Microbiology of Periodontal Disease — Present Status and Future Considerations by S. S. Socransky*

that this misconception persisted for close to four dec­ ades. The feeling that plaques were reasonably similar in composition was derived in part from studies of the infectious potential of plaque on subcutaneous injec­ tion into experimental animals and partly from studies of the microbial composition of pooled dental plaque. Experimental abscess studies indicated that the patho­ genic potential of plaque taken from healthy individ­ uals or individuals with different periodontal diseases was approximately equal (on a wet weight basis) when subcutaneously injected into experimental a n i m a l s . It was assumed that pathogenic potential mirrored mi­ crobial composition and thus the studies indirectly sug­ gested similarites in microbial composition. M o r e sig­ nificant were direct studies of microbial composition. Such studies usually employed pooled plaque and dif­ ferences in the subgingival microbiota were obscured by the simple act of combining supragingival and subgingival samples from several teeth. Since supragin­ gival plaque is usually more abundant (and more easily removed) than subgingival plaque, the samples often reflected the organisms dominant in the supragingival sites. Other difficulties encountered were more technical in nature including problems in dispersion of plaque samples (while maintaining cell viability) and recovery of microorganisms which were often oxygen sensitive or fastidious in their growth requirements. Technical and conceptual advances in the last decade have per­ mitted a more realistic view of dental plaque. Such advances include the routine use of continuous anaerobiosis techniques, better techniques of sample taking and dispersion, as well as improvements i n culture media and methods of identification of organisms. M i ­ crobiologic sampling from discrete sites and microscopy of sections of in situ human plaque have proven to be synergistic approaches which have permitted a clearer understanding of the localization and patterns of colo­ nization of possible subgingival pathogens. M u c h of this work is relatively recent and technically difficult to carry out. Thus information is more limited than one would hope. A brief synthesis of existing information might be helpful in understanding the approaches cur­ rently taken in the study of the microbiology of peri­ odontal diseases. The reader must be cautioned that gaps in our knowledge may alter some but certainly not all of the viewpoints expressed. Healthy periodontal tissues of humans appear to be associated with a scanty microbial flora located almost entirely supragingivally on the tooth surface. Microbial cell accumulations are usually 1 to 20 cells in thickness and are comprised mainly of Gram-positive coccal forms. The microorganisms commonly encountered in such sites in adults include Streptococcus mitis, Strepto­ coccus sanguis, Staphylococcus epidermidis, Rothia dentocariosa, Actinomyces viscosus, Actinomyces naeslundii, and occasionally species of Neisseria and Veillon ella. This list is not meant to exclude other forms which 18,19

PRESENT STATUS T H E R E IS A B U N D A N T evidence to implicate microorga­

nisms as the primary etiologic agents of various forms of periodontal disease (for reviews see ) . Particularly convincing were the demonstrations by Löe and co­ workers that removal of dental plaque by rigorous plaque control procedures or antiseptic a g e n t s could prevent or reverse clinical gingivitis in human volunteers. More recently, Lindhe and N y m a n and Rosling et a l . demonstrated that progress of destruc­ tive periodontitis could be halted and partially reversed by surgical procedures when accompanied by twice monthly professional tooth cleaning. These studies in­ dicated that suppression of the total microbiota could be effective in controlling both gingivitis and destruc­ tive periodontitis in humans. What the studies did not and could not indicate is whether all or only segments of the microbiota were responsible for the observed clinical response. The success of antibiotic therapy in controlling the acute phase of acute necrotizing ulcera­ tive gingivitis indicates the etiologic role of micro­ organisms in this form of human periodontal disease. Since only some of the species resident in bacterial plaque are sensitive to a given antibiotic, it is clear that only a finite segment of the microbiota is responsible for this disease. It would seem that there is sufficient evidence that microorganisms play a primary role in the etiology of most forms of human periodontal disease. The question is no longer whether organisms cause periodontal dis­ eases but rather are specific organisms responsible for specific disease forms? 1 - 6

7,8

9,10

11

1 2

13-17

M I C R O B I A L COMPOSITION O F P L A Q U E S A S S O C I A T E D WITH P E R I O D O N T A L T I S S U E S

Recent evidence from a number of laboratories sug­ gests that different forms of periodontal disease may have specific microbial etiologies. Examination of the microbiota associated with healthy tissues and tissues with different forms of disease revealed previously un­ suspected striking differences in microbial composition. The once prevalent view that dental plaque composi­ tion was reasonably consistent from individual to indi­ vidual and site to site is clearly not valid. It is of interest * Forsyth Dental Center, 140 Fenway, Boston, Mass 02115. 497

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frequently can be detected, but to indicate the orga­ nisms most likely to be encountered. In experimental gingivitis, there is an increase in the total mass of plaque and cell layers which often extend to 100 to 300 cells in thickness. The increase in plaque mass is accompanied by an increase in proportions of members of the genus Actinomyces. This group of or­ ganisms tends to be the dominant genus associated with supragingival plaque frequently comprising 5 0 % or more of the isolates. Thus, the predominant cultivable microbiota in developing plaques of this type is almost entirely Gram-positive and appears to represent an overgrowth of some of the forms found in plaques associated with healthy sites. In long standing gingivitis, approximately 2 5 % of the microbiota may be Gram-negative including species of Veillonella, Campylobacter and Fusobacterium. The Gram-nega­ tive cells appear to be located primarily on the surface of the plaque in subgingival s i t e s . In one form of periodontal disease, invasion of un­ derlying tissues is a prominent feature. Examination of lesions of acute necrotizing ulcerative gingivitis ( A N U G ) patients, by electron microscopy has revealed the presence of intermediate sized spirochetes with multiple axial fibrils invading the ulcerated tissues. Subsequent work on additional patients revealed that the spirochetes were in much higher concentration in the forefront of the lesion and in plaque immediately over the ulcer than in plaque located more coronally. Fusiform shaped organisms were also numerous imme­ diately coronal to the u l c e r . Studies of the microbial composition of lesions of periodontosis patients revealed the presence of a sparse microbiota which was predominated by Gram-negative capnophilic and anaerobic r o d s . Healthy subgingi­ val sites in the same patients revealed large percentages of Gram-positive organisms more typical of supragingi­ val plaque. The predominant organisms found in the lesions had not been previously associated with peri­ odontal disease and several types had not been previ­ ously described. One of the organisms most frequently isolated and isolated in highest numbers, was a Gramnegative fusiform shaped rod which would glide on agar surfaces. The characteristics of this organism are con­ sistent with the species Bacteroides ochraceus. How­ ever, extensive characterization of isolates of this group reveal major differences from the genus Bacteroides and a new genus Capnocytophaga will be proposed. Another Gram-negative anaerobic round-ended rod was isolated in high numbers from most patients. This organism would fit the genus Bacteroides but its charac­ teristics were not consistent with any recognized spe­ cies. Additional groups of Gram-negative rods were found in periodontosis patients but less frequently and in lower numbers. Light and electron microscopic ob­ servations of in situ plaque of periodontosis patients were consistent with the above microbiologic find­ ings. 20-23

20, 2 4 , 2 5

21,26

27

28,29

30-32

21

Microbiologic examination of subgingival plaque in rapidly destructive periodontitis revealed a predomi­ nance of Gram-negative rods. However, the types of organisms isolated were in large part different from those isolated from periodontosis lesions. A t least two patterns of subgingival colonization may be ob­ served. One pattern appeared to be dominated by Bac­ teroides melaninogenicus ss. asaccharolyticus and often harbored, "6-12-6" axial fibrilled spirochetes. A sec­ ond pattern appeared to be comprised of large numbers of monotrichously flagellated organisms and "corrod­ ing" bacteria, including an undescribed genus of anaer­ obic vibrios, "corroding" Bacteroides and Eikenella corrodens. Additional species found in these pockets included Fusobacterium nucleatum, and a newly de­ scribed group of fusiform shaped "gelatin loving" Bac­ teroides. Structural studies of in situ plaque associated with destructive periodontitis revealed a more complex pic­ ture than that observed in periodontosis. Plaque is usually more abundant and often consists in part of a zone of primarily Gram-positive organisms which are apparently attached to the tooth surface. Between this zone and the epithelium, one finds a zone of loosely "packed" Gram-negative organisms and spirochetes. This loose zone extends to the apical portion of the pocket. Destructive diseases of children of ages 5 to 12, appear to be characterized by a rather heterogeneous group of organisms. Most notable has been the fre­ quent isolation of high numbers of Bacteroides oralis strains as well as Group I V Bacteroides, Selenomonas sputigena, Clostridium species and anaerobic actinomycetes. Only additional cultural studies will reveal how con­ sistent these microbial patterns will be. It is possible that the pathologic processes may be better character­ ized by their microbiota than by their clinical appear­ ance or the age of the infected patient. In spite of the small numbers of patients examined to date, it is clear that disease sites are predominated by microorganisms which are not dominant in supragingival plaque. It appears likely that members of the unusual subgingival groups may be responsible for the observed tissue de­ struction. 33,3 4

21

35

P A T H O G E N I C P O T E N T I A L OF H U M A N PERIODONTAL ISOLATES

Data from animal pathogenicity testing has been interesting but far from conclusive in clarifying the etiologic agents of human destructive periodontal dis­ ease. In general, it has been extremely difficult to establish human oral organisms in the oral cavity of conventional animals. Thus, pathogenicity testing of human oral isolates has been largely confined to gnotobiotic animal systems. Early studies seeking etiologic agents of hamster or rice rat disease revealed that certain Gram-positive microorganisms including Acti-

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Microbiology

nomyces viscosus were capable of transmitting destruc­ tive periodontal disease from animal to a n i m a l . Initial studies of the pathogenic potential of human isolates in gnotobiotic rat systems revealed that certain Gram-positive organisms which would form plaque in vivo on high sucrose diets could accelerate destruction of alveolar bone. Such organisms included Streptococ­ cus mutans. Streptococcus salivarius, Actinomyces naeslundii, Actinomyces viscosus, Bacillus and Nocardia species. More recently, certain Gram-negative iso­ lates have been shown to accelerate alveolar bone loss when implanted as monocontaminants in gnotobiotic rats. These included a Bacteroides strain isolated from periodontosis, Capnocytophaga strains isolated from periodontosis and periodontitis, Eikenella corrodens, Bacteroides melaninogenicus ss asaccharolyticus, Fusobacterium nucleatum and Selenomonas sputigena strains from periodontitis. The Gram-positive and Gram-negative experimental infections, differed on a clinical and histopathologic basis. Disease induced by Gram-positive organisms tended to exhibit root caries, more plaque, and less abundant osteoclastic response than disease induced by Gram-negative o r g a n i s m s . ' Disease induced by either group of organisms demonstrated a minimal inflammatory response, with polymorphonuclear leu­ kocytes present in the pocket, but with few white blood cells present in the underlying connective tissue. L y m ­ phocytes or plasma cells were limited or absent in sections of tissue at sites of destruction. It is difficult to interpret the animal pathogenicity testing data. One feels that destruction induced by an organism reveals the potential of the organism to lead to loss of supporting structures. However, the gnoto­ biotic animal is a somewhat artificial situation, in that the animal is exposed to a pure culture of a human isolate without the possible ameliorating effects of other microorganisms. In addition, the host response, at least histologically is not typical of that detected in human lesions in which lymphocytes and plasma cells are quite numerous. 36-39

40-45

46-48

44,46,47

49

50

B A C T E R I A L SPECIFICITY I N D E S T R U C T I V E PERIODONTAL DISEASE

It is doubtful whether Koch's postulates can be ful­ filled for human periodontal disease and it is probably time that alternative criteria are set up for establishing etiology in human periodontal disease. The problem is somewhat unique in that one attempts to establish etiologic significance of an organism in the presence of continual infection by large numbers of possibly non­ pathogenic or even beneficial species. A t the moment at least two approaches seem theoretically possible in establishing etiology of a specific group of microorga­ nisms in human periodontal disease. The first would implant a suspected pathogen in a human free of the organism and induce the disease. This approach is not feasible on ethical grounds. The second would be to

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eliminate a suspected pathogen from an individual with active disease and determine if the disease stops. It is the second approach which has been of recent interest. The relatively limited spectrum of microorganisms found in sites of active destructive periodontal disease as well as the pathogenic potential of some of the isolates in gnotobiotic animal systems suggested the possibility that eliminating specific organisms by anti­ microbial therapy might be effective in controlling these disease forms. Preliminary studies in the clinics of Forsyth Dental Center suggest that a combination of surgical and sys­ temic antibiotic therapy can be effective in stopping the progress of certain destructive diseases including classic molar incisor periodontosis, and rapidly destructive periodontitis of adults. Since it was not known which organisms were responsible for destructive disease (if any) antibiotics were chosen which would affect the majority of isolates from pathologic sites of the individ­ ual patient. Antibiotics utilized on the basis of in vitro testing included tetracycline, penicillin and erythromy­ cin. The studies lacked an untreated control group or the more precise measurements offered by standard­ ized radiographs. Nonetheless, lesions did not measur­ ably progress for as long as 4 years post therapy. It should be noted that this therapy was not effected simply by a reduction in the quantity of plaque orga­ nisms. In some periodontosis patients more plaque was present after therapy than before but the plaque ap­ peared to be of different composition. The approach is discussed, less for its definitive na­ ture than for its potential as a probe in studying the microbial etiology of periodontal diseases. The use of antimicrobial agents with a more limited spectrum, coupled with a careful monitoring of disease status and the composition of the microbiota, might provide a useful approach in distinguishing possible host-compat­ ible and pathogenic microorganisms. Taken together, the demonstration of distinct micro­ bial populations in healthy sites and sites with different forms of periodontal disease, the differences in patho­ genic potential of different human pocket isolates, and the efficacy of therapy which suppresses some but not all members of the pocket microbiota suggests the like­ lihood that different forms of periodontal disease have specific microbial etiologies. This is not to say that a single species is responsible for all destructive disease (although the possibility cannot be ruled out), but rather that infectious diseases of the periodontium, like those in other parts of the body, can be initiated by any of a number of pathogens. Thus while 30 or more pathogens can lead to diseases of the lung or lower gastro-intestinal tract, the majority of infections in either site may be due to only a dozen or so organisms. It is likely that a similar situation exists in periodontal diseases. Perhaps 6 to 12 microbial species may be responsible for the majority of destructive periodontal disease, and additional forms may be responsible for

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destructive disease in a small percentage of the popula­ tion. R E L A T I O N S H I P OF GINGIVITIS A N D D E S T R U C T I V E PERIODONTAL DISEASE

The relationship between aggressive destructive peri­ odontal diseases and gingivitis is undergoing a re-evalu­ ation and is worth discussing. Page and Schroeder in an excellent review of the pathogenesis of inflamma­ tory periodontal disease clearly distinguished between the initial, early and established lesions of gingivitis and the advanced lesions of aggressive destructive peri­ odontal disease. They suggested that gingivitis may be a response to the accumulation of microorganisms but were uncertain as to the mechanism by which gingivitis switched to destructive disease. Two hypotheses were suggested. In the first, an activation of host immunopathologic processes would exacerbate the disease and lead to destruction of the tissues. In the second, an alteration of the local bacterial component, either by local overgrowth or addition of a pathogenic new spe­ cies would initiate tissue destructive processes. Existing data, summarized earlier, support the second hypothe­ sis. There appear to be qualitative and quantitative differences between the microbial composition of plaques associated with destructive periodontal dis­ eases and those associated with healthy tissues or tis­ sues exhibiting only gingival inflammation. In general, the microbial plaque associated with gingivitis appears to be predominately Gram-positive, often dominated by members of the genus Actinomyces. The microbiota associated with destructive lesions is usually dominated by Gram-negative organisms and frequently contains large percentages of motile forms. It is tempting to speculate that the most common form of periodontal disease, gingivitis, may be due to an accumulation of any of a relatively wide spectrum of microorganisms — especially Actinomyces species. The destructive dis­ eases which are less frequently encountered would require at least five conditions to be met. 1. A pathogenic species would have to be present in sufficient numbers to initiate disease. 2. The organism must be spatially located in such a way that the organism or its products can gain access to the target tissues. 3. The environment of the organism must permit its survival and multiplication. 4. Inhibiting organisms, i.e. organisms which "de­ toxify", dilute or destroy the pathogen, would have to be absent or present in low numbers. 5. The host must be "susceptible".* 50

50

50

The rather stringent proposed requirements for ac­ tive disease may in part explain the less common occur­ rence of destructive periodontitis. The requirements also would lead one to predict the frequent occurrence of the carrier state —the state in which an individual harbors a pathogenic organism but shows no signs or symptoms of disease. A pathogen might be detected in a given individual, but absence of any of the five "pre­ requisites" of disease would inhibit destruction from taking place. T H E Q U E S T I O N OF D E S T R U C T I V E D I S E A S E A C T I V I T Y

Lesions of established gingivitis can apparently per­ sist for years without leading to further destruction of the periodontium. It is not clear, however, whether destructive periodontal disease is really chronic in na­ ture. Two possibilities exist. Destructive periodontal diseases may progress at a slow relatively consistent rate with the cumulative tissue loss eventually leading to the loss of the tooth or there may be periods of exacerbation and remission in the progress of destruc­ tive disease. There is little hard evidence to clearly demonstrate whether one or both possibilities occur in different individuals. The first possibility theoretically exists and this type of destruction may occur in some forms of disease. However, a relatively consistent 3 µ/ day attachment loss for a 20-year period seems less likely than periods of remission interspersed with brief periods of more active destruction. In other words destructive diseases may be more episodic than chronic in nature. The implications of exacerbations and remissions from a microbiologic point of view are interesting. Assuming that the prerequisites of active disease listed earlier were fulfilled, then disease could be stopped by alteration of any one of them. For example, a decrease in numbers of pathogenic organisms, an increase in the distances between the organisms and the target tissue (e.g. by the tissue being destroyed) or an increase in numbers of competitive organisms could temporarily stop progress of the infection. O f particular interest would be a change in host susceptibility in which the host's immunologic system recognized and effectively dealt with an offending organism or metabolite of the organism. 50

4

CHEMOTHERAPY

Since most forms of periodontal disease appear to be initiated by microorganisms, it is not surprising that there is a growing interest in possible chemotherapeutic approaches to their control. The reader is referred to Loesche's fine review of the chemotherapy of dental infections for a detailed discussion of the current status of antimicrobial therapy and possible future applica­ tions. O f particular relevance was the discussion of the nonspecific plaque hypothesis. If periodontal diseases are nonspecific microbial infections, then all species in plaque would have to be suppressed continually 52

* Of all the terms which we use in discussing disease, susceptible and resistant are among the most convenient and the least precise. For many infectious diseases, it is not clear which features of the host make them susceptible or resistant. This situation does not apply to diseases in which antibodies are formed which neutralize the toxins of microorganism or prevent entry of viruses into cells. The role of the host response in periodontal diseases is under intensive investigation and has been discussed in some detail. 51

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Microbiology

throughout an individual's life. Chemotherapeutic agents would have to be chosen which were broad spectrum in activity, would not select resistant forms and had no additional biological side effects. The ubiq­ uitous occurrence of gingivitis and the widespread pres­ ence of its associated organisms suggest that less speci­ ficity may exist in this clinical condition than in other forms of periodontal disease. Thus chemotherapy of gingivitis might have to rely on long term use of anti­ septics or continual mechanical debridement. Chemotherapeutic control of destructive forms of periodontal disease may be more feasible. If there is specificity in the etiology of destructive periodontal diseases as suggested in previous sections, then elimi­ nation or suppression of a pathogen by antimicrobial agents would be a realistic goal. Determination of the species of organisms which cause destructive disease would permit laboratory monitoring of the efficacy of therapy and could lead to the possible prevention of disease by the elimination of pathogens prior to the initiation of destruction. A t the present time the clinician who employs chem­ otherapeutic agents is forced to work " b l i n d " because there are no simple, reliable methods to detect patho­ genic organisms or even certain knowledge of which organisms are pathogenic. For this reason, broad spec­ trum antibiotics such as tetracycline or rovamycin are usually employed. Often such agents lead to spectacu­ lar successes in controlling destructive disease. Occa­ sionally the agents fail. Therapy is not completely pre­ dictable because of uncertainty as to which organism is responsible for a given individual's disease. In spite of these difficulties, it is surprising how often antibiotic therapy appears to be successful. This fortui­ tous occurrence may be due in part to the broad spec­ trum of the chemotherapeutic agents employed and in part to the sensitivity of many of the target organisms. In spite of successes, antimicrobial therapy as currently employed cannot be considered to be optimal. It is not clear that the best agents are chosen for each clinical disease. In addition, the dosage employed, mode of administration, duration of therapy and need for asso­ ciated mechanical debridement or surgery all remain to be worked out. The essential first step in any of these approaches will be to delineate accurately the patho­ gens in each form of destructive disease. Once this has been accomplished, optimal methods of control can be intelligently worked out. FUTURE CONSIDERATIONS

This relatively brief summary of the present status of the microbiology of periodontal diseases omitted stud­ ies of classification, metabolism, ecology and patho­ genic determinants of organisms resident at or in the gingival crevice and periodontal pocket. This is not to suggest that such studies are not significant, but that space limitations precluded an exhaustive review of the literature. The interested reader may expand his or her

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knowledge in these areas by consulting a number of relatively recent r e v i e w s . The microbiologic control of periodontal diseases must rest on a sound foundation of fundamental infor­ mation. Unfortunately there are large gaps in our knowledge of the periodontal microbiota. For example, many of the organisms resident in the pocket cannot be classified by existing classification schemes. There has been a tendency on the part of oral microbiologists to "squeeze" or "force" their isolates into existing species descriptions. Great reliance has been placed on Bergey's M a n u a l , the Anaerobe Lab Manual ( V P I ) or the Wadsworth Manual ( U C L A ) for identification of oral isolates. The authors of the last 2 manuals warn their readers that the species descriptions are derived largely from isolates from clinical medical infections and are unlikely to be adequate for identification of organisms isolated from other human sites. It is clear that oral microbiologists must work out classifications for the microorganisms isolated from the periodontal pocket as an essential first step in distinguishing patho­ genic from host-compatible species. This does not mean that isolates from other sites in nature may not be the same as those from the oral cavity but rather that one must not count on such fortuitous occurrences to permit identification of isolates from this critical area of interest. The diversity of the species resident in the periodon­ tal pocket could be considered to be a bacterial physiol­ ogist's delight (or nightmare). Oral organisms in gen­ eral are reasonably to extremely fastidious in their requirements, varying considerably in terms of their energy sources, growth factor and physico-chemical requirements. The inability of investigators to culti­ vate many of the organisms resident in periodontal pockets continues to limit our ability to evaluate the role of the organisms in periodontal diseases. For ex­ ample, the failure to cultivate the intermediate spiro­ chetes observed in lesions of A N U G hampers further study of the role of this organism in the acute phase of disease. Studies of the metabolic potential of the orga­ nisms of the periodontal pocket have been extremely limited in terms of number and scope. Undoubtably studies of the physiology of the microorganisms will provide a fertile field for future investigation and could suggest possible approaches for their chemotherapeutic control. The ecological relationships of the periodontal mi­ crobiota have been only cursorily examined. The ques­ tion of when microorganisms establish in the pocket, their source, the reasons why organisms establish in one site and not another, their metabolic interrelation­ ships and attachment mechanisms remain in large part unanswered. Answers to these questions may permit a more thorough understanding of when to initiate pre­ vention or treatment and how one may be able to establish a more favorable environment for a hostcompatible microbiota. 1 - 6 , 5 3 , 5 4

55

56

5 7

58

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A relatively finite number of studies have attempted to seek determinants of microbial pathogenicity includ­ ing enzymes, toxins, toxic products, significant anti­ gens, etc. It is the view of this writer that such studies may be somewhat premature in that an individual may be seeking biochemical determinants of pathogenicity in microorganisms not adequately demonstrated to be involved in human periodontal diseases. If one sub­ scribes to the hypothesis that all organisms are essen­ tially equally pathogenic then one is on safer grounds on a philosophical basis but may not be better off in terms of determining virulence factors relevant to hu­ man periodontal disease. For this reason and others discussed earlier, it would seem imperative to determine with as much certainty as possible which microorganisms are involved in the ag­ gressive breakdown of periodontal supporting struc­ tures and to distinguish clearly between such orga­ nisms, organisms which initiate gingivitis, and orga­ nisms which are compatible with the host. Approaches to this problem are complicated by a number of factors. 1. The continual presence of a "contaminating" host-compatible microbiota both in healthy and dis­ eases sites. 2 . Failure to grow all of the organisms resident in the pocket. 3 . Inadequacies of classification of organisms cur­ rently cultivated. 4 . Technical difficulties in enumeration of micoorganisms in plaque samples and obtaining samples rep­ resentative of the microbiota associated with a specific clinical condition. 5. Problems in determining disease activity. Because distinguishing between host-compatible and destructive organisms will not be simple, a number of guideline considerations will be reluctantly suggested. 1. A pathogenic organism should be present at the site of active disease in higher numbers than in healthy sites in the same individual. The demonstration of a pathogenic organism in a site without disease may re­ flect a carrier state, a resistant host or the presence of a competing microbiota. 2 . Examination of microbial changes during the nat­ ural history of periodontal disease as it proceeds from normal to the periodontitis state may demonstrate an alteration in one or more species prior to or at the initiation of destructive lesions. This is potentially one of the best approaches to the problem although rather time consuming in terms of laboratory and clinical requirements. 3 . Elimination of suspected pathogens from sites of active destruction and concomitant monitoring of clini­ cal disease has already been discussed. One would have to demonstrate that other organisms remained and that the host response was not altered in other ways. 4 . Transmission of possible pathogens either pur­ posely or by chance may be instructive in terms of

demonstration of the etiologic role of certain microor­ ganisms. In the course of therapy, organisms might be transferred from an active site to one free of disease in the same individual. Demonstration of the organism's establishment and clinical fate of the sites would be instructive. The research community would frown upon the introduction of suspected pathogens into individ­ uals free of disease. However, if such transmission could be followed in the course of natural spread of infection (e.g. between husband and wife) then useful information on the role of suspected pathogens might be derived. 5. Pathogenic potential of an isolate in animal model systems only suggests that the organism may be patho­ genic in a similar fashion in the human, (but not neces­ sarily). The converse, lack of pathogenic potential in the animals is no more easily interpreted. Failure to induce disease in animals may reflect a lack of an appropriate model rather than a lack of virulence of the organism. For example, there are no good animal models for most of the treponematoses and throat in­ fections caused by beta hemolytic streptococci. 6. The host response may provide clues to a patho­ genic role of an organism. A n excessive or depressed immunologic response to a given species may delineate an organism involved in destructive disease. Alterna­ tively, the host may respond to antigens of harmless organisms which enter tissues damaged by the patho­ gens. In view of the finite capacity of gingival tissues to respond to a variety of antigens the failure of the host to distinguish between pathogenic and nonpathogenic organisms could have detrimental effects. Thus, inabil­ ity of a host to stop the progress of destructive lesions conceivably could be due in part to the host "wasting" its immunologic response on the wrong antigens. 59

A

FINAL

C O M M E N T

It would seem that the microbiological control of periodontal diseases (other than by mechanical de­ bridement) will have to proceed in two phases. In the first, pathogenic microorganisms must be targeted, rapid methods for their identification in clinical samples developed and optimal methods for their elimination established. The second phase would emphasize pre­ vention. It is by no means clear how periodontal diseases can be prevented other than by repeated removal of dental plaque. A t least three approaches come to mind. In the first, one would eliminate or suppress potential pathogens before destructive disease is initiated. The second approach is an offshoot of the first in that a host-compatible microbiota would be established in in­ dividual patients which would discourage the establish­ ment of potential pathogens. The third would involve immunization of populations against possible patho­ gens or their products. The feasibility of these ap­ proaches remains to be established. 60,62

Volume 48 Number 9

Microbiology REFERENCES

1. Genco, R . J . , Evans, R . T . , and Ellison, S. A . : Review of dental research: Dental research in microbiology with emphasis on periodontal disease. J Am Dent Assoc 78: 1016, 1969. 2. E l l i s o n , S. A . : O r a l bacteria and periodontal disease. / Dent Res 49: 198, 1970. 3. Keyes, P . H . : A r e periodontal pathoses caused by bac­ terial infections on cervicoradicular surfaces of teeth? J Dent Res 49: 223, 1970. 4. Socransky, S. S.: Relationship of bacteria to the etiol­ ogy of periodontal disease. J Dent Res 49: 203, 1970. 5. Kelstrup, J . , and Theilade, E . : Microbes and periodon­ tal disease. J Clin Periodontal 1: 15, 1974. 6. Socransky, S. S., and Crawford, A . C . R . : Recent advances in the microbiology of periodontal disease. Current Therapy, ed. 5, in press. St. Louis, C . V . Mosby, 1977. 7. Löe, H . , Theilade, E . , and Jensen, S. B . : Experimental gingivitis in man. J Periodontol 36: 177, 1965. 8. Theilade, E . , Wright, W . H . , Jensen, S. B . , and Löe, H . : Experimental gingivitis in man. II. A longitudinal, clini­ cal and bacteriological investigation. J Periodont Res 1: 1, 1966. 9. Löe, H . , and Schiott, C . R . : The effect of mouth rinses and topical application of chlorhexidine on the development of dental plaque and gingivitis in man. J Periodont Res 5: 79, 1970. 10. Löe, H . , Schiott, C . R . , Glavind, L . , and K a r r i n g , T . : T w o years oral use of chlorhexidine in man. I. General design and clinical effects. J Periodont Res Hi 135, 1976. 11. Lindhe, J . , and N y m a n , S.: The effect of plaque con­ trol and surgical pocket elimination on the establishment and maintenance of periodontal health. A longitudinal study of periodontal therapy in cases of advanced periodontitis. J Clin Periodontol 2: 67, 1975. 12. Rosling, B . , N y m a n , S., and Lindhe, J . : The effect of systematic plaque control on bone regeneration in infrabony pockets. J Clin Periodontol 3: 38, 1976. 13. Schuessler, C . F . , Fairchild, J . M . , and Stransky, I. M . : Penicillin in the treatment of Vincent's Infection. J Am Dent Assoc 32: 551, 1945. 14. Goldhaber, P . , and G i d d o n , D . B . : Present concepts concerning the etiology and treatment of acute necrotizing ulcerative gingivitis. Int Dent J 14: 468, 1964. 15. Mitchell, D . F . , and Baker, B . R . : Topical antibiotic control of necrotizing ulcerative gingivitis. J Periodontol 39: 81, 1968. 16. L o z d a n , J . , Sheiham, A . , Pearlman, B . A . , Keiser, B . , Rachanis, C . C , and M e y e r , P . : The use of nitrimidazine in the treatment of acute ulcerative gingivitis. A double blind controlled trial. Brit Dent J 130: 294, 1971. 17. Shinn, D . L . S.: Metronidazole in acute ulcerative gingivitis. Lancet 1: 1191, 1962. 18. Foley, G . , and Rosebury, T . : Comparative infectivity for guinea pigs of fusospirochetal exudates from different diseases. J Dent Res 21: 375, 1942. 19. Courant, P . R . , Paunio, I., and Gibbons, R . J . : Infec­ tivity and hyaluronidase activity of debris from healthy and diseased gingiva. Arch Oral Biol 10: 119, 1965. 20. Listgarten, M . A . , M a y o , H . E . , and Tremblay, R . : Development of dental plaque on epoxy resin crowns in man. A light and electron microscopic study. J Periodontol 46: 10, 1975. 2 1 . Listgarten, M . A . : Structure of the microbial flora associated with periodontal disease and health in man. A light and electron microscopic study. J Periodontol 47: 1, 1976. 22. Socransky, S. S., Manganiello, A . D . , Propas, D . ,

of Periodontal Disease

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O r a m , V . and van Houte, J : Bacteriological studies of devel­ oping supragingival dental plaque. J Periodont Res 12: 90, 1977. 2 3 . Slots, J . : The microflora in the healthy gingival sulcus in man. Scand J Dent Res 85: 247, 1977. 24. Loesche, W . J . , and Syed, S. A . : Bacteriology of dental plaque in experimental gingivitis. I. Relationship be­ tween gingivitis and flora. A.A.D.R. Abstract N o . 108, 1975. 25. Syed, S. A . , Loesche, W . J . , and Löe, H . : Bacteriol­ ogy of dental plaque in experimental gingivitis. 2. Relation­ ship between time, plaque score and flora. A.A.D.R. Ab­ stract N o . 109, 1975. 26. van Palenstein Helderman, W . H . : Total viable count and differential count of vibrio (Campylobacter) sputorum, fusobacterium nucleatum, selenomonas sputigena, bacte­ roides ochraceus and veillonella in the inflamed and noninflamed human gingival crevice. J Periodont Res 10: 294, 1976. 27. Listgarten, M . A . , and Socransky, S. S.: Ultrastructural characteristics of a spirochete in lesions of acute necro­ tizing ulcerative gingivostomatitis (Vincent's Infection). Arch Oral Biol 9: 95, 1964. 28. Listgarten, M . A . : Electron microscopic observations on the bacterial flora of acute necrotizing ulcerative gingivitis. J Periodontol 36: 328, 1965. 29. Listgarten, M . A . , and Lewis, D . W . : The distribution of spirochetes in the lesion of acute necrotizing ulcerative gingivitis: A n electron microscopic and statistical survey. J Periodontol 38: 379, 1967. 30. Slots, J . : The predominant cultivable organisms in juvenile periodontitis. Scand J Dent Res 84: 1, 1976. 3 1 . Newman, M . G . , Socransky, S. S., Savitt, E . D . , Propas, D . A . , and Crawford, A . : Studies of the microbiol­ ogy of periodontosis. J Periodontol 47: 373, 1976. 32. Newman, M . G . , and Socransky, S. S.: Predominant cultivable microbiota in periodontosis. J Periodont Res 12: 120, 1977. 33. Crawford, A . , Socransky, S. S. and Bratthall, G . : Predominant cultivable microbiota of advanced periodontitis. A.A.D.R. Abstract N o . 209, 1975. 34. Slots, J . : The predominant cultivable microflora of advanced periodontitis. Scand J Dent Res 85: 114, 1977. 35. Sasaki, S., Socransky, S. S., Lescord, M . , and Swee­ ney, E . A . : Destructive periodontal disease of children. II. Microbiological and immunological findings. A.A.D.R. Ab­ stract N o . 422, 1977. 36. Keyes, P . H . and Jordan, H . V . : Periodontal lesions in the Syrian hamster. III. Findings related to an infectious and transmissible component. Arch Oral Biol 9: 377, 1964. 37. Jordan, H . V . , and Keyes, P . H . : A e r o b i c , G r a m positive, filamentous bacteria as etiologic agents of experi­ mental periodontal disease in hamsters. Arch Oral Biol 9: 401, 1964. 38. D i c k , D . S., and Shaw, J . H . : The infectious and transmissible nature of the periodontal syndrome of the rice rat. Arch Oral Biol 11: 1095, 1966. 39. D i c k , D . S., Shaw, J . H . , and Socransky, S. S.: Fur­ ther studies on the microbial agent or agents responsible for the periodontal syndrome in the rice rat. Arch Oral Biol 13: 215, 1968. 40. Gibbons, R . J . , B e r m a n , K . S., Knoettner, P . , and Kapsimalis, B . : Dental caries and alveolar bone loss in gnotobiotic rats infected with capsule forming streptococci of hu­ man origin. Arch Oral Biol 11: 549, 1966. 4 1 . Gibbons, R . J . , and Banghart, S.: Induction of dental caries in gnotobiotic rats with a levan-forming streptococcus and a streptococcus isolated from subacute bacterial endocar­ ditis. Arch Oral Biol 13: 297, 1968.

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Socransky

42. Socransky, S. S., Hubersak, C , and Propas, D . : In­ duction of periodontal destruction in gnotobiotic rats by a human oral strain of Actinomyces naeslundii. Arch Oral Biol 15: 993, 1970. 43. Jordan, H . V . , Keyes, P . H . , and Bellack, S.: Peri­ odontal lesions in hamsters and gnotobiotic rats infected with Actinomyces of human origin. Arch Oral Biol 17: 175, 1972. 44. Irving, J . T . , Socransky, S. S., and Heeley, J . D . : Histological changes in experimental periodontal disease in gnotobiotic rats and conventional hamsters. J Periodont Res 9: 73, 1974. 45. Kelstrup, J . , and Gibbons, R . J . : Induction of dental caries and alveolar bone loss by a human isolate resembling Streptococcus salivarius. Caries Res 4: 360, 1970. 46. Irving, J . T . , Newman, M . G . , Socransky, S. S., and Heeley, J . D . : Histologic changes in experimental periodon­ tal disease in rats mono-infected with a G r a m negative orga­ nism. Arch Oral Biol 20: 219, 1975. 47. Irving, J . T . , Socransky, S. S., Newman, M . G . , and Savitt, E . : Periodontal destruction induced by Capnocytophaga in gnotobiotic rats. IA.D.R. Abstract N o . 783, 1976. 48. Crawford, A . C . R . , Socransky, S. S., Smith, E . , and Phillips, R . : Pathogenicity testing of oral isolates in gnoto­ biotic rats. AA.D.R. Abstract N o . 275, 1977. 49. Garant, P . R . : A n electron microscopic study of the periodontal tissues of germfree rats and rats monoinfected with Actinomyces naeslundii. J Periodont Res suppl. 15: 1, 1976. 50. Page, R . C , and Schroeder, H . E . : Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Invest 33: 235, 1976. 51. Clagett, J . A . , and Page, R . C : Insoluble immune complexes and chronic periodontal disease. Arch Oral Biol (In press). 52. Loesche, W . J . : Chemotherapy of dental plaque infec­

tions. Oral Sci Rev 9: 65, 1976. 53. Gibbons, R . J . : Adherence of bacteria to host tissues. Microbiology in Press, 1977. 54. Gibbons, R . J . , and van Houte, J . : Bacterial adher­ ence in oral microbial ecology. Annu Rev Microbiol 29: 19, 1975. 55. Buchanan, R . E . and Gibbons, N . E . : Bergey's Man­ ual of Determinative Bacteriology, ed 8, Baltimore, The Wil­ liams & Wilkins C o . , 1974. 56. Holdeman, L . V . , and M o o r e , W . E . C ; Anaerobe Laboratory Manual. Virginia Polytechnic Institute and State University, Blacksburg, Virginia, 1972. 57. Sutter, V . L . , V a r g o , V . L . , and Finegold, S. M . : Wadsworth Anaerobic Bacteriology Manual, ed 2. Anaerobic Bacteriology Laboratory, Wadsworth Hospital, L o s Angeles, 1975. 58. Loesche, W . J . : Importance of nutrition in gingival crevice microbial ecology. Periodontics 6: 245, 1968. 59. Sasaki, S., and Takazoe, I.: Antigenic competition in guinea pigs through gingival inoculation of antigens. Bull Tokyo Dent Coll 16: 59, 1975. 60. Lightner, L . M . , O ' L e a r y , T . J . , D r a k e , R . B . , C r u m p , P . P . , and A l l e n , M . F . : Preventive periodontic treatment procedures: results over 46 months. J Periodontol 42:555, 1971. 61. Suomi, J . D . , Greene, J . C , V e r m i l l i o n , J . R . , Doyle, J . , Chang, J . J . , and Leatherwood, E . C : The effect of controlled oral hygiene procedures on the progression of periodontal disease in adults: Results after third and final year. J Periodontol 42: 152, 1971. 62. Axelsson, P . , and L i n d h e , J . : The effect of a preven­ tive programme on dental plaque, gingivitis and caries in school children. Results after one and two years. J Clin Periodontol 1: 126, 1974.

Announcements T E M P L E U N I V E R S I T Y S C H O O L OF D E N T I S T R Y Temple University School of Dentistry, an equal opportunity employer, anticipates that several new, full-time clinic positions will be available after July 1, 1977, incident to expansion of facilities. Applications are invited for the following: ENDODONTICS FIXED PROSTHODONTICS PERIODONTICS PEDODONTICS

RADIOLOGY ORAL MEDICINE & DIAGNOSIS OPERATIVE DENTISTRY

Demonstrated professional and teaching experience is essential for success in these positions. Specialty board qualification or board eligibility, as appropriate, is required. Academic rank and salary are commensurate with responsibility, preparation, and experience. Mi­ nority and women candidates are encouraged to apply. Applicants should submit a curriculum vitae and other pertinent and supportive data to: Arthur L . Young, Assistant to Dean for Administration, Office of Dean, Temple University School of Den­ tistry, 3223 N Broad St., Philadelphia, Pa 19140. WESTCHESTER A L U M N I CHAPTER ALPHA O M E G A FRATERNITY The Westchester Alumni Chapter of Alpha Omega Fraternity announces that the 22nd Annual Seminar will be held on October 19, 1977 at the Hilton Inn in Tarrytown, New York. The speakers and their topics are: DR. ARNOLD WEISGOLD

"Occlusal Adjustment of the Natural Dentition"

DR. RALEIGH WILLIAMS

"Down-to-Earth Orthodontic Treatment with Stable Results" The presentations will run simultaneously all day. For further information contact: Robert H . Bruskin, D . M . D . , 333 Halstead Avenue, Mamaroneck, New York 10543. TUFTS U N I V E R S I T Y S C H O O L OF D E N T A L MEDICINE Tufts University School of Dental Medicine announces the annual IRVING GLICKMAN MEMORIAL LECTURE on Saturday, October 2 9 , 1977, at the Tufts Dental Health Sciences Building Auditorium, One Kneeland Street, Boston, Massachusetts. The Program follows: 9 AM-12 Noon

Introduction: DR. M A X J. PERLITSH "Periodontics and the Practice of Dentistry: Pre­ vention, Interception and the Why, When, and How of Therapy" —DR. ABRAM I. CHASENS, Fairleigh Dickinson University School of Den­ tistry .

1:00-3:30 PM

"Periodontal Therapy— Aspirations and Realiza­ tions"—DR. S. SIGMUND STAHL, New York University Dental Center College of Dentistry.

3:30-4:00 PM

Questions and Answers: DR. CHASENS AND DR. STAHL

Moderator: DR. JEROME B . SMULOW The annual Irving Glickman Memorial Lecture is presented under the auspices of the Irving Glickman Memorial Fund. This program is open to all dentists, free of charge, but reservations must be made by contacting the Department of Periodontology at 617-956-6530.