Effects of antimicrobial therapy on the microbial flora of the adenoids

Itzhak Brook*

Department of Pediatrics, Georgetown University School of Medicine, 4431 Albemarle St. NW, Washington, DC 20016, USA


    Abstract
 Top
 Abstract
 Introduction
 Bacterial interference
 Microbiology of the adenoids
 Similarities and differences in...
 Production of ß...
 Effect of antimicrobials on...
 Therapeutic implications
 References
 
The core of the adenoids contains polymicrobial aerobic and anaerobic flora and also includes potential respiratory pathogens. Similar flora, although in higher numbers and with a higher frequency of pathogens, are found in inflamed or hypertrophic adenoids and many of these bacteria are resistant to antimicrobial agents. Exposure to antimicrobial therapy can alter the colonization patterns and select for resistant organisms. Production of ß-lactamase is one of the major mechanisms of resistance of these organisms. The adenoids of healthy individuals, in contrast to those with recurrent respiratory tract infections, are generally colonized by aerobic and anaerobic organisms that are capable of interfering with the growth of potential pathogens. Maintaining the beneficial effects of normal flora by avoiding unnecessary exposure to antimicrobial therapy may be a useful tool in preventing colonization of the adenoids by potential pathogens. This review discusses the unique microbiology of the adenoids in individuals with a variety of pathological conditions, the interactions between the various organisms and the effects of antimicrobial therapy on the microbial flora of the adenoids.

Keywords: adenoid, anaerobes, interference, Haemophilus, Streptococcus


    Introduction
 Top
 Abstract
 Introduction
 Bacterial interference
 Microbiology of the adenoids
 Similarities and differences in...
 Production of ß...
 Effect of antimicrobials on...
 Therapeutic implications
 References
 
The adenoids are believed to play a role in several infectious and non-infectious upper airway illnesses. They are implicated in the aetiology of otitis media,16 rhinosinusitis,1,4,7,8 adenotonsillitis9 and chronic nasal obstruction.10,11

The core of the adenoids in healthy children contains polymicrobial aerobic and anaerobic flora and also includes potential respiratory pathogens.9,12 The nasopharynx and adenoids of healthy individuals in contrast to those with recurrent respiratory tract infections are also generally colonized by aerobic and anaerobic organisms that are capable of interfering with the growth of potential pathogens.1315

The number of bacteria in the adenoid tissue in healthy children varies between 103 and 106 organisms per gram.16 The aerobic and anaerobic organisms isolated from ‘normal’ adenoids are similar to those recovered from the cores of ‘normal’ tonsils17 and the number of anaerobic bacteria exceeds the number of aerobic bacteria in a ratio of 100 to 1. Similar polymicrobial flora, although in higher numbers and with a higher frequency of pathogens, are found in inflamed or hypertrophic adenoids and many of these bacteria are resistant to antimicrobial agents.16 Exposure to antimicrobial therapy can alter the colonization patterns and select for resistant organisms.18,19

This review discusses the unique microbiology of the adenoids in individuals with a variety of pathological conditions, the interactions between the various organisms and the effects of antimicrobial therapy on the microbial flora of the adenoids.


    Bacterial interference
 Top
 Abstract
 Introduction
 Bacterial interference
 Microbiology of the adenoids
 Similarities and differences in...
 Production of ß...
 Effect of antimicrobials on...
 Therapeutic implications
 References
 
Competitive interactions between microorganisms take place in the process of the colonization of mucous membranes, as well as in clinical infections. Bacteria interact with each other when they attempt to establish themselves and dominate their environment.20 Some of these interactions are synergic whereas others are antagonistic, as organisms can interfere with each other’s growth and compete for their ecological space. Bacterial interference (BI) may play a major role in the maintenance of the normal flora of skin and mucous membranes, by preventing invasion by potentially exogenous pathogens. This may be one of the important mechanisms that prevent certain infectious diseases.

BI is expressed through several mechanisms. These include the production of antagonistic substances, changes in the bacterial microenvironment and reduction of needed nutritional substances.20,21 The mediators of BI vary and include the production of complex materials such as bacteriocins, bacteriophages or bacteriolytic enzymes, and less complex molecules such as hydrogen peroxide, lactic or fatty acids and ammonia.20,21

The nasopharynx and adenoids of healthy individuals are generally colonized by relatively non-pathogenic aerobic and anaerobic organisms,14 some of which possess the ability to interfere with the growth of potential pathogens.13,15 These organisms include the aerobic {alpha}-haemolytic streptococci (AHS, mostly Streptococcus mitis and Streptococcus sanguis),22 anaerobic streptococci (Peptostreptococcus anaerobius) and Prevotella melaninogenica.23 Conversely, nasopharyngeal and adenoidal carriage of potential upper respiratory tract pathogens such as Streptococcus pneumoniae, Haemophilus influenzae and Moraxella catarrhalis increases significantly in otitis media-prone (OMP) children and in the general population of young children during respiratory illness.24 The presence of organisms with interfering potential in the nasopharynx and adenoids may play a role in the prevention of upper respiratory tract infections.

Clinical evidence for BI

In a study to determine the quantitative nasopharyngeal bacteriology of AHS and non-typeable H. influenzae in 34 OMP and 25 non-OMP children, Bernstein et al.22 recovered a significantly greater number of AHS in the adenoids of non-OMP children compared with OMP ones. In contrast, they concomitantly recovered a higher number of H. influenzae isolates in the OMP group compared with the non-OMP one. These findings suggest the potential protective nature of AHS in the prevention of otitis media.

A recent study compared the isolation rate of potential pathogens and aerobic and anaerobic interfering bacteria in the adenoids of 25 OMP children with their isolation in 25 non-OMP children who had elective adenoidectomy.25 Twenty-seven potential pathogens were isolated from OMP children and 10 were recovered from the non-OMP children (P < 0.05). BI was noted in 71 instances against four potential pathogens (H. influenzae, M. catarrhalis, S. pneumoniae and Streptococcus pyogenes) by 26 normal flora isolates that were recovered from the OMP group, and in 193 instances by 63 isolates from the non-OMP group (P < 0.05). These interfering organisms included {alpha}- and non-haemolytic streptococci, Prevotella spp. and Peptostreptococcus spp. These data indicate that the adenoids of OMP children contain fewer organisms with interfering capability and more potential pathogens compared with non-OMP children.

Effect of antimicrobial therapy on BI

Administration of antimicrobials can influence the composition of nasopharyngeal and adenoid bacterial flora.18 Members of the oral flora with interfering capability (e.g. aerobic and anaerobic streptococci as well as penicillin-susceptible Prevotella spp.) are generally susceptible to amoxicillin. All of these members of the oral flora are relatively resistant to second- and third-generation cephalosporin therapy.

The effect of antimicrobial therapy with amoxicillin or a second-generation cephalosporin (cefprozil) on the bacterial flora of the adenoids was recently studied.26 Sixty children scheduled for elective adenoidectomy because of recurrent otitis media (ROM) were randomized prior to surgery into three groups of either no therapy, or 10 days of either amoxicillin or cefprozil therapy. Core adenoid materials were quantitatively cultured for aerobic and facultative bacteria. The number of organisms in adenoids obtained from patients treated with either antibiotic was reduced compared with controls. However, a significant decline in the number of interfering AHS occurred only in patients treated with amoxicillin. In contrast, no change was noted in the frequency of recovery of interfering AHS in those treated with cefprozil. This study showed that some antimicrobials can have a selective activity against ‘protective’ members of the oral flora and reduce their number. Their use may leave the adenoids more susceptible to colonization by potential pathogens.


    Microbiology of the adenoids
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 Abstract
 Introduction
 Bacterial interference
 Microbiology of the adenoids
 Similarities and differences in...
 Production of ß...
 Effect of antimicrobials on...
 Therapeutic implications
 References
 
Adenoids are liable to inflammatory changes and frequently are infected concomitantly with the tonsils. Acute adenoiditis may occur alone or in association with rhinitis or tonsillitis. Chronic adenoiditis may result from repeated acute attacks or from persistent infection. Adenoid hypertrophy is defined as an enlargement of the adenoids, which may be simple or inflammatory, and the symptoms may be referable to hypertrophy, infection or both. Recurrent adenotonsillitis is often a bacterial–viral illness. The common causative viruses are adenoviruses and Epstein–Barr virus.27

Establishing the unique microbiology of the adenoids of individuals with a variety of pathological conditions is of importance, as it can assist in their management. Several studies have explored the aerobic bacterial microbiology of the adenoids,9,12,16,2832 and only a few studies have investigated the role of anaerobic bacteria in the adenoids.9,16

Microbiologically, patients with inflamed adenoids of any aetiology harbour an abnormal microflora. The flora generally contains >105 organisms/g of adenoid tissue and between two and five bacterial species that are often associated with head and neck infections (i.e. S. pyogenes, Staphylococcus aureus, H. influenzae and S. pneumoniae).12,29 Especially noticeable is the higher prevalence of H. influenzae in patients with chronic adenotonsillitis compared with those with adenoid hypertrophy.9,12,16,2832

Brook9 has compared the aerobic and anaerobic bacteriology of the core of adenoids from 18 children with chronic adenotonsillitis with those recovered from 12 children with adenoid hypertrophy. Mixed flora was obtained from all patients (average of 7.8 isolates, 4.6 anaerobes and 3.2 aerobes/specimen). The predominant anaerobes in both groups were Gram-negative bacilli, Fusobacteria, and peptostreptococci and the main aerobes were {alpha}-, {gamma}- and ß-haemolytic streptococci, S. aureus, S. pneumoniae and Haemophilus spp. ß-Lactamase producing bacteria (BLPB) were more frequently isolated in children with chronic adenotonsillitis. Fearon et al.28 studied the aerobic and anaerobic bacteriology of the adenoids of 10 children with adenoid hypertrophy and 29 children with chronic adenoiditis. The most common isolates were: H. influenzae, diphtheroids, Neisseria spp., and {alpha}- and {gamma}-haemolytic streptococci. No differences were detected either in organism distribution or in total counts in chronic adenoiditis compared with adenoid hypertrophy. Pillsbury et al.29 evaluated the levels of aerobic and anaerobic bacteria per gram in adenoids removed from 48 patients (seven patients had obstruction alone, 17 chronic serous otitis media and 24 recurrent suppurative otitis media). Using the criterion that >105 organisms/g of tissue constitutes infection, they found that 83% of patients in the recurrent suppurative otitis media group had infected adenoids, as opposed to only 15% in the first and second groups combined.

Brook et al.16 determined the qualitative and quantitative aerobic and anaerobic microbiology of core adenoid tissue obtained from four groups of 15 children each: with ROM, recurrent adenotonsillitis (RAT), obstructive adenoid hypertrophy (OAH), and occlusion or speech abnormalities (controls).

Polymicrobial aerobic–anaerobic flora were present in all instances. The predominant aerobes in all groups were {alpha}- and {gamma}-haemolytic streptococci, H. influenzae, S. aureus, S. pyogenes and M. catarrhalis. The main anaerobes were Peptostreptococcus, Prevotella and Fusobacterium spp. The number and distribution of types of most organisms did not vary among the three groups of diseased adenoids but was higher than the control group (>106/g). However, the number of all organisms, the potential pathogens and BLPB was lower in the control than the diseased adenoids (P < 0.001). The study highlights the importance of the bacterial load in the adenoids in contributing to the aetiology of ROM, RAT and OAH. The presence of normal flora devoid of pathogens (seen in two-thirds of the ‘normal’ adenoids) may prevent colonization with potential pathogens and subsequent infection.

Several studies9,12,16,2832 found H. influenzae to be a predominant colonizer of adenoids, with similar rates of isolation and bacterial load in ROM, RAT or OAH. A high rate of colonization with this organism was also reported in hypertrophic33 and recurrently infected tonsils.34 These data indicate that H. influenzae, as well as other organisms, may play a role in the development of hypertrophic adenoids.

Brodsky & Koch30 correlated the qualitative and quantitative aerobic flora with clinical presentation in 69 children undergoing adenoidectomy for OAH or chronic adenoid infection and in 16 adenoid core biopsy specimens from 16 non-diseased controls. Only a quarter of the controls harboured potential pathogens, compared with about half of the other adenoids. H. influenzae was found in about half of the diseased adenoids compared with only 19% in the controls (P < 0.05).

Suzuki et al.31 isolated H. influenzae and S. aureus more frequently in adenoids of patients with otitis media with effusion (OME) than in those without this condition. Lee & Rosenfeld32 correlated sinonasal symptoms in 84 children that had adenoidectomy with the prevalence of bacterial pathogens in the adenoid core. One or more bacterial pathogens were recovered from all adenoids, with a concentration >105 organisms/g in 31 specimens (26%). A high number of pathogens (e.g. H. influenzae, S. pyogenes and S. aureus) was significantly correlated with sinonasal infection symptoms.


    Similarities and differences in the bacteriology of adenoids and tonsils
 Top
 Abstract
 Introduction
 Bacterial interference
 Microbiology of the adenoids
 Similarities and differences in...
 Production of ß...
 Effect of antimicrobials on...
 Therapeutic implications
 References
 
Adenoids are liable to inflammatory changes and frequently are infected concomitantly with the tonsils. Similarities and differences exist in individuals between the bacteriology of recurrently inflamed adenoids and tonsils.12,35

DeDio et al.12 investigated the tonsil and adenoid flora of 50 children undergoing tonsillectomy and adenoidectomy for either recurrent infection or airway obstruction. The most common isolates found in similar distribution in all patients were AHS, Neisseria, Haemophilus, S. aureus and Corynebacteria. Isolates from the tonsils and adenoids were similar in number and frequency. Three-quarters of the patients shared a common pathogen in tonsil and adenoid tissue. Haemophilus was recovered in 54% of patients and S. aureus in 46%.

Brook & Shah investigated the microbiology of the adenoids and tonsils removed from 25 children, with a history of recurrent group A ß-haemolytic streptococci (GABHS) adenotonsillitis.33 Mixed flora was present in all instances with an average of 9.1 isolates/specimen (Table 1). The predominant aerobes were Streptococcus spp., H. influenzae, GABHS, and the prevalent anaerobes were Peptostreptococcus, Prevotella and Fusobacterium spp. BLPB were recovered from 22 (88%) tonsils and from 21 (84%) adenoids.


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Table 1.  Predominant organisms isolated from the core of excised tonsils and adenoids from 25 children25
 
Discrepancies in the recovery of organisms were found between the tonsils and adenoids. Of the aerobes, 18% were only isolated in tonsils and 18% only in adenoids. Of the anaerobes, 20% were found only in tonsils and 26% only in adenoids. In the case of GABHS, concordance between adenoids and tonsils was only present in four instances; five were only found in adenoids and four only in tonsils (Table 1). These findings demonstrate the polymicrobial aerobic–anaerobic flora in both adenoids and tonsils, and the discrepancies in recovery of pathogens such as GABHS. The adenoids may serve as a potential source of tonsillitis due to this organism.


    Production of ß-lactamase
 Top
 Abstract
 Introduction
 Bacterial interference
 Microbiology of the adenoids
 Similarities and differences in...
 Production of ß...
 Effect of antimicrobials on...
 Therapeutic implications
 References
 
Brook et al.16 found significant differences in the presence of aerobic and anaerobic BLPB in different types of patients. These organisms were present in 83% of patients with chronic adenotonsillitis compared with 25% in those with OAH. This could be the result of selective pressure of repeated antimicrobial therapy given to these patients.

Karlidag et al.34 investigated the relationship between the resistant bacteria in the adenoid tissue and the middle ear effusion of children who underwent myringotomy and adenoidectomy with the diagnosis of OME. H. influenzae, S. pneumoniae and M. catarrhalis were isolated from 71% (29/41) of adenoids of the study group and 48% (20/41) of the controls (P < 0.01). BLPB were found in 48% (20/41) of the study group and 16% (4/25) of the controls (P < 0.05). Bacterial growth was observed in 29% (9/31) of the middle ear cultures of the study group and resistant bacteria were isolated in 78% (7/9). The same pathogens that were recovered in the middle ear cultures were also present in the adenoid tissue cultures. The isolation of resistant bacteria in most of the adenoid tissue samples of the children with OME, suggests the possible role of these bacteria in the development of OME.

The existence of BLPB within the adenoid core may explain the persistence of many pathogens where they may be shielded from the activity of penicillins. The disappearance of these bacteria from the nasopharyngeal flora between episodes of infection may be only temporary, and their reappearance may be due to their re-emergence from the core of adenoids or tonsils.35 The chronically infected adenoids may also be a factor in the recurrence of middle ear disease by causing Eustachian tube dysfunction and serving as a source for pathogens.46


    Effect of antimicrobials on adenoid flora
 Top
 Abstract
 Introduction
 Bacterial interference
 Microbiology of the adenoids
 Similarities and differences in...
 Production of ß...
 Effect of antimicrobials on...
 Therapeutic implications
 References
 
The effect on the adenoid bacterial flora of 10 day therapy with either amoxicillin, co-amoxiclav or clindamycin18,19 prior to adenoidectomy for ROM was recently studied (Table 2). The total number of isolates and bacteria per gram of tissue were lower in those treated with any of the antibiotics. However, the number of potential pathogens and BLPB was lower in those treated with co-amoxiclav and clindamycin compared with amoxicillin and controls (P < 0.001). The superiority of co-amoxiclav and clindamycin over amoxicillin in eradicating penicillin-susceptible pathogens such as S. pneumoniae and GABHS may be due to their activity against aerobic and anaerobic BLPB.18,19,35 The elimination of both potential pathogenic and non-pathogenic BLPB may be beneficial, as these organisms might ‘shield’ penicillin-susceptible pathogens from penicillins.35 This phenomenon might explain the survival of penicillin-susceptible bacteria such as S. pneumoniae in children treated with amoxicillin.


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Table 2.  Predominant bacteria isolated from the core of excised adenoids from 60 children with ROM18, 19
 

    Therapeutic implications
 Top
 Abstract
 Introduction
 Bacterial interference
 Microbiology of the adenoids
 Similarities and differences in...
 Production of ß...
 Effect of antimicrobials on...
 Therapeutic implications
 References
 
Adenoidectomy and tonsillectomy are frequently carried out to relieve recurrent ear infections and chronic adenoiditis associated with persistent ear effusions in children.36 Adenoidectomy may also be indicated with symptoms such as persistent mouth breathing, nasal speech and ‘adenoid facies’.

There are no solid data to support adenoidectomy for the treatment of recurrent nasopharyngitis. However, a limited and short-term efficacy was noted on the rate of ROM37 and otitis media with effusion38 after adenoidectomy. These children are usually treated with multiple courses of antibiotics before surgery; however, many continue to harbour pathogenic bacteria in the pharynx and the adenoids and many of these bacteria are resistant to antibiotics.39 Removal of the tonsils and adenoids is associated, in many instances, with a reduction in pathogenic organisms such as GABHS and S. aureus.3

McClay39 recovered resistant organisms (S. pneumoniae, H. influenzae or M. catarrhalis) in 56% (26/46) of adenoids in children with adenoid hypertrophy with ear or sinus disease compared with 22% (4/18) of children with adenoid hypertrophy but with no ear or sinus disease (P < 0.02). Resistant isolates were found in 65% (23/35) of S. pneumoniae, 37% (18/49) of H. influenzae and 100% (19/19) of M. catarrhalis isolates.

Various theories were suggested to explain the persistence of these pathogenic organisms in the oropharynx, including appearance of penicillin-resistant AHS and penicillin-tolerant GABHS and increased numbers of BLPB such as S. aureus and some strains of H. influenzae.

The isolation of BLPB from chronically inflamed adenoids in children raises the question of whether the currently used antimicrobial therapy of chronic adenotonsillitis is always adequate and whether therapy for this infection should also be directed at the eradication of the more prevalent of these potential pathogens.

Indirect evidence for the potential importance of microorganisms in adenoid hypertrophy was recently provided by Sclafani et al.40 who demonstrated a significant reduction of the need of adenotonsillectomy following 30 day therapy with co-amoxiclav compared to placebo in children with hypertrophic adenoids and tonsils. The effect of co-amoxiclav therapy may be due to its activity against aerobic and anaerobic BLPB that are found in higher numbers in the cores of hypertrophic adenoids and tonsils with or without a history of recurrent infection.

Although no other prospective studies were done on children with adenotonsillitis, when antibiotics such as clindamycin,36,40 and co-amoxiclav 41,42 were administered to patients suffering from chronic recurrent tonsillitis, they were found to be more efficacious than penicillin. This may be due to the effectiveness of those drugs not only against GABHS, but also against other organisms that may ‘protect’ the pathogenic organisms such as streptococci by producing ß-lactamase.

Maintaining the beneficial effects of normal flora by avoiding unnecessary exposures to antimicrobial therapy may be a useful tool in preventing colonization of the adenoids by potential pathogens.43 However, further studies are warranted that would compare the efficacy of antimicrobial agents that are active against BLPB with other agents that are not active against these organisms in the treatment of adenoid and tonsillar hypertrophy. Such studies may shed more light on the role of specific bacteria in this condition and could determine whether the use of antimicrobial agents is an adequate substitute for surgical removal of the adenoids and tonsils.


    Footnotes
 
* Tel: +1-301-295-2698; Fax: +1-646-390-2494; E-mail: ib6{at}georgetown.edu Back


    References
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 Abstract
 Introduction
 Bacterial interference
 Microbiology of the adenoids
 Similarities and differences in...
 Production of ß...
 Effect of antimicrobials on...
 Therapeutic implications
 References
 
1 . Tuohimaa, P. & Palva, T. (1987). The effect of tonsillectomy and adenoidectomy on the intra-tympanic pressure. Journal of Laryngology and Otology 101, 892–6.[ISI][Medline]

2 . Gates, G. A., Avery, C. A., Prihoda, T. J. & Cooper, J. C., Jr (1987). Effectiveness of adenoidectomy and tympanostomy tubes in the treatment of chronic otitis media with effusion. New England Journal of Medicine 317, 1444–51.[Abstract]

3 . Gates, G. A., Avery, C. A. & Prihoda, T. J. (1988). Effect of adenoidectomy upon children with chronic otitis media with effusion. Laryngoscope 98, 58–63.[ISI][Medline]

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6 . Ruokenen, J., Sandelin, K. & Makinen, J. (1979). Adenoids and otitis media with effusion. Annals of Otology, Rhinology and Laryngology 88, 166–71.[ISI][Medline]

7 . Fukuda, K., Matsune, S., Ushikai, M., Imamura, Y. & Ohyama, M. (1989). A study of the relationship between adenoid vegetation and rhinosinusitis. American Journal of Otolaryngology 10, 214–6.[CrossRef][ISI][Medline]

8 . Lund, V. J. (1994). Bacterial sinusitis: etiology and surgical management. Pediatric Infectious Disease Journal 13, Suppl. 1, 558–63.

9 . Brook, I. (1981). Aerobic and anaerobic bacteriology of adenoids in children: a comparison between patients with chronic adenotonsillitis and adenoid hypertrophy. Laryngoscope 91, 377–82.[ISI][Medline]

10 . Klein, G. L., Timms, R. & Ziering, R. W. (1984). Obstructive sleep apnea presenting as mouth breathing in a five year old. Immunology and Allergy Practice 6, 59–61.

11 . Schiffman, R., Faber, J. & Eidelman, A. L. (1985). Obstructive hypertrophic adenoids and tonsils as a cause of infantile failure to thrive: reversed by tonsillectomy and adenoidectomy. International Journal of Pediatric Otorhinolaryngology 9, 183–7.[ISI][Medline]

12 . DeDio, R. M., Tom, L. W. C., McGowan, K. L., Wetmore, R. F., Handler, S. D. & Potsic, W. P. (1988). Microbiology of the tonsils and adenoids in a pediatric population. Archives of Otolaryngology—Head and Neck Surgery 114, 763–5.

13 . Sanders, S. S., Nelson, G. E. & Sanders, W. E., Jr (1977). Bacterial interference IV. Epidemiological determinants of the antagonistic activity of the normal flora against Group A streptococci. Infection and Immunity 16, 599–606.[ISI][Medline]

14 . Mackowiak, P. A. (1982). The normal flora. New England Journal of Medicine 307, 83–93.[ISI][Medline]

15 . Sprunt, K. & Redman, W. (1968). Evidence suggesting importance of role of interbacterial inhibition in maintaining balance of normal flora. Annals of Internal Medicine 68, 579–87.[ISI][Medline]

16 . Brook, I., Shah, K. & Jackson, W. (2000). Microbiology of healthy and diseased adenoids. Laryngoscope 110, 994–9.[CrossRef][ISI][Medline]

17 . Brook, I. & Foote, P. A. (1990). Microbiology of ‘normal’ tonsils. Annals of Otology, Rhinology and Laryngology 99, 980–2.[ISI][Medline]

18 . Brook, I. & Shah, K. (2001). Effect of amoxicillin with or without clavulanate on adenoid bacterial flora. Journal of Antimicrobial Chemotherapy 48, 269–73.[Abstract/Free Full Text]

19 . Brook, I. & Shah, K. (2003). Effect of amoxicillin or clindamycin on the adenoids bacterial flora. Otolaryngology and Head and Neck Surgery, in press.

20 . Brook, I. (1999). Bacterial interference. Critical Reviews in Microbiology 25, 155–72.[ISI][Medline]

21 . Smith, H. (1995). The revival of interest in mechanisms of bacterial pathogenicity. Biological Reviews of the Cambridge Philosophical Society, 70, 277–316.[ISI][Medline]

22 . Bernstein, J. M., Sagahtaheri-Altaie, S., Dryja, D. M. & Wactawski-Wende, J. (1994). Bacterial interference in nasopharyngeal bacterial flora of otitis-prone and non-otitis-prone children. Acta Oto-rhino-laryngologica Belgica 48, 1–9.

23 . Murray, P. R. & Rosenblatt, J. E. (1976). Bacterial interference by oropharyngeal and clinical isolates of anaerobic bacteria. Journal of Infectious Diseases 134, 281–5.[ISI][Medline]

24 . Faden, H., Waz, M. J., Bernstein, J. M., Brodsky, L., Stanievich, J. & Ogra, P. L. (1991). Nasopharyngeal flora in the first three years of life in normal and otitis-prone children. Annals of Otology, Rhinology and Laryngology 100, 612–5.[ISI][Medline]

25 . Brook, I. & Yocum, P. (1999). Bacterial interference in the adenoids of otitis media prone children. Pediatric Infectious Disease Journal 18, 835–7.[CrossRef][ISI][Medline]

26 . Brook, I. & Foote, P. A. (1997). Bacterial interference and beta-lactamase-producing bacteria in the adenoids after antimicrobial therapy. Review of Infectious Diseases 25, 493.

27 . Ylikoski, J. & Karjalainen, J. (1989). Acute tonsillitis in young men: etiological agents and their differentiation. Scandinavian Journal of Infectious Diseases 21, 169–74.[ISI][Medline]

28 . Fearon, M., Bannatyne, R. M., Fearon, B. W., Turner, A. & Cheung, R. (1992). Differential bacteriology in adenoid disease. Journal of Otolaryngology 21, 434–6.[ISI][Medline]

29 . Pillsbury, H. C., III, Kveton, J. F., Sasaki, C. T. & Frazier, W. (1981). Quantitative bacteriology in adenoid tissue. Otolaryngology and Head and Neck Surgery 89, 355–63.[ISI][Medline]

30 . Brodsky, L. & Koch, R. J. (1993). Bacteriology and immunology of normal and diseased adenoids in children. Archives of Otolaryngology—Head and Neck Surgery 119, 821–9.

31 . Suzuki, M., Watanabe, T. & Mogi, G. (1999). Clinical, bacteriological, and histological study of adenoids in children. American Journal of Otolaryngology 20, 85–90.[CrossRef][ISI][Medline]

32 . Lee, D. & Rosenfeld, R. M. (1997). Adenoid bacteriology and sinonasal symptoms in children. Otolaryngology and Head and Neck Surgery 116, 301–7.[ISI][Medline]

33 . Brook, I. & Shah, K. (2001). Bacteriology of adenoids and tonsils in children with recurrent adenotonsillitis. Annals of Otology, Rhinology and Laryngology 110, 844–8.[ISI][Medline]

34 . Karlidag, T., Demirdag, K., Kaygusuz, I., Ozden, M., Yalcin, S. & Ozturk, L. (2002). Resistant bacteria in the adenoid tissues of children with otitis media with effusion. International Journal of Pediatric Otorhinolaryngology 64, 35–40.[CrossRef][ISI][Medline]

35 . Brook, I. (1984). The role of ß-lactamase-producing bacteria in the persistence of streptococcal tonsillar infection. Review of Infectious Diseases 6, 601–7.[ISI][Medline]

36 . Darrow, D. H. & Siemens, C. (2002). Indications for tonsillectomy and adenoidectomy. Laryngoscope 112, 6–10.[CrossRef][ISI][Medline]

37 . Paradise, J. L., Bluestone, C. D., Colborn, D. K., Bernard, B. S., Smith, C. G., Rockette, H. E. et al. (1999). Adenoidectomy and adenotonsillectomy for recurrent acute otitis media: parallel randomized clinical trials in children not previously treated with tympanostomy tubes. Journal of the American Medical Association 282, 945–53.[Abstract/Free Full Text]

38 . Marchant, C. D. & Collison, L. M. (1987). Serous and recurrent otitis media. Pharmacological or surgical management? Drugs 34, 695–701.[ISI][Medline]

39 . McClay, J. E. (2000). Resistant bacteria in the adenoids: a preliminary report. Archives of Otolaryngology—Head and Neck Surgery 126, 625–9.

40 . Sclafani, A. P., Ginsburg, J., Shah, M. K. & Dolitsky, J. N. (1998). Treatment of symptomatic chronic adenotonsillar hypertrophy with amoxicillin/clavulanate potassium: short- and long-term results. Pediatrics 101, 675–81.[Abstract/Free Full Text]

41 . Brook, I. & Hirokawa, R. (1985). Treatment of patients with a history of recurrent tonsillitis due to group A beta-hemolytic streptococci: a prospective randomized study comparing penicillin, erythromycin and clindamycin. Clinical Pediatrics 24, 331–6.[ISI][Medline]

42 . Kaplan, E. L. & Johnson, D. R. (1988). Eradication of group A streptococci from the upper respiratory tract by amoxicillin with clavulanate after oral penicillin V treatment failure. Journal of Pediatrics 113, 400–3.[ISI][Medline]

43 . Brook, I. & Gober, A. E. (1998). Bacterial interference in the nasopharynx following antimicrobial therapy of acute otitis media. Journal of Antimicrobial Chemotherapy 41, 489–92.[Abstract]





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Articles by Brook, I.
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Articles by Brook, I.