The bacteriology of dentogenous pyogenic infections

The bacteriology of dentogenous pyogenic infections L. Aderhold, DrMed., Dr.Med.Dent.,* H. Knothe, ProjIDr.Med.,** and G. Frenkel, ProjDrMed., Dr.Med.Dent., * Frankfurt am Main, West Germany JOHANN-WOLFGANG-GOETHE

UNIVERSITY

The resistance spectra of aerobic and anaerobic bacteria from dentogenous abscesses were investigated in a filter study. Aerobic-anaerobic bacterial complexes of endogenous origin are characteristic of dentogenous pyogenic infections. These bacteria as a whole proved to be very sensitive to antibiotics.

D

entogenous pyogenic infections of the maxillofacial region play an important role in maxillary surgery, even now, in the era of antibacterial chemotherapy, because of the danger of spreading and complications through general and metastatic infection. Knowledge of the potential spectrum of pathogens, as well as the regional resistance status, is important for rational chemotherapy. Increasing numbers of infections due to anaerobic and gramnegative pathogenic organisms have been reported by workers in various medical specialties. Since very contradictory data exist up to now concerning the participation of these bacteria in dentogenous abscesses,it was considered of interest to investigate the aerobic and anaerobic pathogens and their resistance patterns. MATERIALS

AND METHODS

Fifty acute abscessesof dentogenous origin were selected for study. They had not previously been treated locally. None of them had any connection to either the oral mucosa or the external skin through a fistula or perforation. The roots of the compromised teeth had not been previously treated. Only aspirations of at least 0.5 ml. of purulent exudate obtained with antiseptic precautions we’e

This study was supported by a grant from Upjohn GmbH, FRG. *Department of Dentril, Oral and Maxillo-facial Surgery (Chief: Prof. G. Frenkel). **Department of Medical Microbiology (Chief: Prof. H. Knothe). 0030-4220/81/120583

+ 05$OU.50/0 0 1981 The C. V. Mosby Co.

I. Bacterial distribution in pure and mixed, aerobic and anaerobic cultures

Table

Culture

Pure culture Mixed culture: 2 strains 3 strains 4 strains 5 strains 6 strains 7 strains

Aerobes Anaerobes I

1

I

5 3 5

Aerobelanaerobe

Total 2

2 9 11 7 4 1

8 12 16 7 4 1

utilized for this bacteriologic study. Specimens were processedimmediately after collection. Whenever a protracted period prior to culture was considered possible, transport medium (Port-A-Cul; Becton, Dickinson & Co., Heidelberg) was employed. For each specimen, a microscopic smear as well as two anaerobic cultures (Schaedler agar with 10 percent blood, Schaedler K.V. with 5 percent blood) were prepared. One culture from each medium was then incubated in gas packs for 2 and for 7 days. A Tarozzi broth culture was additionally prepared from each specimen. A 5 percent blood agar plate was used for aerobic culture and incubated for 24 hours. After isolation of pure cultures, identification of the strains was done on the basis of Cram stains and macroscopic and microscopic morphology, as well as biochemical criteria (API system; API Laboratory Systems,Inc., Wiesbaden). Follow-up sensitivity testswere performed by agar diffusion on Schaedler agar with 10 or 5 percent blood agar plates, respec583

584 Aderhold, Knothe, and Frenkel Table

Oral Surg. December, I98 I

II. Distribution of aerobic and anaerobic cocci and bacilli Aspiraiion Strains

Extraoral

strains

Intraoral

Cases Total

NO.

%

Aerobic:

Gram-positive cocci Gram-negative cocci Gram-positive bacilli Gram-negative bacilli

22 2 1 1

22 0 2 0

44 2 3 I

35 2 3 I

70 4 6 2

23 2 4

19 3 II

42 5 15

33 5 13

66 10 26

36

35

71

45

90

Anaerobic,:

Gram-positive cocci Gram-negative cocci Gram-positive bacilli Gram-negative bacilli

Table

III. Culture results

-,,_ Aerobe/anaerobe Anaerobe Aerobe

18

16

34

68

I 1

7 1

14

28

2

4

tively. Particulars of specimen collection and transport techniques are detailed in a prior publication. ’ RESULTS

Aspiration of purulent samples was performed in 52 percent of the casesextraorally and in 48 percent intraorally. One to seven strains (average 3.66 strains) were identified from each culture (Table I). A mixed culture of aerobic and anaerobic flora was used in 68 percent of the cases. Pure anaerobic cultures were noted in 28 percent of the cultures, and pure aerobic cultures in 40 percent (Table III). Anaerobic bacteria were thus cultured in a total of 96 percent of the specimens tested. The distribution of aerobic and anaerobic species as pure and mixed cultures is indicated in Table I and II. Comparison of the species distribution for the extraoral and intraoral routes of aspiration revealed nearly identical results. The various aerobic and anaerobic species cultured are shown in Table IV. B. fragilis was not isolated in any instance. The combination of aerobic streptococci with Bacteroides was isolated in 60 percent of the cases(Table V). Aerobic streptococci, Bacteroides, and fusobacteria, alone or in combination with other anaerobes (particularly peptocdcci and peptostreptococci), were identified in 30 percent of the specimens. The antibiotic sensitivity profiles for aerobes and

anaerobes are compiled in Tables VI and VII. The strains isolated are generally very sensitive. Sulfonamide (average r = 38 percent) is weakly active against the tested strains. This is much more pronounced in the case of aerobes. Aminoglycosides showed the weakest activity of all through the resistance of anaerobic bacteria. Chloramphenicol was the only antibiotic active against all strains. No great differences existed in the sensitivity spectra of the other antibiotics. The resistance quotient for all tested strains was found to lie between 0.6 and 2.3 percent. One Bacteroides strain was shown to be sensitive only to chloramphenicol, erythromycin, and clindamycin. DISCUSSION

Anaerobic bacteria in dentogenous abscesses were isolated by Head and ROOS’ in 1919.Due to the difficulty of isolation, anaerobes were not often taken into consideration in the past. Moreover, results of bacteriologic tests showed a large number of sterile cultures. Examination of aerobically cultured dental abscessesin the Department of Maxillo-facial Surgery, University of Frankfurt, for the period 1977 to 1978. showed 29 percent sterile cultures. These results are congruent with current findings that indicate pure anaerobic cultures in 28 percent of cases.No negative culture was noted in any of the casesreported. It is particularly difficult to compare bacteriologic investigations because of the differing methods and materials used. Thus results from studies that only partially investigate the aerobic spectrum differ substantially from the currently submitted data. Previous studies that did not encompass anaerobic culture techniques invariably resulted in the predominant recovery of staphylococci and streptococci and an increase in gram-negative aerobic pathogens. Thus far, only relatively few filter studies performed by accurate aerobic and anaerobic cul-

Bacteriology of dentogenouspyogenic infections

Volume 52 Number 6

Table IV.

585

Spectrum of aerobic and anaerobic species Anaerobes

Aerobes Identification

I.P.’

of organism

Gram-positive cocci: Streptococci, not serologically grouped Alpha-hemolytic streptococci Beta-hemolytic streptococci Streptococci, serologically grouped: Streptococci, group A Streptococci, group C Streptococci, group G Enterococci (serologic group D) Gram-negative cocci: Neisseriae Gram-positive bacilli: Corynebacterium pseudodiphtheriticum Sporulating organisms Gram-negative bacilli: Haemophilus influenzae Gram-positive cocci: Streptococcus: S. intermedius S. constellatus Peptostreptococcus: P. anaerobius Peptococcus: P. prevotii P. magnus P. asaccharolyticus Gram-negative cocci: Veillonella: V. alcalescens Gram-positive bacilli: Eubacterium: E. lentum Propionibacterium: P. acnes Clostridia Undifferentiated Gram-negative bacilli: Bacteroides B. melaninogenicus B. mel. ss. asaccharolyticus B. mel. ss. intermedius B. corrodens B. oralis B. ruminicola Bacteroides undifferentiated Fusobacterium F. nucleatum F. varium F. necrophorum Fusobacterium undifferentiated Undifferentiated ‘I.P. = intraoral aspiration; E.P. = extraoral

16 1

E.P.*

I. P.

E.P.

44 35 33 2 8 1

17

0

2

1

1 0

0

1

Total

4 0

2 1

6

3

5 4 0

4 5 8

3

2

5

I

I 1 4

1 0 2

11 6 0 0 0 0 1

7 9 1 3 I 1 I

11 2 1 1 2

6 3 2 0 2

2 1 2 2 3 2 I 1 1 42 1 6 1 9 9 26 9 9 8 5 5 5 I5 6 6 2 2 1 6 71 41 18 15 1 3 I 1 2 26 7 5 3 1 4

aspiration.

ture techniques have been reported.3-s In addition, there are only two retrospective investigationsg-1o that include the anaerobic spectrum. The predominance of mixed aerobic-anaerobic cultures has been confirmed in all these studies. The

highest average pathogen count per abscess was shown to be 6.05,fiand the lowest 1.92.j The pathogen count of 3.66 in this current study coincides very well with the data of Chow and associates.”as well as with those of Sabiston and associates.* The

586

Aderhold, Knothe, and Frenkel

Table V.

Oral Surg. December, 1981

Bacterial combinations-doublet Aerobic s1reptococci

Aerobic streptococci Anaerobic streptococci Peptococci Peptostreptococci Veillonella Eubacterium Bacteroides Fusobacterium

combination

Anaerobic sireptococci

Peptococci

6

14 2

6 14 9

2 0

4

3 2 30 17

1 1 5 3

2 1 17 II

Table VI. Antibiotic aerobic strains No.

Percent

S*

MS*

Penicillin G/V Ampicillin Oxacillin Ticarcillin Azlocillin Mezlocillin Cephalothin Cefazolin Cefamandole Cefuroxime Cefoxitin Tetracycline Chloramphenicol Gentamicin Sisomicin Tobramycin Amikacin Erythromycin Clindamycin Sulfonamide

22 49 36 37 38 38 49 37 39 37 42 49 48 49 43 42 39 49 49 49

44 98 72 74 76 76 98 74 78 74 84 98 96 98 86 84 78 98 98 98

19 45 35 36 37 37 43 36 37 37 38 39 48 6 5 5 4 41 40 13

2 4 0 1 1 I 4 0 2 0 2 8 0 23 21 20 19 5 5 12

Eubacterium

Bacteroides

Fusobacterium

9

3

2

30

17

0

I

I

5

3

4

2 0

I I

17 8

11 5

0

4 6

3 2 18

0 I 8 5

sensitivity and resistance of

Antibiotic

Veillonellu

Peptostreptococci

0 4 3

6 2

18

Table VII. Antibiotic sensitivity and resistance of anaerobic strains

R*

Percent R

Antibiotic

No.

Percent

S*

1 0 I 0 0 0 2 1 0 0 2 2 0 20 17 17 16 3 4 24

4.6 0 2.8 0 0 0 4.1 2.1 0 0 4.8 4.1 0 40.8 39.5 40.5 41.0 6.1 8.2 49.0

Penicillin Ampicillin Oxacillin Ticarcillin Azlocillin Mezlocillin Cephalothin Cefazolin Cefamandole Cefuroxime Cefoxitin Tetracycline Chloramphenicol Gentamicin Sisomicin Tobramycin Amikacin Erythromycin Clindamycin Sulfonamide

56 130 103 104 118 118 114 104 122 122 119 130 130 129 105 105 104 129 129 129

43.1 100.0 79.2 80.0 90.8 90.8 87.7 80.0 93.9 93.9 91.5 100.0 100.0 99.2 80.8 80.8 80.8 99.2 99.2 99.2

56 126 102 103 115 117 112 103 121 119 117 127 130 0 0 0 I 123 129 66

MS* 0 2 0 0 2 0 1 0 0 1 1 2 0 0 0 0 0 5 0 18

R’ 0 2 1 1 I 1 1 I 1 2 1 1 0 129 105 105 103 I 0 45

Percent R 0 1.5 1.0 I.0 0.9 0.9 0.9 1.0 0.8 1.6 0.8 0.8 0 100.0 100.0 100.0 99.0 0.8 0 34.9

*S = sensitive; MS = moderately sensitive; R = resistant.

*S = sensitive; MS = moderately sensitive; R = resistant.

preponderance of anaerobic bacteria in mixed cultures was also shown by Chow and associates,” Bartlett and O’Keefe,” and Sabiston and associates.h With respect to the aerobic species found, every study, inclusive of the current one, has shown a predominance of microaerophilic, alpha-hemolytic streptococci. From 1977 to 1978 our laboratory aerobically isolated 9.8 percent gram-negative bacilli, whereas 2 percent, well below the previous figure, were cultured in the current investigation. Geiger and Graf,GBartlett and O’Keefe,” Chow and associates,l Sabiston and associates,” and Sims”’ were also able to culture a proportion up to 4 percent. Thus it does not appear, as noted in other medical

areas,that an increased proportion of aerobic gramnegative bacilli had occurred in dentogenous pyogenie infections. No staphylococci were isolated from the current samples reliably obtained from dentogenously derived abscesses.Sims’” could isolate only two staphylococcal strains from unequivocal dentogenous abscessesin 1,000 cases. It must therefore be concluded that the high proportion of staphylococci isolated in previous studies were commensals on the skin or were introduced by the collection technique used. This present low proportion of staphylococci has been confirmed by other investigators.:‘, 5.6 As for anaerobic strains, all studies mentioned note an

Volume 52 Number 6

extensive mixed flora. The dominant organisms are above all Bacteroides, fusobacterial, peptococcal, and peptostreptococcal species. There are no references in the literature concerning bacterial combinations. The results of the current study indicate a predisposition toward specific combinations. It is suspected that in the early phase of abscessformation an aerobic-anaerobic mixed infection is present wherein aerobic streptococci through consumption of oxygen prepare the medium for anaerobic bacteria. Pure anaerobic infections are produced in the late stage of abscessformation through overgrowth of anaerobes. The significance of individual pathogens in the inflammatory process is not yet clearly known. Though most of the bacteria in such mixed infections are not credited as pathogens themselves, they are in all probability meaningful for the pathogenicity of bacterial complexes. They contribute to the infectious milieu in the form of bacterial synergism. Bacteroides melaninogenicus appears to occupy a central position in this complex. Mucosa is the natural habitat for all isolated bacteria. Bacteria in mixed infections must be classified as facultative pathogens that endogenously become initiators of disease in the host only under special conditions. Currently conducted sensitivity tests indicate that the strains isolated are sensitive to most antibiotics. Sabiston and Grigsby” and Geiger and GrW also obtained similar results. On the basis of these data, penicillin, erythromycin, and, in particular clindamycin, which is highly effective against anaerobes, are recommended for ambulant oral therapy. An oral penicillin agent is recommended for antibiotic therapy in urgent situations. In cases of allergy, resistance to penicillin, or severe infections, clindamycin should be used. For parenteral therapy, the newer acyl-ureido-penicillins such as azlocillin, mezlocillin as well as piperacillin, can be used and, if necessary, in combination with clindamycin or aminoglycosides. Furthermore, successful treatment can be expected with the newest cephalosporins (cefuroxime, cefamandole, cefazolin, cefoxitin, cefotaxime). Surgical treatment must always be in the fore-

Bacteriology of dentogenouspyogenic infections 587 ground in the therapy of dentogenous abscesses. Decompression through incision prevents progressive liquefaction of tissue, migration of toxins, and thereby later scars with reduced function as well as residual foci of infection. The employment of antibiotics depends on the clinical presentation, and must be guided by a confirmed indication. Inadequate diagnoses and uncritical use of chemotherapy can mask the clinical picture, since important symptoms would be suppressed. Chemotherapy should be instituted when surgical modalities have failed, or a therapeutic success cannot be adequately ensured. REFERENCES 1. Aderhold, L.: Bakteriologische Diagnostik pyogener Infektionen im Kiefer-Gesichtsbereich, Dtsch. 2. Mund-Kiefer Ges. Chir. 3: 233-237, 1979. 2. Head, .I., and Roos, C.: On the Bacteriology of Apical Abscesses, J. Dent. Res. 1: 13, 1919. 3. Bartlett, J. G., and O’Keefe, P.: The Bacteriology of Perimandibular Space Infections, J. Oral Surg. 37: 407-409, 1979. 4. Chow, A. W., Roser, S. M., and Brady, F. A.: Orofacial Odontogenic Infections, Ann. Intern, Med. 88: 392-402, 1978. 5. Feldmann, G., and Larje, 0.: The Bacterial Flora of Submucous Abscesses Originating From Chronic Exacerbating Osteitis, Acta Odontol. Stand. 24: 129-145, 1966. 6. Geiger, S. A., and Graf, W.: Zur Problematik der bakteriolo&hen Diagnostik und gezielten Antibiotikatherapie bei nvoeenen Infektionen im Kiefer-Gesichtsbereich. Dtsch. yahiaerztl. Z. 33: 771-773. 1978. 7. Sabiston. C. B., and Gold, A. W.: Anaerobic Bacteria in Oral Infections, ORAL SURG. 38: 187-192, 1974. 8. Sabiston, C. B., Grigsby, W. R., and Segerstrom, N.: Bacterial Study of Pvoaenic infections Of Dental Origin, L. ORAL SURG. 4i: 430~i35: 1976. 9. Schuppan. K., Pape. H. D.. Schaal, K. P.. and Schuppan, I.: Ausldsende Ursachen und Erregerspektrum der unspezifischen Weichteilentztindung im Kiefer-Gesichtsbereich im Raum KBln, Dtsch. Zahnaerztl. Z. 33: 766-770, 1978. 10. Sims, W.: The Clinical Bacteriology of Purulent Oral Infections, Br. J. Oral Surg. 12: 1, 1974. 11. Sabiston, C. B.. and Grigsby. W. R.: The Microbiology of Dentalpyogenic Infections, Crit. Rev. Clin. Lab. Sci. 8: 213-240. 1977. Reprint requests to: Dr. Dr. L. Aderhold Department of Dental, Oral, and Maxillo-facial Johann Wolfgang Goethe University, Theodor-Stern-Kai 7 6000 Frankfurt am Main 70 (FRG) West Germany

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