Effects of Pneumococcal Vaccination in Children Under Five Years of Age in the Democratic Republic of Congo: A Systematic Review
Abstract
:1. Introduction
2. Materials and Methods
2.1. DRC Context
2.2. Study
2.3. Documentary Search Strategy
2.4. Inclusion Criteria
2.5. Measuring the Effects of PCV13
2.5.1. Measures from Studies
2.5.2. Estimation of the Burden of Pneumococcal Infections Prevented in the DRC
3. Results
3.1. Selection of Studies
3.2. Profile of Studies Included in This Review and Effects of PCV13
3.3. Overall Effect of PCV13 on the Burden of Pneumococcal Infections in the DRC
4. Discussion
4.1. PCV13 Effects
4.2. PCV13 Serotypes
4.3. Limitations
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Disclaimer
References
- Bentley, S.D.; Lo, S.W. Global genomic pathogen surveillance to inform vaccine strategies: A decade-long expedition in pneumococcal genomics. Genome Med. 2021, 13, 84. [Google Scholar] [CrossRef] [PubMed]
- Feldman, C.; Anderson, R. Recent advances in the epidemiology and prevention of Streptococcus pneumoniae infections. F1000Research 2020, 9, 338. [Google Scholar] [CrossRef] [PubMed]
- Wahl, B.; O’Brien, K.L.; Greenbaum, A.; Majumder, A.; Liu, L.; Chu, Y.; Lukšić, I.; Nair, H.; McAllister, D.A.; Campbell, H.; et al. Burden of Streptococcus pneumoniae and Haemophilus influenzae type b disease in children in the era of conjugate vaccines: Global, regional, and national estimates for 2000–2015. Lancet Glob. Health 2018, 6, e744–e757. [Google Scholar] [CrossRef] [PubMed]
- Troeger, C.; Blacker, B.; Khalil, I.A.; Rao, P.C.; Cao, J.; Zimsen, S.R.M.; Albertson, S.B.; Deshpande, A.; Farag, T.; Abebe, Z.; et al. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of lower respiratory infections in 195 countries, 1990–2016: A systematic analysis for the Global Burden of Disease Study 2016. Lancet Infect. Dis. 2018, 18, 1191–1210. [Google Scholar] [CrossRef]
- Johnson, H.L.; Deloria-Knoll, M.; Levine, O.S.; Stoszek, S.K.; Hance, L.F.; Reithinger, R.; Muenz, L.R.; O’Brien, K.L. Systematic evaluation of serotypes causing invasive pneumococcal disease among children under five: The pneumococcal global serotype project. PLoS Med. 2010, 7, e1000348. [Google Scholar] [CrossRef]
- Adegbola, R.A.; DeAntonio, R.; Hill, P.C.; Roca, A.; Usuf, E.; Hoet, B.; Greenwood, B.M. Carriage of Streptococcus pneumoniae and other respiratory bacterial pathogens in low and lower-middle income countries: A systematic review and meta-analysis. PLoS ONE 2014, 9, e103293. [Google Scholar] [CrossRef]
- Russell, F.; Sanderson, C.; Temple, B.; Mulholland, K. Global review of the distribution of pneumococcal disease by age and region. In WHO Pneumococcal Epidemiology Report 31102011 v3; World Health Organization: Geneva, Switzerland, 2011. [Google Scholar]
- Scelfo, C.; Menzella, F.; Fontana, M.; Ghidoni, G.; Galeone, C.; Facciolongo, N.C. Pneumonia and invasive pneumococcal diseases: The role of pneumococcal conjugate vaccine in the era of multi-drug resistance. Vaccines 2021, 9, 420. [Google Scholar] [CrossRef]
- Musher, D.M.; Anderson, R.; Feldman, C. The remarkable history of pneumococcal vaccination: An ongoing challenge. Pneumonia 2022, 14, 5. [Google Scholar] [CrossRef]
- Fleming-Dutra, K.E.; Conklin, L.; Loo, J.D.; Knoll, M.D.; Park, D.E.; Kirk, J.; Goldblatt, D.; Whitney, C.G.; O’brien, K.L. Systematic review of the effect of pneumococcal conjugate vaccine dosing schedules on vaccine-type nasopharyngeal carriage. Pediatr. Infect. Dis. J. 2014, 33 (Suppl. S2), 152–160. [Google Scholar] [CrossRef]
- Reyburn, R.; Tsatsaronis, A.; von Mollendorf, C.; Mulholland, K.; Russell, F.M. Systematic review on the impact of the pneumococcal conjugate vaccine ten valent (PCV10) or thirteen valent (PCV13) on all-cause, radiologically confirmed and severe pneumonia hospitalisation rates and pneumonia mortality in children 0–9 years old. J. Glob. Health 2023, 13, 05002. [Google Scholar] [CrossRef]
- Corcoran, M.; Vickers, I.; Mereckiene, J.; Murchan, S.; Cotter, S.; Fitzgerald, M.; Mcelligott, M.; Cafferkey, M.; O’Flanagan, D.; Cunney, R.; et al. The epidemiology of invasive pneumococcal disease in older adults in the post-PCV era. Has there been a herd effect? Epidemiol. Infect. 2017, 145, 2390–2399. [Google Scholar] [CrossRef] [PubMed]
- Countdown to 2030. Tracking Progress Towards Universal Coverage for Women’s, Children’s and Adolescents’ Health; The 2017 Report; United Nations Children’s Fund (UNICEF) and the World Health Organization (WHO): Washington, DC, USA, 2017; Available online: https://www.countdown2030.org/publications/tracking-progress-towards-universal-coverage-for-womens-childrens-and-adolescents-health (accessed on 30 October 2024).
- Countdown to 2015. A Decade of Tracking Progress for Maternal, Newborn and Child Survival; The 2015 Report; World Health Organization: Geneva, Switzerland, 2015. [Google Scholar]
- Jo, Y.; Labrique, A.B.; Lefevre, A.E.; Mehl, G.; Pfaff, T.; Walker, N.; Friberg, I.K. Using the Lives Saved Tool (LiST) to Model mHealth Impact on Neonatal Survival in Resource-Limited Settings. PLoS ONE 2014, 9, e102224. [Google Scholar] [CrossRef] [PubMed]
- République Démocratique du Congo, Ministère de la Santé Publique, Programme Élargi de Vaccination. Plan Pluriannuel Complet du PEV 2013–2015 (Version Révisée); Ministère de la Santé Publique: Kinshasa, Democratic Republic of the Congo, 2015; Available online: https://extranet.who.int/countryplanningcycles/sites/default/files/planning_cycle_repository/democratic_republic_of_congo/ppac_rdc_2013-2015_mercredi_12_nov_2012_vf_-_alexis_2.pdf (accessed on 30 October 2024).
- Lassane, K. Impact Assessment of Childhood Immunization Programs in Limited-Resource Settings: Challenges in Ascertaining Vaccination Status and Application to Pneumococcal Conjugate Vaccine in Burkina Faso. Ph.D. Thesis, Faculté de Médecine, University of Geneva , Geneva, Switzerland, 2021. [Google Scholar]
- Birindwa, A.M.; Gonzales-Siles, L.; Nordén, R.; Geravandi, S.; Manegabe, J.T.; Morisho, L.; Mushobekwa, S.S.; Andersson, R.; Skovbjerg, S. High bacterial and viral load in the upper respiratory tract of children in the Democratic Republic of the Congo. PLoS ONE 2020, 15, e0240922. [Google Scholar]
- Coulibaly, A. Impact of Pneumococcal Conjugate Vaccine Thirteen Valent on the Reduction of Invasive Pneumococcal Disease. Ph.D. Thesis, Walden University, Minneapolis, MN, USA, 2016. Available online: https://scholarworks.waldenu.edu/dissertations/2116 (accessed on 30 October 2024).
- Izurieta, P.; Bahety, P.; Adegbola, R.; Clarke, C.; Hoet, B. Public health impact of pneumococcal conjugate vaccine infant immunization programs: Assessment of invasive pneumococcal disease burden and serotype distribution. Expert. Rev. Vaccines 2018, 17, 479–493. [Google Scholar] [CrossRef]
- Muhandule Birindwa, A. Acute Respiratory Infections Among Children in the Democratic Republic of the Congo—Nasopharyngeal Pathogens, Antibiotic Resistance and Vaccination. Ph.D. Thesis, University of Gothenburg, Gothenburg, Sweden, 2020. Available online: http://hdl.handle.net/2077/63279 (accessed on 30 October 2024).
- Mazamay, S.; Bompangue, D.; Guégan, J.F.; Muyembe, J.J.; Raoul, F.; Broutin, H. Understanding the spatio-temporal dynamics of meningitis epidemics outside the belt: The case of the Democratic Republic of Congo (DRC). BMC Infect. Dis. 2020, 20, 291. [Google Scholar] [CrossRef]
- Birindwa, A.M.; Kasereka, J.K.; Gonzales-Siles, L.; Geravandi, S.; Mwilo, M.; Tudiakwile, L.K.; Mwinja, N.L.; Muhigirwa, B.; Kashosi, T.; Manegabe, J.T.; et al. Bacteria and viruses in the upper respiratory tract of Congolese children with radiologically confirmed pneumonia. BMC Infect. Dis. 2021, 21, 837. [Google Scholar] [CrossRef]
- Touhami, K.O.; Sakkali, H.E.B.; Maaloum, F.; Diawara, I.; Touhami, M.O.; Bezzari, M.; Zerouali, K.; Belabbes, H. Meningitis caused by Streptococcus pneumoniae serotype 7a in an infant vaccinated with two doses of 13-valent pneumococcal conjugate vaccine: A case study. Pan. Afr. Med. J. 2019, 32, 203. [Google Scholar]
- Engo, S.M.I. Dynamique Spatio-Temporelle et Écologie des Méningites Bactériennes en Dehors de la Ceinture de la Méningite en Afrique: Cas de la République Démocratique du Congo. Ph.D. Thesis, Université Montpellier, Montpellier, France, 2019. [Google Scholar]
- Birindwa, A.M.; Emgård, M.; Nordén, R.; Samuelsson, E.; Geravandi, S.; Gonzales-Siles, L.; Muhigirwa, B.; Kashosi, T.; Munguakonkwa, E.; Manegabe, J.T.; et al. High rate of antibiotic resistance among pneumococci carried by healthy children in the eastern part of the Democratic Republic of the Congo. BMC Pediatr. 2018, 18, 361. [Google Scholar] [CrossRef]
- Manegabe, J.T.; Kitoga, M.; Mwilo, M.; Yoyu, J. Identified Bacteria and Virus in the Cerebrospinal Fluid of under Five Years Hospitalized Children for Clinical Meningitis at Panzi Hospital in the Eastern Part of DRC. Open J. Pediatr. 2023, 13, 676–688. [Google Scholar] [CrossRef]
- Mazamay, S.; Broutin, H.; Bompangue, D.; Muyembe, J.J.; Guégan, J.F. The environmental drivers of bacterial meningitis epidemics in the Democratic Republic of Congo, central Africa. PLoS Negl. Trop. Dis. 2020, 14, e0008634. [Google Scholar] [CrossRef]
- Wang, S. Global burden of pneumococcal disease in children under 5. In Proceedings of the PAHO Regional Symposium of New Vaccines, Lima, Peru, 1–3 December 2009. [Google Scholar]
- Bollinger, L.; Stover, J.; Hecht, K.; Podk, T.; Schmidt, J. Spectrum de Spectrum: Système Spectrum Pour les Modèles de Politiques; Avenir Health: Glastonbury, CT, USA, 2022. [Google Scholar]
- Armijo-Olivo, S.; Stiles, C.R.; Hagen, N.A.; Biondo, P.D.C.G. Assessment of study quality for systematic reviews: A comparison of the Cochrane Collaboration Risk of Bias Tool and the Effective Public Health Practice Project Quality Assessment Tool: Methodological research. J. Eval. Clin. Pract. 2012, 18, 12–18. [Google Scholar] [CrossRef] [PubMed]
- Bouyer, J.; Cordier, S.; Levallois, P. Épidémiologie. In Environnement et Santé Publique: Fondements et Pratiques; Gérin, M., Gosselin, P., Cordier, S., Viau, C., Quénel, P., Dewailly, É., Eds.; Edisem: Paris, France, 2003; pp. 89–118. [Google Scholar]
- Nagaraj, G.; Govindan, V.; Ganaie, F.; Venkatesha, V.T.; Hawkins, P.A.; Gladstone, R.A.; McGee, L.; Breiman, R.F.; Bentley, S.D.; Klugman, K.P.; et al. Streptococcus pneumoniae genomic datasets from an indian population describing pre-vaccine evolutionary epidemiology using a whole genome sequencing approach. Microb. Genom. 2021, 7, e1062–e1070. [Google Scholar] [CrossRef] [PubMed]
- Kaboré, L.; Adebanjo, T.; Njanpop-Lafourcade, B.M.; Ouangraoua, S.; Tarbangdo, F.T.; Meda, B.; Velusamy, S.; Bicaba, B.; Aké, F.; McGee, L.; et al. Pneumococcal Carriage in Burkina Faso after 13-Valent Pneumococcal Conjugate Vaccine Introduction: Results from 2 Cross-sectional Population-Based Surveys. J. Infect. Dis. 2021, 224, S258–S266. [Google Scholar] [CrossRef] [PubMed]
- Chan, J.; Lai, J.Y.R.; Nguyen, C.D.; Vilivong, K.; Dunne, E.M.; Dubot-Pérès, A.; Fox, K.; Hinds, J.; A Moore, K.; Nation, M.L.; et al. Indirect effects of 13-valent pneumococcal conjugate vaccine on pneumococcal carriage in children hospitalised with acute respiratory infection despite heterogeneous vaccine coverage: An observational study in Lao People’s Democratic Republic. BMJ Glob. Health 2021, 6, e005187. [Google Scholar] [CrossRef]
- Downs, S.L.; Olwagen, C.P.; Van Der Merwe, L.; Nzenze, S.A.; Nunes, M.C.; Madhi, S.A. Streptococcus pneumoniae and other bacterial nasopharyngeal colonization seven years post-introduction of 13-valent pneumococcal conjugate vaccine in South African children. Int. J. Infect. Dis. 2023, 134, 45–52. [Google Scholar] [CrossRef]
- Bar-Zeev, N.; Swarthout, T.D.; Everett, D.B.; Alaerts, M.; Msefula, J.; Brown, C.; Bilima, S.; Mallewa, J.; King, C.; von Gottberg, A.; et al. Impact and effectiveness of 13-valent pneumococcal conjugate vaccine on population incidence of vaccine and non-vaccine serotype invasive pneumococcal disease in Blantyre, Malawi, 2006–2018: Prospective observational time-series and case-control studies. Lancet Glob. Health 2021, 9, e989–e998. [Google Scholar] [CrossRef]
- Mackenzie, G.A.; Hill, P.C.; Jeffries, D.J.; Hossain, I.; Uchendu, U.; Ameh, D.; Ndiaye, M.; Adeyemi, O.; Pathirana, J.; Olatunji, Y.; et al. Effect of the introduction of pneumococcal conjugate vaccination on invasive pneumococcal disease in The Gambia: A population-based surveillance study. Lancet Infect. Dis. 2016, 16, 703–711. [Google Scholar] [CrossRef]
- Grant, L.R.; Slack, M.P.E.; Theilacker, C.; Vojicic, J.; Dion, S.; Reinert, R.R.; Jodar, L.; Gessner, B.D. Distribution of Serotypes Causing Invasive Pneumococcal Disease in Children from High-Income Countries and the Impact of Pediatric Pneumococcal Vaccination. Clin. Infect. Dis. 2023, 76, E1062–E1070. [Google Scholar] [CrossRef]
- Deloria Knoll, M.; Bennett, J.C.; Garcia Quesada, M.; Kagucia, E.W.; Peterson, M.E.; Feikin, D.R.; Cohen, A.L.; Hetrich, M.K.; Yang, Y.; Sinkevitch, J.N.; et al. Global landscape review of serotype-specific invasive pneumococcal disease surveillance among countries using PCV10/13: The pneumococcal serotype replacement and distribution estimation (PSERENADE) project. Microorganisms 2021, 9, 742. [Google Scholar] [CrossRef]
- Méroc, E.; Fletcher, M.A.; Hanquet, G.; Slack, M.P.E.; Baay, M.; Hayford, K.; Gessner, B.D.; Grant, L.R. Systematic Literature Review of the Epidemiological Characteristics of Pneumococcal Disease Caused by the Additional Serotypes Covered by the 20-Valent Pneumococcal Conjugate Vaccine. Microorganisms 2023, 11, 1816. [Google Scholar] [CrossRef]
Ref. | Author, Year | Specific Objective | Medium | Children’s Profile | No. | Type of Study | Study Period (Data Collection) | Judgment Criteria | Comparison | Measurement of Effect |
---|---|---|---|---|---|---|---|---|---|---|
[26] | Birindwa, A.M., 2018 | Nasopharyngeal carriage and conditions predisposing to pneumococcal colonization in healthy children after PCV13 introduction | South Kivu: Health Centers during preschool consultations | Healthy children aged 1 to 60 months | 794 | Cross-sectional | 2014 to June 2015 | S. pneumoniae carriage | PCV13 vs. Non-PCV13 | 2–3 vs. 0 doses: aOR = 0.07 95% CI: 0.03–0.14 1 vs. 0 dose: aOR = 0.84 95% CI: 0.55–1.27 |
[19] | Coulibaly, A., 2016 | To examine the relationship between childhood PCV13 immunization rates in DRC provinces and the incidence of invasive pneumococcal disease | Kinshasa: sentinel surveillance sites of Kalembelembe and Kingasani, and Lubumbashi at Sendwe hospital | Sick children treated in sentinel surveillance sites | 380 | Quasi-experimental, with control group | 2009, July 2013 | Incidence of invasive pneumococcal disease | PCV13 vs. Non-PCV13 | aOR = 0.33 95% CI: 0.63–0.18 |
[27] | Manegabe, J.T., 2023 | Determining the presence of bacteria and viruses in the CSF of hospitalized children with meningitis | South Kivu: pediatric department of Panzi hospital | Children hospitalized due to meningitis | 150 | Cross-sectional | April 2021 to end of March 2022 | CSF Presence of S. Pneumoniae in children | PCV13 vs. non-PCV13 | OR = 4.0 95% CI: 1.06–15.0 |
Author, Year | Outcomes | Number of Children | Odds Ratio (95%CI) | FIP at PCV13 % (95%CI) |
---|---|---|---|---|
Birindwa, A.M., 2018 [26] | S. pneumoniae carriage | 794 | 0.07 (0.03–0.14) † | 93.2 (86.3–96.6) |
Coulibaly, A., 2016 [19] | Incidence of invasive pneumococcal disease | 380 | 0.33 (0.63–0.18) | 66.7 (37.2–82.2) |
Manegabe, J.T., 2023 [27] | Presence of S. pneumoniae in children | 150 | 4.0 (1.06–15.0) | 75.0 (6.0–93.3) |
Children’s Profile | Included in PCV13 | Birindwa, A.M., 2018 [26] | Birindwa, A.M., 2020 [18] | Manegabe, J.T., 2023 [27] |
---|---|---|---|---|
Healthy Children | 2 to 59 Months Hospitalized for Pneumonia | Children Hospitalized with Meningitis | ||
Children with isolated serotypes(n) | 163 | 375 | 37 | |
% with S. pneumoniae | 20.5 | 77.0 | 37.8 | |
Included in PCV13 (%) ⱡ | 46.0 | 47.4 | 10.2 | |
Children PCV13 (%) ꬸ | 100.0 | 100.0 | 100.0 | |
1 | Yes | 0.0 | 2.8 | 0.0 |
19A | Yes | 8.7 | 13.9 | 0.0 |
19F | Yes | 52.2 | 44.4 | 100.0 |
14 | Yes | 4.3 | 2.8 | 0.0 |
23F | Yes | 8.7 | 2.8 | 0.0 |
9A/V | Yes | 4.3 | 5.6 | 0.0 |
3 | Yes | 8.7 | 0.0 | |
6ABCD | Yes | 8.7 | 0.0 | |
5 | Yes | 4.3 | 27.8 | 0.0 |
Non-PCV13 children (%) | 0.0 | 0.0 | 0.0 | |
18C | Yes | 0.0 | 0.0 | 0.0 |
4 | Yes | 0.0 | 0.0 | 0.0 |
Not included in PCV13 | 54.0 | 52.6 | 89.8 | |
Child PCV13 (%) | 14.8 | 0.0 | 73.3 | |
Unknown | 0.0 | 0.0 | 55.6 | |
13 | 0.0 | 0.0 | 11.1 | |
18 | 100.0 | 0.0 | 0.0 | |
23A | 0.0 | 0.0 | 2.0 | |
22F | 0.0 | 0.0 | 11.1 | |
33F | 0.0 | 0.0 | 11.1 | |
15B | 0.0 | 0.0 | 11.1 | |
Non-PCV13 children (%) | 85.2 | 100.0 | 26.7 | |
11A/D | 21.7 | 15.0 | 0.0 | |
10A | 8.7 | 15.0 | 0.0 | |
15B/C | 4.3 | 17.5 | 0.0 | |
12 | 4.3 | 7.5 | 0.0 | |
35B/35C | 30.4 | 17.5 | 0.0 | |
20 | 0.0 | 2.5 | 0.0 | |
38 | 0.0 | 7.5 | 0.0 | |
34/17A | 13.0 | 0.0 | 0.0 | |
9N/L | 4.3 | 0.0 | 0.0 | |
17 | 4.3 | 0.0 | 0.0 | |
2 | 4.3 | 2.5 | 66.7 | |
7C | 4.3 | 7.5 | 33.3 | |
22F | 0.0 | 2.5 | 0.0 | |
20 | 0.0 | 2.5 | 0.0 | |
7AF | 0.0 | 2.5 | 0.0 |
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Nimpa, M.M.; Ntambue, A.; Ngandu, C.; Danovaro-Holliday, M.C.; Bita Fouda, A.; Cikomola, A.M.-W.; Mukendi, J.-C.; Mwamba, D.; Aluma, A.D.L.; Yapi, M.D.; et al. Effects of Pneumococcal Vaccination in Children Under Five Years of Age in the Democratic Republic of Congo: A Systematic Review. Vaccines 2025, 13, 603. https://doi.org/10.3390/vaccines13060603
Nimpa MM, Ntambue A, Ngandu C, Danovaro-Holliday MC, Bita Fouda A, Cikomola AM-W, Mukendi J-C, Mwamba D, Aluma ADL, Yapi MD, et al. Effects of Pneumococcal Vaccination in Children Under Five Years of Age in the Democratic Republic of Congo: A Systematic Review. Vaccines. 2025; 13(6):603. https://doi.org/10.3390/vaccines13060603
Chicago/Turabian StyleNimpa, Marcellin Mengouo, Abel Ntambue, Christian Ngandu, M. Carolina Danovaro-Holliday, André Bita Fouda, Aimé Mwana-Wabene Cikomola, Jean-Crispin Mukendi, Dieudonné Mwamba, Adèle Daleke Lisi Aluma, Moise Désiré Yapi, and et al. 2025. "Effects of Pneumococcal Vaccination in Children Under Five Years of Age in the Democratic Republic of Congo: A Systematic Review" Vaccines 13, no. 6: 603. https://doi.org/10.3390/vaccines13060603
APA StyleNimpa, M. M., Ntambue, A., Ngandu, C., Danovaro-Holliday, M. C., Bita Fouda, A., Cikomola, A. M.-W., Mukendi, J.-C., Mwamba, D., Aluma, A. D. L., Yapi, M. D., Nikiema, J. B., Hama Sambo, B., & Ishoso, D. K. (2025). Effects of Pneumococcal Vaccination in Children Under Five Years of Age in the Democratic Republic of Congo: A Systematic Review. Vaccines, 13(6), 603. https://doi.org/10.3390/vaccines13060603