Post-Vaccination Surveillance of Invasive Pneumococcal Disease in Ghana
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Site and Design
2.2. Patient Recruitment and Specimen Collection
2.3. Laboratory Investigations
2.4. Data Analysis
2.5. Ethical Considerations
3. Results
3.1. Demographic Features of the Patients Recruited in the Study
3.2. Clinical Features of the Patients Recruited in the Study
3.3. Prevalence of IPD, Causative Serotypes, and AMR
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
| AMC | Amoxicillin–clavulanate |
| AMR | Antimicrobial resistance |
| AST | Antimicrobial susceptibility testing |
| BSI | Bloodstream infection |
| CAP | Community-acquired pneumonia |
| CDC | Centres for Disease Control and Prevention |
| CLSI | Clinical and Laboratory Standards Institute |
| CSF | Cerebrospinal fluid |
| EML | Essential Medicines List |
| ERH | Eastern Regional Hospital |
| GARH | Greater Accra Regional Hospital |
| HRH | Ho Regional Hospital |
| KBTH | Korle Bu Teaching Hospital |
| IPD | Invasive pneumococcal disease |
| MDR | Multidrug-resistant |
| NHISML | National Health Insurance Scheme Medicines List |
| PCV | Pneumococcal conjugate vaccine |
| PML | Princess Marie Louise Children’s Hospital |
| PPV | Pneumococcal polysaccharide vaccine |
| SXT | Sulphamethoxazole–trimethoprim |
| STGs | Standard Treatment Guidelines |
| WHO | World Health Organization |
| ZPHRLT | Zonal Public Health and Reference Laboratory, Tamale |
References
- O’Brien, K.L.; Wolfson, L.J.; Watt, J.P.; Henkle, E.; Deloria-Knoll, M.; McCall, N.; Lee, E.; Mulholland, K.; Levine, O.S.; Cherian, T.; et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: Global estimates. Lancet 2009, 374, 893–902. [Google Scholar] [CrossRef]
- 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 2000-15. Lancet Glob. Health 2018, 6, e744–e757. [Google Scholar] [CrossRef] [PubMed]
- Marquart, M.E. Pathogenicity and virulence of Streptococcus pneumoniae: Cutting to the chase on proteases. Virulence 2021, 12, 766–787. [Google Scholar] [CrossRef]
- World Health Organization. Pneumococcal conjugate vaccine for childhood immunization—WHO position paper. Wkly. Epidemiol. Rec. 2012, 87, 129–144. [Google Scholar]
- Geno, K.A.; Gilbert, G.L.; Song, J.Y.; Skovsted, I.C.; Klugman, K.P.; Jones, C.; Konradsen, H.B.; Nahm, M.H. Pneumococcal capsules and their types: Past, present, and future. Clin. Microbiol. Rev. 2015, 28, 871–899. [Google Scholar] [CrossRef] [PubMed]
- Daniels, C.C.; Rogers, P.D.; Shelton, C.M. A review of pneumococcal vaccines: Current polysaccharide vaccine recommendations and future protein antigens. J. Pediatr. Pharmacol. Ther. 2016, 21, 27–35. [Google Scholar] [CrossRef]
- Ganaie, F.; Saad, J.S.; McGee, L.; Van Tonder, A.J.; Bentley, S.D.; Lo, S.W.; A Gladstone, R.; Turner, P.; Keenan, J.D.; Breiman, R.F.; et al. A New Pneumococcal Capsule Type, 10D, is the 100th Serotype and Has a Large cps Fragment from an Oral Streptococcus. mBio 2020, 11, e00937-20. [Google Scholar] [CrossRef]
- Bogaert, D.; De Groot, R.; Hermans, P.W. Streptococcus pneumoniae colonisation: The key to pneumococcal disease. Lancet Infect. Dis. 2004, 4, 144–154. [Google Scholar] [CrossRef]
- Simell, B.; Auranen, K.; Käyhty, H.; Goldblatt, D.; Dagan, R.; O’Brien, K.L.; Pneumococcal Carriage Group. The fundamental link between pneumococcal carriage and disease. Expert Rev. Vaccines 2012, 11, 841–855. [Google Scholar] [CrossRef]
- Sleeman, K.L.; Griffiths, D.; Shackley, F.; Diggle, I.; Gupta, S.; Maiden, M.C.; Moxon, E.R.; Crook, D.W.; Peto, T.E.A. Capsular serotype-specific attack rates and duration of carriage of Streptococcus pneumoniae in a population of children. J. Infect. Dis. 2006, 194, 682–688. [Google Scholar] [CrossRef]
- Turner, P.; Hinds, J.; Turner, C.; Jankhot, A.; Gould, K.; Bentley, S.D.; Nosten, F.; Goldblatt, D. Improved detection of nasopharyngeal cocolonization by multiple pneumococcal serotypes by use of latex agglutination or molecular serotyping by microarray. J. Clin. Microbiol. 2011, 49, 1784–1789. [Google Scholar] [CrossRef]
- Usuf, E.; Bottomley, C.; Adegbola, R.A.; Hall, A. Pneumococcal Carriage in Sub-Saharan Africa—A Systematic Review. PLoS ONE 2014, 9, e85001. [Google Scholar] [CrossRef] [PubMed]
- Petraitienė, S.; Alasevičius, T.; Stacevičienė, I.; Vaičiūnienė, D.; Kačergius, T.; Usonis, V. The influence of Streptococcus pneumoniae nasopharyngeal colonization on the clinical outcome of respiratory tract infections in preschool children. BMC Infect. Dis. 2015, 15, 403. [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]
- Weinberger, D.M.; Malley, R.; Lipsitch, M. Serotype replacement in disease after pneumococcal vaccination. Lancet 2011, 378, 1962–1973. [Google Scholar] [CrossRef]
- van der Poll, T.; Opal, S.M. Pathogenesis, treatment, and prevention of pneumococcal pneumonia. Lancet 2009, 374, 1543–1556. [Google Scholar] [CrossRef]
- Pelton, S.I.; Weycker, D.; Farkouh, R.A.; Strutton, D.R.; Shea, K.M.; Edelsberg, J. Risk of pneumococcal disease in children with chronic medical conditions in the era of pneumococcal conjugate vaccine. Clin. Infect. Dis. 2014, 59, 615–623. [Google Scholar] [CrossRef]
- Weycker, D.; Farkouh, R.A.; Strutton, D.R.; Edelsberg, J.; Shea, K.M.; Pelton, S.I. Rates and costs of invasive pneumococcal disease and pneumonia in persons with underlying medical conditions. BMC Health Serv. Res. 2016, 16, 182. [Google Scholar] [CrossRef]
- Miller, M.L.; Gao, G.; Pestina, T.; Persons, D.; Tuomanen, E. Hypersusceptibility to invasive pneumococcal infection in experimental sickle cell disease involves platelet-activating factor receptor. J. Infect. Dis. 2007, 195, 581–584. [Google Scholar] [CrossRef] [PubMed]
- Cheong, D.; Song, J.Y. Pneumococcal disease burden in high-risk older adults: Exploring impact of comorbidities, long-term care facilities, antibiotic resistance, and immunization policies through a narrative literature review. Hum. Vaccines Immunother. 2024, 20, 2429235. [Google Scholar] [CrossRef] [PubMed]
- World Health Organization. Pneumococcal conjugate vaccines in infants and children under 5 years of age: WHO position paper. Wkly. Epidemiol. Rec. 2019, 94, 85–104. [Google Scholar]
- McGee, L.; McDougal, L.; Zhou, J.; Spratt, B.; Tenover, F.; George, R.; Hakenbeck, R.; Hryniewicz, W.; Lefévre, J.C.; Tomasz, A.; et al. Nomenclature of major antimicrobial-resistant clones of Streptococcus pneumoniae defined by the pneumococcal molecular epidemiology network. J. Clin. Microbiol. 2001, 39, 2565–2571. [Google Scholar] [CrossRef]
- Xu, X.; Cai, L.; Xiao, M.; Kong, F.; Oftadeh, S.; Zhou, F.; Gilbert, G.L. Distribution of serotypes, genotypes, and resistance determinants among macrolide resistant Streptococcus pneumoniae isolates. Antimicrob. Agents Chemother. 2010, 54, 1152–1159. [Google Scholar] [CrossRef]
- Weiser, J.N.; Ferreira, D.M.; Paton, J.C. Streptococcus pneumoniae: Transmission, colonization and invasion. Nat. Rev. Microbiol. 2018, 16, 355. [Google Scholar] [CrossRef] [PubMed]
- Cornick, J.; Bentley, S. Streptococcus pneumoniae: The evolution of antimicrobial resistance to beta-lactams, fluoroquinolones and macrolides. Microb. Infect. 2012, 14, 573–583. [Google Scholar] [CrossRef]
- Van Bambeke, F.; Reinert, R.R.; Appelbaum, P.C.; Tulkens, P.M. Multidrug-resistant Streptococcus pneumoniae infections: Current and future therapeutic options. Drugs 2007, 67, 2355–2382. [Google Scholar] [CrossRef]
- Mills, R.O.; Twum-Danso, K.; Owusu-Agyei, S.; Donkor, E.S. Epidemiology of pneumococcal carriage in children under five years of age in Accra, Ghana. Infect. Dis. 2015, 47, 326–331. [Google Scholar] [CrossRef]
- Pilishvili, T.; Lexau, C.; Farley, M.M.; Hadler, J.; Harrison, L.H.; Bennett, N.M.; Reingold, A.; Thomas, A.; Schaffner, W.; Craig, A.S.; et al. Sustained Reductions in Invasive Pneumococcal Disease in the Era of Conjugate Vaccine. J. Infect. Dis. 2010, 201, 32–41. [Google Scholar] [CrossRef]
- Waight, P.A.; Andrews, N.J.; Ladhani, S.N.; Sheppard, C.L.; Slack, M.P.; Miller, E. Effect of the 13-valent pneumococcal conjugate vaccine on invasive pneumococcal disease in England and Wales 4 years after its introduction: An observational cohort study. Lancet Infect. Dis. 2015, 15, 535–543. [Google Scholar] [CrossRef]
- Farrar, J.L.; Childs, L.; Ouattara, M.; Akhter, F.; Britton, A.; Pilishvili, T.; Kobayashi, M. Systematic Review and Meta-Analysis of the Efficacy and Effectiveness of Pneumococcal Vaccines in Adults. Pathogens 2023, 12, 732. [Google Scholar] [CrossRef] [PubMed]
- Hayford, K.; Tort, M.J.; Huang, L.; Forbes, C.; Pustulka, I.; Chapman, R.; Theilacker, C. Clinical effectiveness and impact of 13-valent pneumococcal conjugate vaccines in preventing invasive pneumococcal disease among children with risk conditions: A systematic literature review. Hum. Vaccines Immunother. 2026, 22, 2614133. [Google Scholar] [CrossRef] [PubMed]
- Amegah, J.K.; Danso, S.K.; Adjei, S. Is health expenditure on immunisation associated with immunisation coverage in sub-Saharan Africa? A multicountry analysis, 2013–2017. BMJ Open 2024, 14, e073789. [Google Scholar] [CrossRef]
- Dhaliwal, B.K.; Weeks, R.; Huber, J.; Fofana, A.; Bobe, M.; Mbailamen, A.D.; Legge, G.; Cisse, G.; Shet, A. Introduction of the pneumococcal conjugate vaccine in humanitarian and fragile contexts: Perspectives from stakeholders in four African countries. Hum. Vaccines Immunother. 2024, 20, 2314828. [Google Scholar] [CrossRef] [PubMed]
- Shiri, T.; Datta, S.; Madan, J.; Tsertsvadze, A.; Royle, P.; Keeling, M.J.; McCarthy, N.D.; Petrou, S. Indirect effects of childhood pneumococcal conjugate vaccination on invasive pneumococcal disease: A systematic review and meta-analysis. Lancet Glob. Health 2017, 5, e51–e59. [Google Scholar] [CrossRef]
- Tsaban, G.; Ben-Shimol, S. Indirect (herd) protection, following pneumococcal conjugated vaccines introduction: A systematic review of the literature. Vaccine 2017, 35, 2882–2891. [Google Scholar] [CrossRef]
- Bennett, J.C.; Knoll, M.D.; Kagucia, E.W.; Quesada, M.G.; Zeger, S.L.; Hetrich, M.K.; Yang, Y.; Herbert, C.; Ogyu, A.; Hanquet, G. Global impact of ten-valent and 13-valent pneumococcal conjugate vaccines on invasive pneumococcal disease in all ages (the PSERENADE project): A global surveillance analysis. Lancet Infect. Dis. 2024, 25, 457–470. [Google Scholar] [CrossRef]
- Gambia Pneumococcal Surveillance Group; Mackenzie, G.A.; Hill, P.C.; Jeffries, D.J.; Ndiaye, M.; Sahito, S.M.; Hossain, I.; Uchendu, U.; Ameh, D.; Adeyemi, O.; et al. Impact of the introduction of pneumococcal conjugate vaccination on invasive pneumococcal disease and pneumonia in The Gambia: 10 years of population-based surveillance. Lancet Infect. Dis. 2021, 21, 1293–1302. [Google Scholar] [CrossRef] [PubMed]
- Du, Q.-Q.; Shi, W.; Yu, D.; Yao, K.-H. Epidemiology of non-vaccine serotypes of Streptococcus pneumoniae before and after universal administration of pneumococcal conjugate vaccines. Hum. Vaccines Immunother. 2021, 17, 5628–5637. [Google Scholar] [CrossRef]
- King, L.M.; Andrejko, K.L.; Kobayashi, M.; Xing, W.; Cohen, A.L.; Self, W.H.; Resser, J.J.; Whitney, C.G.; Baughman, A.; Kio, M.; et al. Pneumococcal serotype distribution and coverage of existing and pipeline pneumococcal vaccines. J. Infect. Dis. 2025, 232, e609–e620. [Google Scholar] [CrossRef]
- Micoli, F.; Romano, M.R.; Carboni, F.; Adamo, R.; Berti, F. Strengths and weaknesses of pneumococcal conjugate vaccines. Glycoconj. J. 2023, 40, 135–148. [Google Scholar] [CrossRef]
- Donkor, E.S.; Dayie, N.T.; Badoe, E.V. Vaccination against pneumococcus in West Africa: Perspectives and prospects. Int. J. Gen. Med. 2013, 6, 757–764. [Google Scholar] [CrossRef] [PubMed]
- Dayie, N.T.; Arhin, R.E.; Newman, M.J.; Dalsgaard, A.; Bisgaard, M.; Frimodt-Møller, N.; Slotved, H.C. Penicillin resistance and serotype distribution of Streptococcus pneumoniae in Ghanaian children less than six years of age. BMC Infect. Dis. 2013, 13, 49. [Google Scholar] [CrossRef]
- Brueggemann, A.B.; Pai, R.; Crook, D.W.; Beall, B. Vaccine Escape Recombinants Emerge after Pneumococcal Vaccination in the United States. PLoS Pathog. 2007, 3, e168. [Google Scholar] [CrossRef] [PubMed]
- Wyres, K.L.; Lambertsen, L.M.; Croucher, N.J.; McGee, L.; von Gottberg, A.; Liñares, J.; Jacobs, M.R.; Kristinsson, K.G.; Beall, B.W.; Klugman, K.P.; et al. Pneumococcal Capsular Switching: A Historical Perspective. J. Infect. Dis. 2012, 207, 439–449. [Google Scholar] [CrossRef]
- Eldholm, V.; Osnes, M.N.; Bjørnstad, M.L.; Straume, D.; Gladstone, R.A. A genome-based survey of invasive pneumococci in Norway over four decades reveals lineage-specific responses to vaccination. Genome Med. 2024, 16, 123. [Google Scholar] [CrossRef]
- Kalizang’oma, A.; Swarthout, T.D.; Mwalukomo, T.S.; Kamng’ona, A.; Brown, C.; Msefula, J.; Demetriou, H.; Chan, J.M.; Roalfe, L.; Obolski, U.; et al. Clonal expansion of a Streptococcus pneumoniae serotype 3 capsule variant sequence type 700 with enhanced vaccine escape potential after 13-valent pneumococcal conjugate vaccine introduction. J. Infect. Dis. 2024, 230, e189–e198. [Google Scholar] [CrossRef]
- Miller, E.; Andrews, N.J.; Waight, P.A.; Slack, M.P.; George, R.C. Herd immunity and serotype replacement 4 years after seven-valent pneumococcal conjugate vaccination in England and Wales: An observational cohort study. Lancet Infect. Dis. 2011, 11, 760–768. [Google Scholar] [CrossRef]
- Feikin, D.R.; Kagucia, E.W.; Loo, J.D.; Link-Gelles, R.; Puhan, M.A.; Cherian, T.; Levine, O.S.; Whitney, C.G.; O’bRien, K.L.; Moore, M.R.; et al. Serotype-Specific Changes in Invasive Pneumococcal Disease after Pneumococcal Conjugate Vaccine Introduction: A Pooled Analysis of Multiple Surveillance Sites. PLoS Med. 2013, 10, e1001517. [Google Scholar] [CrossRef] [PubMed]
- Moore, M.R.; Link-Gelles, R.; Schaffner, W.; Lynfield, R.; Holtzman, C.; Harrison, L.H.; Zansky, S.M.; Baumbach, J.; Thomas, A.; Reingold, A.; et al. Effect of use of 13-valent pneumococcal conjugate vaccine in children on invasive pneumococcal disease in children and adults in the USA: Analysis of multisite, population-based surveillance. Lancet Infect. Dis. 2015, 15, 301–309. [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]
- Ladhani, S.N.; Collins, S.; Djennad, A.; Sheppard, C.L.; Borrow, R.; Fry, N.K.; Andrews, N.J.; Ramsay, M.E. Rapid increase in non-vaccine serotypes causing invasive pneumococcal disease in England and Wales, 2000–2017: A prospective national observational cohort study. Lancet Infect. Dis. 2018, 18, 441–451. [Google Scholar] [CrossRef]
- Hanquet, G.; Krizova, P.; Dalby, T.; Ladhani, S.N.; Nuorti, J.P.; Danis, K.; Mereckiene, J.; Knol, M.J.; Winje, B.A.; Ciruela, P.; et al. Serotype Replacement after Introduction of 10-Valent and 13-Valent Pneumococcal Conjugate Vaccines in 10 Countries, Europe. Emerg. Infect. Dis. 2022, 28, 137–138. [Google Scholar] [CrossRef]
- Russomando, G.; Fariña, N.; Amour, S.; Grau, L.; Guillen, R.; Abente, S.; Aldama, M.; Hahn, I.; Castro, H.; Messaoudi, M.; et al. Streptococcus pneumoniae carriage, antimicrobial resistance, and serotype distribution in children and adults from Paraguay in the post-vaccinal era. Front. Public Health 2025, 13, 1584857. [Google Scholar] [CrossRef]
- WHO African Region, Ghana. Geneva: World Health Organization. 2013. Available online: http://www.who.int/countries/gha/en/ (accessed on 17 April 2025).
- Ohene-Frempong, K.; Oduro, J.; Tetteh, H.; Nkrumah, F. Screening newborns for sickle cell disease in Ghana. Pediatrics 2008, 121, S120–S121. [Google Scholar] [CrossRef]
- Satzke, C.; Turner, P.; Virolainen-Julkunen, A.; Adrian, P.V.; Antonio, M.; Hare, K.M.; Henao-Restrepo, A.M.; Leach, A.J.; Klugman, K.P.; Porter, B.D.; et al. Standard method for detecting upper respiratory carriage of Streptococcus pneumoniae: Updated recommendations from the World Health Organization Pneumococcal Carriage Working Group. Vaccine 2014, 32, 165–179. [Google Scholar] [CrossRef] [PubMed]
- Dayie, N.T.; Tettey, E.Y.; Newman, M.J.; Bannerman, E.; Donkor, E.S.; Labi, A.K.; Slotved, H.C. Pneumococcal carriage among children under five in Accra, Ghana, five years after the introduction of pneumococcal conjugate vaccine. BMC Pediatr. 2019, 19, 316. [Google Scholar] [CrossRef] [PubMed]
- Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing, 33rd ed.; CLSI supplement M100; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2023. [Google Scholar]
- Donkor, E.S.; Newman, M.J.; Oliver-Commey, J.; Bannerman, E.; Dayie, N.T.K.D.; Badoe, E.V. Invasive disease and paediatric carriage of Streptococcus pneumoniae in Ghana. Scand. J. Infect. Dis. 2010, 42, 254–259. [Google Scholar] [CrossRef]
- Dayie, N.T.K.D.; Arhin, R.E.; Newman, M.J.; Dalsgaard, A.; Bisgaard, M.; Frimodt-Møller, N.; Slotved, H.C. Multidrug-resistant Streptococcus pneumoniae isolates from healthy Ghanaian preschool children. Microb. Drug Resist. 2015, 21, 636–642. [Google Scholar] [CrossRef]
- Kwambana-Adams, B.A.; Asiedu-Bekoe, F.; Sarkodie, B.; Afreh, O.K.; Kuma, G.K.; Owusu-Okyere, G.; Foster- Nyarko, E.; Ohene, S.A.; Okot, C.; Worwui, A.K.; et al. An outbreak of pneumococcal meningitis among older children (≥5 years) and adults after the implementation of an infant vaccination programme with the 13-valent pneumococcal conjugate vaccine in Ghana. BMC Infect. Dis. 2016, 16, 575. [Google Scholar] [CrossRef] [PubMed]
- Donkor, E.S.; Annan, J.A.; Badoe, E.V.; Dayie, N.T.K.D.; Labi, A.K.; Slotved, H.C. Pneumococcal carriage among HIV infected children in Accra, Ghana. BMC Infect. Dis. 2017, 17, 133. [Google Scholar] [CrossRef]
- Dayie, N.T.K.D.; Tetteh-Ocloo, G.; Labi, A.K.; Olayemi, E.; Slotved, H.C.; Lartey, M.; Donkor, E.S. Pneumococcal carriage among sickle cell disease patients in Accra, Ghana: Risk factors, serotypes and antibiotic resistance. PLoS ONE 2018, 13, e0206728. [Google Scholar] [CrossRef] [PubMed]
- Letsa, T.; Noora, C.L.; Kuma, G.K.; Asiedu, E.; Kye-Duodu, G.; Afari, E.; Kuffour, O.A.; Opare, J.; Nyarko, K.M.; Ameme, D.K.; et al. Pneumococcal meningitis outbreak and associated factors in six districts of Brong Ahafo region, Ghana, 2016. BMC Public Health 2018, 18, 781. [Google Scholar] [CrossRef]
- Dayie, N.T.; Baffuor-Asare, M.; Labi, A.K.; Obeng-Nkrumah, N.; Olayemi, E.; Lartey, M.; Slotved, H.-C.; Donkor, E.S. Epidemiology of pneumococcal carriage among HIV-infected individuals in the conjugate vaccine era: A study in southern Ghana. Biomed. Res. Int. 2019, 2019, 3427174. [Google Scholar] [CrossRef]
- Mills, R.O.; Abdullah, M.R.; Akwetey, S.A.; Sappor, D.C.; Cole, I.; Baffuor-Asare, M.; Bolivar, J.A.; Gámez, G.; van der Linden, M.P.G.; Hammerschmidt, S. Post-Vaccination Streptococcus pneumoniae Carriage and Virulence Gene Distribution among Children Less Than Five Years of Age, Cape Coast, Ghana. Microorganisms 2020, 8, 1987. [Google Scholar] [CrossRef]
- Leimkugel, J.; Adams Forgor, A.; Gagneux, S.; Pflüger, V.; Flierl, C.; Awine, E.; Naegeli, M.; Dangy, J.P.; Smith, T.; Hodgson, A.; et al. An outbreak of serotype 1 Streptococcus pneumoniae meningitis in northern Ghana with features that are characteristic of Neisseria meningitidis meningitis epidemics. J. Infect. Dis. 2005, 192, 192–199. [Google Scholar] [CrossRef] [PubMed]
- Aku, F.Y.; Lessa, F.C.; Asiedu-Bekoe, F.; Balagumyetime, P.; Ofosu, W.; Farrar, J.; Ouattara, M.; Vuong, J.T.; Issah, K.; Opare, J.; et al. Meningitis outbreak caused by vaccine-preventable bacterial pathogens—Northern Ghana, 2016. MMWR Morb. Mortal. Wkly. Rep. 2017, 66, 806–810. [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]
- Jochems, S.P.; Weiser, J.N.; Malley, R.; Ferreira, D.M. The immunological mechanisms that control pneumococcal carriage. PLoS Pathog. 2017, 13, e1006665. [Google Scholar] [CrossRef] [PubMed]
- Bozio, C.H.; Abdul-Karim, A.; Abenyeri, J.; Abubakari, B.; Ofosu, W.; Zoya, J.; Ouattara, M.; Srinivasan, V.; Vuong, J.T.; Opare, D.; et al. Continued occurrence of serotype 1 pneumococcal meningitis in two regions located in the meningitis belt in Ghana five years after introduction of 13-valent pneumococcal conjugate vaccine. PLoS ONE 2018, 13, e0203205. [Google Scholar] [CrossRef]
- Loo, J.D.; Conklin, L.; Fleming-Dutra, K.E.; Knoll, M.D.; Park, D.E.; Kirk, J.; Goldblatt, D.; O’Brien, K.L.; Whitney, C.G. Systematic review of the indirect effect of pneumococcal conjugate vaccine dosing schedules on pneumococcal disease and colonization. Pediatr. Infect. Dis. J. 2014, 33, S161–S171. [Google Scholar] [CrossRef]
- Løvlie, A.; Vestrheim, D.F.; Aaberge, I.S.; Steens, A. Changes in pneumococcal carriage prevalence and factors associated with carriage in Norwegian children, four years after introduction of PCV13. BMC Infect. Dis. 2020, 20, 29. [Google Scholar] [CrossRef]
- Cooper, L.V.; Stuart, J.M.; Okot, C.; Asiedu-Bekoe, F.; Afreh, O.K.; Fernandez, K.; Ronveaux, O.; Trotter, C.L. Reactive vaccination as a control strategy for pneumococcal meningitis outbreaks in the African meningitis belt: Analysis of outbreak data from Ghana. Vaccine 2019, 37, 5657–5663. [Google Scholar] [CrossRef]
- Dobay, O. The complexity of serotype replacement of pneumococci. Hum. Vaccines Immunother. 2019, 15, 2725–2728. [Google Scholar] [CrossRef]
- Steinberg, M.H. Pneumococcus and sickle cell disease: The beginning of the end? Clin. Infect. Dis. 2007, 44, 1434–1435. [Google Scholar] [CrossRef] [PubMed]
- Moïsi, J.C.; Makawa, M.S.; Tall, H.; Agbenoko, K.; Njanpop-Lafourcade, B.M.; Tamekloe, S.; Amidou, M.; Mueller, J.E.; Gessner, B.D. Burden of pneumococcal disease in northern Togo before the introduction of pneumococcal conjugate vaccine. PLoS ONE 2017, 12, e0170412. [Google Scholar] [CrossRef]
- Abbey, M.; Afagbedzi, S.K.; Afriyie-Mensah, J.; Antwi-Agyei, D.; Atengble, K.; Badoe, E.; Batchelor, J.; Donkor, E.S.; Esena, R.; Goka, B.Q.; et al. Pneumonia in Ghana-a need to raise the profile. Int. Health 2018, 10, 4–7. [Google Scholar] [CrossRef] [PubMed]
- Kwambana-Adams, B.A.; Liu, J.; Okoi, C.; Mwenda, J.M.; Mohammed, N.I.; Tsolenyanu, E.; Renner, L.A.; Ansong, D.; Tagbo, B.N.; Bashir, M.F.; et al. Etiology of Pediatric Meningitis in West Africa Using Molecular Methods in the Era of Conjugate Vaccines against Pneumococcus, Meningococcus, and Haemophilus influenzae Type b. Am. J. Trop. Med. Hyg. 2020, 103, 696–703. [Google Scholar] [CrossRef]
- Voysey, M.; Fanshawe, T.R.; Kelly, D.F.; O’brien, K.L.; Kandasamy, R.; Shrestha, S.; Thorson, S.; Hinds, J.; Pollard, A.J. Serotype-Specific Correlates of Protection for Pneumococcal Carriage: An Analysis of Immunity in 19 Countries. Clin. Infect. Dis. 2017, 66, 913–920. [Google Scholar] [CrossRef]
- Swarthout, T.D.; Henrion, M.Y.R.; Thindwa, D.; Meiring, J.E.; Mbewe, M.; Kalizang’Oma, A.; Brown, C.; Msefula, J.; Moyo, B.; Mataya, A.A.; et al. Waning of antibody levels induced by a 13-valent pneumococcal conjugate vaccine, using a 3 + 0 schedule, within the first year of life among children younger than 5 years in Blantyre, Malawi: An observational, population-level, serosurveillance study. Lancet Infect. Dis. 2022, 22, 1737–1747. [Google Scholar] [CrossRef] [PubMed]
- von Specht, M.; Gabarrot, G.G.; Mollerach, M.; Bonofiglio, L.; Gagetti, P.; Kaufman, S.; Vigliarolo, L.; Toresani, I.; Lopardo, H.A. Resistance to β-lactams in Streptococcus pneumoniae. Rev. Argent. Microbiol. 2021, 53, 266–271. [Google Scholar] [CrossRef]
- Ktari, S.; Ben Ayed, N.; Ben Rbeh, I.; Garbi, N.; Maalej, S.; Mnif, B.; Rhimi, F.; Hammami, A. Antibiotic resistance pattern, capsular types, and molecular characterization of invasive isolates of Streptococcus pneumoniae in the south of Tunisia from 2012 to 2018. BMC Microbiol. 2023, 23, 36. [Google Scholar] [CrossRef]
- Kulkarni, N.; Routray, A.; Taur, S. A Multicenter Evaluation of Overall Susceptibility and Antimicrobial Resistance Among Streptococcus pneumoniae Isolates. Cureus 2023, 15, e41984. [Google Scholar] [CrossRef] [PubMed]
- Bidell, M.R.; Pai, M.A.P.; Lodise, T.P. Use of Oral Tetracyclines in the Treatment of Adult Patients with Community-Acquired Bacterial Pneumonia: A Literature Review on the Often-Overlooked Antibiotic Class. Antibiotics 2020, 9, 905. [Google Scholar] [CrossRef]
- Liu, L.; Wang, Y.; Ge, L.; Hu, D.; Xiang, X.; Fu, Y.; Lu, J.; Li, X.; Yu, Y.; Tu, Y.; et al. Integrated genomic analysis of antibiotic resistance and virulence determinants in invasive strains of Streptococcus pneumoniae. Front. Cell. Infect. Microbiol. 2023, 13, 1238693. [Google Scholar] [CrossRef]
- Dharmapalan, D.; Bielicki, J.; Sharland, M. Harmonization of amoxicillin dose, duration, and formulation for acute childhood respiratory infections. Antibiotics 2023, 12, 1138. [Google Scholar] [CrossRef]
- Adetifa, I.M.O.; Adamu, A.L.; Karani, A.; Waithaka, M.; Odeyemi, K.A.; Okoromah, C.A.N.; Bello, M.M.; Abubakar, I.S.; Inem, V.; Scott, J.A.G. Nasopharyngeal pneumococcal carriage in Nigeria: A two-site, population-based survey. Sci. Rep. 2018, 8, 3509. [Google Scholar] [CrossRef]
- Centers for Disease Control and Prevention. Active Bacterial Core Surveillance (ABCs) Report, Emerging Infections Program Network, Streptococcus Pneumoniae. 2019. Available online: https://www.cdc.gov/abcs/downloads/SPN_Surveillance_Report_2019.pdf (accessed on 17 April 2025).
- Yevutsey, S.K.; Buabeng, K.O.; Aikins, M.; Anto, B.P.; Biritwum, R.B.; Frimodt-Møller, N.; Gyansa-Lutterodt, M. Situational analysis of antibiotic use and resistance in Ghana: Policy and regulation. BMC Public Health 2017, 17, 896. [Google Scholar] [CrossRef]
- Cottagnoud, P.; Gerber, C.M.; Cottagnoud, M.; Täuber, M.G. Gentamicin increases the efficacy of vancomycin against penicillin-resistant pneumococci in the rabbit meningitis model. Antimicrob. Agents Chemother. 2002, 46, 188–190. [Google Scholar] [CrossRef]
- Beek, D.V.D.; Brouwer, M.C.; Thwaites, G.E.; Tunkel, A.R. Advances in treatment of bacterial meningitis. Lancet 2012, 380, 1693–1702. [Google Scholar] [CrossRef]
- Arhin, R.E.; Donkor, E.S.; Slotved, H.C.; Kotey, F.C.N.; Dayie, N.T.K.D. Etiologic profile of the Pneumococcus in Ghana: A systematic review. BioMed Res. Int. 2024, 2024, 8368996. [Google Scholar] [CrossRef] [PubMed]
- Donkor, E.S.; Odoom, A.; Osman, A.-H.; Darkwah, S.; Kotey, F.C.N. A Systematic Review on Antimicrobial Resistance in Ghana from a One Health Perspective. Antibiotics 2024, 13, 662. [Google Scholar] [CrossRef] [PubMed]

| Feature | Number | % | |
|---|---|---|---|
| Age groups (years) | <1 | 53 | 0.36 |
| 1–5 | 1959 | 13.42 | |
| 6–10 | 1342 | 9.19 | |
| 11–20 | 4175 | 28.60 | |
| 21–30 | 3433 | 23.52 | |
| 31–40 | 1097 | 7.52 | |
| 41–50 | 1155 | 7.91 | |
| 51–60 | 1087 | 7.45 | |
| >60 | 296 | 2.03 | |
| Sex | Male | 7259 | 49.70 |
| Female | 7338 | 50.30 | |
| Region | Greater Accra | 11,818 | 80.96 |
| Eastern | 938 | 6.43 | |
| Volta | 946 | 6.48 | |
| Northern | 895 | 6.13 | |
| Study site | GARH | 2180 | 14.93 |
| KBTH | 3742 | 25.64 | |
| 37 MH | 181 | 1.24 | |
| PML | 5715 | 39.15 | |
| HRH | 946 | 6.48 | |
| ERH | 938 | 6.43 | |
| ZPHRLT | 895 | 6.13 | |
| Features | Frequency of Pneumococci (n = 97) | |
|---|---|---|
| Vaccine Serotypes n (%) | Non-Vaccine Serotypes n (%) | |
| Age groups ** | ||
| <1 year (n = 0) | 0 (0.00%) | 0 (0.00%) |
| 1 to 5 years (n = 1) | 1 (100.00%) | 0 (0.00%) |
| 6 to 10 years (n = 6) | 4 (66.67%) | 2 (33.33%) |
| 11 to 20 years (n = 55) | 48 (87.27%) | 7 (12.73%) |
| 21 to 30 years (n = 5) | 5 (100.00%) | 0 (0.00%) |
| 31 to 40 years (n = 16) | 9 (56.25%) | 7 (43.75%) |
| 41 to 50 years (n = 8) | 6 (75.00%) | 2 (25.00%) |
| 51 to 60 years (n = 1) | 1 (100.00%) | 0 (0.00%) |
| >60 years (n = 5) | 5 (100.00%) | 0 (0.00%) |
| Gender ** | ||
| Male (n = 55) | 48 (87.27%) | 7 (12.73%) |
| Female (n = 42) | 39 (92.86%) | 3 (7.14%) |
| Serotype | No. | % | 95% CI (%) | Vaccines Within Which the Serotypes Are Captured |
|---|---|---|---|---|
| 1 | 57 | 58.76 | 48.82–68.19 | PCVs 10, 13, 15, 20, and PPV 23 |
| 8 | 1 | 1.03 | 0.002–0.056 | PCV 20, PPV 23 |
| 10A | 1 | 1.03 | 0.002–0.056 | PCV 20, PPV 23 |
| 12F | 8 | 8.24 | 0.042–0.155 | PCV 20, PPV 23 |
| 14 | 1 | 1.03 | 0.002–0.056 | PCVs 10, 13, 15, 20, and PPV 23 |
| 20 | 2 | 2.06 | 0.006–0.071 | PPV 23 |
| 23A | 3 | 3.09 | 0.011–0.086 | – |
| 23B | 11 | 11.34 | 0.065–0.192 | – |
| 33F | 9 | 9.28 | 0.050–0.167 | PCVs 15 and 20, PPV 23 |
| 38 | 4 | 4.12 | 0.016–0.101 | – |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2026 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license.
Share and Cite
Kotey, F.C.N.; Arhin, R.E.; Dayie, N.T.K.D.; Ampah, E.O.; Abdul-Karim, A.; Baah, D.A.; Afful, R.M.; Tetteh-Ocloo, G.; Kom-Zuta, R.T.; Tetteh, F.K.M.; et al. Post-Vaccination Surveillance of Invasive Pneumococcal Disease in Ghana. Diseases 2026, 14, 162. https://doi.org/10.3390/diseases14050162
Kotey FCN, Arhin RE, Dayie NTKD, Ampah EO, Abdul-Karim A, Baah DA, Afful RM, Tetteh-Ocloo G, Kom-Zuta RT, Tetteh FKM, et al. Post-Vaccination Surveillance of Invasive Pneumococcal Disease in Ghana. Diseases. 2026; 14(5):162. https://doi.org/10.3390/diseases14050162
Chicago/Turabian StyleKotey, Fleischer C. N., Reuben E. Arhin, Nicholas T. K. D. Dayie, Emmanuel O. Ampah, Abass Abdul-Karim, Deric A. Baah, Ruth M. Afful, Georgina Tetteh-Ocloo, Roland T. Kom-Zuta, Francis K. M. Tetteh, and et al. 2026. "Post-Vaccination Surveillance of Invasive Pneumococcal Disease in Ghana" Diseases 14, no. 5: 162. https://doi.org/10.3390/diseases14050162
APA StyleKotey, F. C. N., Arhin, R. E., Dayie, N. T. K. D., Ampah, E. O., Abdul-Karim, A., Baah, D. A., Afful, R. M., Tetteh-Ocloo, G., Kom-Zuta, R. T., Tetteh, F. K. M., Osei, M.-M., Brew, Y. N. A., Nyarko, M. Y., Asafo-Adjei, K., Tetteh-Quarcoo, P. B., Tette, E. M. A., & Donkor, E. S. (2026). Post-Vaccination Surveillance of Invasive Pneumococcal Disease in Ghana. Diseases, 14(5), 162. https://doi.org/10.3390/diseases14050162

