Periodontology 2000, Vol.

28, 2002, 206239 Printed in Denmark All rights reserved

Copyright C Munksgaard 2002

PERIODONTOLOGY 2000
ISSN 0906-6713

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

N G UNNAR D AHLE
Dental or dentoalveolar abscesses are infections of dental origin, the majority with an endodontic or a periodontal pocket origin. Dental abscesses also include pericoronitis and abscesses caused by trauma and surgical infections. The incidence of serious odontogenic infections has decreased dramatically over the last half century due to preventive dental care and the availability of more effective antibiotics. However, dental abscesses still occur, and they may lead to serious consequences by spreading, involving the bone or various spatia, which might result in lifethreatening conditions. Periapical and periodontal abscesses may advance into combined periodontalendodontic lesions. Most dental abscesses are caused by the resident oral microora that enters normally sterile tissues. Mechanical removal of necrotic infected tissues and surgical drainage are the most important treatment steps. Antibiotics are indicated in case of systemic symptoms and to limit the spread of the infection. This chapter reviews present knowledge of the dental abscess in respect to pathology, microbiology and treatment. main types: the endodontic (periapical) abscess formed after necrosis of the dental pulp and subsequent infection of the root canal, and the periodontal abscess formed after infection of the periodontal tissues by bacteria of the subgingival microbiota. A special variant of the periodontal abscess is pericoronitis, which may develop as an infection of the pericoronal soft tissue overlying the crown of the tooth. Inamed pockets normally drain continuously, but microorganisms and debris may become entrapped in the pocket, leading to an acute infection. Abscess formation is readily identied clinically due to concurrent signs and symptoms such as pain, redness and swelling of the abscess area, regional lymph node enlargement, spasm of the muscles and trismus (57). The expanding lesion can spread considerably through soft tissue. An abscess that only involves soft tissue is termed cellulitis. The spreading may also involve bone (osteitis) or the bone marrow (osteomyelitis), which both constitute serious complications (147). Destruction of bony tissue may not occur immediately, and radiographic signs of bone destruction are not always detectable. Dental abscesses and abscesses in general expand through tissue providing least resistance by forming a sinus tract (stula). In case of the periodontal abscess, drainage is most likely to take place through the periodontal pocket since this is usually the path of least resistance. In case of a periapical abscess, the spread is primarily dictated by the thickness of the overlying bone and the location of the abscess in relation to muscle attachments. In the maxilla, periapical abscesses drain through the palatal bone into the oral cavity or rarely into sinus maxillaris or the nasal cavity. The mandibular periapical abscess drains commonly through the buccal bone into the oral cavity. Infection may occasionally spread along facial spaces or by the

Denition and clinical characterization of dental abscesses and periodontal-endodontic lesions

An abscess is a localized collection of pus in a cavity formed by the disintegration of tissues. The formation of pus is termed suppuration. To emphasize the presence of pus in abscesses, the term purulent abscess is often used. Abscesses of odontogenic origin are dental abscesses formed in or around the tooth and dentoalveolar abscesses that also involve the alveolar bone, but the two terms are often used synonymously. Dentoalveolar abscesses consist of two

206

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions Fig. 1. Equation of infection

redox potential (216). Obstruction, stasis, necrosis, tissue destruction, vascular insufciency and foreignbody presence are local factors commonly involved in dental abscess development.

Acute and chronic infection

Infection can be dened as the invasion of the body by pathogenic microorganisms and reaction of the tissues to their presence or to the toxins generated by them (42). The acute infection is characterized by invading and multiplying bacteria. Host tissues respond with vascular dilatation and increased blood ow, accumulation of liquid (edema) and inux of phagocytic leukocytes, in particular polymorphonuclear leukocytes, possibly resulting in abscess formation. The tissue reaction is a rapid and primarily unspecic inammatory response to foreign materials, bacteria and bacterial products entering the tissues. If bacteria and their products are accidentally forced into the tissue, such as by pocket probing or endodontic instrumentation beyond the apex, the host response may be efcient enough to phagocytize entering microorganisms with no clinically detectable consequences. The critical stage arises when bacteria survive and start multiplying within the tissues (185). The anaerobic infection is usually polymicrobial and thus different from infections caused by many facultative pathogens. The frequently low virulence of single anaerobic species and the need for cooperation and synergism between bacteria to form pathogenic combinations are characteristics of anaerobic infections (159). It is also probable that in a locally or systemically compromised host, the presence of certain virulent microorganisms or an increased number of microorganisms or combinations of certain microorganisms may invade host cells or tissue and induce clinical infection (Fig. 1). Evidence for the occurrence of bacterial invasion in oral tissues is given in Table 1. Depending on the

lymphatics to regional lymph nodes (18). Spread via the bloodstream is rare; however, in patients undergoing surgical incision and drainage of the dentoalveolar abscess, bacterial spreading by blood is quite common (56, 140). The mandibular periapical abscess may expand below musculus myohyoideus and reach facial spaces. If the sublingual and submandibular (Ludwigs angina) or pterygomandibular space are involved, respiratory obstruction or other lifethreatening conditions may occur (20). Mediastinitis, orbital infections and brain involvement are rare complications of dental abscesses (58, 132, 190). In periodontal health, the stula drains rarely from a periapical abscess along the root surface into the gingival pocket. On the other hand, in periodontally diseased sites, it is plausible that the periapical infection drains through the deep periodontal pocket to form a periodontal-endodontic lesion. Even after drainage of the abscess, the causative bacteria may not be completely eliminated but may reside in the tissues, such as in the apical part of the root canal or in the root-cement layer of the tooth. If so, the abscess may transform into a chronic state.

Pathology of dental abscess

Anaerobic infection
The vast majority of dental abscesses are polymicrobial anaerobic infections (54). Anaerobic infections are opportunistic in the sense that they develop under certain general and/or local predisposing conditions (54). Diabetes mellitus, corticosteroids, neutropenia, hypogammaglobulinemia, malignancy, immunosuppression and cytotoxic drugs are well-known systemic conditions that favor the bacteria in the delicate balance (microbial homeostasis) between the host and the parasites (140). Local factors that may disrupt the microbial homeostasis and facilitate the tissue invasion of microorganisms are related to decreased

Table 1. Evidence for tissue invasion by oral bacteria

Invasion due to trauma bacteremia Invasion due to bacterial growth bacteria in dentine tubuli in caries lesions and root surfaces in periodontitis Invasion due to bacterial motility spirochetal invasion in acute necrotizing ulcerative gingivitis Invasion due to cell phagocytosis neutrophilic granulocytes and pocket epithelial cells

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n Dahle

efciency of the host defense to combat invading bacteria or their products and depending on the ability of the bacteria to survive and withstand the host defense, the abscess may cease or continue to expand. An important outcome of the host defense is the limitation of the infection, supported by formation of a brotic capsule. The formation of a sinus tract to drain the area of pus is also an important step in controlling clinical infection. If the host response is insufcient, the bacteria continue to multiply, with the risk of expanding the infection. The bacteria may then enter the lymphatic system. The lymph nodes react with increased blood ow, swelling and pain. Systemic symptoms such as general discomfort, fever and dizziness indicate progressive infection. In rare cases spread into the blood system (bacteremia or sepsis) may occur. Pain and other symptoms of dental infections can be abundant and lead patients to seek emergency dental care. Hard tissues may be involved, but the resorption of bone and teeth is not always identiable on radiographs, making the infection difcult to localize. Furthermore, dental abscesses may cause pain and tenderness over a large area, complicating identication of the infected tooth. Chronic infections occur when microorganisms cease to be invasive but for various reasons are retained within the tissues. The development of a chronic inammatory lesion is quite common for dental abscesses due to possibility for bacterial retention, either endodontically in the root canal (apical portion) or periodontally in deep pockets or in the necrotic root-cement layer. Adhering bacteria show increased resistance to phagocytosis by neutrophils (225), favoring bacterial retention. Chronic inammation is related to the formation of a granulation tissue with a variety of cells, especially lymphocytes that participate in immunological activities (116). The granuloma forms in response to inammatory stimuli that activate components of the immune system and is characterized more by tissue reorganization than tissue destruction. Granulation tissue aims to conne bacterial presence to the area of the original infection. However, the formation of relatively infection-resistant tissue has its price in terms of loss of normal tissue. Similarly to acute infection, chronic infections may also involve bone destruction which, however, is usually detectable on radiographs. In longstanding chronic periapical lesions, the bone surrounding the lesion may be sclerotic, thereby potentiating the demarcation of the infection (35). It is important to appreciate the immune events

in chronic infections. Genco & Slots (60) argued that antibodies and other immune reactions in fact stimulate healing and brosis of chronic lesions. Similarly, in monkeys preimmunized against bacterial species that later were introduced into the root canal, the host response in periapical lesions showed a more distinct demarcation zone and less inammation compared with the host response in non-immunized monkeys (30). Periodontitis cannot be prevented by high levels of circulating antibodies in immunized animals (98), but antibodies may facilitate the formation of relatively resistant tissue architecture and function. Circulating antibodies may also combat bacterial species commonly found in experimental dental abscesses (33, 44, 62, 104). Immununological reactions of periodontal and periapical lesions are beyond the scope of this chapter and are reviewed elsewhere (41, 98, 116, 187, 199). A chronic infection shows little or no symptoms, and patients may not even be aware of the existence of the lesion. It is also important to recognize that a chronic infection may transform into an acute lesion due to changes in homeostasis between the host and microorganisms. This occurs quite often in endodontic therapy, by overinstrumentation of the root canal le beyond the apex, which creates bleeding or increased exudation into the canal, which provides stimuli for multiplication of microorganisms. Clinically, acute exacerbation is referred to as a are-up (6). Periodontal probing and scaling may cause a similar disturbance in the balance (homeostasis) between the host and the subgingival ora, causing certain bacteria to multiply and invade periodontal tissues. The possibility of an occasional negative effect from periodontal mechanical debridement is sparsely recognized in the literature (23, 40).

The pathology of the periapical abscess

The pathological features of the periapical abscess depend on the microbial activity occurring in the apical part of the root canal, having little room for expansion except through the apical foramen. The necrotic pulp of the root canal serves as an important source of bacterial nutrition. Proteolytic bacteria predominate the root canal ora, which changes over time to a more anaerobic microbiota (49, 196). Even when the infection occurs outside the apical foramen and in the periapical tissues, immediate drainage is not possible and ongoing tissue destruction and pus formation may result. The abscess usually expands through the bone by a sinus tract

208

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

formation. The dentist may also create drainage through the root canal and the pulp chamber. Actinomycosis Actinomycosis is a rare disease that mostly is described in the literature as case reports (161). In its classical form, actinomycosis is a chronic suppurative infection that occurs in three locations: cervicofacial, abdominal and pulmonary. The cervicofacial form may develop from a periapical lesion on teeth with infected root canals and exhibits a specic histological picture of Actinomyces colonies forming a rosette within an apical granuloma (157). Actinomycotic lesions may also be purulent and drain through multiple stula. Although Actinomyces israelii is the most common etiology, Arachnia propionica and other Actinomyces spp. have also been isolated from actinomycotic lesions (14, 157). Actinomyces also occurs in chronic periapical granulomas (periapical actinomycosis) in therapyresistant cases (81, 82). Although Actinomyces cells can be phagocytized in vitro under experimental conditions, they collectively evade elimination by phagocytic cells in vivo by forming their characteristic colonies, enabling the organism to survive during the acute inammatory phase (53). Actinomycotic osteomyelitis is being increasingly identied and may develop from longstanding periapical actinomycosis (7, 99, 141).

40). Also if drainage through the pocket is obstructed by gingival occlusion after improved supragingival hygiene, the result may be increased activity of subgingival bacteria and abscess development. Foreign bodies such as calculus and food debris may be pushed into gingival tissue during debridement and cause abscess formation (40). Periodontal abscesses around barrier membranes in guided tissue regeneration have also been reported (59). In ligatureinduced experimental periodontitis in animals (114, 115), the foreign body of the ligature placed in the periodontal pocket apparently drives the balance between bacteria and host in favor of infection, causing rapid periodontal breakdown, although abscess formation is usually not reported. Using Staphylococcus aureusinfected sutures in an experimental model, Elek & Conan (45) showed that 107 cells were needed to cause infection by subcutaneous injection but, if retained in a suture, less than 100 cells were required to induce infection. Pericoronitis is a special form of the periodontal abscess that develops in the pericoronal soft tissue that partially overlies the crown of the tooth. If microorganisms and debris become entrapped in the periodontal pocket and obstruct drainage, the pericoronal infection may spread to form an abscess. Third molar teeth of the mandible are most frequently involved.

The pathology of the periodontal-endodontic lesion

The periodontal-endodontic lesion develops by expansion of either (a) a periodontal destruction apically combining with an existing periapical lesion or (b) an endodontic lesion merging marginally with an existing periodontal lesion. As long as the pulp is vital, the lesion should be diagnosed as a periodontal lesion and treated as such. In case of loss of pulp vitality, it can be difcult to determine whether the lesion is primarily of periodontal or endodontic origin. If there is periodontal breakdown around a nonvital or root-lled tooth, an endodontic infection should always be considered. Diagnostic difculty may occur if a root canal infection communicates with the marginal periodontium through lateral canals, perforations or root fractures, which may lead the dentist to overlook the endodontic inammation (11). As stated by Bergenholtz et al. (11): Although, clinically, one may be able to bring a probe through both lesions, it is important from a therapeutic point of view to understand that the coronal part is directed towards an infection in the marginal peri-

The pathology of the periodontal abscess

The periodontal abscess has been dened as a suppurative lesion associated with periodontal breakdown and localized pus in the gingival wall of the periodontal pocket (90). The prevalence of periodontal abscesses is lower than that of periapical abscesses (90). Although the pathology of the periodontal abscess is not known in detail, it is reasonable to assume that its basic pathogenic mechanism is similar to that of abscesses in general. Multiplication and invasion by one or a group of subgingival species constitute the starting-point of abscess formation. The increased bacterial activity may be due to either (a) a disturbance of the microbial homeostasis, (b) a destruction of the epithelial barrier or (c) random events. Reports indicate that treatment with systemic antibiotics in patients with advanced periodontitis may cause abscess formation, probably due to overgrowth of resistant pathogens (89, 203). Traumatic injury and bleeding may also predispose for acute exacerbation of untreated periodontitis (23,

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n Dahle

odontium and the apical part to an infection emerging from the root-canal system. The manifestation of an acute endodontic lesion in the marginal periodontium leads to rapid destruction of apical periodontal attachment. Drainage may take place through two routes: (a) a sinus tract along the periodontal ligament or (b) an extraosseous stulation (11). Both routes may drain marginally through the gingival pocket. Both clinical and animal experiments have revealed that the vitality of the pulp is not impaired by scaling and root-planing procedures (11). If localized inammation occurs in the pulp as a consequence of root surface instrumentation, it normally heals uneventfully. The prognosis of a tooth with a periodontal-endodontic lesion suspected of being primarily of endodontic origin is usually good, even in case of nonvital and infected pulp tissue.

Diagnosis Many studies do not explicitly describe the precise origin (endodontic, periodontal or other) of the dental abscesses investigated. However, since the prevalence of endodontic abscesses is considerably higher than other types of dentoalveolar abscesses, the reports reviewed in Table 2 may be expected to incorporate mostly dentoalveolar abscesses of endodontic origin. Studies on dental abscesses with a designated origin as endodontic, periodontal or pericoronitis are reviewed separately (Tables 35). Microbial sampling Obtaining samples from dental abscesses without contamination from saliva and the surrounding mucosal surface is fraught with difculties. Studies of acute dental infections that collected microbial samples on swabs and cultured samples after possible delay using limited anaerobic culture methods describe an average of 1.01.6 isolates per sample and a predominance of viridans streptococci and staphylococci (130). In contrast, studies employing aspiration through a sterilized mucosal surface and promptly culturing using strict anaerobic techniques show a mean number of bacterial isolates per sample of 2.57.4 species with a predominance of strictly anaerobic organisms. In samples collected through the periodontal pocket, relevant microorganisms may be overshadowed by bystanders in the subgingival ora that do not necessarily participate in the periodontal abscess process. The microbiota responsible specically for the periodontal abscess process may therefore be difcult to identify. Sampling through a stula is also hampered by contamination of surface bacteria with little relationship to the abscess. In case of a stula, the problem might be reduced by antiseptically treating the orice of the stula and by collecting a separate sample from the orice and outer part of the stula canal to identify the species that might potentially constitute contaminants. Sampling from an endodontic abscess may be facilitated by taking the sample through the root canal. The tooth can readily be isolated with a rubber dam and thoroughly sterilized with high percentage hydrogen peroxide and iodine tincture and the sterility veried by a sample of the eld of operation (153). Another problem in sampling of dental abscesses is the risk of false-negative results. False-negative cultures may occur in sampling pus in the central

Microbiology of dental abscesses

Difculty in evaluating dental abscess microbiology
Dental abscesses contain 37 or even more bacterial species with a predominance of anaerobic organisms (130). The vast majority of species isolated from the dental abscess originate from the resident oral ora. Microbial specicity of dental abscesses is low, and the heterogeneity of the microbial composition is striking. However, certain organisms are more frequently recovered than others and might therefore play a determinative role in the infection process. Earlier studies on the microbiology of acute dental infections showed a predominance of streptococci and staphylococci (35, 130), probably mainly due to sample contamination and inadequate anaerobic culture techniques. Mo ller (153) emphasized the importance of proper sampling technique and anaerobic culture conditions in endodontic microbial examinations. Even though relatively recent studies (130) describe a predominance of facultative cocci, most studies on dental abscesses over the last 30 years have underscored the importance of anaerobic organisms (Table 2). As listed above, factors of importance in the evaluation of dental abscess microbiota include: O O O O O clinical diagnosis microbial sampling microbial transportation methods for microbiological evaluation interpretation of microbiological ndings.

210

Table 2. Microbial ndings in studies of dentoalveolar abscesses of mixed or non-specied origin that contained pus by aspiration
Total number of isolates and predominant species within each bacterial group Gram-positive anaerobic cocci 2 Peptostreptococcus spp. 26 19 Veillonella spp. 37 No data 3 Actinomyces spp. Lactobacillus spp. 12 Bacteroides spp. 4 Fusobacterium spp. 1 F. nucleatum 7 Gram-negative anaerobic cocci Gram-positive anaerobic rods Gram-negative anaerobic rods Facultatively anaerobic isolates 7 Streptococcus spp. 6 S. epidermidis

Study 17 (68)

Number of abscesses

Total number of isolates

Total number of anaerobes (%)

Sabiston & Gold (174)

25

Ingham et al. (95)

25

185

134 (72)

52 51 B. melaninogenicus 13 Streptococcus spp. 21 Fusobacterium spp. 10 S. aureus 2 S. albus 13 Neisseria spp. 6 Haemophilus spp. 6 49 B. melaninogenicus 15 B. oralis 4 B. pneumosintes 4 B. fragilis 3 B. capillosus 3 B. corrodens 3 B. ruminicola 3 Fusobacterium spp. 7 Campylobacter spp. 2 22 Streptococcus spp. 14 Pseudomonas spp. 3 Candida spp. 2

Chow et al. (24)

31

119

93 (78)

28 P . micros 8 P . anaerobius 6 P . intermedius 4

3 Veillonella spp.

13 Actinomyces spp. 4 Lactobacillus spp. 3 Eubacterium spp. 4

Bartlett & OKeefe (8)

20

124

91 (73)

25 Peptostreptococcus spp. 2 P . intermedius 5 P . anaerobius 4 P . micros 3 P . prevotii spp. 4 P . magnus 3 P . asaccharolyticus 2 P . morbillorum 2 39 P . intermedius 4 P . constellatus 7 P . morbillorum 4 P . anaerobius 3 P . micros 3 P . prevotii 4 4 V. parvula 3

3 Veillonella spp. 3

28 Actinomyces spp. 2 A. naeslundii 2 Propionibacterium spp. 4 Lactobacillus spp. 1 E. lentum 8 E. limnosum 2

25 Bacteroides spp. 18 B. melaninogenicus 9 B. corrodens 2

26 Streptococcus spp. 6 hemolytic streptococci 5 alpha-streptococci 13 E. corrodens 3

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

Kannagara et al. (101)

61

201

118 (59)

2 A. israelii 6 Actinomyces spp. 5 Eubacterium spp. 5

53 B. fragilis 18 B. capillosus 7 B. furcosus 4 B. corrodens 4 B. coagulans 4 Fusobacterium spp. 6

82 Streptococcus spp. 7 S. epidermidis 27 S. aureus 6 Enterococcus spp. 5 Neisseria spp. 4 Klebsiella spp. 4 Corynebacterium spp. 9

211

212
Total number of isolates and predominant species within each bacterial group Gram-positive anaerobic cocci 30 S. constellatus 7 S. intermedius 22 Peptostreptococcus spp. 2 P . micros 4 P . asaccharolyticus 6 P . magnus 7 P . prevotii 3 9 V. parvula 9 31 92 Actinomyces spp. 2 B. intermedius 3 Propionibacterium B. melaninogenicus 3 spp. 3 B. oralis 15 Lactobacillus spp. 6 B. ureolyticus 2 Bidobacterium spp. 2 B. distasonis 1 Eubacterium spp. 5 B. capillosus 2 E. lentum 5 B. uniformis 1 Clostridium spp. 2 Bacteroides spp. 27 Fusobacterium spp. 29 F. nucleatum 9 29 Lactobacillus spp. 7 Eubacterium spp. 5 E. lentum 13 Gram-negative anaerobic cocci Gram-positive anaerobic rods Gram-negative anaerobic rods Facultatively anaerobic isolates 25 S. milleri 9 Streptococcus spp. 7 S. faecalis 4 Haemophilus spp. 2 Total number of anaerobes (%) 178 (88) 157 (89) 35 S. intermedius 11 S. morbillorum 2 P . micros 15 9 V. parvula 9 85 20 Bacteroides spp. 15 S. milleri 15 B. melaninogenicus 15 S. mitior 3 B. ruminicola 14 B. corrodens 6 F. nucleatum 20 47 Streptococcus spp. 45 S. aureus 3 S. epidermidis 4 Enterobacter spp. 2 Acinetobacter spp. 2 115 (71) 23 Peptostreptococcus spp. 2 P . productus 4 P . anaerobius 2 P . magnus 6 P . asaccharolyticus 4 5 V. parvula 5 10 77 P . acnes 2 Bacteroides spp. 10 Lactobacillus spp. 2 B. intermedius 12 Bidobacterium spp. 2 B. melaninogenicus 10 Eubacterium 4 B. ruminicola 12 B. distasonis 2 B. capillosus 2 B. asaccharolyticus 4 F. nucleatum 3 Fusobacterium spp. 5 0 3 B. asaccharolyticus 2 5 (20) 1 2 19 S. albus 4 Streptococcus spp. 8 E. corrodens 3 B. catarrhalis 3 10 V. parvula 10 28 Lactobacillus spp. 7 E. lentum 11 Eubacterium spp. 7 96 B. asaccharolyticus 3 P . melaninogenica 15 P . oralis 5 P . ruminicola 17 B. ureolyticus 5 B. capillosus 2 F. nucleatum 26 22 S. milleri 18 Streptococcus spp. 4 174 (89) 40 Streptococcus spp. 8 S. constellatus 2 S. intermedius 10 S. morbillorum 2 P . micros 17

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Table 2. continued

Study

Number of abscesses

Total number of isolates

von Konow et al. (111)

57

203

von Konow & Nord (112)

55

177

Labriola et al. (124)

50

162

Cumming et al. (27)

10

25

Heimdahl et al. (88)

58

196

Table 2. continued
Total number of isolates and predominant species within each bacterial group Gram-positive anaerobic cocci 50 Peptostreptococcus spp. 14 Peptococcus spp. 32 S. intermedius 3 S. constellatus 1 58 S. constellatus 6 S. intermedius 16 P . micros 27 9 V. parvula 5 29 Actinomyces spp. 3 Lactobacillus spp. 6 Eubacterium spp. 19 3 Veillonella 3 9 Lactobacillus spp. 3 Actinomyces spp. 3 Gram-negative anaerobic cocci Gram-positive anaerobic rods Gram-negative anaerobic rods 68 B. oralis 20 B. gingivalis 14 P . melaninogenica 12 P . ruminicola 6 F. nucleatum 6 121 B. asaccharolyticus 4 B. corrodens 4 B. ruminicola 16 B. ureolyticus 5 Bacteroides spp. 47 F. nucleatum 18 Fusobacterium 24 No data B. forsythus 22% P . endodontalis 59% P . gingivalis 93% T. denticola 85% Facultatively anaerobic isolates 36 S. milleri 25 S. mitior 3 S. sanguis 3 H. parainuenzae 2 C. ochracea 1 E. corrodens 1 64 S. milleri 18 S. mitior 18 Streptococcus spp. 7 Staphylococcus spp. 8 Haemophilus spp. 5

Study 130 (78)

Number of abscesses

Total number of isolates

Total number of anaerobes (%)

Lewis et al. (128)

50

166

von Konow et al. (113)

59

284

220 (77)

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

Ashimoto et al. (4)

27

Polymerase chain reaction analysis for ve species

No data

No data

No data

E. corrodens 19%

213

214
Total number of isolates and predominant species within each bacterial group Gram-positive anaerobic cocci 12 7 Veillonella spp. 14 Lactobacillus spp. 6 6 Fusobacterium spp. 4 Gram-negative anaerobic cocci Gram-positive anaerobic rods Gram-negative anaerobic rods Facultatively anaerobic isolates 84 Streptococcus spp. 46 Enterococcus spp. 4 S. aureus 2 S. epidermidis 2 Neisseria spp. 7 Corynebacterium 14 Candida spp. 2 61 Streptococcus spp. 41 S. epidermidis 8 S. aureus 2 Lactobacillus spp. 6 35 24 B. melaninogenicus 11 Streptococcus spp. 21 B. asaccharolyticus 6 F. nucleatum 11 F. varium 2 25 B. asaccharolyticus 2 B. melaninogenicus 6 B. oralis 3 B. corrodens 3 Porphyromonas spp. 2 F. nucleatum 3 Fusobacterium spp. 2 3 A. viscosus 3 4 Lactobacillus spp. 2 9 B. intermedius 2 F. nucleatum 7 No data 25 Bacteroides spp. 6 B. melaninogenicus 3 B. ruminicola 2 B. oralis 3 B. corrodens 3 F. nucleatum 6 3 V. parvula 3 9 Actinomyces spp. 3 Propionibacterium spp. 2 Lactobacillus spp. 3 68 B. gingivalis 14 B. intermedius 5 B. melaninogenicus 12 B. oralis 20 B. ruminicola 6 F. nucleatum 6 6 Streptococcus spp. 3 S. salivarius 3 Total number of anaerobes (%) 39 (2) 138 (69) 44 P . micros 13 P . anaerobius 9 S. intermedius 5 S. morbillorum 5 19 S. intermedius 4 P . anaerobius 6 P . prevotii 5 P . magnus 4 17 P . constellatus 3 P . intermedius 3 P . micros 4 Streptococcus spp. 5 4 V. parvula 4 3 V. alcalescens 3 11 E. lentum 5 10 V. parvula 6 V. alcalescens 4 30 5 Actinomyces spp. 10 B. intermedia 8 Lactobacillus spp. 8 B. melaninogenicus 2 Bidobacterium spp. 6 B. oralis 3 Eubacterium spp. 5 B. ruminicola 8 F. nucleatum 14 68 (74) 53 (90) 7 Actinomyces spp. 3 Lactobacillus spp. 3 15 (60) 3 P . anaerobius 2 P . micros 1 8 P . micros 5 0 10 S. mitis 6 S. faecalis 3 3 S. milleri 1 S. epidermidis 2 37 (93) 130 (77) 50 S. intermedius 3 Peptostreptococcus spp. 32 Peptococcus spp. 32 36 S. milleri 25 S. sanguis 3 Haemophilus spp. 2

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Table 3. Microbial ndings in dentoalveolar abscesses of endodontic origin and in aspirated pus

Study

Number of abscesses

Total number of isolates

Feldman & Larje (51)

64

123

Sabiston et al. (175)

58

199

Aderholt et al. (1)

50

92

Brook et al. (15)

12

59

Oguntebi et al. (164)

10

25

Williams et al. (215)

10

40

Lewis et al. (127)

50

168

Table 3. continued
Total number of isolates and predominant species within each bacterial group Gram-positive anaerobic cocci 17 P . productus 5 P . anaerobius 3 P . intermedius 3 P . parvulus 3 P . constellatus 2 18 Peptostreptococcus spp. 6 P . anaerobius 3 P . micros 6 P . prevotii 2 2 V. parvula 2 3 Eubacterium spp. 2 1 4 6 Bacteroides spp. 6 Gram-negative anaerobic cocci Gram-positive anaerobic rods Gram-negative anaerobic rods Facultatively anaerobic isolates 55 S. epidermidis 29 S. aureus 5 Streptococcus spp. (group A) 8 E. coli 9 23 Streptococcus spp. 14 S. milleri 3 S. faecalis 3 Haemophilus spp. 2

Study 28 (34)

Number of abscesses

Total number of isolates

Total number of anaerobes (%)

Sklavounos et al. (182)

40

83

Brook et al. (18)

39

78

55 (70)

32 B. oralis 4 B. gingivalis 7 B. melaninogenicus 3 B. intermedius 2 Bacteroides spp. 7 F. nucleatum 5 Fusobacterium spp. 4 24 P . intermedia 9 P . buccae 3 P . ureolytica 2 Prevotella spp. 4 F. nucleatum 5

Klecki et al. (118)

13

70

42 (60)

12 Peptostreptococcus spp. 12

28 Streptococcus spp. 10 S. epidermidis 4 S. aureus 2 Neisseria spp. 4 Corynebacterium spp. 4 E. corrodens 3 3 54 P . oris 9 P . intermedia 4 P . oralis 3 P . buccae 3 P . melaninogenica 3 Prevotella spp. 8 P . gingivalis 4 B. gracilis 3 F. nucleatum 3 Fusobacterium spp. 10 31 Streptococcus spp. 8 S. constellatus 8 S. intermedius 8 S. epidermidis 3

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

Sakamoto et al. (176)

23

112

81 (72)

17 Peptostreptococcus spp. 12 P . micros 3 G. morbillorum 2

7 Veillonella 7

215

216
Frequency (%) of isolated bacteria (mean % of total viable count) Gram-positive anaerobic cocci 44 (9.1) 11 (2.7) 20 (6.6) Gram-negative anaerobic rods Gram-positive anaerobic rods Gram-negative anaerobic isolates rods 100 (49.0) B. asaccharolyticus (10.4) B. intermedius (4.4) Fusobacterium spp. (5.9) Campylobacter spp. (11.5) 100 (39.0) B. gingivalis (19.5) B. intermedius (4.8) F. varium (5.1) F. nucleatum (6.6) 100 (37.4) P . gingivalis (22) P . intermedia (7.3) F. nucleatum (1.8) C. rectus (6.3) No data P . gingivalis 50 (13.6) P . intermedia 62.5 (8.5) P . melaninogenica 16.7 (15.6) B. forsythus 47.1 (3.6) F. nucleatum 70.8 (2.6) Campylobacter spp. 4.2 (0.7) Facultatively anaerobic isolates 100 (36.9) Facultative cocci (17.7) No data No data 70 (13.0) Actinomyces spp. (6.9) Propionibacterium spp. (3.1) Lactobacillus spp. (1.7) No data 45 (8.9) S. intermedius (5.6) No data No data 44 (3.8) Capnocytophaga spp. (3.8) No data P . micros 70.6 (9.3) No data No data No data A. actinomycetemcomitans 0 (0)

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Table 4. Microbial ndings in studies of periodontal abscesses

Study

Number of cases

Number of anaerobes

Newman & Sims (160)

100 (63.1)

Topoll et al. (203)

20

100 (59.5)

Hafstrm et al. (77)

20

No data

Herrera et al. (91)

24

No data

Table 5. Microbial ndings in studies of pericoronitis infections

Frequency of detection (mean % of positive samples) Gram-positive anaerobic cocci No data No data No data Gram-negative anaerobic cocci Gram-positive anaerobic rods Gram-negative anaerobic rods Facultatively anaerobic isolates

Study No data

Number of cases Fusobacterium spp. (80) No data Spirochetes (75) (Giemsa stain) 6 (40) B. gingivalis 0 B. intermedius 5 B. melaninogenicus 1 Selenomonas spp. 1 Fusobacterium spp. 2 147 P . gingivalis 0 P . intermedia 45 P . melaninogenica 22 B. gracilis 11 P . oralis 6 P . oris 11 P . buccalis 5 F. nucleatum 20 Campylobacter spp. 6 Selenomonas spp. 8 30 B. gracilis 4 P . gingivalis 5 Prevotella spp. 9 Fusobacterium spp. 3 Campylobacter spp. 3 43 A. odontolyticus 10 Eubacterium spp. 6 Lactobacillus spp. 7 A. israelii 5 83 P . intermedia/ nigrescens 11 P . melaninogenica 8 F. nucleatum 10 B. gracilis 8 F. necrophorum 4 C. rectus 5 P . buccae 6 P . denticola 6 P . gingivalis 1

Number of isolates

Number of anaerobes (%)

Nitzan et al. (162) No data 6.4 5 (5.3) Veillonella spp. 4 6 (11.3) A. odontolyticus 2 A. naeslundii 6 A. viscosus 6

82

Mixed microbial population

Mombelli et al. (151)

6 (Group C)

No data

6 (9.0) Capnocytophaga spp. 3 A. actinomycetemcomitans 1

Wade et al. (208) 20

361

302 (84)

62 P . micros 43 P . anaerobius 12

33 Veillonella spp. 29

60 A. naeslundii 12 Eubacterium spp. 25 A. viscosus 6 Bidobacterium spp. 5

59 S. mitis 19 S. sanguis 1 Streptococcus spp. 19 Corynebacterium spp. 2 Capnocytophaga spp. 6

Leung et al. (126)

5 (Group B)

74

54 (73)

5 P . micros 4

3 Veillonella spp. 3

16 Actinomyces spp. 10 Propionibacterium spp. 2 Eubacterium spp. 3

20 Streptococcus spp. 6 S. anginosus 4 Staphylococcus 2 Neisseria 1 Haemophilus 1 Capnocytophaga 6 62 Streptococcus 10 Neisseria spp. 5 Haemophilus spp. 5 S. milleri 8 S. mutans 5 Corynebacterium spp. 6 Capnocytophaga spp. 10

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

Rajasuo et al. (168)

11

210

148 (70)

16 P . micros 8 P . anaerobius 6

6 Veillonella spp. 6

217

n Dahle

B. gracilis elevated P . nigrescens elevated F. nucleatum elevated S. noxia elevated P . gingivalis not detected B. forsythus not detected

65 P . melaninogenica 17 P . buccalis 13 P . intermedia 6 P . oralis 4 F. nucleatum 1 Spirochetes 19

Gram-negative anaerobic rods

part of the abscess, where bacteria might have lost their viability or at least are inhibited. Methods employed to avoid false-negative and false-positive results are not sufciently described in many studies, and the microbiological ndings are therefore sometimes difcult to evaluate. Caution should also be exercised when sampling patients already on antibiotic administration, due to the bacteriostatic effect of antibiotics on parts of the ora. The abscess-producing bacterial species may not be detected unless a specic antibiotic inactivation procedure is enacted (153). Microbial transportation If microbial samples cannot be processed and cultured promptly, it is possible for routine analysis to delay culturing for 24 hours by using transport media such as VMGA III or RTF (34, 153, 189). Methods for microbiological evaluation Culture is considered the gold standard in microbiological evaluation of dental abscesses. Correctly employed with consideration to transportation, media selection, anaerobiosis and other atmosphere conditions, length of incubation etc., culture remains the best choice for unbiased searching for the predominant species in a sample with a polymicrobial mixture. However, few studies carry the microbial identication to species level but group them at genus level or into other groups based on limited phenotypic characteristics. Furthermore, taxonomic insufciency or reclassication may confuse identication. Microscope evaluation has been used for detection of noncultivable species, such as Treponema spp. (205, 206). Recent studies have used immunouorescence, DNA probe or PCR methods in microbial identication (10, 66, 191). It is plausible that molecular detection methods may reveal microorganisms that have not yet been identied in dental abscesses (43).

No difference compared with controls

Gram-positive anaerobic rods

Frequency of detection (mean % of positive samples)

Gram-negative anaerobic cocci

Gram-positive anaerobic cocci

No difference compared with controls

Number of anaerobes (%)

Number of isolates

DNA checkerboard hybridization

Number of cases

419

182 (43)

6 P . micros

10 Veillonella spp. 3

No difference compared with controls

101 R. dentocariosa 21 A. naeslundii 20 Bidobacterium spp. 15 A. israelii 14 Lactobacillus spp. 14

No difference compared with controls

237 S. milleri 29 S. sanguis 18 S. mutans 17 S. oralis 15 S. mucilaginosus 26

Facultatively anaerobic isolates

Table 5. continued

Microbiology of the dentoalveolar abscess (Table 2)

Anaerobic streptococci Anaerobic streptococci (Peptostreptococcus spp., Peptococcus spp. and Streptococcus spp.) belong to one of the most frequently isolated group of organisms in the dentoalveolar abscess. Among the

21

218

Study

PeltrocheLlacsa-huanga et al. (167)

Blakey et al. (13)

37

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

strictly anaerobic genera, Peptostreptococcus spp. predominate. Commonly isolated species are Peptostreptococcus anaerobius, Peptostreptococcus micros and Peptostreptococcus prevotii. Peptococcus species are less frequently reported, although Peptococcus magnus and Peptococcus asaccharolyticus have been identied in several studies. The microaerophilic streptococcal species are frequently recovered, but some streptococci are true anaerobes (Streptococcus intermedius and Streptococcus constellatus), whereas other strains of the Streptococcus milleri group (such as Streptococcus anginosus) are commonly placed among facultative species. Gemella (formerly Streptococcus) morbillorum, belonging to this microaerophilic group, has also been reported in dental abscesses. Gram-negative anaerobic cocci Gram-negative anaerobic cocci, often represented by Veillonella parvula, are reported in most studies although in a limited number of cases (Table 2). Gram-postive anaerobic rods Gram-positive anaerobic rods are commonly recovered from dental abscesses. Since several species are aero-tolerant and other species are strictly anaerobic, the classication of the isolates into anaerobes or facultative anaerobes can sometimes give rise to confusion. Actinomyces isolates are often not speciated. However, A. israelii, Actinomyces meyeri, Actinomyces odontolyticus, Actinomyces viscosus and Actinomyces naeslundii are among the species reported. Actinomyces spp. are important due to their ability to cause actinomycosis, attributed mostly to A. israelii, even if other species may also participate. Actinomyces species have been reported to persist in the periapical granuloma, especially in treatment-resistant cases (82, 181). Lactobacillus is often isolated from dental abscesses but, similarly to Actinomyces, it is seldom speciated. Lactobacillus spp. have been regarded as having low virulence (48), even if they are frequently present in endodontic lesions and dental abscesses. The frequent isolation in endodontic failures indicates a need for reconsidering the pathogenicity of oral lactobacilli (150). Lactobacillus plantarum, Lactobacillus casei, Lactobacillus acidophilus and Lactobacillus fermentum have been identied in oral infections. Oral Bidobacterium isolates belong mainly to the Bidobacterium brevis species. In the Eubacterium genus, isolates of Eubacterium alacto-

lyticus, Eubacterium lentum and Eubacterium yuri are most commonly recovered from the oral cavity (38). Propionibacterium acnes and Propionibacterium propionica (formerly A. propionica) are also reported by several studies of oral abscesses (Table 2). Clostridium species are very rare isolates from dental abscesses. Gram-negative anaerobic rods Gram-negative anaerobic rods are the most frequent isolates in dentoalveolar abscesses. Heimdahl et al. noted that, the more severe the abscesses, the more gram-negative anaerobes and S. milleri were recovered (88). However, the taxonomy is confusing, and literature older than 10 years refers to isolates as either Bacteroides or Fusobacterium species. The most commonly reported group according to modern taxonomy is Prevotella spp. Prevotella intermedia may best represent this group of organisms. Current differentiation into P . intermedia and Prevotella nigrescens should be considered. It is interesting to note that, whereas P . intermedia tended to be associated with severe periodontal infections, Prevotella nigrescens was more frequently isolated from endodontic infections (5). Prevotella melaninogenica is also frequently reported in dentoalveolar abscesses and, together with P . intermedia and Porphyromonas species, have placed the black-pigmented gram-negative rods (Bacteroides) in focus as major pathogens in dentoalveolar abscesses (217, 218). The importance of black-pigmented species has been further stressed by several authors relating these organisms to the presence of symptoms in acute infections. Sundqvist (192) suggested a relationship between black-pigmented Bacteroides and pain and sinus tract formation in acute endodontic infections, later supported by Griffee et al. (71) and Baumgartner et al. (10). These studies also revealed a higher frequency of saccharolytic species (Prevotella) than asaccharolytic species (Porphyromonas) in acute endodontic infections. On the other hand, Haapasalo et al. (73) stressed the presence of Porphyromonas species in symptomatic cases and isolated both P . gingivalis and Porphyromonas endodontalis from acute endodontic infections. It seems that P . endodontalis for some reason is selected for in root canal infections and, together with P . intermedia, is present in symptomatic teeth (217, 219). Other studies have also described a relationship between black-pigmented gram-negative species and symptoms but also underscored the importance of other bacterial species in acute infections. Non-pigmented Prevotel-

219

n Dahle

la, Peptostreptococcus, Peptococcus, Eubacterium and Fusobacterium species have been signicantly associated with endodontic symptoms (65, 83, 98, 223). In dentoalveolar abscesses, non-pigmented Prevotella species (such as Prevotella oralis, Prevotella ruminicola, Prevotella buccae, Prevotella oris, Prevotella bivius and Prevotella oulorum) are almost as common as the black-pigmented species (75). However, some reports on species occurrence are difcult to interpret due to changed taxonomy. Bacteroides ruminicola should probably have been classied as P . buccae, P . oris or Prevotella heparinolytica (98). Bacteroides ureolyticus may sometimes have been referred to as Bacteroides corrodens, whereas the related Bacteroides gracilis (now Campylobacter gracilis) is rarely reported, probably due to misidentication. Species sparsely reported are Dialister (Bacteroides) pneumosintes and Prevotella (Mitsuokella) dentalis (24, 74). In the Fusobacterium genus, isolates of Fusobacterium nucleatum and its subspecies predominate. In fact, F. nucleatum is one of the most frequent isolates and is reported in virtually all studies on dental abscesses (Table 1). Fusobacterium varium and Fusobacterium periodonticum as well as Fusobacterium necrophorum have also been described in dental abscesses, but only sparsely. Motile bacterial species such as Wolinella and Campylobacter, including Campylobacter rectus and C. gracilis (formerly B. gracilis) or Selenomonas spp. are sparsely reported in dentoalveolar abscesses. These motile species are present in both endodontic and periodontal infections (including periodontal abscesses) but may have been overlooked in many studies. Underestimation is very likely for Treponema species, which are not usually recovered in culture studies. However, if the microbiological analysis is completed with microscopic (including immunouorescence) or nucleic acid analysis, Treponema is commonly found (205). Dahle et al. (28) suggested that Treponema species constitutes 10% of the ora in endodontic abscesses. The taxonomic classication of Treponema is uncertain, and small as well as large spirochetes have been identied in endodontic infections (28, 29). Gram-positive facultative cocci Older literature reports on predominance of Streptococcus species in dentoalveolar abscesses, and these species may still be overestimated due to the difculty in avoiding contamination from the surface

ora and saliva. The microaerophilic streptococcal species are the organisms most frequently reported; the polysaccharide-producing species of the viridans group are seldom involved in dentoalveolar abscesses, and species such as Streptococcus mutans, Streptococcus sanguis, Streptococcus oralis and Streptococcus salivarius can often be suspected of constituting contaminants. The predominant abscess-producing streptococcal organisms belong to the S. milleri group, which has been considered synonymously to viridans until recently (178), but differs from other alpha-hemolytic streptococci by being microaerophilic. Some streptococcal species are hemolytic and are grouped in Lanceeld group F. b-Hemolytic S. milleri strains were detected in 22% of oral abscesses (178). Hemolytic streptococci of group A have not been identied in dental abscesses. Other hemolytic isolates may have been classied as enterococci (Lanceeld group D). The occurrence of Enterococcus species in endodontic infections can create a serious problem due to its resistance to antimicrobial agents. Enterococci are therefore often selected for by the endodontic treatment procedures. The presence of enterococci in dental abscesses and are-ups is, however, low, and this species is seldom involved in acute infections. Enterococci occur in high frequency in endodontic samples from teeth with therapy-resistant endodontic infection or root-lled teeth with periapical destruction (149, 197). Molander et al. (149) examined re-treated root-lled teeth and found enterococci in 50% of culture-positive samples. Other frequent isolates in that study were streptococci and lactobacilli (149). Streptococci and enterococci are not very prevalent in dental abscess material, which may explain why are-ups at root-lled teeth with apical periodontitis are rather uncommon despite the very high prevalence of these organisms in the oral cavity. Staphylococcus spp. are seldom reported in modern studies, which is in contrast to the literature from the pre-anaerobic era. The low prevalence of staphylococci does not mean that these organisms are irrelevant in dentoalveolar infections. Especially the presence of Staphylococcus aureus should be considered of potential pathoetiological importance. S. aureus is the most common cause of osteomyelitis in bones of other parts of the body; it may also occur in clinical infections of the jaws. Osteomyelitis occurs rarely in the maxilla due to the spongeous bone texture, which does not predispose for this condition, while mandibular osteomyelitis is a quite fre-

220

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

quent complication of oral infections. S. aureus may sporadically occur in endodontic lesions as well as in jaw fractures, especially in cases with extraoral communication, and might be a cause of mandibular osteomyelitis (209). Chow et al. (24) investigated 13 cases of suppurative osteomyelitis and found Bacteroides, Fusobacterium, Peptostreptococcus and Peptococcus species but no S. aureus. Gram-negative facultative cocci Gram-negative facultative cocci represented by Neisseria spp. are not usually reported in dental abscesses, and if occurring, contamination from the surface should be suspected (35). Gram-positive facultative rods Finding of gram-positive facultative rods other than those referred to as Actinomyces spp. or Lactobacillus spp. should be interpreted with caution. Corynebacterium spp. has been reported sparsely. Contamination at the time of sampling or in the laboratory should always be suspected if Bacillus spp. occur in dental abscess material (35). Gram-negative facultative rods Enteric rods including Escherichia coli, Enterobacter spp., Klebsiella spp. and Pseudomonas spp. are occasionally isolated from dentoalveolar abscesses (8, 51, 124) and may occur as monoinfections (169). The organisms are often resistant to mechanical endodontic treatment and may persist in root canal infections that do not respond to conventional therapy (72, 180). Haemophilus, Eikenella and Capnocytophaga spp. are infrequently found in dental abscesses (67, 68, 95, 111, 113, 128). Yeasts Yeasts have been isolated in 7% of culture-positive samples from infected root canals (210). Yeasts are usually isolated in mixed cultures, and the most common species is Candida albicans. The role of yeasts in endodontic infection is not clear. It is possible that local medicaments allow for the proliferation of yeasts, when other microorganisms are suppressed (211). Candida spp. are rarely isolated from samples of dental abscesses and are presented in case reports (142, 146). Approximately 20% of adult periodontitis patients

also harbor subgingival yeasts (36, 183). C. albicans is the most common species isolated (80). Its role in periodontitis progression is unclear; the organism has not been reported from periodontal abscesses or pericoronitis infections.

Specic microbiology of the periapical abscess (Table 3)

The most frequently detected bacterial species in periapical abscesses are microaerophilic streptococci of the S. milleri group (S. anginosus, S. constellatus and S. intermedius), anaerobic streptococci (P . anaerobius and P . micros), gram-positive anaerobic rods (Eubacterium spp., Actinomyces spp. and Propionibacterium spp.) and gram-negative anaerobic rods (Porphyromonas spp., Prevotella spp., Bacteroides spp., Campylobacter spp., Fusobacterium spp. and Treponema spp.). Although there is striking microbiological similarity between dental abscesses of various origins, some features are characteristic for endodontic abscesses. The rare isolation of P . endodontalis in oral infections other than those of endodontic origin is one important exception (217, 218). Furthermore, Actinobacillus actinomycetemcomitans is very rare in root canal infections and has not been reported in periapical abscesses (38). B. forsythus is not usually recovered from infected root canals unless specic anarobic methods are employed (66); however, the organism may have been overlooked in most abscess studies. The nonoral Bacteroides fragilis species has been reported in several studies, but there is reason to believe that these isolates were misclassied. B. fragilis rarely causes infections above the mediastinum (54). There are few reports on the specic bacteriology of dental abscesses with sinus tract formation, perhaps because these infections are of lower clinical priority, because they have passed the acute phase of infection or because of difculty in obtaining microbial samples without contaminating bacteria. The microbial composition of the sinus tract from a dentoalveolar abscess that drains through the periodontal pocket is impossible to distinguish from that of the subgingival microbiota. Haapasalo et al. (76) showed in a sinus tract infection sampled by aspiration that, although the acute phase of the infection had passed after antibiotic treatment, the periapical region still harbored metronidazole-resistant bacteria (microaerophilic streptococci, Propionibacterium acnes) and some other anaerobic species (P . intermedia and Peptostreptococcus spp.). Supposedly, the infection persisted within the periapical tissues

221

n Dahle

(the root canal lled with calcium hydroxide interappointment paste). Apical surgery was necessary to eliminate the infection. Mo ller (153) found that granulomas did not contain bacteria, but Tronstad et al. (204) showed the presence of bacteria in cases with sinus tracts, indicating that, in acute forms of the periapical lesion, bacteria can persist in the tissues outside the root canal. In an ultrastructural study, Nair (156) investigated 31 periapical lesions, of which ve were symptomatic and contained bacteria. Weiger et al. (212) performed microbiological sampling through the sinus tract of 12 cases and were able to isolate 6.3 strains per sample. Although in that study, the percentage of anaerobes was somewhat higher in the root canal than in the sinus tract, most species that were isolated from the canal were also recovered from the extraradicular sample, including Peptostreptococcus, Prevotella, Fusobacterium, Lactobacillus and microaerophilic streptococci (S. intermedius and G. morbillorum).

tive sample from the infected area and delineating the species involved in the disease process. However, it might be possible to use the noninfected contralateral site to exclude the microora normally present at the site. Leung et al. (126) found no signicant difference between the abscess ora and the ora of healthy third molar sites of control patients. Anaerobic species predominate and gram-negative anaerobic rods constitute the most frequent organisms of the pericoronitis microbiota (Table 5). While P . intermedia, P . melaninogenica, C. gracilis and F. nucleatum were common isolates in most studies, P . gingivalis and B. forsythus were sparsely found or not reported in pericoronitis abscess cases (13, 150, 168, 208). However, Leung et al. (126) isolated P . gingivalis and P . endodontalis from all ve pericoronitis lesions with symptoms but in none from asymptomatic lesions. P . intermedia was recovered in ve of six pericoronitis cases with acute pain and suppuration from the pericoronal pouch and constituted 29% of the cultivable ora (150).

Specic microbiology of the periodontal abscess (Table 4)

In dental abscesses of periodontal origin, P . gingivalis, B. forsythus, T. denticola and P . micros are the most prevalent species and are more commonly isolated from periodontal than from endodontic abscesses (90, 91). Especially P . gingivalis constitutes signicant proportions, ranging from 1022% of the cultivable ora in periodontal abscesses (77, 91, 160, 203). Sims & Newman (160), who performed a predominant culture study of periodontal abscesses and collected samples with a barbed broach from the apical part of the periodontal abscess, might have obtained more representative samples than other studies that used paper point sampling. All studies on periodontal abscesses, however, suffer from the apparent problem of mixing the abscess ora with that of the periodontal pocket. It is thus difcult to determine whether the reported similarity between the ora in periodontal abscesses (Table 4) and that associated with advanced periodontitis is a relevant nding or mostly a consequence of the sampling method used.

Microbiology of the periodontal-endodontic lesion

The microbiology of the combined periodontal-endodontic lesions reects the microbiota of the separate endodontic (125) and periodontal lesions. Accordingly, it might be impossible to obtain a sample that is representative of either the periodontal or the endodontic lesion. The literature contains no description of the periodontal-endodontic lesion microbiology. Due to great similarity between the microbiota of periodontal and endodontic lesions, the periodontal-endodontic lesion might show no unique microbiological prole.

Experimental abscess formation

Experimental infections with oral bacteria
A number of animal models have been developed to study odontogenic diseases. Most studies of oral bacteria aimed to illustrate the virulence of single bacterial species as well as of various bacterial combinations. It soon became clear that dental infections involving anaerobic bacteria were usually polymicrobial and originated from the oral resident ora. Dental abscesses thus comprise endogenous opportunistic infections (140). In the experimental abscess model in animals, it seems clear that abscess formation by anaerobic

Specic microbiology of pericoronitis (Table 5)

The microbiology of pericoronitis generally shows the same microbiological prole as other types of dental abscesses. It also shares the problem with other periodontal lesions in obtaining a representa-

222

Table 6. Experimental abscess formation by oral microorganisms

Study Guinea pigs Hamster Mice Guinea pigs Transmissible subcutaneous infections Subcutaneous 109 110 days 100% with K. pneumoniae with E. coli with A. viscosus Severe abscess Yes 108 59% 5 days No data Cheek pouch Subcutaneous 106107 105106 2 days 3 days 91% 75% No data No data Subcutaneous 10 10
7 8

Microbial combination 3 days 100% No data

Experimental animal Model system Animal death

Observation Size of inoculum period for (colony-forming abscess units/ml) formation

Frequency of pus or abscess formation % of inoculates

Other observations Heat-killed 0% Single 0% Diluted 1/10 0% Diluted 1/10 0% No infections if Bacteroides spp. was excluded Succinate produced stimulated growth Hemin supports infectivity

Takazoe & Nakamura (200)

B. melaninogenicus (B. oralis) Corynebacterium spp. Anaerobic

Sundqvist et al. (193) Guinea pigs

7 bacterial combinations from dental root canals

Mayrand & McBride (143) Guinea pigs Mice Rats Mice Subcutaneous 5109 3 days Subcutaneous Proportional to body weight 1 day

B. asaccharolyticus (oral)

Kastelein et al. (102)

B. asaccharolyticus (strain W83)

Yes Bacteria isolated from the cardiac blood

Other Bacteroides strains that W83 were less virulent Less severe abscesses seen in rats Only B. gingivalis 60% for W83, W50 strains produced 50% for 381, 382 abscesses Strains W83, W50 and 376 produced phlegmonous; the other strains caused gravity abscesses

van Steenbergen et al. (188)

26 strains of black-pigmented Bacteroides

Sundqvist et al. (194)

B. intermedius AB 13af, PIIak B. gingivalis W83, 381 B. endodontalis BNIIaf Mice Groin injection

Guinea pig

Subcutaneous Teon wound chambers

AB 13af109 PIIak 109 W83109 W83109 381109 BNIIaf 109 LD50 measurement

17 17 17 17 17 17

days days days days days days 7 days

100% 100% 100% 100% 0% 0% 100% when two anaerobes were combined

No No Yes No No No Yes, if anaerobes were combined with facultatives

W83 produced a uid with high proteolytic activity, degrading various types of serum proteins Virulent combinations with two anaerobes if one was B. asaccharolyticus F. varium F. nucleatum B. fragilis

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

Brook et al. (16)

22 strains of aerobic and anaerobic strains

223

224
Experimental animal Model system Animal death No data Mice Subcutaneous 10 10
7 8

n Dahle

Table 6. continued

Study 13 days 100%

Microbial combination

Observation Size of inoculum period for (colony-forming abscess units/ml) formation

Frequency of pus or abscess formation % of inoculates

Other observations Bacteroides spp. enhanced growth rate of facultatives such as group A streptococci E. coli S. aureus K. pneumoniae Hemin enhanced the mortality rate up to 100%

Brook (17)

42 combinations including B. asaccharolyticus B. intermedius B. melaninogenica B. fragilis B. vulgatus B. ovatus Mice Subcutaneous 51010 214 days Spreading infections with necrosis 6 strains highly infective 100% 30% 0100%

McKee et al. (144) Guinea pig Subcutaneous 41081011 No data

B. gingivalis W50

Grenier & Mayrand (70) Rabbit Subcutaneous steel net wound chamber 107 104 35 days abscess detected after 3 days 5 days

B. gingivalis

No data

Infectivity correlated with collagenolytic activity 0 0 Combinations with S. faecalis, B. oralis, A. bovis gave abscess in 30% S. milleri, P . anaerobius, B. oralis, F. necrophorum, B. oralis, F. nucleatum gave abscess in 60%

n Dahle et al. (32)

8-strain collection from a root canal infection B. oralis F. nucleatum F. necrophorum P . anaerobius P . acnes A. bovis S. milleri S. faecalis Rabbit Subcutaneous steel net wound chamber 1081010 14 days

n & Dahle Slots (33)

B. gingivalis B. intermedius B. fragilis A. actinomycetemcomitans Single or in combination

No Yes 100% No No No No

B. gingivalis 381 100% W83 100% B. fragilis 100% A. actinomycetemcomitans (3 strains) 0% B. gingivalis A. actinomycetemcomitans 100% B. intermedius A. actinomycetemcomitans 100% 7108 109 6109 1421 days

Immunization reduced infectivity of B. gingivalis 381 and W83 single or in combination

McKee et al. (145)

B. gingivalis W50 W50/BR1 W50/BE1 Mice

Mice

Subcutaneous

Spreading infections with necrosis 100% 20% 0% Subcutaneous 1010 314 days 10 strains invasive 6 strains caused 5 strains gave local depth 25100% abscess

Both mutants were less vurulent than parent strain

Neiders et al. (158)

B. gingivalis

Table 6. continued

Study Mice Subcutaneous 1081010 steel net wound chambers A7436 100% W83 60% W50 60% W50/BEI 75% ATCC33277 83% HG 405 100% ATCC33238 0% 576 100% 234 100% Yes, when sensitized with glucosamine Yes 80% Yes 40% Yes 40% No No No 26 days

Microbial combination

Experimental animal Model system Animal death

Observation Size of inoculum period for (colony-forming abscess units/ml) formation

Frequency of pus or abscess formation % of inoculates

Other observations All strains reduced systemic IgG response

Genco et al. (61)

P . gingivalis strains W83, W50 A7436, W50/BEI HG405, ATCC33277

Kesavalu et al. (108)

W. recta

Mice

Subcutaneous

1081011 13 days

Dexamethasone, hydrazine sulfate, dextran beads enhanced virulence immunization decreased lesion size Yes P . intermedia F. nucleatum isolated from cardiac blood P . anaerobius, V. parvula, F. nucleatum were pathogenic in pure culture; P . gingivalis and P . intermedia enhanced F. nucleatum pathogenicity

Baumgartner et al. (9)

P . intermedia P . gingivalis P . endodontalis P . asaccharolyticus P . anaerobius P . micros V. parvula

Mice

Subcutaneous

107108 21 days

P . gingivalis P . intermedia P . asaccharolyticus when combined with F. nucleatum

Genco et al. (62)

P . gingivalis A7436, W83 ATCC33277, HG405 and 381 Mice Subcutaneous 10101011

Mice

Subcutaneous 109 wound chambers

128 days

A7436 47% 90% W83 100% 90% abscess in abdomen

Immunization with A7436 or W83 and other P . gingivalis caused milder lesions and no death 13 days W50 51010 100% W50 21010 80% W50 11010 60% 100% 100% 100% Immunization with formalin killed cells or outer membrane fraction reduced lesion size and mortality rate

Kesavalu et al. (104)

P . gingivalis W50 ATCC33277 A7A128

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

Kesavalu et al. (105)

P . gingivalis W50 3079.03 NG4B19 BEI, SW5

Mice

Subcutaneous

1011

15 days

W50, 3079.03 100% 40%

W50 treated with protease inhibitor, or inhibitor decient mutants caused small lesions and no death

225

226
Experimental animal Model system Animal death Mice Subcutaneous 1091010 3 days Combination gave No data enhanced spreading of lesions Observation Size of inoculum period for (colony-forming abscess units/ml) formation Frequency of pus or abscess formation % of inoculates Rabbit Subcutaneous 105108 Teon wound chambers 14 days 33100% 0 Rabbit Subcutaneous 109 Teon wound chambers 14 days B. forsythus, P . gingivalis 100% or B. forsythus and F. nucleatum 1675% 100% 67% P . gingivalis and B. forsythus isolated from cardiac blood 0 Mice Subcutaneous 1091011 7 days Mice Subcutaneous 1071011 15 days 100% dependent on Yes challenge and dose of two bacterial species in combination 15 days P . gingivalis No data P . gingivalis T. denticola gave greater lesions than T. denticola alone No data 5 days 100% S. milleri strains less severe than F. nucleatum or combinations AF50 abscess formation or LD50 lethal dose No data AF50108.5 AF50 1010.2 AF50 107 AF50 106 Necrotic lesions Necrotic lesions Submandible 0 Lesions could be minimized with development of immunity Mice Subcutaneous 1010 Mice Subcutaneous Mice LD501010.6 1011 107 108.3 108.9 109.4

n Dahle

Table 6. continued

Study

Microbial combination

Other observations Infection with F. nucleatum 4 hours prior or 1 hour after P . gingivalis enhanced abscess development No difference in abscess formation between P . intermedia and P . nigrescens isolates

Feuille et al. (52)

P . gingivalis T22, NG4B19, 3079.03 F. nucleatum

Hafstrm & n (78) Dahle

P . intermedia (2) P . nigrescens (6) P . gingivalis S. mitis A. actinomycetemcomitans

Takemoto et al. (201)

B. forsythus P . gingivalis F. nucleatum

Kesavalu et al. (106)

T. T. T. T.

denticola socranskii pectivorum vincentii

No relation between protease production and virulence

Ebersole et al. (44)

P . gingivalis W50 F. nucleatum

Kesavalu et al. (107)

T. denticola P . gingivalis

Protease activity enhanced virulence

Nagashima et al. (155)

S. constellatus S. anginosus S. intermedius F. nucleatum

Strongest synergistic effect in a combination of S. constellatus and F. nucleatum

Kuriyama et al. (120)

S. constellatus P . micros F. nucleatum P . oralis P . gingivalis P . intermedia

LD50lethal dose for 50% of the animals. AF50abscess formation dose in 50% of the animals.

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

bacteria depends on synergism, often in combination with facultative bacteria (94, 165, 166, 214). Table 6 summarizes studies on the experimental abscess model using oral bacteria. Pioneering work by Rosebury & Macdonald (135, 136, 172) and Socransky & Gibbons (186) conrmed that oral indigenous bacteria were pathogenic and caused clinical infection in polymicrobial mixtures. Takazoe & Nakamura (200) found little difference in infectivity among guinea pigs, hamsters and mice inoculated subcutaneously with oral bacteria. Rats, however seem to develop less severe inammatory reactions (102). Sundqvist et al. (193) showed in experimental infections using microbial combinations from endodontic lesions that a species of Bacteroides (later identied as P . endodontalis) was essential to developing transferable abscesses. Similarly to nonoral anaerobic combinations, the synergistic interaction between oral anaerobic and facultative species may cause mortality among experimental animals (143). A series of experiments (102, 188) showed that certain strains of P . gingivalis were more virulent than others and produced phlegmonous abscesses and mortality among the experimental animals. Inoculates of 107 or more cells have been commonly used to obtain experimental abscesses. However, a mixture of eight different strains in inoculates of 104 cells was able to induce abscess formation (32, 37). Using virulent strains of P . gingivalis, Kesavalu and co-workers (44, 52, 103107) showed in subcutaneous experiments in mice that dexamethasone, hydrazine, galactosamine, protease inhibitors, protease activity and antibodies were important determinants of abscess development. P . intermedia, P . nigrescens, B. forsythus, Treponema spp. and C. rectus can also participate in abscess formation that may lead to the death of the experimental animal (77, 103, 106, 107, 201). In several studies, the bacterial strains used to induce abscess formation could be isolated from cardiac blood, emphasizing the capacity of oral bacteria to invade and spread throughout tissues. Recently, Kuriyama et al. (119 123) used a murine model to determine the virulence of anaerobes other than Porphyromonas, Prevotella and Bacteroides spp. S. constellatus, P . micros and F. nucleatum were lethal to mice when injected subcutaneously in various combinations.

Experimental endodontic infections

The dental root canal and the pulp chamber can be used as an experimental model of infection to determine the patho-etiology of endodontic lesions and

abscesses in or close to bony tissues (Table 7). The model can also be used for endodontic treatment studies (137). However, the abscess formation in the root canal model seems to be relatively mild, and chronic apical periodontitis usually occurs only after experiments at durations of months or years (48). The difference in pathological characteristics between endodontic infections and subcutaneous injection or wound chamber experimental infections may be due to the need for relatively few inoculating cells (infection dose) or due to the minute contact area in the apical region of the tooth between the root canal infection and the surrounding periapical tissues. Rodents have been used, however, for a random exposure of dental pulps to the oral ora to evaluate the capacity of the oral ora to cause pathogenic changes, including abscess formation in the periapical tissues (100, 117, 202). Fabricius and coworkers (49, 154) exposed traumatized dental pulps of monkeys to the oral ora. Their studies showed that a complex microora was associated with radiographic and/or histological pathogenic lesions in almost all cases and clinical abscesses or sinus tract formation in 23% of the study teeth (154). Their studies also demonstrated the pathogenic importance of anaerobes in endodontic infections. The rodent model cannot be used for endodontic infections with selected strains inoculated into the pulp chamber because of difculty in avoiding contamination due to the small tooth size; dog and monkey models do not experience similar contamination problems. However, dogs are less relevant due to a quite different and complex anatomical architecture in the apical part of the root canal causing very little contact between the main canal and the periapical tissues and thus a low frequency of periapical reac n, unpublished observations). Monkeys tions (Dahle constitute excellent models due to anatomical and histological similarities with humans. Inoculating microorganisms into root canals of animals can be used to determine virulence and pathogenicity in this very specic endodontic model; however, the relevance of the ndings should be interpreted with caution (2, 173). By using monkeys, Fabricius and coworkers (30, 31, 50) evaluated the pathogenicity of various types of bacterial combinations and found that abscesses only developed in the presence of complex microora. Fabricius et al. (49) also noticed that abscesses with sinus tract were frequent after 90 days of inoculation but less frequent after longer periods, indicating that if abscesses drain through a sinus tract, they transform into a chronic phase with formation of granulation tissue.

227

228
Animal Rat Rat Rat Dog 50100 days No data Radiolucency observed in most roots 90% 100% Chronic inammation 2 days1 year No data Periapical destruction after 1 month Abscess formed Anachoretic effect observed 31 days No data 80% Abscesses in 70% 142 days Pulps were necrotic No data Abscess formed S. mutans recovered from blood Observation time Clinical observation Radiographic observation Histological observation Comments and conclusions Monkey 67 months 23% Predominant species: Streptococcus spp. Eubacterium spp. Bacteroides spp. Fusobacterium spp. No data 20% of total viable count for peptostreptococci in 2/16 gram-positive anaerobic rods 7/16 black-pigmented anaerobic rods 7/16 100% 92% No data All strains were reisolated; 90% of the ora were anaerobes 93% (immunized) 87% (nonimmunized) 86% 69% 25% 70% Chronic inammation but no abscess detected No abscess detected Monkey 90 days 190 days 1060 days 7 abscesses 4 abscesses 1 abscesses Monkey 6 months No abscess found Monkey 69 months No abscess found Monkey 69 months No abscess found Rat 715 days Periapical lesions 100% at day 15 No data No data Anaerobes 24% S. oralis B. pneumosintes B. ureolyticus

n Dahle

Table 7. Experimental infections in animals using the dental root canal as a model

Study

Microbial combination

Kakehashi et al. (106)

Oral ora

Rosengren et al. (173)

S. mutans

Tagger & Massler Oral ora (198)

Allard et al. (2)

S. aureus S. sanguis P . aeruginosa B. fragilis

Mller et al. (154)

Oral ora

Fabricius et al. (49)

Oral ora

Fabricius et al. (50)

8-strain collection form an infected root canal

n et al. Dahle (30)

S. faecalis A. bovis B. oralis

n et al. Dahle (31)

S. faecalis A. bovis B. oralis F. necrophorum

Tani-Ishgii et al. (202)

Oral ora

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

Experimental periodontal abscess model

Experimental animal studies have been widely employed to support the etiological role of microorganisms in periodontal disease. Two main models have been used: (a) germ-free or specically infected rodents or (b) ligature-induced periodontal breakdown in dogs or monkeys. Certain microorganisms isolated from human periodontal pockets can initiate periodontal destruction in rodents (96, 97, 133, 222) or even invade gingival rat tissue (3). Placement of a ligature in subgingival sites of beagle dogs or monkeys results in plaque accumulation, gingival inammation, pocket formation and loss of periodontal attachment. The periodontitis-associated microbiota in animals shows a predominance of gram-negative anaerobes (114, 115, 224).

ment or bony pockets. Removal of necrotic pulpal tissue and drainage are performed by mechanical debridement of the root canal wall to the apical foramen. Apical surgery may sometimes be necessary to reach the apical part of the root for debridement. Especially in longstanding periapical lesions, the apical part of the cementum may become necrotic and have to be removed by apical surgery to obtain complete healing. Pericoronitis is treated by incision of the lesion and/or irrigation of the pericoronitis pouch with antiseptics.

Local antiseptics and antibiotics

Periodontal and endodontic lesions can be treated locally with antimicrobial agents used in concentrations that will ensure strong microbicidal activity (22, 153, 171). Root canal treatment has an apparent advantage, because antimicrobial agents can be applied in the canal for prolonged periods of time (22). On the other hand, antimicrobial agents in the root canal exert little or no effect periapically. In the acute phase, placement in a vehicle of local antimicrobial agents is not recommended because of potential interference with drainage. Periodontal abscesses can be successfully treated by a combination of drainage and systemic antibiotics (77). Herrera et al. (92), found a similar response using either azithromycin or amoxicillin and clavulanic acid. In the periodontal-endodontic lesions, the value of local antimicrobial agents has not been studied. However, it is recommended that the acute periodontal-endodontic lesion be drained and irrigated.

Treatment
The strategy in treatment of dentoalveolar abscesses includes a combination of mechanical treatment, surgery and systemic antibiotics. The purpose of mechanical treatment and surgical incision is to drain to reduce the infectious load; the purpose of systemic antibiotics is to prevent spreading and complications from the infection.

Mechanical treatment and surgery

The most important and immediate step in treating a dentoalveolar abscess, whether it is of endodontic, periodontal or other origin, is to mechanically incise the abscess and create drainage. Mechanical treatment of the root canal or periodontal pocket has a similar purpose: to debride and clean the root canal wall or the root surface of tissue or debris and to facilitate drainage. Irrigation with antiseptic solutions aims to remove debrided material and kill residual microorganisms. After the site of an acute infection is identied, surgical incision of the dental abscess should be performed and proper drainage established (63). In an endodontic infection, drainage can be established through the root canal. With the risk of bacteremia in mind, extraction of the affected tooth is an effective but intrusive means of creating drainage (139). After abscess resolution, endodontic or periodontal infections should continue to be treated by removing necrotic infected pulpal tissues or by subgingival scaling and root planing, especially in anatomically complicated situations such as furcation involve-

Systemic antibiotics
Systemic antibiotic treatment of dental abscesses aims at preventing bacterial spreading and serious complications. The concentration of antibiotics in the abscess is considerably lower than that in blood, and because of poor blood supply the concentration peaks later in the abscess than in blood. In addition to antibiotics, a dental abscess should always receive surgical and mechanical therapy (177, 179). Antimicrobial treatment is of secondary importance to surgical incision and drainage of abscesses (87). Antimicrobial agents are indicated when the patient shows signs of fever and general discomfort, indicating that the infectious process is at risk of spreading. Antimicrobial treatment in immunocompromised patients is especially important and should be considered for all dentoalveolar abscesses

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n Dahle

Table 8. The susceptibility rate (%) for gram-negative anaerobic species isolated from orofacial infections according to four studies (46, 119, 123, 163)

Veillonella spp.

(87). The choice of antibiotics should be based on sound pharmacological and microbiological principles and include the following three situations:
(46) n28

Porphyromonas spp.

O The emergency case. Penicillin is still considered to be the primary choice of antibiotics (63, 64, 69, 79, 122, 148). Since resistance to penicillin is increasing, metronidazole or amoxicillin/clavulanic acid may serve as alternative antibiotics. In case of penicillin allergy, metronidazole is the drug of choice. O The failing case in which a microbiological diagnosis has been made. Change of drug regimen should be based on the clinical situation, the microbiological prole and antibiotic susceptibility testing. O The failing case in which no microbiological diagnosis has been made. Change of antibiotic to one with a broader spectrum is recommended. Amoxicillin/clavulanic acid or clindamycin are alternative antibiotics. Clindamycin is recommended in penicillin allergy cases. The duration of antibiotic therapy has become steadily shorter over the years. Seven to 10 days of antibiotics is no longer recommended. Most dentists prescribe 5 days of penicillin or 3 days of metronidazole for acute orofacial infections (129). Martin et al. (139) concluded that the duration of anaerobic infections in most patients with dentoalveolar infections can be as low as 23 days provided that drainage has been established. The susceptibility of oral bacteria to antibiotics may be signicantly different from one country to another (221). The higher frequency of b-lactamaseproducing strains in the subgingival microora of adult periodontitis patients from Spain than from the Netherlands may be due to higher consumption of antibiotics in Spain (93). The susceptibility of oral bacteria to various antibiotics has been evaluated in numerous studies. The overall pattern is reviewed below (Tables 8, 9) and is related to the treatment of dentoalveolar abscesses. Antibiotic susceptibility studies pertaining to periodontal treatment are reviewed elsewhere (220), and some data on antibiotic susceptibility of root canal isolates have also been published previously (125, 207). Penicillin Penicillin has traditionally been regarded as the drug of choice in the treatment of dentoalveolar infections (47, 87). Heimdahl & Nord (87) found that 93%

89

71

100 100 100 100 100 100 100 100 100 100 100 100 Metronidazole 100

(163) n40

(123) n90

100*

029 88 94 94 2753 8187 8187 77100 Erythromycin

Fusobacterium spp.

(119) n57

89

98.5*

(46) n13

82.5

61

(123) n18

100*

92

100

(119) n35

100*

(46) n6

Non-pigmented Prevotella

7397*

100

83

(123) n47

(119) n56

100*

82

(46) n6

63

Black-pigmented Prevotella

1095

8197

(123) n59

8194

(119) n93

72

(46) n32

66

97

Clindamycin

Tetracycline

Ampicillin

100
Doxycycline. *Minocycline.

230

Antibiotic

Penicillin

100

100

93

100

9397

081

100

100

100

83

100

98.2

100

100

100

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

Table 9. Antibiotic susceptibility rate (%) among facultatively anaerobic and gram-positive anaerobic strains isolated from orofacial infections according to four studies (25, 46, 111, 119)
Facultatively anaerobic bacteria (111) n25 100 84 0

Antibiotics Penicillin Ampicillin Tetracycline Metronidazole Erythromycin Clindamycin

Viridans streptococci (119) n139 77 94100 055 054

Anaerobic bacteria (111) n178 98 92 70 84 94

Gram-positive Gram-positive anaerobic rods1 anaerobic rods2 (119) n105 (25) n32 (46) n29 (25) n22 86 100* 8089 100 94 50 78 100 42 86 57 100 100 18 91 95

Anaerobic streptococci Peptostreptococcus spp.

88 84

*Minocycline. Doxycyline. Tinidazole. 1 Propionibacterium acnes and Eubacterium lentum.2Anaerobic species from unspecied pediatric cases.

of 336 anaerobic isolates from orofacial infections were susceptible to 1.0 mg/ml of penicillin (Table 8). In the same study clindamycin was effective against 96% and nitroimidazoles against 70% of the isolates studied. In a prospective evaluation of penicillin versus clindamycin in the treatment of odontogenic infections, Gilmore et al. (64) found no failures in either antibiotic group. The resistance rates for anaerobic isolates were 8.9% for penicillin and 1.9% for clindamycin (64). In a study of 78 patients providing 143 facultative and 188 strict anaerobic bacterial isolates, 23% were resistant to penicillin and 5% resistant to amoxicillin/clavulanic acid (131). It has long been known that anaerobic microorganisms are not always sensitive to penicillin (55). Strains of P . intermedia, P . ruminicola, P . oralis and F. nucleatum may produce b-lactamase (55), and an increasing proportion of infections is due to b-lactamase-producing strains (85, 86, 131). Later studies (Table 8) have found a susceptibility rate to penicillin of 66% to 72% for pigmented Prevotella spp. (46, 119), 63% to 82% for non-pigmented Prevotella spp., 61% to 89% for Fusobacterium spp. and 83% to 100% for Porphyromonas isolates. Kuriyama et al. (123) conrmed that b-lactamase-producing Prevotella occur in dentoalveolar and pericoronitis infections. The highest incidence of b-lactamase-positive strains among anaerobic gram-negative rods was found for P . intermedia (22.5%), P . melaninogenica (71.4%), P . oralis (40.7%) and P . buccae (23.5%). Kuriyama et al. (123) also showed that b-lactamase-producing strains exhibited 100% susceptibility to clindamycin and metronidazole. Treatment with ampicillin/ amoxicillin drugs combined with clavulanic acid may be indicated for dental abscesses involving blactamase-producing bacteria (79, 92, 122, 131, 221).

Gram-positive anaerobes show variable susceptibility to penicillin. According to Eick et al. (46), 41% of the gram-positive bacterial isolates were pencillin resistant. Eighty-six percent of Peptostreptococcus spp. isolates were susceptible, while gram-positive anaerobic rods showed great diversity in penicillin susceptibility. In infections due to Actinomyces spp., P . acnes or Eubacterium, ampicillin or amoxicillin seem to be effective (25). Konow et al. (111) found that all viridans streptococci (S. milleri) tested were sensitive to penicillin. Erythromycin Erythromycin has been used as an alternative drug for treatment of patients allergic to penicillin (63). However, an increasing number of important anaerobes are resistant to erythromycin (55). The susceptibility rate is 87% for black-pigmented Prevotella and 53% for non-pigmented Prevotella (123). Only 27% of nonpigmented b-lactamase-positive Prevotella strains were susceptible to erythromycin (123). The susceptibility rate for Fusobacterium is 9% (123). Similarly, the effectiveness of erythromycin against viridans streptococci is poor (122). Other macrolides, such as azithromycin and spiramycin, have been used in treating dentoalveolar infections (134). Azithromycin is more effective than spiramycin and might serve as an alternative antibiotic against odontogenic infection. Azithromycin may also be effective in the treatment of periodontal abscesses (92). Metronidazole Metronidazole and other nitroimidazoles (ornidazole and tinidazole) are effective against strictly anaer-

231

n Dahle

obic bacterial strains, including b-lactamase-positive anaerobic gram-negative rods. As shown in Table 8, the susceptibility of pigmented and non-pigmented Prevotella, Porphyromonas spp. and Fusobacterium spp. to metronidazole is 100% (46). For peptostreptococci the susceptibility rate is 94%. Tinidazole has demonstrated a susceptibility rate of 70% among 178 anaerobic strains (11). The susceptibility rate for gram-positive anaerobic rods, including Actinomyces and Propionibacterium, varies from 18% to 57% (Table 9). Facultatively anaerobic strains, including viridans streptococci, are resistant to metronidazole. Ingham et al. (95) found that acute dental infections responded satisfactorily to both metronidazole and penicillin. Konow et al. (112) showed ornidazole to be more effective than penicillin in treating orofacial infections. Nitroimidazoles therefore constitute a valuable alternative to penicillin in the treatment of dentoalveolar infection. Their effectiveness against anaerobic bacteria, including b-lactamase-producing strains, may very well compensate for their ineffectiveness against facultative bacteria present in the dental abscess. Nitroimidazoles may be the best alternative to penicillin in the treatment of odontogenic infections, especially in the presence of b-lactamase-producing anaerobes or in patients allergic to penicillin (63, 112). Clindamycin Clindamycin shows excellent activity against anaerobic bacteria. Anaerobic streptococci, gram-positive rods and most gram-negative anaerobic rods show susceptibility rates of 93100% (46, 119, 123). Clindamycin penetrates oral tissues (21) and constitutes an excellent alternative to penicillin, especially in recalcitrant oral infections (69, 138). In a clinical trial, clindamycin and penicillin showed no signicant difference in the treatment of acute orofacial infections (113). The ability of clindamycin to reach efcient concentrations in vascularly impaired bone tissue makes it the primary choice in mandibular osteomyelitis (21, 113). Clindamycin is also effective against S. aureus. However, because of its adverse effects on the gastrointestinal microora (113), clindamycin may not be the primary drug of choice in dentoalveolar infections in general. Tetracyclines Tetracyclines, including doxycycline and minocycline, are effective against most gram-negative anaerobes, but the activity against gram-positive bac-

teria is low (46). Some doxycycline- and minocycline-resistant strains (Prevotella and Porphyromonas) have been identied (46, 119). Due to the afnity of tetracyclines for calcied tissue, they may be used as alternative antibiotics in dentoalveolar infections. Tetracycline was successfully used concomitantly with surgical incision in the treatment of periodontal abscesses (77). Fluoroquinolones Fluoroquinolones were introduced as a therapeutic choice in oral infections, including periodontitis involving A. actinomycetemcomitans, enteric rods or Pseudomonas (184, 220). The activity of quinolone antibiotics, such as ciprooxacin and ooxacin, against most anaerobes is limited, and quinolones used as monotherapies are poor choices in the treatment of dentoalveolar abscesses caused by a mixed anaerobic ora (84).

Antibiotics in various specic infections

Cloxacillin, dicloxacillin or ucloxacillin have been recommended for oral S. aureus infections (110). No methicillin-resistant S. aureus strains have so far been isolated from the oral cavity or dental abscesses, but susceptibility tests should be performed routinely (109, 110). Enterococcal infections, although occuring rarely, require special attention due to widespread resistance of enterococci to penicillin and other commonly used antibiotics. Because of varying susceptibility of both periodontal and endodontic isolates of enterococci, susceptibility testing is always recommended (39, 170). Until now, no vancomycin-resistant enterococci in oral infections have been reported. Susceptibility testing is also recommended for gram-negative enteric rods and Pseudomonas isolates. The drug of choice seems to be ciprooxacin (220).

Conclusions
The localization of the abscess and the possibility of obtaining drainage are essential considerations for successful treatment. Antibiotics should be prescribed in case of general symptoms or if complications can be suspected. Penicillin has traditionally been the drug of choice in the treatment of odontogenic abscesses. Metroni-

232

Microbiology and treatment of dental abscesses and periodontal-endodontic lesions

dazole may be used in case of penicillin allergy. Amoxicillin/clavulanic acid or metronidazole are useful in infections involving b-lactamase-producing strains. Proper mechanical debridement and local antiseptic irrigation should be carried out after resolution of the acute inammatory phase.

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