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RESEARCH REPORT |
1 Department of Oral and Maxillofacial Diseases, Mikkeli Central Hospital, Porrassalmenkatu 35-37, FIN-50100 Mikkeli, Finland;
2 Central Military Hospital, Helsinki, Finland;
3 National Public Health Institute, Helsinki, Finland; and
4 Institute of Dentistry, University of Helsinki, and Department of Oral and Maxillofacial Diseases, Helsinki University Central Hospital, Finland;
* corresponding author, ari.rajasuo{at}esshp.fi
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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KEY WORDS: bacteremia • tooth extraction • molar • third
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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Spontaneous bacteremia is a significantly greater cause of infective endocarditis than is bacteremia caused by invasive dental procedures (Lockhart and Durack, 1999; Roberts, 1999). After a routine tooth extraction, transient bacteremia was detected in all patients, whereas third-molar surgery caused bacteremia in only 55% (Heimdahl et al., 1990). Post-extraction bacteremia is mostly caused by anaerobes (71%), dominated by Eubacterium, Peptostreptococcus, Propionibacterium, and Lactobacillus species (Okabe et al., 1995). The clinical importance of anaerobic bacteremia, however, is not fully understood.
In previous studies investigating post-extraction bacteremia by modern microbiological methods, follow-up time has been up to only 10 min. We therefore studied Finnish soldiers in need of wisdom tooth surgery but otherwise in good health, to learn whether bacteria could still be detected in blood samples half an hour after tooth extraction. The study hypothesis was that 10 minutes’ follow-up is too short for the reliable assessment of the duration of transient bacteremia. Based on our observations on third-molar-associated bacteriology, we chose anaerobic species. We identified the actual source of the bacteremia by also sampling from the surgical area.
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MATERIALS & METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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The basic oral health status of these patients was good. Of the 16 subjects, four had dental caries in, on average, 2.3 teeth per subject. Each had a mean 6.4 ± 5.8 filled teeth. Periodontal status was assessed according to the WHO Community Index for Periodontal Treatment Need. The mean number of healthy gingival sextants was 4.4 per subject. Of the 16, ten had all sextants healthy except for three who had dental calculus in the mandibular incisor area only. None had sextants with deepened gingival pockets.
Status Findings Related to Mandibular Third Molars Surgically Extracted
The surgically extracted wisdom teeth were partly erupted, with the occlusal surfaces in all but two cases less than half visible; four had palpation tenderness in the retromolar tissue. Visible pus was detected in 38% of the pericoronal pockets. Mean probing depth of the pericoronal pockets was 8.1 ± 2.5 mm. Occlusal surfaces of all the teeth were at the mandibular occlusal plane. Inclination of most of the teeth (n = 13) was either vertical (angulation 85–95° in relation to the mandibular occlusal plane) or mildly disto-angular, with 3 out of 16 teeth mesio-angularly inclined.
Surgery and Bacterial Sampling
Gingival tissue at the sampling site was cleaned with swabs soaked in 70% ethanol. During sampling, contamination was carefully prevented by saliva suction and cotton swabs. A 0.8-mm-thick sterile endodontic paper-point was inserted into the depth of the pericoronal pocket and left in place for 30 sec (Dahlén et al., 1990; Rajasuo et al., 1996).
One mandibular third molar was surgically extracted from each subject by an experienced oral surgeon (K.P.). Surgery was carried out with the subject under local anesthesia, and the wound was closed with absorbable polyglycolic acid sutures. Average duration of the operation was 11 ± 5 min. After the buccal soft tissues were opened, 12 of the 16 third molars required bone relief, and 11 required sectioning, with surgical drills and saline rinsing. Immediately after the operation, a second endodontic paper-point was inserted into the extraction socket for 30 sec. Contamination by saliva was prevented as above.
Both samples were placed into a non-nutrient transport medium, VMGA III (viability preserving medium no. III, University of Gothenburg, Sweden; Dahlén et al., 1993) and transported to the Anaerobe Reference Laboratory of the National Public Health Institute, Helsinki, Finland. The samples were processed within 1 hr of collection. For blood sampling, a continuous-flow three-way 1.2-mm Viggo Venflon cannula (BOC Ohmeda Ab, Helsingborg, Sweden) was pre-operatively inserted into the ante-cubital vein of each subject, with 16 mL of blood drawn through the cannula into a syringe. The first sample was taken 1 min after the initial incision, and the second 1 min after extraction of the last piece of the tooth. Repeated samples were then taken 5, 10, 15, and 30 min after surgery.
Bacterial Culture and Identification
Paper-point samples in the VMGA III vials were dispersed by being blended in a Vortex mixer (Vortex-Genie model K-550-GE, Scientific Industries, Bohemia, NY, USA). Ten-µL aliquots of the sample and its 1:100 dilutions were spread evenly onto agar plates on a rotator. The following media were inoculated: blood and chocolate agars for the isolation of aerobes and capnophilic bacteria, Streptococcus mitis/Streptococcus salivarius agar for the selective isolation of Streptococcus mutans, and Sabouraud dextrose agar with antibiotics for the isolation of yeasts. The anaerobic media included: blood-, hemin-, and vitamin K1-supplemented Brucella agar for determination of total bacterial counts; kanamycin (75 µg/mL)/vancomycin (2 µg/mL) laked blood agar for isolation of Prevotella species, Porphyromonas species, and Bacteroides species; fastidious anaerobe agar with neomycin/vancomycin for isolation of Fusobacterium species; trypticase soy serum agar with bacitracin/vancomycin for the selective isolation of Actinobacillus actinomycetemcomitans and some agar-pitting Gram-negative rods and Capnocytophaga species; cadmium-fluoride-acriflavin-tellurite agar for isolation of Actinomyces species; phenyl-ethyl alcohol blood agar for isolation of Gram-positive cocci and other anaerobes; Lactobacillus-selective agar for isolation of lactobacilli; and Bacteroides bile-esculin agar with gentamycin for isolation of the Bacteroides fragilis group and Bilophila species. A 100-µL aliquot of VMGA medium was placed additionally into a thioglycollate medium for enrichment, incubated for 5 days, and subcultured on blood, chocolate, and Brucella agars (Holdeman et al., 1977; Slots, 1982; Moore et al., 1991; Summanen et al., 1992; Jousimies-Somer et al., 1995; Murray et al., 1995).
Aerobic cultures were incubated at 36°C in air containing 5% CO2 for 5 to 7 days. Anaerobic cultures were incubated in jars filled with a gas mixture (80% N2, 10% CO2, 10% H2) at 36°C for 7 to 14 days before the plates were discarded. The colonies were enumerated and isolated, and subcultures were identified according to established methods, including Gram-staining, determination of colonial morphology, aerotolerance testing, determination of sensitivity profiles to special potency antibiotic identification disks, determination of biochemical and fermentation reactions in pre-reduced anaerobically sterilized media, profiles of pre-formed enzyme reactivities, and gas liquid chromatography for profiles of short-chain fatty acids (Summanen et al., 1992; Jousimies-Somer et al., 1995).
Blood Cultures
Five-mL aliquots of ante-cubital venous blood samples were distributed between an aerobic and an anaerobic blood culture bottle (New Bactec 50; Becton Dickinson Caribe, Cayey, Puerto Rico, USA), and 8-mL aliquots were sent to an Isolator IO tube (Carter-Wallace, Inc., New York, NY, USA). The Isolator tubes were processed according to manufacturer’s instructions. After centrifugation of the tube, the pellet was quantitatively cultured on blood, chocolate, and supplemented Brucella agar plates and incubated in an atmosphere conducive to the isolation of aerobic, capnophilic, and anaerobic organisms, as described above. The Bactec bottles were incubated at 36°C for one day for the first subculture and thereafter for 5, 10, and 14 days for the final subculture on blood, chocolate, and Brucella agars as above. Isolates from the plates were enumerated, isolated, and identified by established methods (see above).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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shows the frequency of bacterial species in the blood circulation in relation to time of sampling. Half the subjects showed bacteremia immediately after the incision, whereas 44% were culture-positive at 1 and 10 min after extraction. Two subjects still had positive results 30 min after surgery.
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). Anaerobic Prevotella, Eubacterium, and Peptostreptococcus species predominated, whereas viridans-group streptococci and Streptococcus milleri group were the most common aerobic species. All but one bacteremia-positive subject (93%) had at least one species detected both in the blood and in the pericoronal pocket samples. Forty-three percent of the cases had at least one and the same species detected simultaneously in the extraction socket sample and in the blood. For details, see Table 2.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS & METHODSRESULTSDISCUSSIONREFERENCES |
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In the Heimdahl et al.(1990) study, the frequency of bacteremia was significantly higher in blood samples taken during tooth extraction than in those samples taken 10 min afterward. Okabe et al.(1995) showed bacteremia in 72% of the patients when blood samples were taken 2 min after tooth extraction. In their study, a high frequency of bacteremia was also associated with dental infections, with a high number of teeth being extracted, and with age (the elderly being more prone to bacteremia). Bacteremia was also prevalent if more than 50 mL of blood was lost during the operation and if its length exceeded 100 min (Okabe et al., 1995). Our subjects had good general and dental health, and our aim was not to compare oral findings with the frequency or magnitude of bacteremia. However, on average, in blood from ten of 16 gingivally healthy (mandibular molar region) subjects, 3.7 ± 2.9 bacterial species were detected, in comparison with only 3.0 ± 2.7 species from the other six subjects who had bleeding during probing of the gingival pockets. This difference, however, was not significant.
Bacteremia is also known to result from a variety of conservative dental procedures. For example, periodontal probing has caused bacteremia in 40% of patients diagnosed with untreated adult periodontitis, in contrast to 10% when the diagnosis was chronic gingivitis (Daly et al., 2001). Even the placement of a rubber dam or matrix band and wedge has caused bacteremia in 31% and 32% of patients, respectively (Roberts et al., 2000). Debelian et al.(1998) showed that when the teeth in question were asymptomatic and the diagnosis was apical periodontitis, bacteremia ranged from 31% to 54% of the cases during and after endodontal therapy. Local anesthetic injection has been shown (Roberts et al., 1998) to cause bacteremia in 16% of children examined when the technique used was normal buccal infiltration. Bacteremia frequency was as high as 97% when the anesthetic was injected directly into the periodontal ligament through the gingival crevice, but only 50% when the anesthetic was introduced through the attached gingiva. These examples show that dental treatments indeed lead to the spread of oral bacteria into the blood stream. This fact has been known for more than a century, but only now have modern microbiological techniques made possible the study of the details and extent of this phenomenon (McGowan and Shulman, 1998).
Earlier findings were that the majority of bacterial species found in blood samples after dental treatment are anaerobic (Heimdahl et al., 1990; Okabe et al., 1995). This was also the case in all our samples. In our patients, bacteremia was at its highest soon after extraction: 44% of the patients were positive 1 to 10 min after surgery. When studying the reproducibility of isolation in repeated blood samples, we showed that, of the aerobes, only S. intermedius was isolated from the same subject both from the sample 1 min and 5 min after surgery. Of the anaerobes, P. micros was isolated once from 5 min to 30 min post-operatively, and F. nucleatum, P. melaninogenica, and E. timidum from 1 min to 10 min after surgery. Veillonella species, P. anaerobius, and C. rectus were isolated repeatedly in the same subject during a shorter follow-up time (see Table 2
).
Because most of the species we detected were indeed anaerobic, we may also question whether current recommendations for antimicrobial prophylaxis should be modified for a wider spectrum against anaerobic species (Dajani et al., 1997). Gram-positive aerobic streptococci or staphylococci, however, seem to cause four out of five cases of infective endocarditis (Taubert and Dajani, 2001), making anaerobic bacteria an uncommon but important cause of endocarditis. Mortality rates in such cases range from 21 to 43% (Brook, 2002). Furthermore, prophylactic administration of antibiotics does not significantly lower the incidence or magnitude of bacteremia after tooth extraction (Hall et al., 1993, 1996a; Kaneko et al., 1995). The mechanism for prophylaxis against bacterial endocarditis may be the inhibition of bacterial attachment or of bacterial growth (Hall et al., 1993, 1996b).
Evidence is increasing that natural, spontaneous bacteremia causes infective endocarditis more often than does any surgical procedure in the oral cavity or respiratory tract, or in the esophageal, gastrointestinal, or genito-urinary regions (Roberts, 1999; Taubert and Dajani, 2001). In dentistry, greater emphasis should thus be placed on improving the oral health of risk patients in general to reduce spontaneous bacteremia—for example, due to loosening of teeth because of untreated adult periodontitis (Seymour et al., 2000).
We know little about the role and importance of anaerobic bacteremia in triggering adverse systemic reactions in the body. Infection and inflammation seem to play a key role in cardiovascular and other systemic diseases (Lorber, 1996); therefore, further study is needed on the importance of anaerobic bacteria of oral origin.
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ACKNOWLEDGMENTS |
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Received February 12, 2003; Last revision September 2, 2003; Accepted December 3, 2003
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