Anne Schuchat, M.D., Katherine Robinson, M.P.H., Jay D. Wenger, M.D., Lee H. Harrison, M.D., Monica Farley, M.D., Arthur L. Reingold, M.D., Lewis Lefkowitz, M.D., Bradley A. Perkins, M.D., for The Active Surveillance Team
Background Before the introduction of the conjugate vaccines,Haemophilus influenzae type b was the major cause of bacterialmeningitis in the United States, and meningitis was primarilya disease of infants and young children. We describe the epidemiologicfeatures of bacterial meningitis five years after the H. influenzaetype b conjugate vaccines were licensed for routine immunizationof infants.
Methods Data were collected from active, population-based surveillancefor culture-confirmed meningitis and other invasive bacterialdisease during 1995 in laboratories serving all the acute carehospitals in 22 counties of four states (total population, morethan 10 million). The rates were compared with those for 1986obtained by similar surveillance.
Results On the basis of 248 cases of bacterial meningitis inthe surveillance areas, the rates of meningitis (per 100,000)for the major pathogens in 1995 were Streptococcus pneumoniae,1.1; Neisseria meningitidis, 0.6; group B streptococcus, 0.3;Listeria monocytogenes, 0.2; and H. influenzae, 0.2. Group Bstreptococcus was the predominant pathogen among newborns, N.meningitidis among children 2 to 18 years old, and S. pneumoniaeamong adults. Pneumococcal meningitis had the highest case fatalityrate (21 percent) and in 36 percent of cases was caused by organismsthat were not susceptible to penicillin. From these data, weestimate that 5755 cases of bacterial meningitis were causedby these five pathogens in the United States in 1995, as comparedwith 12,920 cases in 1986, a reduction of 55 percent. The medianage of persons with bacterial meningitis increased greatly,from 15 months in 1986 to 25 years in 1995, largely as a resultof a 94 percent reduction in the number of cases of H. influenzaemeningitis.
Conclusions Because of the vaccine-related decline in meningitisdue to H. influenzae type b, bacterial meningitis in the UnitedStates is now a disease predominantly of adults rather thanof infants and young children.
Few medical advances in recent decades have affected pediatricinfectious diseases as much as conjugate vaccines against Haemophilusinfluenzae type b disease.1 In the United States, before theadvent of conjugate vaccines, H. influenzae type b meningitisor invasive disease developed in nearly 1 in 200 children byfive years of age,2 and 70 percent of bacterial meningitis amongchildren under five was attributable to H. influenzae.3 Now,reports of dramatic declines in the disease from several countriesafter conjugate vaccines entered routine use suggest that theelimination of the disease may be attainable.4,5,6,7
The near elimination of H. influenzae type b disease will radicallyalter the view of bacterial meningitis as a major health problemof children. Because clinicians typically initiate therapy formeningitis before an etiologic agent is confirmed, the decreasein H. influenzae meningitis and the increase in antimicrobialresistance among pneumococci influence choices for empiricalmanagement of meningitis.8 Evaluation of the epidemiology ofbacterial meningitis in the era of the H. influenzae type bvaccine thus has important implications for both public healthplanning and clinical management. We report the results of laboratory-basedsurveillance for bacterial meningitis in 1995, five years afterthe licensure of conjugate H. influenzae type b vaccines foruse in infants.
Methods
Surveillance for invasive disease due to Neisseria meningitidis,H. influenzae, group B streptococcus, Listeria monocytogenes,and Streptococcus pneumoniae was performed during 1995 in eightcounties in Georgia, in five counties in Tennessee, and in sixcounties in Maryland, and from October 1, 1994, to September30, 1995, in three counties in California. These 22 countieshad a total population of 10,281,746, or 3.9 percent of theU.S. population. Blacks represented 24 percent of the surveillancepopulation, as compared with 12 percent of the U.S. population.
Invasive disease was defined as disease in which an organismhad been isolated from a sterile site (such as blood or cerebrospinalfluid) in a resident of the surveillance area. A case of invasivedisease was considered to be meningitis if a clinical diagnosisof meningitis had been entered in the patient's medical record.
In each surveillance area, project personnel communicated everytwo weeks with contacts in all microbiology laboratories servingacute care hospitals and completed standardized case-reportforms. Clinical isolates were sent to the Centers for DiseaseControl and Prevention (CDC) in Atlanta for serogrouping (N.meningitidis) and serotyping (L. monocytogenes and H. influenzae).S. pneumoniae isolates were tested for antimicrobial susceptibilityat either the CDC or the University of Texas Health ScienceCenter at San Antonio by the broth-dilution method.9
The sensitivity of surveillance, determined by audits of alllaboratories, was defined as the proportion of all cases identifiedby laboratory audit that were also identified by initial surveillance.
Rates for 1995 were calculated from U.S. Census Bureau populationestimates for 1992, the most recent year for which relevantdata at the county level were available. Rates for 1986 wereobtained from previous surveillance.3 For national projectionsof cases, we applied race- and age-specific rates of diseasefrom the total surveillance area to the U.S. population. Racewas handled as a dichotomous variable (black or nonblack) forthese analyses.
Statistical analysis was performed with SAS for Windows (version6.12, SAS Institute, Cary, N.C.) and EpiInfo (version 6.02)software. The chi-square test was used to compare proportions.Relative risks were determined with the Statcalc feature ofEpiInfo.
Results
Bacterial meningitis due to N. meningitidis, H. influenzae,group B streptococcus, L. monocytogenes, and S. pneumoniae wasidentified in 248 residents of the surveillance areas during1995. Nine of these cases were identified by laboratory audit,yielding a sensitivity of 96 percent for surveillance of meningitis(range, 92 to 100 percent, according to area).
The agent most commonly associated with bacterial meningitiswas S. pneumoniae (47 percent of cases), followed by N. meningitidis(25 percent) and group B streptococcus (12 percent) (Table 1).The case fatality rate of meningitis varied significantly accordingto organism (P = 0.02) (Table 1). The median age of the patientswith bacterial meningitis was 25 years.
Table 1. Causes of 248 Cases of Bacterial Meningitis in 1995 and Overall Case Fatality Rate According to Organism.
The predominant agents associated with meningitis varied accordingto age group (Figure 1 and Table 2). The main pathogen causingmeningitis in the neonatal period was group B streptococcus.In infants 1 to 23 months of age, S. pneumoniae (45 percent)and N. meningitidis (31 percent) together caused three quartersof cases of meningitis. Among those 2 to 18 years of age, N.meningitidis caused the majority of cases (59 percent). S. pneumoniaecaused 62 percent of meningitis cases in persons 19 years ofage or older. Only about one third (31 percent) of bacterialmeningitis cases due to these pathogens occurred in childrenunder five years of age.
Table 2. Age-Specific Incidence in 1995 of Bacterial Meningitis and of All Invasive Bacterial Disease.
The rates of meningitis due to S. pneumoniae, N. meningitidis,and group B streptococcus were significantly higher among blacks,with relative risks ranging from 2.1 to 2.6. The rates of meningitisdue to H. influenzae did not differ according to race.
The age- and race-specific rates of disease in the surveillancepopulation were used to estimate the total number of cases ofbacterial meningitis due to the five pathogens in the UnitedStates in 1995 (Figure 2).
Figure 2. Projected Number of Cases of Bacterial Meningitis in the United States in 1995, According to Pathogenic Agent and Age Group.
Race-specific rates from a multistate population of 10.2 million were projected to the racial distribution of the United States to obtain these totals.
Haemophilus Influenzae
H. influenzae was associated with meningitis in 18 of the 181H. influenzae infections (10 percent). Of the 12 cases of meningitisfor which the serotype was determined, serotype b was identifiedin 4. Three cases of meningitis occurred among children underfive years old, two of whom had serotype b disease. None ofthe three was reported to have received H. influenzae type bvaccine. Ampicillin susceptibility was reported for 12 casesof H. influenzae meningitis. Isolates were reported as susceptiblein nine cases of H. influenzae meningitis, intermediate in two,and resistant to ampicillin in one. Invasive H. influenzae diseasedue to other capsular serotypes was identified in 15 cases (serotypef, 11 cases; serotype a, 2 cases; and serotype e, 2 cases).Only 1 of these 15 cases occurred in a person under five yearsof age.
Streptococcus pneumoniae
Meningitis occurred in 117 of the 2679 invasive infections dueto S. pneumoniae (4 percent). Although meningitis was rare inall age groups, the clinical presentations of meningitis dueto other pathogens varied according to age. Overall, bacteremicpneumonia accounted for 1230 of the cases of invasive pneumococcaldisease (46 percent), and bacteremia with no other focus accountedfor 1176 of such cases (44 percent). Most cases (374 of 537,or 70 percent) of invasive pneumococcal disease among childrenunder 5 years old presented as bacteremia without a focus ofinfection, whereas the majority of cases (1078 of 1901, or 57percent) of invasive disease in persons over 18 years of agepresented as bacteremic pneumonia. The case fatality rate forpneumococcal meningitis was 21 percent (23 of 112 patients),significantly higher than the case fatality rate of 13 percentassociated with invasive pneumococcal pneumonia (151 of 1200patients) or the case fatality rate of 8 percent (95 of 1132patients) in bacteremia without a focus.
The case fatality rate also varied according to age. Invasivecases among persons 60 years of age or older were three timesas likely to be fatal (20 percent vs. 7 percent; relative risk,3.0; 95 percent confidence interval, 2.4 to 3.8; P<0.001).Only 1 percent of cases of invasive pneumococcal disease amongchildren under the age of two years were fatal. Isolates from84 of 117 cases of pneumococcal meningitis were tested for susceptibilityto penicillin. Fifty-four isolates (64 percent) were susceptibleto penicillin (minimal inhibitory concentration [MIC] of penicillin,0.06 µg per milliliter or less); 18 isolates (21 percent)had intermediate susceptibility (MIC, 0.12 to 1.00 µgper milliliter), and 12 isolates (14 percent) were resistantto penicillin (MIC, 2.00 µg per milliliter or more). Theproportion of isolates from cases of pneumococcal meningitisthat were susceptible to penicillin differed significantly amongthe four areas (P = 0.007). In San Francisco 15 of 18 isolates(83 percent) were susceptible to penicillin; in Tennessee only4 of 14 isolates (29 percent) were susceptible.
Neisseria meningitidis
Meningitis was diagnosed in 62 of 130 cases of invasive diseasedue to N. meningitidis (48 percent). Other clinical syndromesassociated with N. meningitidis were bacteremia (62 cases; 48percent) and bacteremic pneumonia (4 cases; 3 percent). Thecase fatality rate was 11 percent (14 of 124 cases) for allinvasive disease, but it was significantly higher for meningococcalbacteremia (17 percent) than for meningococcal meningitis (3percent, P<0.05). Most cases of invasive disease due to N.meningitidis occurred in children and young adults; 56 percentof meningococcal cases occurred in persons 18 years of age oryounger, and 67 percent occurred among persons under 30. Of130 cases of invasive meningococcal disease, 96 isolates (74percent) were serogrouped. Serogroup C was the most common isolatein three areas, accounting for 39 percent of all isolates thatwere serogrouped. In Maryland, serogroup Y was the most commonserogroup, accounting for 32 percent of all isolates that wereserogrouped.
Group B Streptococcus
Meningitis accounted for 4 percent of all cases of invasivedisease due to group B streptococcus. Six percent of cases ofgroup B streptococcal disease among newborns were diagnosedas meningitis, as compared with less than 1 percent of casesamong persons 60 years of age or older. Of the pathogens undersurveillance, group B streptococcus was the dominant cause bothof meningitis and of all invasive disease among newborns. Fifty-twopercent (16 of 31) of all cases of group B streptococcal meningitisoccurred during the first month of life. Sixty-one percent (508of 829) of all cases of invasive disease due to group B streptococcusoccurred in persons 19 years of age or older. The case fatalityrate was similar for meningitis and for other group B streptococcalinvasive syndromes (7 percent vs. 10 percent, P not significant).The case fatality rate for all group B streptococcal invasivedisease was higher among persons 60 years of age or older (18percent) than in those under 60 (6 percent).
Listeria monocytogenes
Meningitis occurred in 36 percent of all cases of invasive listeriosis.All five listerial infections in newborns were associated withmeningitis, as compared with 30 percent of the listerial infectionsin older persons (P = 0.004 by Fisher's exact test). Forty-fivepercent of cases of invasive disease due to L. monocytogenesoccurred in persons 60 years of age or older. Serotype datawere available for 41 invasive cases (75 percent). Serotypes4b and 1/2b each caused 39 percent of the cases.
Discussion
Until recently, bacterial meningitis was a greatly feared infectiousdisease because it struck and killed rapidly, many of its victimswere children, and as many as 25 percent of survivors had sequelaesuch as permanent brain damage, mental retardation, or hearingloss. There were once 10,000 to 20,000 cases each year in theUnited States,3 but there have been major efforts to improvetreatment8 and prevent bacterial meningitis.
Over a period of just nine years, the median age of patientswith meningitis due to the five pathogens surveyed in this studyhas shifted remarkably: from 15 months in 1986 to 25 years in1995. In 1986, two thirds of patients with bacterial meningitiswere between one month and five years of age. By 1995, meningitisin this age group had dropped by 87 percent, resulting in adecline of 55 percent for all cases of bacterial meningitis.This achievement highlights the ultimate advantage of preventionover improvements in therapy and suggests the tremendous benefitsfor children throughout the world if access to the vaccine couldbe expanded.
Population-based studies from the 1970s and 1980s demonstratedthat five pathogens — H. influenzae type b, S. pneumoniae,N. meningitidis, group B streptococcus, and L. monocytogenes3,10,11,12— caused at least 80 percent of all cases of bacterialmeningitis. These studies, as well as the current one, clearlyshowed that the relative importance of these pathogens differsaccording to age. Treatment and prevention programs have beendesigned to address these age-specific patterns.
There were efforts to improve antibiotic therapy for bacterialmeningitis8 and to reduce neurologic sequelae by administeringcorticosteroids to acutely ill children. Although slight declineswere noted in mortality due to meningitis caused by each ofthe three main agents during the 1980s,13 major improvementsin survival and reduction of long-term morbidity did not occurover the past several decades, and antibiotic resistance inH. influenzae type b14,15 and S. pneumoniae16 began to appearin the United States during the late 1970s and early 1990s,respectively, complicating efforts to improve clinical outcomethrough treatment regimens.
In parallel with advances in therapy, vaccine development wasaggressively pursued.17,18,19 The first vaccines for H. influenzaetype b, S. pneumoniae, and N. meningitidis became availablein the 1960s and 1970s. Based on the polysaccharide capsulesof their respective organisms, these vaccines could induce protectiveresponses in older children and adults, but their effectivenessin young infants was variable. Conjugation to a carrier proteinwas used to convert H. influenzae type b polysaccharide intoa T-cell–dependent antigen that could induce immune responsesin young infants. After licensure and the recommendation thatH. influenzae type b conjugate vaccines be used routinely fortwo-year-old children, and then, in 1990, for two-month-oldinfants, the incidence of H. influenzae type b meningitis andinvasive disease dropped dramatically,4 partly because of theunexpected impact of vaccines on nasopharyngeal carriage.20,21,22In our surveillance areas, serotype b has not been replacedby other types of H. influenzae. Thus, our data confirm thatthe introduction of H. influenzae type b vaccines produced amajor change in the epidemiology of bacterial meningitis inthe United States (Figure 3 and Table 3).
Figure 3. Number of Cases of Bacterial Meningitis Due to Five Major Pathogens in the United States in 1986 and 1995 According to Age Group.
Race-specific rates from a multistate population of 34 million in 1986 and 10.2 million in 1995 were projected to the racial distribution of the United States to obtain these totals. The five pathogens were N. meningitidis, H. influenzae, L. monocytogenes, group B streptococcus, and S. pneumoniae.
Table 3. Incidence in 1986 and 1995 of Bacterial Meningitis and Total Invasive Disease.
Vaccines against other causes of meningitis raise the hope offurther progress in the prevention of meningitis, but theseother pathogens present more complicated challenges. Meningococci,unlike the other encapsulated bacteria, sometimes cause epidemics.Recent outbreaks of serogroup C meningococcal disease in NorthAmerica led to the immunization of millions of children withthe polysaccharide vaccine.23,24 Meningococci are now the principalcause of bacterial meningitis among persons 2 to 18 years ofage. Although the total number of cases of invasive diseasecaused by meningococci in children and young adults is far lowerthan the number caused by pneumococci, the numbers of deathsin this age group due to the two pathogens are similar. Further,meningococcal disease places a burden on the public health system,since each case requires local public health personnel to ensurethat chemoprophylaxis is administered to household and otherclose contacts.25
Several difficult hurdles must be cleared before preventionof meningococcal disease through routine immunization can becomea reality. The risk of contracting meningococcal disease extendsfrom infancy through early adulthood, so effective vaccinesmust either provide long-term protection or be administeredrepeatedly during childhood and adolescence. Meningococcal vaccinesmust protect against multiple capsular groups. New serogroupA and C meningococcal conjugate vaccines with enhanced immunogenicityin children are now undergoing clinical trials. The serogroupB capsule is not immunogenic in humans, so immunization strategieshave focused primarily on noncapsular antigens,26 and severalvaccines of moderate efficacy in older children and adults havebeen developed from specific strains of serogroup B meningococci.27,28However, strain-specific differences in expression of theseantigens suggest that these vaccines may not provide protectionagainst all serogroup B meningococci. In addition, efficacyin young children has not been demonstrated.29
Pneumococci pose a similar prevention problem not only for adults,for whom they are the primary cause of both pneumonia and meningitis,but also for children under five years old. Our data show that,in the absence of H. influenzae type b, pneumococci are nowthe principal cause of invasive bacterial disease in this group.Although polysaccharide vaccines are available for use in childrenolder than 2 years and in adults at risk, coverage among adultsover 65 years of age was recently estimated to be only 28 to30 percent.30 Additional efforts to use the available vaccinescould further reduce the incidence of bacterial meningitis inadults but would probably have little effect on the remainingincidence in children. Conjugate pneumococcal vaccines are nowundergoing clinical trials, although the large number of capsularserotypes needed for a useful pneumococcal vaccine makes thetask complex and costly. The primary motivation for the developmentof these vaccines is to prevent disease in children, but theymay also be more effective in adults.
In neonates, group B streptococcus is the most common pathogenassociated with meningitis, and L. monocytogenes also causesdisease. Vaccines are not yet available for the prevention ofneonatal meningitis, but other prevention strategies are beingpromoted. Consensus recommendations for the administration ofantibiotics during labor to women at risk for transmitting groupB streptococcus to their newborns have recently been issued.31,32,33Appropriate implementation of these recommendations could reduceneonatal group B streptococcal disease by more than 60 percent.Further disease control may result from the use of group B streptococcalconjugate vaccines, which are undergoing clinical trials.34Enhanced efforts to reduce the contamination of processed foodsby L. monocytogenes and dietary recommendations for personsat risk may have contributed to a recent decrease in diseasedue to L. monocytogenes.35,36
Our data can be used to assess the burden of disease and thusset priorities for vaccine development and use. However, certainlimitations should be noted. Our surveillance system did notrecord cases of clinical meningitis without positive culturesof cerebrospinal fluid or blood and may have underestimatedthe real burden caused by these infections. We did not determinewhether there has been a reduction in the use of lumbar puncturesfor suspected meningitis, which could reduce the sensitivityof our surveillance method. We did not assess disease causedby pathogens other than the five major agents identified inearlier studies, although enteric pathogens are an importantcause of neonatal meningitis. As a component of community-acquiredbacterial meningitis, however, such pathogens are not likelyto constitute a major burden of disease.
Widespread use of H. influenzae type b conjugate vaccines hasdrastically reduced the threat of bacterial meningitis in childrenfrom one month to five years of age. Prevention programs forgroup B streptococcal infections and for listeriosis may furtherreduce the disease burden, even without the introduction ofnew vaccines. We need continued evaluation of the epidemiologyof the disease to identify appropriate targets for immunizationor other preventive strategies. Surveillance linked to laboratorycharacterization of isolates is critical to the developmentof appropriate vaccines, as illustrated by the recent emergenceof serogroup Y meningococci,37 serotype V group B streptococcus,38and antibiotic-resistant pneumococci.39 The development of effectivevaccines for the meningococcus, the pneumococcus, and groupB streptococcus raises the hope of making bacterial meningitislargely a problem of the past.
Supported in part by the National Vaccine Program Office andthe National Center for Infectious Diseases Emerging InfectionPrograms.
* The members of the Active Surveillance Team are listed in theAppendix.
Source Information
From the Respiratory Diseases Branch (A.S., K.R., J.D.W.) and the Meningitis and Special Pathogens Branch (B.A.P.), Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta; Johns Hopkins School of Hygiene and Public Health, Baltimore (L.H.H.); Veterans Affairs Medical Services and Emory University School of Medicine, Atlanta (M.F.); the California Emerging Infections Program, Berkeley (A.L.R.); and Vanderbilt Medical Center, Nashville (L.L.).
Address reprint requests to Dr. Schuchat at Mailstop C-23, Respiratory Diseases Branch, Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, GA 30333.
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