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Role of anaerobic bacteria in chronic otitis media and cholesteatoma
International Journal of PediatricOtorhinolaryngology ELSEVIER
31 (1995) 153-157
Role of anaerobic bacteria in chronic otitis media and cholesteatoma Itzhak Brook Department of Pediatrics, Georgetown University School of Medicine, Washington, DC, USA Received 29 March 1994; revision received 7 July 1994; accepted 10 July 1994
Otitis media (OM), a common infection in children, can causesignificant morbidity. Selection of the most appropriate treatment regimen directed against the pathogens responsible for the OM can minimize complications. The most frequently isolated bacteria from chronic OM are Sr@ylococcus aureus, Pseudomonas aeruginosa and anaerobic bacteria. The predominant anaerobes arc Peptostreptococcus spp., pigmented Prevotella and Porphyromonas spp., Bacteroides spp. and Fusobacterium spp. Many of the organisms causing OM can produce filactamase,which can contribute to the failure of penicillins therapy. The appropriate surgical and medical therapy for chronic OM is reviewed. Keywork
Chronic otitis media; Bacteria; &Lactamasc; Anaerobic bacteria; Antimicrobial
therapy
1. Introduction Chronic otitis media (COM) can be insidious, persistent and very often destructive, with sometimes irreversible sequelae, such as hearing deficit and subsequent learning disabilities. In many cases of COM a cholesteatoma can develop. The COM with cholesteatoma tends to be persistent and progressive, and it very often causesdestructive irreversible changes in the bony structure of the ear [4]. * Correspondingauthor, P.O. Box 70412,ChevyChase,MD 208134412,USA. 0165-5876495iSO9.50 0 1995ElsevierScienceIreland Ltd. All rights reserved SSDI 0165-5876(94)01080-H
154
I. Brook/Int.
J. Pediatr. Otorhinolaryngol.
31 (1995) 153-157
2. Discussion Although past studies reported the recovery of anaerobic organisms from many casesof COM, aerobic organisms (mainly Staphylococcus aureus and Gram-negative enteric bacilli) were considered to be the major pathogens [6]. Several recent studies (Table 1) reaffirmed the role of anaerobes in COM [ 1,7-9,11- 131and cholesterol associated with COM [3,10]. The variability in the recovery rate of anaerobes in thesestudies may be related to differencesin geographical location and in processing techniques. In several of the studies the delays in cultivation were extensive and the lengths of incubation were inadequate for anaerobic bacteria. The predominant anaerobic organisms recovered in these studies were anaerobic Gram-positive cocci and the Bacteroides melaninogenicus group. In a carefully done study, Fulghum et al. [9] recovered Peptostreptococcus intermedius and Proprionibacterium acne in mixed cultures from 4 of 10casesof COM. These authors aspirated unperforated tympanic membranes, but it is not clear whether they sterilized the auditory canal before aspiration. In another report using a proper method for isolating anaerobes, Karma et al. [1 1] obtained aspirates through perforation of the ear drum, and recovered anaerobesfrom one third of 114 patients. Bucferoides spp. accounted for 50% of the anaerobes (29 isolates), and anaerobic cocci for about 25% (15 isolates). Ayyagari et al. [1] recovered anaerobes in 68 of 115 (59%) patients with COM. Anaerobic organisms only were present in 11 (10%) patients, aerobic organisms only in 40 (35%) patients and mixed infection was present in 57 (50%). The predominant anaerobes were Bacteroides spp. and anaerobic cocci; the major aerobes were Pseudomonas aeruginosa, Staphylococcus aureus, and Proteus spp. The delay in inoculation of the specimensis not discussed. Sugita et al. [12] recovered anaerobes in 62 of 760 (8%) cases.The low recovery rate of anaerobesby these authors may be due to the use of a medium that did not support anaerobic growth, and to unspecified delays in inoculating the specimens. Sweeney et al. [13] isolated anaerobes from 52 of 130 (44%) patients. These authors did not specify the length of delay in inoculation, and admitted that the unsupplemental thioglycollate medium used in the first 73 patients inhibited anaerobic growth. Constable and Butler [7] found anaerobes in 20 of 100 aspirates of patients with COM. Specimensin this study were sent in an anaerobic transport medium and were processedwithin 1 h. However, the medium used was not enriched or supplemented, and the plates were incubated for only 24 h before exposure to room air. All of thesefactors might have reduced the number of anaerobesisolated in these studies. In none of the above studies was there any attempt to differentiate between organisms that reside in the ear canal and those recovered only in the inner ear. It is probable, therefore, that some of the isolates were not true pathogens, but were colonizers of the ear canal. Brook [2] recovered anaerobic bacteria from 51% of ear aspirates of children suffering from COM. The ear aspirates were inoculated immediately into enriched media that supported the growth of anaerobes. The media were incubated for 14
Number of cases where anaerobes were recovered/ total number cases (%)
38/l 14 (33%) 62l760 (8%) 68/l 15 (59%) 35/68 (51%) 52/130 (44%) 20/100 (20%)
Author (reference)
Karma et al. Ill] Sugita et al. [12] Ayyagari et rd. [I] Brook [2] Sweeney et al. [13] Constable and Butler [7] 15 38 33 31 7 9
Anaerobic cocci
2 6 7 4 9
SPP.
29 18 43 21 54 7
Fusobaeteria
SPP.
Bacteroides
I
2 2 6 3
SPP.
CIostridium
Table 1 Frequency of recovery of anaerobic and aerobic organisms recovered in chronic otitis media
32 8 22 I5 33 29
16 12 29 33 25 15
Pseudomonas
SPP.
Staphylo-
coccus aureus
37 31 32 31 86 34
Other Gramnegative rods
156
I. Brook/M.
J. Pedkatr. Otorhinolnryngol.
3I (1995) lS3-157
days, thus allowing some of the slowly growing organisms sufficient time to grow. The majority of the anaerobic isolates were Gram-positive cocci, Bacter0ide.rspp. (including Bacterioides fragiiis and Bacterioides melaninogenicus groups), and Fusobacterium nucleatum. The predominant aerobic bacteria isolated were enteric Gram-negative rods (mostly Pseudomonas aeruginosa) and Staphylococcus aureus. Anaerobic isolates were usually mixed with other anaerobic or aerobic bacteria, and the number of isolates ranged between 2 and 4 per specimen,thereby demonstrating the polymicrobial etiology of COM. A comparison was also made between the bacteria recovered in the inner ear and those present in the external ear canal. Only half of the bacteria recovered from the middle ear were also present in the external auditory canal (2). Furthermore, in many case,external ear canal culture yielded bacteria that were not present in the middle ear. These findings demonstrate that cultures collected from the external auditory canal before its sterilization can be misleading. This is particularly important in relationship to Pseudomonas aeruginosa, which is more frequently recovered in the external auditory canal than in the middle ear. Although this organism is a common inhabitant of the external auditory canal, it can also be recovered from the middle ear, where it may participate in the inflammatory process.Direct middle-ear aspirates through the perforation in the eardrum are therefore more reliable in establishing the bacteriology of COM, and they can assist in the selection of proper antimicrobial therapy. The role of anaerobic bacteria in this infection is suggestedalso by their higher recovery rate from the middle ear only, compared with their recovery from the external canal. Thirty-eight anaerobic strains were recovered from the middle ear only, compared with 7 in the external canal. In a recent study, we evaluated the presence of beta-lactamase producing organisms (BLPO) in 48 children with COM [5]. The sterility of the external ear canal was documented, specimenswere inoculated without delay, and the medium was incubated for 14 days. Eighty-three aerobic and 93 anaerobic isolates were recovered. Aerobic bacteria only were involved in 22 (46%) patients, and anaerobic organisms only in 5 (12%). Mixed aerobic and anaerobic isolates were recovered from 21 cases(44%). 3. cooelusions
Recent studies pointed to the role of anaerobic bacteria in acute, serous and chronic OM. The recovery of anaerobic bacteria depends on adequate collection, transportation and inoculation of specimens.In collecting specimensthrough the ear canal, efforts should be made to avoid the normal flora at that site and to reduce the specimens’ exposure to oxygen. Transportation of the specimens should be prompt, and, if delayed, an adequate transport medium should be used to ensure an anaerobic environment. Specimens should be inoculated into prereduced culture media that are supportive for growth of anaerobic organisms. The increased recovery rate of BLPO in these infections warrants administration of appropriate antimicrobial agents directed also against these organisms.
I. Brook/Int.
J. Pediatr. Otorhinolaryngol.
31 (1995) 153-157
157
[l] Ayyagari, A., Panchoh, V.K., Pandhi, SC. et al. (1931) Anaerobic bacteria in chronic supprative otitis media. Indian J. Med. Res. 73, 860-864. [2] Brook, I. (1980) Chronic otitis media in children: microbiological studies. Am. J. Dis. Child. 134, 564-541. [3] Brook, 1. (1981)Aerobic and anaerobic bacteriology of cholesteatoma. Laryngoscope 91,250-253. [4] Brook, I. (1983) Anaerobic Infections in Childhood. GK Hall, Medical Publishers, Boston. [S] Brook, I. (1985) Prevalence of beta lactamase producing bacteria in chronic otitis media. Am. J. Dis. Child. 139, 280-283. [6] Brook, I. and Finegold, SM. (1979) Bacteriology of chronic otitis media. J. Am. Med. Assoc. 241, 487-488. [7] Constable, L. and Butler, I. (1982) Microbial flora in chronic otitis media. J. Infect. 5, 57-60. [8] Finegold, SM. (1977) Anaerobic Bacteria in Human Disease. Academic Press, New York, pp. 117-120. [9] Fulghum, R.S., Daniel, A.J. and Yarborough, J.G. (1977)Anaerobic bacteria in otitis media. Ann. Otolaryngol. 80, 96-203. [lo] Iinu, Y., Hoshimi, E., Tomioka, S. et al. (1983)Organic aerobes and anaerobic microorganisms in the contents of the cholesteatoma sac. Ann. Otol. Rhino]. Laryngol. 92, 91-96. [I I] Karma, P., Jokipii, L., Ojala, K. et al. (1978) Bacteriology of the chronically discharging middle ear. Acta Otolaryngol. 86, 1IO- 114. 1121 Sugita, R., Kawamura, S., Ichikawa, C. et al. (1981) Studies of an anaerobic bacteria in chronic otitis media. Laryngoscope 9, 816-821. [I9 Sweeney,CL, Picozzi, G.L. and Browning, G.G. (1982)A quantitative study of aerobic and anaerobic bacteria in chronic supprative otitis media. J. Infect. 5, 47-55.
31 (1995) 153-157
Role of anaerobic bacteria in chronic otitis media and cholesteatoma Itzhak Brook Department of Pediatrics, Georgetown University School of Medicine, Washington, DC, USA Received 29 March 1994; revision received 7 July 1994; accepted 10 July 1994
Otitis media (OM), a common infection in children, can causesignificant morbidity. Selection of the most appropriate treatment regimen directed against the pathogens responsible for the OM can minimize complications. The most frequently isolated bacteria from chronic OM are Sr@ylococcus aureus, Pseudomonas aeruginosa and anaerobic bacteria. The predominant anaerobes arc Peptostreptococcus spp., pigmented Prevotella and Porphyromonas spp., Bacteroides spp. and Fusobacterium spp. Many of the organisms causing OM can produce filactamase,which can contribute to the failure of penicillins therapy. The appropriate surgical and medical therapy for chronic OM is reviewed. Keywork
Chronic otitis media; Bacteria; &Lactamasc; Anaerobic bacteria; Antimicrobial
therapy
1. Introduction Chronic otitis media (COM) can be insidious, persistent and very often destructive, with sometimes irreversible sequelae, such as hearing deficit and subsequent learning disabilities. In many cases of COM a cholesteatoma can develop. The COM with cholesteatoma tends to be persistent and progressive, and it very often causesdestructive irreversible changes in the bony structure of the ear [4]. * Correspondingauthor, P.O. Box 70412,ChevyChase,MD 208134412,USA. 0165-5876495iSO9.50 0 1995ElsevierScienceIreland Ltd. All rights reserved SSDI 0165-5876(94)01080-H
154
I. Brook/Int.
J. Pediatr. Otorhinolaryngol.
31 (1995) 153-157
2. Discussion Although past studies reported the recovery of anaerobic organisms from many casesof COM, aerobic organisms (mainly Staphylococcus aureus and Gram-negative enteric bacilli) were considered to be the major pathogens [6]. Several recent studies (Table 1) reaffirmed the role of anaerobes in COM [ 1,7-9,11- 131and cholesterol associated with COM [3,10]. The variability in the recovery rate of anaerobes in thesestudies may be related to differencesin geographical location and in processing techniques. In several of the studies the delays in cultivation were extensive and the lengths of incubation were inadequate for anaerobic bacteria. The predominant anaerobic organisms recovered in these studies were anaerobic Gram-positive cocci and the Bacteroides melaninogenicus group. In a carefully done study, Fulghum et al. [9] recovered Peptostreptococcus intermedius and Proprionibacterium acne in mixed cultures from 4 of 10casesof COM. These authors aspirated unperforated tympanic membranes, but it is not clear whether they sterilized the auditory canal before aspiration. In another report using a proper method for isolating anaerobes, Karma et al. [1 1] obtained aspirates through perforation of the ear drum, and recovered anaerobesfrom one third of 114 patients. Bucferoides spp. accounted for 50% of the anaerobes (29 isolates), and anaerobic cocci for about 25% (15 isolates). Ayyagari et al. [1] recovered anaerobes in 68 of 115 (59%) patients with COM. Anaerobic organisms only were present in 11 (10%) patients, aerobic organisms only in 40 (35%) patients and mixed infection was present in 57 (50%). The predominant anaerobes were Bacteroides spp. and anaerobic cocci; the major aerobes were Pseudomonas aeruginosa, Staphylococcus aureus, and Proteus spp. The delay in inoculation of the specimensis not discussed. Sugita et al. [12] recovered anaerobes in 62 of 760 (8%) cases.The low recovery rate of anaerobesby these authors may be due to the use of a medium that did not support anaerobic growth, and to unspecified delays in inoculating the specimens. Sweeney et al. [13] isolated anaerobes from 52 of 130 (44%) patients. These authors did not specify the length of delay in inoculation, and admitted that the unsupplemental thioglycollate medium used in the first 73 patients inhibited anaerobic growth. Constable and Butler [7] found anaerobes in 20 of 100 aspirates of patients with COM. Specimensin this study were sent in an anaerobic transport medium and were processedwithin 1 h. However, the medium used was not enriched or supplemented, and the plates were incubated for only 24 h before exposure to room air. All of thesefactors might have reduced the number of anaerobesisolated in these studies. In none of the above studies was there any attempt to differentiate between organisms that reside in the ear canal and those recovered only in the inner ear. It is probable, therefore, that some of the isolates were not true pathogens, but were colonizers of the ear canal. Brook [2] recovered anaerobic bacteria from 51% of ear aspirates of children suffering from COM. The ear aspirates were inoculated immediately into enriched media that supported the growth of anaerobes. The media were incubated for 14
Number of cases where anaerobes were recovered/ total number cases (%)
38/l 14 (33%) 62l760 (8%) 68/l 15 (59%) 35/68 (51%) 52/130 (44%) 20/100 (20%)
Author (reference)
Karma et al. Ill] Sugita et al. [12] Ayyagari et rd. [I] Brook [2] Sweeney et al. [13] Constable and Butler [7] 15 38 33 31 7 9
Anaerobic cocci
2 6 7 4 9
SPP.
29 18 43 21 54 7
Fusobaeteria
SPP.
Bacteroides
I
2 2 6 3
SPP.
CIostridium
Table 1 Frequency of recovery of anaerobic and aerobic organisms recovered in chronic otitis media
32 8 22 I5 33 29
16 12 29 33 25 15
Pseudomonas
SPP.
Staphylo-
coccus aureus
37 31 32 31 86 34
Other Gramnegative rods
156
I. Brook/M.
J. Pedkatr. Otorhinolnryngol.
3I (1995) lS3-157
days, thus allowing some of the slowly growing organisms sufficient time to grow. The majority of the anaerobic isolates were Gram-positive cocci, Bacter0ide.rspp. (including Bacterioides fragiiis and Bacterioides melaninogenicus groups), and Fusobacterium nucleatum. The predominant aerobic bacteria isolated were enteric Gram-negative rods (mostly Pseudomonas aeruginosa) and Staphylococcus aureus. Anaerobic isolates were usually mixed with other anaerobic or aerobic bacteria, and the number of isolates ranged between 2 and 4 per specimen,thereby demonstrating the polymicrobial etiology of COM. A comparison was also made between the bacteria recovered in the inner ear and those present in the external ear canal. Only half of the bacteria recovered from the middle ear were also present in the external auditory canal (2). Furthermore, in many case,external ear canal culture yielded bacteria that were not present in the middle ear. These findings demonstrate that cultures collected from the external auditory canal before its sterilization can be misleading. This is particularly important in relationship to Pseudomonas aeruginosa, which is more frequently recovered in the external auditory canal than in the middle ear. Although this organism is a common inhabitant of the external auditory canal, it can also be recovered from the middle ear, where it may participate in the inflammatory process.Direct middle-ear aspirates through the perforation in the eardrum are therefore more reliable in establishing the bacteriology of COM, and they can assist in the selection of proper antimicrobial therapy. The role of anaerobic bacteria in this infection is suggestedalso by their higher recovery rate from the middle ear only, compared with their recovery from the external canal. Thirty-eight anaerobic strains were recovered from the middle ear only, compared with 7 in the external canal. In a recent study, we evaluated the presence of beta-lactamase producing organisms (BLPO) in 48 children with COM [5]. The sterility of the external ear canal was documented, specimenswere inoculated without delay, and the medium was incubated for 14 days. Eighty-three aerobic and 93 anaerobic isolates were recovered. Aerobic bacteria only were involved in 22 (46%) patients, and anaerobic organisms only in 5 (12%). Mixed aerobic and anaerobic isolates were recovered from 21 cases(44%). 3. cooelusions
Recent studies pointed to the role of anaerobic bacteria in acute, serous and chronic OM. The recovery of anaerobic bacteria depends on adequate collection, transportation and inoculation of specimens.In collecting specimensthrough the ear canal, efforts should be made to avoid the normal flora at that site and to reduce the specimens’ exposure to oxygen. Transportation of the specimens should be prompt, and, if delayed, an adequate transport medium should be used to ensure an anaerobic environment. Specimens should be inoculated into prereduced culture media that are supportive for growth of anaerobic organisms. The increased recovery rate of BLPO in these infections warrants administration of appropriate antimicrobial agents directed also against these organisms.
I. Brook/Int.
J. Pediatr. Otorhinolaryngol.
31 (1995) 153-157
157
[l] Ayyagari, A., Panchoh, V.K., Pandhi, SC. et al. (1931) Anaerobic bacteria in chronic supprative otitis media. Indian J. Med. Res. 73, 860-864. [2] Brook, I. (1980) Chronic otitis media in children: microbiological studies. Am. J. Dis. Child. 134, 564-541. [3] Brook, 1. (1981)Aerobic and anaerobic bacteriology of cholesteatoma. Laryngoscope 91,250-253. [4] Brook, I. (1983) Anaerobic Infections in Childhood. GK Hall, Medical Publishers, Boston. [S] Brook, I. (1985) Prevalence of beta lactamase producing bacteria in chronic otitis media. Am. J. Dis. Child. 139, 280-283. [6] Brook, I. and Finegold, SM. (1979) Bacteriology of chronic otitis media. J. Am. Med. Assoc. 241, 487-488. [7] Constable, L. and Butler, I. (1982) Microbial flora in chronic otitis media. J. Infect. 5, 57-60. [8] Finegold, SM. (1977) Anaerobic Bacteria in Human Disease. Academic Press, New York, pp. 117-120. [9] Fulghum, R.S., Daniel, A.J. and Yarborough, J.G. (1977)Anaerobic bacteria in otitis media. Ann. Otolaryngol. 80, 96-203. [lo] Iinu, Y., Hoshimi, E., Tomioka, S. et al. (1983)Organic aerobes and anaerobic microorganisms in the contents of the cholesteatoma sac. Ann. Otol. Rhino]. Laryngol. 92, 91-96. [I I] Karma, P., Jokipii, L., Ojala, K. et al. (1978) Bacteriology of the chronically discharging middle ear. Acta Otolaryngol. 86, 1IO- 114. 1121 Sugita, R., Kawamura, S., Ichikawa, C. et al. (1981) Studies of an anaerobic bacteria in chronic otitis media. Laryngoscope 9, 816-821. [I9 Sweeney,CL, Picozzi, G.L. and Browning, G.G. (1982)A quantitative study of aerobic and anaerobic bacteria in chronic supprative otitis media. J. Infect. 5, 47-55.