Dental bacterial plaques Nature and role in periodontal disease
Lars A. Christersson, Joseph J, Zambon and Robert J. Genco Departments of Oral Biology and Periodontology, School of Dental Medicine, State University of New York at Buffalo, 3435 Main Street, Buffalo, N.Y 14214, USA
Christersson LA, Zambon JJ and Genco RJ: Dental bacterial plaques. Nature and role in periodontal disease. J Clin Periodontol 1991; 18: 441—446. Abstract. Antony van Leeuwenhoek first described oral bacteria. However, not until almost 200 years later was the famous Koch postulate introduced. Since then, research has extensively been performed regarding the development and microbiology of dental plaques. In spite of the complexity of the developing flora of supragingival plaque, culture studies have shown a remarkably orderly succession of organisms. Lately, the concept of microbial specificity in the etiology of periodontal diseases has been widely suggested, i.e., that different forms of periodontal disease are associated with qualitatively distinct dental plaques. Cross-sectional and longitudinal studies of the predominant cultivable microflora reveal that only a small number of the over 300 species found in human subgingival plaques are associated with periodontal disease. Among the commonly mentioned are: Actinobacillus actinomycetemcomitans, Bacteroides gingivalis, Bacteroides intermedius, Capnocytophaga sp., Eikenella corrodens, Fusobacterium nucleatum, and Wolinella recta, as well as certain gram-positive bacteria such as Eubacterium species. Anti-infective therapy for many systemic infections equals the use of antimicrobial drugs. However, for localized infections like periodontal diseases, treatment may consist of a combination of mechanical wound debridement and the application of an antimicrobial agent. The general effectiveness of mechanical anti-infective therapy and successful oral hygiene in the management of periodontal disease is well established in the literature and has met the test of success in clinical practice for most cases of periodontitis in adults. The definition of periodontal pathogens as either opportunistic pathogens, or as exogenous pathogens carries with it significant implications. If periodontal disease results from an opportunistic infection by indigenous micro-organisms, then preventive efforts should be directed toward removing most plaque from all tooth surfaces. However, if periodontal diseases result from a subgingival infection with exogenous pathogens, appropriate preventive strategies may be used for control of oral colonization or subgingival growth.
Antony van Leeuwenhoek 1683, in a letter to the Royal Society in London, was the first one to describe oral bacteria (animacules) (Dobell 1960). He described his oral hygiene efforts, including the use of salt, and concluded that despite these, he could observe more living organisms in his oral cavity than human beings in his home country The Netherlands. He also made the observation that he had exceptionally good oral health, and that his gums did not bleed when cleaned. Despite this remarkable accomplishment, it took almost 200 years until mankind 1 .'alized the relationship between baci.ria and disease when Koch (1876) i lowed that anthrax in cattle was caused 1 V a specific bacteria. His extensive re5 arch later led to the development of 1 och's postulate, i.e. that to claim bact rial specificity: (1) a bacteria should be
Key words: dental plaques; exogenous pathogens; preventive strategies; specific periodontitis pathogens Accepted for publication 19 December 1990
In contrast, Bass & Johns (1915) hyable to be isolated from the diseased pothesized that a specific micro-organtissues; (2) pure cultures can be obtained; ism, Endoameba buccalis, was the cause (3) that the bacteria when inoculated in experimental animals should cause the of periodontal disease and that a vaccine disease; (4) that the bacteria should be developed against this micro-organism could be used to prevent tooth loss. Acable to be isolated from the diseased tissues in the experimental animal. As cording to one of the first suggestions of early as 1890, Miller, one of Koch's pu- what is now called the specific plaque hypils, made efforts to isolate the organism pothesis, dental plaques from diseased responsible for pyorrhea. The efforts, sites are different from those adjacent to however, were unsuccessful, and Miller healthy sites and those in normal subconcluded that several organisms were jects. Nevertheless, bacteria-forming plaresponsible for this disease (Miller 1973) which is one of the first statements of ques on the teeth, either supragingivally what has become known as the non-spe- or subgingivally, are the causative agents cific plaque hypothesis. According to responsible for gingivitis and periothis hypothesis, dental plaque is a homo- dontitis (Loe & Silness 1963). Plaque geneous bacterial mass causing peri- control therefore, plays a central key role odontal disease when accumulating to in the therapeutic arsenal directed the point of exceeding host defense ca- toward these diseases, and it is important to understand the formation, developpacity.
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ment and structure of dental plaques (Lindhe & Nyman 1975). Dental plaque is almost exclusively an aggregation of micro-oTganisms and their extracellularly secreted polysaccharides and other matrix substances (Carlsson 1968). Plaques exhibit a definite microscopic architecture with the bacterial cells arranged in clumps or columns of microcolonies. The cellular density varies, and depends on diet and bacterial composition, Supragingivai plaques in general have a higher density than subgingival plaques, which have both solid aad semi-liquid states. Plaque formation
Dental plaque development on exposed tooth surfaces begins with the precipitation of a salivary derived pellicle (Dawes et al. 1963). This salivary pellicle forms on artificial tooth surfaces and cientures as well as on natural teeth (Sonju & Glantz 1975), and is an organic film derived mainly from the saliva which is deposited on the tooth surface. Saliva per se consists of 95% water and 5% soluble organic (potassium, sodium, calcium, chloride, carbonate and hypophosphate ions) and inorganic components (mucopolysaccharides - glycoproteias) (Sonju & Glantz 1975). Whole saliva also contains cellular elements, including bacteria, PMN cells, epithelial cells and, associated with gingival inflammation, erythrocytes. The bacterial density in saliva corresponds to approximately 2x10** bacteria/ml. Pellicle contains few bacteria in its early stages, however, a few hours after its deposition, oral bacteria adhere to the pellicle, forming the basis for plaque accumulation. Microbiological studies of developing plaque formation have shown that bacterial adhesion to the pellicle takes place very rapidly, within a few minutes after pumicing the surface (Van Houte et al. 1970,1971). The first types of organisms found on the tooth surface are cocci and rods. Mainly, Streptococcus sanguis (Krasse 1954, Gibbons et a.1. 1964, Carlsson 1967) and gram-positive facultative pleomorphic rods like Actinomyces viscosvs and Actinomyces israelii. Few or no gram-negative orgaaisms are detected in these very early plaques (Gibbons & Van Houte 1973). Studies of plaque composition in healthy oral cavities over a period of 2 to 3 weeks led Loe et al. (1965) to describe microbial maturation of plaques associated with experimental gingivitis. Start-
ing with a cleaned tooth surface, there are three relatively distinct phases of plaque formation with some deviation dependent on individual variations. The first phase (days 0-2) exhibits a proliferation of gram-positive cocci and rods and an addition of 30% gram-negative cocci and rods, proportions reflecting the usual distribution of these components in whole saliva. The second phase (1 to 4 days) is characterized by the appearance and increase in numbers of fusobacteria and filaments and the third phase (4 to 9 days) is characterized by the appearance of spirilla and spirochetes. Gingivitis is clinically detectable at the time of formation of these complex, mature supragingivai plaques found in 4—9 days.
forms are present in small numbers, frequently on the outer surface of the microhial layer and few fiagellated cells or spirochetes are observed in the microhial flora associated with the normal state. In gingivitis only, the microbial flora is associated with the enamel surface of the tooth. A variety of micro-organisms including coccoid as well as filamentous forms are present. The deeper layers of the bacterial mass have undergone lysis, and mineralization of cells and zones is common. Filamentous bacteria are relatively more numerous than in the normal samples, and the dense masses are occasionally covered with "corncob" formations comprised of long filaments covered with cocci (Gibbons & Nygaard 1970). Flagellated bacteria and spirochetes are observed in the apical Microbial Composition of Dentai portions of the plaque adjacent to the Piaques gingiva. In spite of the complexity of the deIn periodontitis, the plaques extend veloping flora of supragingivai plaque subgingivally into an area bordered by left undisturbed for 7 to 10 days, culture the root surface and the pocket epithestudies have shown a remarkably or- lium. Filamentous forms are prominent, derly succession of organisms. Strepto- but the morphological cell types encocci and Actinomyces are involved in countered in the gingivitis sample are earliest plaques. As the plaque matures, also observed in the periodontitis there are increases in proportions of sample. these organisms, with addition of others The suhgingival plaque has a loosely such as Fusobacterium, Veillonella, Tre- arranged zone of motile organisms. On ponema, and Bacteroides species. This the surface of this adherent layer, at the order of succession is mainly due to de- bacterial-tissue interface, many of the pendencies related to local ecology and micro-organisms, are fiagellated. There nutritional demands (Socransky 1977), are also many "bristle-hrush" or "test and the mature plaque is often associ- tube-brush" formations, surrounded by ated with gingivitis. spirochetes and other small motile orSubgingival plaque appears under the ganisms (Listgarten 1976). light microscope as a mass of bacterial The subgingival microhial mass cells with filamentous bacteria at right closest to the pocket epithehum is generangles to the pellicle near the tooth sur- ally covered with polymorphonuclear face. Closer to the periphery, the fila- leukocytes and a few mononuclear cells. ments are curved and irregular. In the These neutrophils occasionally contain outer, younger portion of plaque, many internalized bacteria, and often appear cocci and other small bacterial forms degranulated. Some of the suhgingival are found (Saxton 1973). bacteria attach to and penetrate the ginThe microhial flora associated with gival pocket epithelium (Alhini et al. the tooth and periodontal tissues in 1988). various states of health and disease The surfaces of the teeth extracted show a high level of organization (Li- from localized juvenile periodontitis pastgarten 1976), with marked differences tients are remarkable for their usual between plaques seen in health and dis- lack of grossly detectable calculus or ease (Slots 1977, 1979, Listgarten 1984). other surface deposits corresponding tc In the normal state of periodontal the pocket size (Baer 1971). Wher health, the dental plaque microbial flora examined microscopically, however is supragingivai, mostly confined to the these tooth surfaces are frequently enamel surface. Bacteria associated with covered with a thick cuticle exhibiting healthy gingiva are predominantly coc- an irregular contour and bacteria coid in shape, with a majority exhibiting plaques. Small clumps of gram-negativ gram-positive cell wall features. Gram- coccoid bacteria and polymorphonu negative organisms and filamentous clear leukocytes in varying stages of dis
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integration are intimately associated hence, it is impossible to identify the the oral micro-organisms which has with the lobulated root surface cuticle. specific micro-organisms responsible been strongly implicated in the pathoThin filaments with loosely adapted for periodontal disease using the criteria genesis of localized juvenile periogram-negative cell walls form deposits for Koch's postulate. Alternative cri- dontitis (Zambon 1985). This micro-orcovering the cemental surface. The bac- teria have been proposed by Socransky ganism is also associated with cases of terial population associated with these (1977) to identify the key micro-organ- adult periodontitis in which alveolar teeth is a sparse gram-negative flora and isms in periodontal infections. These in- bone loss occurs at an unusually rapid rate (Tanner et al. 1979) and periorelatively simple when compared to the clude the following: dontitis which continues to progress (1) The presence of the putative populations seen in periodontitis and pathogen in proximity to the peri- after meticulous scaling, root planing, gingivitis (Listgarten 1976). Ultrastructural studies have shown odontal lesions and in high numbers plaque control, and even periodontal that there are many types of microbes compared to either the absence of the surgery (Slots 1986, Slots et al. 1986, associated with periodontal tissues in micro-organism or its presence in much Van Winkelhoff et al. 1989b). Initial studies of the microflora in health and disease. In periodontitis and smaller numbers (carrier state) in perilocalized juvenile periodontitis, the odontally normal subjects or in subjects LJP lesions revealed high numbers of subgingival plaques fill the periodontal with other forms of periodontal disease. an unknown gram-negative rod (Slots 1976, Newman & Socransky 1977), a pockets with a loosely arranged fiora (2) Patients infected with these perifound at the advancing front of the odontal pathogens often develop high micro-organism identified as A. actinomycetemcomitans. Subsequent studies lesion. The microbes at this tissue inter- levels of antibody in serum, saliva, and face are likely to be of major importance gingival crevicuiar fluid and may also of localized juvenile periodontitis pain the destructive events occurring in develop a cell-mediated immune re- tients often demonstrated that a large sponse to the putative pathogen. (3) proportion of the subgingival flora periodontal disease. These micro-organisms can often dem- comprises A. actinomycetemcomitans in onstrate in vivo production of virulence lesion sites while adjacent periodontally Bacterial Specificity in Dentai factors that can be correlated with clin- healthy sites exhibited few if any A. actiPlaques ical histopathology. (4) Experimental nomycetemcomitans (Slots et al. 1980). During the past two decades, a new idea implantation of the organism into the Today, several independent studies has emerged: the concept of microbial gingival crevice of an appropriate ani- show that A. actinomycetemcomitans is almost invariably associated with LJP specificity in the etiology of periodontal mal model should lead to development (Ranney et al. 1982, Slots & Rosling of at least some of the characteristics disease (Loesche 1976, 1979, Socransky 1983, Zambon et al. 1983, Genco et al. 1977). Previously, it was believed that of the naturally occurring disease, e.g., 1985, Zambon 1985, Asikainen et al. inflammation, connective tissue disrupperiodontal disease resulted from the 1986, Mandell et al. 1986). gross non-specific accumulation of den- tion, and bone loss. (5) Clinical treatSerological (Zambon et al. 1983) and tal plaques. The many different forms of ment that eliminates these micro-organisms from periodontal lesions should reimplantation studies (Christersson et al. periodontal disease are now, however, 1985) suggest that A. actinomycetemcothought to be associated with qualitat- sult in clinical improvement. mitans can be transmitted among family ively distinct dental plaques. Out of the members. It does not appear to be read300 to 400 bacterial species which can Gingivitis and Periodontitis as ily transmissible, and multiple contacts inhabit the human oral cavity, crossSpecific Infections are probably required for oral colonizsectional and longitudinal studies of the predominant cultivable microflora re- Continuous loss of connective tissue ation to occur. However, individual case veal that only a small number of species attachment is an uncommon event even reports, as well as the studies on A. are associated with human periodontal in patients who have had previous actinomycetemcomitans distribution, indisease (Moore et al. 1983). The concept periodontitis and who still have a sig- dicate that the disease may be considered transmissable (Zambon et al. of bacterial specificity has been further nificant degree of gingival inflammation 1983, Preus & Olsen 1988). supported by clinical observations, by (Goodson et al. 1982, Lindhe et al. 1983, B. gingivalis is found in high frethe therapeutic effect of control of these Listgarten et al. 1985). Furthermore, organisms, and by experimental models loss of attachment is not always seen quency and in high numbers, often as of periodontitis in both gnotobiotic and even in patients with severe forms of a major component of the subgingival conventionally maintained animals. gingival inflammation. These obser- flora, in adult periodontitis lesions. In A variety of predominantly gram- vations suggest that gingivitis and perio- contrast, subgingival dental plaque negative organisms have been impli- dontitis may be discrete disease pro- from periodontally normal subjects shows a much lower frequency and cated in the etiology of periodontal dis- cesses with distinct etiologies. The identification of specific oral fewer number or none at all of B. ginease, including Actinobacillus actinomycetemcomitans, Bacteroides gingivalis, micro-organisms, associated with les- givalis. Furthermore, B. gingivalis is not Fsacteroides intermedius, Capnocytopha- ions in different forms of human peri- detectable in subgingival flora of pam sp., Eikenella corrodens, Fusobacteri- odontal disease has significant impli- tients with gingivitis who are not affect:/in nucleatum, and WoUnella recta, as cations. Several advances have been ed by periodontitis (Christersson et al. 1989). 'ell as certain gram-positive bacteria made, particularly regarding the imInterestingly, black-pigmented Bacportance of A. actinomycetemcomitans ach as Eubacterium species (Moore et in human periodontal disease, as well as teroides is not often found in the suprai, 1983). gingival plaque from adult periodontitis Periodontal disease occurs in an area the role of some Bacteroides species. patients, but it appears that B. gingivalis A. actinomycetemcomitans is one of . ormally inhabited by many bacteria.
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colonizes the saliva and most oral mucous surfaces of periodontitis patients. Preliminary studies of the vagina, the gut, and feces have not yielded B. gingivalis, so it appears that the primary ecologic niche of S. gingivalis is the oral mucous membranes and the subgingival region of subjects with adult forms of periodontitis (Van Winkelhoff et al. 1989).
In clinical practice as well as in research on periodontal therapy, dental plaque is often scored as a dichotomy, presence or absence of detectable plaque. A simple but reliable data acquisition, based on yes or no answers collected over an extended number of surfaces are intuitively more relevant and useful in analyses, as well as in conclusions regarding clinical significance.
Clinical Assessment of Dental Plaques .
Principles for Anti-infective Periodontal Therapy
Supragingival plaques are readily detectable with tile naked eye after reaching a certain thickness. This occurs in 1 or 2 days in areas where the plaques are not removed ititentionally or by the forces of mastication and other oral functions. They are yellow or whitish and often thickest along the gingival third of the tooth, and in the interproximal areas. When too sparse to be detected, the presence of dental plaque may be determined by use of disclosing solution. Plaque can also be detected by scraping the tooth surface with a probe or sealer. Siipragingival plaque is usually found at the gingival third of the crown, an area which is not naturally self-cleansing. The abrasiveness of food, oral hygiene, and the action of normal mastication are often sufficient to prevent significant plaque deposits from forming on the smooth occlusal surfaces and the areas occlusal of the buccal and lingual prominence of the crown. Also, plaque deposits are regularly present in fissures, pits and irregularities such as cracks or undulations of the surfaces. Subgingival plaques are usually thin, contained within the periodontal pocket or gingival cre\^ice, and hard to visualize in situ. Subgingival deposits can be detected after removal from the pocket by scraping the root surface with a probe or sealer. There are several sampling procedures for the microbial assessment of the periodontal flora which require sampling of subgingival plaques with absorbent sterile paper points or with other sampling devices. Such subgingival samples are then evaluated microbiologically, by culturing, or by rapid tests using specific a.ntibodies or nucleic acid probes, for their content of periodontal pathogens. Plaque indices are often used in clinical experiments to demonstrate rather small changes and to obtain manageable data suited for statistical analyses.
Anti-infective therapy, i.e., those procedures which control the disease-causing micro-organisms, for many systemic infections equals the use of antimicrobial drugs. For localized infections like periodontal diseases, treatment often consists of a combination of mechanical wound debridement and the application of antimicrobial agents. The most important part of the battery of anti-infective procedures employed in the treatment of gingivitis and periodontitis, is personal oral hygiene resulting in regular supragingival plaque removal. Several studies show that mechanical debridement procedures to remove the bulk of the infection are effective in the treatment of gingivitis and most mild to moderate forms of periodontitis in adults (Badersten et al. 1981, Ramfjord 1987). While anti-infective therapy is adequate for mild to moderate periodontitis patients, periodontal surgery may be necessary for patients with advanced periodontitis with deep pockets to provide access for complete root debridement (AntczakBoukoms & Weinstein 1977). Mechanical anti-infective therapy, combined with successful oral hygiene, has proven its general effectiveness in the management of periodontal disease, and has been used successfully in clinical practice for most cases of gingivitis, and mild to moderate periodontitis in adults (Badersten et al. 1981, Ramfjord 1987). The paramount role of supragingival plaque control is clearly shown. In an experimental model for the evaluation of different surgical periodontal therapies, Rosling et al. (1976) showed that the key element for a successful outcome of therapy was total plaque control, in these studies achieved by bi-weekly professional tooth cleanings for up 2 years. As a "bonus", information derived from these studies, which is not often recognized, includes the fact that periodontal
surgical therapy followed by poor infection control, i.e. inadequate personal plaque control, may lead to an exacerbation of the periodontal condition (Rosling et al. 1976). Later, Lindhe & Nyman (1984) described long-term results of periodontal therapy and again confirmed the pivotal role of plaque control level reached by the patients. Summary and Conclusions
The concept of periodontal diseases being associated with specific microorganisms not regularly found in the healthy gingival sulci and/or oral cavity, raises questions as to the nature of these species. Those organisms for which the oral cavity is a primary habitat and which do not normally cause disease, are the indigenous or resident fiora. On the other hand, those which are not part of the resident microfiora and which cause disease, are exogenous pathogens. Indigenous and many exogenous microorganisms are normally non-pathogenic bacteria but can, under circumstances such as reduced host resistance or overgrowth, cause disease in which case they may be considered opportunistic pathogens. The definition of periodontal pathogens as either opportunistic pathogens or as exogenous pathogens carries with it significant implications. If periodontal disease results from an opportunistic infection by indigenous microorganisms, then preventive efforts should be directed toward removing most plaque from all tooth surfaces. Such a protocol will likely suppress the emergence of opportunistic pathogens and prevent the development of gingivitis and some forms of periodontitis. This may, however, be over-treatment for the majority of individuals. If periodontal disease results from subgingival infection with exogenous pathogens, an appropriate preventive strategy may be interference with oral colonization or subgingival growth of the exogenous pathogen(s). This antiinfective approach could be targeted to specific micro-organisms rather than to the plaque mass as a whole. The methods for such an anti-infective approach to suppress exogenous pathogens include: (a) specific agents whicl: will eliminate the pathogens from the flora, (b) immunization to inhibit colon ization or (c) replacement therapy ii which a stable, periodontal health-as sociated subgingival flora is establishec
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bacillus actinomycetemcomitans-assodated Goodson, J. M. & Socransky, S. S. (1986) periodontal disease. Journal of PeriodontThe effect of treatment on Actinobaciifus ology 56, 41-50. actinomycetemcomitans in localized juvenile periodontitis. Journal of Periodontology Gibbons, R. J., Kapsimalis, B. & Socransky, 57, 94-99. S. S. (1964) The source of salivary bacteria. Archives of" Oral Biology 9, 101-103. Miller, W. D. (1973) Micro-organisms of the Acknowledgements Gibbons, R. J. & Nygaard, M. (1970) Interhuman mouth. Basel, Switzerland: S, bacterial aggregation of plaque bacteria. Karger. Supportd in part by USPHS Grant no. Archives of Oral Biology 15, 1397-1400. Moore, W. E. C, Holdeman, L. Y, Cato, B, DE04898. The authors also wish to Gibbons, R. J. & Van Houte, J. (1973) On P., Smibert, R. M., Burmeister, J. A. & thank Mrs. Susan Hanlon and Ms. the formation of dental plaque. Journal of Ranney, R. R. 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by introducing innocuous bacteria into the oral cavity to block subsequent colonization by exogenous pathogens.
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givalis and Bacteroides intermedius in deand Streptococcus sanguis on the human structive periodontal disease in adults. tooth surface. Archives of Oral Biology 15, Journal of Clinical Periodontoiogy 13, 1025-1034. 570-577. Van Houte, J., Gibbons, R. J. & Pulkkinen, Socranscky, S. S. (1977) Microbiology of A. J. (1971) Adherence as an ecological periodontal disease - Present status and determinant for Streptococci in the human future considerations. Journal of Periomouth. Archives of Oral Biology 16, dontoiogy 48, 497-504. 1131-1141. Sonju, T. & Glantz, P.-O. (1975) Chemical Van Winkelhoff, A. J., Christersson, L. A., composition of salivary integuments Batt, R. E., Zambon, J. J., Reynolds, H. & formed in vivo on solids with some estabGenco, R. J. (1989a) Black-pigmented lished surface characteristics. Archives of Bacteroides on non-oral mucous memOral Biology 20, 687-691. branes. Journal of Dental Research 68, Tanner, A. C, Haffer, C , Bratthall, G. T., AADR abstr no. 602. Visconti, R. A. & Socransky, S. S. (1979) Van Winkelhoff, A. J., Rodenburg, J. P., :; A study of the bacteria associated with Goene, R. J., Abbas, K, Winkel, E. G. & . advancing periodontitis in man. Journal of De Graaff, J. (1989b) Metronidazole plus Clinical Periodontoiogy 6, 278-307. amoxycillin in the treatment of ActinoVan Houte, J., Gibbons, R. J. & Banghart, bacillus actinomycetemcomitans associated S. B. (1970) Adherence as a determinant periodontitis. Journal of Clinical Periodontoiogy 16, 128-131. .; of the presence of Streptococcus salivarius
Zambon, J. J. (1985) Actinobacillus actinomycetemcomitans in human periodontal disease. Journal of Clinical Periodontoiogy 12, 1-20. Zambon, J. J., Christersson, L. A. & Slots, J. (1983) Actinobacillus actinomycetemcomitans in human periodontal disease. Prevalence in patient groups and distribution of biotypes and serotypes within families. Journal of Periodontoiogy 54, 707-711. Address: L. A. Christersson Departments of Oral Biology and Periodontoiogy School of Dental Medicine SUNY at Buffalo 3435 Main Street Buffalo, NY 14214 USA
Lars A. Christersson, Joseph J, Zambon and Robert J. Genco Departments of Oral Biology and Periodontology, School of Dental Medicine, State University of New York at Buffalo, 3435 Main Street, Buffalo, N.Y 14214, USA
Christersson LA, Zambon JJ and Genco RJ: Dental bacterial plaques. Nature and role in periodontal disease. J Clin Periodontol 1991; 18: 441—446. Abstract. Antony van Leeuwenhoek first described oral bacteria. However, not until almost 200 years later was the famous Koch postulate introduced. Since then, research has extensively been performed regarding the development and microbiology of dental plaques. In spite of the complexity of the developing flora of supragingival plaque, culture studies have shown a remarkably orderly succession of organisms. Lately, the concept of microbial specificity in the etiology of periodontal diseases has been widely suggested, i.e., that different forms of periodontal disease are associated with qualitatively distinct dental plaques. Cross-sectional and longitudinal studies of the predominant cultivable microflora reveal that only a small number of the over 300 species found in human subgingival plaques are associated with periodontal disease. Among the commonly mentioned are: Actinobacillus actinomycetemcomitans, Bacteroides gingivalis, Bacteroides intermedius, Capnocytophaga sp., Eikenella corrodens, Fusobacterium nucleatum, and Wolinella recta, as well as certain gram-positive bacteria such as Eubacterium species. Anti-infective therapy for many systemic infections equals the use of antimicrobial drugs. However, for localized infections like periodontal diseases, treatment may consist of a combination of mechanical wound debridement and the application of an antimicrobial agent. The general effectiveness of mechanical anti-infective therapy and successful oral hygiene in the management of periodontal disease is well established in the literature and has met the test of success in clinical practice for most cases of periodontitis in adults. The definition of periodontal pathogens as either opportunistic pathogens, or as exogenous pathogens carries with it significant implications. If periodontal disease results from an opportunistic infection by indigenous micro-organisms, then preventive efforts should be directed toward removing most plaque from all tooth surfaces. However, if periodontal diseases result from a subgingival infection with exogenous pathogens, appropriate preventive strategies may be used for control of oral colonization or subgingival growth.
Antony van Leeuwenhoek 1683, in a letter to the Royal Society in London, was the first one to describe oral bacteria (animacules) (Dobell 1960). He described his oral hygiene efforts, including the use of salt, and concluded that despite these, he could observe more living organisms in his oral cavity than human beings in his home country The Netherlands. He also made the observation that he had exceptionally good oral health, and that his gums did not bleed when cleaned. Despite this remarkable accomplishment, it took almost 200 years until mankind 1 .'alized the relationship between baci.ria and disease when Koch (1876) i lowed that anthrax in cattle was caused 1 V a specific bacteria. His extensive re5 arch later led to the development of 1 och's postulate, i.e. that to claim bact rial specificity: (1) a bacteria should be
Key words: dental plaques; exogenous pathogens; preventive strategies; specific periodontitis pathogens Accepted for publication 19 December 1990
In contrast, Bass & Johns (1915) hyable to be isolated from the diseased pothesized that a specific micro-organtissues; (2) pure cultures can be obtained; ism, Endoameba buccalis, was the cause (3) that the bacteria when inoculated in experimental animals should cause the of periodontal disease and that a vaccine disease; (4) that the bacteria should be developed against this micro-organism could be used to prevent tooth loss. Acable to be isolated from the diseased tissues in the experimental animal. As cording to one of the first suggestions of early as 1890, Miller, one of Koch's pu- what is now called the specific plaque hypils, made efforts to isolate the organism pothesis, dental plaques from diseased responsible for pyorrhea. The efforts, sites are different from those adjacent to however, were unsuccessful, and Miller healthy sites and those in normal subconcluded that several organisms were jects. Nevertheless, bacteria-forming plaresponsible for this disease (Miller 1973) which is one of the first statements of ques on the teeth, either supragingivally what has become known as the non-spe- or subgingivally, are the causative agents cific plaque hypothesis. According to responsible for gingivitis and periothis hypothesis, dental plaque is a homo- dontitis (Loe & Silness 1963). Plaque geneous bacterial mass causing peri- control therefore, plays a central key role odontal disease when accumulating to in the therapeutic arsenal directed the point of exceeding host defense ca- toward these diseases, and it is important to understand the formation, developpacity.
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ment and structure of dental plaques (Lindhe & Nyman 1975). Dental plaque is almost exclusively an aggregation of micro-oTganisms and their extracellularly secreted polysaccharides and other matrix substances (Carlsson 1968). Plaques exhibit a definite microscopic architecture with the bacterial cells arranged in clumps or columns of microcolonies. The cellular density varies, and depends on diet and bacterial composition, Supragingivai plaques in general have a higher density than subgingival plaques, which have both solid aad semi-liquid states. Plaque formation
Dental plaque development on exposed tooth surfaces begins with the precipitation of a salivary derived pellicle (Dawes et al. 1963). This salivary pellicle forms on artificial tooth surfaces and cientures as well as on natural teeth (Sonju & Glantz 1975), and is an organic film derived mainly from the saliva which is deposited on the tooth surface. Saliva per se consists of 95% water and 5% soluble organic (potassium, sodium, calcium, chloride, carbonate and hypophosphate ions) and inorganic components (mucopolysaccharides - glycoproteias) (Sonju & Glantz 1975). Whole saliva also contains cellular elements, including bacteria, PMN cells, epithelial cells and, associated with gingival inflammation, erythrocytes. The bacterial density in saliva corresponds to approximately 2x10** bacteria/ml. Pellicle contains few bacteria in its early stages, however, a few hours after its deposition, oral bacteria adhere to the pellicle, forming the basis for plaque accumulation. Microbiological studies of developing plaque formation have shown that bacterial adhesion to the pellicle takes place very rapidly, within a few minutes after pumicing the surface (Van Houte et al. 1970,1971). The first types of organisms found on the tooth surface are cocci and rods. Mainly, Streptococcus sanguis (Krasse 1954, Gibbons et a.1. 1964, Carlsson 1967) and gram-positive facultative pleomorphic rods like Actinomyces viscosvs and Actinomyces israelii. Few or no gram-negative orgaaisms are detected in these very early plaques (Gibbons & Van Houte 1973). Studies of plaque composition in healthy oral cavities over a period of 2 to 3 weeks led Loe et al. (1965) to describe microbial maturation of plaques associated with experimental gingivitis. Start-
ing with a cleaned tooth surface, there are three relatively distinct phases of plaque formation with some deviation dependent on individual variations. The first phase (days 0-2) exhibits a proliferation of gram-positive cocci and rods and an addition of 30% gram-negative cocci and rods, proportions reflecting the usual distribution of these components in whole saliva. The second phase (1 to 4 days) is characterized by the appearance and increase in numbers of fusobacteria and filaments and the third phase (4 to 9 days) is characterized by the appearance of spirilla and spirochetes. Gingivitis is clinically detectable at the time of formation of these complex, mature supragingivai plaques found in 4—9 days.
forms are present in small numbers, frequently on the outer surface of the microhial layer and few fiagellated cells or spirochetes are observed in the microhial flora associated with the normal state. In gingivitis only, the microbial flora is associated with the enamel surface of the tooth. A variety of micro-organisms including coccoid as well as filamentous forms are present. The deeper layers of the bacterial mass have undergone lysis, and mineralization of cells and zones is common. Filamentous bacteria are relatively more numerous than in the normal samples, and the dense masses are occasionally covered with "corncob" formations comprised of long filaments covered with cocci (Gibbons & Nygaard 1970). Flagellated bacteria and spirochetes are observed in the apical Microbial Composition of Dentai portions of the plaque adjacent to the Piaques gingiva. In spite of the complexity of the deIn periodontitis, the plaques extend veloping flora of supragingivai plaque subgingivally into an area bordered by left undisturbed for 7 to 10 days, culture the root surface and the pocket epithestudies have shown a remarkably or- lium. Filamentous forms are prominent, derly succession of organisms. Strepto- but the morphological cell types encocci and Actinomyces are involved in countered in the gingivitis sample are earliest plaques. As the plaque matures, also observed in the periodontitis there are increases in proportions of sample. these organisms, with addition of others The suhgingival plaque has a loosely such as Fusobacterium, Veillonella, Tre- arranged zone of motile organisms. On ponema, and Bacteroides species. This the surface of this adherent layer, at the order of succession is mainly due to de- bacterial-tissue interface, many of the pendencies related to local ecology and micro-organisms, are fiagellated. There nutritional demands (Socransky 1977), are also many "bristle-hrush" or "test and the mature plaque is often associ- tube-brush" formations, surrounded by ated with gingivitis. spirochetes and other small motile orSubgingival plaque appears under the ganisms (Listgarten 1976). light microscope as a mass of bacterial The subgingival microhial mass cells with filamentous bacteria at right closest to the pocket epithehum is generangles to the pellicle near the tooth sur- ally covered with polymorphonuclear face. Closer to the periphery, the fila- leukocytes and a few mononuclear cells. ments are curved and irregular. In the These neutrophils occasionally contain outer, younger portion of plaque, many internalized bacteria, and often appear cocci and other small bacterial forms degranulated. Some of the suhgingival are found (Saxton 1973). bacteria attach to and penetrate the ginThe microhial flora associated with gival pocket epithelium (Alhini et al. the tooth and periodontal tissues in 1988). various states of health and disease The surfaces of the teeth extracted show a high level of organization (Li- from localized juvenile periodontitis pastgarten 1976), with marked differences tients are remarkable for their usual between plaques seen in health and dis- lack of grossly detectable calculus or ease (Slots 1977, 1979, Listgarten 1984). other surface deposits corresponding tc In the normal state of periodontal the pocket size (Baer 1971). Wher health, the dental plaque microbial flora examined microscopically, however is supragingivai, mostly confined to the these tooth surfaces are frequently enamel surface. Bacteria associated with covered with a thick cuticle exhibiting healthy gingiva are predominantly coc- an irregular contour and bacteria coid in shape, with a majority exhibiting plaques. Small clumps of gram-negativ gram-positive cell wall features. Gram- coccoid bacteria and polymorphonu negative organisms and filamentous clear leukocytes in varying stages of dis
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integration are intimately associated hence, it is impossible to identify the the oral micro-organisms which has with the lobulated root surface cuticle. specific micro-organisms responsible been strongly implicated in the pathoThin filaments with loosely adapted for periodontal disease using the criteria genesis of localized juvenile periogram-negative cell walls form deposits for Koch's postulate. Alternative cri- dontitis (Zambon 1985). This micro-orcovering the cemental surface. The bac- teria have been proposed by Socransky ganism is also associated with cases of terial population associated with these (1977) to identify the key micro-organ- adult periodontitis in which alveolar teeth is a sparse gram-negative flora and isms in periodontal infections. These in- bone loss occurs at an unusually rapid rate (Tanner et al. 1979) and periorelatively simple when compared to the clude the following: dontitis which continues to progress (1) The presence of the putative populations seen in periodontitis and pathogen in proximity to the peri- after meticulous scaling, root planing, gingivitis (Listgarten 1976). Ultrastructural studies have shown odontal lesions and in high numbers plaque control, and even periodontal that there are many types of microbes compared to either the absence of the surgery (Slots 1986, Slots et al. 1986, associated with periodontal tissues in micro-organism or its presence in much Van Winkelhoff et al. 1989b). Initial studies of the microflora in health and disease. In periodontitis and smaller numbers (carrier state) in perilocalized juvenile periodontitis, the odontally normal subjects or in subjects LJP lesions revealed high numbers of subgingival plaques fill the periodontal with other forms of periodontal disease. an unknown gram-negative rod (Slots 1976, Newman & Socransky 1977), a pockets with a loosely arranged fiora (2) Patients infected with these perifound at the advancing front of the odontal pathogens often develop high micro-organism identified as A. actinomycetemcomitans. Subsequent studies lesion. The microbes at this tissue inter- levels of antibody in serum, saliva, and face are likely to be of major importance gingival crevicuiar fluid and may also of localized juvenile periodontitis pain the destructive events occurring in develop a cell-mediated immune re- tients often demonstrated that a large sponse to the putative pathogen. (3) proportion of the subgingival flora periodontal disease. These micro-organisms can often dem- comprises A. actinomycetemcomitans in onstrate in vivo production of virulence lesion sites while adjacent periodontally Bacterial Specificity in Dentai factors that can be correlated with clin- healthy sites exhibited few if any A. actiPlaques ical histopathology. (4) Experimental nomycetemcomitans (Slots et al. 1980). During the past two decades, a new idea implantation of the organism into the Today, several independent studies has emerged: the concept of microbial gingival crevice of an appropriate ani- show that A. actinomycetemcomitans is almost invariably associated with LJP specificity in the etiology of periodontal mal model should lead to development (Ranney et al. 1982, Slots & Rosling of at least some of the characteristics disease (Loesche 1976, 1979, Socransky 1983, Zambon et al. 1983, Genco et al. 1977). Previously, it was believed that of the naturally occurring disease, e.g., 1985, Zambon 1985, Asikainen et al. inflammation, connective tissue disrupperiodontal disease resulted from the 1986, Mandell et al. 1986). gross non-specific accumulation of den- tion, and bone loss. (5) Clinical treatSerological (Zambon et al. 1983) and tal plaques. The many different forms of ment that eliminates these micro-organisms from periodontal lesions should reimplantation studies (Christersson et al. periodontal disease are now, however, 1985) suggest that A. actinomycetemcothought to be associated with qualitat- sult in clinical improvement. mitans can be transmitted among family ively distinct dental plaques. Out of the members. It does not appear to be read300 to 400 bacterial species which can Gingivitis and Periodontitis as ily transmissible, and multiple contacts inhabit the human oral cavity, crossSpecific Infections are probably required for oral colonizsectional and longitudinal studies of the predominant cultivable microflora re- Continuous loss of connective tissue ation to occur. However, individual case veal that only a small number of species attachment is an uncommon event even reports, as well as the studies on A. are associated with human periodontal in patients who have had previous actinomycetemcomitans distribution, indisease (Moore et al. 1983). The concept periodontitis and who still have a sig- dicate that the disease may be considered transmissable (Zambon et al. of bacterial specificity has been further nificant degree of gingival inflammation 1983, Preus & Olsen 1988). supported by clinical observations, by (Goodson et al. 1982, Lindhe et al. 1983, B. gingivalis is found in high frethe therapeutic effect of control of these Listgarten et al. 1985). Furthermore, organisms, and by experimental models loss of attachment is not always seen quency and in high numbers, often as of periodontitis in both gnotobiotic and even in patients with severe forms of a major component of the subgingival conventionally maintained animals. gingival inflammation. These obser- flora, in adult periodontitis lesions. In A variety of predominantly gram- vations suggest that gingivitis and perio- contrast, subgingival dental plaque negative organisms have been impli- dontitis may be discrete disease pro- from periodontally normal subjects shows a much lower frequency and cated in the etiology of periodontal dis- cesses with distinct etiologies. The identification of specific oral fewer number or none at all of B. ginease, including Actinobacillus actinomycetemcomitans, Bacteroides gingivalis, micro-organisms, associated with les- givalis. Furthermore, B. gingivalis is not Fsacteroides intermedius, Capnocytopha- ions in different forms of human peri- detectable in subgingival flora of pam sp., Eikenella corrodens, Fusobacteri- odontal disease has significant impli- tients with gingivitis who are not affect:/in nucleatum, and WoUnella recta, as cations. Several advances have been ed by periodontitis (Christersson et al. 1989). 'ell as certain gram-positive bacteria made, particularly regarding the imInterestingly, black-pigmented Bacportance of A. actinomycetemcomitans ach as Eubacterium species (Moore et in human periodontal disease, as well as teroides is not often found in the suprai, 1983). gingival plaque from adult periodontitis Periodontal disease occurs in an area the role of some Bacteroides species. patients, but it appears that B. gingivalis A. actinomycetemcomitans is one of . ormally inhabited by many bacteria.
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colonizes the saliva and most oral mucous surfaces of periodontitis patients. Preliminary studies of the vagina, the gut, and feces have not yielded B. gingivalis, so it appears that the primary ecologic niche of S. gingivalis is the oral mucous membranes and the subgingival region of subjects with adult forms of periodontitis (Van Winkelhoff et al. 1989).
In clinical practice as well as in research on periodontal therapy, dental plaque is often scored as a dichotomy, presence or absence of detectable plaque. A simple but reliable data acquisition, based on yes or no answers collected over an extended number of surfaces are intuitively more relevant and useful in analyses, as well as in conclusions regarding clinical significance.
Clinical Assessment of Dental Plaques .
Principles for Anti-infective Periodontal Therapy
Supragingival plaques are readily detectable with tile naked eye after reaching a certain thickness. This occurs in 1 or 2 days in areas where the plaques are not removed ititentionally or by the forces of mastication and other oral functions. They are yellow or whitish and often thickest along the gingival third of the tooth, and in the interproximal areas. When too sparse to be detected, the presence of dental plaque may be determined by use of disclosing solution. Plaque can also be detected by scraping the tooth surface with a probe or sealer. Siipragingival plaque is usually found at the gingival third of the crown, an area which is not naturally self-cleansing. The abrasiveness of food, oral hygiene, and the action of normal mastication are often sufficient to prevent significant plaque deposits from forming on the smooth occlusal surfaces and the areas occlusal of the buccal and lingual prominence of the crown. Also, plaque deposits are regularly present in fissures, pits and irregularities such as cracks or undulations of the surfaces. Subgingival plaques are usually thin, contained within the periodontal pocket or gingival cre\^ice, and hard to visualize in situ. Subgingival deposits can be detected after removal from the pocket by scraping the root surface with a probe or sealer. There are several sampling procedures for the microbial assessment of the periodontal flora which require sampling of subgingival plaques with absorbent sterile paper points or with other sampling devices. Such subgingival samples are then evaluated microbiologically, by culturing, or by rapid tests using specific a.ntibodies or nucleic acid probes, for their content of periodontal pathogens. Plaque indices are often used in clinical experiments to demonstrate rather small changes and to obtain manageable data suited for statistical analyses.
Anti-infective therapy, i.e., those procedures which control the disease-causing micro-organisms, for many systemic infections equals the use of antimicrobial drugs. For localized infections like periodontal diseases, treatment often consists of a combination of mechanical wound debridement and the application of antimicrobial agents. The most important part of the battery of anti-infective procedures employed in the treatment of gingivitis and periodontitis, is personal oral hygiene resulting in regular supragingival plaque removal. Several studies show that mechanical debridement procedures to remove the bulk of the infection are effective in the treatment of gingivitis and most mild to moderate forms of periodontitis in adults (Badersten et al. 1981, Ramfjord 1987). While anti-infective therapy is adequate for mild to moderate periodontitis patients, periodontal surgery may be necessary for patients with advanced periodontitis with deep pockets to provide access for complete root debridement (AntczakBoukoms & Weinstein 1977). Mechanical anti-infective therapy, combined with successful oral hygiene, has proven its general effectiveness in the management of periodontal disease, and has been used successfully in clinical practice for most cases of gingivitis, and mild to moderate periodontitis in adults (Badersten et al. 1981, Ramfjord 1987). The paramount role of supragingival plaque control is clearly shown. In an experimental model for the evaluation of different surgical periodontal therapies, Rosling et al. (1976) showed that the key element for a successful outcome of therapy was total plaque control, in these studies achieved by bi-weekly professional tooth cleanings for up 2 years. As a "bonus", information derived from these studies, which is not often recognized, includes the fact that periodontal
surgical therapy followed by poor infection control, i.e. inadequate personal plaque control, may lead to an exacerbation of the periodontal condition (Rosling et al. 1976). Later, Lindhe & Nyman (1984) described long-term results of periodontal therapy and again confirmed the pivotal role of plaque control level reached by the patients. Summary and Conclusions
The concept of periodontal diseases being associated with specific microorganisms not regularly found in the healthy gingival sulci and/or oral cavity, raises questions as to the nature of these species. Those organisms for which the oral cavity is a primary habitat and which do not normally cause disease, are the indigenous or resident fiora. On the other hand, those which are not part of the resident microfiora and which cause disease, are exogenous pathogens. Indigenous and many exogenous microorganisms are normally non-pathogenic bacteria but can, under circumstances such as reduced host resistance or overgrowth, cause disease in which case they may be considered opportunistic pathogens. The definition of periodontal pathogens as either opportunistic pathogens or as exogenous pathogens carries with it significant implications. If periodontal disease results from an opportunistic infection by indigenous microorganisms, then preventive efforts should be directed toward removing most plaque from all tooth surfaces. Such a protocol will likely suppress the emergence of opportunistic pathogens and prevent the development of gingivitis and some forms of periodontitis. This may, however, be over-treatment for the majority of individuals. If periodontal disease results from subgingival infection with exogenous pathogens, an appropriate preventive strategy may be interference with oral colonization or subgingival growth of the exogenous pathogen(s). This antiinfective approach could be targeted to specific micro-organisms rather than to the plaque mass as a whole. The methods for such an anti-infective approach to suppress exogenous pathogens include: (a) specific agents whicl: will eliminate the pathogens from the flora, (b) immunization to inhibit colon ization or (c) replacement therapy ii which a stable, periodontal health-as sociated subgingival flora is establishec
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bacillus actinomycetemcomitans-assodated Goodson, J. M. & Socransky, S. S. (1986) periodontal disease. Journal of PeriodontThe effect of treatment on Actinobaciifus ology 56, 41-50. actinomycetemcomitans in localized juvenile periodontitis. Journal of Periodontology Gibbons, R. J., Kapsimalis, B. & Socransky, 57, 94-99. S. S. (1964) The source of salivary bacteria. Archives of" Oral Biology 9, 101-103. Miller, W. D. (1973) Micro-organisms of the Acknowledgements Gibbons, R. J. & Nygaard, M. (1970) Interhuman mouth. Basel, Switzerland: S, bacterial aggregation of plaque bacteria. Karger. Supportd in part by USPHS Grant no. Archives of Oral Biology 15, 1397-1400. Moore, W. E. C, Holdeman, L. Y, Cato, B, DE04898. The authors also wish to Gibbons, R. J. & Van Houte, J. (1973) On P., Smibert, R. M., Burmeister, J. A. & thank Mrs. Susan Hanlon and Ms. the formation of dental plaque. Journal of Ranney, R. R. (1983) Bacteriology of modFrigg Sellevoll for preparing the manuPeriodontology 6, 347-360. erate (chronic) periodontitis in mature script. Goodson, J. M., Tanner, A. C. R., Haffajee, adult humans. Infection and Immunity 42, A. D., Sornberger, G. C. & Socransky, S. 510-515. S. (1982) Patterns of progression and reNewman, M. G. & Socransky, S. S. (1977) gression of advanced destructive periPredominant cultivable microbiota in References odontal disease. Journal of Clinical Perioperiodontosis. Journal of Periodontal Redontology 9, 472-481. search 12, 120-128. Albini, B., Zappa, U., Christersson, L. A., Preus, H. R. & Olsen, L (1988) Possible transKrasse, B. (1954) The proportional distriZambon, J. J. & Genco, R. J. (1988) Bacmittance of A. actinomycetemcomitans bution of Streptococcus salivarius and teria in periodontal tissues in adult periofrom a dog to a child with rapidly destruc^ other streptococci in various parts of the dontitis. Journal of Dental Research 67, tive periodontitis. 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Zambon, J. J. (1985) Actinobacillus actinomycetemcomitans in human periodontal disease. Journal of Clinical Periodontoiogy 12, 1-20. Zambon, J. J., Christersson, L. A. & Slots, J. (1983) Actinobacillus actinomycetemcomitans in human periodontal disease. Prevalence in patient groups and distribution of biotypes and serotypes within families. Journal of Periodontoiogy 54, 707-711. Address: L. A. Christersson Departments of Oral Biology and Periodontoiogy School of Dental Medicine SUNY at Buffalo 3435 Main Street Buffalo, NY 14214 USA
