NCBI Bookshelf. A service of the National Library of Medicine, National Institutes of Health.

Baron S, editor. Medical Microbiology. 4th edition. Galveston (TX): University of Texas Medical Branch at Galveston; 1996.

Cover of Medical Microbiology

Medical Microbiology. 4th edition.

Show details

Chapter 99Microbiology of Dental Decay and Periodontal Disease


General Concepts

Bacteriology of Dental Infections

The mouth is colonized by 200 to 300 bacterial species, but only a limited number of these species participate in dental decay (caries) or periodontal disease.

Dental Decay

Dental decay is due to the irreversible solubilization of tooth mineral by acid produced by certain bacteria that adhere to the tooth surface in bacterial communities known as dental plaque.


Streptococcus mutans is the main cause of dental decay. Various lactobacilli are associated with progression of the lesion.


The tooth surface normally loses some tooth mineral from the action of the acid formed by plaque bacteria after ingestion of foods containing fermentable carbohydrates. This mineral is normally replenished by the saliva between meals. However, when fermentable foods are eaten frequently, the low pH in the plaque is sustained and a net loss of mineral from the tooth occurs. This low pH selects for aciduric organisms, such as S mutans and lactobacilli, which (especially S mutans) store polysaccharide and continue to secrete acid long after the food has been swallowed.

Clinical Manifestations

Caries become intensely painful when the lesion approaches the tooth pulp.

Microbiologic Diagnosis

New, chair-side culture procedures allow for an estimate of the number of S mutans organisms in saliva.

Prevention and Treatment

The widespread use of fluoride in the water supply, in dentifrices, and in local applications by the dentist has reduced the prevalence of caries by 30 to 50 percent among young people in many industrialized countries. In clinical trials, the use of topical antimicrobial agents to eradicate diagnosed S mutans infections usually significantly reduces decay.

Periodontal Disease


Periodontal disease can establish itself when the gums detach from the teeth as a result of an inflammatory response to plaque.


Periodontal infections are usually mixed, most often involving anaerobes such as Treponema denticola and Porphyromonas gingivalis. The microaerophile Actinobacillus actinomycetemcomitans causes a rare form known as localized juvenile periodontitis.


Plaque bacteria elaborate various compounds (H2S, NH3, amines, toxins, enzymes, antigens, etc.) that elicit an inflammatory response that is protective but also is responsible for loss of periodontal tissue, pocket formation, and loosening and loss of teeth.

Clinical Manifestations

There is no apparent pain until very late when abscesses may occur. Bleeding gums and bad breath may occur.

Microbiologic Diagnosis

Microbiologic diagnosis is usually not sought. Spirochetes and other motile organisms are found upon dark-field microscopic examination. Immunologic reagents, DNA probes and enzyme assays have been developed for P gingivalis, T denticola, Bacteroides forsythus, A actinomycetemcomitans and other organisms.

Prevention and Treatment

Daily toothbrushing and regular professional cleanings by the dentist appear to be adequate to prevent periodontal disease. Rigorous debridement of tooth surfaces is the standard treatment. Often, some form of surgery is used to improve access to root surfaces. Recent studies suggest that short-term use of antimicrobial agents, especially metronidazole and doxycycline, is beneficial.


The tooth surfaces are unique in that they are the only body part not subject to metabolic turnover. Once formed, the teeth are, under the correct conditions, essentially indestructible, as witnessed by their importance in fossil records and forensic medicine. Yet in the living individual, the integrity of the teeth is assaulted by a microbial challenge so great that dental infections rank as the most universal affliction of humankind. The discomfort caused by these infections and their enormous cost (dental infections rank third in medical costs, behind heart disease and cancer, in the United States) gives dental diseases prominence despite their non-life-threatening nature.

This chapter reviews the bacterial aspects of dental caries and periodontal disease and suggests that, in the future, treatment will be directed toward eliminating or suppressing certain bacterial species that appear to be overt pathogens in the dental plaque.

Dental Caries (Decay)

Dental decay is due to the dissolution of tooth mineral (primarily hydroxyapatite, Ca10 (P04)6(0H)2) by acids derived from bacterial fermentation of sucrose and other dietary carbohydrates. These bacteria live in bacterial communities known as dental plaque which accumulates on the tooth surface. For almost a century it was believed that any bacterial community on the tooth surface could cause decay, and treatment was almost exclusively the mechanical cleaning of these surfaces by toothbrushing, using some type of mild abrasive. Such treatments based upon debridement and, in extreme cases, upon dietary carbohydrate restriction, were singularly unsuccessful in reducing dental decay. In fact, the prevalence of dental decay was so high among young men that it was the major cause of rejection from military service in World Wars I, II, and the Korean War. This staggering amount of dental morbidity led to the formation of dentistry as a separate health profession in the late 19th century; to the expectation that all people would, if they lived long enough, be edentulous (toothless); and to a dental health bill to the public of approximately 34 billion dollars per year in 1990.

Things have changed. Water fluoridation has proven to be a most cost-effective way of reducing decay; fluoride dentifrices were even more effective than initially projected; and research findings indicate that most carious lesions actually reflect a sucrose-dependent Streptococcus mutans infection. Individuals at risk for this infection can be diagnosed and treated by frequent mechanical intervention, by intensive application of prescription levels of fluorides or other antimicrobials (such as chlorhexidine), by restriction of ingestion of sucrose between meals, or by use of products that contain sucrose substitutes (such as xylitol). The net result is that dental decay in the late 20th century is a controllable infection and should be preventable in many individuals. Almost 50% of young children are caries-free, and the level of edentia among individuals over 65, has dropped from 50% to about 20%.


Dental decay has been known since recorded history, but was not an important health problem until sucrose became a major component of the human diet. When sucrose is consumed frequently, an organism known as Streptococcus mutans emerges as the predominant organism, and it is this organism that has been uniquely associated with dental decay.

In 1924 S mutans was isolated from human carious lesions, but subsequently was not thoroughly studied until the 1960s when it was re-identified as the etiologic agent of a transmissible caries infection in rodent models. In these studies, all of Koch's postulates for infectivity were fulfilled in animal models. However, it proved difficult to show that S mutans was a human dental pathogen, because S mutans appears to be a member of the normal flora on the teeth, and it was difficult to show that an increase in S mutans actually preceded and/or coincided with the earliest clinical lesion.

Dental decay is measured clinically as a cavitation on the tooth surface (Figure 99-1). However, cavitation is a late event in the pathogenesis of decay, being preceded by a clinically detectable subsurface lesion known as a white spot (Figure 99-1), and prior to that by subsurface demineralization that can only be detected microscopically. From a diagnostic and treatment perspective, the lesion should be detected at the white spot stage. This usually cannot be done without rigorous descriptive criteria (not all white spots are due to the decay process) and because the white spot stage in the caries-prone fissures and approximal surfaces of the tooth cannot be directly visualized during a dental examination.

Figure 99-1. Schematic drawing of a cross-section of tooth showing decay and white spot lesions.

Figure 99-1

Schematic drawing of a cross-section of tooth showing decay and white spot lesions.

The prevalence of dental morbidity is documented in terms of the number of teeth (T) or tooth surfaces (S) that have obvious decay (D), contain a dental restoration or filling (F), or are missing (M). These DMF teeth (DMFT) and DMF surface (DMFS) scores do not discriminate as to the relative proportions of the score due to decay, versus fillings and extractions. This insensitivity of the DMFT and DMFS scores in quantitating the actual decay, independent of morbidity led in early clinical studies to unimpressive associations between S mutans and DMFT or DMFS scores. However, when the comparison was limited to individuals with decayed teeth or when the plaque samples were taken from a decayed tooth site, a significant association between S mutans and decay was evident.

This association is clearly seen in individuals who developed xerostomia secondary to radiation treatment of head and neck cancer. S mutans and lactobacilli are normally present in low numbers in the plaque of these individuals. When the salivary flow decreases, the pH in the plaque drops, leading to a selection for aciduric (acid-tolerant) bacteria, such as S mutans and lactobacilli. New decayed lesions become obvious within 3 months after radiotherapy and the patient may average one or more new decayed surfaces per post-radiation month. During the development of decay, the proportions of, first, S mutans and then lactobacilli increased significantly. This sequence of events indicated that S mutans was involved with the initiation of decay, whereas the lactobacilli were associated with the progression of the lesion.

This bacterial succession is illustrated in Figure 99-2, which shows the sequence of events occurring on the surface of a caries-free tooth that either becomes carious or remains caries free. In either case, the tooth surface initially represents a carrier state relative to harboring a primary cariogen, such as S mutans, in the plaque on a smooth surface. The proportion of the cariogen in the flora is similar in both cases, but the location of S mutans differs within the plaques. In the tooth destined to develop decay, S mutans is located on the enamel surface, whereas in the tooth destined to remain caries free, S mutans is confined to the saliva-plaque interface. Debriding procedures, such as toothbrushing and flossing, might remove most plaque organisms, but could leave untouched those bacteria either firmly attached to the enamel surface or sequestered in defects in the enamel surface. In surfaces destined to become carious, the residual organisms would include S mutans, whereas in surfaces destined to remain caries free, S mutans would be absent. Over time these caries-free surfaces might alternately acquire and lose S mutans, thereby having an intermittent carrier-state status. However, in those surfaces in which caries will eventually develop, S mutans becomes a dominant member of the flora, undoubtedly secondary to frequent sucrose ingestion.

Figure 99-2. Relationship between location of cariogenic bacteria and development of dental caries.

Figure 99-2

Relationship between location of cariogenic bacteria and development of dental caries.

The incipient or white spot lesion occurs when the acidogenic activity of the cariogen causes tooth mineral to be mobilized from the subsurface enamel to buffer the pH at the plaque-enamel interface. Bacteriologic sampling at this stage should reveal both a proportional and an absolute increase in the levels of S mutans. When the lesion progresses to the stage of cavitation, the organisms penetrate into the enamel crystals (Fig. 99-2). Also, secondary cariogens, such as the lactobacilli, appear as a result of the selection for aciduric organisms in the plaque. When the lesion reaches the advanced clinical stage, conditions may be such that S mutans can no longer survive, and only secondary cariogens like the lactobacilli and opportunistic organisms can be found.

This model predicts that a bacterial succession occurs during the progression of a carious lesion and that the flora of the advanced lesion may bear little resemblance to the flora of the incipient lesion. Thus it was necessary to sample the plaque during the initial lesion or white spot stage to find the etiologic agents of decay. When this was done, S mutans dominated in the flora. However, for the lesion to progress to the stage of cavitation, lactobacilli seem necessary. Thus while S mutans could be isolated from both progressive and nonprogressive lesions, L casei could only be isolated from progressive lesions.


These clinical studies indicated that of the 200 to 300 species which can be isolated from plaque, only S mutans, and to a lesser extent the lactobacilli, can be consistently associated with dental decay. What makes these organisms cariogenic relative to all other bacterial types found in the plaque?

In the 19th century, microbial acid production from dietary substrates was linked to the etiology of dental decay in what was called the chemoparasitic theory of decay. But researchers were not able to associate any single acidogenic species with decay, and concluded that decay was bacteriologically nonspecific and due to the increased amounts of acid formed when bacteria accumulated in plaque on the tooth surfaces. It was noted that decay occurred at retentive sites on the teeth and recommended mechanical debridement of these sites as the best method of reducing decay. While the clinical observations were correct, there was no way of determining that the retentive sites were caries prone because they provide the micro-environment which selects for S mutans and lactobacilli. In this section we shall examine those attributes of S mutans and the lactobacilli that enable them to be successful on retentive sites and show that these attributes constitute, in effect, the virulence factors which make these organisms specific odontopathogens.

Sucrose in the diet

Considerable evidence from epidemiologic observations and animal experiments indicates that, shortly after sucrose is introduced into the diet, a notably higher incidence of decay occurs. The relationship between sucrose ingestion and dental caries is reasonably well understood. The supragingival plaque flora derives its nutrients from various sources that include diet, saliva, sloughed epithelial cells, dead microbes, and gingival crevice fluid or exudate. All sources, except the foods in the diet provide only small amounts of nutrients. Dietary components are normally high-molecular-weight polymers (such as starch and proteins) that are in the mouth for short periods. They have a minimal effect on plaque growth except in those instances when food is retained between and on the teeth. Sucrose, however, changes this pattern because it is a low-molecular-weight disaccharide that can be rapidly sequestered and utilized by the plaque flora. Plaque organisms capable of fermenting sucrose have a decided advantage over the non-sucrose fermenters in that they can proliferate during periods of sucrose ingestion and thereby become the dominant plaque organisms.

Sucrose fermentation produces a rapid drop in the pH, to 5.0 or lower, at the point of interface between plaque and enamel. When sucrose is ingested during meals, sufficient saliva is secreted to buffer the plaque pH and decay does not occur. In fact, studies show that as much as one-half of a pound of sucrose consumed daily at meals for two years was not associated with an increase in dental decay; however, when the same or lesser amounts of sucrose were ingested between meals, subjects developed new decay at the rate of about three to four tooth surfaces per year. The frequent ingestion of sucrose has been shown to increase the lengths of time that sucrose could be detected in the saliva. This means that if this sucrose were available for microbial fermentation in the plaque, low plaque pHs would be present for long periods each day. When the plaque pH value falls below 5.0-5.2, the salivary buffers are overwhelmed and as lactic acid diffuses into the tooth, enamel begins to dissolve, releasing Ca and PO4 ions from sites beneath the surface enamel (Figure 99-3). Normally, the bathing saliva replenishes these minerals, but if the length of the flux from the enamel is great, repair does not occur and cavitation results. Thus, sucrose consumption per se does not cause decay, but the frequent ingestion of sucrose by prolonging the time period by which the plaque is acidic, is cariogenic.

Figure 99-3. Pathogenesis of dental decay.

Figure 99-3

Pathogenesis of dental decay.

Plaque bacteria that ferment sucrose produce acids, which in vitro lower the pH value to below 5.0. However, only S mutans of all these species reliably caused decay in germ-free animals fed a high-sucrose diet. This suggested that microbial acid production was not the exclusive determinant of decay and that S mutans had to possess other attributes which were responsible for its virulence. S mutans was subsequently shown to metabolize sucrose in a remarkably diverse fashion that is not matched by any other known plaque organism. The major pathway is concerned with energy metabolism; in this process, the enzyme invertase splits sucrose into its component glucose and fructose molecules, which are then converted to lactic acid by the glycolytic pathway. Other enzymes, called glucosyltransferases, split sucrose but transfer the glucose moiety to a glucose polymer known as a glucan. S mutans forms several complex glucans that differ in their core linkage, amount of branching, and molecular weight. The first glucan identified had a core linkage consisting of an a1–6 bond that classified it as a dextran. Later, a unique glucan having an a1–3 core linkage was identified and given the name mutan. S mutans also has enzymes that split sucrose and transfer the fructose moiety to a fructose polymer known as a fructan. Other plaque bacteria can use sucrose to synthesize one or more of these polymers, with the exception of mutan. Only S mutans can form all of them, a fact that led to an inquiry into the relationship between polymer production and caries formation.

A series of in vitro experiments showed that the glucans enable S mutans to adhere to surfaces. This suggested that in vivo these adhesive polymers would enable S mutans to adhere tenaciously to the tooth surface and to accumulate on these surfaces, thereby causing decay in the underlying surface.

Animal experiments in which rodents were infected with mutants of S mutans that lacked the ability to form either dextran or mutan, indicated that the absence of mutan was associated with a greater reduction in smooth surface decay than was the absence of dextran. In each instance, the amount of pit and fissure decay was not significantly affected by these mutations. Decay on smooth surfaces seems to depend on the retentive polymers formed by S mutans, whereas in sites where retention is provided by the anatomy of the teeth (pits, fissures, and contact points between teeth), these polymers are not as important. Accordingly, pit and fissure decay may be caused simply by any acidogenic organism that can survive in these retentive sites.

This nonspecific explanation does not seem completely satisfactory, because in animal models and in human caries, S mutans, again, is the dominant organism involved or associated with pit and fissure decay. A few other organisms, such as Lactobacillus casei and Streptococcus faecalis, can cause fissure decay in germ-free rats. These three organisms are all relatively aciduric compared to other plaque bacteria; that is, they not only produce acids, but they are relatively resistant to the resulting low pH caused by acid accumulation. Lactobacilli are the most aciduric of the plaque bacteria, but these organisms only predominate by the time the carious lesion has extended into the dentin. At the time the earliest carious lesion is detected, only S mutans has reached significant levels and proportions (Figure 99-2). When S mutans, lactobacilli, and other plaque species were compared in vitro for their ability to ferment sucrose at different pH values, S mutans was found to be more active than the other bacteria at pH 5.0, and thus, it is probably most active in vivo at the very pH at which the teeth begin to demineralize.

This aciduricity best explains the involvement of both S mutans and lactobacilli in human decay. A retentive site is colonized by those organisms present in saliva. S mutans, although scarce in the initial inoculum (fewer than 0.1% of the initial colonizers), is selected for if the average pH value in the site is not well buffered by saliva. Frequent ingestion of sucrose-containing products predisposes toward lower pH values and thus selects for S mutans. When the pH remains in the vicinity of 5.0–5.5, tooth mineral is solubilized, thereby buffering the plaque and maintaining an environment suitable for growth of S mutans. Eventually, enough mineral is lost so that a cavitation occurs in the enamel, and if this enlarges so that it extends into the dentin, a semiclosed system is formed in which the pH value drops below 5.0. Under these acidic conditions, growth of lactobacilli is favored, and these organisms succeed as the predominant flora in the carious lesion.

Clinical Manifestation

Dental decay occurs at discrete sites on the surface of the enamel. Progress through the enamel is usually slow because of the remineralizing action of the saliva, and is asymptomatic. When decay spreads into the dentin, the process accelerates, most likely because the very low pH that can arise in this semiclosed environment denatures the collagen scaffold that holds the hydroxyapatite salts in place and rapidly solubilizes them. When the dentinal decay approaches the innervated tooth pulp, the pain can be intermittent or continuous, and dull or excruciating. Pain is the chief complaint of the patient.

Microbiologic Diagnosis

A microbiologic diagnosis for a S mutans/lactobacilli infection is rarely sought, primarily because the acute pain that brings the patient to the dentist is almost always relieved by a dental restoration or extraction. Thus, the knowledge of an underlying S mutans infection would not change the treatment. However, microbiologic diagnosis would be advantageous in the management of the patient to prevent or minimize future decay. Such situations would occur whenever an expensive treatment is planned, such as orthodontic treatment, or the placement of dental crowns and bridges to replace missing teeth. Microbiologic examination would also be useful at the end of any restorative treatment to determine the residual level of S mutans and lactobacilli colonization on the teeth.

Scandinavian investigators have empirically determined that 106 CFU S mutans per milliliter of stimulated saliva can be associated with future caries activity. Accordingly, they have recommended active intervention with fluoride, dietary counseling, and antimicrobial agents in individuals so infected. They have designed simple chairside tests that can, in a semiquantitated manner provide information on the salivary levels of S mutans. All of these tests rely on the fact that S mutans is resistant to 5 ug/ml of bacitracin and that it will grow in the presence of 20% sucrose. In liquid media containing these additives, S mutans will form adherent colonies on the side of glass, plastic strips, or any other solid surfaces that are present.

In a practical application of these tests, the clinician would not place orthodontic bands on an individual with 106 CFU of S mutans, because this individual would be apt to develop decay around the margins of the bands. Likewise an individual who is having extensive bridgework (the placing of dental restorations across an edentulous space) would be at risk of developing new decay around the margins of these restorations. In both instances, the patient needs to be treated for S mutans infection prior to the placement of the dental devices or restorations.

Prevention and Treatment

Conventional dental therapy has not yet incorporated any microbiologically-based strategy into its armamentarium. Instead, a treatment based on response to symptoms has prevailed. The bankruptcy of this approach, which depends on a turn-of-the-century biologic base, has been demonstrated in the Scandinavian countries, where a socialized dental delivery system has made quality dentistry available to everyone. Because of the emphasis on treatment rather than prevention, the results have only prolonged the life span of the tooth by about 10 years, a rather poor therapeutic result. In England, where the health care system also emphasized treatment rather than prevention, one-half of the people over 35 years of age were edentulous in the 1970s. The Scandinavians, especially in Sweden, have changed their approach and have instituted plaque prophylactic programs for children and adults. Thorough dental cleaning with a 5% fluoride paste given at 2–4 week intervals combined with oral hygiene education, has lowered dental decay in children by about 80%–90%, compared to youngsters receiving symptomatic treatment. (Symptomatic treatment involves placing dental restorations in an obviously carious tooth, and pulling teeth.) Similar success has been achieved in adults with and without periodontal disease.

Thorough cleaning with fluoride apparently selects for the more desirable bacterial types, such as S sanguis and S mitis, which are capable of rapidly colonizing the tooth surfaces. S mutans presumably does not have an opportunity to become dominant, because the frequent debridement neutralizes its ability to be selected for by the low pH values that characterize an undisturbed plaque. Also, the 5% fluoride paste has an immediate bacteriostatic effect on the plaque organisms.

Fluoride as an Antimicrobial Agent in Plaque

The mechanisms by which fluoride prevents decay are multiple, and the relative contributions of each mechanism are not fully understood. The 30%–50% reduction in decay that follows water fluoridation is generally attributed to the fluoride replacing hydroxyl groups in the tooth crystal, thereby forming fluorapatite (Fig. 99-4). Fluorapatite is less soluble in acid than hydroxyapatite, which means that a tooth containing fluorapatite dissolves slowly in the low pH value found in plaque, and accordingly, remineralizes faster in the intervals between sugar ingestion. These explanations do not completely account for the proved efficacy of topically-applied fluorides and raises questions about other modes of fluoride action.

Figure 99-4. Anti-caries mechanisms of fluoride.

Figure 99-4

Anti-caries mechanisms of fluoride.

The fluoride ion (F) inhibits the bacterial enzyme enolase, thereby interfering with production of phosphoenolpyruvate (PEP). PEP is a key intermediate of the glycolytic pathway and, in many bacteria, is the source of energy and phosphate needed for sugar uptake. The presence of 10–100 ppm of F, inhibits acid production by most plaque bacteria (Fig. 99-4). These levels are delivered easily by most prescription fluoride preparations, such as were used in the Swedish studies. Of equal interest is the finding that at acidic pH values (5.5 or below), low levels of F (1–5 ppm) inhibit the oral streptococci. These levels are found in plaque, especially in individuals who drink fluoridated water or who use fluoridated dentifrices. If this plaque fluoride is derived from the tooth, an antibacterial mode of action, which involves a depot effect, can be postulated for systemic (water) and topical fluoride administration.

The depot effect comes about in this manner. Water fluoridation promotes the formation of fluorapatite, whereas topical fluorides cause a net retention by the enamel of fluoride as fluorapatite or as more labile calcium salts. Microbial acid production in the plaque may solubilize this enamel-bound fluoride, which at the prevailing low pH in the plaque microenvironment could become lethal for the acid-producing microbes. Such a sequence would discriminate against S mutans and lactobacilli because they, as a result of their aciduric nature, are most likely the numerically dominant acid producers at the plaque-enamel interface. The fluoridated tooth thus contains a depot of a potent antimicrobial agent that is not only released at an acid pH value but is most active at this pH value. This hypothesis, then, attributes some of the success of water fluoridation and topical fluorides to an antimicrobial effect. It further suggests that judicious use of topical fluorides would be effective in patients with highly active caries.

The most effective dose schedule and fluoride preparation have not been determined. Neutral 1.0% sodium fluoride given daily to adults, who normally would experience rampant caries secondary to a xerostomia following irradiation for jaw cancer, has resulted in few or no caries. Controls, who were given a placebo as well as the best available hygiene instruction, averaged over two new decayed surfaces per post-radiation month (Table 99-1). When the control patients were placed on the daily fluoride regimen, their decay rate dropped almost to zero. In another study, 5- to 6-year-old children, who had 10 or more carious tooth surfaces, were given the necessary dental restorations and either 1.2% F as a neutral sodium fluoride gel or a placebo gel. The gels were taken unsupervised at home, twice a day for 1 week. After 2 years, the fluoride group had about 40% less decay than the placebo group. Eleven of 20 of these formerly rampant caries children had no new decay in their permanent teeth. In these xerostomia and pediatric patients, the initially high proportions of S mutans were decreased by the fluoride treatments which resulted in reduced decay.

Table 99-1. Effect of Topical Fluoride (1% NaF) Gel, Oral Hygiene and/or Dietary Sucrose Restriction on the Incidence of Dental Caries in Patients With Radiation Xerostomia.

Table 99-1

Effect of Topical Fluoride (1% NaF) Gel, Oral Hygiene and/or Dietary Sucrose Restriction on the Incidence of Dental Caries in Patients With Radiation Xerostomia.

Sucrose Substitutes that Aid in Caries Control

Eating foods that contain sucrose between meals can be highly cariogenic. Dietary counseling, that instructs patients to avoid between meal snacks may help to decrease the incidence of dental decay, but only if the patients are compliant. Another dietary approach to caries control is to recommend that patients eat snack foods that contain compounds that provide the hedonistic appeal of sucrose, but are not fermented by the plaque flora to the low pH levels associated with enamel demineralization.

The least acidogenic sucrose substitutes are the polyols, such as sorbitol, mannitol, and xylitol. Few plaque bacteria can ferment these substances, and those that can (S mutans and L. casei ferment sorbitol and mannitol) exhibit a slow fermentation, because glucose catabolite repression keeps the necessary degradative enzymes at minimum levels. Xylitol, the only polyol with a sweet taste comparable to that of sucrose, and the only one that cannot be fermented by S mutans, has been shown to be anticariogenic when substituted for sucrose in either foods or chewing gum. In a chewing gum study, young adults who consumed about 6 to 7 g of xylitol gum per day had, after one year, an 80% reduction in caries increment compared to a control group who consumed 6 to 7 g of sucrose gum per day. In later studies, this type of intensive use of a xylitol chewing gum was shown to decrease salivary and plaque levels of S mutans. When the between-meal sucrose supply is reduced, the levels of S mutans will decline, as the low plaque pH values that selected for them are not as dominant a factor in the plaque microecology. Thus, xylitol can satisfy the craving for sweets, discriminate against S mutans, and significantly reduce the incidence of dental decay.

Periodontal Disease

Periodontal disease is the general description applied to the inflammatory response of the gingiva and surrounding connective tissue to the bacterial or plaque accumulations on the teeth. These inflammatory responses are divided into two general groupings: gingivitis or periodontitis. Gingivitis is extremely common, and is manifested clinically as bleeding of the gingival or gum tissues without evidence of bone loss or deep periodontal pockets. Pocketing is the term given to the pathologic loss of tissue between the tooth and the gingiva, creating spaces that are filled by dental plaque (Figure 99-1). Periodontitis occurs when the plaque-induced inflammatory response in the tissue results in actual loss of collagen attachment of the tooth to the bone, to loss of bone, and to deep periodontal pockets which, in some cases, can extend the entire length of the tooth root (15 to 20 mm).

Periodontitis is usually graded according to the severity of the tissue loss and the number of teeth involved. Periodontitis is not as prevalent as once thought: a recent survey of American adults revealed that only 8% of the population surveyed had one tooth site with attachment loss measuring 6 mm or more. This finding was surprising, given past surveys, which indicated that almost everyone would experience advanced forms of periodontal disease as they aged, but is in agreement with recent population surveys in other countries which show that from 5 to 15% of the population has periodontitis.

Etiology and Pathogenesis

The most important new finding concerning periodontal disease is the realization that these clinical entities are really specific infections. These infections are unusual in that massive or even obvious bacterial invasion of the tissues is rarely encountered. Rather, bacteria in the plaque touching the tissue elaborate various compounds, such as H2S, NH3, amines, endotoxins, enzymes (such as collagenases) and antigens, all of which penetrate the gingiva and elicit an inflammatory response. This inflammatory response, although overwhelmingly protective, appears to be responsible for a net loss of periodontal supporting tissue, and leads to periodontal pocket formation, loosening of the teeth, and eventual tooth loss. As will be described subsequently, neutrophils are extremely important in this inflammatory response and, if they are absent, as in various neutropenias, or compromised as a result of chemotherapy, an aggressive form of periodontitis is encountered. T4 helper cells play a role in this defense, as witnessed by the periodontitis encountered in patients with acquired immune deficiency syndrome.


The simplest form of gingivitis is associated with the accumulation of supragingival plaque along the gingival margins of the teeth. This form of gingivitis has been extensively studied in human volunteers, and the sequence of events is well described. In these studies, individuals are brought to a state of health and then refrain from all forms of oral hygiene for a 3- to 4-week period. The initial colonizers of the teeth are streptococci, which proliferate and in turn become colonized by other bacteria present in saliva, such as various Actinomyces species and Veillonella. The greatest growth of the plaque occurs at the gingival margin, where plaque accumulations usually are visible after several days. This plaque may, in some instances, provoke a bleeding gingivitis in which spirochetes and Actinomyces viscosus are prominent members of the plaque flora. If this plaque remains undisturbed, the flora gradually shifts toward an anaerobic, Gram-negative flora that includes black pigmented bacteroides and several types of spirochetes. The increase in these anaerobic organisms can be explained by the low oxidation-reduction potential of the aged plaque and by nutrients derived from the inflammatory exudate at the site.

The gingivitis may resolve itself or fester subclinically for an indeterminate period; however, the potential for the formation of a periodontal pocket (periodontitis) exists at any time. When pockets are detected clinically, they usually are associated with calcified plaque deposits, called calculus, present on the tooth surfaces. For many years, calculus was thought to be the etiologic agent of periodontitis, because inflammation usually subsided when it was removed and the tooth surfaces were mechanically cleaned. However, calculus is always covered by plaque, and removal of calculus would be synonymous with debridement of plaque. The subgingival plaque flora associated with periodontitis is dominated by an anaerobic, Gram-negative flora in all cases but one, and that is a unique clinical entity formerly known as periodontosis, and now as localized juvenile periodontitis (LJP). LJP is an important clinical entity because of the understanding it has provided of the complex and dynamic interactions between the host and the flora in the pocket ecosystem.

Localized Juvenile Periodontitis (LJP)

LJP is different from all other periodontal infections, as it is not associated with plaque accumulations or calculus (in fact the absence of such led early investigators to consider it as a degenerative condition), is localized to certain anterior or front teeth and first molars, and is seen following puberty. It is a rather rare entity, occurring in about 0.1 to 0.5% of teenagers, but when found, is often clustered within families. This familial background suggested a genetic predisposition, which subsequently has been identified as a neutrophil defect associated with reduced chemotaxis. Bacterial examinations of subgingival plaque from affected teeth and adjacent healthy teeth, revealed that the diseased teeth were colonized by an essentially Gram-negative flora dominated by organisms subsequently identified as various Capnocytophaga and Wolinella species and Actinobacillus actinomycetemcomitans. It is A actinomycetemcomitans that appears to be the etiologic agent of LJP, and the arguments for its involvement are illustrative of the arguments made to implicate other species in other forms of periodontitis.

Once LJP has been recognized clinically, most of the tissue damage has already occurred, thereby permitting only a retrospective diagnosis of an A actinomycetemcomitans infection. A actinomycetemcomitans is found at a higher prevalence in tooth sites associated with LJP and at a lower prevalence in healthy sites in the same mouth, or at sites in periodontally healthy individuals. It is often found among other family members in a household with an LJP individual, and indeed among siblings at risk to LJP, there is suggestive data that colonization by A actinomycetemcomitans precedes the development of a pocket and subsequent bone loss. But what has been the most important reason for implicating A actinomycetemcomitans as a periodontopathogen, is its killing effect on neutrophils.

A actinomycetemcomitans produces a leukotoxin that kills neutrophils in vitro. It is clear that this leukotoxin is expressed in vivo, because patients with LJP have developed circulating antibodies which can neutralize this toxin in vitro. From this finding, a scenario can be developed that explains the localized nature of LJP. Children with a neutrophil chemotactic defect become colonized by A actinomycetemcomitans in early life, presumably by contact with infected household members. The colonization spreads to those permanent teeth that erupted at ages 5 to 7, but remains quiescent as an infection during the time that the primary or baby teeth are lost, and new permanent teeth appear at about ages 11 to 13. The individual entering puberty, has a dentition composed of first molars and incisors that are colonized by A actinomycetemcomitans and newly erupted teeth that either are not colonized or only minimally colonized.

Something then triggers the relative overgrowth of A actinomycetemcomitans in the subgingival plaque, and some of these organisms invade the gingival tissue and cause attachment and bone loss in the absence of an obvious inflammatory response. The latter can be explained by both a sluggish neutrophil response to the bacteria and by the leukotoxin inhibiting the neutrophils, and thereby preventing a protective host response in the pocket microenvironment. The leukotoxin is antigenic and elicits an antibody response which may neutralize the leukotoxin at other tooth sites, thereby limiting the infection to the originally colonized molars and incisors.

This scenario, while incomplete, does explain the localized nature of LJP, partially explains the absence of an inflammatory response in the tissue, and demonstrates the dynamic role of neutrophils and circulating antibodies in defending the periodontium. Presumably, this theme is operating in the more commonly found cases of adult periodontitis. Certainly, the central role of the neutrophils in host defense is unquestioned, as individuals with neutropenias, chronic granulomatous disease and various leukemias often present with advanced forms of periodontal disease.

Early-Onset Periodontitis (EOP) and Adult Periodontitis (AP)

The more common forms of periodontitis comprise at least two clinical entities, an early onset form in mainly young individuals and a chronic form seen in older adults. The early-onset periodontitis (EOP) is more aggressive looking, while the adult periodontitis (AP) may reflect a stable, but tenuous, stand-off between the host's defensive systems and the plaque bacteria. It is not clear whether these entities represent multiple types of infections with two clinical manifestations, or a single mixed anaerobic infection with different levels of host containment.

The inability to distinguish microbiologically between these two general patterns reflects methodologic procedures relating to the sampling of the subgingival plaque and the inability of any one culture medium and/or technique to give the total picture of the 200 to 300 bacterial species found in the plaque flora. For example, the spirochetes cannot be quantitatively cultured and may account for more than 40% of the flora in EOP and AP. They can be enumerated by microscopic examination of the plaque but would be ignored in cultural studies. These cultural studies, in turn, reveal a bewildering array of species, many of them either newly-described or as yet unspeciated. None of these cultivable species predominates in all disease-associated plaques. For example, Bacteroides forsythus, a nonpigmenting fusiform organism has been associated with the active periodontal lesion. B forsythus is present in 13% of the active sites and at 8% of the inactive sites, a difference which is hardly indicative of etiologic association. Yet the authors concluded that B forsythus is a probable periodontal pathogen because its levels, when present, were on the average 4 times higher in the active sites than in the inactive sites, i.e., 2.5% vs 0.6%. This difference is well within the error of the methods used to isolate the organisms.

Despite these problems in assigning virulence to any one species, it is clear that the bacterial communities at disease sites are different from the communities at healthy and successfully-treated periodontal sites (Table 99-2). The diseased sites are dominated by anaerobes, and in particular, by spirochetes and black-pigmented bacteroides species, such as Porphyromonas gingivalis and Prevotella intermedia. Among the latter, P gingivalis most often is associated with EOP, whereas P intermedia is found in both EOP and AP. No species, except the ubiquitous spirochetes, are consistently found in all lesions. Among the spirochetes, Treponema denticola is the only species that can be reliably cultured. It has been shown to possess a wide array of enzymes, such as a collagenase, peptidases, hyaluronidase, and a keratinolytic enzyme, and to produce noxious end products, such as butyrate, NH3, H2S, and endotoxin, that could cause, if they entered the periodontal tissue, an inflammatory response. However, comparable enzymes occur in P gingivalis and other anaerobic species found in the plaque, so that it would be difficult to assign etiologic significance to any one of these organisms based on the production of these enzymes. This being the case, it may be best to consider that the collective overgrowth of all these anaerobic species in the plaque causes a mixed infection that is responsible for tissue loss in EOP and AP.

Table 99-2. Bacterial Profiles of Subgingival Plaques Isolated from Various Clinical Forms of Periodontitis and from Periodontally Healthy Sites.

Table 99-2

Bacterial Profiles of Subgingival Plaques Isolated from Various Clinical Forms of Periodontitis and from Periodontally Healthy Sites.

Clinical Manifestations

Periodontal disease is usually painless until late in the disease process, when the teeth are so loose that some discomfort may appear upon chewing. Retention of food in a pocket site may provoke a sudden burst of microbial growth which could result in a painful abscess. At other times, the anterior teeth may become so loose that they separate and the patient visits a dentist because of the resulting poor aesthetics. However, under ordinary circumstances, it is bleeding upon brushing and/or concern over halitosis that brings the patient to the dentist. A thorough dental examination should find any pockets which may exist. If these pockets bleed upon probing, such bleeding is synonymous with tissue inflammation and warrants therapeutic intervention.

Microbiological Diagnosis

Microbiologic diagnosis is not commonly used in the management of periodontal disease. Several methodologies are, or soon will be, available that permit identification and quantification of the periodontopathogens listed in Table 99-2. The oldest method is the use of darkfield and phase contrast microscopy to identify spirochetes and other motile organisms in plaque samples. However, as spirochetes are detectable in most plaques, it is necessary to establish some critical value above which a spirochetal infection can be diagnosed. Our experience suggests that ≥ 20% spirochetes in any plaque sample permits the diagnosis of an anaerobic infection.

A microscopic examination cannot distinguish the species of bacteria present unless one uses an immunologic staining reagent specific for the organism in question. Such immunodiagnostic reagents have been used to detect and quantitate the levels of P gingivalis, P intermedia, T denticola, and A actinomycetemcomitans in the plaque. Cultural methods can, if the appropriate nonselective and selective media are used, provide information on the levels of A actinomycetemcomitans, black pigmented species, Campylobacter species, and other periodontopathogens. Also, because viable organisms are available, antibiotic sensitivities of the isolated organisms can be determined, which may be useful in certain instances.

Other diagnostic reagents are being developed to detect, in plaque, specific microbes or metabolites or enzymes unique to inflammation or infection. For example, specific microbes can be demonstrated in plaque by the use of DNA probes. Probes for A actinomycetemcomitans, P intermedia and P gingivalis are commercially available for testing via a reference laboratory. Future diagnostic procedures may rely on the detection of hydroxyproline, a collagen degradation product; prostaglandin, an inflammatory mediator; and enzymes, derived from either the host or the microbes. A trypsin-like enzyme is present in T denticola, P gingivalis, and B forsythus and is absent from at least 60 other subgingival plaque organisms. This enzyme can be detected by the hydrolysis of the trypsin substrate benzoyl-DL-arginine naphthylamide (BANA). The ability of subgingival plaque to hydrolyze BANA was associated with elevated levels and proportions of spirochetes and with probing depths greater than 6 mm. Subsequently, BANA hydrolysis was shown to be related to the T denticola and P gingivalis content of the plaque and to the clinical diagnosis of health or disease. As T denticola, P gingivalis and B forsythus are anaerobes, a positive BANA test may be useful in the diagnosis of an anaerobic plaque infection.

When these identification procedures were performed on the same plaque samples, the DNA probes and immunological reagents were significantly more likely to detect P gingivalis, B forsythus, A actinomycetemcomitans and T denticola than was the traditional cultural approach. In fact, this study suggested that culturing may be the least accurate detection procedure for these plaque species. When the probes and immunological reagents were compared to the BANA test, the probes and antibodies were slightly more accurate, i.e., 88% vs. 83%. All three approaches were essentially comparable indicating that reliable non-cultural methods are available to aid in the microbiological diagnosis of periodontal infections. Because the BANA test detects an enzyme(s) found in three anaerobic species, it may be used to detect an anaerobic periodontal infection.

Prevention and Treatment

Gingivitis can be prevented by good oral hygiene and professional surveillance. Gingivitis can be effectively treated by debridement of the teeth, and, if needed, by short-term use of products containing chlorhexidine, stannous fluoride, or other antimicrobial agents. Mouth rinses, gels, and toothpastes, when used in conjunction with toothbrushing and flossing, are probably adequate to deliver any antimicrobial agents to subgingival sites that are 1 to 3 mm in depth. At probing depths greater than 3 mm, there may not be sufficient penetration of the agent to the bottom of the pocket, and infection may persist. Subgingival scaling (debridement) by a professional is indicated, and additional benefits can usually be obtained by the use of irrigating devices containing an antimicrobial agent.

There is rarely any need to use systemic antimicrobial agents to treat gingivitis associated with pocket depths of 1 to 4 mm, with the exception of an increasingly rare and painful condition known today as acute necrotizing ulcerative gingivitis (ANUG) and formerly as trench mouth. Cases of ANUG that are refractory to mechanical debridement and topical antimicrobial agents respond, quickly and dramatically, to systemic metronidazole. The recognition of metronidazole's efficacy in ANUG led to the discovery that metronidazole has bactericidal activity against anaerobes. ANUG is characterized by tissue invasion by spirochetes and possibly other anaerobes and by elevated plaque levels of spirochetes and P intermedia (Table 99-2). ANUG thus resembles periodontitis in being an anaerobic infection.

Clinical dentistry has been about 80 to 85% successful in treating periodontitis by debridement and surgical procedures. However, surgery is labor intensive, and therefore costly. This limits the number of individuals who can be treated in a cost-efficient manner. However, if the majority of clinical cases of periodontitis represent specific bacterial infections, then an alternate treatment strategy would be to diagnose and treat the infection. It would seem that the crucial determination for the clinician in his treatment plan will be the diagnosis of either a micro-aerophilic infection, due to A actinomycetemcomitans, or an anaerobic infection characterized by the overgrowth of spirochetes and other anaerobic species.

A actinomycetemcomitans is sensitive to tetracycline, and early uncontrolled studies showed that tetracycline, scaling and root planing, periodontal flap surgery, and topical treatment with chlorhexidine were able, to save hopeless teeth in LJP patients. Additional studies, but none of a double-blind nature, confirm the usefulness of tetracycline in the treatment of LJP. Subsequently it was shown that tetracycline is concentrated in the fluid that seeps out of the periodontium into the pocket micro-environment. This fact, combined with the demonstration that A actinomycetemcomitans can be found in some plaques associated with EOP and AP (Table 99-2), has led to the use of tetracycline in those clinical entities. Results have been equivocal, but this has not detracted from the popularity of tetracycline as a treatment for periodontitis.

Most bacteriologic studies implicate anaerobes as the etiologic agent(s) of EOP and AP, and this would point to the use of a drug such as metronidazole. However, early animal studies that employed lifetime feeding of extremely high dosages of metronidazole suggested that the drug might be tumorigenic. These studies have not been confirmed and, indeed, in 1981 the FDA approved metronidazole for treatment of anaerobic infections. In dentistry, this concern has caused a reluctance to use metronidazole, but has also allowed time for well controlled clinical trials of metronidazole.

Six double-blind studies have demonstrated that metronidazole, given for periods of time as short as 1 week, can significantly improve periodontal health. In all cases, the metronidazole was given in conjunction with professional debriding of the teeth. Maximal benefits were obtained when the metronidazole was given after the debridement. The best clinical response was often noted in patients with more advanced disease, in which the pocket depths were ≥ 6 mm, whereas there was only a moderate benefit when the pocket depths were from 4 to 6 mm. In these advanced cases some teeth, that were initially scheduled for extraction upon reexamination, were found no longer to need extraction and thus, in a sense, were saved.

Metronidazole has subsequently been evaluated to determine whether it can reduce the need for periodontal surgery. In three double-blind studies, the unsupervised usage of metronidazole for one week, when combined with the standard debridement procedures, was able to significantly reduce the number of teeth needing surgery when compared to the debridement procedures plus placebo treatment. This sparing effect on surgery has lasted for several years after the one-week period of systemic treatment.

The localized nature of the periodontal infection and the easy access of the teeth has prompted the development of delivery systems which release the antimicrobial agent directly into the periodontal pocket. The first of these delivery systems that is commercially available is a tetracycline impregnated cord which can be wrapped around the tooth below the gingival margin. This cord releases over 100μg of tetracycline per ml of gingival crevicular fluid during the entire period that it is in situ. In this manner, patient compliance is assured and the plaque microbes are constantly exposed to therapeutic levels of the agent.

These data from the double-blind metronidazole studies indicate that EOP and AP respond to treatment as if they were anaerobic infections and would seem to presage the more frequent usage of anti-anaerobic agents, such as metronidazole, in the future treatment of periodontal disease. Further developments of delivery systems which release antimicrobials directly into the periodontal pocket should assure that in the future, most periodontal infections will be medically managed.


  1. Christersson LA, Wikesjo UM, Albini B, Zambon JJ, Genco RJ. Tissue localization of Actinobacillus actinomycetemcomitans in human periodontitis: II. Correlation between immunofluorescence and culture techniques. J Periodontol. 1987;58:540–5. [PubMed: 3305857]
  2. Dzink JL, Socransky SS, Haffajee AD: The predominant cultivable microbiota of active and inactive lesions of destructive peridontal disease. J Clin Periodontol 15:316:323, 1988 . [PubMed: 3292595]
  3. Genco RJ, VanDyke TE, Levine MJ. et al. Molecular factors influencing neutrophil defects in periodontal disease. J Dent Res. 1986;65:1379. [PubMed: 3023465]
  4. Keyes PH: The infectious and transmissible nature of experimental dental caries. Findings and implications. Archs Oral Biol 304, 1960 . [PubMed: 14408737]
  5. Krasse B: Caries Risk: A Practical Guide for Assessment and Control. Quintessence Publishing Co., Chicago , 1985 .
  6. Lamster I. Host mediators in gingival crevicular fluid: Implications for the pathogenesis of periodontal disease. Crit Rev Oral Biol Med. 1992;3:31–60. [PubMed: 1730070]
  7. Linhe J, Liljenberg B. Treatment of localized juvenile periodontitis: results after 5 years. J Clin Periodontol. 1984;11:399–410. [PubMed: 6378984]
  8. Loesche WJ, Giordano J. Metronidazole in Periodontitis V: Debridement should precede medication. Compendium. 1994;15:1198–1217. [PubMed: 7987887]
  9. Loesche WJ, Giordano J, Hujoel PP. The utility of the BANA test for monitoring anaerobic infections due to spirochetes (Treponema denticola) in periodontal disease. J Dent Res. 1990;69:1696–1702. [PubMed: 2212216]
  10. Loesche WJ. DNA probe and enzyme analysis in periodontal diagnostics. J Periodontol. 1992;63:1102–1109. [PubMed: 1336048]
  11. Loesche WJ. Role of Streptococcus mutans in human dental decay. Microbiol Rev. 1986;50:353. [PMC free article: PMC373078] [PubMed: 3540569]
  12. Miller WD: The Microorganisms of the Human Mouth. The SS White Manufacturing Co. Philadelphia, 1890 .
  13. NIDR: Oral Health of United States Adults. NIH Publ. No. 87-2868, 1987 .
  14. Page RC. The role of inflammatory mediators in the pathogenesis of periodontal disease. J Periodont Res. 1991;26:230–42. [PubMed: 1679130]
  15. Zambon JJ. Actinobacillus actinomycetemcomitans in human periodontal disease. J Clin Periodontol. 1985;12:1. [PubMed: 3882766]
Copyright © 1996, The University of Texas Medical Branch at Galveston.
Bookshelf ID: NBK8259PMID: 21413316
PubReader format: click here to try


  • PubReader
  • Print View
  • Cite this Page

Related information

  • PMC
    PubMed Central citations
  • PubMed
    Links to pubmed

Related citations in PubMed

See reviews...See all...

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...