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Infections in Medicine®

Pediatric Infection: Otitis Media Therapy and Drug Resistance Part 2: Current Concepts and New Directions

Eugene Leibovitz, MD, Ron Dagan, MD, Soroka University Medical Center, Ben-Gurion University of the Negev, Beer-Sheva, Israel


Abstract

Acute otitis media (AOM) is the most common illness that requires a visit to a physician in the developed world, and the number of cases has increased substantially in the past 2 decades. This same period has been marked by a significant increase in drug resistance among pathogens that cause AOM. We provide an evaluation of the agents used to control infections with these pathogens. Prophylactic modalities are also discussed. Advent of the Streptococcus pneumoniae polysaccharide conjugate vaccine, coupled with more judicious use of antibiotics, will improve management of AOM in the coming years. [Infect Med 18(5):263-270, 2001. © 2001 Cliggott Publishing Co., Division of SCP/Cliggott Communications, Inc.]


Introduction

In Part 1 of this article (Infect Med. 2001;18:212-216), we presented an overview of drug resistance in acute otitis media (AOM), described specific pathogens and the pharmacokinetics/pharmacodynamics of specific antibiotic agents, and outlined the correlation between antibiotic resistance and clinical/bacteriologic outcome. In this second part of the article, we discuss nasopharyngeal colonization in AOM, provide an in-depth analysis of drug resistance linked to various anti-AOM agents, and describe current methods of chemoprophylaxis and immunoprophylaxis.

Nasopharyngeal Flora During AOM

Nasopharyngeal colonization with Streptococcus pneumoniae, Haemophilus influenzae (nontypable strains), and Moraxella catarrhalis increases significantly in temporal association with AOM.[1-3] S pneumoniae can be isolated in 25% to 60% of nasopharyngeal cultures obtained from healthy children.[4,5] Its main reservoirs are infants and young children who become colonized with the organism during their first 2 years of life. The pathogen is spread via close contact, especially among children in day-care facilities.[6-8]

Significant changes in nasopharyngeal colonization with S pneumoniae occur during antibiotic treatment. Generally, children who harbor penicillin-susceptible strains will have a major decrease of S pneumoniae in the nasopharyngeal carriage during the first weeks following the completion of a ß-lactam therapeutic regimen.[9-13] However, a rapid and early selection of nonsusceptible S pneumoniae isolates in the nasopharynx is common during AOM therapy.[10,11] This phenomenon was particularly and extensively observed when azithromycin and trimethoprim-sulfamethoxazole (TMP-SMX) were used in the treatment of AOM.[10,11,14] Although the overall carriage of S pneumoniae was reduced from 57% (on day 1) to 29% (on days 4 and 5) during azithromycin therapy, all the remaining strains were resistant to azithromycin.[10] A 10-day regimen of TMP-SMX for AOM was shown to cause an early increase in the carriage rate of both TMP-SMX-resistant and penicillin-resistant S pneumoniae, which persisted for at least 1 month after therapy.[11]

Furthermore, we have recently shown that antibiotic therapy in AOM may induce middle ear fluid (MEF) superinfection by acquisition of preexisting nasopharyngeal antibiotic-resistant S pneumoniae.[12] Nasopharyngeal colonization with penicillin-nonsusceptible S pneumoniae was found to be associated with an increased incidence of nonresponsive AOM.[14,15]

Nasopharyngeal cultures have also been evaluated as predictors of the presence of pathogens in the MEF of patients with AOM. A low positive predictive value (22% to 45% for S pneumoniae) was uniformly reported for the use of this method in the bacterial assessment of AOM.[15,16]

Antimicrobial Agents For AOM

Physicians prescribe antibiotics for the majority of infants and children with AOM because usually they are unable to determine by physical examination which patients will have spontaneous resolution of their disease. In general, antibiotics must be administered if AOM is diagnosed in infants and young children who have recurrent AOM, in those who have structural or immunologic abnormalities, and in those who are severely ill. Children aged 2 years and older, patients without fever, and those with minimal clinical signs may be managed without antibiotics, but a follow-up evaluation is required 24 to 72 hours later.

Factors to be considered in choosing the appropriate antibiotic therapy for AOM include activity of the drug against the main AOM pathogens, local epidemiology, adverse events, tolerability, and cost. For example, marked variations were shown in the acceptance of and compliance with oral antibiotic suspensions prescribed for children. In a previous study performed in southern Israel, 76% of the children who received cefaclor reported acceptance of the drug without problems, while the respective figures for amoxicillin, TMP-SMX, and cefuroxime axetil were 60%, 55%, and 20%, respectively.[17]

The most commonly used antibiotic drugs, their expected MEF levels, and activity against the main pathogens that cause AOM are shown in Table 1. While most of the drugs approved for the treatment of AOM may have relatively good in vitro activity against the common AOM pathogens, there are many variations among these drugs in terms of their in vitro activity and their penetration into the MEF. Double-tympanocentesis studies discerned major differences in bacteriologic efficacy, suggesting that the current armamentarium of antibiotics used in the treatment of AOM should be limited to only those drugs that have proven bacteriologic effectiveness.

Amoxicillin

Amoxicillin is the most commonly used oral antibiotic for the treatment of AOM. At the standard dosages of 40 to 50 mg/kg/d, it is highly effective against H influenzae that do not produce ß-lactamase and against penicillin-susceptible and intermediately resistant S pneumoniae. It achieves its effectiveness by reaching MEF concentrations of 1 to 6 µg/mL.[18,19] However, these concentrations may not be high enough to eradicate penicillin-fully resistant S pneumoniae with minimum inhibitory concentrations (MICs) greater than 2 µg/mL. Higher dosages of amoxicillin (70 to 90 mg/kg/d) are recommended in those situations in which the presence of these pneumococci is suspected or proved.[20-22]

The MICs of amoxicillin are generally about equal to or 2 to 4 times less than the MIC of benzyl penicillin, and high-level resistance to penicillin has been previously associated with low-level resistance to amoxicillin.[23] Recently, S pneumoniae with high-level resistance to amoxicillin (MICs of 4 µg/mL or greater) has emerged in France, most probably under the strong selective pressure caused by the extensive use of high doses of this drug and other ß-lactams.[24] In addition, amoxicillin is not effective against ß-lactamase-producing H influenzae.

At present, amoxicillin in a dosage of 40 to 50 mg/kg/d is recommended for the empiric treatment of the first episode of AOM in children of all ages when antibiotic therapy is indicated. In areas with a low prevalence of antibiotic-resistant S pneumoniae, amoxicillin (40 to 50 mg/kg/d) and amoxicillin/clavulanate (depending on the prevalence of ß-lactamase-producing H influenzae) represent the drugs of choice for the empiric treatment of uncomplicated AOM.

The higher dosage (70 to 90 mg/kg/d) of amoxicillin is advised for the empiric treatment of AOM in infants and children younger than 2 years in areas with a high rate of recovery of antibiotic-resistant S pneumoniae. It is also recommended for the therapy of culture-proven AOM caused by penicillin-intermediate and fully resistant S pneumoniae.

Amoxicillin/clavulanate

Amoxicillin/clavulanate is a combination antibiotic containing amoxicillin and clavulanate potassium, a ß-lactamase inhibitor that extends the spectrum of amoxicillin against ß-lactamase-producing bacteria. A twice-daily regimen (45 mg/kg/d of amoxicillin, 6.4 mg/kg/d of clavulanate in 2 divided doses for 10 days) was recently proved to be as effective as the previously used 3-times-daily regimen (40 mg/kg/d of amoxicillin, 10 mg/kg/d of clavulanate in 3 divided doses). In addition, the twice-daily preparation was associated with a decrease in adverse effects (particularly diarrhea and abdominal upset) and increased patient compliance.[25,26]

Recently, a multicenter study evaluated the bacteriologic efficacy of this twice-daily regimen and reported an overall eradication rate of AOM pathogens of 83% (87% forH influenzae and 90% for S pneumoniae).[27] In this study, the bacteriologic success rates were consistently high for both H influenzae and S pneumoniae and the amoxicillin/clavulanate MICs were within the susceptible range for the great majority of these pathogens. The clinical efficacy rate with this regimen, measured at the end of therapy and on days 22 to 28, paralleled the bacteriologic efficacy rate.[27]

The possible additional benefits of a higher dosage of amoxicillin/clavulanate (90 mg/kg/d of amoxicillin, 6.4 mg/kg/d of clavulanate in 2 divided doses for 10 days) are presently being evaluated in a prospective, multicenter double-tympanocentesis study. Preliminary results of this study, summarized for the first 521 children enrolled, showed that all penicillin-susceptible and -intermediate S pneumoniae and 97% of penicillin-resistant strains were eradicated by this regimen. In addition, 95% and 100% of H influenzae and M catarrhalis organisms, respectively, were also eradicated.[28]

Cephalosporins

Among oral cephalosporins, cefuroxime axetil is the only one that reaches MEF levels above the MIC values for both S pneumoniae and H influenzae for about 40% of the dosing interval.[29] The bacteriologic and clinical efficacy of cefuroxime axetil has been recently proved in a double-tympanocentesis study.[30-32] Cefaclor, cefixime, loracarbef, and ceftibuten are less active in vitro against S pneumoniae, particularly against penicillin-intermediate and -resistant strains.[31-33]

Cefpodoxime has good in vitro activity against H influenzae, M catarrhalis, and antibiotic-resistant S pneumoniae,[34] but its bacteriologic efficacy has not yet been evaluated in prospective, comparative, double-tympanocentesis studies. Cefprozil has a good in vitro sensitivity profile against AOM pathogens, but the limited data available suggest a poor eradication rate of H influenzae from the MEF.[35]

MEF concentrations of ceftriaxone exceed the MICs for AOM pathogens for about 56 hours after a single 50 mg/kg intramuscular injection.[36] However, with ceftriaxone MICs for penicillin- and ceftriaxone-resistant S pneumoniae higher than 2 µg/mL and 1 µg/mL, respectively, MEF concentrations of the drug may decline below therapeutic values and therefore failures may be expected.

While a single 50 mg/kg dose of ceftriaxone was approved by the FDA for the treatment of AOM, we consider that there is no place today for ceftriaxone therapy in the management of simple, uncomplicated AOM, with the exception of cases of persistent vomiting and lack of compliance with oral drugs. The use of ceftriaxone should be limited to second- and even third-line therapy for nonresponsive AOM.[37,38]

Recently, a 3-day 50 mg/kg/d ceftriaxone regimen was shown to be significantly superior clinically and bacteriologically to a 1-day regimen in the treatment of nonresponsive AOM, and this difference was found to be mainly caused by the superior eradication rate of penicillin-resistant S pneumoniae by the 3-day regimen.[39] It is important to mention, however, that the eradication rate of H influenzae and penicillin-susceptible S pneumoniae was 100% in the 1-day ceftriaxone-treated patients, and therefore such a regimen is appropriate for nonresponsive AOM caused by these pathogens.[39]

Macrolides and clindamycin

Erythromycin. The resistance of S pneumoniae to erythromycin has increased substantially in every area of the world, and considerable cross-resistance exists between this drug and ß-lactams.[40-43] Moreover, this agent shows lack of activity against H influenzae. Therefore, erythromycin currently has no place in the empiric treatment of AOM, as either a first- or a second-line therapy.

Azithromycin. This newer azalide is closely related to the macrolide class, with good in vitro activity against macrolide-susceptible S pneumoniae, M catarrhalis and, to a lesser extent, H influenzae. In addition, it has the advantages of single daily dosing, short duration of therapy (3 to 5 days), and a low rate of adverse events.

Clinical efficacy studies performed during the last 10 years demonstrated a beneficial effect of this drug in AOM,[44-46] but many of the patients enrolled in these studies were older than 2 years and had a milder form of disease. Double-tympanocentesis studies demonstrated the lack of bacteriologic efficacy of azithromycin in AOM caused by H influenzae and macrolide-resistant S pneumoniae.[33,47,48]

These bacteriologic efficacy results were in fact very close to the results obtained with placebo. In addition to low bacteriologic efficacy, a recent study also demonstrated an inferior clinical efficacy for azithromycin (on days 12 to 14 of therapy) when compared with amoxicillin/clavulanate.[27] The poor results in these studies are probably related to the specific pharmacokinetic and pharmacodynamic properties of azithromycin, which may allow the achievement of higher drug concentrations in polymorphonuclear cells and much lower concentrations in the extracellular compartment of the MEF, where the pathogens that cause AOM concentrate.[47-49]

Clindamycin. This antimicrobial agent has good activity against most penicillin-nonsusceptible S pneumoniae and may be used to treat pneumococcal AOM that is unresponsive to ß-lactam antibiotics. The drug has no activity against H influenzae and M catarrhalis. Prospective, controlled studies of the bacteriologic and clinical efficacy of clindamycin in the treatment of AOM are missing. Before deciding to use this drug, the physician should be certain via MEF culture that the AOM episode was caused by S pneumoniae -- which is unfeasible in most common practices.

Trimethoprim-sulfamethoxazole

TMP-SMX has been used extensively in the past as a first- and second-line agent in the treatment of AOM and also as a prophylactic agent. However, given the high resistance rate of S pneumoniae to TMP-SMX (greater than 50% in many areas of the world), there is no place today for its use in the empiric treatment of AOM as either a first- or a second-line agent. A recently completed double-tympanocentesis study performed in patients with AOM who were treated with TMP-SMX showed a 56% and 15% overall bacteriologic failure rate for S pneumoniae and H influenzae, respectively.[14]

In patients with AOM caused by TMP-SMX-resistant organisms, the bacteriologic failure rates were much higher: 79% and 46% for S pneumoniae and H influenzae, respectively, similar to the failure rates encountered when placebo was administered.[14,50]

Short-Term Antibiotic Therapies

An analysis of 27 clinical trials involving 3766 patients with AOM who received various antibiotic drugs for a shortened period (fewer than 10 days) concluded that the prospects for a successful outcome seem quite high for most uncomplicated cases of AOM.[51] However, most of these studies had major design flaws, such as lack of bacteriologic efficacy data and the under-representation of children younger than 2 years. In addition, many of these studies were performed before the emergence of antibiotic-resistant S pneumoniae as the major challenge in the treatment of AOM.

Further studies evaluating shortened antibiotic regimens for AOM will have to be performed in children younger than 2 years and patients with nonresponsive AOM; these studies will need to investigate the bacteriologic outcome of these shortened antibiotic regimens in addition to their clinical efficacy. Until the results of these studies are available, we cannot recommend shortened antibiotic regimens in the routine management of AOM or in the treatment of AOM in the following groups:

Prevention

Chemoprophylaxis

The efficacy of different antibiotic regimens for the prevention of AOM -- such as amoxicillin or sulfisoxazole at half the therapeutic daily doses -- has been evaluated in many previous controlled clinical trials. A meta-analysis study found a significant reduction of new and symptomatic episodes of AOM in the treated groups.[54-59] The major concern related to the extensive use of chemoprophylaxis for AOM is the risk of emergence of resistant organisms.

At present, we must consider the tremendous increase in the resistance to antibiotics of the main pathogens that cause AOM ( particularly S pneumoniae) and the high rate of nasopharyngeal colonization with these pathogens in infants and toddlers, as well as the potential of prolonged antibiotic administration to considerably increase the resistance of these organisms. As a result, the decision to start antibiotic prophylaxis in a patient who has AOM must be made on an extremely selective basis.

This prophylactic approach should be limited to only those few patients who have entered the vicious circle in which they spend weeks and months almost continuously taking antibiotic treatment for recurrent AOM. The present recommendations reserve antimicrobial prophylaxis for children with recurrent AOM defined by having 3 or more documented episodes in 6 months or 4 or more episodes in 12 months.[59]

The concern for increased antibiotic resistance has led various investigators to examine the role of oligosaccharides and xylitol in the prevention of AOM episodes.[60-63] Children who used daily xylitol chewing gum or suspension were found to have significantly fewer AOM episodes than children who used sucrose chewing gum or suspension.[63,64]

Immunoprophylaxis

Prevention of pneumococcal invasive diseases and also of AOM caused by pneumococci represents a tremendous challenge, especially in this era of antibiotic-resistant organisms. The excellent results obtained with the large-scale use of H influenzae type b conjugate vaccine have paved the way for the development of multivalent pneumococcal conjugate vaccines to be used for the prevention of pneumococcal invasive diseases and AOM.

Immunogenicity studies have indicated that infants respond to each conjugate polysaccharide type with concentrations of antibodies believed to be protective.[64] In addition, the use of conjugate vaccines in infants and toddlers has been shown to decrease the nasopharyngeal carriage of many pneumococcal serotypes, especially the resistant strains included in the vaccine.[65-68]

Three recent studies have demonstrated the clinical benefit of the conjugated vaccines in the prevention of AOM caused by S pneumoniae. Two of them, performed in California[69] and Finland,[70,71] showed a reduction in pneumococcal AOM after the administration of a 7-valent pneumococcal conjugate vaccine in infants. The third study, from Israel,[72] showed a reduction in respiratory infections, including AOM, and a reduction in antibiotic use in toddlers attending day-care centers following the administration of a 9-valent pneumococcal CRM197 vaccine.

Future studies require more complete answers to additional questions related to the reduction in the carriage of resistant strains, the possible replacement of vaccine strains by nonvaccine strains, the overall impact on the prevalence of multidrug-resistant strains, and the serum and local antibody levels required to confer protection against AOM.

Management Recommendations

Clinicians involved in the treatment of children should be aware of the major increase in the proportion of resistant organisms that cause AOM and of the direct relationship between this increase and antibiotic use. It is well known that in some Western European countries, the treatment policy for AOM is to withhold antimicrobial drugs in patients with AOM, using antibiotics only after a 1- to 3-day observation period during which the patient remains ill.[73] However, no evidence-based data exist to support the withholding of antibiotic therapy in children younger than 2 years with AOM, patients with complicated AOM, or children attending day-care centers. Therefore, the policy of observation alone may be recommended only in children older than 2 years who are mildly symptomatic.[43]

Table 2 summarizes recommendations for first- and second-line therapy for AOM. The Drug-resistant Streptococcus pneumoniae Therapeutic Working Group of the CDC has recently published new guidelines for the antibiotic treatment of AOM in the present era of pneumococcal resistance.[43] According to these guidelines, amoxicillin (40 to 50 mg/kg/d or the higher dosage of 70 to 90 mg/kg/d) represents the first-line treatment of choice for AOM. High-dose amoxicillin or amoxicillin/clavulanate or cefuroxime axetil is recommended as first-line treatment of AOM in those patients who have received antimicrobial therapy during the month preceding the AOM episode.

In cases of clinical failure after 3 full days of therapy, we recommend the performance of a diagnostic (and in many situations therapeutic) tympanocentesis, particularly in areas with a high prevalence of antibiotic-resistant S pneumoniae.

The 3 second-line antibiotic drugs recommended for clinical failures are:

  • Amoxicillin/clavulanate (the 45 mg/kg/d amoxicillin dosage or in the future a 90 mg/kg/d dosage) for 10 days.
  • Cefuroxime axetil (30 mg/kg/d) for 10 days.
  • Intramuscular ceftriaxone (50 mg/kg/d) for 3 days.

 

Drs Leibovitz and Dagan are with the pediatric infectious disease unit, Soroka University Medical Center, and the Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel.

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