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Clinical Microbiology Reviews, January 2009, p. 46-64, Vol. 22, No. 1
0893-8512/09/$08.00+0     doi:10.1128/CMR.00028-08
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

Microbiology of Odontogenic Bacteremia: beyond Endocarditis

N. B. Parahitiyawa,1 L. J. Jin,2 W. K. Leung,2 W. C. Yam,3 and L. P. Samaranayake1*

Oral Bio-Sciences,1 Periodontology, Faculty of Dentistry,2 Department of Microbiology, Li Ka Shing Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China3

SUMMARY
INTRODUCTION
    Bacterial Entry into the Bloodstream
OBJECTIVES
    Search Strategy
HISTORICAL PERSPECTIVES
TRIGGERING FACTORS IN ODONTOGENIC BACTEREMIA
    Chewing
    Personal Oral Hygiene Measures
    Periodontal Procedures
    Tooth Extraction
    Orthodontic Procedures
    Endodontic Procedures
    Miscellaneous Oral Procedures
TEMPORAL NATURE OF ODONTOGENIC BACTEREMIA
SYSTEMIC OR END ORGAN INFECTIONS WITH ORAL BACTERIA
    CNS
    Skeletal Infections
    Respiratory Infections
    Septicemia
    Infections in Pregnancy
DIAGNOSING THE SOURCE OF BACTEREMIA
BACTERIAL DIVERSITY IN ODONTOGENIC BACTEREMIA
CONCLUDING REMARKS
REFERENCES

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SUMMARY
 
Summary: The human gingival niche is a unique microbial habitat. In this habitat, biofilm organisms exist in harmony, attached to either enamel or cemental surfaces of the tooth as well as to the crevicular epithelium, subjacent to a rich vascular plexus underneath. Due to this extraordinary anatomical juxtaposition, plaque biofilm bacteria have a ready portal of ingress into the systemic circulation in both health and disease. Yet the frequency, magnitude, and etiology of bacteremias due to oral origin and the consequent end organ infections are not clear and have not recently been evaluated. In this comprehensive review, we address the available literature on triggering events, incidence, and diversity of odontogenic bacteremias. The nature of the infective agents and end organ infections (other than endocarditis) is also described, with an emphasis on the challenge of establishing the link between odontogenic infections and related systemic, focal infections.


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INTRODUCTION
 
Recent advances in bacterial identification methods, particularly culture independent approaches such as 16S rRNA gene sequencing, have shown that oral niches are inhabited by more than 6 billion bacteria representing in excess of 700 species belonging to at least nine different phyla (1, 33, 36, 70, 96). Since some 30 to 40% of the bacteria normally residing in the human mouth remain to be identified, the 16S rRNA sequencing approach also provides a tool to arbitrarily estimate the diversity of these organisms (24). The bacterial flora of the mouth, like most other resident floras of the human body, such as those of the skin and the gut, exhibits commensalism, a survival mechanism that benefits the microbes without harming the host. Yet these largely innocuous commensal residents of the human body have the propensity to become pathogenic in the event of translocation to a different niche (58).

Oral commensals, particularly those residing in periodontal niches, commonly exist in the form of biofilm communities on either nonshedding surfaces, such as the teeth or prostheses, or shedding surfaces, such as the epithelial linings of gingival crevices or periodontal pockets. A feature that is unique to the oral bacterial biofilm, particularly the subgingival plaque biofilm, is its close proximity to a highly vascularized milieu (90). This environment is different from other sites where bacteria commonly reside in the human body. For example, the ingress of cutaneous flora into the circulation is prevented by the relatively thick and impermeable keratinized layers of the skin, while the mucosal flora of the gastrointestinal and genitourinary tracts is commandeered by the rich submucosal lymphatics, which keep microorganisms under constant check. Their covering epithelia are continuously shed at a quick rate, denying prolonged colonization by the bacterial flora. Although innate defense by polymorphonuclear neutrophils is highly developed at the dentogingival junction and backed up by a highly organized lymphatic system, the oral biofilms, if left undisturbed, can establish themselves permanently on nonshedding tooth surfaces subjacent to the dentogingival junction. Under these circumstances, any disruption of the natural integrity between the biofilm and the subgingival epithelium, which is at most about 10 cell layers thick, could lead to a bacteremic state (Fig. 1) (116).


Figure 1
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  		FIG. 1. Possible routes of bacterial entry from teeth into the systemic circulation. Pathway 1, entry via the root canal (RC) or from periapical lesions (PA) into the alveolar blood vessels (AW); pathway 2, entry from the periodontium, where bacteria in the gingival crevices (GC) translocate to the capillaries (C) in the gingival connective tissues, possibly through the junctional epithelium (JE). E, enamel; D, dentine; L, periodontal ligament; and AB, alveolar bone. (Panels i and ii are modified from reference 116 with permission from Elsevier. Panel iii is courtesy of Lu Qian [Oral Bio-Sciences, Faculty of Dentistry].) Note that the junctional epithelium was detached from the enamel due to processing for microscopy.

All too often, in common inflammatory conditions such as gingivitis and chronic periodontitis, which are precipitated by the buildup of plaque biofilms, the periodontal vasculature proliferates and dilates, providing an even greater surface area that facilitates the entry of microorganisms into the bloodstream. Often, these bacteremias are short-lived and transient, with the highest intensity limited to the first 30 min after a trigger episode, as discussed in the following sections (Fig. 2). On occasions, this may lead to seeding of organisms in different target organs, resulting in subclinical, acute, or chronic infections. Bacterial endocarditis is a well-known complication of such bacteremias of odontogenic origin and has been a matter of great concern for dentists, cardiologists, and microbiologists alike for many a decade. The literature and guidelines on the prevention and management of bacteremia of odontogenic origin have been under constant review, particularly with regard to prophylactic antibiotics and dental procedures, with differing opinions expressed on both sides of the Atlantic, particularly in recent months (51, 108, 143). Yet there are a number of other organs and body sites that may be affected by focal bacteremic spread from the oral cavity. Hence, the focus of this review is on issues that are unrelated to the connectivity between bacterial endocarditis and odontogenic bacteremias, with emphasis on other local and systemic morbidities due to such bacteremias.


Figure 2
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  		FIG. 2. Chart indicating the time course distribution of the incidence of odontogenic bacteremias from 50 studies reported in the literature. The lowest and highest incidences reported at a given time point are annotated in the chart, with the percentage shown in bold. (Note that at time point A the sampling was done during the intervention or immediately thereafter.)

Bacterial Entry into the Bloodstream

Based on the current evidence, it is likely that bacteria gain entry into the bloodstream from oral niches through a number of mechanisms and a variety of portals. First, and most commonly, when there is tissue trauma induced by procedures such as periodontal probing, scaling, instrumentation beyond the root apex, and tooth extractions, a breakage in capillaries and other small blood vessels that are located in the vicinity of the plaque biofilms may lead to spillage of bacteria into the systemic circulation (Fig. 1). Obviously, a higher microbial load would facilitate such dissemination, as it is known that individuals with poor oral hygiene are at a higher risk of developing bacteremias during oral manipulative procedures (48). Second, innate microbial factors may play a role in the latter phenomenon, as only a few species are detected in experimental bacteremias despite the multitude of diverse bacteria residing within the periodontal biofilm. Species that are commonly found in the bloodstream have virulence attributes that could be linked to vascular invasion (Table 1). Of particular note are attributes such as endothelial adhesion of Streptococcus spp., degradation of intercellular matrices by Porphyromonas gingivalis, and impedance of phagocytic activity by Aggregatibacter actinomycetemcomitans and Fusobacterium nucleatum.


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  		TABLE 1. Major bacterial species recovered from odontogenic bacteremias and putative virulence factors thought to facilitate their entry and survival in blood


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OBJECTIVES
 
The focus of this review is threefold. The first aim is to evaluate the evidence base on triggering mechanisms and underlying predisposing factors that lead to odontogenic bacteremias, the second aim is to determine the diversity and frequency of causative bacterial species in relation to various oral manipulative procedures, and the final aim is to assess the role of odontogenic bacteremia as a causative factor in systemic and end organ infections other than endocardial infections. We have particularly focused on systemic or end organ affections other than bacterial endocarditis, primarily because the pathogenesis of endocarditis secondary to odontogenic bacteremia has been reviewed extensively elsewhere (for a recent review, see reference 40).

Search Strategy

We searched the PubMed database for articles on bacteremia in human subjects, limiting the search to articles published in English. In order to elicit the events that lead to bacteremia of oral origin, the search query was worded "bacteremia," coupled with "procedure" and the Boolean operator "and." Bacterial diversity in the mouth was studied by analyzing the records cited in the database that had adopted the rRNA sequence-based phylogenetic approach, while diversity of oral bacteremias was appraised by combining the search for "bacterial genera" with the term "bacteremia." On all occasions, records were sorted according to relevance, and if it was deemed necessary, references cited in a given record were further analyzed. In total, 170 citations were derived for the search "bacteremia and procedure." By relevance, 6 citations in relation to physiological and personal hygiene activities, 13 regarding periodontal procedures, 19 regarding different modalities of tooth extractions, 5 regarding orthodontic appliances, 3 regarding endodontic procedures, and 5 regarding miscellaneous procedures were further appraised. In relation to systemic affections consequent to odontogenic bacteremia, 27 citations were evaluated based on relevance.


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HISTORICAL PERSPECTIVES
 
The link between dental procedures and resultant bacteremias has been under scrutiny for more than half a century. Some early work dates back to the 1930s, when it was found that the extent of gum disease has a confounding effect on the development of bacteremia following dental extractions. In one of the earliest reports, in 1939, Elliot (41) noted in an article to the Royal Society of Medicine in the United Kingdom that the incidence of postextraction bacteremia due to streptococci was increased when the condition of the periodontal health declined from minimally detectable gum disease to moderate and marked periodontitis. Furthermore, the intensity of the bacteremia was also observed to be highest among subjects with periodontal disease (41). In subsequent studies, the decline in incidence and the efficacy of antimicrobials, such as sulfanilamide, that were in use during the period in reducing bacteremias were evaluated, and the higher incidence of viridans group streptococcal bacteremias was reported (10). In 1954, Cobe evaluated the degree of dental and periodontal trauma that resulted in bacteremia in a cohort of 1,350 subjects assigned to five groups based on operative or surgical procedure. His findings in this landmark study indicated the highest incidence of bacteremia with periodontal cleaning (40%), followed by exodontia (tooth extraction) (35%), brushing (24%), and hard mastication (chewing hard candy) (17%) (25). The more "innovative" approach of other early investigators, who inoculated hapless subjects with bacteria and lytic enzymes to evaluate the degree of bacteremia, cannot even be contemplated in the present-day context of medical ethics (17, 25)! Nevertheless, these studies helped to highlight the significance and importance of the gingival crevice as a portal of bacterial entry into the bloodstream.


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TRIGGERING FACTORS IN ODONTOGENIC BACTEREMIA
 
Any disruption of the finely and harmoniously balanced bacterial biofilm within the gingival tissue niche leads to dissemination of organisms into the bloodstream (116). Not only oral procedures such as periodontal probing, scaling, root planing, and tooth extractions but also routine oral hygiene activities such as brushing, flossing, and other physiological phenomena, such as chewing, can be assumed to be disruptive to the delicate anatomical and functional barrier between the oral biofilm and the host tissues. For these reasons, it can be anticipated that the presence of inflammation in situations such as periodontitis, gingivitis, pulpal or root canal infections, or oral trauma by poorly fabricated appliances poses an increased risk of bacteremia, especially following mechanical manipulations of the oral cavity.

The literature reveals a vast number of studies on the factors triggering odontogenic bacteremia, varying from prospective controlled studies to clinical trials and case reports. As described in detail below, these fall essentially into bacteremias related to the following: chewing, personal oral hygiene measures such as toothbrushing, periodontal procedures such as scaling and root planing, tooth extractions, insertion of orthodontic appliances, endodontic procedures, and miscellaneous procedures such as sialography (Table 2).


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  		TABLE 2. Summary of clinical trials and controlled studies on odontogenic bacteremias from 1966 to 2007 (in chronological order)

Chewing

The normal physiological act of chewing has marked individual variations, making it one of the most difficult aspects to control in an experimental setting. Despite the theoretical possibility that in susceptible individuals chewing could give rise to a bacteremic state, the data available in the literature so far are inconclusive. In one of the earlier studies of odontogenic bacteremia, it was shown that 17% of the subjects who chewed hard candy (hard mastication) developed bacteremia, while none was detected with gentle mastication (25). Similar results were observed in a later study where postchewing bacteremia was detected in 20% of subjects who had evidence of periodontal inflammation, while none was detected in periodontally healthy subjects and subjects with gingivitis (i.e., superficial inflammation of the gums but not the deep periodontal tissues) (48). However, Murphy and coworkers (89) showed in a controlled study that chewing failed to seed detectable numbers of bacterial species into the bloodstream at different time intervals, irrespective of periodontal health status. Interestingly, in a parallel approach, Geerts et al. (49) noted significantly raised levels of bacterial endotoxins in subjects with chronic periodontitis, as assessed by the Limulus amoebocyte lysate assay. Whether this is a sequel of odontogenic bacteremia or endotoxemia from the inflamed periodontal niches remains to be determined.

Personal Oral Hygiene Measures

The effect of routine personal oral hygiene measures on the development of bacteremia is also difficult to evaluate. Therefore, procedures such as toothbrushing, flossing, and tooth picking and their relationship to bacteremia have been evaluated under controlled conditions, although in reality such exercises could be deemed rather artificial. Nevertheless, Forner and coworkers (48) found that toothbrushing did not cause significant bacteremia of oral origin in either healthy subjects or those with gingivitis, as no positive blood cultures were found in their controlled clinical trial of 60 subjects. Although the latter findings need to be confirmed by further work, these data indicate that mild gingivitis may not cause bacteremia during oral manipulation. Also, in another study of 30 healthy military recruits, it was shown that the true incidence of bacteremia was zero after brushing with soft-bristled toothbrushes. Of the 180 aerobic and anaerobic cultures that were analyzed, only 3 yielded detectable growth, and even these were identified as Propionibacterium acnes, a well-known skin contaminant of blood cultures (56). In early studies, detectable levels of bacteremia ranging from 17 to 44% were noted following toothbrushing in healthy subjects when brushing was performed by the investigator (25, 120). Thus, it appears that at least in adults with a healthy periodontium, brushing is not a significant factor contributing to systemic bacterial dissemination from the mouth.

On the other hand, subjects wearing orthodontic appliances demonstrated bacteremias of odontogenic origin following toothbrushing, with an incidence of 25% (119). For children, there is some evidence to indicate that bacteremias ensue upon toothbrushing performed under general anesthesia and nasotracheal intubation. Furthermore, the incidence was higher when electric sonicating toothbrushes rather than conventional tooth brushes were used (12). The latter finding on bacteremia under general anesthesia needs to be interpreted cautiously, as prolonged intubation in itself causes bacteremia and the magnitude of bacteremia in terms of incidence and diversity increases with the duration of the intubation (93).

With regard to dental flossing, a procedure that could mechanically disturb the periodontal plaque biofilms, bacteremia was associated with sporadic flossing, while no significant bacteremia was detected with daily flossing, even in subjects with gingivitis (19). However, due to the paucity of data and given the fact that flossing is an oral hygiene measure widely advocated for those with gingivitis and periodontitis, prospective randomized controlled studies with larger numbers of subjects are necessary to arrive at a definitive conclusion.

Periodontal Procedures

Various degrees of bacterial dissemination are associated with periodontal probing (27, 28), scaling (22, 68), root planing, and subgingival irrigation (5, 77, 106, 141). The presence of inflammation in the periodontal site is an important contributory factor to bacterial dissemination, as shown by the increased incidence of bacteremia in subjects with periodontitis compared to those with gingivitis (where the degree of inflammation is considered less severe) and those with healthy periodontium (48). For instance, the incidence of bacteremia varies from 5 to 75% for subjects with periodontitis, as opposed to 5 to 20% for subjects with gingivitis (27, 48). Despite the foregoing, the inflammation associated with gingivitis can be less than that with periodontitis, but not always. In very severe cases of gingivitis, the intensity and inflammation can be equal to or exceed that associated with some cases of periodontitis. In addition, there is no uniform agreement on a positive association between various indices used to measure the degree of periodontal inflammation, such as the presence of bleeding upon probing, gingival index, and plaque index, and systemic bacterial dissemination (Table 2).

Subgingival irrigation with antiseptics such as chlorhexidine prior to scaling and root planing is practiced by some dental surgeons. Waki and his group (141) found no significant decline in the incidence of bacteremia due to this supplementary procedure, nor was there a significant relationship with the quality of the irrigation fluid used, whether sterile water, clean water, or antiseptics (77, 106). However, there is some evidence that the bacteremic incidence does drop with continuous and regular rinsing with chlorhexidine or povidone-iodine irrigation of gingival sulci (5, 102).

In laboratory microbiological terms, although there is no significant influence on reducing the incidence of bacteremia, some workers found the intensity of bacteremia, measured by the number of CFU per milliliter, to be significantly lower when antiseptic mouth rinses were used prior to ultrasonic scaling (46). Taken together, the foregoing data imply that when periodontal procedures are performed on individuals with poor oral hygiene (as indicated by increased plaque indices), there is a higher risk of developing a bacteremia.

As for methods that reduce the incidence and intensity of bacteremia during periodontal manipulations, promising results have been shown with the use of a diode laser as an adjunct to ultrasonic scaling, and this could be attributed to the lesser degree of tissue trauma inflicted. In addition, lasers may also possess a degree of antibacterial activity (8). However, large-scale and well-controlled studies are necessary to confirm the latter finding.

Tooth Extraction

Tooth extraction, or exodontia, and associated tissue trauma cause bacteremia, and this is by far the most-studied oral surgical procedure evaluated to assess odontogenic bacteremias. According to a number of studies, the incidence of bacteremia ranges from 13 to 96%, depending on the evaluated time intervals as well as other experimental variables studied (Table 2). It has been shown that bacteremias can follow simple dental extractions as well as extractions of impacted teeth that entail minor surgical intervention (76, 103, 109, 110, 132, 137, 140). In such circumstances, the bacteremic incidence appears to be influenced positively by the presence of gingivitis, periodontitis, and other odontogenic infections, such as dentoalveolar abscesses, suggesting a direct relationship between an increased bacterial biofilm burden and bacteremia (15, 26, 128, 132). Other contributory factors for the phenomenon are the extent and duration of the surgical period and the magnitude of blood loss (92). When surgical incisions were made to facilitate the extraction of teeth, particularly impacted third molars, with subsequent insertion of sutures, nearly 10% of individuals had a bacteremia following the removal of sutures, and the incidence was not reduced by the use of preoperative antiseptic rinses (16).

Despite the fact that intubation is associated with bacteremia (93), no significant change in bacteremic incidence was observed when extractions were performed under general anesthesia (128). In addition, there is no apparent change in the incidence of bacteremia with increased numbers of teeth extracted or the use of mucoperiosteal elevators (103, 111, 133). Similarly, pre- and perioperative administration of antimicrobial agents, such as clindamycin, erythromycin, josamycin, and cefaclor, appears to have no significant effect in reducing the incidence of bacteremia (18, 53, 54). Similar results have been observed with the use of perioperative topical antibiotic applications (137).

Only a few procedures related to exodontia appear to reduce surgical bacteremias, and these include preoperative administration of antimicrobial agents, such as amoxicillin, cefuroxime, and moxifloxacin, that significantly reduce the incidence of such bacteremias (39, 140). Moreover, broad-spectrum degerming rinses, such as povidone-iodine, chloramine-T, and chlorhexidine, have been shown to reduce the incidence of bacteremia when administered as a rinse or irrigation prior to the extraction procedure or instrumentation, and povidone-iodine was shown to be the most potent in reducing the incidence (84, 121, 127, 144).

Orthodontic Procedures

Insertion of fixed orthodontic appliances involves manipulation of the oral tissues, particularly the teeth and the gingivae, and this may lead to systemic bacterial dissemination. However, the evidence to date shows that significant bacteremia is associated only with the insertion of separators that mechanically push teeth apart with significant force to create space for unerupted teeth (83). Other orthodontic procedures, such as taking alginate impressions, banding, debonding, removal of fixed appliances, and gold chain adjustments, appear to produce no significant bacteremia (42, 43, 83, 113).

Endodontic Procedures

It is highly likely that endodontic procedures that entail instrumentation of pulp chambers of either single or multiple root canals of teeth with reamers and broaches may introduce bacteria into the periapical vasculature of the teeth, with consequent bacteremic episodes. One important determinant of the onset of bacteremia in such situations appears to be the degree of tissue trauma caused by the instrumentation. Not surprisingly, therefore, the incidence of bacteremia was reportedly higher when the reamers reached beyond the confines of the root canal than in atraumatic endodontic procedures (11, 30, 31).

Miscellaneous Oral Procedures

Apart from the routine therapeutic and preventive dental procedures such as extractions and periodontal surgery discussed above, elective esthetic procedures, such as tooth polishing and whitening, which are now very popular and which are known to induce gingival epithelial abrasion and trauma, have not been shown to produce bacteremia (59). There is, however, a paucity of literature in this area and a need for large-scale controlled clinical trials.

Sialography, a procedure commonly carried out by specialists in oral medicine for imaging of the major salivary glands, entails injection of radio-opaque dyes into the ductal system of the glands. Bacteremias of streptococcal origin have been observed by some workers during different stages of such procedures (72). One reason for this could be the translocation of mucosal flora into the salivary duct system due to the pressure of the injecting dye.

Dentoalveolar abscesses are known to induce inflammation and vascular proliferation essentially at the periapical region of the tooth. Bacteremias have been reported when the purulent content of such lesions was drained by simple incisions. However, needle aspiration of pus prior to incision and drainage of the abscess was shown to reduce or totally eliminate the bacterial dissemination, possibly by reduction of the pressure inside the abscess before the surgical manipulation of the tissues (47).

To conclude, then, with reference to all of the dental treatment procedures discussed above, it appears that the following two major parameters dictate bacteremic episodes: first, and most importantly, the degree of inflammation present at the site, which is often directly related to the microbial load of the biofilm, as seen in generalized aggressive periodontitis (7, 29, 94); and second, the amount of tissue trauma that is inflicted. As for measures to eradicate odontogenic bacteremia, no single method (either topical or systemic antimicrobials or degerming antiseptic agents) has been effective, despite the fact that some measures may reduce the incidence significantly relative to others.


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TEMPORAL NATURE OF ODONTOGENIC BACTEREMIA
 
It is generally accepted that odontogenic bacteremias are transient in nature. Furthermore, it has been surmised that at least in healthy individuals, the bacteria are scavenged from the bloodstream relatively quickly by the innate and adaptive defense mechanisms (20, 100). Despite this general contention, some studies indicate that an episode of odontogenic bacteremia could last as long as 60 min (39, 110, 132), and most studies report the presence of bacterial species in blood for up to 30 min (Table 2; Fig. 2). This incidence profile can be observed in all forms of odontogenic bacteremias irrespective of the triggering factors, underlying predisposing conditions, or detection methods. A schematic illustration compiled from the data in the literature on the relationship between the incidence of bacteremia and the postprocedure time is given in Fig. 2. From the cumulative data, it can be deduced that the bacteremic incidence peaks within the first few minutes and then gradually declines after 10 to 20 min. Furthermore, depending on the threshold sensitivity of the detection method, the total reduction in the bacteremic load may vary from 10 to 90% at 30 s and from 2 to 20% at 60 min. It is important, however, that in spite of an initial steep fall, a few bacteria survive in the circulation after a bacteremic challenge from the oral cavity. The role of these persisters and how they survive host defenses need to be evaluated further, as they may well be the ones that evade the initial host immune burst and have the propensity to seed target organs and cause systemic and distant infections (34, 73).


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SYSTEMIC OR END ORGAN INFECTIONS WITH ORAL BACTERIA
 
The relationship between focal infection in the oral cavity, such as chronic periodontitis and gingivitis, and systemic diseases, including heart disease, diabetes, adverse pregnancy outcomes, and stroke, has aroused much concern lately (104). Apart from the seeding infection as a direct consequence of transient bacteremia, such oral-systemic interactions and outcomes could be due to other, indirect reasons, such as metastatic inflammation as a result of circulating macromolecular complexes and/or metastatic injury due to soluble toxins and bacterial lipopolysaccharide (50, 58, 74).

Although virtually any system or tissue can be affected by disseminated infection from the oral niches, endocarditis is the most well known and highly evaluated such affection. As stated earlier, literature on the latter subject is vast and extensive, and we make no attempt to review this aspect herein. Available data in the literature on other systemic and end organ infections due to oral origin are summarized in Table 3.


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  		TABLE 3. Summary table annotating the literature on systemic infections (apart from endocarditis) due to oral bacteria

CNS

The central nervous system (CNS), principally the brain and the spinal cord, is encased in an anatomical and functional covering. Thus, circulation to the brain is dependent upon a meshwork of blood vessels in juxtaposition with specialized brain cells known as the blood-brain barrier. Bacteria circulating in the bloodstream could ingress into the CNS through the blood-brain barrier. In addition, because of anatomical proximity, organisms could directly ascend to the brain or the upper part of the spinal cord from oral niches. For these reasons, it is apparent that the CNS could be a vulnerable relocation site for oral bacteria. In a review of cases of pyogenic infections in the brain and the spinal cord, Ewald and coworkers (44) pointed out that predominant oral bacterial species, such as Fusobacterium nucleatum, Veillonella, Streptococcus anginosus, Streptococcus oralis, and Actinomyces meyeri, could be detected in both the primary lesions and either cerebrospinal fluid or the blood. In addition, most subjects demonstrated one or more intraoral pathologies, such as periodontitis, gingivitis, caries, or periapical osteitis. Arguably, these lesions could serve as the primary infective focus for the dissemination and subsequent seeding of bacteria into an end organ site. For a majority of episodes, the absence of other detectable infective foci led researchers to conclude that the oral cavity, by default, is the primary source of infection (57, 61, 63, 67, 86, 88, 114, 126, 139). However, these studies, mainly case reports, suggest a relationship between pyogenic CNS infections and an oral origin of bacteria such as Abiotrophia spp., Dalister pneumosintes, Streptococcus intermedius, S. oralis, Streptococcus constellatus, Fusobacterium spp., F. nucleatum, Aggregatibacter actinomycetemcomitans, and Porphyromonas gingivalis (57, 61, 63, 67, 86, 88, 114, 126, 139). These organisms are all members of the oral resident flora, particularly that of the subgingival niche. In most reports, there is concomitant circumstantial evidence of poor oral hygiene, periodontitis, dental abscesses, mucositis with oral ulcerations, and the CNS lesions. Interestingly, in a few reports, phenotypic or genotypic homogeneity of the CNS and oral isolates was also traced (86, 139).

Skeletal Infections

As evident from the data presented in Table 3, odontogenic infections of the bones and joints are not as frequent as CNS infections. Yet there is clear evidence of oral bacteria causing multiple discitis and sacroiliitis, prosthetic hip joint infections, acute osteomyelitis, and paraspinal abscesses (Table 3). Apart from the presence of chronic oral infections such as periodontitis, recent invasive oral procedures, such as tooth extraction and ultrasonic scaling, have also been implicated as potential triggering factors for these infections. Common oral bacterial species such as Abiotrophia defectiva, Streptococcus intermedius, viridans group streptococci, Haemophilus aphrophilus, and Haemophilus paraphrophilus have all been implicated in such infections (37, 62, 75, 117, 142).

Respiratory Infections

Pulmonary infections consequential to odontogenic bacteremia have been described, although this is controversial because it can always be argued that bacteria could translocate into the lungs through direct anatomical routes. However, involvement of more than one lung, the multiplicity of lesions, and the nature of the organisms favor an oral-hematogenous spread. It has therefore been argued that such episodes are a result of spread from an oral niche due to the presence of poor oral hygiene or recent orogingival manipulation. Selenomonas spp., viridans group streptococci, Streptococcus intermedius, and Actinomyces odontolyticus have been implicated in acute respiratory distress syndrome, infection of the postpneumonectomy space, septic pulmonary embolism, and lung abscesses, respectively (13, 23, 38, 129). Interestingly, however, almost all subjects with such pulmonary infections were shown to have a compromised immune status due to advanced malignancies.

Septicemia

Similarly, there are many reports implicating odontogenic bacteremia as a causal factor for septicemia, particularly in individuals with hematological malignancies (35, 64, 97, 98, 105, 131, 138). In a recent study, even among otherwise healthy subjects, a majority of subjects with Leptotrichia buccalis septicemia were shown to have some form of intraoral infective focus (135). Yet in a vast majority of these cases, the connectivity between the oral cavity and the systemic focus is tenuous and, at best, circumstantial.

Infections in Pregnancy

Although a recent well-controlled randomized trial by Michalowicz and coworkers (87) found no association between periodontal indices and pregnancy outcomes, there is increasing evidence to indicate that adverse pregnancy outcomes, such as preterm birth and premature rupture of the membranes, are associated with poor maternal oral health, particularly chronic periodontitis (14, 69, 78, 79, 130). This could be due to a low level of chronic bacteremia as well as to chronic inflammation, which upregulates the levels of cytokines and other inflammatory modulators.

Furthermore, periodontopathic bacteria could also be detected in placentas of pre-eclamptic women (9). Despite the fact that most infections of the gravid uterus, fetus, newborn, or postpartum uterus originate from the reproductive tract, records indicate at least one instance where oral bacterial species with identical genetic homogeneity were recovered from both the in utero infection and the oral cavity (55). Given the well-known historical fact that the syphilitic spirochete Treponema pallidum crosses the fetoplacental barrier, resulting in neonatal syphilis and associated dental abnormalities (e.g., mulberry molars and Hutchinson's incisors), it is tempting to speculate that oral bacteria, including the spirochete Treponema microdentium and others, may affect the fetus, possibly through fetoplacental passage. Immunological studies have also revealed higher levels of periodontopathogen-specific immunoglobulin M in umbilical cord blood in babies born preterm (14). Whether this is a result of fetoplacental bacterial passage and dissemination or a generalized immune response has yet to be determined. Therefore, much more research is warranted to establish a link between odontogenic bacteremias and fetal and maternal health.


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DIAGNOSING THE SOURCE OF BACTEREMIA
 
The traditional gold standard for the detection of bacteremia is the use of in vitro cultures. For this purpose, liquid, solid, or biphasic culture media have been used with various incubation periods (124). In clinical microbiology laboratories, automated blood culture systems such as the Bactec system are now routinely used for this purpose (21). These automated systems enable the rapid recognition of bacterial growth by emitting fluorescence or a color change of the sample. Once growth is detected, aliquots are subcultured onto different agar media for further definitive identification of the offending organism(s). These automated methods are rapid, yet quantification of bacteremia is difficult, and for this purpose, the lysis filtration method is generally used. Briefly, lysis filtration involves treatment of a defined volume of blood with a medium that can digest the cellular contents and filtering through a membrane of defined pore size to capture the bacteria. The membrane is then inoculated in a growth medium to evaluate bacterial growth. The data yielded are quantitative and thus are more sensitive than those obtained with conventional and automated culture techniques (82, 145).

Once cultured, the bacteria are usually identified using phenotypic characteristics, such as the presence or absence of metabolic pathways, alterations in metabolic pathways, the utilization of substrates, and end product profiles. These tests are miniaturized and packaged into standardized, commercially available kits that allow comparison of the activity profile indices (e.g., API tests). One drawback of these identification methods is that they are exclusively dependent on the growth of the organism in either a liquid or solid culture medium. Given the fact that a large number of oral bacterial species are now known to be extremely slow growing or uncultivable, the value of standard culture methods and growth-dependent identification profiling has recently been questioned (3). As a partial solution to this problem, molecular probe-based identification methods are used and are gaining popularity (45, 99). Unfortunately, though, most of the latter methods are also dependent upon the successful isolation of the bacterial species in the primary culture. The latest approaches in detecting bloodstream infections, such as PCR-single-strand conformation polymorphism and direct amplification and sequencing of the 16S rRNA genes, which do not rely on in vitro culture, appear to be the solution to this impasse (101, 134). Nevertheless, such approaches have yet to be used and validated in prospective trials of experimental odontogenic bacteremias.

Whenever a bacterial species is isolated from a clinical blood sample, the next issue that needs to be addressed is its origin. A vast number of studies on odontogenic bacteremias and systemic infections of odontogenic origins are based on circumstantial evidence that relates the oral organism and those of the infective focus. These include factors such as poor oral hygiene in the affected individual, a history of dental treatment in the immediate past, or a traumatic event related to the oral cavity (Table 3). The veracity of these assumptions and the significance of the information can be ascertained only when the same phenotype is isolated, in particular when the isolates from the two niches are genotypically identical. Phenotypic similarities between the isolates from the two sites have been demonstrated by biochemical profiles, chromatographic evidence of cellular macromolecules, sodium dodecyl sulfate-polyacrylamide gel electrophoresis of cellular proteins, and antibiotic sensitivity patterns (11, 31, 103). However, only a few workers have attempted to determine the genetic homogeneity of the isolates, despite the greater robustness of this method. For the latter purpose, pulsed-field gel electrophoresis of genomic DNA and ribotyping have commonly been used, although more recently, the use of 16S rRNA gene sequence homogeneity and bioinformatics-based methods has shown promising results in assessing clonality (30, 55, 64, 65, 86, 118).

Also notable is the fact that molecular sequence-based approaches have higher sensitivities than do cultivation-based approaches. In addition, sequence-based detection methods based on universal 16S rRNA genes or other specific bacterial gene markers could be employed as markers of a treatment response when cultures fail to show bacterial growth. One drawback of these rapid and sensitive molecular diagnostic methods, however, is that they do not lend themselves to antimicrobial sensitivity testing, as the organism cannot be physically grown in culture. This information is important for clinicians, who rely on laboratory antimicrobial sensitivity tests to initiate or modify treatment (107). In clinical terms, the molecular typing methods to determine clonality should be considered adjuncts in situations where the clinical presentation is atypical or when there is no or a poor response to antimicrobial therapy.


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BACTERIAL DIVERSITY IN ODONTOGENIC BACTEREMIA
 
As opposed to the more than 700 bacterial species that inhabit the oral cavity, relatively fewer species have been isolated from blood cultures for odontogenic bacteremias. As shown in Table 4, there are at least eight bacterial taxonomic families that are represented in different oral niches. Of these, members of the family Firmicutes occupy the bulk of the microbiome in terms of the numbers of genera and bacterial species (1, 36, 70). Phylogenetic studies of the oral microbiome have shown that a large proportion of the oral bacteria comprise the genus Streptococcus. This holds true for the isolates in experimental odontogenic bacteremias as well (Table 2). In a number of controlled clinical trials, streptococci were the predominant organisms isolated, ranging from 40 to 65% of isolates (39, 48, 109, 110, 132, 140). Other genera of the Firmicutes family have been isolated from the bloodstream, to a lesser extent than streptococci, and include species of the Abiotrophia, Dialister, Selenomonas, and Solobacterium genera, in descending order. The Fusobacteria family is the second most commonly isolated bacterial family from the bloodstream and includes genera such as Leptotrichia and Fusobacteria, while other families, such as Actinobacteria, Synergistes, and Bacteroidetes, are far less common. Finally, there are no data in the literature describing the dissemination of either Spirochaetes or recently detected families, such as the Obsidian pool and TM7 bacteria, from the mouth in experimental odontogenic bacteremias or systemic infections secondary to dental treatment procedures. The last two families are not known to possess any cultivable species thus far.


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  		TABLE 4. Bacterial families and genera that inhabit oral nichesa


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CONCLUDING REMARKS
 
On appraising the literature on odontogenic bacteremia, it is clear that a number of oral manipulative procedures can give rise to bacteremias of oral origin. The highest incidence of bacteremia results from tooth extractions. Periodontal manipulations are also shown to produce a long-lasting (>30 min) bacteremia. This is probably a reflection of the bacterial load and tissue trauma or associated inflammation at these niches. Other oral procedures are not as significant, at least for individuals with healthy oral cavities. Routine oral hygiene measures such as brushing or flossing are unlikely to cause a significant degree of bacteremia, but sporadic cleaning after accumulation of a heavy plaque load should be considered a potential risk factor for a bacteremic state.

As evident from Tables 2 and 3, bacteria of potential oral origin detected in odontogenic bacteremias show some degree of diversity, but to a much lesser extent than that of the oral cavity. It is probable that this lack of diversity of blood-borne bacterial species is due to (i) their virulence attributes that facilitate entry into the bloodstream, (ii) the rapid clearance of the bacteria by host defenses, and (iii) the low threshold of the current detection methods used in clinical laboratories. However, as in the oral niche, the predominant bacterial genus isolated from the blood is Streptococcus. More than half of systemic affections are of streptococcal etiology, indicating that the predominance of streptococci in the oral niche could be a factor in determining their entry into the bloodstream (136).

A vast majority of bacteremias have been detected by cultivation and subsequent phenotypic characterization. Different forms of aerobic and anaerobic culture methods have been utilized. Comparison of different experimental bacteremia studies is difficult because there is no uniform agreement between timing of sampling, volume of blood drawn, and bacteriological identification methods. However, irrespective of the culture method, a larger volume of blood drawn does not necessarily concur with a higher incidence of bacteremia. Quantification of bacteria has often been done using lysis filtration of a defined volume of blood. Novel, more sensitive bacterial detection and identification methods, such as 16S rRNA gene sequencing, have not been used on a large scale. Strangely, though, the two studies that employed PCR of 16S rRNA genes showed lower incidences of bacteremia due to oral manipulations than that reported by culture techniques (68, 118). These differences could possibly be overcome by increasing the template volume as well as the sample size.

Most of the bacteremias considered odontogenic in the literature are based on circumstantial evidence. Hence, it is imperative that future workers study the genetic relatedness of organisms, rather than their phenotypes, in evaluating experimental odontogenic bacteremias.

Apart from bacterial endocarditis, there are a number of other systemic affections caused by bacteria residing in the oral cavity. However, most of the records on such infections are presented in the literature in the form of case reports or as a summary of a few cases. Since case reports are not the preferred mode of editorial boards due to a lack of originality, it is safe to assume that a large number of these go unreported.

It is safe to conclude, then, that odontogenic bacteremias are likely to cause systemic and end organ infections, but it is likely that most such infections are occult and dealt with swiftly by body defenses. The available data provide us only a glimpse of the reality, and much more work, using sophisticated sampling, detection, and analytical techniques, is required to draw firm conclusions. It is hoped that the availability of novel molecular and genomic tests will help to demystify the connection between odontogenic bacteremia and end organ infections in the not too distant future.


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FOOTNOTES
 
* Corresponding author. Mailing address: Oral Bio-Sciences, Faculty of Dentistry, The University of Hong Kong, Hong Kong SAR. Phone: (852) 2859 0342. Fax: (852) 2547 6257. E-mail: Lakshman{at}hkucc.hku.hk Back


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Clinical Microbiology Reviews, January 2009, p. 46-64, Vol. 22, No. 1
0893-8512/09/$08.00+0     doi:10.1128/CMR.00028-08
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