PEDIATRICS Vol. 106 No. 4 October 2000, pp. 695-699

Pneumococcal Mastoiditis in Children

Sheldon L. Kaplan, MD^*, Edward O. Mason Jr., PhD^*, Ellen R. Wald, MD, Kwang Sik Kim, MD^§, Laurence B. Givner, MD, John S. Bradley, MD^¶, William J. Barson, MD^#, Tina Q. Tan, MD^**, Gordon E. Schutze, MD, and Ram Yogev, MD^**

From the Pediatric Infectious Disease Sections of ^* Baylor College of Medicine, Houston, Texas;  University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania; ^§ University of Southern California School of Medicine, Los Angeles, California;  Wake Forest University School of Medicine, Winston-Salem, North Carolina; ^¶ Children's Hospital San Diego, San Diego, California; ^# Ohio State University College of Medicine and Public Health, Columbus, Ohio; ^** Northwestern University Medical School, Chicago, Illinois; and  University of Arkansas for Medical Sciences, Little Rock, Arkansas.

	ABSTRACT

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Objective.  To determine the impact of antibiotic resistance on the frequency, clinical features, and management/outcome of mastoiditis attributable to Streptococcus pneumoniae.

Design.  Retrospective review of the medical records of children with mastoiditis caused by S pneumoniae from September 1993 through December 1998.

Patients.  Infants and children with pneumococcal mastoiditis cared for at 8 children's hospitals in the United States.

Results.  Thirty-four children with pneumococcal mastoiditis were identified. The median age of the children was 12 months (range: 2 months-12.5 years); 28 (82%) were 2 years old. Six children had recurrent otitis media. A subperiosteal abscess was noted in 13 children (37%). The mastoids were abnormal in all 25 patients on whom computed tomography was performed. There was no trend toward increasing numbers of cases per year despite increasing proportions of pneumococcal isolates, which were nonsusceptible to penicillin. Serogroup 19 accounted for 57% of isolates, serogroup 23 for 14.3% of isolates, and serotype 3 for 10.7% of isolates. Except for receipt of less antibiotic therapy in the previous 30 days, children with penicillin-susceptible isolates had similar demographic features and clinical findings and surgical treatment as did children whose isolates were nonsusceptible to penicillin.

Conclusions.  Pneumococcal mastoiditis occurs primarily in children <2 years of age and usually is not associated with a history of recurrent otitis media. The number of cases of mastoiditis caused by S pneumoniae occurring among 8 children's hospitals has remained stable despite increasing rates of antibiotic-resistant S pneumoniae. Serogroup 19 is the leading serogroup associated with pneumococcal mastoiditis.Streptococcus pneumoniae, mastoiditis, serotypes, resistance.

Although mastoiditis occurs less than often than it did in the preantibiotic era, it remains the most common complication of acute or chronic otitis media within the temporal bone.^1,2 Streptococcus pneumoniae is the most frequent causal agent of acute mastoiditis in children.^3-6 Since the late 1980s, antibiotic resistance among S pneumoniae isolates has increased dramatically in most areas of the United States; pneumococcal isolates recovered from cultures of middle ear fluid typically have rates of resistance that are greater than isolates from systemic sources such as blood or cerebrospinal fluid.^7-9 Whether the increase in antibiotic resistance has impacted the frequency or outcome of acute mastoiditis is not certain.

As a part of an ongoing surveillance study of pneumococcal infection in children cared for at 8 pediatric hospitals in the United States, the medical records of children with documented pneumococcal mastoiditis were reviewed to: 1) describe the clinical features of this infection, and 2) determine the impact of antibiotic resistance on the frequency, management, and outcome of mastoiditis caused by S pneumoniae.

	METHODS

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Since September 1, 1993, investigators from 8 children's hospitals in the United States have previously identified children evaluated at their respective institutions with invasive infections caused by S pneumoniae.¹⁰ Isolates from mastoid cultures have been included since September 1, 1993, and middle ear fluid isolates have been collected since September 1, 1994. The period studied was September 1, 1993 to December 31, 1998. Based on review of the medical record, a diagnosis of acute or chronic mastoiditis was assigned and standard information (including demographic, clinical, and microbiologic data) was collected for each patient. Acute mastoiditis was determined by the findings of post or suprauricular erythema or swelling or, in their absence, evidence of mastoiditis on computed tomography of the temporal bone (osteitis, coalescence of air cells, and subperiosteal abscess).³ Chronic mastoiditis was determined by a history of prolonged ear drainage, previous placement of pressure equalization tubes or evidence on computed tomography or pathology specimens.¹ Recurrent otitis media was defined as >3 episodes in 6 months. For the set of children with mastoiditis, a more detailed collection form was completed that included specific information about the history, the physical examination, laboratory and radiographic evaluation, hospital course, and management.

Isolates from each center were sent to a central laboratory (Baylor College of Medicine, Houston, TX) for serotyping and to determine susceptibility to penicillin and ceftriaxone by microbroth dilution as previously described.¹⁰ Susceptibility categories were determined by the 1999 National Committee for Clinical Laboratory Standards guidelines for breakpoints (penicillin: .06 µg/mL = susceptible; .1-1.0 µg/mL = intermediate; 2.0 µg/mL = resistant; ceftriaxone: .5 µg/mL = susceptible; 1.0 µg/mL = intermediate; 2.0 µg/mL = resistant).¹¹ Isolates in the intermediate or resistant categories were considered nonsusceptible. Six isolates were not available for typing, but the antibiotic susceptibility results from the original laboratory testing were accepted for this study.

Dichotomous variables were analyzed by ² test, the ² test for trend, or Fisher's exact test, and continuous variables were tested with Student's t test, or the Kruskal-Wallis or Mann-Whitney U tests for nonparametric data (Epistat, Richardson, TX).

	RESULTS

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Thirty-four children with pneumococcal mastoiditis were identified among the 8 children's hospitals from September 1, 1993 to December 31, 1998. The mean age of the patients was 12 months (range: 2 months-12.5 years); 28 (82%) were 2 years old and 18 (53%) were 12 months old. Additional demographic data are shown in Table 1. Four children had underlying conditions (Goldenhar's syndrome with ventriculo-peritoneal shunt and tetralogy of Fallot; anoxic encephalopathy; former premature infant; and ventricular septal defect). Three children had a history of chronic or recurrent mastoiditis; 6 children (including 1 with chronic mastoiditis) had recurrent otitis media. Twenty-one of the patients had received an antibiotic in the month before the episode of pneumococcal mastoiditis.

The presenting features of the history and findings on physical examination of the 34 children are summarized in Table 2. A white blood cell count was available in 29 children. The median white blood cell count was 16 300/mm³ (range: 4000-28 000/mm³). The median percentages of polymorphonuclear leukocytes and bands were 38% (range: 0%-62%) and 1% (range: 0%-41%), respectively. Computed tomography of the mastoids was performed on 25 patients; all were abnormal. Eight demonstrated coalescence of air cells; 14 showed opacification, cloudiness, or fluid; and 11 had evidence of bony erosion or a subperiosteal abscess. One child had plain radiographs of the mastoid and 9 patients had no radiographic evaluations. At presentation a subperiosteal abscess was noted in 13 patients including 1 child with thrombosis of the adjacent sigmoid sinus. Epidural abscess or facial paralysis was not reported for any patient.

S pneumoniae was isolated from the mastoid bone or postauricular abscess in 18 of 19 children, from middle ear effusion by myringotomy, tympanocentesis, or from spontaneous drainage through the tympanic membrane in 23 of 24 children, and from blood in 2 of 8 children. Nine children had positive culture results from 2 sites. The 1 child who died within 24 hours of admission also had bacteremia and meningitis. Antibiotic susceptibility is shown in Table 3. Overall 44% of isolates were nonsusceptible to penicillin and 24% were nonsusceptible to ceftriaxone. There was no apparent sustained increase in the number of cases of mastoiditis that occurred during the years 1994-1998. However, the proportion of cases of mastoiditis attributable to penicillin-nonsusceptible strains increased each year, as it had for pneumococcal isolates recovered from children with systemic infections over the same period (Fig 1).

View larger version (42K): [in this window] [in a new window]   Fig. 1.   Number of pneumococcal mastoiditis cases per year and number attributable to penicillin-nonsusceptible isolates. The percentage above the total cases represents the percentage of pneumococcal mastoiditis cases of all systemic pneumococcal isolates each year.

Among the isolates recovered from children with mastoiditis, serogroup 19 was the most common (57%) followed by serotype 23F (14.3%), and serotype 3 (10.7%). Compared with isolates recovered from systemic sites, the distribution of serotypes in children with mastoiditis was different. Serogroup 19 and serotype 3 were more frequent among the mastoiditis isolates during the same period (P < .000001 and P = .002, respectively). In contrast, the proportion of isolates in serogroups 6 or 14 was reduced among the mastoiditis isolates (P = .015 and P = .05, respectively; Table 4).

Children with nonsusceptible pneumococcal isolates received antibiotics in the month before presentation significantly more frequently (14/15) than children whose isolates were susceptible to penicillin (7/19; P = .001). There were no other significant differences for the demographic or clinical features between patients with mastoiditis attributable to penicillin-susceptible versus penicillin-nonsusceptible strains.

Treatment and Outcome

A summary of the surgical procedures, antibiotic therapy, duration of fever after any therapy was initiated, and duration of hospitalization is shown in Table 5. Only 3 of the 34 patients did not undergo some surgical procedure and 1 died with bacteremia and meningitis. Three children received vancomycin for 5 days. For the 8 children with mastoiditis attributable to penicillin-resistant strains (minimal inhibitory concentration: 2.0 µg/mL), 4 received a second or third generation cephalosporin for 7 to 30 days, 3 received ticarcillin-clavulanate or ampicillin-sulbactam for 3 to 21 days, and 5 received clindamycin intravenously or orally for 3 to 35 days (several patients received >1 antibiotic). Amoxicillin-clavulanate and cefixime were administered to 1 patient each for 3 weeks. The durations of parenteral antibiotics and of hospitalization were different among the 30 children undergoing some type of surgical procedure; children with myringotomy and pressure equalization tube placement received fewer days of parenteral antibiotics and were hospitalized for a shorter period of time. Penicillin susceptibility was not associated with a greater likelihood of undergoing mastoidectomy versus no surgery or myringotomy and pressure equalization tube placement. For children with penicillin-nonsusceptible isolates, 10/15 underwent mastoidectomy versus 6/18 children whose isolates were penicillin-susceptible (P = .12). All surviving patients were successfully treated; 1 patient required a revision of the original mastoidectomy 1 day after discharge.

	DISCUSSION

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Because the incidence of acute mastoiditis has diminished greatly since the introduction of antibiotic therapy for acute otitis media, multicenter studies are required to collect adequate descriptive information regarding mastoiditis in a relatively timely manner. In our surveillance study among 8 children's hospitals, 34 cases of pneumococcal mastoiditis were documented over a 52-month period. Despite the increase in antimicrobial resistance among S pneumoniae isolates in these centers, the prevalence of pneumococcal mastoiditis did not increase from 1994 through 1998. Our study is limited to only those children with mastoiditis whose cultures grew S pneumoniae. Thus, we cannot determine from this study whether the frequency of mastoiditis in general is increasing in children. In 1 study that included both children and adults, pneumococcal related rates of acute mastoiditis expressed as a proportion of yearly hospital admissions did increase over a 12-year period.¹² In 7 of the 8 cases caused by S pneumoniae in the last 3 years of that study, the isolate was resistant to penicillin.

In this large collection of cases of mastoiditis attributable to S pneumoniae, more than one half of our patients were <12 months old and many did not have a history of recurrent acute otitis media. As in other studies of acute mastoiditis, males outnumbered females 2 to 1. The signs and symptoms as well as findings on physical examination were very similar to those reported by Ogle and Lauer.³ Except for a history of recent antibiotic administration, there were no differences in the presenting histories or physical findings between children with penicillin-susceptible or penicillin-nonsusceptible isolates. Computed tomography of the mastoid bone was abnormal in all 25 children undergoing this imaging procedure.

Nearly 60% of the pneumococcal isolates causing mastoiditis belonged to serogroup 19 (10/16 serogroup 19 isolates were 19F). Serotypes 23F and 3 were the next most common. Serotype 19F has been the predominant type recovered from middle ear fluid in association with otitis media and accounted for 19% to 28% of pneumococcal isolates in studies reported from 1970 to 1986.^13-17 In 2 studies the highest frequency of relapse of acute otitis media was associated with serotypes 14 and 19.^13,14 In contrast, no serogroup 6 isolates were identified in our study despite the observation that this serogroup is generally the second or third most common (12%-15%) among pneumococcal isolates from middle ear cultures.¹⁶ The striking association between serotype 19F and mastoiditis suggests a unique ability of this capsular serotype to persist or invade in the mastoid air cells. In the chinchilla otitis media model, a type 19F pneumococcus was more virulent than pneumococcal serotype 6B, 14, or 23F isolates.¹⁸ However, when a serogroup 19 isolate was inoculated by intravenous or intraperitoneal routes into 6- to 8-week-old mice, mortality was virtually zero.¹⁹

All but 3 of these patients with mastoiditis underwent a surgical procedure; one half had a mastoidectomy. Children with penicillin-nonsusceptible pneumococci were not more likely to undergo mastoidectomy (10/15) than were those with penicillin-susceptible strains (6/18). Only 1 child had an intracranial complication of mastoiditis (thrombosis of the adjacent sigmoid sinus). Because penicillin alone was not administered to any patient with a penicillin-resistant isolate, no conclusions can be drawn regarding the role of penicillin therapy for treatment of mastoiditis attributable to such isolates.

The conjugate pneumococcal vaccines under investigation each contain the polysaccharides of serotypes 19F and 23F, which together accounted for 70% of the pneumococcal serotypes for the isolates associated with mastoiditis in our study.²⁰

In one clinical trial, a heptavalent pneumococcal vaccine administered at 2, 4, 6, and 12 to 15 months of age was associated with a ~20% reduction for physician visits for recurrent otitis media (5 episodes in 6 months or 6 episodes in 1 year), as well as a 20% reduction in the placement of ventilation tubes.²¹ A study in Finland evaluated the efficacy of the same heptavalent pneumococcal vaccine in preventing serotype specific acute otitis media from culture-confirmed cases.²² The vaccine prevented against 57% of culture-confirmed acute otitis media attributable to serotypes in the vaccine, 34% of culture-confirmed pneumococcal acute otitis media, and 6% of acute otitis media of any cause. Hopefully, the pneumococcal conjugate vaccines will lead to a further reduction in the incidence of mastoiditis caused by S pneumoniae.

	ACKNOWLEDGMENTS

This study was supported in part by a grant Roche Laboratories.

We thank Linda Lamberth and Rebekah Lichenstein for technical support. We also acknowledge the help of the following individuals: Andrea Forbes, RN Nancy Tucker, RN; Michelene Ortenzo; Bev Petrites, RN; and Susan Aragon, RN.

	FOOTNOTES

Received for publication Aug 9, 1999; accepted Jan 3, 2000.

Reprint requests to (S.L.K.) Department of Pediatrics, Baylor College of Medicine, Infectious Disease Service, Texas Children's Hospital, 6621 Fannin St, Houston, TX 77030-2399. E-mail: skaplan{at}bcm.tmc.edu

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