Review article

Similarities in the microfloras of root canals and deep periodontal pockets

Kerekes K, Olsen I. Similarities in the microfloras of root canals and deep periodontal pockets. Endod Dent Traumatol 1990; 6: 1-5. Abstract Although not universally accepted, retrospective histological, roentgcnological and microbiological studies have indicated that cross-infection can occur between infected pulps and deep periodontal pockets. This review provides examples of similarities in the microfloras of these adjacent oral sites, supporting the idea that infection spreads from one site to the other. The organisms most often involved are probably bacteroides, fusobacteria, eubacteria, spirochetes, wolinellas, selenomonas, campylobacter, and peptostreptococci. Important qualities of crossinfecting organisms may be the ability to survive in highly reduced environments and motility. Precautions should be taken to prevent in vivo seeding of such micro-organisms, particularly in compromised teeth and hosts. , Kasmer Kerekes', Ingar Olsen^
Departments of 'Endodontics and ^Microbiology, Dental Faculty, University ot Osio, Oslo, Norway

Key words: endodontics; periodontoiogy; crossinfection. Dr. Kasmer Kerekes, Dental Faculty, University of Oslo, Box 1109, Blindern, 0317 Oslo 3, Norway. Accepted for publication July 7, 1989.

Knowledge about the etiology and pathogenesis of periodontal diseases has increased in recent years. The most important factor may be the increasing recognition that certain micro-organisms or complexes of organisms may be more important as pathogens than others in vexed periodontal flora (1-3). Endodontal microbiology has also received increasing attention during recent years (4). Continuous anaerobic culture techniques have provided a more detailed knowledge of the microflora within and apically to the root canal. Such techniques have increased the recovery of anaerobic bacteria, and periapical lesions, frequently considered sterile, have now been found to harbour anaerobes (5). Demonstration of bacteria in periapical lesions is not consistent. Using light and electron microscopy, Nair (6) found that only a small fraction of the periapical lesions revealed bacteria within the body of the lesions, but such lesions were invariably acute and symptomatic. Recent research has demonstrated large similarities in the microfloras of advanced periodontitis and pulpal lesions, suggesting that cross-infection between these sites can occur (7). This review gives examples of this similarity, focusing on the bacteria most likely to participate in such cross-infection.

The floras of the root canal and periodontal pocket will not be fully reviewed. Gram-negative bacteria dominate in root canais of intact teeth with necrotic pulps and in periodontai pockets The predominance of gram-negative anaerobic bacteria in root canal infections and in marginal periodontitis has been demonstrated repeatedly. Sundqvist (8) showed by culture that as much as 90% of the microflora of necrotic pulps of intact, previously traumatized teeth contained gram-negative rods. Slots (9) found that gram-negative anaerobic rods constituted 74.9% of the predominant cultivable flora from the apical portion of deep periodontal pockets. In patients with localized juvenile periodontitis, Newman & Socransky (10) found that 50% or more of the most apical pocket flora contained gram-negative rods. Furthermore, Listgarten (11), using transmission electron microscopy, demonstrated that periodontal pockets exhibited diflerent microbial zones and that the most apical portion consisted of gram-negative bacteria. Regional variation in the composition of the flora has also been demonstrated in the root canal (12). The more apically the sample is taken, the larger 1

Kerekes & Oisen the chance for recovering anaerobes through cultivation.

ed as the only black-pigmenting Bacteroides species from deep periodontal pockets. B. intermedius may be involved in acute ulcerative gingivitis and pregnancy gingivitis (1). B. gingivalis is frequently the Ciinicai symptoms vs microflora dominant species in deep periodontal poekets of Sundqvist (8) and, later, Griflee et al. (13) showed adults, where it can constitute more than 40% of that in cases with acute clinical symptoms related the cultivable flora (18). Both B. gingivalis and B. to root canal infection, Bacteroides melaninogenicusintermedius can constitute major parts of the flora could be isolated. Recently, Sundqvist et al. (14) associated with generalized periodontitis. In deep found that 16 of 22 root canals containing blackpockets B. gingivalis may proliferate at the expense i pigmented Bacteroides were associated with acute of other organisms through the production of hema-; apical abscesses and purulent drainage through the tin and bacteriocin (19). '\ root canal. Haapasalo et al. (15) recovered B. gingiB. gingivalis has also been isolated from necrotic valis, B. endodontalis and B. buccae exclusively frompulps (14, 15), which emphasizes that the perio-' pulps with acute symptoms. Further, Yoshida (16) dontal pocket is not the only ecological niche of this j frequently isolated Bacteroides species and Peptococcusorganism. ! magnus in clinically acute cases, and Heimdal et al. B. endodontalis is regarded as a speciflc agent of (17) found Fusobacterium nucleatum to be especially endodontal infections. Sundqvist (8) found this or- j associated with the severity of orofacial infections of ganism, which later acquired its name (20), in 11% \ odontogenic origin. These results seem to indicate of root canal infections of intact teeth. B. endodontalis] that certain bacterial species are more important is closely related to B. asaccharolyticus, which is generthan others in inducing pyogenic endodontal infecally considered a habitant of the gastrointestinal tion. However, the accompanying flora may also tract. The reason why B. endodontalis is usually found contribute, for example, by providing growth factors for key organisms. Thus, Bacteroides is provided in the root canal may be its lack of flmbriae (21), which probably makes adhesion to oral soft tissues with naphthoquinone and succinate (1). diflicult. In comparison, B. gingivalis possesses fim-! It has also been possible to associate certain bacbriae and adheres well to host tissue cells and gramteria with clinical symptoms in advanced periopositive bacteria of preformed dental plaque (22). dontitis. A correlation has been demonstrated beLike B. gingivalis, B. endodonialis seems to have a tween the degree of clinical inflammation, including pronounced ability to induce purulent infections the tendency to suppuration, and the quantity o{B. (23). gingivalis cultured (18). When B. intermedius was the predominant agent, no such correlation could be established. .: 'Hi Nonpigmenting Bacteraides Biack-pigmenting Bacteroiiles Nonpigmenting Bacteroides have received little atten-

Bacteroides is the dominating anaerobic genus of root tion in oral microbiology. However, nonpigmenting Bacteroides occur in the root canal quite as frequently canal infections, but the rate of recovery by cultias pigmenting Bacteroides (24). The most frequent; vation varies in different studies. This may be respecies are B. buccae, B. oris and B. oralis. lated to variances in the cases examined and in the Nonpigmenting Bacteroides are also isolated from! methodology used. Sundqvist et al. (14) detected black-pigmenting Bacteroides in 22 root canals of 72 marginal periodontitis and were originally de-i scribed as B. ruminicola subsp. brevis. Kornman & teeth with apical periodontitis; Haapasalo et al. (15) recovered black-pigmenting Bacteroides from 50% of Holt (25) described a new Bacteroides species, B. capillus, which constituted the major cultivable part infected, necrotic root canals of noncarious teeth. Among these isolates, B. intermedius, B. endodontalis of the flora associated with advanced periodontitis.: and B. denticola were detected most frequently (14, B. buccae is a synonym for B. capillus. Infected, necro tic root canals where B. buccae is present are fre15). The prevalence of the latter may have been quently associated with subjective symptoms (24).j underscored in previous reports because the optimal This organism has a surface (S) layer of crystallin'ej pigmentation of this organism requires specific host protein highly immunogenic in rabloits (24). Its highj blood in the medium. The association between B. intermedius and mar- antigenicity may be an explanation for the acute, ginal periodontitis is unclear. B. intermedius is fre- symptoms. Interestingly, B. heparinolyticus and B.I forsjthus, of which the latter has been associated with quently isolated from advanced periodontitis of active marginal periodontitis, also have an S-layen adults but usually together with a higher number .-,,,, J of 5. gingivalis. Sporadically, B. intermedius is recover- (26,27). 2

Microfloras periodontal pockets the number of spirochetes increases as the periodontal conditions deteriorate, except for localized juvenile periodontitis, in which Fusobacterium, Eubacterium, Peptostreptococcus and Cam- few spirochetes are usually present (37). Spirochetes pylobacter are the most frequent genera in infected, can constitute up to 50% of the microflora of deep necrotic root canals of intact teeth, in addition to pockets in postjuvenile and actively progressive Bacteroides (8). Indeed, this is a limited number of periodontitis (37). The microscopic profile of spirogenera considering the large number that can be chetes follows numerically the culture profile of B. found in periodontal pockets. These observations gingivalis. Plaque taken from stable pockets, i.e. are supported, however, by lindings in experimenpockets that have not exhibited bone loss during tally infected monkey teeth, as the number of bac1 year or more, contains only small numbers of terial genera that survived in an orally sealed root spirochetes (3%) (37). It is generally accepted that canal decreased considerably with time (12, 28). spirochetes can invade tissue. Some of them have Others have also found Fusobacterium as a domina- an S-layer (38). ting genus in the root canal. Haapasalo et al. (15) detected F. nucleatum in 12% of all root canal isolates Actinobacillus actinamycatamcomitans and Sundqvist et al. (14) found this organism in 12 of 16 teeth with apical abscesses. Actinobacillus actinomycetemcomitans is considered to be F. nucleatum is among the dominant speeies of deep the main etiologie agent in localized juvenile perioperiodontal pockets. Slots (9) isolated this organism dontitis (39). Besides, Tanner et al. (18) found A. from all patients with advanced periodontitis, and actinomycetemcomitans as one of the most frequent isoit dominated in 2 of the patients. Moore et al. (29) lates in advanced periodontitis of adults. In infected found that F. nucleatum, which was the most common neerotic pulps of intact teeth this organism seems to bacterial speeies, constituted 82% of 2305 isolates be rare. Haapasalo (15) isolated A. actinomycetemcomifrom patients with moderately pronounced or juventans from only 1 of 62 necrotic pulps. This is supile periodontitis. Fubacterium has been isolated in ported by experimental studies. Strict anaerobic orlarge quantities from advanced periodontitis of ganisms survive better in root canals that are closed adults and juvenile periodontitis (10, 29). Moore et after exposure than do facultatively anaerobic oral. (29) isolated 19 diflerent Eubacterium species, ganisms (12). which constituted 12.1%, of the cultivable flora. Fusobacterium, Eubaetarium, Peptostreptoeaccus and Campylobactar
Peptostreptococcus and Campylobacter seem to be more

abundant in the pocket flora than in the root canal. Motiie bacteria During recent years interest has been devoted not only to Campylobacter but also to other motile bacteria. Both Wolinella and Selenomonas can be among the dominating genera in periodontal pockets with attachment loss (29, 30). W. recta is frequently isolated from periodontal sites with aetive disease, together with nonmotile fusiform Bacteroides, B. intermedius and Actinobacillus actinomycetemcomitans (30).

Microfiora of root canal and adjacent periodontal pocket Remarkably few studies have directly compared the microflora of the root canal and that of the adjacent periodontal pocket in the same patient. Kipioti et al. (7) found large similarity in such floras. The examined teeth were intact and without periapical lesions, which supported the idea that the pocket can be regarded as a possible source of root canal infection. In such cases there is a correlation between the existence of bacteria in the root canal and radiographically recorded marginal bone loss rather than with radioluceiicy of the periapical bone (8, 40). Roots of periodontally diseased teeth can also act as bacterial reservoirs in the recolonization of mechanically treated root surfaces and can infect the dental pulp (41). Since these bacterial reservoirs are not eliminated by conventional mechanical periodontal treatment, it has been suggested that mechanical periodontal therapy be combined with the use of chemotherapeutic agents (42). Conclusions Similarities in the endodontal and periodontal microflora of intact teeth without periapical lesions indicate that cross-infection between the root canal 3

In one study anaerobic, gram-negative motile rods including speeies of the genera Wollinella and Selenomonas constituted 9% of the cultivable root canal , flora (15). Interestingly, Tanner et al. (31) found large DNA/DNA homology between W. recta from root canals and periodontal pockets. All the endodontal W. recta isolates came from teeth with periapical radiolucencies. The periodontal isolates were cultured from pockets with pronounced bone loss and clinically demonstrable inflammation. W. recta has a crystalline surface layer (32-34). Spirochetes have been demonstrated with dark fleld microscopy in samples from nonexposed root canals (35) and endodontal abscesses (36). In deep

Kerekes & Olsen and periodontal pocket can occur. This idea is supported by theoretieaOy communicable pathways between the pulp and the periodontal ligament (43). Considering the large variety of organisms colonizing the periodontal pocket vs that recovered from necrotic pulps of intact teeth, the number of species participating in such cross-infection must be limited. First of all, they include anaerobes such as Bacteroides, Fusobacteria, Eubacteria, Spirochetes, Wolinella, Selenomonas, and Peptostreptococcus. (Most peptococci

to symptoms associated with pulpal necrosis. Orat Surg Orat Med Orat Pathot 1980; 50: 457-61. 14. SuND^jvisT G, JOHANSSON E, SJOGREN U. Prevalence of blackpigmented Bacteroides species in root canal infections. J Endod 1989; 15: 13-19.
15. HAAPASALO M , RANTA H , RANTA K , SHAH H . Black-pig-

mented Bacteroides spp. in human apical periodontitis. Infect Immun 1986; 53: 149-53. 16. YOSHIDA M . Gorrelation between clinical symptoms and microorganisms isolated from root canals of teeth with periapical pathosis. J Endod 1987; 13: 24-6.

17. HEIMDAL A, VON KONOW L , SATOH T, NORD G E . Glinical .'

appearance of orofacial infections of odontogenic origin in have now been transferred to genus Peptostreptococrelation to microbiological findings. J Ctin Microbiot 1985cus.) Of these spirochetes, wolineflas and selenomon22: 299-302. as are motile. Facultatively anaerobic and motile 18. TANNER A G R , HAFFER G, BRATTHALL G T , VISCONTI R A , campylobacter may also participate, whereas faSOCRANSKY SS. A study of the bacteria associated with ad- vancing periodontitis in man. J Ctin Microbiot 1979; 6: cultative, nonmotile actinobacilli do not. The pro278-307. portion of anaerobic and motile organisms suggests 19. TAKAZOE I, NAKAMURA T, OKUDA K . Golonization of the that the ability to sustain highly reduced environsubgingival area by Bacteroides gingivatis. J Dent Res 1984; 63 ments and motility are not prerequisites for cross422-6. 20. VAN STEENBERGEN T J M , VAN WINKELHOFF AJ, MAYRAND infection, but they are bacterial qualities likely to be D, GRENIER D R , DE GRAAFF J. Bacteroides endodontalis sp of advantage. A chronic infection in the periodontal nov., an asaccharolytic black-pigmented Bacteroides species pocket or in the root canal may represent a persistfrom infected root canals, hit J Syst Bacteriol 1984; 34: 118-20. ent supply of bacteria to the bloodstream, spreading 21. HAAPASALO M , RANTA H , SHAH H , RANTA K , LOUNATMAA organisms to nonaffected parts of the tooth organ K. Isolation and characterization of a new variant of blackpigmented asaccharolytic Bacteroides. EEMS Microbiot Lett as well as to other organs of the body. Precautions 1984; 23: 269-74. should be taken to prevent such in vivo seeding, 22. SLOTS J, GIBBONS RJ. Attachment of Bacteroides metaninoparticularly in compromised teeth and individuals. genicus subsp. asacctiarotyticus to oral surfaces and its possibl

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