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Bacteremia Following Dental Extractions in Patients with and without Penicillin Prophylaxis
Bacteremia Following Dental Extractions inPatients with and without Penicillin Prophylaxis ALDONA L. BAL TCH, M.D. HOWARD L. PRESSMAN, D.D.S. MARK C. HAMMER, M.S. NANCY C. SUTPHEN, B.S. RA YMOND P. SMITH, M.D. MEHDI SHAYEGANI, Ph.D.
Abstract: This study describes the type, rate and magnitude of bacteremia in 128 patients undergoing dental extractions with and without penicillin prophylaxis. The most prolonged and highest rates of bacteremia occurred in patients undergoing extractions and alveoplasty while under general anesthesia following nasotracheal intubation. The most common aerobes in patients receiving no penicillin were streptococci. Bacteroides sp. were detected most often in patients receiving penicillin prophylaxis. The . overall bacteremia, streptococcal and .polymicrobial bacteremia rates were lowest for the patients receiving penicillin. Only two of 66 patients given penicillin prophylaxis had recoverable streptococci in blood cultures. Our study indicates that both intravenous and oral penicillin G prophylaxis for dental extractions decreased bacteremia rates significantly, including the recovery of streptococci. [Am J Med Sci 1982; 283(3):129-140.] KEY INDEXING TERMS
Bacteremia Dental extractions
Bacteremia is known to occur in asymptomatic human subjects but its significance as far as systemic disease is concerned is not fully understood. '12 In 1923, Lewis et al suggested that transient asymptomatic bacteremia may
Penicillin G Anesthesia
be the cause of endocarditis in patients with abnormal heart valves. 3 Subsequently, the relationships between oral procedures and bacteremia,4-9 and oral procedures and endo,o carditis have been described. -12 More recent-
From the InJectious Disease and Oral-MaxilloJacial Surgery Sections oj the VA Medical Celller. Alban), Medical College. and the Division oj Laboratories and Research. Nell' York State Departmelll oj Health. Alban.\'. Nell' York. This research lI'as supported by Medical Research Service oj the Veterans Administration. Reprint requests: A Idona L. Baltch. M. D.. Chief, InJectious Disease Section. Veterans Administration Medical Center. Albany. NY 12208. THE AMERICAN JOURNAL OF THE MEDICAL SCIENCES
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BACTEREMIA FOLLOWING DENTAL EXTRACTIONS
Iy, interest in bacteremia rates following other invasive procedures has increased. ))-20 It has been difficult to compare various studies concerned with bacteremia associated with oral procedures because of the differences in patient selection, blood culture sampling and the use of local or systemic antimicrobial agents. Prevention of endocarditis has continued to be of great concern in patients with prosthetic heart valves or in older patients with damaged heart valves. 21 - 28 Although endocarditis continues to be related primarily to streptococci originating from the oral cavity, more fastidious microorganisms including anaerobes have been described. 21 ,28-32 Data on the pathogenesis, pathologic findings and prevention of endocarditis in animals have indicated that certain antimicrobial agents, singly or in combination, and certain doses of these drugs might be recommended for prophylaxis in humans. 33 - 38 However, the effectiveness of the suggested prophylactic regimens remains to be tested in humans for the prevention of bacteremia as well as endocarditis. 38 Although two recent reviews indicate the need and support the use of prophylactic antimicrobial agents in the prevention of endocarditis, Petersdorf challenges the presently recommended prophylaxis and suggests a more conservative regimen. 39 - 41 The present study describes the type, rate and magnitude of bacteremia in patients undergoing dental extractions with and without penicillin prophylaxis. Materials and Methods Patient Selection This prospective study included 128 patients (all but two were males). No patients were febrile (rectal temperature not above 37° C), none received antimicrobial agents or had intravenous, urinary or other catheters for at least four weeks before the procedure. No patients were receiving prednisone or other immunosuppressive drugs. Sixty-two procedures (48.8%) were done on outpatients and 65 procedures (51.2%) were performed on inpatients. The patients were divided into four 130
groups: i) 33 received intravenous (IV) potassium penicillin G and local anesthesia; 2) 36 received oral phenoxymethyl penicillin (Penicillin V) and local anesthesia; 3) 29 received no penicillin and had the procedure done under local anesthesia; 4) 30 received no penicillin and had the procedure done following naso-endotracheal intubation and while under general anesthesia. The average age of patients in Group I was 46 years (range 2069), in Group 2 was 42 years (19-61), in Group 3 was 42 years (20-83), and in Group 4 was 35 years (21-61). Only patients with known valvular heart disease received aqueous penicilJin G 2 million units IV via heparin well before the procedure and every four hours thereafter for 72 hours. The penicillin was infused during a 30-40 minute period and the surgical procedure was started 15 minutes following the completion of the infusion. Penicillin V was administered 30 minutes before the procedure in doses of 0.5-1 gm to patients with soft tissue swelling of the face. Ten of the 36 patients in this group received additional Penicillin V 0.5-1 gm every six hours for 24 to 48 hours before the extractions because of the severity of inflammation of the soft tissues of the oral cavity, face and/or submandibular area with or without the presence of a periapical dental abscess. None of the patients receiving oral penicillin had valvular heart disease documented by history or physical examination. Table I depicts the number of patients in each of the four groups undergoing a single extraction (40 patients), 2-6 extractions (50 patients) and 7 or more extractions (38 patients). The average time required for extractions done under local anesthesia in patients receiving IV penicillin G was 36 minutes, and in patients receiving oral penicillin V or no penicillin the average time was 21 minutes. In contrast, an average of 105 minutes was required for patients undergoing dental extractions while under general anesthesia (no penicillin prophylaxis). All hospitalized patients were evaluated immediately after the procedure and every 4 hours for 24 hours for the development of MAY/JUNE 1982 VOLUME 283 NUMBER 3
BALTCH ET AL
TABLE I NUMBER OF PATIENTS WITH AND WITHOUT PENICILLIN PROPHYLAXIS WHILE UNDERGOING SINGLE OR MULTIPLE DENTAL EXTRACTIONS
Oralt
Penicillin None
None
Local
Local
Anesthesia Local
General
9
15 8
Intravenous* Number of teeth extracted 2-6
10
7+
14
14 18 4
Total
33
36
Total
2
40 50
6
14 14
29
30
128
38
*Aqueous penicillin G 2 million units IV 30 minutes beJore the procedure and every Jour hours Jor 72 hours'thereaJter. t Phenoxymethyl penicillin (Penicillin V) orally 0.5 - I gm 30-45 minutes beJore the procedure.
fever. In addition, patients receiving parenteral penicillin G were followed up for 12-36 months for the possible development of endocarditis. Dental Extraction Procedure All extractions were performed by one oral surgeon (H .P.). Procedures in patients requiring mUltiple dental extractions or full mouth exodontia were combined with alveoplasty (recontouring of alveolar bone for future dental prostheses). Patients requiring local anesthesia had regional anesthetic nerve blocks. Procedures done on patients while under general anesthesia (thiopental, nitrous oxide, halothan~) were performed in the operating room. These patients had nasoendotracheal intubation. Patients in all four groups also received a local gingival and mucosal anesthetic infiltration with 2% xylocaine combined with epinephrine (I: 100,000) to aid hemostasis. Blood Cultures Blood cultures were obtained by performing a separate venipuncture before, and 5 and 30 minutes following the completion of the oral procedure. Additional blood cultures were obtained from patients undergoing
general anesthesia just before and immediately following naso-endotracheal intubation (the latter sample was considered the pre-extraction sample). The skin was cleansed with providone-iodine using three scrubs. Eight milliliters of blood were placed into 100 ml trypticase soy broth (Difco), and 4 ml into 50 ml of thiol (Difco), thioglycollate (BBL) and either brucella broth or brain heart infusion (Scott) respectively. All media bottles had a partial vacuum with 5% CO 2 and contained 0.03% sodium polyanetholsulfonate. Blood cultures were incubated at 37°C, subcultured at 24-48 hours and again at 14 days. Subcultures were performed using fresh 5% horse blood agar plates supplemented with hemin, yeast extract and Vitamin K, and incubated at 37°C in 5% C02 for aerobic conditions and in Gas-Pakjars with disposable hydrogen-carbon dioxide generator envelopes with a palladium catalyst for anaerobic growth (BBL, Cockeysville, MD). Theaerobic plates were read in 24-48 hours, and the anaerobic growth was read at 72-96 hours. In addition, quantitative pour plates were done by placing one and one-half milliliters of blood into 15 ml of trypticase soy agar for aerobic culture and into Schaedler's agar for anaerobic culture in 79 patients. Colonies
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BACTEREMIA FOLLOWING DENTAL EXTRACTIONS
TABLE 2 PERCENT OF PATIENTS WITH POSITIVE BLOOD CULTURES AT 5 AND 30 MINUTES FOLLOWING DENTAL EXTRACTIONS AND ALVEOPLASTY
Time in minutes after dental extraction 5
Intravenous*
Oralt
Penicillin None
None
Local
Local
Anesthesia Local
Generalt
34.4
47.2
58.6
76.7
(17/36)
(17/29)
(23/30)
(11/32)** 30
12.1
13.9
26.7
51.7
( 4/33)
( 5/36)
( 8/29)
(15/29)
TablC' I. TablC' I. :1:34.5% (10/29) lIwe bacterelllic folloll'illg lIaso-t/'{/cheal intubatioll. **NulllbC'r (~r patiC'nt.l' with bact('fC'lIIia/llulllber of all patiellts ill the group. *SC'C'
t SC'C'
were counted at 48 hours in the aerobic plates and at 72-96 hours in the anaerobic plates. Following the isolation of individual bacterial strains, all identification and speciation was performed at the New York State Department of Health, Division of Laboratories and Research, Albany, New York. Identification of aerobes was done using conventional methods. Gram stain, colonial morphology, biochemical analyses and gasliquid chromatography were used for the identification of anaerobes.
Statistical Methods Statistical inferences were made using the Chi square test of association 42 for unpaired samples of categorical data and the McNemar test and the McNemar-like test for paired samples. 42 For small sample sizes the hypergeometric (unpaired samples) and the binomial (paired samples) distributions were used to calculate the exact probabilities in the statistical tests of the null hypotheses. 42 The one way analysis ofvariance 43 on the FreemanTukey modification 42 of the square root transformation of the number of different organisms cultured was used to test the null hypothesis of the equality of means. Selected 132
contrasts among the means and among the rates were also investigated. The level of significance was set at 0.05.
Results The bacteremia rates at 5 and 30 minutes following extractions and alveoplasty in patients with and without penicillin prophylaxis while under local or general anesthesia are shown in Table 2. None of the 128 patients were bacteremic before the start of the dental procedure. Highest rates of positive blood cultures were observed in patients under general anesthesia. One-third of these patients were bacteremic following nasotracheal intubation for general anesthesia. All patients bacteremic after intu bation were also bacteremic 5 minutes following dental extractions, a procedure which took an average of 105 minutes. Five of these 30 patients were also bacteremic at 30 min utes. Of the 19 patients with negative blood cultures after intubation, 6 were positive at both 5 and 30 minutes .. The 76.7% bacteremia rate at 5 minutes represents a significant increase while the 51.7% rate at 30 minutes is not significantly different from the rate following intubation. These findings suggest that in patients under general anesMAY/JUNE 1982 VOLUME 283 NUMBER 3
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TABLE 3 PERCENT OF PATIENTS WITH POSITIVE BLOOD CULTURES CONTAINING STREPTOCOCCI AT 5 AND 30 MINUTES AFTER DENTAL EXTRACTIONS AND ALVEOPLASTY
Penicillin
Anesthesia
Time (min) Arter Procedure
Percent with Streptococci in Bacteremic Patients
Percent with Streptococci in all Patients
Intravenous*
Local
5 30
9.1 (I/II)tt 0.0 (0/4)
3.1 (I/32)U 0.0 (0/32)
Oralt
Local
5 30
5.9 (1/17) 0.0 (0/5)
2.8 (1/36) 0.0 (0/36)
None
Local
5 30
76.5 (13/17) 25.0 (2/8)
44.8 (13/29) 6.9 (2/29)
None
General
5 30
73.9 (17/23)** 40.0 (6/15)
56.7 (l7/30lt 20.7 (6/29)
*See
Table I. t See Table I. tI3.8% (4/29) 0/ paliel1fs lI'ere bacleremic a/IeI' Ilaso-Iraclleal il1fllbatioll. **40.0 (4/10) 0/ paliel1fs lI'ere bacleremic a/IeI' lla.I'O-lraclleal il1fllbatioll. tt Paliel1fs bacleremic lI'illl sireptococci/ paliel1fS lI'illl bacleremia. ttPaliellls bacleremic lI'illl sireplococci/all patiellls.
thesia both procedures (intubation and extractions) influence the observed high rate of bacteremia. Among the four patient groups at 5 and 30 minutes respectively the bacteremia rates were significantly different. However, selected contrasts could not be shown to be statistically significant, most probably because of the size of the samples. For each group, the observed drop in the rate of bacteremia from 5 to 30 minutes was not attributable to chance. Of note was the observation that 85% of patients with negative blood cultures at 5 minutes were also negative at 30 minutes. Table 3 shows the percent of patients with positive blood cultures containing streptococci. Four of the 29 patients in the general anesthesia group had streptococcal bacteremia following naso-tracheal intubation. In this group, there was a significant increase in the recovery of streptococci at 5 minutes (56.7%) with a significant drop at 30 minutes (20.7%). The observed rates of bacteremia after intubation and at 30 minutes were similar. Lesser rates of streptococcal bacte-
remia were observed in patients whose extractions were performed while under local anesthesia without penicillin prophylaxis, 44.8% and 6.9% at 5 and 30 minutes respectively. The observed rates of bacteremia at 5 minutes in patients receiving no penicillin was significantly higher than in the patients receiving either type of penicillin prophylaxis. In fact, only one patient in each group of patients receiving penicillin had streptococcal bacteremia. Although the recovery rate of streptococci for the groups receiving no penicillin was lower at 30 than at 5 minutes, the rate at 30 minutes for the general anesthesia patients was significantly higher than that seen for the local anesthesia group" The percent of patients with polymicrobial bacteremia (2' to 15 strains recovered in different patients) are seen in Table 4. The highest rate at 5 minutes occurred in the general anesthesia group and represents a significant increase over the rate immediately following intubation and the rate at 30 minutes. The differences in polymicrobial bacteremia in the two groups of patients
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BACTEREMIA FOLLOWING DENTAL EXTRACTIONS
TABLE 4 PERCENT OF PATIENTS WITH POLYMICROBIAL BACTEREMIA AT 5 AND 30 MINUTES AFTER DENTAL EXTRACTION AND ALVEOPLASTY
Penicillin
Anesthesia
Time in Minutes after Dental Extraction
Percent Polymicrobial Bacteremia in Bacteremia Patients
Percent Polymicrobial Bacteremia in all Patients
Intravenous*
Local
S 30
36.4 (4/ 11m SO.O ( 2/4)
12.S ( 4/32)tt 6.1 ( 2/33)
Oralt
Local
5 30
64.7 (\ 1/17) 20.0 ( I/S)
30.6 (11/36) 2.8(1/36)
None
Local
S 30
82.4 (14/17) 7S.0 ( 6/8)
48.3 (14/29) 20.7 ( 6/29)
None
General
S 30
82.6 (19/23)t 26.7 ( 4/ IS)
63.3 (19/30)** 13.8 ( 4/29)
*See Table I. t See Table I. pO.O% (5/10) of bacteremic patiell/s lwei polymicrobial bacteremia q(ter lIa.m-tracheal ill/libatioll. **17.2% (5/29) of all patiell/s after illwbatioll hael polymicrobial bacteremia. tt Patiell/s with polymicrobial bacteremia/patiell/s with bacteremia. HPatiell/s with polymicrobial bacteremia/all patiell/s.
receiving no prophylaxis could not be shown to be statistically significant. There is a significantly lower rate of polymicrobial bacteremia at 5 and 30 minutes in patients receiving either type of penicillin prophylaxis than that seen in patients without penicillin. For all but the IV penicillin group the decrease in the polymicro bial bacteremia rate from 5 to 30 minutes is significant. The total number of isolates and the average number of isolates per positive blood culture recovered at 5 and 30 minutes for each ofthe four patient groups is seen in Table 5. At 5 minutes the average number of isolates recovered per positive blood culture varies significantly among the groups. The average number of recovered isolates for patients receiving no penicillin was significantly higher than that found in patients with penicillin prophylaxis. Following intubation the 10 bacteremic patients had 1.9 isolates per positive blood culture. A significant increase to 4.3 isolates per positive culture was seen in these patients 5 minutes after extractions. Of interest was a significantly lower average 134
isolate recovery rate in this group at 30 minutes when compared with the group of patients under local anesthesia without penicillin prophylaxis (1.8 vs. 4.0). Tables 6 and 7 present the aerobic/facultative and anaero bic isolates recovered in this study. Three hundred and four bacterial species (128 aerobic/facultative and 176 anaerobic) were recovered from patients following and none before the oral procedures. One half of the aerobic/facultative isolates were streptococci in patients receiving no penicillin prophylaxis. Of the II strains of streptococci recovered, Streptococcus sanguis and S. mitis were most frequent; no enterococci were isolated. Twenty-two other aero bic/ facultative bacterial species were recovered and only three bacillary forms could not be identified. Of the 37 anaerobic species, the most commonly detected anaerobes were in the Bacteroides group, followed by peptostreptococci, Propionibacterium, Veillonella and peptococcal groups. Only four Actinomyces and one clostridial species were detected. Twelve bacillary and 5 coccal forms could not MAY/JUNE 1982 VOLUME 283 NUMBER 3
BALTCH ET AL
TABLE 5 NUMBER OF ISOLATES RECOVERED AND AVERAGE NUMBER OF ISOLATES PER POSITIVE BLOOD CULTURE AT 5 AND 30 MINUTES AFTER DENTAL EXTRACTION AND ALVEOPLASTY AND FOLLOWING NASOTRACHEAL INTUBATION
Penicillin
Anesthesia
Time
Total Number of Isolates
IV·
Local
5 30
18 10
II
4
1.6 2.5
Number of Positive Cultures
Average Number of Isolates Per Positive Culture
pot
Local
5 30
42 6
17 5
2.5 1.2
None
Local
5 30
70 32
17 8
4.1 4.0
None
General
5 30
100 27
23 15
4.3 1.8
19
10
1.9
After Intubation
·See Table I. t See Table I.
be identified. The magnitude of bacteremia as measured with quantitative aero bic and anaerobic pour plates was low. Only 8.2% of the aerobic plates (1-2 colonies/ 1.5 ml blood) and 9.8% of the anaerobic plates (1-6 colonies/ 1.5 ml blood) were positive. The clinical follow-up of all 32 patients with valvular heart disease (oral surgery performed under local anesthesia following IV penicillin prophylaxis) indicated that none were febrile immediately following and for 24 hours after the oral procedure. In a 12-36 month followup none of these patients developed infectious complications.
Discussion In the present study bacteremia of the greatest magnitude occurred in patients undergoing mUltiple dental extractions while under general anesthesia. Immediately after endotracheal intubation one-third of the patients were bacteremic and one-half of those remained bacteremic at 5 and 30 minutes following extractions and alveoplasty. In addition, six of the I 9 patients not bacteremic
after intubation became bacteremic after extractions. The time for extractions including alveoplasty while under general anesthesia varied from one to two hours depending on the complexities of the intraoral surgery. Clearly, in this group of patients both intubation and intraoral surgery contributed to the rate of bacteremia. Patients having oral procedures done while under local anesthesia and no penicillin had a considerably shorter surgical time (ranging from 12 to 54 minutes) than patients under general anesthesia and lower rates of bacteremia. Although at 5 minutes streptococci were recovered in one half of the patients in both groups, at 30 minutes a significant drop in streptococcal bacteremia was 0 bserved (2 I % in the general anesthesia and 7% in the local anesthesia groups). The relationship of surgical trauma with resulting bacteremia suggested previously is demonstrated in our study.44,45 Ninety percent of our patients had dental extractions because of severe periodontitis, periapical abscess or impacted 3rd molars with or without pericoronitis. However, in
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BACTEREMIA FOLLOWING DENTAL EXTRACTIONS
TABLE 6 AEROBIC AND FACULTATIVE MICROORGANISMS ISOLATED FROM BACTEREMIA PATIENTS WITH AND WITHOUT PENICILLIN PROPHYLAXIS Penicillin Intravenous·
Oralt
None
None
Anesthesia Local Bacterial Isola tes Streptococcus sanguis S. mitis S. mutans S. salivarius S. agalactiae S. MG - intermedius S. F - Lancefield S. a hem }nonS. {3 hem} groupS. nonhem } able S. microaerophilic Actinomyces sp. A. naeslundii A. microaerophilic Staphylococcus epid. Lactobacillus sp. L. microaerophilic Micrococcus sp. Aerococcus viridans Corynebacterium sp. C. xerosis C. ovis Actinobacillus actinomycetem-comita ns Actinobacillus sp. Eikenella corrodens Catena bacterium sp. Pse udomonas maltophlia Gemella hemolysan s Vibrio extorquens Neisseria sicca Streptomyces sp. Gram + bacilli Gram-bacilli
No.
I
Local
%
No.
Local
%
3.1
I
3.1
I
3.1
I I I
3.1 3.1 3.1
I
2.1
I
2.1
I I
2.1 2. 1
3 I
6.4 2.1
I
I
General
No.
%
No.
%
6 3 I
6.4 3.2 1.1
15 6 2 I
11.0 4.4 1.5 0.1
2
2.1 2 3 4 I 2 4 1 I I 8 4 2 I I I I I
1.5 2.2 2.9 0.1 1.5 2.9 5.1 0.1 0.1 5.9 2.9 1.5 0.1 0.1 0.1 0.1 0.1
I
0.1
I
0.1
I
0.1
3 3 2 2 6
3.2 3.2 2.1 2.1 6.4
I 3 I I I I
1.1 3.2 1.1 1.1 1.1 1.1
2
2. 1
I
l.l
I
1.1
I
1.1
2. 1
3.1
Total aerobes Total anaerobes
1 20
25.9 14.0
9 38
19.0 80.9
41 53
43.9 56.9
11 65
51.1 41.4
Overall Total
21
100.0
41
100.0
94
100.0
136
100.0
• See Table I.
t See Tobit· I.
\36
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TABLE 7 ANAEROBIC MICROORGANISMS ISOLATED FROM BACTEREMIC PATIENTS WITH AND WITI-IOUT PENICILLIN PROPHYLAXIS Penicillin Intravenous*
Ora It
Local
Local
None
None
Local
General
Anesthesia Bacterial Isolates Bacteroides sp. B. corrodens B. melaninogenicus B. pneumonsintes B. nigrescens B. CDC Group FI B. CDC Group F2 Peptostreptococcus sp. P. micros P. productus P. anaerobius P. CDC Group 2 P. CDC Group 3 Peptococcus sp. P. variabilis P. prevotii P. intermedius P. morbillorum P. magnus Propionibacterium sp. P. acnes P. granulosum Fusobacterium sp. F. nucleatum Veillonella alcalescens V. parvula V. CDC Group 3 Eubacterium sp. F. lentum F. alactolyticum F. aerofaciens Actinomyces sp. A. israelii Lactobacillus sp. Clostridium bifermentans Selenomonas sputigena Campylobacter sputorum Gram + bacilli Gram + cocci Gram - bacilli Gram - cocci
No.
%
No.
%
No.
%
No.
%
3 2 2
Il.l 7.4 7.4
6 3 I I
12.8 6.4 2.1 2.1
3 5 4
3.2 5.3 4.3
4 I 3 I
2.9 0.7 2.2 0.7
I I I I I I I I
l.l l.l 1.1 1.1 l.l l.l l.l 1.1
I I 4
0.7 0.7 2.9
I
0.7
2
2.1
4 I 2
2.9 '0.7 1.5
I
1.1 2 I 2 8
1.5 0.7 1.5 5.9
I 3 6 5 I
0.7 2.2 4.4 3.7 0.7
3 I I I
2.2 0.7 0.7 0.7
2
1.5
2 3
1.5 2.2
I 2
I
3.7 7.4
3.7 11.1
I
3.7
I I I
4.3 4.3 2.1
2 I 2
4.3 2.1 4.3
3.7
I 3
I
2 2 I
I 4
2.1 8.5
I
2.1
I 3 2
2.1 6.4 4.3
I I 2 3 5 2
l.l 1.1 2.1 3.2 5.3 2.1
2 3
2.1 3.2
I
1.1
I I
1.1 l.l
I 3 I 3
1.1 3.2 1.1 3.2
3.7
3.7 3.7 3.7
I
2.1
I
2.1
I
2.1
I I
2.1 2.1
Total anaerobes Total aerobes
20 7
74.0 25.9
38 9
80.9 19.0
53 41
56.9 43.9
65 71
47.4 51.7
Overall Total
27
100.0
47
100.0
94
100.0
136
100.0
*See TaMe I. t See Table I.
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BACTEREMIA FOLLOWING DENTAL EXTRACTIONS
contrast to O'Keli et ai, who found bacteremia in 10.9% of patients before dental extractions, none of our patients were bacteremic before the oral procedure. II None of the microorganisms isolated in our study were considered contaminants. Although the overall number of bacterial strains recovered from blood cultures of patients receivingprophylacticadministration of penicillin was considerably smaller than the number found in. patients without penicillin prophylaxis (90 vs. 230), this decrease was more evident for the aerobes and facultative microbial strains than for the anaerobes. Only 16 compared with III aerobes and 58 compared with 118 anaerobes were recovered from patients receiving and not receiving penicillin, respectively. In patients given no penicillin, the most common aerobes and anaerobes were streptococci (23.4-29.3%) and Bacteroides sp. (7.9-17.2%), respectively. In contrast. 32-37% of the isolates were Bacteroides sp. and only 2.1-3 .7% were streptococci in patients receiving penicillin prophylaxis. The presence of anaero bes in post-extraction blood cultures was emphasized first by Khairat and subsequently by several other studies. 9 ,.16,.17 Although our data revealed fewer anaerobic isolates than that by Crawford et al. the difference may have been related to the different timing of blood sampling as well as selection of different blood culture media. 46 Penicillinase was not added to blood cultures in our study in order to avoid any possible contamination. Several earlier studies indicated that the use of penicillinase may increase the recovery of microorganisms from blood cultures of patients receiving penicillin prophylaxis.J,5,.1S,.I9 However, in these studies the doses of penicillin used in prophylaxis and the concentrations and times penicillinase was added to the blood cultures varied widely. Therefore. these variables did not allow for an adequate comparison of these studies with our data. In an attempt to decrease bacteremia following oral surgical procedures. prophylactic use of antimicrobial agents has been tried by a number of investigators. Only a minimal 138
and unsustained effect was observed with sulfonamides. 50 With penicillin the decrease in positive blood cultures varied from 9%51 to 42%8 depending on the penicillin preparation administered and method of blood culturing. With other antibiotics the decrease varied from 25 to 61 % . 48,52-54 Recently a small study comparing oral amoxycillin with Penicillin V indicated more sustained serum concentrations with amoxycillin and therefore fewer 49 positive blood cultures. I n the present study. the overall streptococcal and polymicrobial bacteremia rates were lowest for the groups receiving penicillin. There were only two patients with streptococci in blood cultures at 5 minutes and no patients with streptococcal bacteremia 30 minutes after the surgical procedures with intravenous or oral penicillin prophylaxis. In summary. our data indicate that bacteremia of greatest magnitude occurred in patients undergoing dental extractions while under general anesthesia after intubation. Intravenous or oral penicillin prophylaxis decreased the bacteremia rates significantly. including the recovery of streptococci. Acknowledgments The authors thank Anna May Lee. Robert Meidenbauer and George E. Hannett of the Division of Laboratories and Research. New York State Department of Health. for technical help. and Shirley Boyce of the Dental Service for assistance with patients. The secretarial assistance of Charlotte Manning and Judy Dean is greatly appreciated.
References I. Hockett RN. Loesche WJ. Sodeman TM: Bacteremia in asymptomalic human subjects. Arch Oral Bioi 22:91-98. 1977. 2. Wilson WR. Van Scoy RE. Washington JA: Incidence of bacteremia in adults without infection. J elill /'I'licrobiol 1:94-95. 1976. 3. Lewis T. Grant RT: Observations relating to subacute infective endocarditis. Hf'url 10:21-29. 1923. 4. Burket LW. Burn CG: Bacteremias following dental extraction: Demonstration of source of bacteria by means of nonpathogen (Serratia marcescens). J Df'1/I Rf'S 16:521-530.1937. 5. Elliott SD: Bacteremia and oral sepsis. Proc Roy Soc Mf'c/ 32:747-754. 1939.
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6. McEntegart MG, Porterfield JS: Bacteremia following dental extractions. Lancet 2:596-598, 1949. 7. Robinson L, Krause FW, Lazansky JP: Collective review: Bacteremias of dental origin. A review of the literature. Oral Surg 3:519-531, 1950. 8. Schirger A, Martin WJ, Royer RQ et al: Bacterial invasion of blood after oral surgical procedures. J Lab Clin Ml!d 55:376-380, 1960. 9. Khairat 0: The non-aerobes of post-extraction bacteremia. J Delli Res 45:1191-1197,1966. 10. Rushton MA : Subacute bacterial endocarditis following the extraction of teeth. Guy's Hasp Rep 80:39-44, 1930. II. O'Kell CC, Elliott SD: Bacteremias and oral sepsis. With special reference to the aetiology of subacute endocarditis. Lancet 2:869-872, 1935. 12. McGowan DA, Hardie J M: Production of bacterial endocarditis in prepared rabbits by oral manipulation. Br Delli J 137: 129-131, 1974. 13. Sullivan N M, Sutter VL, Carter WT et al: Bacteremia after genitourinary tract manipulation: Bacteriological aspects and evaluation of various blood culture systems. Appl Microbiol 23: 11011106, 1972. 14. Sullivan NM, Sutter VL, Mims MM et al: Clinical aspects of bacteremia after manipulation of the genitourinary tract. J In/ect Dis 127:49-55, 1973. 15. Baltch AL, Buhac I, Agrawal A et al: Bacteremia 'Ifter upper gastrointestinal endoscopy. Arch IllIern Med 137:594-597, 1977. 16. Shull HJ Jr, Greene BM, Allen SD et al: Bacteremia with upper gastrointestinal endoscopy. Anll III/ern Mecl83:212-214,1975. 17. Buchman E, Berglund EM: Bacteremia following sigmoidoscopy. Am Heart J 60:863-866, 1960. 18. McCloskey RV, Gold M, Waser E: Bacteremia after liver biopsy. Arch IllIern Med 132:213-215, 1973. 19. Berry FA Jr, Blankenbaker WL, Ball CG: A comparison of bacteremia occurring with nasotracheal and orotracheal intubation. Anesth Analg (Cleve) 52:873-876, 1973. 20. Kane RC, Cohen M H, Fossieck BE et al: Absence of bacteremia after fiberoptic bronchoscopy. Am Rev Respir Dis III: 102-104, 1975. 21. Kaye D: Infecting microorganisms. In Kaye D (ed): In/ectil'e Endocarditis. Baltimore, Univ Park Press, 1976, pp 43-54. 22. Killen DA, Collina HA, KoenigGA et al: Prosthetic cardiac valves and bacterial endocarditis. Ann Thorac Surg 9:238-247, 1970. 23. Slaughter L, Morris J E, Starr A: Prosthetic valvular endocarditis: A 12 year review. Circulation 47: 13191326, 1973. 24. Dismukes WE, Karchmer A W, Buckley MJ et al: Prosthetic valve endocarditis: Analysis of 38 cases. Circulation 48:365-377, 1973. 25. Sande MA, Johnson WD Jr, Hook EW et al: Sustained bacteremia in patients with prosthetic cardiac valves. N Ellgi J M ed 286: 1067-1070, 1972.
26. Wilson WR, Jaumin PM, Danielson GK et al: Prosthetic valve endocarditis. Ann IllIern Med 82:751-756,1975. 27. Karchmer A W, Dismukes WE, Buckley MJ et al: Late prosthetic valve endocarditis. Clinical features influencing therapy. Am J Med 64: 199-206, 1978. 28. Dismukes WE, Karchmer A W: The diagnosis of infected prosthetic heart valves: Bacteremia versus endocarditis. In Duma RJ ct al: In/ections 0/
Prosthetic Heart
Valves and Vascular Grafts.
Baltimore Univ Park Press, 1977, pp 65-68. 29. Feiner JM, Dowell VR: Bacteroides bacteremia. Am J Med 50:787-796, 1971. 30. Galgiani IN, Busch DF, Brass C et al: Bacteroides fragilis endocarditis, bacteremia and otherinfections treated with oral or intravenous metronidazole. Am J Med 65:284-289, 1978. 31. Feiner IN, Dowell VR Jr: Anaerobic bacterial endocarditis. N Engl J Med 283: 1188-1192, 1970. 32. Garvey GJ, Neu H: Infective endocarditis - An evolving disease. Medicine 57: I 05-127, 1978. 33. Durack DT, Petersdorf RG: Chemotherapy of experimental streptococcal endocarditis. I. Comparison of commonly recommended prophylactic regimens. J Clin Im'est 42:592-598, 1973. 34. Durack DT, Pelletier LL, Petersdorf RG : Chemotherapy of experimental streptococcal endocarditis. II. Synergism between penicillin and streptomycin against penicillin-sensitive streptococci. J Clin Invest 53:829-833, 1974. 35. Pelletier LL Jr, Durack DT, Petersdorf RG: Chemotherapy of experimental streptococcal endocarditis. IV. Further observations on prophylaxis. J Clin Invest 56:319-330, 1975. 36. Sande MA, Irvin RG: Penicillin -Aminoglycoside synergy in experimental streptococcus viridans endocarditis. J In/ect Dis 129:572-576, 1974. 37. Durack DT, Starkebaum MK , Petersdorf RG: Chemotherapy of experimental streptococcal endocarditis. VI. Prevention of enterococcal endocarditis. J Lab Clin Med90 :171-179, 1977. 38. Kaplan EL: American Heart Assoc report : Prevention of bacterial endocarditis. Circulat iOIl 56: 139A143A, 1977. 39. Everett ED, Hirschmann JV: Transient bacteremia and endocarditis prophylaxis. A review. Medicine 56:61-77, 1977. 40. Sipes IN, Thompson RL, Hook EW: Prophylaxis of infective endocarditis: A re-evaluation. Ann Rev Med 28:371-391, 1977. 41. Petersdorf RG : Antimocrobial prophylaxis of bacterial endocarditis: Prudent caution or bacterial overkill? Am J Med 65:220-223, 1978. 42. Bishop YM M, Fienberg SE, Holland PW: Discrete Multivariate Analysis: Theory and Practice. Cambridge, M A. The M IT Press, 1978, pp 59, 124, 258364, 492. 43. Scheffe H: The Analysis 0/ Variances. New York, John Wiley and Sons, Inc., 1959, pp 55-59.
THE AMERICAN JOURNAL OF THE MEDICAL SCIENCES
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BACTEREMIA FOLLOWING DENTAL EXTRACTIONS
44. Bender IB, Pressman RS, Tashman SG: Comparative effects of local and systemic antibiotic therapy in the prevention of post-extraction bacteremia. J Am Delli Assoe 57:54-66, 1958. 45. Rogosa M, Hampp EG, Nevin TA et al: Blcod sampling and cultural studies in the detection of postoperative bacteremias. J Am Delli As.we 60:171-180,1960. 46. Crawford JJ, Sconyers JR, Moriarty JD et al: Bacteremia after tooth extractions studied with the aid of pre-reduced anaerobically sterilized culture media. Appl Microbio/27:927-932, 1974. 47. Wank HA, Levison ME, Rose LF et al: A quantitative measurement of bacteremia and its relationship to plaque control. J Periodontol 47:683-686, 1976. 48. Glaser RJ, Dankner A, Mathes SB et al: Effect of penicillin on bacteremia following dental extraction. Am J Med 4:55-65, 1948. 49. Shanson DC, Cannon P, Wilks M: Amoxycillin compared with penicillin V for the prophylaxis of
50.
51.
52.
53.
54.
dental bacteremia. J Antimierob Chemolher 4:431436, 1978. Pressman RS, Bender 18: Effect of sulfonamide compounds on transient bacteremia following extraction of teeth: Sulfanilamide. Arch IllIern Med 74:346-353, 1944. Hirsh HL, Vivino JJ, Merril A et al: Effect of prophylactically administered penicillin on incidence of bacteremia following extraction of teeth. Arch IllIern Med 81:868-878, 1948. Khairat 0: An effective antibiotic cover for the prevention of endocarditis following dental and other postoperative bacteremias. J CUll Patlwl 19:561-566, 1966. Roth 0, Cavallaro AL, Parrott RH et al: Aureomycin in prevention of bacteremia following tooth extraction. Arch Intern Med 86: 498-504, 1950. Cooley FH, Haberman S: The use of antibiotics for the prevention of bacteremia following oral surgery. J Delli Res 36:294-303, 1957.
An Invitation Charles B. Slack, Inc. actively pursues development of worthwhile new and meritorious publications. Advancement for the health professions with timely and appropriate editorial projects is our objective. We are probably best known through the fifteen specialty journals we publish and the professional association seIYices we offer. How ever, we are not limited. Perhaps you, in your area of interest, have identified a topic that we can explore with meeting today's educational needs. We invite you to share with us your thoughts for a more effective book publishing program. We encourage, welcome and await your contributions.
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140
MAY/JUNE 1982 VOLUME 283 NUMBER 3
Abstract: This study describes the type, rate and magnitude of bacteremia in 128 patients undergoing dental extractions with and without penicillin prophylaxis. The most prolonged and highest rates of bacteremia occurred in patients undergoing extractions and alveoplasty while under general anesthesia following nasotracheal intubation. The most common aerobes in patients receiving no penicillin were streptococci. Bacteroides sp. were detected most often in patients receiving penicillin prophylaxis. The . overall bacteremia, streptococcal and .polymicrobial bacteremia rates were lowest for the patients receiving penicillin. Only two of 66 patients given penicillin prophylaxis had recoverable streptococci in blood cultures. Our study indicates that both intravenous and oral penicillin G prophylaxis for dental extractions decreased bacteremia rates significantly, including the recovery of streptococci. [Am J Med Sci 1982; 283(3):129-140.] KEY INDEXING TERMS
Bacteremia Dental extractions
Bacteremia is known to occur in asymptomatic human subjects but its significance as far as systemic disease is concerned is not fully understood. '12 In 1923, Lewis et al suggested that transient asymptomatic bacteremia may
Penicillin G Anesthesia
be the cause of endocarditis in patients with abnormal heart valves. 3 Subsequently, the relationships between oral procedures and bacteremia,4-9 and oral procedures and endo,o carditis have been described. -12 More recent-
From the InJectious Disease and Oral-MaxilloJacial Surgery Sections oj the VA Medical Celller. Alban), Medical College. and the Division oj Laboratories and Research. Nell' York State Departmelll oj Health. Alban.\'. Nell' York. This research lI'as supported by Medical Research Service oj the Veterans Administration. Reprint requests: A Idona L. Baltch. M. D.. Chief, InJectious Disease Section. Veterans Administration Medical Center. Albany. NY 12208. THE AMERICAN JOURNAL OF THE MEDICAL SCIENCES
129
BACTEREMIA FOLLOWING DENTAL EXTRACTIONS
Iy, interest in bacteremia rates following other invasive procedures has increased. ))-20 It has been difficult to compare various studies concerned with bacteremia associated with oral procedures because of the differences in patient selection, blood culture sampling and the use of local or systemic antimicrobial agents. Prevention of endocarditis has continued to be of great concern in patients with prosthetic heart valves or in older patients with damaged heart valves. 21 - 28 Although endocarditis continues to be related primarily to streptococci originating from the oral cavity, more fastidious microorganisms including anaerobes have been described. 21 ,28-32 Data on the pathogenesis, pathologic findings and prevention of endocarditis in animals have indicated that certain antimicrobial agents, singly or in combination, and certain doses of these drugs might be recommended for prophylaxis in humans. 33 - 38 However, the effectiveness of the suggested prophylactic regimens remains to be tested in humans for the prevention of bacteremia as well as endocarditis. 38 Although two recent reviews indicate the need and support the use of prophylactic antimicrobial agents in the prevention of endocarditis, Petersdorf challenges the presently recommended prophylaxis and suggests a more conservative regimen. 39 - 41 The present study describes the type, rate and magnitude of bacteremia in patients undergoing dental extractions with and without penicillin prophylaxis. Materials and Methods Patient Selection This prospective study included 128 patients (all but two were males). No patients were febrile (rectal temperature not above 37° C), none received antimicrobial agents or had intravenous, urinary or other catheters for at least four weeks before the procedure. No patients were receiving prednisone or other immunosuppressive drugs. Sixty-two procedures (48.8%) were done on outpatients and 65 procedures (51.2%) were performed on inpatients. The patients were divided into four 130
groups: i) 33 received intravenous (IV) potassium penicillin G and local anesthesia; 2) 36 received oral phenoxymethyl penicillin (Penicillin V) and local anesthesia; 3) 29 received no penicillin and had the procedure done under local anesthesia; 4) 30 received no penicillin and had the procedure done following naso-endotracheal intubation and while under general anesthesia. The average age of patients in Group I was 46 years (range 2069), in Group 2 was 42 years (19-61), in Group 3 was 42 years (20-83), and in Group 4 was 35 years (21-61). Only patients with known valvular heart disease received aqueous penicilJin G 2 million units IV via heparin well before the procedure and every four hours thereafter for 72 hours. The penicillin was infused during a 30-40 minute period and the surgical procedure was started 15 minutes following the completion of the infusion. Penicillin V was administered 30 minutes before the procedure in doses of 0.5-1 gm to patients with soft tissue swelling of the face. Ten of the 36 patients in this group received additional Penicillin V 0.5-1 gm every six hours for 24 to 48 hours before the extractions because of the severity of inflammation of the soft tissues of the oral cavity, face and/or submandibular area with or without the presence of a periapical dental abscess. None of the patients receiving oral penicillin had valvular heart disease documented by history or physical examination. Table I depicts the number of patients in each of the four groups undergoing a single extraction (40 patients), 2-6 extractions (50 patients) and 7 or more extractions (38 patients). The average time required for extractions done under local anesthesia in patients receiving IV penicillin G was 36 minutes, and in patients receiving oral penicillin V or no penicillin the average time was 21 minutes. In contrast, an average of 105 minutes was required for patients undergoing dental extractions while under general anesthesia (no penicillin prophylaxis). All hospitalized patients were evaluated immediately after the procedure and every 4 hours for 24 hours for the development of MAY/JUNE 1982 VOLUME 283 NUMBER 3
BALTCH ET AL
TABLE I NUMBER OF PATIENTS WITH AND WITHOUT PENICILLIN PROPHYLAXIS WHILE UNDERGOING SINGLE OR MULTIPLE DENTAL EXTRACTIONS
Oralt
Penicillin None
None
Local
Local
Anesthesia Local
General
9
15 8
Intravenous* Number of teeth extracted 2-6
10
7+
14
14 18 4
Total
33
36
Total
2
40 50
6
14 14
29
30
128
38
*Aqueous penicillin G 2 million units IV 30 minutes beJore the procedure and every Jour hours Jor 72 hours'thereaJter. t Phenoxymethyl penicillin (Penicillin V) orally 0.5 - I gm 30-45 minutes beJore the procedure.
fever. In addition, patients receiving parenteral penicillin G were followed up for 12-36 months for the possible development of endocarditis. Dental Extraction Procedure All extractions were performed by one oral surgeon (H .P.). Procedures in patients requiring mUltiple dental extractions or full mouth exodontia were combined with alveoplasty (recontouring of alveolar bone for future dental prostheses). Patients requiring local anesthesia had regional anesthetic nerve blocks. Procedures done on patients while under general anesthesia (thiopental, nitrous oxide, halothan~) were performed in the operating room. These patients had nasoendotracheal intubation. Patients in all four groups also received a local gingival and mucosal anesthetic infiltration with 2% xylocaine combined with epinephrine (I: 100,000) to aid hemostasis. Blood Cultures Blood cultures were obtained by performing a separate venipuncture before, and 5 and 30 minutes following the completion of the oral procedure. Additional blood cultures were obtained from patients undergoing
general anesthesia just before and immediately following naso-endotracheal intubation (the latter sample was considered the pre-extraction sample). The skin was cleansed with providone-iodine using three scrubs. Eight milliliters of blood were placed into 100 ml trypticase soy broth (Difco), and 4 ml into 50 ml of thiol (Difco), thioglycollate (BBL) and either brucella broth or brain heart infusion (Scott) respectively. All media bottles had a partial vacuum with 5% CO 2 and contained 0.03% sodium polyanetholsulfonate. Blood cultures were incubated at 37°C, subcultured at 24-48 hours and again at 14 days. Subcultures were performed using fresh 5% horse blood agar plates supplemented with hemin, yeast extract and Vitamin K, and incubated at 37°C in 5% C02 for aerobic conditions and in Gas-Pakjars with disposable hydrogen-carbon dioxide generator envelopes with a palladium catalyst for anaerobic growth (BBL, Cockeysville, MD). Theaerobic plates were read in 24-48 hours, and the anaerobic growth was read at 72-96 hours. In addition, quantitative pour plates were done by placing one and one-half milliliters of blood into 15 ml of trypticase soy agar for aerobic culture and into Schaedler's agar for anaerobic culture in 79 patients. Colonies
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BACTEREMIA FOLLOWING DENTAL EXTRACTIONS
TABLE 2 PERCENT OF PATIENTS WITH POSITIVE BLOOD CULTURES AT 5 AND 30 MINUTES FOLLOWING DENTAL EXTRACTIONS AND ALVEOPLASTY
Time in minutes after dental extraction 5
Intravenous*
Oralt
Penicillin None
None
Local
Local
Anesthesia Local
Generalt
34.4
47.2
58.6
76.7
(17/36)
(17/29)
(23/30)
(11/32)** 30
12.1
13.9
26.7
51.7
( 4/33)
( 5/36)
( 8/29)
(15/29)
TablC' I. TablC' I. :1:34.5% (10/29) lIwe bacterelllic folloll'illg lIaso-t/'{/cheal intubatioll. **NulllbC'r (~r patiC'nt.l' with bact('fC'lIIia/llulllber of all patiellts ill the group. *SC'C'
t SC'C'
were counted at 48 hours in the aerobic plates and at 72-96 hours in the anaerobic plates. Following the isolation of individual bacterial strains, all identification and speciation was performed at the New York State Department of Health, Division of Laboratories and Research, Albany, New York. Identification of aerobes was done using conventional methods. Gram stain, colonial morphology, biochemical analyses and gasliquid chromatography were used for the identification of anaerobes.
Statistical Methods Statistical inferences were made using the Chi square test of association 42 for unpaired samples of categorical data and the McNemar test and the McNemar-like test for paired samples. 42 For small sample sizes the hypergeometric (unpaired samples) and the binomial (paired samples) distributions were used to calculate the exact probabilities in the statistical tests of the null hypotheses. 42 The one way analysis ofvariance 43 on the FreemanTukey modification 42 of the square root transformation of the number of different organisms cultured was used to test the null hypothesis of the equality of means. Selected 132
contrasts among the means and among the rates were also investigated. The level of significance was set at 0.05.
Results The bacteremia rates at 5 and 30 minutes following extractions and alveoplasty in patients with and without penicillin prophylaxis while under local or general anesthesia are shown in Table 2. None of the 128 patients were bacteremic before the start of the dental procedure. Highest rates of positive blood cultures were observed in patients under general anesthesia. One-third of these patients were bacteremic following nasotracheal intubation for general anesthesia. All patients bacteremic after intu bation were also bacteremic 5 minutes following dental extractions, a procedure which took an average of 105 minutes. Five of these 30 patients were also bacteremic at 30 min utes. Of the 19 patients with negative blood cultures after intubation, 6 were positive at both 5 and 30 minutes .. The 76.7% bacteremia rate at 5 minutes represents a significant increase while the 51.7% rate at 30 minutes is not significantly different from the rate following intubation. These findings suggest that in patients under general anesMAY/JUNE 1982 VOLUME 283 NUMBER 3
BALTCH ET AL
TABLE 3 PERCENT OF PATIENTS WITH POSITIVE BLOOD CULTURES CONTAINING STREPTOCOCCI AT 5 AND 30 MINUTES AFTER DENTAL EXTRACTIONS AND ALVEOPLASTY
Penicillin
Anesthesia
Time (min) Arter Procedure
Percent with Streptococci in Bacteremic Patients
Percent with Streptococci in all Patients
Intravenous*
Local
5 30
9.1 (I/II)tt 0.0 (0/4)
3.1 (I/32)U 0.0 (0/32)
Oralt
Local
5 30
5.9 (1/17) 0.0 (0/5)
2.8 (1/36) 0.0 (0/36)
None
Local
5 30
76.5 (13/17) 25.0 (2/8)
44.8 (13/29) 6.9 (2/29)
None
General
5 30
73.9 (17/23)** 40.0 (6/15)
56.7 (l7/30lt 20.7 (6/29)
*See
Table I. t See Table I. tI3.8% (4/29) 0/ paliel1fs lI'ere bacleremic a/IeI' Ilaso-Iraclleal il1fllbatioll. **40.0 (4/10) 0/ paliel1fs lI'ere bacleremic a/IeI' lla.I'O-lraclleal il1fllbatioll. tt Paliel1fs bacleremic lI'illl sireptococci/ paliel1fS lI'illl bacleremia. ttPaliellls bacleremic lI'illl sireplococci/all patiellls.
thesia both procedures (intubation and extractions) influence the observed high rate of bacteremia. Among the four patient groups at 5 and 30 minutes respectively the bacteremia rates were significantly different. However, selected contrasts could not be shown to be statistically significant, most probably because of the size of the samples. For each group, the observed drop in the rate of bacteremia from 5 to 30 minutes was not attributable to chance. Of note was the observation that 85% of patients with negative blood cultures at 5 minutes were also negative at 30 minutes. Table 3 shows the percent of patients with positive blood cultures containing streptococci. Four of the 29 patients in the general anesthesia group had streptococcal bacteremia following naso-tracheal intubation. In this group, there was a significant increase in the recovery of streptococci at 5 minutes (56.7%) with a significant drop at 30 minutes (20.7%). The observed rates of bacteremia after intubation and at 30 minutes were similar. Lesser rates of streptococcal bacte-
remia were observed in patients whose extractions were performed while under local anesthesia without penicillin prophylaxis, 44.8% and 6.9% at 5 and 30 minutes respectively. The observed rates of bacteremia at 5 minutes in patients receiving no penicillin was significantly higher than in the patients receiving either type of penicillin prophylaxis. In fact, only one patient in each group of patients receiving penicillin had streptococcal bacteremia. Although the recovery rate of streptococci for the groups receiving no penicillin was lower at 30 than at 5 minutes, the rate at 30 minutes for the general anesthesia patients was significantly higher than that seen for the local anesthesia group" The percent of patients with polymicrobial bacteremia (2' to 15 strains recovered in different patients) are seen in Table 4. The highest rate at 5 minutes occurred in the general anesthesia group and represents a significant increase over the rate immediately following intubation and the rate at 30 minutes. The differences in polymicrobial bacteremia in the two groups of patients
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BACTEREMIA FOLLOWING DENTAL EXTRACTIONS
TABLE 4 PERCENT OF PATIENTS WITH POLYMICROBIAL BACTEREMIA AT 5 AND 30 MINUTES AFTER DENTAL EXTRACTION AND ALVEOPLASTY
Penicillin
Anesthesia
Time in Minutes after Dental Extraction
Percent Polymicrobial Bacteremia in Bacteremia Patients
Percent Polymicrobial Bacteremia in all Patients
Intravenous*
Local
S 30
36.4 (4/ 11m SO.O ( 2/4)
12.S ( 4/32)tt 6.1 ( 2/33)
Oralt
Local
5 30
64.7 (\ 1/17) 20.0 ( I/S)
30.6 (11/36) 2.8(1/36)
None
Local
S 30
82.4 (14/17) 7S.0 ( 6/8)
48.3 (14/29) 20.7 ( 6/29)
None
General
S 30
82.6 (19/23)t 26.7 ( 4/ IS)
63.3 (19/30)** 13.8 ( 4/29)
*See Table I. t See Table I. pO.O% (5/10) of bacteremic patiell/s lwei polymicrobial bacteremia q(ter lIa.m-tracheal ill/libatioll. **17.2% (5/29) of all patiell/s after illwbatioll hael polymicrobial bacteremia. tt Patiell/s with polymicrobial bacteremia/patiell/s with bacteremia. HPatiell/s with polymicrobial bacteremia/all patiell/s.
receiving no prophylaxis could not be shown to be statistically significant. There is a significantly lower rate of polymicrobial bacteremia at 5 and 30 minutes in patients receiving either type of penicillin prophylaxis than that seen in patients without penicillin. For all but the IV penicillin group the decrease in the polymicro bial bacteremia rate from 5 to 30 minutes is significant. The total number of isolates and the average number of isolates per positive blood culture recovered at 5 and 30 minutes for each ofthe four patient groups is seen in Table 5. At 5 minutes the average number of isolates recovered per positive blood culture varies significantly among the groups. The average number of recovered isolates for patients receiving no penicillin was significantly higher than that found in patients with penicillin prophylaxis. Following intubation the 10 bacteremic patients had 1.9 isolates per positive blood culture. A significant increase to 4.3 isolates per positive culture was seen in these patients 5 minutes after extractions. Of interest was a significantly lower average 134
isolate recovery rate in this group at 30 minutes when compared with the group of patients under local anesthesia without penicillin prophylaxis (1.8 vs. 4.0). Tables 6 and 7 present the aerobic/facultative and anaero bic isolates recovered in this study. Three hundred and four bacterial species (128 aerobic/facultative and 176 anaerobic) were recovered from patients following and none before the oral procedures. One half of the aerobic/facultative isolates were streptococci in patients receiving no penicillin prophylaxis. Of the II strains of streptococci recovered, Streptococcus sanguis and S. mitis were most frequent; no enterococci were isolated. Twenty-two other aero bic/ facultative bacterial species were recovered and only three bacillary forms could not be identified. Of the 37 anaerobic species, the most commonly detected anaerobes were in the Bacteroides group, followed by peptostreptococci, Propionibacterium, Veillonella and peptococcal groups. Only four Actinomyces and one clostridial species were detected. Twelve bacillary and 5 coccal forms could not MAY/JUNE 1982 VOLUME 283 NUMBER 3
BALTCH ET AL
TABLE 5 NUMBER OF ISOLATES RECOVERED AND AVERAGE NUMBER OF ISOLATES PER POSITIVE BLOOD CULTURE AT 5 AND 30 MINUTES AFTER DENTAL EXTRACTION AND ALVEOPLASTY AND FOLLOWING NASOTRACHEAL INTUBATION
Penicillin
Anesthesia
Time
Total Number of Isolates
IV·
Local
5 30
18 10
II
4
1.6 2.5
Number of Positive Cultures
Average Number of Isolates Per Positive Culture
pot
Local
5 30
42 6
17 5
2.5 1.2
None
Local
5 30
70 32
17 8
4.1 4.0
None
General
5 30
100 27
23 15
4.3 1.8
19
10
1.9
After Intubation
·See Table I. t See Table I.
be identified. The magnitude of bacteremia as measured with quantitative aero bic and anaerobic pour plates was low. Only 8.2% of the aerobic plates (1-2 colonies/ 1.5 ml blood) and 9.8% of the anaerobic plates (1-6 colonies/ 1.5 ml blood) were positive. The clinical follow-up of all 32 patients with valvular heart disease (oral surgery performed under local anesthesia following IV penicillin prophylaxis) indicated that none were febrile immediately following and for 24 hours after the oral procedure. In a 12-36 month followup none of these patients developed infectious complications.
Discussion In the present study bacteremia of the greatest magnitude occurred in patients undergoing mUltiple dental extractions while under general anesthesia. Immediately after endotracheal intubation one-third of the patients were bacteremic and one-half of those remained bacteremic at 5 and 30 minutes following extractions and alveoplasty. In addition, six of the I 9 patients not bacteremic
after intubation became bacteremic after extractions. The time for extractions including alveoplasty while under general anesthesia varied from one to two hours depending on the complexities of the intraoral surgery. Clearly, in this group of patients both intubation and intraoral surgery contributed to the rate of bacteremia. Patients having oral procedures done while under local anesthesia and no penicillin had a considerably shorter surgical time (ranging from 12 to 54 minutes) than patients under general anesthesia and lower rates of bacteremia. Although at 5 minutes streptococci were recovered in one half of the patients in both groups, at 30 minutes a significant drop in streptococcal bacteremia was 0 bserved (2 I % in the general anesthesia and 7% in the local anesthesia groups). The relationship of surgical trauma with resulting bacteremia suggested previously is demonstrated in our study.44,45 Ninety percent of our patients had dental extractions because of severe periodontitis, periapical abscess or impacted 3rd molars with or without pericoronitis. However, in
THE AMERICAN JOURNAL OF THE MEDICAL SCIENCES
135
BACTEREMIA FOLLOWING DENTAL EXTRACTIONS
TABLE 6 AEROBIC AND FACULTATIVE MICROORGANISMS ISOLATED FROM BACTEREMIA PATIENTS WITH AND WITHOUT PENICILLIN PROPHYLAXIS Penicillin Intravenous·
Oralt
None
None
Anesthesia Local Bacterial Isola tes Streptococcus sanguis S. mitis S. mutans S. salivarius S. agalactiae S. MG - intermedius S. F - Lancefield S. a hem }nonS. {3 hem} groupS. nonhem } able S. microaerophilic Actinomyces sp. A. naeslundii A. microaerophilic Staphylococcus epid. Lactobacillus sp. L. microaerophilic Micrococcus sp. Aerococcus viridans Corynebacterium sp. C. xerosis C. ovis Actinobacillus actinomycetem-comita ns Actinobacillus sp. Eikenella corrodens Catena bacterium sp. Pse udomonas maltophlia Gemella hemolysan s Vibrio extorquens Neisseria sicca Streptomyces sp. Gram + bacilli Gram-bacilli
No.
I
Local
%
No.
Local
%
3.1
I
3.1
I
3.1
I I I
3.1 3.1 3.1
I
2.1
I
2.1
I I
2.1 2. 1
3 I
6.4 2.1
I
I
General
No.
%
No.
%
6 3 I
6.4 3.2 1.1
15 6 2 I
11.0 4.4 1.5 0.1
2
2.1 2 3 4 I 2 4 1 I I 8 4 2 I I I I I
1.5 2.2 2.9 0.1 1.5 2.9 5.1 0.1 0.1 5.9 2.9 1.5 0.1 0.1 0.1 0.1 0.1
I
0.1
I
0.1
I
0.1
3 3 2 2 6
3.2 3.2 2.1 2.1 6.4
I 3 I I I I
1.1 3.2 1.1 1.1 1.1 1.1
2
2. 1
I
l.l
I
1.1
I
1.1
2. 1
3.1
Total aerobes Total anaerobes
1 20
25.9 14.0
9 38
19.0 80.9
41 53
43.9 56.9
11 65
51.1 41.4
Overall Total
21
100.0
41
100.0
94
100.0
136
100.0
• See Table I.
t See Tobit· I.
\36
MAY/JUNE 1982 VOLUME 283 NUMBER 3
BALTCH ET AL
TABLE 7 ANAEROBIC MICROORGANISMS ISOLATED FROM BACTEREMIC PATIENTS WITH AND WITI-IOUT PENICILLIN PROPHYLAXIS Penicillin Intravenous*
Ora It
Local
Local
None
None
Local
General
Anesthesia Bacterial Isolates Bacteroides sp. B. corrodens B. melaninogenicus B. pneumonsintes B. nigrescens B. CDC Group FI B. CDC Group F2 Peptostreptococcus sp. P. micros P. productus P. anaerobius P. CDC Group 2 P. CDC Group 3 Peptococcus sp. P. variabilis P. prevotii P. intermedius P. morbillorum P. magnus Propionibacterium sp. P. acnes P. granulosum Fusobacterium sp. F. nucleatum Veillonella alcalescens V. parvula V. CDC Group 3 Eubacterium sp. F. lentum F. alactolyticum F. aerofaciens Actinomyces sp. A. israelii Lactobacillus sp. Clostridium bifermentans Selenomonas sputigena Campylobacter sputorum Gram + bacilli Gram + cocci Gram - bacilli Gram - cocci
No.
%
No.
%
No.
%
No.
%
3 2 2
Il.l 7.4 7.4
6 3 I I
12.8 6.4 2.1 2.1
3 5 4
3.2 5.3 4.3
4 I 3 I
2.9 0.7 2.2 0.7
I I I I I I I I
l.l l.l 1.1 1.1 l.l l.l l.l 1.1
I I 4
0.7 0.7 2.9
I
0.7
2
2.1
4 I 2
2.9 '0.7 1.5
I
1.1 2 I 2 8
1.5 0.7 1.5 5.9
I 3 6 5 I
0.7 2.2 4.4 3.7 0.7
3 I I I
2.2 0.7 0.7 0.7
2
1.5
2 3
1.5 2.2
I 2
I
3.7 7.4
3.7 11.1
I
3.7
I I I
4.3 4.3 2.1
2 I 2
4.3 2.1 4.3
3.7
I 3
I
2 2 I
I 4
2.1 8.5
I
2.1
I 3 2
2.1 6.4 4.3
I I 2 3 5 2
l.l 1.1 2.1 3.2 5.3 2.1
2 3
2.1 3.2
I
1.1
I I
1.1 l.l
I 3 I 3
1.1 3.2 1.1 3.2
3.7
3.7 3.7 3.7
I
2.1
I
2.1
I
2.1
I I
2.1 2.1
Total anaerobes Total aerobes
20 7
74.0 25.9
38 9
80.9 19.0
53 41
56.9 43.9
65 71
47.4 51.7
Overall Total
27
100.0
47
100.0
94
100.0
136
100.0
*See TaMe I. t See Table I.
THE AMERICAN JOURNAL OF THE MEDICAL SCIENCES
137
BACTEREMIA FOLLOWING DENTAL EXTRACTIONS
contrast to O'Keli et ai, who found bacteremia in 10.9% of patients before dental extractions, none of our patients were bacteremic before the oral procedure. II None of the microorganisms isolated in our study were considered contaminants. Although the overall number of bacterial strains recovered from blood cultures of patients receivingprophylacticadministration of penicillin was considerably smaller than the number found in. patients without penicillin prophylaxis (90 vs. 230), this decrease was more evident for the aerobes and facultative microbial strains than for the anaerobes. Only 16 compared with III aerobes and 58 compared with 118 anaerobes were recovered from patients receiving and not receiving penicillin, respectively. In patients given no penicillin, the most common aerobes and anaerobes were streptococci (23.4-29.3%) and Bacteroides sp. (7.9-17.2%), respectively. In contrast. 32-37% of the isolates were Bacteroides sp. and only 2.1-3 .7% were streptococci in patients receiving penicillin prophylaxis. The presence of anaero bes in post-extraction blood cultures was emphasized first by Khairat and subsequently by several other studies. 9 ,.16,.17 Although our data revealed fewer anaerobic isolates than that by Crawford et al. the difference may have been related to the different timing of blood sampling as well as selection of different blood culture media. 46 Penicillinase was not added to blood cultures in our study in order to avoid any possible contamination. Several earlier studies indicated that the use of penicillinase may increase the recovery of microorganisms from blood cultures of patients receiving penicillin prophylaxis.J,5,.1S,.I9 However, in these studies the doses of penicillin used in prophylaxis and the concentrations and times penicillinase was added to the blood cultures varied widely. Therefore. these variables did not allow for an adequate comparison of these studies with our data. In an attempt to decrease bacteremia following oral surgical procedures. prophylactic use of antimicrobial agents has been tried by a number of investigators. Only a minimal 138
and unsustained effect was observed with sulfonamides. 50 With penicillin the decrease in positive blood cultures varied from 9%51 to 42%8 depending on the penicillin preparation administered and method of blood culturing. With other antibiotics the decrease varied from 25 to 61 % . 48,52-54 Recently a small study comparing oral amoxycillin with Penicillin V indicated more sustained serum concentrations with amoxycillin and therefore fewer 49 positive blood cultures. I n the present study. the overall streptococcal and polymicrobial bacteremia rates were lowest for the groups receiving penicillin. There were only two patients with streptococci in blood cultures at 5 minutes and no patients with streptococcal bacteremia 30 minutes after the surgical procedures with intravenous or oral penicillin prophylaxis. In summary. our data indicate that bacteremia of greatest magnitude occurred in patients undergoing dental extractions while under general anesthesia after intubation. Intravenous or oral penicillin prophylaxis decreased the bacteremia rates significantly. including the recovery of streptococci. Acknowledgments The authors thank Anna May Lee. Robert Meidenbauer and George E. Hannett of the Division of Laboratories and Research. New York State Department of Health. for technical help. and Shirley Boyce of the Dental Service for assistance with patients. The secretarial assistance of Charlotte Manning and Judy Dean is greatly appreciated.
References I. Hockett RN. Loesche WJ. Sodeman TM: Bacteremia in asymptomalic human subjects. Arch Oral Bioi 22:91-98. 1977. 2. Wilson WR. Van Scoy RE. Washington JA: Incidence of bacteremia in adults without infection. J elill /'I'licrobiol 1:94-95. 1976. 3. Lewis T. Grant RT: Observations relating to subacute infective endocarditis. Hf'url 10:21-29. 1923. 4. Burket LW. Burn CG: Bacteremias following dental extraction: Demonstration of source of bacteria by means of nonpathogen (Serratia marcescens). J Df'1/I Rf'S 16:521-530.1937. 5. Elliott SD: Bacteremia and oral sepsis. Proc Roy Soc Mf'c/ 32:747-754. 1939.
MAY/JUNE 1982 VOLUME 283 NUMBER 3
BALTCH ET AL
6. McEntegart MG, Porterfield JS: Bacteremia following dental extractions. Lancet 2:596-598, 1949. 7. Robinson L, Krause FW, Lazansky JP: Collective review: Bacteremias of dental origin. A review of the literature. Oral Surg 3:519-531, 1950. 8. Schirger A, Martin WJ, Royer RQ et al: Bacterial invasion of blood after oral surgical procedures. J Lab Clin Ml!d 55:376-380, 1960. 9. Khairat 0: The non-aerobes of post-extraction bacteremia. J Delli Res 45:1191-1197,1966. 10. Rushton MA : Subacute bacterial endocarditis following the extraction of teeth. Guy's Hasp Rep 80:39-44, 1930. II. O'Kell CC, Elliott SD: Bacteremias and oral sepsis. With special reference to the aetiology of subacute endocarditis. Lancet 2:869-872, 1935. 12. McGowan DA, Hardie J M: Production of bacterial endocarditis in prepared rabbits by oral manipulation. Br Delli J 137: 129-131, 1974. 13. Sullivan N M, Sutter VL, Carter WT et al: Bacteremia after genitourinary tract manipulation: Bacteriological aspects and evaluation of various blood culture systems. Appl Microbiol 23: 11011106, 1972. 14. Sullivan NM, Sutter VL, Mims MM et al: Clinical aspects of bacteremia after manipulation of the genitourinary tract. J In/ect Dis 127:49-55, 1973. 15. Baltch AL, Buhac I, Agrawal A et al: Bacteremia 'Ifter upper gastrointestinal endoscopy. Arch IllIern Med 137:594-597, 1977. 16. Shull HJ Jr, Greene BM, Allen SD et al: Bacteremia with upper gastrointestinal endoscopy. Anll III/ern Mecl83:212-214,1975. 17. Buchman E, Berglund EM: Bacteremia following sigmoidoscopy. Am Heart J 60:863-866, 1960. 18. McCloskey RV, Gold M, Waser E: Bacteremia after liver biopsy. Arch IllIern Med 132:213-215, 1973. 19. Berry FA Jr, Blankenbaker WL, Ball CG: A comparison of bacteremia occurring with nasotracheal and orotracheal intubation. Anesth Analg (Cleve) 52:873-876, 1973. 20. Kane RC, Cohen M H, Fossieck BE et al: Absence of bacteremia after fiberoptic bronchoscopy. Am Rev Respir Dis III: 102-104, 1975. 21. Kaye D: Infecting microorganisms. In Kaye D (ed): In/ectil'e Endocarditis. Baltimore, Univ Park Press, 1976, pp 43-54. 22. Killen DA, Collina HA, KoenigGA et al: Prosthetic cardiac valves and bacterial endocarditis. Ann Thorac Surg 9:238-247, 1970. 23. Slaughter L, Morris J E, Starr A: Prosthetic valvular endocarditis: A 12 year review. Circulation 47: 13191326, 1973. 24. Dismukes WE, Karchmer A W, Buckley MJ et al: Prosthetic valve endocarditis: Analysis of 38 cases. Circulation 48:365-377, 1973. 25. Sande MA, Johnson WD Jr, Hook EW et al: Sustained bacteremia in patients with prosthetic cardiac valves. N Ellgi J M ed 286: 1067-1070, 1972.
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Prosthetic Heart
Valves and Vascular Grafts.
Baltimore Univ Park Press, 1977, pp 65-68. 29. Feiner JM, Dowell VR: Bacteroides bacteremia. Am J Med 50:787-796, 1971. 30. Galgiani IN, Busch DF, Brass C et al: Bacteroides fragilis endocarditis, bacteremia and otherinfections treated with oral or intravenous metronidazole. Am J Med 65:284-289, 1978. 31. Feiner IN, Dowell VR Jr: Anaerobic bacterial endocarditis. N Engl J Med 283: 1188-1192, 1970. 32. Garvey GJ, Neu H: Infective endocarditis - An evolving disease. Medicine 57: I 05-127, 1978. 33. Durack DT, Petersdorf RG: Chemotherapy of experimental streptococcal endocarditis. I. Comparison of commonly recommended prophylactic regimens. J Clin Im'est 42:592-598, 1973. 34. Durack DT, Pelletier LL, Petersdorf RG : Chemotherapy of experimental streptococcal endocarditis. II. Synergism between penicillin and streptomycin against penicillin-sensitive streptococci. J Clin Invest 53:829-833, 1974. 35. Pelletier LL Jr, Durack DT, Petersdorf RG: Chemotherapy of experimental streptococcal endocarditis. IV. Further observations on prophylaxis. J Clin Invest 56:319-330, 1975. 36. Sande MA, Irvin RG: Penicillin -Aminoglycoside synergy in experimental streptococcus viridans endocarditis. J In/ect Dis 129:572-576, 1974. 37. Durack DT, Starkebaum MK , Petersdorf RG: Chemotherapy of experimental streptococcal endocarditis. VI. Prevention of enterococcal endocarditis. J Lab Clin Med90 :171-179, 1977. 38. Kaplan EL: American Heart Assoc report : Prevention of bacterial endocarditis. Circulat iOIl 56: 139A143A, 1977. 39. Everett ED, Hirschmann JV: Transient bacteremia and endocarditis prophylaxis. A review. Medicine 56:61-77, 1977. 40. Sipes IN, Thompson RL, Hook EW: Prophylaxis of infective endocarditis: A re-evaluation. Ann Rev Med 28:371-391, 1977. 41. Petersdorf RG : Antimocrobial prophylaxis of bacterial endocarditis: Prudent caution or bacterial overkill? Am J Med 65:220-223, 1978. 42. Bishop YM M, Fienberg SE, Holland PW: Discrete Multivariate Analysis: Theory and Practice. Cambridge, M A. The M IT Press, 1978, pp 59, 124, 258364, 492. 43. Scheffe H: The Analysis 0/ Variances. New York, John Wiley and Sons, Inc., 1959, pp 55-59.
THE AMERICAN JOURNAL OF THE MEDICAL SCIENCES
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BACTEREMIA FOLLOWING DENTAL EXTRACTIONS
44. Bender IB, Pressman RS, Tashman SG: Comparative effects of local and systemic antibiotic therapy in the prevention of post-extraction bacteremia. J Am Delli Assoe 57:54-66, 1958. 45. Rogosa M, Hampp EG, Nevin TA et al: Blcod sampling and cultural studies in the detection of postoperative bacteremias. J Am Delli As.we 60:171-180,1960. 46. Crawford JJ, Sconyers JR, Moriarty JD et al: Bacteremia after tooth extractions studied with the aid of pre-reduced anaerobically sterilized culture media. Appl Microbio/27:927-932, 1974. 47. Wank HA, Levison ME, Rose LF et al: A quantitative measurement of bacteremia and its relationship to plaque control. J Periodontol 47:683-686, 1976. 48. Glaser RJ, Dankner A, Mathes SB et al: Effect of penicillin on bacteremia following dental extraction. Am J Med 4:55-65, 1948. 49. Shanson DC, Cannon P, Wilks M: Amoxycillin compared with penicillin V for the prophylaxis of
50.
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53.
54.
dental bacteremia. J Antimierob Chemolher 4:431436, 1978. Pressman RS, Bender 18: Effect of sulfonamide compounds on transient bacteremia following extraction of teeth: Sulfanilamide. Arch IllIern Med 74:346-353, 1944. Hirsh HL, Vivino JJ, Merril A et al: Effect of prophylactically administered penicillin on incidence of bacteremia following extraction of teeth. Arch IllIern Med 81:868-878, 1948. Khairat 0: An effective antibiotic cover for the prevention of endocarditis following dental and other postoperative bacteremias. J CUll Patlwl 19:561-566, 1966. Roth 0, Cavallaro AL, Parrott RH et al: Aureomycin in prevention of bacteremia following tooth extraction. Arch Intern Med 86: 498-504, 1950. Cooley FH, Haberman S: The use of antibiotics for the prevention of bacteremia following oral surgery. J Delli Res 36:294-303, 1957.
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