeseeable future, novel diagnostic tools will be ableto test simultaneously for both microbial and hostvariables and provide better insights into the determi-nants of health and disease. The new diagnosticmethods may help to identify periodontal diseaseactivity, microbial composition and early inamma-tory changes, including connective tissue metabo-lites, as well as the response to periodontal therapy atboth the microbial and the host level.

Periodontal microbiology in LatinAmerica

Studies of periodontal microbiology in Latin Americahave employed culture, ELISA, checkerboard DNADNA hybridization, conventional PCR and, morerecently, real-time PCR for bacterial and viral identi-cation (23).

Brazil

Brazil is the leading Latin American country inresearch on periodontal microbiology, and A. actino-mycetemcomitans in severe periodontal disease hasbeen a particularly important topic of study (4245,93, 97, 104, 194, 201) (Table 1). The prevalence ofA. actinomycetemcomitans in aggressive periodontitiswas found to range between 67% and 80%, with themajority of isolates belonging to biotype X (7, 194). Inchronic periodontitis, the prevalence of A. actinomy-cetemcomitans periodontitis was 18% with a predomi-

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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 theadolescents parents and 43.9% in their siblings

Chronic periodontitis

Avila-Campos et al. (2002) (9) Cultures showed a signicant association betweenA. actinomycetemcomitans and periodontitis, along with Tannerellaforsythia 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 canbe isolated from localized juvenile periodontitis and from patients withAIDS/necrotizing ulcerative periodontitis, but A. actinomycetemcomitanswith high leukotoxic activity is more frequent in localized juvenileperiodontitis 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 werepositive for A. actinomycetemcomitans. The deletion was not detected inindividuals with periodontal health

Cortelli et al. (2005) (42) A higher prevalence of leukotoxic strains of A. actinomycetemcomitans wasdetected in Brazilian subjects with aggressive periodontitis and with thedeepest pockets (>6 mm)

Cortelli et al. (2003) (45) There was a signicant correlation between highly leukotoxicA. actinomycetemcomitans and aggressive periodontitis (v2 = 22.06).However, a signicant correlation was not detected when analyzingseparate 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 harboredhighly leukotoxic A. actinomycetemcomitans. Biotype II was the mostprevalent, and no correlation between biotypes and leukotoxic activity wasobserved

Vieira et al. (2009) (202) In Indians from the Umutina Reservation, Mato Grosso, allA. actinomycetemcomitans strains were grouped as non-JP2 clones based onthe 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 withperiodontitis. Black-pigmented bacteria and Fusobacterium spp. werecommon. 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 Braziliansubjects. The most predominant bacteria were P. intermedia/Prevotellanigrescens (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 countsthan in peri-implant healthy sites. Porphyromonas gingivalis, T. denticola andT. 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 tonguethan on the cheek. Diverse niches of the oral cavity can harbor periodontopathicbacteria


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Table 1. (Continued)


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 Eikenellacorrodens (14%). Forty-nine Xingu Indians with gingivitis were positive forP. gingivalis (20%), A. actinomycetemcomitans (10%) and E. corrodens (2%)

Missailidis et al. (2004) (136) Porphyromonas gingivalis occurred in 89.4% of patients with periodontal attachmentloss, in 30% of patients with gingivitis and in 8.0% of healthy subjects. The mostprevalent P. gingivalis genotypes in patients with periodontitis were mAIIand mAIb. Genotype V was not detected in any of the samples andgenotype IV was the most common in patients with gingivitis

Teixeira et al. (2009) (189) An association was found between P. gingivalis mAIV and disease severityin smokers with chronic periodontitis

Trevilatto et al. (2002) (195) Actinobacillus actinomycetemcomitans, P. gingivalis, T. forsythia andT. denticola were detected in a family with aggressive periodontitis

Heller et al. (2012) (93) Actinomyces gerensceriae, Actinomyces israelii, Eubacterium nodatum andPropionibacterium acnes showed signicantly higher counts in generalizedaggressive periodontitis, whereas Capnocytophaga ochracea, Fusobacteriumperiodonticum, Staphylococcus aureus and Veillonella parvulapredominated 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 associationwith classical periodontopathogens, were strongly associated withperiodontitis

Bonifacio et al. (2011) (16) A high frequency of periodontal pathogens was associated with the severityof 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 chronicperiodontitis included a high prevalence of the classical periodontalpathogens 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 andC. rectus were also recovered from periodontal lesions of HIV-positivepatients

Diabetes mellitus

da Cruz et al. (2008) (51) Diabetic and nondiabetic patients did not differ signicantly in microbialcomposition (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 andatheromas

Romito et al. (2004) (160) In patients with heart transplants, subgingival samples yielded a prevalenceof 93% for P. intermedia, 66% for Fusobacterium nucleatum , 66% forParvimonas micra and 30% for C. rectus

Studies on other bacteria

Gebara et al. (2004) (77) Helicobacter pylori was found in the saliva of three (10%) patients, in thesupragingival plaque in six (20%) patients and in the subgingival plaque ineight (26.6%) patients. However, the organism was not recovered from thedorsum of the tongue of any patient. The presence of H. pylori was similarin patients with gingivitis and chronic periodontitis

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Silva et al. (2010) (168) Helicobacter pylori was detected in supragingival plaque, but not in subgingivalplaque, of individuals with periodontal disease and upper gastric diseases

Oliveira et al. (1998) (146) Fusobacterium bacteriocins were found in periodontally diseased and healthysubjects

Loberto et al. (2004) (117) Staphylococcus spp. were recovered from subgingival sites of patients withchronic 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%), Serratiamarcescens (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 generalizedaggressive periodontitis

Faveri et al. (2011) (66) Peri-implantitis sites showed a signicantly higher prevalence of Archaeathan did peri-implant healthy sites and natural teeth

Matarazzo et al. (2011) (132) The levels and proportions of Archaea were higher in generalized aggressiveperiodontitis than in periodontal health. The predominant species wasMethanobrevibacter oralis

Souto et al. (2006) (185) Predominant species in 600 subgingival samples from 14 subjects withchronic periodontitis included Corynebacterium diphtheriae, Enterococcusfaecalis, S. aureus and Escherichia coli

Souto et al. (2008) (186) Enterococcus faecalis was detected signicantly more often in saliva (40.5%) and insubgingival samples (47.8%) of patients with periodontitis compared withcontrols (14.6% and 17.1%, respectively)

Bacterial resistance studies

Avila-Campos et al. (1989) (8) The minimal inhibitory concentration of mercuric chloride was 4 lg/ml

Feres et al. (2002) (70) Metronidazole-resistant microorganisms: A. naeslundii 1, Streptococcusconstellatus, A. naeslundii 2, Streptococcus mitis, Streptococcus oralis,Actinomyces odontolyticus and Streptococcus sanguisAmoxicillin-resistant microorganisms: S. constellatus, P. nigrescens,Eubacterium saburreum, A. naeslundii 1, Streptococcus oralis, Prevotellamelaninogenica and P. intermedia

Rodrigues et al. (2004) (159) Tetracycline-resistant microorganisms: Streptococcus spp., V. parvula,P. micra, P. intermedia, Gemella morbillorum andA. actinomycetemcomitans

Clinical trials

Matarazzo et al. (2008) (131) Evaluated the clinical and microbiological effects of scaling and root planingalone or in combination with metronidazole (N = 15) or withmetronidazole + amoxicillin (N = 14) in smokers with chronic periodontitis.The scaling and root planing + metronidazole + amoxicillin therapyshowed signicant reductions in the mean counts and proportions ofT. forsythia, P. gingivalis and T. denticola, and the considerable increase inproportions of non-periodontopathic species

Feres et al. (2009) (69) The clinical and microbiological effects were assessed of scaling and rootplaning, alone, or combined with mechanical (professional plaque control)or chemical (chlorhexidine rinsing) treatment of supragingival plaque in 60patients with chronic periodontitis. Overall, the chlorhexidine rinsetreatment showed a signicant reduction in the proportions of red andorange bacterial complexes


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nance of biotype II (125). Leukotoxic strains of A. ac-tinomycetemcomitans (JP2 clone, serotype b) were acommon nding in aggressive periodontitis in SouthAmerica, with a particularly high prevalence in Brazil(84, 161). Cortelli et al. (42) found a higher occurrenceof A. actinomycetemcomitans and of highly leukotoxicstrains in Brazil than in other South American coun-tries, and linked highly leukotoxic strains to a greaterloss of periodontal attachment compared with mini-mally leukotoxic strains. Another study by Cortelliet al. (45) recovered the highly leukotoxic genotypefrom young subjects with aggressive periodontitisand suggested a role for A. actinomycetemcomitansleukotoxic strains in the development of the dis-ease, and possibly also in chronic periodontitis (74).Cortelli et al. (43, 44) proposed that the presence, insaliva, of leukotoxic strains of A. actinomycetemcomi-tans was a useful marker of aggressive periodontitisin children and adolescents. The association of theJP2 clone with aggressive periodontitis has also beendocumented outside Latin America (73, 8992, 111).In a 2-year prospective study in Morocco, Haubek etal. (91) found that adolescents, who were initiallyfree of periodontitis but harbored the JP2 clone, hada signicantly higher relative risk (18.0; 95% CI: 7.841.2) for developing destructive periodontal diseasethan did individuals infected with other types ofbacteria (3.0; 95% CI 1.37.1). Aggregatibacter actino-mycetemcomitans serotype c demonstrates low path-ogenicity compared with the JP2 clone (serotype b),and individuals from Asia with little or no periodon-tal disease harbor predominantly strains of the cserotype (90, 188, 193).The highly leukotoxic JP2 clone seems to be partic-

ularly prominent in individuals of African descent,which may account, in part, for the observed highlevel of aggressive periodontitis in African-Americansand in black Latin-American people (39, 4345). Dif-ferent levels of the population with African ancestrymay explain the different prevalence of A. actinomy-cetemcomitans and of the JP2 clonal type in Brazil(many people of African descent) (4345) and Chile(few people of African descent) (76, 120). The

A. actinomycetemcomitans leukotoxin may directlydestroy polymorphonuclear leukocytes or may inter-act with host genetic-susceptibility factors (13, 54,110, 118). The leukotoxin may be a particularly potentvirulence factor in young individuals, who may notyet have developed effective immunity against theorganism (92, 134, 142). However, individuals colo-nized by A. actinomycetemcomitans clones other thanthe JP2 clonal type can also develop periodontitis (6,44, 74, 89, 137). Subgingival A. actinomycetemcomi-tans was detected in 26% of subjects with chronicperiodontitis from the Umutina Indian Reservation atthe Mato Grosso region of Brazil, and none of theA. actinomycetemcomitans isolates was of the leuko-toxic phenotype (202).The cytolethal-distending toxin is another potential

virulence factor of A. actinomycetemcomitans. In astudy of 40 clinical isolates from Brazil, Kenya, Japanand Sweden (64), the three cdt genes (ABC) weredetected in 34 of the 40 strains. One strain fromKenya did not possess cdtA or cdtB genes andexpressed no toxic activity (64). Quantitative differ-ences in cytotoxicity exist among cdt gene-containingstrains, but no clear relationship has been foundbetween cytolethal-distending toxin activity andperiodontal disease status.The red complex of bacteria (P. gingivalis, T. for-

sythia and T. denticola) (181) is found at elevated levelsin Latin American patients with periodontitis (75, 76,158) and peri-implantitis (167). Specically, black-pig-mented bacteria of the Porphyromonas and Prevotellaspecies were detected in subjects with periodontitis(58%), gingivitis (37%) and healthy periodontium(15%) (42). Orange complex pathogens, such as Fuso-bacterium species (201), and other groups of bacteria,such as Staphylococcus aureus (and even yeasts) mayalso contribute to chronic periodontitis (27, 117).Dental implants can harbor relatively unique bacte-ria, but may also share the microbiota of periodontitis(71, 167). Faveri et al. (65) suggested that tongue dor-sum acts as a reservoir for periodontopathic bacteriaand may be a source of microbial transmission andrecolonization of periodontal sites. Feres et al. (69)



Haas et al. (2012) (85) Azithromycin was ineffective in lowering the subgingival levels of importantputative periodontal pathogens in young subjects with aggressiveperiodontitis compared with placebo

Novaes et al. (2012) (144) Antimicrobial photodynamic therapy associated with scaling and rootplaning may be benecial for the nonsurgical treatment of aggressiveperiodontitis

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recommended chlorhexidine oral rinse, along withscaling and root planning, to reduce periodontalpathogens in patients with periodontal disease.Recent ndings from Argentina point to sodiumhypochlorite (dilute bleach) oral rinse as an effectivemeans of controlling dental biolm and gingivalinammation (57). The low-cost bleach therapy couldstrengthen periodontal health efforts in poor ruraland urban areas with limited access to professionaldental 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. Thismicroorganism is a major pathogen of chronic peri-odontitis and can also be involved in aggressive peri-odontitis (76, 113). Its average prevalence is 89% inperiodontitis patients, 30% in gingivitis patients and8% in periodontally healthy subjects (136). Porphyro-monas gingivalis strains that possess a vast array ofpotent virulence factors are linked to severe periodon-tal disease, whereas P. gingivalis strains of reducedpathogenicity may be associated with minimal disease.The genetic polymorphism of the mA gene, which

encodes the subunit of P. gingivalis mbriae, hasattracted signicant research interest because of theimportance of mbriae in adherence to host tissues(3). Six genetic types of mA (I, Ib, II, III, IV and V) havebeen identied. Among these, type II, followed by typeIV, predominated in periodontitis patients from Japan,China, Europe and a multiethnic population in Brazil,whereas mAI strains predominantly inhabitedhealthy carriers (2, 3, 12, 136, 139, 198, 209). The mostprevalent genotype in smokers was mAIV, and thatgenotype was associated with clinical attachment lossand deep pocket depths. FimAIV was detected in69.6% of infected periodontal sites with no differencebetween shallow and deep pockets (189).Six capsular serotypes have been identied in the

P. gingivalis species, but a signicant proportion ofP. gingivalis isolates express little or no capsularmaterial. All six capsular serotypes of P. gingivalis,except K1, were found in an Indonesian population,but no particular serotype was related to the extent ofperiodontal attachment loss (200). Likewise, studies inthe USA showed that antibody responses to all six ser-otypes were common in both chronic and aggressiveperiodontitis (26). Virtually all (96%) subgingival iso-lates of P. gingivalis from an ethnically homogeneousSwedish population were phenotypically homoge-neous in biochemical tests, enzyme prole and antibi-otic susceptibility, and belonged to somatic antigenserotype A (53). To our knowledge, there are no reportsfrom Latin America on P. gingivalis capsular serotypes.

The periodontal microbiota of special patient cate-gories has been studied in Brazil. Tannerella forsythiawas a prevalent periodontal species in HIV-positivepatients, and Eikenella corrodens, D. pneumosintes,Streptococcus intermedius and C. rectus were alsocommon periodontal isolates from patients with HIV/AIDS (80, 83, 155). Patients with diabetes mellitusshowed a periodontal microbiota that resembled thatof non-diabetic individuals (51). Enterococcus faecaliswas recovered from 42% of patients with periodonti-tis, and species of the Enterobacteriaceae family, suchas Enterobacter cloacae, Klebsiella pneumoniae, Serra-tia marcescens, Enterobacter aerogenes and Escherichi-a coli, and even Archaea organisms, may also inhabitperiodontitis lesions (15, 52, 66, 81, 115, 132, 185,186). The presence of nonoral bacteria in periodontalsites may be related to immunosuppression, malnu-trition, poor sanitary conditions, or an indiscriminateuse of antibiotics.Studies from Brazil have examined the microbial

relationship between periodontal disease and systemicdiseases. Helicobacter pylori, which is involved in gas-tric ulcer and gastric cancer, can be recovered fromsaliva and from supragingival and subgingival plaque,suggesting that the oral cavity can serve as a reservoirfor the organism (77, 168). Atheromatous plaqueobtained from coronary arteries of periodontitispatients may contain periodontopathic bacterial DNA(126, 160). Periodontitis patients with inammatorybowel disease (Crohns disease) harbored higher levelsof periodontopathic bacteria than did control subjects(25). It may be that the interaction between periodon-tal and systemic diseases is a two-way street that cangive 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 sensitiveto mercuric chloride with a minimum inhibitory con-centration of 4 mg/ml. Feres et al. (70) and Rodrigueset al. (159) evaluated the resistance of periodontalbacteria to metronidazole, amoxicillin and tetracy-cline. Actinomyces naeslundii type 2, Streptococcusmitis, Actinomyces odontolyticus and Streptococcussanguinis were resistant to metronidazole. Prevotellanigrescens, Eubacterium saburreum, Prevotella mel-aninogenica and P. intermedia were resistant toamoxicillin. Actinomyces naeslundii type 1, Strepto-coccus constellatus and Streptococcus oralis wereresistant to both metronidazole and amoxicillin. Spe-cies that were resistant to amoxicillin were also resis-tant to tetracycline.Clinical trials performed to compare different peri-

odontal treatments have been conducted in Brazil.


65

Matarazzo et al. (131) studied the clinical and micro-biological effects of scaling and root planing, usedalone or in combination with metronidazole, or in acombined metronidazole+amoxicillin therapy.Patients treated with scaling and root planingtogether with the two antibiotics experienced areduction in the red and orange complexes of patho-gens (131). A clinical trial by Novaes et al. (144) sug-gested that a combination of photodynamic therapyand scaling and root planing constituted a promisingnew approach to the nonsurgical treatment of aggres-sive periodontitis.

Colombia

The rst studies on periodontal infections in Colom-bia were performed by Jimenez and coworkers in1975 and 1993, and reviewed in 2005 (106108)(Table 2). These authors found that necrotizing ulcer-ative gingivitis was a precursor to noma (cancrumoris), and that low socio-economic status, acute her-petic gingivostomatitis, measles, leukemia, malnutri-tion and poor oral hygiene were associated withnoma. Pathogenetic synergy between the major peri-odontal pathogens T. denticola and P. gingivalis, incombination with cytomegalovirus, may also contrib-ute to the development of necrotizing oral diseases(37, 170, 172).The microbiota of chronic and aggressive peri-

odontitis has been a major research emphasis inColombia. Botero et al. (18) detected P. gingivalis,T. forsythia and E. corrodens in higher proportions inaggressive than in chronic periodontitis or in peri-odontal health (P < 0.05). Gram-negative enteric rodswere frequent inhabitants of periodontitis lesionsand, in particular, of aggressive periodontitis lesions(P < 0.01) (18). Martinez-Pabon et al. (130) deter-mined that T. denticola was closely related to chronicperiodontitis (P < 0.05), and they were able to identifythe organism in patients saliva (129). A study inBogota found that chronic and aggressive periodonti-tis lesions were associated with a high prevalence ofP. gingivalis, T. forsythia, P. intermedia/P. nigrescens,C. rectus, Fusobacterium species and E. corrodens,and a relatively low prevalence of P. micra, A. actino-mycetemcomitans, D. pneumosintes and gram-nega-tive enteric rods (133). A multicenter study ofperiodontitis patients in the ve largest Colombiancities found a high prevalence of P. gingivalis (72%),T. forsythia (59%), C. rectus (58%), A. actinomycetem-comitans (24%) and gram-negative enteric rods (35%)(113). Aggregatibacter actinomycetemcomitans wasincreased in aggressive periodontitis compared to

chronic periodontitis (113). Tannerella forsythia,C. rectus and E. corrodens had a relatively lowpresence in periodontitis patients in the West-Pacic and Central regions of Colombia, andgram-negative enteric rods occurrred with increasedfrequency in the Central region of Colombia(P < 0.05) (113). Another study recovered P. gingivalisand gram-negative enteric rods from subjects withchronic periodontitis at frequencies of 67% and 26%,respectively, and found the organisms to correlatepositively with increased probing depth, clinicalattachment loss and bleeding on probing (P < 0.001)(4). However, a longitudinal study of untreatedperiodontitis found that the gram-negative entericrods were not consistantly observed in many subjectsthroughout a 1-month study period, indicating thatgram-negative enteric rods are frequently transientmicroorganisms in subgingival sites (128). Apart fromthe enteric rods, other unusual microorganisms canalso inhabit periodontal pockets, perhaps as superin-fecting or transient occupants (15, 128).The periodontal microbiota of special patient cate-

gories has also been an important research topic inColombia. In HIV-infected patients, Botero et al. (17)detected a higher frequency of periodontopathic bac-teria in HIV-negative periodontitis patients than inHIV-positive periodontitis patients and in periodon-tally healthy subjects (P < 0.05), but HIV-positivepatients harbored higher levels of superinfectingmicroorganisms, including Pseudomonas aeruginosa,E. cloacae and K. pneumoniae (P < 0.05). Castrillonet al. (32) studied the periodontal microbiota of dia-betic patients. The red complex microorganisms(P. gingivalis, T. forsythia and T. denticola) weredetected at a lower frequency in patients with diabe-tes, but A. actinomycetemcomitans occurred at an ele-vated level in diabetic patients (P < 0.05) (32).Porphyromonas gingivalis was associated with peri-odontitis in nondiabetic patients (P < 0.05), andA. actinomycetemcomitans was associated with peri-odontitis in diabetic patients (P < 0.05) (32). Contre-ras et al. (38) studied the periodontal microbiota inwomen with pre-eclampsia and periodontitis. Mostpatients 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. cor-rodens were more prevalent in pre-eclamptic subjectsthan in control subjects (P < 0.01).A variety of special dental conditions has been stud-

ied in Colombia. Botero et al. (21) found that implantswith peri-implantitis harbored more P. gingiva-lis, P. intermedia/P. nigrescens and gram-negativeenteric rods than did control implants (P < 0.05) (21).

Contreras et al.

66

Table 2. Studies on the subgingival microbiota in Colombia

Author Year Subjects Technique Findings

Jimenez & Baer(106)

1975 28 patients with acutenecrotizing ulcerativegingivitis

Clinicalevaluation

Acute necrotizing ulcerative gingivitis occurredonly in children from low socio-economicgroups and was associated with poor oralhygiene and malnutrition. In the case of noma,previous infection with a virus or an intestinalparasite appeared to be important predisposingfactors

Jimenez et al.(108)

2005 29 patients with necrotizingulcerative gingivitis, 7 withnecrotizing ulcerativeperiodontitis and 9 withnoma

Clinicalevaluation

Malnutrition and poor oral hygiene favoredprogression of the necrotic gingival lesion intodeeper periodontal tissue and other structuresof the oral cavity or of the facial tissues. Thepopulation presented predisposing and/orcontributing factors such as acute herpeticgingivostomatitis, measles and leukemia.Necrotizing ulcerative gingivitis may progress toulcerative necrotizing stomatitis, necrotizingulcerative periodontitis and, nally, to noma

Botero et al. (18) 2007 68 patients with chronicperiodontitis, 12 withaggressive periodontitis and30 healthy subjects

Microbiologicalculture, PCR

There was a higher frequency of Porphyromonasgingivalis, Tannerella forsythia and Eikenellacorrodens in patients with aggressiveperiodontitis than in those with chronicperiodontitis and with healthy periodontium(P < 0.05). Gram-negative enteric rods were morefrequent in patients with aggressive periodontitis(P < 0.01)

Martinez-Pabonet al. (130)

2008 37 patients with chronicperiodontitis, 24 withaggressive periodontitis and28 healthy subjects

PCR The prevalence of Treponema denticola inpatients with chronic periodontitis wassignicantly higher than in periodontallyhealthy subjects and in those with aggressiveperiodontitis (P < 0.05)

Martinez-Pabonet al. (129)

2010 97 patients with chronicperiodontitis and 51 healthysubjects

PCR Salivary carriage of T. denticolamay be a riskindicator for chronic periodontitis

Mayorga-Fayadet al. (133)


Microbiologicalculture

Parvimonas micra, Aggregatibacteractinomycetemcomitans, Dialister pneumosintesand enteric rods (mostly Klebsielleae spp.)were recovered. P. gingivalis was isolatedmore frequently than A. actinomycetemcomitansfrom patients with aggressiveperiodontitis

Lafaurie et al.(113)


PCR Frequency in periodontitis: P. gingivalis, 71.5%;T. forsythia, 58.5%; Campylobacter rectus,57.5%; A. actinomycetemcomitans, 23.6%; andenteric rods, 34.5%. Porphyromonas gingivalis,T. forsythia and C. rectus were the most prevalentperiodontopathic microorganisms in periodontitispatients from large Colombian cities

Ardila et al. (4) 2011 76 patients with chronicperiodontitis


Porphyromonas gingivalis and gram-negativeenteric rods correlated positively with probingdepth, clinical attachment level and bleeding onprobing (P < 0.0001)


67

Jaramillo et al. (101) studied the microbiology of peri-odontal abscesses and found a high prevalence ofFusobacterium species (75%), P. intermedia/P. nigres-cens (60%), P. gingivalis (51%) and A. actinomycetem-comitans (30%). Naranjo et al. (141) studied changesin the periodontal microbiota following orthodontic

treatment. Orthodontic bracket placement causedan increase in plaque index, gingival index and bleed-ing on probing (P < 0.05), and an increase in P. gingiva-lis, P. intermedia/P. nigrescens, T. forsythia, andFusobacterium species compared with controls(P < 0.01). Superinfecting E. cloacae, Klebsiella oxytoca,



Castrillon et al.(32)

2013 60 patients with diabetesmellitus and 62 nondiabeticpatients

PCR The red complex microorganisms occurred at alower rate in patients with diabetes. Thedetection rate of A. actinomycetemcomitans washigher in patients with diabetes andperiodontitis than in systemically healthypatients without periodontitis (P < 0.05).Porphyromonas gingivalis was associated withperiodontitis in nondiabetic patients (P < 0.05)

Botero et al.(21)

2005 16 implants with signs ofpocketing, 12 neighboringteeth and 11 non-neighboring teeth, in 11patients

Clinical,radiographicand anaerobicculture study

Signicant correlations were found betweenimplants and neighboring teeth for gram-negative enteric rods (P = 0.023), and betweenimplants and non-neighboring teeth forP. gingivalis (P = 0.042). The frequency ofdetection of gram-negative enteric rods (75%)and Prevotella intermedia/Prevotella nigrescens(25%) was higher in peri-implant lesions(P < 0.05). Porphyromonas gingivalis comprised1.4% of total isolates in peri-implant lesions

Jaramillo et al.(101)

2005 60 periodontal abscesses from54 patients with chronicperiodontitis


Periodontal abscesses showed Fusobacteriumspp. (75%), P. intermedia/P. nigrescens (60%),P. gingivalis (51%) andA. actinomycetemcomitans (30%). None of thebacteria tested presented resistance toazithromycin. An intermediate resistance wasfound for tetracycline in two of 14 isolates ofP. intermedia/P. nigrescens and in three of fourisolates of A. actinomycetemcomitans. One of 11isolates of P. gingivalis was resistant tometronidazole. One isolate ofA. actinomycetemcomitans and two isolates ofP. intermedia/P. nigrescens were resistant toamoxicillin

Jaramillo et al.(102)

2013 192 patients with aggressiveperiodontitis and 256 withmoderate periodontitis

PCR Elevated levels of high-density lipoprotein (HDL)and triglyceride were present in patients withperiodontitis. Serum IgG1 against P. gingivaliswas associated with HDL-35. Serum IgG1against T. forsythia was associated withtriglyceride and serum IgG2.Aggregatibacter actinomycetemcomitanscorrelated with levels of HDL and HDL-35.The presence of IgG1 against P. gingivalis andA. actinomycetemcomitans correlated withreduced HDL levels

Moreno et al.(139)

2013 49 patients with chronicperiodontitis, 77 withgingivitis and 25 healthysubjects

PCR No difference among study groups was detectedin the distribution of the P. gingivalis mAgenotype. An association was found amongP. gingivalis, T. denticola and T. forsythia inpatients with periodontitis

Contreras et al.

68

K. pneumoniae and Serratia marcescens were alsodetected after bracket placement (141).The systemic impact of periodontal disease was

studied by Lafaurie et al. (114), who evaluated the fre-quency of subgingival anaerobic and facultative bac-teria in the bloodstream following scaling and rootplaning of patients with severe generalized periodon-titis. Eighty-one per cent of peripheral blood sampleswere positive for bacteria immediately after scaling,and the periodontopathic microorganisms most fre-quently identied were P. gingivalis and P. micra,and organisms less often isolated were Campylobacterspecies, E. corrodens, T. forsythia, Fusobacterium spe-cies and P. intermedia. In a similar study, Castilloet al. (31) identied bacteria in peripheral blood afterscaling and root planing in 55% of periodontitispatients; P. gingivalis and A. actinomycetemcomitanswere the periodontal pathogens most frequentlyidentied. Jaramillo et al. (102) studied the relation-ship between untreated periodontal disease andlow-grade systemic inammation and blood lipidalteration. A high IgG1 level against P. gingivalis andA. actinomycetemcomitans may correlate with areduced level of the anti-atherogenic high-densitylipoprotein (102).Moreno et al. (139), in a recent study of P. gingiva-

lis mA genotypes, found no differences in genotypedistribution among chronic periodontitis, gingivitisand healthy periodontium. Microbial antibiotic resis-tance was determined by Jaramillo et al. (103) in iso-lates from patients with aggressive periodontitis andchronic periodontitis and from periodontally healthysubjects. Aggregatibacter actinomycetemcomitans wasresistant to metronidazole, amoxicillin and clindamy-cin, and P. intermedia/nigrescens and Enterobacteria-ceae species were resistant to amoxicillin (103).Finally, Ramirez et al. (154) found an increased levelof important cardiovascular markers and red complexbacteria in patients with severe and moderate chronicperiodontitis.

Chile

Lopez et al. (121) studied the microbiota of chronicperiodontitis in Chilean patients using the checker-board DNADNA hybridization technique (Table 3).The main ndings were high proportions of the redcomplex bacteria P. gingivalis, T. forsythia, and T. den-ticola, and variable levels of the periodontopathicmicroorganisms C. rectus, F. nucleatum, P. micros andTreponema socranskii (121). A study of aggressiveperiodontitis found a low prevalence of Actinomycesspecies, which are considered commensal organisms

in the subgingival area (119). Gajardo et al. (76)determined the predominant periodontopathicbacteria to be P. gingivalis, C. rectus, E. corrodens,P. micra and Capnocytophaga species. Silva et al.(169) compared the occurrence of A. actinomycetem-comitans, P. gingivalis and T. forsythia in progressiveand stable periodontitis, and found a higher percent-age of P. gingivalis in disease-active sites (18%) thanin disease-inactive sites (2%).Lopez et al. (123) studied the consortia of microor-

ganisms associated with periodontitis in differentstages of the disease. Prevotella nigrescens, P. inter-media, P. gingivalis and T. forsythia were present athigh levels in subjects with periodontitis. One clusterof organisms included T. forsythia, C. rectus, P. gingi-valis, P. intermedia, P. nigrescens, P. micra andT. denticola. Another cluster of organisms containedActinomyces oris, Capnocytophaga ochracea, E. corro-dens, S. intermedius, S. noxia, S. oralis, S. sanguinisand Veillonella parvula. Fusobacterium nucleatumwas assigned to both clusters. The personal cluster ofperiodontal bacteria may be an important determi-nant of the outcome of periodontal therapy (165).Lopez et al. (122) also evaluated the clinical and

microbiological effects of treating periodontitissolely with metronidazole plus amoxicillin. Theyfound a marked reduction in the mean counts ofthe red complex bacteria P. gingivalis, T. forsythiaand T. denticola for up to 12 months post-treatmentin both the antibiotic-treated group and the scaledcontrol group. Actinomyces counts increasedsignicantly post-treatment. The authors made theinteresting observation that the antibiotic therapyand periodontal scaling and root planing led tosimilar improvements in clinical and microbiologicalvariables (122).

Mexico

The subgingival microbiota has been described inpatients from Mexico using the checkerboard DNADNA hybridization technique (Table 4). Consistentwith other studies, periodontitis patients presentedhigher quantities of P. gingivalis, T. denticola, T. for-sythia and A. actinomycetemcomitans than did peri-odontally healthy subjects (1, 206). No signicantdifferences were observed in the detection level of 40test species between generalized aggressive periodon-titis and generalized chronic periodontitis. The bacte-rial species that were associated with periodontitiswere also detected in periodontally healthy subjects(205, 206). Another study detected subgingival P. in-termedia in 89%, and subgingival P. gingivalis in 58%,


69

Table 3. Studies on the subgingival microbiota in Chile


Lopezet al. (121)

2004 26 patients with chronicperiodontitis from Chile andthe USA

Checkerboard DNADNAhybridization

Red complex and other periodontopathicmicroorganisms such as Campylobacterrectus, Fusobacterium nucleatum,Parvimonas micra and Treponemasocranskii, as well as yellow complexbacteria, were signicantly elevated inChilean subjects, whereas Actinomycesspp. were higher in US subjects

Gajardoet al. (76)

2005 36 patients with aggressiveperiodontitis from Chile

Microbiological culture Campylobacter rectus, Porphyromonasgingivalis, Eikenella corrodens, P. micraand Capnocytophaga spp. were predominantin aggressive periodontitis lesions, butonly C. rectus was statistically associatedwith periodontitis

Silvaet al. (169)

2008 56 patients with chronicperiodontitis from Chile

ELISA, anaerobemicrobiological culture

Higher RANKL, interleukin-1beta andmatrix metalloproteinase-13 activitylevels were observed in disease-activesites (P 0.05). The proportion ofP. gingivalis, Aggregatibacteractinomycetemcomitans and Tannerellaforsythia, and the number of CD4+ T cells,were higher in disease-active than ininactive periodontal sites

Lopezet al. (122)

2006 22 patients with chronicperiodontitis

Clinical trial, CheckerboardDNADNA hybridization

Metronidazole plus amoxicillin or scalingand root planing were given to patientswith periodontitis harboring highpercentages of Streptococcus gordonii,A. actinomycetemcomitans, Eubacteriumnodatum, Fusobacterium periodonticum,P. gingivalis, Treponema denticola andT. socranskii. At 12 months post-treatment, changes in clinical andmicrobiological parameters were similarin subjects receiving systemic antibioticsor scaling and root planing

Haffajeeet al. (86)

2004 300 subjects from the USA,Sweden, Brazil and Chile(total number ofsamples=6036)

Checkerboard DNADNAhybridization

Porphyromonas gingivalis, comprised adjustedmeans of 7.5, 11.9, 1.6 and 6.6% of themicrobiota in subjects from Brazil, Chile,Sweden and USA (P < 0.001), and meanproportions of T. denticola were 6.7, 4.2,0.8 and 2.3, respectively (P < 0.001).Tannerella forsythiamean proportionsranged from 6.2 to 8.5% and did not differsignicantly among countries.Actinomyces naeslundii genospecies 1and 2 (8.4% and 7.2% respectively) andPrevotella intermedia (6.5%) wereprominent species in Brazil; Prevotellamelaninogenica (6.4%) and Neisseriamucosa (5.3%) were prominent in Chile;A. naeslundii genospecies 2 (8.4%),Capnocytophaga gingivalis (7.1%) andP. micra (5.0%) were prominent inSweden; A. naeslundii genospecies 2(7.5%), Prevotella intermedia (6.8%) andCapnocytophaga gingivalis (6.1%) wereprominent in the USA

Contreras et al.

70

of patients with periodontitis and rheumatoid arthri-tis (127). The same microorganisms were detected byPCR in synovial uid of subjects with periodontitisand rheumatoid arthritis (74% and 42% respectively),but not by culture (127). A study using a multiplex-PCR protocol found P. gingivalis in subjects withchronic periodontitis (37%) as well as with a normalperiodontium (24%) (56).Davila-Perez et al. (55) studied the distribution of

P. gingivalis mA genotypes in type 2 diabeticpatients with periodontitis and in nondiabeticpatients with and without periodontitis. The diabeticpatients harbored manly the mAI, II and III geno-types, the nondiabetic patients harbored the mAI, Iband II genotypes, and the periodontally healthy sub-jects harbored the mAI genotype (55).

Various countries

The periodontal microbiota has also been studiedin Argentina, the Dominican Republic, Guatemala,Haiti, Panama and Venezuela (Table 5). In Argen-tina, A. actinomycetemcomitans, red complex bacte-ria and superinfecting organisms were prevalent inpatients with periodontitis (11, 28, 46, 47, 59, 138,197). Bazzano et al. (11) found that scaling androot planing reduced the occurrence of P. gingiva-lis, T. forsythia and T. denticola in deep periodontalpockets and that no further loss of clinical attach-ment was observed for 12 months in 79% of thetreated sites. In the Dominican Republic, gram-neg-ative enteric rods were prevalent in untreated peri-odontal sites (178). In Guatemala, Pomes et al.(151) identied A. actinomycetemcomitans, yeastand Entamoeba gingivalis as risk indicators of ado-lescent periodontitis. A high prevalence of A. ac-tinomycetemcomitans was also demonstrated inblack Panamanian patients with localized juvenileperiodontitis (61). Two studies from Venezueladescribed periodontal pathogens in patients withgastritis and HIV infection (14, 24).

A few studies have compared the periodontal mic-robiota among different countries in Latin Americaand abroad. Haffejee et al. (86), using checkerboardDNADNA hybridization, found elevated levels ofP. gingivalis and T. denticola in Brazil and Chile com-pared with Sweden and the USA. Samples from Chil-eans of low socio-economic status harbored relativelyhigh proportions of Streptococcus gordonii, A. actino-mycetemcomitans, Eubacterium nodatum, Fusobacte-rium periodonticum, P. gingivalis, T. denticola andT. socranskii, and low percentages of A. naeslundiiand C. gracilis (86).Herrera et al. (94) studied the microbiota of

patients with chronic periodontitis in Colombia, Chileand Spain. Patients from Colombia revealed greaterseverity of periodontitis, signicantly higher total bac-terial colony counts, and increased levels of P. gingi-valis and gram-negative enteric rods. Chileanpatients showed a high prevalence of P. micra andE. corrodens and relatively low percentages of A. ac-tinomycetemcomitans, P. intermedia, T. forsythia andCapnocytophaga species. Spanish patients exhibitedincreased levels of P. intermedia and did not yieldgram-negative enteric rods. The study suggested thatdifferences exist in the periodontopathic microbiotaof subjects in these three countries.Aggressive periodontitis in adolescents (i.e. patients

with localized juvenile periodontitis) has been relatedto A. actinomycetemcomitans and P. gingivalis. Theclassic type of localized juvenile periodontitis starts atthe onset of puberty and involves rst molars andincisors and exhibits very little dental plaque and vir-tually no gingivitis. This type of disease typicallyharbors A. actinomycetemcomitans at a prevalence of73100% (180). Another type of localized juvenile peri-odontitis shows the characteristic rst molar-incisortissue destruction, but also manifests distinct plaqueaccumulation and gingivitis and tends to appear inslightly older patients. This type of disease has beenstudied in Jamaica (135) and Colombia (18, 22, 113)and is predominated by P. gingivalis, which may



Herreraet al. (94)

2008 114 patients with chronicperiodontitis

Anaerobic microbiologicalculture

Aggregatibacter actinomycetemcomitans(19.4%), Prevotella intermedia (19.4%),Tannerella forsythia (16.2%), Capnocytophagaspp. (13.5%), P. micra (29.7%), E. corrodens(34.3%), P. gingivalis (83.8%), Fusobacteriumspp. (63.9%) and superinfecting enterics(17.6%) were detected in chronicperiodontitis of Chilean patients


71

occur as a superinfection or independently of anA. actinomycetemcomitans infection. Studies in Chileof patients with localized juvenile periodontitisyielded A. actinomycetemcomitans at prevalences of3944%, but also P. gingivalis and P. intermedia atrelatively high levels (119, 120).

Human viruses and periodontal disease

Herpesviruses and other human viruses are oftenacquired in childhood and can be identied in theoral cavity of most adult individuals (Table 6). Herpe-sviruses employ various strategies to interact with

Table 4. Studies on the subgingival microbiota in Mexico


Almaguer-Floreset al. (1)

2005 33 patients with chronicperiodontitis; 23 healthysubjects

CheckerboardDNADNAhybridization

The presence of bacterial DNA forPorphyromonas gingivalis, Tannerellaforsythia, Treponema denticola andAggregatibacter actinomycetemcomitans wassignicantly higher in subjects with chronicperiodontitis. Lower proportions ofActinomyces spp. and microorganismsincluded in the yellow complex were foundin patients with chronic periodontitis thanin healthy subjects

Ximenez-Fyvieet al. (205)

2006 19 patients with generalizedaggressive periodontitis; 39patients with generalizedchronic periodontitis; 19healthy subjects


Patients with generalized aggressiveperiodontitis and patients with generalizedchronic periodontitis harbored signicantlyhigher levels of P. gingivalis, T. forsythia andPrevotella nigrescens than did healthysubjects. No signicant differences in any of40 microbial species were detected betweenuntreated generalized aggressiveperiodontitis and untreated generalizedchronic periodontitis

Ximenez-Fyvieet al. (206)



No signicant differences were detected inthe percentage of carriers of any of thespecies tested. The proportions ofP. gingivalis, T. forsythia and red complexspecies (P. gingivalis, T. forsythia andT. denticola) were also signicantly higher inpatients with periodontitis

Martinez-Martinezet al. (127)

2009 19 patients with chronicperiodontitis andrheumatoid arthritis

PCR Subgingival plaque and synovial uid yieldedPrevotella intermedia (89.4% and 73.6%,respectively) and P. gingivalis (57.8% and42.1%, respectively). Culture did not showany bacterial growth

De La Garza-Ramoset al. (56)


Multiplex-PCR In untreated patients with periodontitis, 37%yielded P. gingivalis, 17% yieldedStreptococcus intermedius, and 24.5%yielded both species. Porphyromonas gingivaliswas detected in 23.5% of healthy volunteers,whereas Streptococcus intermedius was notdetected in healthy individuals

Davila-Perezet al. (55)

2007 25 healthy subjects; 25patients with chronicperiodontitis; 25 patientswith type 2 diabetes mellitusand chronic periodontitis

PCR Porphyromonas gingivalis genotypes wereanalyzed. In healthy subjects, type I mAwas the most frequently detected individualgenotype (40%). In subjects with periodontitis,the most frequently detected individual mAgenotype was Ib (20%). In periodontitispatients with type 2 diabetes mellitus, themost frequently detected genotypes weretypes I and III mA (20%)

Contreras et al.

72

Table 5. Studies on the subgingival microbiota in Argentina, Guatemala, Panama, Hait and Venezuela

Country and Author Year Subjects Technique Findings

Argentina

Canigiaet al. (28)

1999 45 patients withchronic periodontitis


In 138 periodontitis sites, the most prevalent specieswere Prevotella intermedia/Prevotella nigrescens(77%), followed by Aggregatibacteractinomycetemcomitans (44%) and Parvimonas micra(39%). Porphyromonas gingivalis was detected in 26%of the sites, and was associated with a greater depthof periodontal pockets. Healthy periodontal sitesyielded mainly viridans streptococci andNeisseria spp. and the previously mentionedspecies were not detected

Cuestaet al. (46)

2010 82 patients withperiodontal disease


The prevalence of Staphylococcus spp. was 42.7% inperiodontal pockets and 69.5% in the oral mucosa,and the prevalence of Candida spp. was 25.6% inperiodontal pockets and 42.7% in the oral mucosa.The coexistence of these species was 13.4% inperiodontal pockets and 36.6% in the oral mucosa.Staphylococcus aureus occurred in 13.4% of theperiodontal pockets and 13.5% in the oral mucosa.Candida albicans was detected in 76.2% of theperiodontal pockets and in 63% of oral mucosa

Cuestaet al. (47)

2011 102 patients withperiodontitis andgingivitis

Microbiologicalculture andPCR

Staphylococcus aureus was found in 10.8% (n = 11) ofperiodontal pockets and in 19.6% (n = 20) of theoral mucosa. This species may behave asan opportunistic pathogen that can colonizethe gingival sulcus, nding an ecological nichethat provides optimal conditions for infection

Monettiet al. (138)

2012 Six patients withgingivitis, 7 with mildchronic periodontitis,23 with moderatechronic periodontitisand 7 with severeperiodontitis

PCR Prevotella denticola + P. intermedia (P = 0.04) andP. intermedia + Tannerella forsythia (P = 0.02) wereassociated with the presence of tumor necrosisfactor-alpha mRNA in 20% and 25% of subjects,respectively. Porphyromonas gingivalis +A. actinomycetemcomitans andA. actinomycetemcomitans + T. forsythia wereassociated with severe periodontal disease andclinical attachment loss, respectively. The associationbetween the presence of P. intermedia and expressionlevels of tumor necrosis factor-alpha was signicant(P = 0.05)

Bazzanoet al. (11)

2012 44 sites from 11patients with chronicperiodontitis

PCR Porphyromonas gingivalis, T. forsythia andTreponema denticola occurred at baseline in66%, 55% and 41%, respectively, of thetest sites. Deep pockets correlated with T. forsythia-Treponema denticola (6.8 mm) and T. forsythia-T. denticola-P. intermedia (7 mm)

Usinet al. (197)

2013 150 pregnant women PCR A high prevalence of P. gingivalis was found inpregnant women, especially in combination withT. forsythia and T. denticola. Older age was a riskfactor for moderate periodontitis (odds ratio = 4.92,95% condence interval = 1.121.3, P = 0.0328). Inpregnant women, the presence of P. gingivalis wasfound to increase the risk for showing a clinicalattachment level >5 mm and for moderateperiodontitis


73



Dominican Republic

Slotset al. (178)

1991 24 patients withperiodontitis


Direct microscopic examination revealed that cocciand nonmotile organisms made up 85% of the totalorganisms and spirochetes as little as 3%.Nonselective culture showed gram-negativeorganisms to constitute 53% of total isolates.Fusobacterium nucleatum averaged 15%, black-pigmented anaerobes 7% and Parvimonas micra10% of the cultivable microora. Enteric rods andacinetobacter species were recovered from16 patients and comprised 23% of the cultivableora. The most common enteric species wereEnterobacter cloacae, Klebsiella oxytoca and 7other species

Guatemala

Dowsetet al. (59)

2002 114 subjectsfrom 45 families


Streptococcus sanguis, Actinomyces naeslundiigenospecies 2 and Fusobacterium nucleatum weresignicantly more common in deep periodontalpockets, and A. naeslundii and P. micra weresignicantly more common in healthy periodontalsites. Aggregatibacter actinomycetemcomitans wasnot detected in any sample

Pomeset al. (151)

2000 62 subjects, 1115 yearsof age

Different testsfor each pairof sites

The prevalence of BANA-positive test results (redbacteria indicator) was 77%, ofA. actinomycetemcomitans was 47%, of yeasts was43% and of Entamoeba gingivalis was 21%. The riskfor severe gingival inammation and/or increasedprobing depth was 1.5 and 5.2 times higher with apositive BANA test or A. actinomycetemcomitans test.No associations were found for yeasts andE. gingivalis

Haiti

Psoteret al. (153)

2011 104 Haitianadolescents

QuantitativePCR

The frequency of Streptococcus mutans was 67.3% insupragingival plaque samples, andA. actinomycetemcomitans had a frequency of 85.1%in subgingival plaque samples

Panama

Eisenmannet al. (61)

1983 12 patients withlocalized juvenileperiodontitis and 10with gingivitis


Aggregatibacter actinomycetemcomitans was presentin all localized juvenile periodontitis lesions studiedand was, on average, recovered in hundred-foldhigher numbers from localized juvenileperiodontitis lesions than from gingivitis lesions.Capnocytophaga was only recovered inapproximately threefold higher numbers fromlocalized juvenile periodontitis than from gingivitis

Wiebeet al. (204)

2003 18 individuals withKindler syndrome

PCR Kindler syndrome periodontitis yielded a prevalenceof 54% for T. denticola, 46% for P. nigrescens, 31% forDialister pneumosintes, 31% for P. gingivalis, 23%for A. actinomycetemcomitans and 15% forT. forsythia

Contreras et al.

74

and subvert host defenses to ensure their continuedexistence and propagation (173). Herpesvirus infec-tions vary considerably in severity, which can rangefrom subclinical infection to encephalitis and cancer,including carcinoma, lymphoma and sarcoma (179).Genomes of herpes simplex virus type 1, human cyto-megalovirus and EpsteinBarr virus have beendetected in periodontal pockets (22, 23, 40, 83), saliva(179) and gingival immune cells (36, 41, 98), and thethree herpesviruses have been associated withchronic periodontitis (22, 40), aggressive periodontitis(203), acute necrotizing ulcerative gingivitis (37) andperiodontal abscesses (50, 164). Herpesviruses canoccasionally be present at low levels in healthy peri-odontal sites (22, 23, 82, 179).In Colombia, Botero et al. (23) cultured cytomegalo-

virus from the gingival crevicular uid of patients

with periodontitis, but with a lower yield than thatobtained by molecular identication. Cytomegaloviruswas detected in patients with periodontitis (53%) andin periodontally healthy subjects (18%) (P < 0.05),and cytomegalovirus-positive sites showed a higheroccurrence of major periodontopathic bacteria andmore loss of periodontal attachment compared withcytomegalovirus-negative sites (22). Botero et al. (19)studied the in vitro effect of human cytomegalovirusinfection on gingival broblast expression of colla-gen I and III and matrix metalloproteinases 1 and 2.Gingival broblasts infected with human cytomega-lovirus exhibited reduced expression of mRNA forcollagens I and III (P < 0.05), and up-regulation ofmRNA expression for matrix metalloproteinases 1and 2 (P < 0.05). Botero et al. (19) also found higherexpression of mRNA for collagens I and III in biop-



Venezuela

Berroteranet al. (14)

2002 32 patients with chronicgastritis and 20healthy subjects

PCR Helicobacter pylori was detected in antral samplesfrom 24 (75%) of 32 patients with chronic gastritis.Helicobacter pylori was also detected in dentalplaque samples of 12 (37.5%) of the 32 patients.Seven patients with chronic gastritis yieldedH. pylori in both antral and dental plaque samples.There was no positive relationship betweenH. pylori and periodontal parameters

Britoet al. (24)

2008 32 HIV-positive and 16HIV-negative patients

PCR The mean values of plaque index, gingival index andclinical attachment loss were similar for HIV-infectedpatients undergoing or not receiving HAART therapy.Linear gingival erythema was observed in HIV-infected patients, and necrotizing ulcerativeperiodontitis occurred only in HIV-positive patientswithout HAART therapy. Prevotella intermedia wasthe 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 theCD4+ count or viral load

Escalonaet al. (63)

2011 20 HIV-positive patientswith periodontaldisease and 7 HIV-negative patients withperiodontal disease

PCR Human papillomaviruses were detected in 46% ofHIV-positive patients under therapy. TheCD4 cell counts in the human papillomavirus-positive patients were not signicantly different fromthose in the human papillomavirus-negative group.Genotypes 6 and 11 were observed in the humanpapillomavirus-positive samples, of which 4 (66.6%)of six presented a co-infection with both types.No signicant differences in the periodontalconditions were observed betweenpatients with human papillomavirus + HIV infectioncompared with patients infected with HIV only.Papillomaviruses were detected only in the gingivalcrevicular uid of HIV-positive patients underHAART, independently of the periodontal condition


75

Tab

le6.

Subgingivald

etectionofm

ammalianvirusesin

LatinAmerica

Author/year

Country

Number

ofsubjects

Virus

EpsteinB

arrvirus-1

Human

cytomegalovirus

Herpes

simplexvirustype1

Botero

etal.2008(23)

Colombia

37patientswithch

ronicperiodontitis,7

patientswithaggressive

periodontitisan

d24

healthysubjects

Periodontitis:

PCR:79.5%

Real-timePCR:47.7%

Culture:2.3%

Healthysubjects:

PCR:25%

Real-timePCR:4.1%,C

ulture:0%

Botero

etal.2007(22)

Colombia

20patientswithch

ronicperiodontitis,10

patientswithaggressive

periodontitisan

d22

healthysubjects

Chronicperiodontitis:60%

Aggressiveperiodontitis:40%

Healthypatients:18.1%

Botero

etal.2008(19)

Colombia

14patientswithch

ronicperiodontitisan

d3

healthysubjects

Gingivalb

iopsies

from

human

cytomegalovirus-positive

individualswithperiodontitishad

higher

expressionofm

RNAfor

collagensIan

dIIIcompared

with

biopsies

from

human

cytomegalovirus-negative

individuals

Watan

abe

etal.2007(203)

Brazil

30patientswithaggressive

periodontitis

Periodontitissites:57%

Gingivitissites:30%

Prevalence:6%

Imbronito

etal.2008(98)

Brazil

40patientswithch

ronicperiodontitis

Subgingivalp

laque:45%

Saliva:37.5%

Blood:25%

Subgingivalp

laque:82.5%

Saliva:75%

Blood:82.5%

Grande

etal.2008(82)

Brazil

50HIV-positive

patientswithch

ronic

periodontitisan

d50

HIV-negativecontrol

patients

Subgingivalp

laque:

HIV+:72%

HIV:

48%

Saliva:

HIV+:62%

HIV:

40%

Blood:

HIV+:18%

HIV:

24%

Subgingivalp

laque:

HIV+:82%

HIV:

80%

Saliva:

HIV+:72%

HIV:

80%

Blood:

HIV+:68%

HIV:

84%

Subgingivalp

laque:

HIV+:6%

HIV:

16%

Saliva:

HIV+:18%

HIV:

24%

Blood:

HIV+:6%

HIV:

8%

Contreras et al.

76

Tab

le6.

(Con

tinued)

Author/year

Country

Number

ofsubjects

Virus

EpsteinB

arrvirus-1

Human

cytomegalovirus

Herpes

simplexvirustype1

Grande

etal.2011(83)

Brazil

27HIV-positive

patientswithch

ronic

periodontitisan

d23

HIV-positive

patients

withgingivitis

Subgingivalp

laque:

Periodontitis:70.4%

Gingivitis:78.3%

Saliva:

Periodontitis:81.5%

Gingivitis:52.2%

Blood:

Periodontitis:22%

Gingivitis:13%

Subgingivalp

laque:

Periodontitis:74%

Gingivitis:91.3%

Saliva:

Periodontitis:77.7%

Gingivitis:65.2%

Blood:

Periodontitis:74.1%

Gingivitis:60%

Subgingivalp

laque:

Periodontitis:3.7%

Gingivitis:8.7%

Saliva:

Periodontitis:14.8%

Gingivitis:17.4%

Blood:

Periodontitis:0%

Gingivitis:13%

Nishiyam

aet

al.2008(143)

Brazil

50patientswithch


d50

healthysubjects

Chronicperiodontitis:3.4%

Healthyperiodontium:0%

Casarin

etal.2010(29)

Brazil

46patientswithch


dtype2diabetes

Ahigher

freq

uen

cyof

EpsteinB

arrvirusin

shallowperiodontal

pocketsofp

atientswith

poorlycontrolleddiabetes

Glycemiccontrold

idnotinuen

cethefreq

uen

cyofh

uman

cytomegalovirus

Escalona

etal.2011(63)

Ven

ezuela

20HIV-positive

patientswithch

ronic

periodontitis,7HIV-negativepatientswith

chronicperiodontitisan

d7HIV-negative

subjectswithhealthyperiodontium


77

sies from cytomegalovirus-positive individuals withperiodontitis than in biopsies from cytomegalovirus-negative patients with periodontitis. The ability ofcytomegalovirus to upregulate the expression ofmRNA for collagens and metalloproteinases maycontribute to the development of periodontitis.Other pathways by which herpesviruses may causeperiodontitis include direct cytopathic effects onbroblasts, keratinocytes and other types of cells(19, 20, 40, 83) and synergistic pathogenetic interac-tions with periodontopathic bacteria (22, 172, 179).In Brazil, Watanabe et al. (203) detected Epstein

Barr virus-1 in 57% of sites with aggressive periodon-titis and in 30% of sites with gingivitis; the relative riskfor periodontitis was 3.05 with a condence intervalof 1.436.47. Cytomegalovirus was found in 6% of thestudy individuals (203). Imbronito et al. (98) identi-ed EpsteinBarr virus-1 in 45% of chronic periodon-titis samples, 38% of salivary samples and 25% ofperipheral blood samples. Cytomegalovirus wasdetected in 82% of the periodontitis and blood sam-ples and in 75% of the saliva samples (98). Grandeet al. (82), in a study of HIV-infected subjects, foundcytomegalovirus in 82% of periodontitis sites of HIV-positive and in 80% of periodontitis sites of HIV-nega-tive patients, and EpsteinBarr virus-1 in 72% of peri-odontitis sites of HIV-positive and in 48% ofperiodontitis sites of HIV-negative patients. Inanother study of HIV, Grande et al. (83) detectedcytomegalovirus and EpsteinBarr virus-1 in, respec-tively, 74% and 70% of periodontitis samples, in 77%and 81% of salivary samples, and in 74% and 22% ofperipheral blood samples. Herpes simplex-1 virusoccurred with a frequency of 4% in periodontitis sam-ples and 15% in salivary samples, and was notdetected in blood samples (83). Nishiyama et al. (143)also found a low occurrence (3%) of herpes simplex-1virus in periodontitis lesions. Casarin et al. (29) stud-ied the relationship between herpesviruses and peri-odontal status in patients with type 2 diabetes andfound EpsteinBarr virus in 81% of shallow periodon-tal sites of patients with poor glycemic control and in43% of shallow periodontal sites of patients with goodglycemic control (P = 0.05). Cytomegalovirusoccurred in 3343% of shallow periodontal sites, withno preference for poorly controlled diabetes (29). Theelevated prevalence of herpesviruses in periodontalsites of patients with type 2 diabetes may partlyexplain the elevated risk of these patients for develop-ing periodontitis.Human viruses other than herpesviruses can also

reside in the periodontium. Escalona et al. (63) inVenezuela studied the presence of human papilloma-

virus in periodontal pocket samples of HIV-infectedpatients. Papillomavirus was detected in 46% of HIV-positive patients receiving anti-retroviral treatment,but was not found in HIV-seronegative patients (63).Horewicz et al. (95) did not detect the oncogenic pap-illomavirus type 16 in samples from chronic peri-odontitis, gingivitis or healthy periodontium. Linset al. (116) found that individuals orally infected withthe human T-lymphotropic virus type I were moreaffected by periodontitis than were noninfectedcontrols.

The future of periodontalmicrobiology in Latin America

A healthy periodontium is important for overall oralhealth, but the increasing evidence that periodontitisalso can have systemic consequences raises treat-ment of periodontal disease to a new level of impor-tance (38, 102, 154, 197). Periodontal disease has aglobal distribution, but is particularly prevalent andsevere in low-income individuals. Many periodontitispatients of Central and South America do not receiveadequate periodontal therapy because of economicand social constrains and a scarcity of affordable den-tal services. There is a need to nd safe and effectivemethods to control periodontal infections in LatinAmerican populations with limited access to profes-sional dental care.Knowledge of the periodontal microbiota is critical

for implementing a successful periodontal therapy.Periodontal therapy aims to control periodontopathicmicroorganisms by means of mechanical pocketdebridement, periodontal pocket irrigation withpotent antiseptics, treatment of advanced diseasewith systemic antibiotics and attention to proper self-care. The worldwide increase in antibiotic-resistantbacteria and the high costs of new, effective antibiot-ics have created interest in the use of inexpensiveantiseptics to combat periodontal infections. Antisep-tics are broad-spectrum microbicidal agents that areapplied topically onto living tissue to prevent or treatclinical infections caused by bacteria, yeasts andviruses (174, 175). Unlike antibiotics, antisepticsdestroy periodontal bacteria and viruses in a nondis-criminative manner and can cover the entire spec-trum of traditional periodontal pathogens, gram-negative enteric rods and superinfecting organisms(190, 191). Low-cost periodontal therapy, based pre-dominantly on antiseptic agents, may help to meetthe unmet treatment needs of large impoverishedpopulations in Latin America (57, 174, 175).

Contreras et al.

78

Although research in periodontal microbiology issteadily increasing in Central and South America,several research issues in periodontology remainunresolved and merit attention. It is critical to estab-lish a clear denition of periodontal diseases andproper periodontal diagnoses to make studies com-parable. Studies that compare the microbiology ofperiodontal disease in various socio-economic groupshave yet to be undertaken in most Latin Americancountries. Microbiological risk factors for periodontaldisease and effective periodontal treatments remainto be identied for immunocompromised and non-compromised patients. And nally, the growing reali-zation that periodontal infections may give rise tosystemic illness, perhaps especially in immunocom-promised individuals, ought to be a high-priorityresearch topic. Signicant progress in molecularmicrobiology has made such studies possible, even inlow-budget laboratories. Continued research in peri-odontal microbiology is poised to generate discover-ies that can form the basis for more effectiveapproaches to the prevention and treatment ofdestructive periodontal disease in Latin America.

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