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. 2024 May 20;19(5):e0297767. doi: 10.1371/journal.pone.0297767

Nasopharyngeal carriage of Streptococcus pneumoniae in Latin America and the Caribbean: A systematic review and meta-analysis

Martín Brizuela 1,*, María Carolina Palermo 2, Tomás Alconada 2, María Macarena Sandoval 2, Eugenia Ramirez Wierzbicki 2, Joaquín Cantos 2, Paula Gagetti 3, Agustín Ciapponi 2,4, Ariel Bardach 2,4, Silvina Ruvinsky 5,6
Editor: Oriana Rivera-Lozada de Bonilla7
PMCID: PMC11104613  PMID: 38768099

Abstract

Background

Streptococcus pneumoniae is a leading cause of morbidity and mortality globally, causing bacteremic pneumonia, meningitis, sepsis, and other invasive pneumococcal diseases. Evidence supports nasopharyngeal pneumococcal carriage as a reservoir for transmission and precursor of pneumococcal disease.

Objectives

To estimate the pneumococcal nasopharyngeal burden in all age groups in Latin America and the Caribbean (LAC) before, during, and after the introduction of pneumococcal vaccine conjugate (PVC).

Methods

Systematic literature review of international, regional, and country-published and unpublished data, together with reports including data from serotype distribution in nasopharyngeal carriage in children and adults from LAC countries following Cochrane methods. The protocol was registered in PROSPERO database (ID: CRD42023392097).

Results

We included 54 studies with data on nasopharyngeal pneumococcal carriage and serotypes from 31,803 patients. In children under five years old, carriage was found in 41% and in adults over 65, it was 26%. During the study period, children under five showed a colonization proportion of 34% with PCV10 serotypes and 45% with PCV13 serotypes. When we analyze the carriage prevalence of PCV serotypes in all age groups between 1995 and 2019, serotypes included in PCV10 and those included in PCV13, both showed a decreasing trend along analysis by lustrum.

Conclusion

The data presented in this study highlights the need to establish national surveillance programs to monitor pneumococcal nasopharyngeal carriage to monitor serotype prevalence and replacement before and after including new pneumococcal vaccines in the region. In addition, to analyze differences in the prevalence of serotypes between countries, emphasize the importance of approaches to local realities to reduce IPD effectively.

Introduction

Streptococcus pneumoniae is a significant cause of morbidity and mortality worldwide producing different types of infections such as bacteremic pneumonia, meningitis, sepsis and other invasive pneumococcal diseases (IPD). Evidence supports nasopharyngeal pneumococcal carriage as a reservoir for transmission and precursor of pneumococcal disease [1, 2].

Complex relationships between S. pneumoniae and the human host were described. The main reservoir of S. pneumoniae is the upper airway, allowing transmission. Host factors are essential for developing pneumococcal disease, mainly acute otitis media, pneumonia, bacteremia, and meningitis. The colonization, transmission, and invasion are related to the capacity to evade immune and inflammatory host responses [3, 4].

As with pneumococcal disease, the epidemiology of pneumococcal carriage varies by age; the highest rate among children < 5 years was reported [3].

Pneumococcal conjugate vaccines (PCVs) are safe and effective and have been used in high-income countries for many years. They have now been widely adopted worldwide. Vaccination with PCV provides herd immunity, reducing the transmission to households and others in the community, and preventing pneumococcal infection in the unvaccinated population [5].

Following the introduction of pneumococcal conjugate vaccines (PCVs) into national immunization programs (NIPs), IPD and nasopharyngeal carriage was reduced in upper-middle and high-income countries [6]. This reduction has been observed primarily among vaccinated children and all ages, including the elderly [7].

In LAC countries, PCVs have been introduced in their NIPs since 2007 with different strategies (“3+1” and “2+1”) [8]. An impact in reducing pneumococcal vaccine-serotypes carriage and increasing non-vaccine serotypes was observed [9]. Despite evidence of almost complete replacement of serotypes in many settings, non-vaccine (NVT) serotypes have replaced vaccine-type (VT) serotypes in colonization and invasive diseases [10, 11].

Data on the epidemiology of pneumococcal carriage in children and adults after the introduction of PCV10 and PCV13 in the region are scarce. Understanding the dynamics of nasopharyngeal colonization in developing regions is crucial to predicting the public health implications of routine PCVs’ use in these settings [12].

This systematic review and meta-analysis aimed to add epidemiological information about pneumococcal nasopharyngeal carriage distribution since PVCs introduction in all age groups in LAC.

Material and methods

We conducted this systematic literature review of international, regional, and country-published and unpublished data, together with reports of routinely recorded data such as registries and MoH, including data from serotype distribution in nasopharyngeal carriage in children and adults from LAC countries.

The Cochrane methods and the 2020 Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) were followed [13] and the established guidelines for Meta- analysis Of Observational Studies in Epidemiology (MOOSE). The protocol was registered in PROSPERO database (ID: CRD42023392097) [14, 15].

Eligibility criteria

We included cohort studies, case-control, cross-sectional studies, epidemiological surveillance reports, hospital-based surveillance studies, case series, control arms of randomized/quasi-randomized controlled trials, controlled before and after (CBA) and uncontrolled before and after (UBA) studies, interrupted time series (ITS), and controlled ITS (CITS), assessing serotyping of nasopharyngeal carriage in LAC. No language restriction was imposed. Studies with at least 20 nasopharyngeal swabs of patients of all ages, published or reported since January 2000, were included. Every Latin American and Caribbean country represented the geographical scope.

Systematic reviews and meta-analyses were considered a source of primary studies. In those cases where data or data subsets were reported in more than one publication, the one with the larger sample size was selected.

Data sources and search strategy

We searched the primary literature, international and regional databases, generic and academic internet searches, and meta-search engines. We searched records from the following databases up to 27 December 2022: MEDLINE (PubMed), EMBASE (Elsevier interface), LILACS/ Scielo, EconLIT (EBSCO Interface), Global Health (OVID), CINAHL (EBSCO Interface), and Web of Science. We also consult websites from the leading regional medical societies, experts, and associations related to the topic. An annotated search strategy for grey literature was included to retrieve information from relevant sources like regional MoH, PAHO, and reports from hospitals. This strategy comprises two blocks plus search limits (from 2000 onwards to cover ten years of pre-vaccination programs) and a geographical string block for LAC. The search had no language restrictions and was limited to humans. The reference lists of the articles were hand-searched for additional information. After consulting the principal investigator, we selected only the publication with the largest sample size. Highly cited authors were contacted to obtain missing or extra information.

Selection of studies, data extraction, and assessment of the risk of bias

Two researchers reviewed each identified record by title and abstract and obtained the full texts of potentially eligible studies. The full-text articles were reviewed for compliance with the inclusion criteria. The selection process was conducted via COVIDENCE [16, 17]. This form was piloted on ten papers to refine the process. If studies had multiple publications, we collated the various reports of the same study under a single study ID with multiple references. Data from eligible studies were extracted by two reviewers using a data extraction form. Two reviewers independently performed all steps. Any disagreements were resolved by discussion with the whole team.

We independently assessed the risk of bias in observational cohort, case-control, cross-sectional, and case-series studies with the National Institute of Health (NIH) Quality Assessment Tool. After answering the different signaling questions ‘‘Yes”, ‘‘No”, ‘‘Cannot determine”, ‘‘Not applicable”, or ‘‘Not reported”, the raters classified the study quality as ‘‘Good”, ‘‘Fair”, or ‘‘Poor”. For consistency with the other designs, we use the classifications ‘‘Low”, ‘‘Unclear” or ‘‘High risk” of bias [18]. When the criteria are rated "uncertain," we obtained more information from the study authors. Pairs of independent reviewers assessed the risk of bias. Discrepancies were solved by consensus of the whole team. For the assessment of cohort studies and cross-sectional studies, the tool comprises 14 items, while nine items apply to the case series studies. For RCTs and quasi-RCTs, we evaluated the following domains: sequence generation, allocation concealment, blinding of participants and personnel, blinding of outcome assessors, incomplete outcome data, selective outcome reporting, and other possible threats to validity [19].

Data synthesis and analysis

Data were collected from observational, comparative, and non-comparative studies, including registries. We conducted a paired meta-analysis for outcomes for which studies were deemed comparable. To estimate the prevalence of pneumococcal serotypes, we conducted a proportional meta-analysis using R software version 4.2.2 [20, 21]. We applied an arc-sine transformation to stabilize the variance of proportions (Freeman-Tukey variant of the arc-sine square root of transformed proportions method) [22]. The pooled proportion was calculated as the back-transformation of the weighted mean of the transformed proportions, using inverse arcsine variance weights for the fixed and random effects model. We applied DerSimonian-Laird weights for the random effects model where heterogeneity between studies was found. We calculated the I2 statistic as a measure of the proportion of the overall variations in the proportion that was attributable to between-study heterogeneity. An I2 of 60–70% was considered significant heterogeneity, and below 30% was considered low heterogeneity [23].

We conducted subgroup analyses classifying the studies by five-year calendar period, country, and age group (0–5 years, 6–64 years, 65 or more years old). We included data on different S. pneumoniae serotypes obtained from nasopharyngeal swabs.

Results

We retrieved 8,600 records from seven different databases. Of these registries, 4,533 references remained for the screening phase after duplicates were removed, and 414 were eligible for full-text review.

Finally, we included 54 studies with data on nasopharyngeal pneumococcal carriage and serotypes from 31,803 patients. Fig 1 and S1 Table in S1 File. The search strategy is available in S1 Annex in S1 File, and the list of studies excluded during the extraction process in S2 Table in S1 File.

Fig 1. Study flowchart.

Fig 1

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The characteristics of the 54 included studies are described in Table 1. We identified 43 studies that included participants below 18 years (n = 27,491), three with an adult population (n = 739), seven studies that included both pediatric and adults (n = 3,500), and one study did not report the age of participants (n = 73).

Table 1. Characteristics of included studies (n = 54).

Author and year of publication Country Study start date dd/mm/yyyy Study ending date dd/mm/yyyy Study design Age range Sample size
Wolf 2000* [24] Brazil 15/03/1998 15/12/1998 Case control <5y 435
Cullotta 2002* [25] Peru 06/06/2000 21/08/2000 Case series <5y 302
Gómez-Barreto 2002* [26] Mexico 01/09/1997 30/09/1999 Cross sectional NR 73
Rey 2002* [27] Brazil 01/01/1998 31/12/1998 Cross sectional <5y 911
Allen 2003* [28] Jamaica 01/06/1999 30/06/1999 Cross sectional <18y 276
Lucarevschi 2003* [29] Brazil 29/06/1998 15/12/1998 Cross sectional <5y 987
Ochoa 2005* [30] Peru 01/09/1996 31/12/2003 Cross sectional/Surveillance <2y 666
Solorzano Santos 2005* [31] Mexico 01/02/2002 31/01/2003 Cross sectional <5y 573
Cardozo 2006* [32] Brazil 01/11/2002 31/07/2003 Cross sectional <18y 1,013
Laval 2006* [33] Brazil 01/05/2000 31/08/2001 Cross sectional/Surveillance <5y 648
Quintero 2006* [34] Venezuela 01/02/2000 31/07/2000 Cross sectional <5y 125
Alturraza Hernaez 2007* [35] Chile 20/08/1998 30/10/1998 Cross sectional >65y 118
Berezin 2007* [36] Brazil 01/06/1997 31/05/2001 Case series <5y 520
Espinosa-de los Monteros 2007* [37] Mexico 01/09/2002 31/12/2002 Cross sectional <5y 2,777
Nicoletti 2007* [38] Brazil 01/03/2000 31/12/2001 Cross sectional ≥18y 385
Rivera Olivero 2007* [39] Venezuela 01/04/2004 31/01/2005 Cross sectional/Surveillance <5y 356
Neves Reis 2008* [40] Brazil 01/07/2000 31/05/2001 Cross sectional All ages 262
Reyna 2008* [41] Mexico 01/01/2006 31/12/2006 Cross sectional <5y 498
Bello González 2010* [42] Venezuela 01/05/2008 31/05/2008 Cross sectional All ages 148
Espinosa-de los Monteros 2010* [43] Mexico 01/02/2002 28/02/2004 Prospective cohort <2y 183
Franco 2010 [44] Brazil 01/08/2005 31/12/2005 Cross sectional <5y 1,192
Sisco 2010** [45] Venezuela NR NR Cross sectional/Surveillance All ages 488
Inverarity 2011* [46] Bolivia 01/05/2007 30/06/2007 Cross sectional <18y 601
Quintero 2011* [47] Venezuela 01/01/2007 28/02/2007 Cross sectional <5y 250
Rivera Olivero 2011* [48] Venezuela 01/12/2006 31/01/2008 Cross sectional/Surveillance <5y 1,004
Lamaro Cardoso 2012* [49] Brazil 01/07/2008 30/09/2008 Cross sectional All ages 224
Lopes 2012* [50] Brazil 01/05/2005 31/01/2006 Cross sectional <1y 139
Mercado 2012* [51] Peru 01/01/2007 31/12/2009 Cross sectional/Surveillance <2y 2,123
Méndez 2013* [52] Panama 25/11/2008 19/12/2008 Cross sectional <5y 397
Neves 2013* [53] Brazil 01/03/2010 30/06/2010 Cross sectional <5y 242
Parra 2013* [54] Colombia 01/01/2005 31/12/2011 Cross sectional <2y 443
Andrade 2014* [55] Brazil 01/12/2010 28/02/2011 Cross sectional <2y 1,287
Grijalva 2014* [56] Peru 01/05/2009 30/09/2011 Cross sectional <5y 309
Laranjeira 2014*** [57] Brazil 01/01/2011 31/12/2011 Cross sectional <5y 291
Rivera Olivero 2014* [58] Venezuela 01/01/2007 31/12/2009 Cross sectional/Surveillance <5y 82
Menezes 2015* [59] Brazil 01/01/2008 31/01/2009 Cross sectional <5y 203
Brandileone 2016* [60] Brazil 22/03/2010 06/06/2013 Cross sectional <2y 901
Melgar 2016* [61] Guatemala 01/11/2012 31/01/2013 Case series <5y 500
Gentile 2017** [62] Argentina 01/06/2015 30/09/2015 Cross sectional <5y 359
Neves 2017* [63] Brazil 20/09/2014 05/12/2014 Cross sectional <5y 522
Toledo Romani 2017* [64] Cuba 01/10/2013 30/11/2015 Cross sectional <5y 2,115
Fernández 2018* [65] Uruguay 01/01/2002 31/12/2015 Cross sectional/Surveillance <2y 831
Nelson 2018* [66] Peru 01/05/2009 30/09/2011 Prospective cohort <5y 1,015
Brandileone 2019* [67] Brazil 16/08/2017 19/08/2017 Cross sectional <2y 531
Cassiolato 2019 [68] Brazil 01/01/2005 31/12/2017 Cross sectional All ages 1,432
Chávez Amaro 2019* [69] Cuba 01/05/2016 30/06/2017 Non-comparative cohort <5y 555
Espinosa-de los Monteros-Pérez 2019* [70] Mexico 01/12/2009 30/06/2010 Cross sectional >50y 236
Pinto 2019* [71] Brazil 01/01/1990 31/12/2014 Cross sectional All ages 783
Kumar 2020** [72] Barbados 01/01/2015 31/12/2016 Cross sectional <5y 216
Dunn 2021* [73] Dominican Republic 01/11/2016 31/07/2017 Prospective cohort <5y 125
Kumar 2021* [74] Barbados 01/01/2016 31/12/2017 Cross sectional <10y 198
Regalado 2021* [75] Ecuador 01/02/2018 30/04/2018 Cross sectional All ages 163
Watkins 2021* [76] Haiti 01/09/2015 31/01/2016 Cross sectional <5y 685
Silva 2022* [77] Brazil 01/02/2013 31/12/2013 Cross sectional/Surveillance <5y 660
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NR: Not Reported

*Full text;

**Abstract/Poster;

***Thesis

The studies were carried out in 17 countries; the most represented countries were Brazil (n = 22 with 14,234 participants), Venezuela (n = 7 with 2,453 participants) and Mexico (n = 6 with 4,340 participants). The inclusion period of participants was from 1990 to 2018.

In 47 studies, data provided was from outpatients, in one from inpatients, and in six studies it was not reported. Nineteen studies included asymptomatic and healthy participants and three included high-risk patients. Comorbidities were reported in 12 studies; respiratory chronic diseases, malnutrition, cardiac diseases, immunodeficiency, and cancer were the most frequent.

All participants came from non-probability sampling. Immunization status was reported in 37 studies: 21 included not vaccinated participants, eight studies with completely vaccinated patients, eight both (complete and incomplete vaccination), and not reported in 17 studies. Immunization scheme was: PCV7 in 5 studies, PCV10 in 3 studies, and PCV13 in 8.

Regarding the methodological design, there were 46 cross-sectional studies, including nine epidemiological surveillance studies, followed by 4 cohort studies, 3 case- series, and one case-control study.

Meta-analysis of pneumococcal nasopharyngeal carriage

The global carriage proportion for all age groups was 38.3% (33% to 44%, CI 95%) from 1995 to 2019. In children under five years old, carriage was found in 41% (35% to 48%, CI 95%), and in adults over 65, 26% (19 to 35%, CI 95%) Figs 2 and 3. Brazil, Mexico, and Venezuela were the most representative countries with data about the nasopharyngeal carriage, including five or more studies. In Brazil, a pooled percentage of 37% (29–45%, CI 95%) was estimated, in Mexico, 34% (22–49%, CI 95%), and in Venezuela, 36% (27–47%, CI 95%). Fig 4.

Fig 2. Meta- analysis of nasopharyngeal carriage ratio by age group.

Fig 2

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Fig 3. Meta- analysis of nasopharyngeal carriage ratio by lustrum.

Fig 3

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Fig 4. Meta-analysis of S. pneumoniae carriage proportion by country.

Fig 4

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When we analyzed the most representative age group to evaluate carriage, preschool children under five years old, we found a stable proportion (33–44%) among all study periods (1995–2019). In a subgroup analysis of children between 0 and 2 years old, a global nasopharyngeal carriage ratio of 40% (32–49%, CI 95%) was found. Fig 5. During the study period, children under five showed a colonization proportion of 34% (27–41%, CI 95%) with PCV10 serotypes and 45% (36–54%, CI 95%) with PCV13 serotypes. Fig 6. Only one study reported pneumococcal nasopharyngeal carriage in the adult population more than 65 years old, and the proportion of serotypes was 51.5% (35% to 68% CI 95%) and 57.6% (41% to 73% CI 95%) for PCV10 and PCV13 respectively.

Fig 5. Meta- analysis nasopharyngeal carriage ratio among children <2 years old.

Fig 5

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Fig 6. Meta- analysis nasopharyngeal carriage ratio among children <5 years old.

Fig 6

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Serotypes included in PCV10 and PCV13 vaccines among nasopharyngeal carriage were analyzed by age (0- 5y, 6- 64y, and more than 65y), lustrum, and country. See S1-S8 Figs in S1 File.

We analyze the carriage prevalence of PCV serotypes in all age groups between 1995 and 2019. Serotypes included in PCV10 were 34% (28% to 40%, CI 95%), and those included in PCV13 serotypes were 45% (38% to 55%, CI 95%). Both showed a decreasing trend along analysis by five-year period. S3 Table in S1 File.

Risk of bias in included studies

Among 46 cross-sectional and four cohorts, 31 studies (62%) were evaluated with a moderate risk of bias; 14 (28%) with a high risk, and 5 (10%) with a low risk of bias. The domains that presented the most significant inconvenience in their evaluation were those related to the sample selection, the calculation of sample size, and the measurements of the results according to different exposures. Likewise, other drawbacks in the evaluation were associated with the validation domains of the results regarding the blinding of the observers and the adjustment for possible confounding variables. Of note, other domains could not be assessed due to the nature of the studies, such as repeated measurements and follow-up in cross-sectional studies S4 Table in S1 File. The only three case series studies had a moderate risk of bias with significant inconvenience in the case definition and statistical results management. The studies did not report if the cases were included consecutively S5 Table in S1 File. Finally, one case-control study was classified with a moderate risk of bias. The study showed the most inconvenience in the statistical management of data, sample size calculation, and blindness of observations S6 Table in S1 File.

Discussion

Streptococcus pneumoniae nasopharyngeal carriage could be a precondition for pneumococcal disease and community transmission [78]. There are approximately one hundred serotypes, several producing invasive pneumococcal disease (IPD). The prevalence of nasopharyngeal carriage reported varies between 20–40% in healthy children and ranges from 5 to 10% among adults less than 65 years old, similar to our finding [4, 79]. While several studies showed colonization data among young children, fewer studies were performed in the elderly population. Almeida S, et al. [80] found a low global nasopharyngeal carriage (2.3%) in the elderly population living in Portugal. In our study, the data about adults older than 65 in the LAC region was found to have a higher prevalence rate of nasopharyngeal colonization, probably due to only one study being included. Pneumococcal carriage is highest during the first five years of life, peaking in the first two years in most developed countries [3].

Regev-Yochay 2004 [81] found that the rate of S. pneumoniae carriage was higher among children than adults in the same community. Hadinegoro 2016 [82] examined healthy children in Indonesia and identified several prevalent serotypes of S. pneumoniae. León 2019 [83] focused on indigenous communities in Ecuador and highlighted the need for studies on respiratory pathogen colonization in high-risk groups. Gámez 2020 [84] investigated nasopharyngeal colonization in children in southwestern Colombia and found a high frequency of S. pneumoniae carriage, including strains resistant to multiple antimicrobial agents.

As was described in developed and undeveloped countries, an inverse relationship between age and carriage exists [85, 86]. In line with those findings, we observed that patients under five have the highest proportion of carriage.

Disparities in the prevalence of carriage between different countries, ranging from relatively low prevalence in countries such as Barbados, Chile, and Cuba to high prevalence in Peru, Argentina, and the Dominican Republic, call for further exploration of underlying factors, such as socioeconomic conditions, health care infrastructure, and vaccination policies.

Regarding the serotype distribution in the nasopharyngeal carriage, the analysis considered the serotypes included in the PCV10 and PCV13 vaccines in the region. Previous studies have shown that the introduction of PCV10 and PCV13 in the NIP led to a decrease in pneumococcal carriage, transmission, and circulation, resulting in a reduction of IPD [87–92]. Introducing pneumococcal conjugated vaccines (PCV) in national immunization programs has increased the nasopharyngeal colonization by serotypes not included in vaccines, with a reduction of vaccine serotypes by replacement [9]. When we analyze the distribution of serotypes in pneumococcal carriage, serotypes included in PCV10 and PCV13 decreased during the last lustrum (2015–2019), probably related to serotype replacement. However, non-PCV10/PCV13 serotypes in nasopharyngeal carriage predominate in all age groups in the region, similar to those reported by Rybak A et al. [93] The effect of vaccination on carriage offers herd protection mediated through a reduction in nasopharyngeal carriage of vaccine serotypes and pneumococcal transmission in the community.

Our study has some limitations; the heterogeneity and risk of bias of study settings and the absence of active nor passive pneumococcal nasopharyngeal carriage surveillance programs in countries in our region. Data about underlying diseases, environmental factors, or pneumococcal vaccination status of studies included were unavailable. In assessing the risk of bias, sample selection, size, and outcome measurement were the most critical aspects. Case series were mostly low or medium risk, with selection and statistical methods concerns.

The present systematic review, which includes 54 studies and covers data from 31,803 patients, offers a novel, detailed, and exhaustive panorama of the nasopharyngeal carriage of S. pneumoniae in the Latin American region. This extensive database provides valuable information on the epidemiology and prevalence of this pathogen, providing data on its impact on public health and possible implications for vaccination strategies. Our study contributes a baseline that could be useful to monitor the impact of new pneumococcal vaccine introduction on nasopharyngeal carriage in LAC.

In conclusion, the data presented in this study highlights the need to establish national surveillance programs to monitor pneumococcal nasopharyngeal carriage to monitor serotype prevalence and replacement before and after including new pneumococcal vaccines in the region. In addition, to analyze differences in the prevalence of serotypes between countries, emphasize the importance of approaches to local realities to reduce IPD effectively.

Supporting information

S1 File

(DOCX)

pone.0297767.s001.docx (3.9MB, docx)

Acknowledgments

The authors thank Mr.Daniel Comande, the Institute for Clinical Effectiveness and Health Policy librarian, for contributing to the bibliographic searches.

Data Availability

All relevant data are within the manuscript and its Supporting information files.

Funding Statement

All authors have received funding by Pfizer Global Medical Grants (GMG) 76436251. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Decision Letter 0

Oriana Rivera-Lozada de Bonilla

12 Dec 2023

PONE-D-23-35902Nasopharyngeal carriage of Streptococcus pneumoniae in Latin America and the Caribbean: a systematic review and meta-analysisPLOS ONE

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https://pubmed.ncbi.nlm.nih.gov/37012114/

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Comments to the Author

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

********** 

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: N/A

Reviewer #3: Yes

********** 

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

********** 

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

********** 

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Reviewer #1: Dear authors,

Thank you for this interesting review article. there are some comments which is not affect the quality of the search:

1. line 59: change Colonization to colonization.

2. line 107: change 2,022 to 2022.

3. line 161, 196: delete the word see (quotation brackets are sufficient).

4. Table 1: It's better if you sort the studies by year of publication, from 2001 to 2022.

5. line 199, 203, 205: fig. 4, 5, 6 change to figure 4, figure 5, figure 6.

Reviewer #2: The review is well designed and I hope it can be repeated with real clinical application. Not only as a review. I hope it could make equal time zone for all investigated areas. Also I wish there is a good evidence for vaccine efficacy.

Reviewer #3: The author outlined detailed information in each section of the manuscript. The data with figures are available in the manuscript. The supporting figures are available and explained very clearly. The article is clear and unambiguous.

********** 

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Reviewer #1: Yes: Awatif Al-Judaibi

Reviewer #2: Yes: Dr Michael Nazmy Agban professor of Microbiology and Immunology faculty of medicine assiut university Egypt. Head of department of molecular biology at molecular biology institute

Reviewer #3: Yes: VenkataVinayKumar Bandarupalli

**********

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PLoS One. 2024 May 20;19(5):e0297767. doi: 10.1371/journal.pone.0297767.r002

Author response to Decision Letter 0

8 Jan 2024

Dear editors and reviewers, thank you very much for your valuable contributions and suggestions. We have followed all suggestions and corrections to improve the quality of our research.

Below we detail the response to each of the points and have highlighted the modifications in the manuscript. Again, thank you very much.

Reviewer Request:

Table 1: It is best to order the studies by year of publication, from 2001 to 2022.

Answer:

All included studies were sorted by date.

Order:

We note that you have a minor occurrence of overlapping text with the following previous publications, which needs to be addressed: https://pubmed.ncbi.nlm.nih.gov/37012114/

Reply:

We have rephrased some material phrases and methods to improve quality and avoid overlaps.

Request financial disclosure: “All authors have received funding from Pfizer Global Medical Grants (GMG) 76436251.”

Reply:

We have added a modified feature of the funder disclosure in our cover letter and in the manuscript.

Request: We note that you have stated that you will provide repository information for your data upon acceptance. If your manuscript is accepted for publication, we will retain it until you provide the relevant accession numbers or DOIs needed to access your data. If you want to make changes to your data availability statement, please describe these changes in your cover letter and we will update your data availability statement to reflect the information you provide.

Response: We have changed all information available in the manuscript and supporting information

Request: Please include a separate title for each figure in your manuscript.

Answer: We have included a separate title for each figure in the manuscript.

Application: Please review your reference list to ensure it is complete and correct.

Answer: All references have been reviewed and are correct.

Request: Please upload a new copy of Figures 1, 2, 3, 4, 5 and 6 as the details are unclear.

Answer: The new files in figures 1 to 6 were uploaded with the best possible quality.

These specific comments and suggestions from reviewer one were modified in the manuscript and highlighted:

1. line 59: change Colonization to colonization. Response: we added The colonization....

2. line 107: change 2,022 to 2022. Response: it was changed

3. line 161, 196: delete the word see (quotation brackets are sufficient). Response: deleted

4. Table 1: It's better if you sort the studies by year of publication, from 2001 to 2022. Response: it was sorted in a cronological order

5. line 199, 203, 205: fig. 4, 5, 6 change to figure 4, figure 5, figure 6. Response: it was changed

Attachment

Submitted filename: Response to Reviewers PONE-D-23-35902.docx

pone.0297767.s002.docx (15.5KB, docx)

Decision Letter 1

Oriana Rivera-Lozada de Bonilla

12 Jan 2024

Portación nasofaríngea de Streptococcus pneumoniae en América Latina y el Caribe: una revisión sistemática y metanálisis

PONE-D-23-35902R1

Estimado Dr. Martín Brizuela ,

Nos complace informarle que su manuscrito ha sido considerado científicamente adecuado para su publicación y será aceptado formalmente para su publicación una vez que cumpla con todos los requisitos técnicos pendientes.

Dentro de una semana, recibirá un correo electrónico detallando las modificaciones requeridas. Una vez que se hayan abordado, recibirá una carta de aceptación formal y se programará la publicación de su manuscrito.

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Atentamente,

Oriana Rivera-Lozada de Bonilla

Editora Académica

PLOS ONE

Acceptance letter

Oriana Rivera-Lozada de Bonilla

5 Feb 2024

PONE-D-23-35902R1

PLOS ONE

Dear Dr. Brizuela,

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team.

At this stage, our production department will prepare your paper for publication. This includes ensuring the following:

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Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Oriana Rivera-Lozada de Bonilla

Academic Editor

PLOS ONE

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    pone.0297767.s002.docx (15.5KB, docx)

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