Decline in Invasive Pneumococcal Disease after the Introduction of Protein–Polysaccharide Conjugate Vaccine
Cynthia G. Whitney, M.D., M.P.H., Monica M. Farley, M.D., James Hadler, M.D., M.P.H., Lee H. Harrison, M.D., Nancy M. Bennett, M.D., Ruth Lynfield, M.D., Arthur Reingold, M.D., Paul R. Cieslak, M.D., Tamara Pilishvili, M.P.H., Delois Jackson, M.S.A., Richard R. Facklam, Ph.D., James H. Jorgensen, Ph.D., Anne Schuchat, M.D., for the Active Bacterial Core Surveillance of the Emerging Infections Program Network
Background In early 2000, a protein–polysaccharide conjugatevaccine targeting seven pneumococcal serotypes was licensedin the United States for use in young children.
Methods We examined population-based data from the Active BacterialCore Surveillance of the Centers for Disease Control and Preventionto evaluate changes in the burden of invasive disease, definedby isolation of Streptococcus pneumoniae from a normally sterilesite. Serotyping and susceptibility testing of isolates wereperformed. We assessed trends using data from seven geographicareas with continuous participation from 1998 through 2001 (population,16 million).
Conclusions The use of the pneumococcal conjugate vaccine ispreventing disease in young children, for whom the vaccine isindicated, and may be reducing the rate of disease in adults.The vaccine provides an effective new tool for reducing diseasecaused by drug-resistant strains.
The efficacy of the vaccine in infants given fewer than fourdoses or in older children is unknown. Because the vaccine doesnot include most of the 90 pneumococcal serotypes, an increasein disease caused by serotypes not included in the vaccine ornot related to those in the vaccine is possible; this effectwas seen during a clinical trial evaluating its efficacy againstotitis media.5 Whether vaccination of young children will reducecarriage and subsequently affect disease in other age groupsis unclear. To evaluate these questions, we examined data fromthe Active Bacterial Core Surveillance of the Centers for DiseaseControl and Prevention (CDC).
Methods
The Active Bacterial Core Surveillance, which is part of theEmerging Infections Program Network of the CDC, is an active,population-based, laboratory-based surveillance system. BetweenJanuary 1, 1996, and December 31, 2001, the Active BacterialCore Surveillance continuously monitored invasive pneumococcalinfections in Portland, Oregon (three counties); San FranciscoCounty, California; Minneapolis and St. Paul, Minnesota (sevencounties); the Baltimore metropolitan area in Maryland (sixcounties); the state of Connecticut; and the Atlanta, Georgia,metropolitan area (eight counties). In 1998, the Atlanta sitewas expanded to include 12 additional counties, and surveillancebegan in Rochester, New York (7 counties). The total populationunder surveillance in 2000 was 16.0 million persons, including433,591 children under two years of age and 652,551 childrenfrom two through four years of age.
A case of invasive pneumococcal disease was defined by the isolationof Streptococcus pneumoniae from a sample of normally sterilebody fluid taken from a surveillance-area resident. To identifycases, surveillance personnel periodically contacted all clinicalmicrobiology laboratories in their areas and conducted auditsof laboratory records at least every six months to ensure completereporting. Data on patients were collected with the use of astandardized questionnaire that elicited information on demographicfeatures, clinical syndromes, and disease outcomes. Data onhuman immunodeficiency virus (HIV) infection and the acquiredimmunodeficiency syndrome (AIDS) were collected in five sites(all except Georgia and New York State). The addition of theNew York site and the expansion of the Georgia site, both beginningin January 1998, were the only changes made to the Active BacterialCore Surveillance between 1996 and 2001; no changes were madein methods of data collection.
Pneumococcal isolates were sent to reference laboratories forserotyping by the quellung reaction. Isolates from Minnesotawere tested at the Minnesota Department of Health, and all otherswere tested at the CDC. Vaccine-type strains included serotypes4, 6B, 9V, 14, 18C, 19F, and 23F. We defined vaccine-relatedstrains as pneumococci with serotypes within the same serogroupas the vaccine types (6A, 9A, 9L, 9N, 18A, 18B, 18F, 19A, 19B,19C, 23A, and 23B). All other serotypes were considered nonvaccinetypes. Serotypes in the 23-valent polysaccharide vaccine butnot in the conjugate vaccine included 1, 2, 3, 5, 7F, 8, 10A,11A, 12F, 15B, 20, 22F, and 33F.
Susceptibility testing of isolates was performed with the useof broth microdilution13 at the CDC, the Minnesota Departmentof Health, or the University of Texas Health Science Centerat San Antonio. Isolates were defined as susceptible, of intermediatesusceptibility, or resistant according to the 2002 definitionsof the National Committee for Clinical Laboratory Standards.13Isolates with intermediate susceptibility and resistant isolateswere classified as nonsusceptible. Strains that were nonsusceptibleto three or more drug classes were considered to be multiplyresistant.
Annual cumulative incidence rates were calculated for 1996 through1999 on the basis of population estimates from the U.S. CensusBureau for those years; the rates for 2000 and 2001 were calculatedfrom 2000 Census data. To calculate serotype-specific diseaserates, we assumed that the distribution of serotypes for caseswith missing serotype data (11.7 percent of cases) was the sameas the distribution for cases with serotype information available.The same method was used to impute missing data on race (11.0percent) and hospitalization (0.2 percent). To verify the results,the analyses of rates were repeated with only cases with completedata included. The rates are reported as cases per 100,000 population.
To assess changes in disease rates after the introduction ofvaccination, we calculated the numbers of cases and noncasesin the surveillance population, using Active Bacterial CoreSurveillance data and U.S. Census figures. We then used thechi-square test or Fisher's exact test to compare the proportionof the population who had invasive disease in the years followingthe introduction of vaccination (2000 or 2001) with a base-linerate (either the average rate for 1998 and 1999 combined orthe rate for 1999 alone). We calculated Pearson's correlationcoefficients to match the changes in disease rates among adultsto those among children. Statistical analyses were conductedwith SAS, version 8.0, and Epi Info, version 6.0,14 software.We calculated 95 percent confidence intervals, and two-sidedP values that were less than 0.05 were considered to indicatestatistical significance.
Results
During the period from 1998 through 2001, a total of 13,568cases of invasive pneumococcal disease were identified; isolateswere available for 11,992 (88 percent). The rates of invasivedisease in 1998, 1999, 2000, and 2001 were 24.2, 24.4, 21.2,and 17.3 cases per 100,000 persons, respectively. The averagefor the base-line period of 1998 and 1999 was 24.3 per 100,000.
Children under Five Years of Age
From 1998 through 2001, 3285 cases of invasive pneumococcaldisease were identified in children under five years of age.The rate declined by 59 percent (95 percent confidence interval,54 to 63 percent), from an average of 96.4 cases per 100,000in 1998 and 1999 to 39.7 per 100,000 in 2001. Significant declinesin disease rates occurred among children two years old or less(59.0 cases per 100,000 in 2001, as compared with 188.0 per100,000 in 1998 and 1999) (Figure 1). As compared with the base-linevalues for 1998 and 1999 combined, the rates of disease in 2000were 17 percent lower among children under 12 months old (139.3cases per 100,000 vs. 168.1; 95 percent confidence interval,5 to 28 percent) and 27 percent lower among children 12 to 23months old (152.7 cases per 100,000 vs. 208.2; 95 percent confidenceinterval, 17 to 35 percent); by 2001, the disease rates were69 percent lower (52.3 cases per 100,000 vs. 168.1; 95 percentconfidence interval, 62 to 75 percent) and 68 percent lower(65.8 vs. 208.2; 95 percent confidence interval, 62 to 74 percent),respectively, in these age groups (P<0.001 for all comparisons).In children 24 to 35 months old, the rate was 44 percent lowerin 2001 than in 1998 and 1999 (35.6 cases per 100,000 vs. 63.3;95 percent confidence interval, 27 to 56 percent). For childrenwho were three or four years of age, the rates in 2001 werenot significantly different from the base-line values.
Figure 1. Rates of Invasive Pneumococcal Disease among Children under Five Years Old, According to Age and Year.
Data are from the Active Bacterial Core Surveillance from 1996 through 2001. The 1996 and 1997 rates do not include data from New York State. Asterisks indicate P<0.05 for comparisons of the rate in 2000 or 2001 with the combined rate for 1998 and 1999.
Among children under two years of age, the magnitude of thedecline from 1998 and 1999 to 2001 was substantially largerfor black children (from 437.6 cases per 100,000 to 119.6) thanfor white children (from 132.7 to 50.6). However, the percentchanges were similar: a 73 percent decline among blacks (95percent confidence interval, 66 to 78 percent) and a 62 percentdecline among whites (95 percent confidence interval, 55 to68 percent). The percent change in the rate of disease requiringhospitalization (from 56.8 cases per 100,000 to 21.2, a declineof 63 percent) among children under two years of age was notsignificantly different from the percent change in the rateof disease treated without hospitalization (from 132.7 to 38.1,a decline of 71 percent). Likewise, the percent change in therate of pneumococcal meningitis (from 10.3 cases per 100,000to 4.2, a decline of 59 percent) was similar to that for therate of other syndromes (from 179.4 to 55.8, a decline of 69percent). The percent change in the rate of disease was largestin California, with a decline of 85 percent (95 percent confidenceinterval, 37 to 96 percent), and New York State, with a declineof 83 percent (95 percent confidence interval, 67 to 92 percent),and smallest in Oregon, with a decline of 38 percent (95 percentconfidence interval, 2 to 61 percent) (Figure 2).
Figure 2. Percent Changes in the Rates of Invasive Pneumococcal Disease, According to Age Group and the State in Which the Active Bacterial Core Surveillance Site Was Located.
The percent decline was calculated by comparing the incidence in 2001 with the average incidence in 1998 and 1999. Within states, the decline among children under 2 years old correlated significantly with the decline among persons 20 to 39 years of age (r=0.89, P=0.008), but not with the decline among persons 40 to 64 years of age (r=–0.09, P=0.85) or 65 years or older (r=0.36, P=0.42).
For children under two years of age, the rate of disease dueto vaccine serotypes declined by 78 percent overall; significantdeclines in disease were seen for all individual serotypes includedin the vaccine (Table 1). As compared with base line, the rateof disease due to vaccine-related strains as a group was 50percent lower in 2001. The rate of disease due to nonvaccineserotypes was 27 percent higher in 2001, but this change wasnot statistically significant.
Table 1. Changes in Estimated Rates of Invasive Pneumococcal Disease among Children under Two Years of Age, According to Year and Serotype, from 1998 through 2001.
Persons Five Years of Age or Older
Disease rates also fell among persons for whom the vaccine isnot recommended (Figure 3). Although no significant change wasobserved among persons 5 through 19 years of age, the rate ofdisease among persons 20 through 39 years of age was 21 percentlower in 2000 than at base line in 1998 and 1999 (8.9 casesper 100,000 vs. 11.2; 95 percent confidence interval, 11 to29 percent) and 32 percent lower in 2001 (7.6 vs. 11.2; 95 percentconfidence interval, 23 to 39 percent; P<0.001). The rateswere significantly lower both for disease caused by vaccineserotypes and for disease caused by nonvaccine serotypes, althoughthe decline was larger for the former (Table 2). Significantdeclines were noted in disease caused by some individual serotypesincluded in the vaccine, particularly 4, 9V, 14, and 19F. Withinsurveillance sites, the size of the decline among persons 20to 39 years of age correlated with the size of the decline amongchildren under 2 years old (r=0.89, P=0.008) (Figure 2). Insites where information on HIV infection and AIDS was recorded,the number of cases in persons without known HIV infection orAIDS dropped by 38 percent, from 270.5 in 1998 and 1999 to 168.0in 2001; there was no significant change in the number of casesin persons with HIV or AIDS (an average of 81 cases in 1998and 1999 and 82 cases in 2001).
Figure 3. Rates of Invasive Pneumococcal Disease among Persons at Least Five Years Old, According to Age Group and Year.
Data are from the Active Bacterial Core Surveillance from 1996 through 2001. The 1996 and 1997 rates do not include data from New York State. Asterisks indicate P<0.05 for comparisons of the rate in 2000 or 2001 with the combined rate for 1998 and 1999.
Table 2. Changes in Estimated Rates of Invasive Pneumococcal Disease among Adults, According to Age Group, Year, and Serotype, from 1998 through 2001.
Among persons 40 to 64 years of age, the overall rate of diseasewas 8 percent lower in 2001 than in 1998 and 1999 (19.7 casesper 100,000 vs. 21.5; 95 percent confidence interval, 1 to 15percent; P=0.03) (Figure 3). The change in the overall rateof disease in this age group was primarily due to a declinein the rate of disease caused by serotypes included in the vaccine(Table 2). Among the individual serotypes included in the vaccine,only the change in the rate of disease due to serotype 14 wasstatistically significant.
Among persons 65 years of age or older, the rate of diseasewas 18 percent lower in 2001 than at base line (49.5 cases per100,000 vs. 60.1; 95 percent confidence interval, 11 to 24 percent;P<0.001) (Figure 3). The rates were lower for disease causedby vaccine serotypes and vaccine-related serotypes; significantdeclines were seen for disease caused by vaccine serotypes 4,9V, 14, and 23F (Table 2). The rate of disease caused by serotypesincluded in the 23-valent polysaccharide vaccine and not inthe conjugate vaccine was the same in 2001 as in 1998 and 1999(11.9 cases per 100,000).
Among nonvaccine serotypes, the rate of serotype 1 disease waslower in some adult age groups in 2001 than in 1998 and 1999:for those between 40 and 64 years old, the rate declined from0.5 to 0.1 case per 100,000 (P<0.001), and for those 65 yearsof age or older, the rate declined from 0.7 to 0.3 (P=0.05).The rate of serotype 5 disease was higher in 2001 than in 1998and 1999 among persons 20 to 39 years old and those 40 to 64years old, but this change was attributable to an increase inthe number of cases caused by serotype 5 in one surveillancesite (California), which had 1 isolate in 1998 and 1999 and14 isolates in 2001.
Drug-Resistant Invasive Disease
The proportion of isolates that were not susceptible to penicillindecreased slightly between 1999 (861 of 3355, 26 percent) and2001 (589 of 2495, 24 percent; P=0.08). In 1999, 11 percentof isolates were of intermediate susceptibility to penicillinand 15 percent were resistant; in 2001, 10 percent were of intermediatesusceptibility and 14 percent were resistant. Between 1999 and2001, the change in the rate of disease caused by strains thatwere not susceptible to penicillin (from 6.3 to 4.1, a declineof 35 percent; 95 percent confidence interval, 28 to 41 percent;P<0.001) did not differ significantly from the change inthe rate of disease caused by penicillin-susceptible strains(from 18.1 to 13.1, a decline of 28 percent; 95 percent confidenceinterval, 23 to 31 percent).
Among children under two years of age, the proportion of isolatesnot susceptible to penicillin was 38 percent in 1999 (258 of684) and 35 percent in 2001 (77 of 218) (P=0.58); the rate ofdisease caused by penicillin-nonsusceptible and penicillin-susceptiblestrains fell by 70 percent (from 70.0 to 20.9; 95 percent confidenceinterval, 62 to 77 percent) and 67 percent (from 115.5 to 38.5;95 percent confidence interval, 60 to 72 percent), respectively.The rate of disease due to penicillin-nonsusceptible strainsalso declined significantly among persons 65 years of age orolder (from 16.7 to 12.6, a decline of 25 percent; 95 percentconfidence interval, 9 to 36 percent). The percent changes inthe rate of disease caused by erythromycin-resistant and multidrug-resistantstrains were similar to those in the rate of disease causedby penicillin-resistant strains.
We cannot determine to what extent the observed changes aredue to the introduction of vaccination or to other factors.Certain findings, such as the significant decline in non–vaccine-typedisease in adults 20 to 39 years of age, suggest that seculartrends may explain some of the observations. However, we foundno change in the rate of disease caused by pneumococci withserotypes unique to the polysaccharide vaccine or in the numberof cases in persons with HIV infection, results suggesting thatthe increasing use of polysaccharide vaccine and highly activeantiretroviral therapy does not explain our findings. The percentchange in the rate of disease among children was similar forhospitalized patients and outpatients and for pneumococcal meningitisand other syndromes, suggesting that changes in culturing practicesdid not explain the observed decline.
Preventing pneumococcal disease is a priority for the UnitedStates. The Healthy People 2010 objectives include decreasingthe incidence of invasive pneumococcal infections to 46 casesper 100,000 persons under 5 years of age and to 42 per 100,000persons 65 years of age or older.23 The target for childrenhas been met, and we are closer to the goal for adults. Moredata are also needed to determine how far disease rates willfall as vaccine coverage increases and to assess the effectof the vaccine on pneumonia and other noninvasive syndromes.Whether vaccine use will slow the emergence of resistant pneumococciand whether disease due to pneumococci with nonvaccine serotypeswill become more common are questions that do not yet have definitiveanswers. Although questions remain, our data indicate that thepneumococcal conjugate vaccine is working well in the U.S. population.
Supported by the Emerging Infections Program of the Centersfor Disease Control and Prevention.
Presented in part at the 41st Interscience Conference on AntimicrobialAgents and Chemotherapy, Chicago, December 16–19, 2001(abstract G-2041); the 3rd International Symposium on Pneumococciand Pneumococcal Diseases, Anchorage, Alaska, May 5–8,2002; and the 42nd Interscience Conference on AntimicrobialAgents and Chemotherapy, San Diego, Calif., September 27–30,2002 (abstract G-1068).
We are indebted to Wendy Baughman, Pam Daily, Peggy Pass, NancyBarrett, Shelly Zansky, Karen Stefonek, Brenda Barnes, DavidStephens, Catherine Lexau, Rich Danila, Sue Johnson, John Besser,Allen Craig, William Schaffner, Elizabeth Zell, Tami HilgerSkoff, Chris Van Beneden, Katherine Deaver Robinson, CarolynWright, M. Leticia McElmeel, Sharon A. Crawford, John Elliot,Ruth Franklin, Andrea Hertz, LaShondra Shealey, and the personnelof the hospitals and laboratories participating in the ActiveBacterial Core Surveillance for their contributions to thisproject.
Source Information
From the Division of Bacterial and Mycotic Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta (C.G.W., T.P., D.J., R.R.F., A.S.); Emory University School of Medicine and the Veterans Affairs Medical Center, Atlanta (M.M.F.); the Connecticut Department of Public Health, Hartford (J.H.); Johns Hopkins University Bloomberg School of Public Health, Baltimore (L.H.H.); the Monroe County Department of Health and the University of Rochester, Rochester, N.Y. (N.M.B.); the Minnesota Department of Health, Minneapolis (R.L.); the School of Public Health, University of California, Berkeley (A.R.); the Oregon Department of Human Services, Health Division, Portland (P.R.C.); and the University of Texas Health Science Center, San Antonio (J.H.J.).
Address reprint requests to Dr. Whitney at CDC Mailstop C-23, 1600 Clifton Rd. NE, Atlanta, GA 30333, or at cwhitney{at}cdc.gov.
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Onwubiko, C., Swiatlo, E., McDaniel, L. S.
(2008). Cross-Sectional Study of Nasopharyngeal Carriage of Streptococcus pneumoniae in Human Immunodeficiency Virus-Infected Adults in the Conjugate Vaccine Era. J. Clin. Microbiol.
46: 3621-3625
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Hotomi, M., Billal, D. S., Kamide, Y., Kanesada, K., Uno, Y., Kudo, F., Ito, M., Kakehata, S., Sugita, R., Ogami, M., Yamanaka, N., for the Advanced Treatment for Otitis Media Study,
(2008). Serotype Distribution and Penicillin Resistance of Streptococcus pneumoniae Isolates from Middle Ear Fluids of Pediatric Patients with Acute Otitis Media in Japan. J. Clin. Microbiol.
46: 3808-3810
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Farrell, D. J., Felmingham, D., Shackcloth, J., Williams, L., Maher, K., Hope, R., Livermore, D. M., George, R. C., Brick, G., Martin, S., Reynolds, R., on behalf of the BSAC Working Parties on Resistanc,
(2008). Non-susceptibility trends and serotype distributions among Streptococcus pneumoniae from community-acquired respiratory tract infections and from bacteraemias in the UK and Ireland, 1999 to 2007. J Antimicrob Chemother
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Eiland, L. S.
(2008). Increasing Prevalence of Pneumococcal Serotype 19A Among US Children. Journal of Pharmacy Practice
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Azzari, C., Moriondo, M., Indolfi, G., Massai, C., Becciolini, L., de Martino, M., Resti, M.
(2008). Molecular detection methods and serotyping performed directly on clinical samples improve diagnostic sensitivity and reveal increased incidence of invasive disease by Streptococcus pneumoniae in Italian children. J Med Microbiol
57: 1205-1212
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Nigrovic, L. E., Malley, R., Macias, C. G., Kanegaye, J. T., Moro-Sutherland, D. M., Schremmer, R. D., Schwab, S. H., Agrawal, D., Mansour, K. M., Bennett, J. E., Katsogridakis, Y. L., Mohseni, M. M., Bulloch, B., Steele, D. W., Kaplan, R. L., Herman, M. I., Bandyopadhyay, S., Dayan, P., Truong, U. T., Wang, V. J., Bonsu, B. K., Chapman, J. L., Kuppermann, N., for the American Academy of Pediatrics, Pediatric,
(2008). Effect of Antibiotic Pretreatment on Cerebrospinal Fluid Profiles of Children With Bacterial Meningitis. Pediatrics
122: 726-730
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Amrine-Madsen, H., Van Eldere, J., Mera, R. M., Miller, L. A., Poupard, J. A., Thomas, E. S., Halsey, W. S., Becker, J. A., O'Hara, F. P.
(2008). Temporal and Spatial Distribution of Clonal Complexes of Streptococcus pneumoniae Isolates Resistant to Multiple Classes of Antibiotics in Belgium, 1997 to 2004. Antimicrob. Agents Chemother.
52: 3216-3220
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Rubin, L. G., Rizvi, A., Baer, A.
(2008). Effect of Swab Composition and Use of Swabs versus Swab-Containing Skim Milk-Tryptone-Glucose-Glycerol (STGG) on Culture- or PCR-Based Detection of Streptococcus pneumoniae in Simulated and Clinical Respiratory Specimens in STGG Transport Medium. J. Clin. Microbiol.
46: 2635-2640
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Ampofo, K., Bender, J., Sheng, X., Korgenski, K., Daly, J., Pavia, A. T., Byington, C. L.
(2008). Seasonal Invasive Pneumococcal Disease in Children: Role of Preceding Respiratory Viral Infection. Pediatrics
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Critchley, I. A., Jacobs, M. R., Brown, S. D., Traczewski, M. M., Tillotson, G. S., Janjic, N.
(2008). Prevalence of Serotype 19A Streptococcus pneumoniae among Isolates from U.S. Children in 2005-2006 and Activity of Faropenem. Antimicrob. Agents Chemother.
52: 2639-2643
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Ongkasuwan, J., Valdez, T. A., Hulten, K. G., Mason, E. O. Jr, Kaplan, S. L.
(2008). Pneumococcal Mastoiditis in Children and the Emergence of Multidrug-Resistant Serotype 19A Isolates. Pediatrics
122: 34-39
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Foster, D., Knox, K., Walker, A. S., Griffiths, D. T., Moore, H., Haworth, E., Peto, T., Brueggemann, A. B., Crook, D. W., on behalf of the Oxford Invasive Pneumococcal Surv,
(2008). Invasive pneumococcal disease: epidemiology in children and adults prior to implementation of the conjugate vaccine in the Oxfordshire region, England. J Med Microbiol
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(2008). Invasive Pneumococcal Disease in Children 5 Years After Conjugate Vaccine Introduction--Eight States, 1998-2005. JAMA
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Jacobs, M. R., Good, C. E., Beall, B., Bajaksouzian, S., Windau, A. R., Whitney, C. G.
(2008). Changes in Serotypes and Antimicrobial Susceptibility of Invasive Streptococcus pneumoniae Strains in Cleveland: a Quarter Century of Experience. J. Clin. Microbiol.
46: 982-990
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Stucki, A., Gerber, P., Acosta, F., Cottagnoud, M., Cottagnoud, P., Jiang, L., Nguyen, P., Wachtel, D., Wang, G., Phan, L. T.
(2008). Effects of EDP-420 on penicillin-resistant and quinolone- and penicillin-resistant pneumococci in the rabbit meningitis model. J Antimicrob Chemother
61: 665-669
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Schenkein, J. G., Nahm, M. H., Dransfield, M. T.
(2008). Pneumococcal Vaccination for Patients With COPD: Current Practice and Future Directions. Chest
133: 767-774
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Adamkiewicz, T. V., Silk, B. J., Howgate, J., Baughman, W., Strayhorn, G., Sullivan, K., Farley, M. M.
(2008). Effectiveness of the 7-Valent Pneumococcal Conjugate Vaccine in Children With Sickle Cell Disease in the First Decade of Life. Pediatrics
121: 562-569
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Clutterbuck, E. A., Oh, S., Hamaluba, M., Westcar, S., Beverley, P. C. L., Pollard, A. J.
(2008). Serotype-Specific and Age-Dependent Generation of Pneumococcal Polysaccharide-Specific Memory B-Cell and Antibody Responses to Immunization with a Pneumococcal Conjugate Vaccine. CVI
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Yu, J., Carvalho, M. d. G. S., Beall, B., Nahm, M. H.
(2008). A rapid pneumococcal serotyping system based on monoclonal antibodies and PCR. J Med Microbiol
57: 171-178
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Schiff, D.
(2008). Multiresistant Pneumococci in Otitis Media. AAP Grand Rounds
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Flamaing, J., Verhaegen, J., Vandeven, J., Verbiest, N., Peetermans, W. E.
(2008). Pneumococcal bacteraemia in Belgium (1994 2004): the pre-conjugate vaccine era. J Antimicrob Chemother
61: 143-149
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Schut, E. S, de Gans, J., van de Beek, D.
(2008). Community-acquired bacterial meningitis in adults. PN
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Broder, K. R., Cohn, A. C., Schwartz, B., Klein, J. D., Fisher, M. M., Fishbein, D. B., Mijalski, C., Burstein, G. R., Vernon-Smiley, M. E., McCauley, M. M., Wibbelsman, C. J., for the Working Group on Adolescent Prevention Pri,
(2008). Adolescent Immunizations and Other Clinical Preventive Services: A Needle and a Hook?. Pediatrics
121: S25-S34
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(2007). Steroids for bacterial meningitis in children?. DTB
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Zhou, F., Kyaw, M. H., Shefer, A., Winston, C. A., Nuorti, J. P.
(2007). Health Care Utilization for Pneumonia in Young Children After Routine Pneumococcal Conjugate Vaccine Use in the United States. Arch Pediatr Adolesc Med
161: 1162-1168
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Dubos, F, Marechal, I, Husson, M O, Courouble, C, Aurel, M, Martinot, A, the Hospital Network for Evaluating the Management,
(2007). Decline in pneumococcal meningitis after the introduction of the heptavalent-pneumococcal conjugate vaccine in northern France. Arch. Dis. Child.
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Pichichero, M. E., Casey, J. R.
(2007). Emergence of a Multiresistant Serotype 19A Pneumococcal Strain Not Included in the 7-Valent Conjugate Vaccine as an Otopathogen in Children. JAMA
298: 1772-1778
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Treanor, J. D.
(2007). Influenza -- The Goal of Control. NEJM
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Smyth, R. L
(2007). Making a difference: the clinical research programme for children. Arch. Dis. Child.
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Rajam, G., Carlone, G. M., Romero-Steiner, S.
(2007). Functional Antibodies to the O-Acetylated Pneumococcal Serotype 15B Capsular Polysaccharide Have Low Cross-Reactivities with Serotype 15C. CVI
14: 1223-1227
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Dias, C. A., Teixeira, L. M., Carvalho, M. d. G., Beall, B.
(2007). Sequential multiplex PCR for determining capsular serotypes of pneumococci recovered from Brazilian children. J Med Microbiol
56: 1185-1188
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Golnik, A.
(2007). Pneumococcal Meningitis Presenting With a Simple Febrile Seizure and Negative Blood-Culture Result. Pediatrics
120: e428-e431
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Melegaro, A., Choi, Y., Pebody, R., Gay, N.
(2007). Pneumococcal Carriage in United Kingdom Families: Estimating Serotype-specific Transmission Parameters from Longitudinal Data. Am J Epidemiol
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Fimbres, A.
(2007). Can We Predict Occult Pneumonia in Children with Only Fever?. AAP Grand Rounds
18: 8-9
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Ip, M., Nelson, E. A. S., Cheuk, E. S. C., Sung, R. Y. T., Li, A., Ma, H., Chan, P. K. S.
(2007). Serotype Distribution and Antimicrobial Susceptibilities of Nasopharyngeal Isolates of Streptococcus pneumoniae from Children Hospitalized for Acute Respiratory Illnesses in Hong Kong. J. Clin. Microbiol.
45: 1969-1971
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Watson, M., Brett, M., Brown, M., Stewart, M. G., Warren, S., for the New South Wales Pneumococcal Network,
(2007). Pneumococci responsible for invasive disease and discharging ears in children in Sydney, Australia. J Med Microbiol
56: 819-823
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Salt, P., Banner, C., Oh, S., Yu, L.-m., Lewis, S., Pan, D., Griffiths, D., Ferry, B., Pollard, A.
(2007). Social Mixing with Other Children during Infancy Enhances Antibody Response to a Pneumococcal Conjugate Vaccine in Early Childhood. CVI
14: 593-599
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Singleton, R. J., Hennessy, T. W., Bulkow, L. R., Hammitt, L. L., Zulz, T., Hurlburt, D. A., Butler, J. C., Rudolph, K., Parkinson, A.
(2007). Invasive Pneumococcal Disease Caused by Nonvaccine Serotypes Among Alaska Native Children With High Levels of 7-Valent Pneumococcal Conjugate Vaccine Coverage. JAMA
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Peters, T. R., Poehling, K. A.
(2007). Invasive Pneumococcal Disease: The Target Is Moving. JAMA
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Niederman, M. S.
(2007). Recent Advances in Community-Acquired Pneumonia: Inpatient and Outpatient. Chest
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Fasching, C. E., Grossman, T., Corthesy, B., Plaut, A. G., Weiser, J. N., Janoff, E. N.
(2007). Impact of the Molecular Form of Immunoglobulin A on Functional Activity in Defense against Streptococcus pneumoniae. Infect. Immun.
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Poehling, K. A., Szilagyi, P. G., Grijalva, C. G., Martin, S. W., LaFleur, B., Mitchel, E., Barth, R. D., Nuorti, J. P., Griffin, M. R.
(2007). Reduction of Frequent Otitis Media and Pressure-Equalizing Tube Insertions in Children After Introduction of Pneumococcal Conjugate Vaccine. Pediatrics
119: 707-715
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Fine, A. M., Nigrovic, L. E., Reis, B. Y., Cook, E. F., Mandl, K. D.
(2007). Linking Surveillance to Action: Incorporation of Real-time Regional Data into a Medical Decision Rule. J. Am. Med. Inform. Assoc.
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Rand, C. M., Shone, L. P., Albertin, C., Auinger, P., Klein, J. D., Szilagyi, P. G.
(2007). National Health Care Visit Patterns of Adolescents: Implications for Delivery of New Adolescent Vaccines. Arch Pediatr Adolesc Med
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Gherardi, G., Fallico, L., Del Grosso, M., Bonanni, F., D'Ambrosio, F., Manganelli, R., Palu, G., Dicuonzo, G., Pantosti, A.
(2007). Antibiotic-Resistant Invasive Pneumococcal Clones in Italy. J. Clin. Microbiol.
45: 306-312
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Rozen, D. E., McGee, L., Levin, B. R., Klugman, K. P.
(2007). Fitness Costs of Fluoroquinolone Resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother.
51: 412-416
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Nigrovic, L. E., Kuppermann, N., Macias, C. G., Cannavino, C. R., Moro-Sutherland, D. M., Schremmer, R. D., Schwab, S. H., Agrawal, D., Mansour, K. M., Bennett, J. E., Katsogridakis, Y. L., Mohseni, M. M., Bulloch, B., Steele, D. W., Kaplan, R. L., Herman, M. I., Bandyopadhyay, S., Dayan, P., Truong, U. T., Wang, V. J., Bonsu, B. K., Chapman, J. L., Kanegaye, J. T., Malley, R., for the Pediatric Emergency Medicine Collaborative,
(2007). Clinical Prediction Rule for Identifying Children With Cerebrospinal Fluid Pleocytosis at Very Low Risk of Bacterial Meningitis. JAMA
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Abuelreish, M., Subedar, A., Chiu, T., Wludyka, P., Rathore, M.
(2007). Increase in Invasive Pneumococcal Disease in Children Associated With Shortage of Heptavalent Pneumococcal Conjugate Vaccine. CLIN PEDIATR
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Dawid, S., Roche, A. M., Weiser, J. N.
(2007). The blp Bacteriocins of Streptococcus pneumoniae Mediate Intraspecies Competition both In Vitro and In Vivo. Infect. Immun.
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O'Neill, S G, Isenberg, D A
(2006). Immunizing patients with systemic lupus erythematosus: a review of effectiveness and safety. Lupus
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Szilagyi, P. G., Griffin, M. R., Shone, L. P., Barth, R., Zhu, Y., Schaffer, S., Ambrose, S., Roy, J., Poehling, K. A., Edwards, K. M., Walker, F. J., Schwartz, B., for the New Vaccine Surveillance Network,
(2006). The Impact of Conjugate Pneumococcal Vaccination on Routine Childhood Vaccination and Primary Care Use in 2 Counties. Pediatrics
118: 1394-1402
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Burton, R. L., Nahm, M. H.
(2006). Development and Validation of a Fourfold Multiplexed Opsonization Assay (MOPA4) for Pneumococcal Antibodies.. CVI
13: 1004-1009
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Block, S. L.
(2006). Comparative Tolerability, Safety and Efficacy of Tablet Formulations of Twice-Daily Clarithromycin 250 mg versus Once-Daily Extended-Release Clarithromycin 500 mg in Pediatric and Adolescent Patients. CLIN PEDIATR
45: 641-648
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Grijalva, C. G., Poehling, K. A., Nuorti, J. P., Zhu, Y., Martin, S. W., Edwards, K. M., Griffin, M. R.
(2006). National Impact of Universal Childhood Immunization With Pneumococcal Conjugate Vaccine on Outpatient Medical Care Visits in the United States. Pediatrics
118: 865-873
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Vergison, A., Tuerlinckx, D., Verhaegen, J., Malfroot, A., for the Belgian Invasive Pneumococcal Disease Stud,
(2006). Epidemiologic Features of Invasive Pneumococcal Disease in Belgian Children: Passive Surveillance Is Not Enough. Pediatrics
118: e801-e809
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Rathore, M. H.
(2006). PCV7: Impact on Invasive Pneumococcal Disease and Resistant S pneumoniae. AAP Grand Rounds
16: 13-14
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Clarke, S. C.
(2006). Control of pneumococcal disease in the United Kingdom - the start of a new era.. J Med Microbiol
55: 975-980
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Clarke, S. C., Jefferies, J. M. C., Smith, A. J., McMenamin, J., Mitchell, T. J., Edwards, G. F. S.
(2006). Pneumococci causing invasive disease in children prior to the introduction of pneumococcal conjugate vaccine in Scotland.. J Med Microbiol
55: 1079-1084
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Chen, Y.-Y., Yao, S.-M., Chou, C.-Y., Chang, Y.-C., Shen, P.-W., Huang, C.-T., Su, H.-P., Li, S.-Y.
(2006). Surveillance of invasive Streptococcus pneumoniae in Taiwan, 2002-2003.. J Med Microbiol
55: 1109-1114
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Navarro, D., Escribano, A., Cebrian, L., Gimeno, C., Garcia-Maset, L., Garcia-de-Lomas, J., the Spanish Pneumococcal Infection Study Network,
(2006). Type-Specific Antibodies to Pneumococcal Capsular Polysaccharide Acquired either Naturally or after Vaccination with Prevenar in Children with Underlying Chronic or Recurrent Lung Diseases. CVI
13: 665-670
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Kronenberg, A., Zucs, P., Droz, S., Muhlemann, K.
(2006). Distribution and Invasiveness of Streptococcus pneumoniae Serotypes in Switzerland, a Country with Low Antibiotic Selection Pressure, from 2001 to 2004.. J. Clin. Microbiol.
44: 2032-2038
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Garbutt, J., Rosenbloom, I., Wu, J., Storch, G. A.
(2006). Empiric first-line antibiotic treatment of acute otitis in the era of the heptavalent pneumococcal conjugate vaccine.. Pediatrics
117: e1087-e1094
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Poehling, K. A., Talbot, T. R., Griffin, M. R., Craig, A. S., Whitney, C. G., Zell, E., Lexau, C. A., Thomas, A. R., Harrison, L. H., Reingold, A. L., Hadler, J. L., Farley, M. M., Anderson, B. J., Schaffner, W.
(2006). Invasive Pneumococcal Disease Among Infants Before and After Introduction of Pneumococcal Conjugate Vaccine. JAMA
295: 1668-1674
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Kyaw, M. H., Lynfield, R., Schaffner, W., Craig, A. S., Hadler, J., Reingold, A., Thomas, A. R., Harrison, L. H., Bennett, N. M., Farley, M. M., Facklam, R. R., Jorgensen, J. H., Besser, J., Zell, E. R., Schuchat, A., Whitney, C. G., Active Bacterial Core Surveillance of the Emerging,
(2006). Effect of Introduction of the Pneumococcal Conjugate Vaccine on Drug-Resistant Streptococcus pneumoniae. NEJM
354: 1455-1463
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Clarke, S. C., Jefferies, J. M., Smith, A. J., McMenamin, J., Mitchell, T. J., Edwards, G. F. S.
(2006). Potential Impact of Conjugate Vaccine on the Incidence of Invasive Pneumococcal Disease among Children in Scotland. J. Clin. Microbiol.
44: 1224-1228
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Beall, B., McEllistrem, M. C., Gertz, R. E. Jr., Wedel, S., Boxrud, D. J., Gonzalez, A. L., Medina, M.-J., Pai, R., Thompson, T. A., Harrison, L. H., McGee, L., Whitney, C. G., the Active Bacterial Core Surveillance Team,
(2006). Pre- and postvaccination clonal compositions of invasive pneumococcal serotypes for isolates collected in the United States in 1999, 2001, and 2002.. J. Clin. Microbiol.
44: 999-1017
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Lin, J., Kaltoft, M. S., Brandao, A. P., Echaniz-Aviles, G., Brandileone, M. C. C., Hollingshead, S. K., Benjamin, W. H., Nahm, M. H.
(2006). Validation of a Multiplex Pneumococcal Serotyping Assay with Clinical Samples. J. Clin. Microbiol.
44: 383-388
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Finn, A., Jenkinson, H. F.
(2006). The pneumococcus: 'old man's friend' and children's foe. Microbiology
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Hollingshead, S. K., Baril, L., Ferro, S., King, J., Coan, P., Briles, D. E., the Pneumococcal Proteins Epi Study Group,
(2006). Pneumococcal surface protein A (PspA) family distribution among clinical isolates from adults over 50 years of age collected in seven countries. J Med Microbiol
55: 215-221
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van de Beek, D., de Gans, J., Tunkel, A. R., Wijdicks, E. F.M.
(2006). Community-Acquired Bacterial Meningitis in Adults. NEJM
354: 44-53
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