Serotype-specific changes in invasive pneumococcal disease after pneumococcal conjugate vaccine introduction: a pooled analysis of multiple surveillance sites

Daniel R Feikin, Eunice W Kagucia, Jennifer D Loo, Ruth Link-Gelles, Milo A Puhan, Thomas Cherian, Orin S Levine, Cynthia G Whitney, Katherine L O'Brien, Matthew R Moore, Serotype Replacement Study Group, Claire A Adegbola, Mary Agocs, Krow Ampofo, Nick Andrews, Theresa Barton, Javier Benito, Claire V Broome, Michael G Bruce, Lisa R Bulkow, Carrie L Byington, Teresa Camou, Thomas Cherian, Heather Cook, Suzanne Cotter, Ron Dagan, Philippe De Wals, Geneviève Deceuninck, Barbara Denham, Giles Edwards, Juhani Eskola, Daniel R Feikin, Margaret Fitzgerald, Emmanouil Galanakis, Gabriela Garcia-Gabarrot, Juan J Garcia-Garcia, Amadeu Gene, Borja Gomez, Helen Heffernan, Thomas W Hennessy, Sigrid Heuberger, Markus Hilty, Helene Ingels, Sanjay Jayasinghe, Eunice W Kagucia, James D Kellner, Nicola P Klein, Andrea Kormann-Klement, Jana Kozakova, Vicki Krause, Paula Kriz, Lotte Lambertsen, Agnès Lepoutre, Orin S Levine, Ruth Link-Gelles, Marc Lipsitch, Jennifer D Loo, Mariana Lopez-Vega, Marguerite Lovgren, Sofia Maraki, Edward O Mason, Peter B McIntyre, Robert Menzies, Allison Messina, Elizabeth Miller, Santiago Mintegi, Matthew R Moore, Jitka Motlova, Lawrence H Moulton, Kathrin Mühlemann, Carmen Muñoz-Almagro, Katherine L O'Brien, David R Murdoch, Daniel E Park, Milo A Puhan, Arthur L Reingold, Raquel Sa-Leao, Abanti Sanyal, Peter G Smith, Lodewijk Spanjaard, Chonnamet Techasaensiri, Richard E Thompson, Koh C Thoon, Gregory J Tyrrell, Palle Valentiner-Branth, Arie van der Ende, Otto G Vanderkooi, Mark P G van der Linden, Emmanuelle Varon, Jan Verhaegen, Didrik F Vestrheim, Imelda Vickers, Anne von Gottberg, Rüdiger von Kries, Pauline Waight, Robert Weatherholtz, Susanne Weiss, Cynthia G Whitney, Arnold Yee, Anita K M Zaidi, Daniel R Feikin, Eunice W Kagucia, Jennifer D Loo, Ruth Link-Gelles, Milo A Puhan, Thomas Cherian, Orin S Levine, Cynthia G Whitney, Katherine L O'Brien, Matthew R Moore, Serotype Replacement Study Group, Claire A Adegbola, Mary Agocs, Krow Ampofo, Nick Andrews, Theresa Barton, Javier Benito, Claire V Broome, Michael G Bruce, Lisa R Bulkow, Carrie L Byington, Teresa Camou, Thomas Cherian, Heather Cook, Suzanne Cotter, Ron Dagan, Philippe De Wals, Geneviève Deceuninck, Barbara Denham, Giles Edwards, Juhani Eskola, Daniel R Feikin, Margaret Fitzgerald, Emmanouil Galanakis, Gabriela Garcia-Gabarrot, Juan J Garcia-Garcia, Amadeu Gene, Borja Gomez, Helen Heffernan, Thomas W Hennessy, Sigrid Heuberger, Markus Hilty, Helene Ingels, Sanjay Jayasinghe, Eunice W Kagucia, James D Kellner, Nicola P Klein, Andrea Kormann-Klement, Jana Kozakova, Vicki Krause, Paula Kriz, Lotte Lambertsen, Agnès Lepoutre, Orin S Levine, Ruth Link-Gelles, Marc Lipsitch, Jennifer D Loo, Mariana Lopez-Vega, Marguerite Lovgren, Sofia Maraki, Edward O Mason, Peter B McIntyre, Robert Menzies, Allison Messina, Elizabeth Miller, Santiago Mintegi, Matthew R Moore, Jitka Motlova, Lawrence H Moulton, Kathrin Mühlemann, Carmen Muñoz-Almagro, Katherine L O'Brien, David R Murdoch, Daniel E Park, Milo A Puhan, Arthur L Reingold, Raquel Sa-Leao, Abanti Sanyal, Peter G Smith, Lodewijk Spanjaard, Chonnamet Techasaensiri, Richard E Thompson, Koh C Thoon, Gregory J Tyrrell, Palle Valentiner-Branth, Arie van der Ende, Otto G Vanderkooi, Mark P G van der Linden, Emmanuelle Varon, Jan Verhaegen, Didrik F Vestrheim, Imelda Vickers, Anne von Gottberg, Rüdiger von Kries, Pauline Waight, Robert Weatherholtz, Susanne Weiss, Cynthia G Whitney, Arnold Yee, Anita K M Zaidi

Abstract

Background: Vaccine-serotype (VT) invasive pneumococcal disease (IPD) rates declined substantially following introduction of 7-valent pneumococcal conjugate vaccine (PCV7) into national immunization programs. Increases in non-vaccine-serotype (NVT) IPD rates occurred in some sites, presumably representing serotype replacement. We used a standardized approach to describe serotype-specific IPD changes among multiple sites after PCV7 introduction.

Methods and findings: Of 32 IPD surveillance datasets received, we identified 21 eligible databases with rate data ≥ 2 years before and ≥ 1 year after PCV7 introduction. Expected annual rates of IPD absent PCV7 introduction were estimated by extrapolation using either Poisson regression modeling of pre-PCV7 rates or averaging pre-PCV7 rates. To estimate whether changes in rates had occurred following PCV7 introduction, we calculated site specific rate ratios by dividing observed by expected IPD rates for each post-PCV7 year. We calculated summary rate ratios (RRs) using random effects meta-analysis. For children <5 years old, overall IPD decreased by year 1 post-PCV7 (RR 0.55, 95% CI 0.46-0.65) and remained relatively stable through year 7 (RR 0.49, 95% CI 0.35-0.68). Point estimates for VT IPD decreased annually through year 7 (RR 0.03, 95% CI 0.01-0.10), while NVT IPD increased (year 7 RR 2.81, 95% CI 2.12-3.71). Among adults, decreases in overall IPD also occurred but were smaller and more variable by site than among children. At year 7 after introduction, significant reductions were observed (18-49 year-olds [RR 0.52, 95% CI 0.29-0.91], 50-64 year-olds [RR 0.84, 95% CI 0.77-0.93], and ≥ 65 year-olds [RR 0.74, 95% CI 0.58-0.95]).

Conclusions: Consistent and significant decreases in both overall and VT IPD in children occurred quickly and were sustained for 7 years after PCV7 introduction, supporting use of PCVs. Increases in NVT IPD occurred in most sites, with variable magnitude. These findings may not represent the experience in low-income countries or the effects after introduction of higher valency PCVs. High-quality, population-based surveillance of serotype-specific IPD rates is needed to monitor vaccine impact as more countries, including low-income countries, introduce PCVs and as higher valency PCVs are used. Please see later in the article for the Editors' Summary.

Conflict of interest statement

The manuscript coauthors and members of the Serotype Replacement Study Group have the following conflicts: RD has, in the last five years, received grants/research support from Berna/Crucell, Wyeth/Pfizer, MSD and Protea; he has been a scientific consultant for Berna/Crucell, GlaxoSmithKline, Norvatis, Wyeth/Pfizer, Protea, MSD; he has been a speaker for Berna/Crucell, GlaxoSmithKline, and Wyeth/Pfizer; he is a shareholder of Protea/NASVAX. PDW has received research grants, honoraria, and travel expense reimbursements from vaccine manufacturers including Glaxo SmithKline, Norvatis, Sanofi Pasteur, Merck, and Wyeth, as well as from governmental agencies including the Quebec Ministry of Health and Social Services, Health Canada, and the Public Health Agency of Canada. JE has served as a member of a data safety monitoring board (DSMB) for Novartis meningococcal and typhoid vaccines and participated in an advisory meeting of their pneumococcal protein vaccine in 2009. JE works at the National Institute for Health and Welfare (THL), Helsinki, Finland, which has a research contract with GSK on pneumococcal vaccines. MH is a lead investigator for the Switzerland IPD surveillance program, which is partly funded by an unrestricted grant from Pfizer. JDK and OV are lead investigators of the Calgary Streptococcus pneumoniae Epidemiology Research (CASPER) study which is sponsored in part by an unrestricted grant from Pfizer, Canada. NPK has received research support from Pfizer, GSK, Merck, Sanofi Pasteur, and Norvatis. ML has received consulting fees from Pfizer. KLO has had research grants from Pfizer and GSK in the past 5 years, and has served on expert panels for GSK, Merck, and Aventis. GJT has received research funding from Wyeth and Pfizer, and has also received funding from Wyeth and Pfizer for serving on Advisory boards and as a speaker in relation to pneumococcal disease. EV has received support for travel to meetings from Wyeth/Pfizer and has been a speaker for Pfizer. IV has received funding support from Pfizer. RvK and SW are investigators of the German pneumococcal surveillance project in children/ESPED study, which is sponsored by an unrestricted grant by Pfizer Germany.

Figures

Figure 1. Flow diagram of datasets included… — **Figure 1. Flow diagram of datasets included in the analysis.**

Figure 2. Pre-PCV7 introduction average annual invasive… — **Figure 2. Pre-PCV7 introduction average annual invasive pneumococcal disease rates and percent vaccine serotype isolates.**
(A) IPD rates as cases per 100,000. (B) Percent VT isolates as a proportion of all pre-PCV7 introduction isolates. *Only children aged <5 years included. Site abbreviations: ABCs, USA Active Bacterial Core Surveillance; AIP, USA Alaska; AUSI, Australian Indigenous Northern Territory; AUSN, Australian Non-Indigenous; CAL, Canada Calgary; CHE, Switzerland; CZE, Czech Republic; DEN, Denmark; E&W, England and Wales; GRC, Greece; ISR, Israel; NAV, USA Navajo; NCK, USA Kaiser Permanente Northern California; NLD, The Netherlands; NOR, Norway; NZL, New Zealand; SCT, Scotland; URY, Uruguay; UTA, USA Utah.

Figure 3. Post-PCV7 introduction invasive pneumococcal disease… — **Figure 3. Post-PCV7 introduction invasive pneumococcal disease summary rate ratios.**
Summary RRs from random effects meta-analysis. Summary RRs estimated by dividing observed over expected rates and calculated for each age-serotype group. 95% confidence interval indicated by error bars. Y-Axis on log scale.

Figure 4. All serotype invasive pneumococcal disease… — **Figure 4. All serotype invasive pneumococcal disease summary rate ratio forest plots by post-introduction year from random effects meta-analysis for children aged**
Site abbreviations: ABCs, USA Active Bacterial Core Surveillance; AIP, USA Alaska; AUSI, Australian Indigenous Northern Territory; AUSN, Australian Non-Indigenous; CAL, Canada Calgary; CHE, Switzerland; CZE, Czech Republic; DEN, Denmark; E&W, England and Wales; GRC, Greece; ISR, Israel; NAV, USA Navajo; NCK, USA Kaiser Permanente Northern California; NLD, The Netherlands; NOR, Norway; NZL, New Zealand; SCT, Scotland; URY, Uruguay; UTA, USA Utah.

Figure 5. Vaccine serotype invasive pneumococcal disease… — **Figure 5. Vaccine serotype invasive pneumococcal disease summary rate ratio forest plots by post-introduction year from random effects meta-analysis for children aged**
Site abbreviations: ABCs (USA Active Bacterial Core Surveillance); AIP (USA Alaska); Site abbreviations: ABCs, USA Active Bacterial Core Surveillance; AIP, USA Alaska; AUSI, Australian Indigenous Northern Territory; AUSN, Australian Non-Indigenous; CAL, Canada Calgary; CHE, Switzerland; CZE, Czech Republic; DEN, Denmark; E&W, England and Wales; GRC, Greece; ISR, Israel; NAV, USA Navajo; NCK, USA Kaiser Permanente Northern California; NLD, The Netherlands; NOR, Norway; NZL, New Zealand; SCT, Scotland; URY, Uruguay; UTA, USA Utah.

Figure 6. Non-vaccine serotype invasive pneumococcal disease… — **Figure 6. Non-vaccine serotype invasive pneumococcal disease summary rate ratio forest plots by post-introduction year from random effects meta-analysis for children aged**
Site abbreviations: ABCs, USA Active Bacterial Core Surveillance; AIP, USA Alaska; AUSI, Australian Indigenous Northern Territory; AUSN, Australian Non-Indigenous; CAL, Canada Calgary; CHE, Switzerland; CZE, Czech Republic; DEN, Denmark; E&W, England and Wales; GRC, Greece; ISR, Israel; NAV, USA Navajo; NCK, USA Kaiser Permanente Northern California; NLD, The Netherlands; NOR, Norway; NZL, New Zealand; SCT, Scotland; URY, Uruguay; UTA, USA Utah.

Figure 7. Post-PCV7 introduction pneumococcal meningitis summary… — **Figure 7. Post-PCV7 introduction pneumococcal meningitis summary rate ratios.**
Summary RRs from random effects meta-analysis. Summary RRs esimated by dividing observed by expected rates and calculated for each age-serotype group. 95% confidence interval indicated by error bars. Y-Axis on log scale.

Figure 8. All serotype invasive pneumococcal disease… — **Figure 8. All serotype invasive pneumococcal disease summary rate ratio forest plots by post-introduction year from random effects meta-analysis for adults aged 18–49 years.**
Site abbreviations: ABCs, USA Active Bacterial Core Surveillance; AIP, USA Alaska; AUSI, Australian Indigenous Northern Territory; AUSN, Australian Non-Indigenous; CAL, Canada Calgary; CHE, Switzerland; CZE, Czech Republic; DEN, Denmark; E&W, England and Wales; GRC, Greece; ISR, Israel; NAV, USA Navajo; NCK, USA Kaiser Permanente Northern California; NLD, The Netherlands; NOR, Norway; NZL, New Zealand; SCT, Scotland; URY, Uruguay; UTA, USA Utah.

Figure 9. Vaccine serotype invasive pneumococcal disease… — **Figure 9. Vaccine serotype invasive pneumococcal disease summary rate ratio forest plots by post-introduction year from random effects meta-analysis for adults aged 18–49 years.**
Site abbreviations: ABCs, USA Active Bacterial Core Surveillance; AIP, USA Alaska; AUSI, Australian Indigenous Northern Territory; AUSN, Australian Non-Indigenous; CAL, Canada Calgary; CHE, Switzerland; CZE, Czech Republic; DEN, Denmark; E&W, England and Wales; GRC, Greece; ISR, Israel; NAV, USA Navajo; NCK, USA Kaiser Permanente Northern California; NLD, The Netherlands; NOR, Norway; NZL, New Zealand; SCT, Scotland; URY, Uruguay; UTA, USA Utah.

Figure 10. Non-vaccine serotype invasive pneumococcal disease… — **Figure 10. Non-vaccine serotype invasive pneumococcal disease summary rate ratio forest plots by post-introduction year from random effects meta-analysis for adults aged 18–49 years.**
Site abbreviations: ABCs, USA Active Bacterial Core Surveillance; AIP, USA Alaska; AUSI, Australian Indigenous Northern Territory; AUSN, Australian Non-Indigenous; CAL, Canada Calgary; CHE, Switzerland; CZE, Czech Republic; DEN, Denmark; E&W, England and Wales; GRC, Greece; ISR, Israel; NAV, USA Navajo; NCK, USA Kaiser Permanente Northern California; NLD, The Netherlands; NOR, Norway; NZL, New Zealand; SCT, Scotland; URY, Uruguay; UTA, USA Utah.

Figure 11. All serotype invasive pneumococcal disease… — **Figure 11. All serotype invasive pneumococcal disease summary rate ratio forest plots by post-introduction year from random effects meta-analysis for adults aged 50–64 years.**
Site abbreviations: ABCs, USA Active Bacterial Core Surveillance; AIP, USA Alaska; AUSI, Australian Indigenous Northern Territory; AUSN, Australian Non-Indigenous; CAL, Canada Calgary; CHE, Switzerland; CZE, Czech Republic; DEN, Denmark; E&W, England and Wales; GRC, Greece; ISR, Israel; NAV, USA Navajo; NCK, USA Kaiser Permanente Northern California; NLD, The Netherlands; NOR, Norway; NZL, New Zealand; SCT, Scotland; URY, Uruguay; UTA, USA Utah.

Figure 12. Vaccine serotype invasive pneumococcal disease… — **Figure 12. Vaccine serotype invasive pneumococcal disease summary rate ratio forest plots by post-introduction year from random effects meta-analysis for adults aged 50–64 years.**
Site abbreviations: ABCs, USA Active Bacterial Core Surveillance; AIP, USA Alaska; AUSI, Australian Indigenous Northern Territory; AUSN, Australian Non-Indigenous; CAL, Canada Calgary; CHE, Switzerland; CZE, Czech Republic; DEN, Denmark; E&W, England and Wales; GRC, Greece; ISR, Israel; NAV, USA Navajo; NCK, USA Kaiser Permanente Northern California; NLD, The Netherlands; NOR, Norway; NZL, New Zealand; SCT, Scotland; URY, Uruguay; UTA, USA Utah.

Figure 13. Non-vaccine serotype invasive pneumococcal disease… — **Figure 13. Non-vaccine serotype invasive pneumococcal disease summary rate ratio forest plots by post-introduction year from random effects meta-analysis for adults aged 50–64 years.**
Site abbreviations: ABCs, USA Active Bacterial Core Surveillance; AIP, USA Alaska; AUSI, Australian Indigenous Northern Territory; AUSN, Australian Non-Indigenous; CAL, Canada Calgary; CHE, Switzerland; CZE, Czech Republic; DEN, Denmark; E&W, England and Wales; GRC, Greece; ISR, Israel; NAV, USA Navajo; NCK, USA Kaiser Permanente Northern California; NLD, The Netherlands; NOR, Norway; NZL, New Zealand; SCT, Scotland; URY, Uruguay; UTA, USA Utah.

Figure 14. All serotype invasive pneumococcal disease… — **Figure 14. All serotype invasive pneumococcal disease summary rate ratio forest plots by post-introduction year from random effects meta-analysis for adults aged ≥65 years.**
Site abbreviations: ABCs, USA Active Bacterial Core Surveillance; AIP, USA Alaska; AUSI, Australian Indigenous Northern Territory; AUSN, Australian Non-Indigenous; CAL, Canada Calgary; CHE, Switzerland; CZE, Czech Republic; DEN, Denmark; E&W, England and Wales; GRC, Greece; ISR, Israel; NAV, USA Navajo; NCK, USA Kaiser Permanente Northern California; NLD, The Netherlands; NOR, Norway; NZL, New Zealand; SCT, Scotland; URY, Uruguay; UTA, USA Utah.

Figure 15. Vaccine serotype invasive pneumococcal disease… — **Figure 15. Vaccine serotype invasive pneumococcal disease summary rate ratio forest plots by post-introduction year from random effects meta-analysis for adults aged ≥65 years.**
Site abbreviations: ABCs, USA Active Bacterial Core Surveillance; AIP, USA Alaska; AUSI, Australian Indigenous Northern Territory; AUSN, Australian Non-Indigenous; CAL, Canada Calgary; CHE, Switzerland; CZE, Czech Republic; DEN, Denmark; E&W, England and Wales; GRC, Greece; ISR, Israel; NAV, USA Navajo; NCK, USA Kaiser Permanente Northern California; NLD, The Netherlands; NOR, Norway; NZL, New Zealand; SCT, Scotland; URY, Uruguay; UTA, USA Utah.

Figure 16. Non-vaccine serotype invasive pneumococcal disease… — **Figure 16. Non-vaccine serotype invasive pneumococcal disease summary rate ratio forest plots by post-introduction year from random effects meta-analysis for adults aged ≥65 years.**
Site abbreviations: ABCs, USA Active Bacterial Core Surveillance; AIP, USA Alaska; AUSI, Australian Indigenous Northern Territory; AUSN, Australian Non-Indigenous; CAL, Canada Calgary; CHE, Switzerland; CZE, Czech Republic; DEN, Denmark; E&W, England and Wales; GRC, Greece; ISR, Israel; NAV, USA Navajo; NCK, USA Kaiser Permanente Northern California; NLD, The Netherlands; NOR, Norway; NZL, New Zealand; SCT, Scotland; URY, Uruguay; UTA, USA Utah.

References

1. World Health Organization (2012) Estimated Hib and pneumococcal deaths for children under 5 years of age, 2008. Available: . Accessed 18 February 2013.
1. Pilishvili T, Lexau C, Farley MM, Hadler J, Harrison LH, et al. (2010) Sustained reductions in invasive pneumococcal disease in the era of conjugate vaccine. J Infect Dis 201: 32–41.
1. Kellner JD, Vanderkooi OG, MacDonald J, Church DL, Tyrrell GJ, et al. (2009) Changing epidemiology of invasive pneumococcal disease in Canada, 1998–2007: update from the Calgary-area Streptococcus pneumoniae research (CASPER) study. Clin Infect Dis 49: 205–212.
1. Singleton RJ, Hennessy TW, Bulkow LR, Hammitt LL, Zulz T, et al. (2007) Invasive pneumococcal disease caused by nonvaccine serotypes among Alaska native children with high levels of 7-valent pneumococcal conjugate vaccine coverage. JAMA 297: 1784–1792.
1. O’Brien KL, Millar EV, Zell ER, Bronsdon M, Weatherholtz R, et al. (2007) Effect of pneumococcal conjugate vaccine on nasopharyngeal colonization among immunized and unimmunized children in a community-randomized trial. J Infect Dis 196: 1211–1220.
1. Huang SS, Platt R, Rifas-Shiman SL, Pelton SI, Goldmann D, et al. (2005) Post-PCV7 changes in colonizing pneumococcal serotypes in 16 Massachusetts communities, 2001 and 2004. Pediatrics 116: e408–e413.
1. Flasche S, Van Hoek AJ, Sheasby E, Waight P, Andrews N, et al. (2011) Effect of pneumococcal conjugate vaccination on serotype-specific carriage and invasive disease in England: a cross-sectional study. PLoS Med 8: e1001017 doi:
1. O'Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, et al. (2009) Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374: 893–902.
1. Abdullahi O, Karani A, Tigoi CC, Mugo D, Kungu S, et al. (2012) The prevalence and risk factors for pneumococcal colonization of the nasopharynx among children in Kilifi District, Kenya. PLoS One 7: e30787 doi:
1. World Health Organization (2010) Changing epidemiology of pneumococcal serotypes after introduction of conjugate vaccine: July 2010 report. Wkly Epidemiol Rec 85: 434–436.
1. Conklin L, Knoll MD, Loo JD, Fleming-Dutra K, Park D, et al.. (2011) Landscape analysis of pneumococcal conjugate vaccine dosing schedules: A systematic review (Report to the Strategic Advisory Group of Experts on Immunization (SAGE), World Health Organization). Available: . Accessed 18 February 2013.
1. Park IH, Moore MR, Treanor JJ, Pelton SI, Pilishvili T, et al. (2008) Differential effects of pneumococcal vaccines against serotypes 6A and 6C. J Infect Dis 198: 1818–1822.
1. Hausdorff WP, Siber G, Paradiso PR (2001) Geographical differences in invasive pneumococcal disease rates and serotype frequency in young children. Lancet 357: 950–952.
1. Weinberger DM, Malley R, Lipsitch M (2011) Serotype replacement in disease after pneumococcal vaccination. Lancet 378: 1962–1973.
1. Hanquet G, Lernout T, Vergison A, Verhaegen J, Kissling E, et al. (2011) Impact of conjugate 7-valent vaccination in Belgium: addressing methodological challenges. Vaccine 29: 2856–2864.
1. Miller E, Andrews NJ, Waight PA, Slack MP, George RC (2011) Herd immunity and serotype replacement 4 years after seven-valent pneumococcal conjugate vaccination in England and Wales: an observational cohort study. Lancet Infect Dis 11: 760–768.
1. Cox C (1990) Fieller’s Theorem, the Likelihood and the Delta Method. Biometrics 46: 709–718.
1. Beaton GH, United Nations. Subcommittee on Nutrition (1992) Effectiveness of vitamin A supplementation in the control of young child morbidity and mortality in developing countries. Nutrition policy discussion paper number 13. Geneva: ACC/SCN. 120p.
1. Sweeting MJ, Sutton AJ, Lambert PC (2004) What to add to nothing? Use and avoidance of continuity corrections in meta-analysis of sparse data. Stat Med 23: 1351–1375.
1. Borenstein M, Hedges L., Rothstein H. (2007) Introduction to meta-analysis. pp.2–303. Available: . Accessed 18 February 2013.
1. Krause VL, Reid SJ, Merianos A (2000) Invasive pneumococcal disease in the Northern Territory of Australia, 1994–1998. Med J Aust 173 Suppl: S27–31.
1. Barry C, Krause VL, Cook HM, Menzies RI (2012) Invasive pneumococcal disease in Australia 2007 and 2008. Commun Dis Intell Q Rep 36: E151–165.
1. Motlova J, Benes C, Kriz P (2009) Incidence of invasive pneumococcal disease in the Czech Republic and serotype coverage by vaccines, 1997–2006. Epidemiol Infect 137: 562–569.
1. Harboe ZB, Valentiner-Branth P, Ingels H, Rasmussen JN, Andersen PH, et al. (2013) Pediatric invasive pneumococcal disease caused by vaccine serotypes following the introduction of conjugate vaccination in Denmark. PLoS ONE 8: e51460 doi:
1. Grall N, Hurmic O, Al Nakib M, Longo M, Poyart C, et al. (2011) Epidemiology of Streptococcus pneumoniae in France before introduction of the PCV-13 vaccine. Eur J Clin Microbiol Infect Dis 30: 1511–1519.
1. Zissis NP, Syriopoulou V, Kafetzis D, Daikos GL, Tsilimingaki A, et al. (2004) Serotype distribution and antimicrobial susceptibility of Streptococcus pneumoniae causing invasive infections and acute otitis media in children. Eur J Pediatr 163: 364–368.
1. Vickers I, Fitzgerald M, Murchan S, Cotter S, O'FlanaganO’Flanagan D, et al. (2011) Serotype distribution of Streptococcus pneumoniae causing invasive disease in the Republic of Ireland. Epidemiol Infect 139: 783–790.
1. Ben-Shimol S, Greenberg D, Givon-Lavi N, Elias N, Glikman D, et al. (2012) Rapid reduction in invasive pneumococcal disease after introduction of PCV7 into the National Immunization Plan in Israel. Vaccine 30: 6600–6607.
1. van Deursen AM, van Mens SP, Sanders EA, Vlaminckx BJ, de Melker HE, et al. (2012) Invasive pneumococcal disease and 7-valent pneumococcal conjugate vaccine, the Netherlands. Emerg Infect Dis 18: 1729–1737.
1. Heffernan HM, Martin DR, Woodhouse RE, Morgan J, Blackmore TK (2008) Invasive pneumococcal disease in New Zealand 1998–2005: capsular serotypes and antimicrobial resistance. Epidemiol Infect 136: 352–359.
1. Vestrheim DF, Lovoll O, Aaberge IS, Caugant DA, Hoiby EA, et al. (2008) Effectiveness of a 2+1 dose schedule pneumococcal conjugate vaccination programme on invasive pneumococcal disease among children in Norway. Vaccine 26: 3277–3281.
1. Lamb KE, Flasche S, Diggle M, Inverarity D, Greenhalgh D, et al... (2013) Trends in serotypes and sequence types among cases of invasive pneumococcal disease in Scotland, 1999–2010. Vaccine. In press.
1. Pilishvili T, Zell ER, Farley MM, Schaffner W, Lynfield R, et al. (2010) Risk factors for invasive pneumococcal disease in children in the era of conjugate vaccine use. Pediatrics 126: e9–e17.
1. Weatherholtz R, Millar EV, Moulton LH, Reid R, Rudolph K, et al. (2010) Invasive pneumococcal disease a decade after pneumococcal conjugate vaccine use in an American Indian population at high risk for disease. Clin Infect Dis 50: 1238–1246.
1. Black S, France EK, Isaacman D, Bracken L, Lewis E, et al. (2007) Surveillance for invasive pneumococcal disease during 2000–2005 in a population of children who received 7-valent pneumococcal conjugate vaccine. Pediatr Infect Dis J 26: 771–777.
1. Byington CL, Samore MH, Stoddard GJ, Barlow S, Daly J, et al. (2005) Temporal trends of invasive disease due to Streptococcus pneumoniae among children in the intermountain west: emergence of nonvaccine serogroups. Clin Infect Dis 41: 21–29.
1. GAVI Alliance (2011) GAVI Alliance Country Eligibility Policy. Available: . Accessed 31 May 2013.
1. Black S (2010) The volatile nature of pneumococcal serotype epidemiology: potential for misinterpretation. Pediatr Infect Dis J 29: 301–303.
1. World Health Organization (2012) Pneumococcal vaccine WHO position paper - 2012. Wkly Epidemiol Rec 14: 129–144.
1. Miller E, Andrews NJ, Waight PA, Slack MP, George RC (2011) Effectiveness of the new serotypes in the 13-valent pneumococcal conjugate vaccine. Vaccine 29: 9127–9131.
1. Palmu AA, Jokinen J, Borys D, Nieminen H, Ruokokoski E, et al. (2012) Effectiveness of the ten-valent pneumococcal Haemophilus influenzae protein D conjugate vaccine (PHiD-CV10) against invasive pneumococcal disease: a cluster randomised trial. Lancet 381: 214–222.
1. Singleton R, Wenger J, Klejka JA, Bulkow LR, Thompson A, et al. (2013) The 13-valent pneumococcal conjugate vaccine for invasive pneumococcal disease in Alaska Native children: results of a clinical trial. Pediatr Infect Dis J 32: 257–263.
1. Brueggemann AB, Peto TE, Crook DW, Butler JC, Kristinsson KG, et al. (2004) Temporal and geographic stability of the serogroup-specific invasive disease potential of Streptococcus pneumoniae in children. J Infect Dis 190: 1203–1211.
1. Bogaert D, Thompson CM, Trzcinski K, Malley R, Lipsitch M (2010) The role of complement in innate and adaptive immunity to pneumococcal colonization and sepsis in a murine model. Vaccine 28: 681–685.
1. Sleeman KL, Griffiths D, Shackley F, Diggle L, Gupta S, et al. (2006) Capsular serotype-specific attack rates and duration of carriage of Streptococcus pneumoniae in a population of children. J Infect Dis 194: 682–688.
1. Weinberger DM, Harboe ZB, Flasche S, Scott JA, Lipsitch M (2011) Prediction of serotypes causing invasive pneumococcal disease in unvaccinated and vaccinated populations. Epidemiology 22: 199–207.
1. Whitney CG, Farley MM, Hadler J, Harrison LH, Bennett NM, et al. (2003) Decline in invasive pneumococcal disease after the introduction of protein-polysaccharide conjugate vaccine. N Engl J Med 348: 1737–1746.
1. Hsu HE, Shutt KA, Moore MR, Beall BW, Bennett NM, et al. (2009) Effect of pneumococcal conjugate vaccine on pneumococcal meningitis. N Engl J Med 360: 244–256.
1. Cohen AL, Harrison LH, Farley MM, Reingold AL, Hadler J, et al. (2010) Prevention of invasive pneumococcal disease among HIV-infected adults in the era of childhood pneumococcal immunization. AIDS 24: 2253–2262.
1. Feikin DR, Klugman KP (2002) Historical changes in pneumococcal serogroup distribution: implications for the era of pneumococcal conjugate vaccines. Clin Infect Dis 35: 547–555.
1. Fenoll A, Martin Bourgon C, Munoz R, Vicioso D, Casal J (1991) Serotype distribution and antimicrobial resistance of Streptococcus pneumoniae isolates causing systemic infections in Spain, 1979–1989. Rev Infect Dis 13: 56–60.
1. Harboe ZB, Benfield TL, Valentiner-Branth P, Hjuler T, Lambertsen L, et al. (2010) Temporal trends in invasive pneumococcal disease and pneumococcal serotypes over 7 decades. Clin Infect Dis 50: 329–337.
1. Lagos R, Munoz A, San Martin O, Maldonado A, Hormazabal JC, et al. (2008) Age- and serotype-specific pediatric invasive pneumococcal disease: insights from systematic surveillance in Santiago, Chile, 1994–2007. J Infect Dis 198: 1809–1817.
1. Hausdorff WP, Feikin DR, Klugman KP (2005) Epidemiological differences among pneumococcal serotypes. Lancet Infect Dis 5: 83–93.
1. Dagan R, Givon-Lavi N, Leibovitz E, Greenberg D, Porat N (2009) Introduction and proliferation of multidrug-resistant Streptococcus pneumoniae serotype 19A clones that cause acute otitis media in an unvaccinated population. J Infect Dis 199: 776–785.
1. Hausdorff WP, Van Dyke MK, Van Effelterre T (2012) Serotype replacement after pneumococcal vaccination. Lancet 379: : 1387–1388; author reply 1388–1389.
1. Black RE, Cousens S, Johnson HL, Lawn JE, Rudan I, et al. (2010) Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 375: 1969–1987.
1. World Health Organization (2012) Review of serotype replacement in the setting of 7-valent pneumococcal conjugate vaccine (PCV-7) use and implications for the PCV10/PCV13 era. Wkly Epidemiol Rec 87: 12–13.
1. Robinson KA, Baughman W, Rothrock G, Barrett NL, Pass M, et al. (2001) Epidemiology of invasive Streptococcus pneumoniae infections in the United States, 1995-1998: Opportunities for prevention in the conjugate vaccine era. JAMA 285: 1729–1735.
1. van Deursen AM, van Mens SP, Sanders EA, Vlaminckx BJ, de Melker HE, et al. (2012) Invasive pneumococcal disease and 7-valent pneumococcal conjugate vaccine, the Netherlands. Emerg Infect Dis 18: 1729–1737.

Source: PubMed

Serotype-specific changes in invasive pneumococcal disease after pneumococcal conjugate vaccine introduction: a pooled analysis of multiple surveillance sites

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