2,050
Views
1
CrossRef citations to date
0
Altmetric
Review

Vaccine strategies to reduce the burden of pneumococcal disease in HIV-infected adults in Africa.

ORCID Icon, , , , &
Pages 1085-1092 | Received 13 Jul 2020, Accepted 26 Oct 2020, Published online: 03 Dec 2020

References

  • O’Brien KL, Wolfson LJ, Watt JP, et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet. 2009;374:893–902.
  • Wahl B, O’Brien KL, Greenbaum A, 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:e744–57.
  • van Aalst M, Lötsch F, Spijker R, et al. Incidence of invasive pneumococcal disease in immunocompromised patients: a systematic review and meta-analysis. Travel Med Infect Dis. 2018;24:89–100.
  • Corcoran M, Vickers I, Mereckiene J, 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.
  • Meiring S, Cohen C, Quan V, et al. HIV infection and the epidemiology of invasive pneumococcal disease (IPD) in South African adults and older children prior to the introduction of a pneumococcal conjugate vaccine (PCV). Plos One. 2016;11:e0149104.
  • Vardanjani HM, Borna H, Ahmadi A. Effectiveness of pneumococcal conjugate vaccination against invasive pneumococcal disease among children with and those without HIV infection: a systematic review and meta-analysis. BMC Infect Dis. 2019;19:685.
  • Cohen C, von Mollendorf C, de Gouveia L, et al. Effectiveness of 7-valent pneumococcal conjugate vaccine against invasive pneumococcal disease in HIV-infected and -uninfected children in South Africa: a matched case-control study. Clin Infect Dis. 2014;59:808–818.
  • Cohen C, von Mollendorf C, de Gouveia L, et al. Effectiveness of the 13-valent pneumococcal conjugate vaccine against invasive pneumococcal disease in South African children:a case-control study. Lancet Glob Health. 2017;5:e359–69.
  • von Gottberg A, de Gouveia L, Tempia S, et al. Effects of vaccination on invasive pneumococcal disease in South Africa. N Engl J Med. 2014;371:1889–1899.
  • Klugman KP, Madhi SA, Huebner RE, et al. Trial of a 9-valent pneumococcal conjugate vaccine in children with and those without HIV infection. N Engl J Med. 2003;349:1341–1348.
  • Whitney CG, Farley MM, Hadler J, et al. Decline in invasive pneumococcal disease after the introduction of protein–polysaccharide conjugate vaccine. N Engl J Med. 2003;348:1737–1746.
  • Hammitt LL, Etyang AO, Morpeth SC, et al. Effect of ten-valent pneumococcal conjugate vaccine on invasive pneumococcal disease and nasopharyngeal carriage in Kenya: a longitudinal surveillance study. Lancet. 2019;393:2146–2154.
  • Ngocho JS, Magoma B, Olomi GA, et al. Effectiveness of pneumococcal conjugate vaccines against invasive pneumococcal disease among children under five years of age in Africa: a systematic review. Plos One. 2019;14:e0212295.
  • Loughlin AM, Hsu K, Silverio AL, et al. Direct and indirect effects of PCV13 on nasopharyngeal carriage of PCV13 unique pneumococcal serotypes in massachusetts’ children. Pediatr Infect Dis J. 2014;33:504.
  • Southern J, Andrews N, Sandu P, et al. Pneumococcal carriage in children and their household contacts six years after introduction of the 13-valent pneumococcal conjugate vaccine in England. Plos One. 2018;13:e0195799.
  • Heinsbroek E, Tafatatha T, Phiri A, et al. Pneumococcal carriage in households in Karonga District, Malawi, before and after introduction of 13-valent pneumococcal conjugate vaccination. Vaccine. 2018;36:7369–7376.
  • Ojal J, Flasche S, Hammitt LL, et al. Sustained reduction in vaccine-type invasive pneumococcal disease despite waning effects of a catch-up campaign in Kilifi, Kenya: a mathematical model based on pre-vaccination data. Vaccine. 2017;35:4561–4568.
  • Lourenço J, Obolski U, Swarthout TD, et al. Determinants of high residual post-PCV13 pneumococcal vaccine-type carriage in Blantyre, Malawi: a modelling study. BMC Med. 2019;17. DOI:10.1186/s12916-019-1450-2..
  • Sigaúque B, Moiane B, Massora S, et al. Early declines in vaccine type pneumococcal carriage in children less than 5 years old after introduction of 10-valent pneumococcal conjugate vaccine in mozambique. Pediatr Infect Dis J. 2018;37:1054.
  • Swarthout TD, Fronterre C, Lourenço J, et al. *High residual carriage of vaccine-serotype Streptococcus pneumoniae after introduction of pneumococcal conjugate vaccine in Malawi. Nat Commun. 2020;11:2222.
  • Aston SJ, Ho A, Jary H, et al. Etiology and risk factors for mortality in an adult community-acquired Pneumonia Cohort in Malawi. Am J Respir Crit Care Med. 2019;200:359–369.
  • Feikin DR, Jagero G, Aura B, et al. High rate of pneumococcal bacteremia in a prospective cohort of older children and adults in an area of high HIV prevalence in rural western Kenya. BMC Infect Dis. 2010;10:186.
  • Cordonnier C, Averbuch D, Maury S, et al. Pneumococcal immunization in immunocompromised hosts: where do we stand? Expert Rev Vaccines. 2014;13:59–74.
  • Madhi SA, Nunes MC. The potential impact of pneumococcal conjugate vaccine in Africa: considerations and early lessons learned from the South African experience. Hum Vaccin Immunother. 2016;12:314–325.
  • Nunes MC, Madhi SA. Safety, immunogenicity and efficacy of pneumococcal conjugate vaccine in HIV-infected individuals. Hum Vaccin Immunother. 2012;8:161–173.
  • Glennie SJ, Sepako E, Mzinza D, et al. Impaired CD4 T cell memory response to Streptococcus pneumoniae precedes CD4 T cell depletion in HIV-infected Malawian adults. PLoS ONE. 2011;6:e25610.
  • Zhang L, Li Z, Wan Z, et al. Humoral immune responses to Streptococcus pneumoniae in the setting of HIV-1 infection. Vaccine. 2015;33:4430–4436.
  • Kerr AR, Paterson GK, Riboldi-Tunnicliffe A, et al. Innate immune defense against pneumococcal pneumonia requires pulmonary complement component C3. Infect Immun. 2005;73:4245–4252.
  • Jochems SP, Weiser JN, Malley R, et al. The immunological mechanisms that control pneumococcal carriage. PLoS Pathog. 2017;13:e1006665.
  • Iwajomo OH, Finn A, Moons P, et al. Deteriorating pneumococcal-specific B-cell memory in minimally symptomatic African children with HIV infection. J Infect Dis. 2011;204:534–543.
  • Picard C, Puel A, Bustamante J, et al. Primary immunodeficiencies associated with pneumococcal disease. Curr Opin Allergy Clin Immunol. 2003;3:451–459.
  • Iwajomo OH, Finn A, Ogunniyi AD, et al. Impairment of pneumococcal antigen specific isotype-switched igg memory B-cell immunity in HIV infected Malawian adults. Plos One. 2013;8:e78592.
  • Eley B. Immunization in patients with HIV infection. Drugs. 2008;68:1473–1481.
  • Glennie SJ, Banda D, Gould K, et al. Defective pneumococcal-specific Th1 responses in HIV-infected adults precedes a loss of control of pneumococcal colonization. Clin Infect Dis. 2013;56:291–299.
  • De Milito A, Mörch C, Sönnerborg A, et al. Loss of memory (CD27) B lymphocytes in HIV-1 infection. AIDS. 2001;15:957.
  • Madhi SA, Kuwanda L, Cutland C, et al. Quantitative and Qualitative Antibody Response to Pneumococcal Conjugate Vaccine Among African Human Immunodeficiency Virus-Infected and Uninfected Children. Pediatr Infect Dis J. 2005;24:410.
  • Jones N, Huebner R, Khoosal M, et al. The impact of HIV on Streptococcus pneumoniae bacteraemia in a South African population. AIDS. 1998;12:2177.
  • Madhi SA, Madhi A, Petersen K, et al. Impact of human immunodeficiency virus type 1 infection on the epidemiology and outcome of bacterial Meningitis in South African children. Inter J Infect Dis. 2001;5:119–125.
  • McEllistrem MC, Mendelsohn AB, Pass MA, et al. Recurrent invasive pneumococcal disease in individuals with human immunodeficiency virus infection. J Infect Dis. 2002;185:1364–1368.
  • Everett DB, Mukaka M, Denis B, et al. Ten years of surveillance for invasive streptococcus pneumoniae during the era of antiretroviral scale-up and cotrimoxazole prophylaxis in Malawi. Plos One. 2011;6:e17765.
  • Heffernan RT, Barrett NL, Gallagher KM, et al. Declining incidence of invasive streptococcus pneumoniae infections among persons with AIDS in an era of highly active antiretroviral therapy, 1995—2000. J Infect Dis. 2005;191:2038–2045.
  • Bar-Zeev N, Mtunthama N, Gordon SB, et al. Minimum incidence of adult invasive pneumococcal disease in Blantyre, Malawi an Urban African setting: a hospital based prospective cohort study. Plos One. 2015;10:e0128738.
  • Bigogo GM, Audi A, Auko J, et al. Indirect effects of 10-valent pneumococcal conjugate vaccine against adult pneumococcal pneumonia in rural Western Kenya. Clin Infect Dis. 2019;69:2177–2184.
  • Nzenze SA, Madhi SA, Shiri T, et al. Imputing the direct and indirect effectiveness of childhood pneumococcal conjugate vaccine against invasive pneumococcal disease by surveying temporal changes in nasopharyngeal pneumococcal colonization. Am J Epidemiol. 2017;186:435–444.
  • Dwyer-Lindgren L, Cork MA, Sligar A, et al. *Mapping HIV prevalence in sub-Saharan Africa between 2000 and 2017. Nature. 2019;570:189.
  • Klugman KP, Rodgers GL. *Population versus individual protection by pneumococcal conjugate vaccination. Lancet. 2019;393:2102–2104.
  • Kuhn L, Goga AE. Moving towards elimination: findings from the South Africa prevention of mother to child transmission evaluation (SAPMTCTE). BMC Infect Dis. 2019;19:782.
  • van Lettow M, Landes M, van Oosterhout J, et al. Prevention of mother-to-child transmission of HIV: a cross-sectional study in Malawi. Bull World Health Organ. 2018;96:256–265.
  • Harries AD, Ford N, Jahn A, et al. Act local, think global: how the Malawi experience of scaling up antiretroviral treatment has informed global policy. BMC Public Health. 2016;16:938.
  • Jahn A, Harries AD, Schouten EJ, et al. Scaling-up antiretroviral therapy in Malawi. Bull World Health Organ. 2016;94:772–776.
  • Mirsaeidi M, Schraufnagel DE. Pneumococcal vaccines: understanding centers for disease control and prevention recommendations. Ann ATS. 2014;11:980–985.
  • Bonnave C, Mertens D, Peetermans W, et al. *Adult vaccination for pneumococcal disease: a comparison of the national guidelines in Europe. Eur J Clin Microbiol Infect Dis. 2019;38:785–791.
  • Ho Y-L, Brandão AP, de Cunto Brandileone MC, et al. Immunogenicity and safety of pneumococcal conjugate polysaccharide and free polysaccharide vaccines alone or combined in HIV-infected adults in Brazil. Vaccine. 2013;31:4047–4053.
  • Lombardi F, Belmonti S, Fabbiani M, et al. Immunogenicity and safety of the 13-valent pneumococcal conjugate vaccine versus the 23-valent polysaccharide vaccine in unvaccinated HIV-infected adults: a pilot, prospective controlled study. Plos One. 2016;11:e0156523.
  • Lu C-L, Hung -C-C, Chuang Y-C, et al. Serologic response to primary vaccination with 7-valent pneumococcal conjugate vaccine is better than with 23-valent pneumococcal polysaccharide vaccine in HIV-infected patients in the era of combination antiretroviral therapy. Hum Vaccin Immunother. 2013;9:398–404.
  • Lesprit P, Pédrono G, Molina J-M, et al. Immunological efficacy of a prime-boost pneumococcal vaccination in HIV-infected adults. AIDS. 2007;21:2425.
  • Feikin DR, Elie CM, Goetz MB, et al. Randomized trial of the quantitative and functional antibody responses to a 7-valent pneumococcal conjugate vaccine and/or 23-valent polysaccharide vaccine among HIV-infected adults. Vaccine. 2001;20:545–553.
  • Søgaard OS, Lohse N, Harboe ZB, et al. Improving the immunogenicity of pneumococcal conjugate vaccine in HIV-infected adults with a toll-like receptor 9 agonist adjuvant: a randomized, controlled trial. Clin Infect Dis. 2010;51:42–50.
  • Peñaranda M, Payeras A, Cambra A, et al. Group the MPS. Conjugate and polysaccharide pneumococcal vaccines do not improve initial response of the polysaccharide vaccine in HIV-infected adults. AIDS. 2010;24:1226.
  • Pedersen RH, Lohse N, Østergaard L, et al. The effectiveness of pneumococcal polysaccharide vaccination in HIV-infected adults: a systematic review. HIV Med. 2011;12:323–333.
  • French N, Nakiyingi J, Carpenter LM, et al. 23–valent pneumococcal polysaccharide vaccine in HIV-1-infected Ugandan adults: double-blind, randomised and placebo controlled trial. Lancet. 2000;355:2106–2111.
  • López‐Palomo C, Martín‐Zamorano M, Benítez E, et al. Pneumonia in HIV-infected patients in the HAART era: incidence, risk, and impact of the pneumococcal vaccination. J Med Virol. 2004;72:517–524.
  • Watera C, Nakiyingi J, Miiro G, et al. 23-Valent pneumococcal polysaccharide vaccine in HIV-infected Ugandan adults: 6-year follow-up of a clinical trial cohort. AIDS. 2004;18:1210–1213.
  • Dworkin MS, Ward JW, Hanson DL, et al. Pneumococcal disease among human immunodeficiency virus-infected persons: incidence, risk factors, and impact of vaccination. Clin Infect Dis. 2001;32:794–800.
  • French N, Gordon SB, Mwalukomo T, et al. *A trial of a 7-valent pneumococcal conjugate vaccine in HIV-infected adults. N Engl J Med. 2010;362:812–822.
  • Bonten MJM, Huijts SM, Bolkenbaas M, et al. Polysaccharide conjugate vaccine against pneumococcal pneumonia in adults. N Engl J Med. 2015;372:1114–1125.
  • WHO. Pneumococcus vaccines position paper. World Health Organisation, Switzerland; 2019.
  • Madhi SA, Moreira M, Koen A, et al. Impact of HIV status and vaccination schedule on bacterial nasopharyngeal carriage following infant immunisation with the pneumococcal non-typeable Haemophilus influenzae protein D conjugate vaccine in South Africa. Vaccine. 2020. DOI:10.1016/j.vaccine.2020.01.062..
  • Miiro G, Kayhty H, Watera C, et al. Conjugate pneumococcal vaccine in HIV-infected ugandans and the effect of past receipt of polysaccharide vaccine. J Infect Dis. 2005;192:1801–1805.
  • Ibarz-Pavon AB, French N. No changes on viral load and CD4+ T-cell counts following immunization with 7-valent pneumococcal conjugate vaccine among HIV-infected adults in Malawi. Vaccine. 2018;36:2504–2506.
  • McLaughlin JM, Swerdlow DL, Isturiz RE, et al. Decision-making for PCV in adults. Hum Vaccin Immunother. 2019;15:584–593.
  • McLaughlin JM, Jiang Q, Isturiz RE, et al. Effectiveness of 13-valent pneumococcal conjugate vaccine against hospitalization for community-acquired pneumonia in older US adults: a test-negative design. Clin Infect Dis. 2018;67:1498–1506.
  • Lee K-Y, Tsai M-S, Kuo K-C, et al. Pneumococcal vaccination among HIV-infected adult patients in the era of combination antiretroviral therapy. Hum Vaccin Immunother. 2014;10:3700–3710.
  • Licciardi PV, Tan EL, Li P, et al. Pneumococcal vaccination for HIV-infected individuals in Singapore. Proc Singapore Healthcare. 2019;28:55–60.
  • Choi YH, Andrews N, Miller E. Estimated impact of revising the 13-valent pneumococcal conjugate vaccine schedule from 2+1 to 1+1 in England and Wales: A modelling study. PLoS Med. 2019;16:e1002845.
  • VACFA. Immunization schedules - Africa Vaccines for Africa 2018. [cited 2020 Aug 27].http://www.vacfa.uct.ac.za/immunization-schedules-africa
  • Gavi, The vaccine alliance. Pneumococcal vaccine support 2017. [cited 2019 Aug 1]. https://www.gavi.org/support/nvs/pneumococcal/
  • Ntshoe GM, McAnerney JM, Archer BN, et al. Measles outbreak in south africa: epidemiology of laboratory-confirmed measles cases and assessment of intervention, 2009–2011. Plos One. 2013;8:e55682.
  • Weinberger DM, Pitzer VE, Regev-Yochay G, et al. Association between the decline in pneumococcal disease in unimmunized adults and vaccine-derived protection against colonization in toddlers and preschool-aged children. Am J Epidemiol. 2019;188:160–168.
  • Le Polain De Waroux O, Flasche S, Prieto-Merino D, et al. The efficacy and duration of protection of pneumococcal conjugate vaccines against nasopharyngeal carriage: a meta-regression model. Pediatr Infect Dis J. 2015;34:858.
  • An Evaluation of PCV13 Vaccine Schedules, Comparing Impact of 2+1 vs 3+0 on Pneumococcal Carriage in Blantyre, Malawi. 2019. [cited 2019 Nov 29]. https://clinicaltrials.gov/ct2/show/NCT04078997
  • Evaluation of PCV Schedules in a Naive Population in Vietnam n.d. [cited 2019 Dec 16]. https://clinicaltrials.gov/ct2/show/NCT02961231
  • Blyth CC, Jayasinghe S, Andrews RM. A rationale for change: an increase in invasive pneumococcal disease in fully vaccinated children. Clin Infect Dis. n.d.. DOI:10.1093/cid/ciz493.
  • Jayasinghe S, Menzies R, Chiu C, et al. Long-term impact of a “3 + 0” schedule for 7- and 13-valent pneumococcal conjugate vaccines on invasive pneumococcal disease in Australia, 2002–2014. Clin Infect Dis. 2017;64:175–183.
  • Usuf E, Bottomley C, Bojang E, et al. Persistence of nasopharyngeal pneumococcal vaccine serotypes and increase of nonvaccine serotypes among vaccinated infants and their mothers 5 years after introduction of pneumococcal conjugate vaccine 13 in the Gambia. Clin Infect Dis. 2019;68:1512–1521.
  • Mackenzie GA, Hill PC, Jeffries DJ, 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.
  • WHO. Pneumococcal conjugate 3rd dose (PCV3) immunization coverage. WHO 2019. [cited 2019 Dec 16]. http://www.who.int/gho/immunization/pneumococcal/en/
  • Keeling MJ, Rohani P. Modeling Infectious Diseases in Humans and Animals. Princeton, New Jersey: Princeton University Press; 2011.
  • Vynnycky E, White R. An introduction to infectious disease modelling. Oxford, New York: Oxford University Press; 2010.
  • Anderson RM, May RM. Infectious diseases of humans: dynamics and control. Oxford, New York: Oxford University Press; 1992.
  • Flasche S, Lipsitch M, Ojal J, et al. *Estimating the contribution of different age strata to vaccine serotype pneumococcal transmission in the pre vaccine era:a modelling study. BMC Med. 2020;18. DOI:10.1186/s12916-020-01601-1.
  • Wyllie AL, Warren JL, Regev-Yochay G, et al. Serotype patterns of pneumococcal disease in adults are correlated with carriage patterns in older children. MedRxiv. 2019;2019:12.18.19015180.
  • Crum-Cianflone NF, Wallace MR. Vaccination in HIV-infected adults. AIDS Patient Care STDS. 2014;28:397–410.
  • Frank TD, Carter A, Jahagirdar D, et al. Global, regional, and national incidence, prevalence, and mortality of HIV, 1980–2017, and forecasts to 2030, for 195 countries and territories: a systematic analysis for the Global Burden of Diseases, Injuries, and Risk Factors Study 2017. Lancet HIV. 2019;6:e831–59.
  • Meyer-Rath G, Johnson LF, Pillay Y, et al. Changing the South African national antiretroviral therapy guidelines: the role of cost modelling. PLoS One. 2017;12. DOI:10.1371/journal.pone.0186557..
  • Cawley C, McRobie E, Oti S, et al. Identifying gaps in HIV policy and practice along the HIV care continuum: evidence from a national policy review and health facility surveys in urban and rural Kenya. Health Policy Plan. 2017;32:1316–1326.
  • Wallace A, Dietz V, Cairns KL. Integration of immunization services with other health interventions in the developing world: what works and why? Systematic literature review. Trop Med Int Health. 2009;14:11–19.
  • Crum-Cianflone NF, Hullsiek KH, Roediger M, et al. A randomized clinical trial comparing revaccination with pneumococcal conjugate vaccine to polysaccharide vaccine among HIV-infected adults. J Infect Dis. 2010;202:1114–1125.
  • Nunes MC, von Gottberg A, de Gouveia L, et al. The impact of antiretroviral treatment on the burden of invasive pneumococcal disease in South African children: a time series analysis. AIDS. 2011;25:453.
  • Heinsbroek E, Tafatatha T, Phiri A, et al. Persisting high prevalence of pneumococcal carriage among HIV-infected adults receiving antiretroviral therapy in Malawi. Aids. 2015;29:1837–1844.
  • Heinsbroek E, Tafatatha T, Chisambo C, et al. Pneumococcal acquisition among infants exposed to HIV in rural Malawi: a longitudinal household study. Am J Epidemiol. 2016;183:70–78.
  • Nunes MC, Shiri T, van Niekerk N, et al. Acquisition of streptococcus pneumoniae in pneumococcal conjugate vaccine-naïve South African children and their mothers. Pediatr Infect Dis J. 2013;32:e192.
  • Shiri T, Auranen K, Nunes MC, et al. Dynamics of pneumococcal transmission in vaccine-naïve children and their HIV-infected or HIV-uninfected mothers during the first 2 years of life. Am J Epidemiol. 2013;178:1629–1637.
  • Hill PC, Cheung YB, Akisanya A, et al. Nasopharyngeal carriage of streptococcus pneumoniae in gambian infants: a longitudinal study. Clin Infect Dis. 2008;46:807–814.
  • Clarke E, Kampmann B, Goldblatt D. Maternal and neonatal pneumococcal vaccination - where are we now? Expert Rev Vaccines. 2016;15:1305–1317.
  • Tigoi CC, Gatakaa H, Karani A, et al. Rates of acquisition of pneumococcal colonization and transmission probabilities, by serotype, among newborn infants in Kilifi District, Kenya. Clin Infect Dis. 2012;55:180–188.
  • Ojal J, Goldblatt D, Tigoi C, et al. Effect of maternally derived anti-protein and anticapsular IgG antibodies on the rate of acquisition of nasopharyngeal carriage of pneumococcus in newborns. Clin Infect Dis. 2018;66:121–130.
  • Abu-Raya B, Smolen KK, Willems F, et al. Transfer of maternal antimicrobial immunity to HIV-exposed uninfected newborns. Front Immunol. 2016;7. DOI:10.3389/fimmu.2016.00338.
  • Gupta A, Mathad JS, Yang W-T, et al. Maternal pneumococcal capsular IgG antibodies and transplacental transfer are low in South Asian HIV-infected mother-infant pairs. Vaccine. 2014;32:1466–1472.
  • Chaithongwongwatthana S, Yamasmit W, Limpongsanurak S, et al. Pneumococcal vaccination during pregnancy for preventing infant infection. Cochrane Database Syst Rev. 2015. DOI:10.1002/14651858.CD004903.pub4.
  • Heesterbeek H, Anderson RM, Andreasen V, et al. Modeling infectious disease dynamics in the complex landscape of global health. Science. 2015;347:aaa4339.
  • le Polain de Waroux O, Flasche S, Kucharski AJ, et al. Identifying human encounters that shape the transmission of Streptococcus pneumoniae and other acute respiratory infections. Epidemics. 2018;25:72–79.
  • le Polain de Waroux O, Cohuet S, Ndazima D, et al. Characteristics of human encounters and social mixing patterns relevant to infectious diseases spread by close contact: a survey in Southwest Uganda. BMC Infect Dis. 2018;18:172.
  • Kiti MC, Kinyanjui TM, Koech DC, et al. Quantifying age-related rates of social contact using diaries in a rural coastal population of Kenya. Plos One. 2014;9:e104786.
  • Melegaro A, Fava ED, Poletti P, et al. Social contact structures and time use patterns in the manicaland province of zimbabwe. Plos One. 2017;12:e0170459.
  • Johnstone-Robertson SP, Mark D, Morrow C, et al. Social mixing patterns within a South African township community: implications for respiratory disease transmission and control. Am J Epidemiol. 2011;174:1246–1255.
  • Voysey M, Kelly DF, Fanshawe TR, et al. The influence of maternally derived antibody and infant age at vaccination on infant vaccine responses. JAMA Pediatr. 2017;171:637–646.
  • Jones C, Pollock L, Barnett SM, et al. The relationship between concentration of specific antibody at birth and subsequent response to primary immunization. Vaccine. 2014;32:996–1002.