Impact after 10-year use of pneumococcal conjugate vaccine in the Brazilian national immunization program: an updated systematic literature review from 2015 to 2020

Figures & data

Table 1. Inclusion and exclusion criteria

	Inclusion criteria	Exclusion criteria
Population	Studies done in human subjects of all ages	Non-human studies All others
Intervention	PHiD-CV vaccine	All others were excluded
Comparator	All	None were excluded based on comparator
Outcome	Epidemiological parameters Prevalence/incidence Effectiveness of vaccination on invasive disease, pneumonia, otitis media, nasopharyngeal carriage, serotype distribution, or herd protection in all age groups	Vaccine immunogenicity or safety studies Studies evaluating treatments such as antibiotics; studies of virus etiology only; studies conducted among populations with chronic diseases not representative of the general population.
Study design	Primary research* Randomized controlled trials (RCTs) Non-randomized studies Observation studies (cohort studies, case-control studies, pre-/post-vaccine introduction time series) Surveillance reports (unpublished and published) Publications/reports from global, regional and local published and unpublished data (if possible)	Non-primary research Reviews** Meta-analysis Public health programs or recommendations Transmission modeling studies Cost-effectiveness or health economics studies Case reports Meta-analysis Letter to editor Newspaper Editorial Comment Opinion paper Studies whose analysis period was unspecified.
Limits
Publication date	May 2015 – May 2020	Articles published outside of dates considered eligible for inclusion
Geographic scope	Brazil	All other countries/regions
Language	English, Spanish and Portuguese	Articles published in any other language besides English, Spanish and Portuguese

* Reference lists of all articles were manually screened for additional relevant original articles (as deemed necessary by the reviewer)

**Review articles from the search were excluded but bibliographies of reviews were manually screened for additional relevant original articles.

Table 2. Impact of PHiD-CV on IPD, pneumonia, CAP, AOM and nasopharyngeal carriage in Brazil

								Incidence or Percent Cases (% or #s)
Reference	Geographic Area	Study Design	Study Period (years after vaccine introduction)	Sample Size	Age	Outcome	Effectiveness/Impact or Percent Change (%)	Pre-Introduction	Post-Introduction
IPD
Andrade et al. 2015 (abstract)^Citation36	Nationwide	Ecological Database Study	2008-2013 (3 years)	Not Stated	< 2 years	PMIPD	-44.4% (95%CI: -72.5; -15.8; p<0.002)
Jarovsky et al. 2016 (abstract)^40	Sao Paulo (Sao Paulo State)/ Uberlandia (Minas Gerais State)	Surveillance	Pre: Jan 2000-2009Post: 2010 to Dec 2013 (3 years)	445 IPD episodes	< 16 years	IPD		Cases: • 60% (<2 years) • 23% (2-5 years) • 16% (>5 years)	Cases: 42% (<2 years) 28% (2-5 years) 25% (>5 years)
Yoshioka et al. 2016 (abstract)^Citation45	Sao Paulo State	Surveillance	Pre: 2005-2010Post: 2011-2016 (6 years)	205 patients	< 15 years	IPD		Cases: 150 Diagnosis: • Pneumonia (66.7%) • Bacteremia (19.3%) • Meningitis (10.7%)	Cases: 55 Diagnosis: • Pneumonia (67.3%) • Bacteremia (14.5%) • Meningitis (12.7%)
Leite et al. 2016^Citation26	Salvador (Bahia State)	Case-series	Post: Jul 2010 to Dec 2013 (3 years)	82 eligible cases	All ages (stratified)	IPD	• 11/14 (78.6%) Sp isolated strains belonged to VT		• Pneumococcal meningitis (n = 64, 78.1%) • Bacteremic pneumococcal pneumonia (n = 12, 14.6%) • Bacteremia (n = 6, 7.3%)
Medeiros et al. 2016^27	Sao Paulo State (University Hospital)	Cross-sectional	1998 to 2013 (3 years)	332 isolated pneumococcal strains in patients with IPD	All ages (stratified)	IPD		n = 205 (61.7%)	n = 46 (13.9%)
Medeiros et al. 2017^Citation28	Sao Paulo State	Surveillance	1998 to 2013 (3 years)	796 patients (isolates)	All ages (stratified)	IPD		n = 479	n = 95 cases
Brandileone et al. 2018^Citation20	Nationwide	Surveillance	Three periods (3 years and 5 years): • Pre- PHiD-CV (Jan 2005-Dec 2009) • Early post- PHiD-CV (Jan 2010-Dec 2013) • Late post- PHiD-CV (Jan 2014-Dec 2015)	8,971 IPD isolates	All ages (stratified)	VT IPDNVT IPD			Reduction in VT-IPD meningitis cases: • 83.4% (2-4 years) • 47.4% (>65 years)
Jarovsky et al. 2017 (abstract)^Citation42	Sao Paulo State	Surveillance	Pre: Jan 2000-2009Post: 2010- Apr 2017 (7 years)	561 patients (440 in analysis)	All ages (stratified)	IPD	IPD decreased from 35.9 to 30.3 cases/year (-15.6%) at all ages
Cassiolato et al. 2018^23	Nationwide	Surveillance	Pre: 2005 - 2009 Post: 2011 - 2017	673 19A isolates (399 19A MLST)	All ages (stratified)	IPD		19A: 2005-2009: 2.8%	19A: 2011-2015: 7.0%2016-2017: 16.4%
Berezin et al. 2020^19	Nationwide	Surveillance	Pre:2005-2009 Post:2011-2015	260 IPD patients	< 17 years	IPD hospitalizations and mortality	260 patients with IPD and positive pneumococcal isolates were identified (198 during the pre-PCV10 period). When comparing both periods, hospitalizations were reduced from 20 cases to 5 cases per 10,000 pediatric admissions (p < 0.0001). Likewise, fatalities reduced from 6.6 to 2.0 cases per 10,000 pediatric admissions (p < 0.0001).
Pneumonia
Kupek et al. 2016^Citation24	Santa Catarina State	Ecological Database Study	Pre: 2006-2009Post: 2010-2013 (3 years)		< 1 year	Pneumonia mortality	Reduction mortality of 11%	29.69/100,000	23.40/100,000
De Oliveira et al. 2017 (abstract)^38	Nationwide (focus on North region and Ampa State)	Ecological Database Study	Pre: 2006Post: 2016 (6 years)	N/A	< 1 year	Pneumonia mortality		Child Mortality Rates by region: • Norte (1.1) • Nordeste (1.08) • Centro-Oeste (0.99) • Sudeste (0.69) • Sul (0.60) North Region: • Amapaá (1.91) • Acre (1.81) • Tocantins (1.33) • Amazonas (1.05) • Paraá (1.01) • Roraima (0.80) • Rondoônia (0.72)	Child Mortality Rates by region: • Norte (1.66) • Nordeste (1.24) • Centro-Oeste (0.98) • Sudeste (0.68) • Sul (0.47) North Region: • Amapaá (1.43) • Acre (3.97) • Roraima (3.19) • Amazonas (1.93) • Rondoônia (1.78) • Paraá (1.34) • Tocantins (0.47)
Kurum et al. 2017^Citation25	Nationwide	Ecological Database Study	2003 to 2013 (3 years)	Unclear	< 2 years	Pneumonia hospitalizations	Reduction: • 0-<12 months: 10% (95%CI: 4–19) • 12–23 months): 7% (95%CI: 1–10) • 24–59 months: 11% (95%CI: 4–13)
Costa et al. 2015 (abstract)^37	Maranhaão State	Ecological Database Study	Pre: 2008 - 2010Post: 2011- 2013 (3 years)	47,429 pneumonia hospitalization (1-4 years)	1–4 years	Pneumonia hospitalizations	Reduction of 10.1% in hospitalizations (not significant)	Hospitalizations: 24,981 (52.7%)Deaths:43 (48.9%)	Hospitalizations: 22,448 (47.3%)Deaths: 45 (51.1%)
Marani et al. 2015 (abstract)^43	Tocantins State	Ecological Database Study	Pre: 2008 - 2010Post: 2011- 2013 (3 years)	14,938 pneumonia hospitalization (1-4 years)	1–4 years	Pneumonia hospitalizations	Reduction of 28% in deaths by pneumonia (significant)	Hospitalizations:Pre: 8,128 (54.4%)Deaths: 107 (58.2%)	Hospitalizations:Post: 6,810 (45.6%)Deaths: 77 (41.8%)
Andrade et al. 2017^17	Nationwide	Ecological Database Study	Pre: Jan 2005 -Dec 2009Post: Jan 2011 - Dec 2015 (5 years)	78,727,692 records analyzed (7,829,895 (9.9%) for pneumonia)	< 6 years	Pneumonia hospitalizations (herd immunity)	Impact: <12 months: -26.5 (95%CI: -35.5; -17.5); p=0.001 2-4 years: -21.5 (95%CI: -29.8; -13.2); p=0.002
Oliveira et al. 2017 (abstract)^44	Nationwide	Ecological Database Study	Pre: 2006-2010Post: 2011-2015 (4 years)	N/A	< 6 years	Pneumonia mortality	Reduction of 21,05% deaths by pneumonia	Child Mortality Rates:Pre: 0,746 deaths/1000 live births	Post: 0,589 deaths/1000 live births
Vieira et al. 2018^35	Santa Catarina State	Ecological database study	Pre: 2006 - 2009 Post: 2010 - 2014	75,891 children admitted to hospital with pneumonia	< 5 years	Pneumonia hospitalizations	Mean hosp rate: <1yoa: 23.3% reduction 1-4yoa: 8.4% reduction	37,703 hospitalizations	30,101 hospitalizations
Schuck-Paim et al. 2019^32	Nationwide	Ecological database study	Pre: 2004-2009 Post: 2010-2014	N/A	< 5 years	Pneumonia mortality		Between 1980 and 2010: national pneumonia mortality in children younger than 5 years decreased from about 150 to 15 deaths per 100 000 children younger than 5 years.	After 2010: vaccine-associated decline of about 10% in national childhood pneumonia mortality with our primary analytical method, with a high degree of uncertainty in the estimates. We observed larger reductions in municipal childhood pneumonia mortality in all three age groups (3–11 months, 3–23 months, and 3–59 months) in municipalities with a high percentage of extreme childhood poverty and mothers with no primary education, with the largest decrease observed in children aged 3–23 months in municipalities with low maternal education (24%, 95% credible interval 7–35).
CAP
Silva et al. 2016^34	Minas Gerais State	Ecological Database Study	2007 to 2013 (3 years)	5,044 cases (admissions)	< 1 year	CAP hospitalizations	Decline in prevalence: 19%	828 cases	624 cases Prevalence ratio: 0.81; 95%CI: 0.74 to 0.89; p<0.05
Sgambatti et al. 2015^33	Goiania (Goias State)	Ecological Database Study	January to December 2012 (2 years)	3,353 records (both databases)	< 2 years	CAP			• SIH-SUS database: 5,285/1000,00 children, 95%CI 5,046 to 5,533) • APS database: 5,054/100,000 children, 95%CI 4,820 to 5,296
de Paulo Santana et al. 2017 (abstract)^39	Rio de Janeiro State	Cross-sectional	Post: Jan 2015 to Sep 2016 (6 years)	63 patients	< 16 years	CAP	Descriptive: Greater number of hospitalizations among those < 6 months of age who were not vaccinated (p = 0.06) and that the hospitalization time was higher among those vaccinated (p = 0.007)
PM
Andrade et al. 2015 (abstract)^36	Nationwide	Ecological Database Study	2008-2013 (3 years)	Not Stated	< 2 years	PMIPD	-44.4% (95%CI: -72.5; -15.8; p<0.002)
Jarovsky et al. 2016^41	Sao Paulo State	Surveillance	Pre: Jan 2000 - 2009 Post: 2010 - Dec 2015 (5 years)	98 eligible cases	All ages (stratified)	PM		Cases: 66 (6.6 cases/year)Median age:315.5 months (26 years)	Cases: 29 (4. 8 cases/year) Median age:76 months (6 years)
Azevedo et al. 2016^18	Salvador (Bahia State)	Surveillance	Pre: Jan 2008 - May 2010Post: Jun 2010 - Dec 2012 (2 years)	148 cases of PM	All ages (stratified)	PM (NVT serotype isolates)		• Annual incidence (2008) - 0.9/100 000 • NVT: 0.69/100 000 • VT: 0.57/100 000	• Annual incidence (2012)- 0.36/100 000 (p<0.05) • NVT: 0.21/100 000 (P<0.76) • VT: 0.21/100 000 (P<1.0)
AOM
Oliveira et al 2016^30	Salvador (Bahia State)	Cohort	Sep 2009 and Oct 2013 (3 years)	576 children of which 422 followed-up	< 2 years	ARIAOM	PHiD-CV was inversely associated with AOM (OR [95%CI]: 0.16 [0.05 to 0.52])
Sartori et al 2017b*^31	Goiania (Goias State)	Ecological Database Study	Pre: Aug 2008 to Jul 2010Post: Aug 2011 to Jul 2015 (5 years)	6,401 OM outpatient visits were recorded in 4,793 children	< 2 years	All-case OM	Impact: 43.0% (95%CI 41.4% to 44.5%)		Visit reduction: 50.7%; 95%CI: 42.2% to 59.2%; p = 0.013
Nasopharyngeal carriage
Brandileone et al. 2016^21	Sao Paulo State	Cross-sectional	Pre: 2010Post: 2013 (3 years)	Overall 501 children (pre/baseline) and 1,167 (post) surveyed (including 400 tested for Sp)	< 2 years	VT Sp carriageVT NTHi carriage	Effectiveness VT carriage: (3+1 schedule) 97.3% (95%CI: 88.7% to 99.3%)(2+1 schedule) 92.7% (95%CI: 79.6% to 97.4%) Sp: PHiD-CV serotypes were found in 19.8% and 1.8% respectively, representing a decline of 90.9% (p < 0.0001).	Sp: 40.3%NTHi: 26.0%	Sp: 48.8%NTHi: 43.6%
Neves et al. 2017^Citation29	Niteroi (Rio de Janeiro State)	Cross-sectional	Post: Sep and Dec 2014 (4 years)	522 children, 118 (22.6%) were pneumococcal carriers	< 6 years	Pneumococcal carriage			• < 2 years: 52/321 (16.2%) • ≥2 years of age: 66/201 (32.8%) colonized with Sp (p < 0.01).
Brandileone et al. 2019^Citation22	Sao Paulo State	Cross-sectional	Pre: 2010 Post: 2013, 2017	531 children	1 - 2 years	VT Spn carriage NVT Spn carriage	Spn carriage increased from 40.3% (baseline) to 59.7% (2017 survey) (p < 0.001). Colonization by VT isolates significantly decreased by 90.9% (19.8–1.8%) and 95.5% (19.8–0.9%) in the 2013 and 2017 surveys, respectively, compared to that at baseline. NVT isolates increased significantly by 128% (19.6–44.8%) and 185% (19.6–55.9%) in the respective post-PCV10 surveys, most led to high prevalence of serotypes 6C (27%), 15B (9.8%), 19A (9.2%), 15A (6.0%), and 16F (5.7%). In 2017, reduction in serotype 6A (4.2–0.6%, p < 0.001) and increase in serotype 19A (1.8–6.0%, p = 0.001) were found.

*Included as abstract in previous article (Moreira et al, 2016).³

Abbreviations: AOM, acute otitis media; CAP, community acquired pneumonia; CI, confidence interval; IPD, invasive pneumococcal disease; NTHi, non-typeable Haemophilus influenzae; NVT, non-vaccine type; PCV, pneumococcal conjugate vaccine; PHiD-CV, 10-valent pneumococcal and non-typeable Haemophilus influenzae protein D conjugate vaccine; PM, pneumococcal meningitis; Sp, Streptococcus pneumoniae; VT, vaccine-type.

Figure 1. PRISMA flow chart of articles and conference abstracts identified for inclusion in the review.

Figure 2. Distribution of studies by (A) Region (state) in Brazil (N = 29)*, (B) Study design (N = 29), (C) Target population (N = 29), and (D) Outcome (N = 29)*

AOM, acute otitis media; CAP, community-acquired pneumonia; IPD, invasive pneumococcal disease; Naso., nasopharyngeal; OM, otitis media. *Total N = 30 because in 1 publication >1 outcome was reported.

Figure 3. Average vaccination coverage of primary and booster doses of PHiD-CV per (A) Brazilian states (2015* – 2019) and (B) year Note: In 2015* there was a 3 + 1 schedule, and after 2016 there is a 2 + 1 schedule.

The health system estimates coverage of the complete schedule by proxy of the coverage of the last dose (in this case, 3rd dose until 2015 and 2nd dose since 2016).

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