Skip to main content
Top
Published in: BMC Infectious Diseases 1/2018

Open Access 01-12-2018 | Research article

Nasopharyngeal carriage of Streptococcus pneumoniae in children under 5 years of age before introduction of pneumococcal vaccine (PCV10) in urban and rural districts in Pakistan

Authors: Muhammad Imran Nisar, Kanwal Nayani, Tauseef Akhund, Atif Riaz, Omar Irfan, Sadia Shakoor, Sehrish Muneer, Sana Muslim, Aneeta Hotwani, Furqan Kabir, Cynthia Whitney, Lindsay Kim, Velusamy Srinivasan, Asad Ali, Anita K. M. Zaidi, Fyezah Jehan

Published in: BMC Infectious Diseases | Issue 1/2018

Login to get access

Abstract

Background

Benefits of pneumococcal conjugate vaccine programs have been linked to the vaccine’s ability to disrupt nasopharyngeal carriage and transmission. The 10-valent pneumococcal vaccine (PCV10) was included in the Expanded Program on Immunization (EPI) in Sindh, Pakistan in February 2013. This study was carried out immediately before PCV10 introduction to establish baseline pneumococcal carriage and prevalent serotypes in young children and to determine if carriage differed in urban and rural communities.

Methods

Nasopharyngeal specimens were collected from a random sample of children 3-11 and 12-59 months of age in an urban community (Karachi) and children 3-11 months of age in a rural community (Matiari). Samples were processed in a research laboratory in Karachi. Samples were transported in STGG media, enriched in Todd Hewitt broth, rabbit serum and yeast extract, cultured on 5% sheep blood agar, and serotyped using the CDC standardized sequential multiplex PCR assay. Serotypes were categorized into PCV10-type and non-vaccine types.

Results

We enrolled 670 children. Pneumococci were detected in 73.6% and 79.5 % of children in the infant group in Karachi and Matiari, respectively, and 78.2% of children 12 to 59 months of age in Karachi. In infants, 38.9% and 33.5% of those carrying pneumococci in Karachi and Matiari, respectively, had PCV10 types. In the older age group in Karachi, the proportion was 30.7%, not significantly different from infants. The most common serotypes were 6A, 23F, 19A, 6B and 19F.

Conclusion

We found that about 3 of 4 children carried pneumococci, and this figure did not vary with age group or urban or rural residence. Planned annual surveys in the same communities will inform change in carriage of PCV10 serotype pneumococci after the introduction and uptake of PCV10 in these communities
Appendix
Available only for authorised users
Literature
1.
go back to reference WHO. Estimated Hib and pneumococcal deaths for children under 5 years of age, 2008; 2008 Contract No.: Document Number|. WHO. Estimated Hib and pneumococcal deaths for children under 5 years of age, 2008; 2008 Contract No.: Document Number|.
2.
go back to reference Bruce MG, Singleton R, Bulkow L, Rudolph K, Zulz T, Gounder P, et al. Impact of the 13-valent pneumococcal conjugate vaccine (pcv13) on invasive pneumococcal disease and carriage in Alaska. Vaccine. 2015 Sep 11;33(38):4813–9.CrossRefPubMed Bruce MG, Singleton R, Bulkow L, Rudolph K, Zulz T, Gounder P, et al. Impact of the 13-valent pneumococcal conjugate vaccine (pcv13) on invasive pneumococcal disease and carriage in Alaska. Vaccine. 2015 Sep 11;33(38):4813–9.CrossRefPubMed
3.
go back to reference Walker CL, Rudan I, Liu L, Nair H, Theodoratou E, Bhutta ZA, et al. Global burden of childhood pneumonia and diarrhoea. Lancet. 2013 Apr 20;381(9875):1405–16.CrossRefPubMedPubMedCentral Walker CL, Rudan I, Liu L, Nair H, Theodoratou E, Bhutta ZA, et al. Global burden of childhood pneumonia and diarrhoea. Lancet. 2013 Apr 20;381(9875):1405–16.CrossRefPubMedPubMedCentral
4.
go back to reference Cohen R, Varon E, Bechet S, Bonacorsi S, Levy C. Comparative impact of pneumococcal conjugate vaccines on pneumococcal meningitis according to underlying conditions. Vaccine. 2016 Sep 22;34(41):4850–6.CrossRefPubMed Cohen R, Varon E, Bechet S, Bonacorsi S, Levy C. Comparative impact of pneumococcal conjugate vaccines on pneumococcal meningitis according to underlying conditions. Vaccine. 2016 Sep 22;34(41):4850–6.CrossRefPubMed
5.
go back to reference Steens A, Bergsaker MA, Aaberge IS, Ronning K, Vestrheim DF. Prompt effect of replacing the 7-valent pneumococcal conjugate vaccine with the 13-valent vaccine on the epidemiology of invasive pneumococcal disease in Norway. Vaccine. 2013 Dec 16;31(52):6232–8.CrossRefPubMed Steens A, Bergsaker MA, Aaberge IS, Ronning K, Vestrheim DF. Prompt effect of replacing the 7-valent pneumococcal conjugate vaccine with the 13-valent vaccine on the epidemiology of invasive pneumococcal disease in Norway. Vaccine. 2013 Dec 16;31(52):6232–8.CrossRefPubMed
6.
go back to reference Ceyhan M, Dagan R, Sayiner A, Chernyshova L, Dinleyici EC, Hryniewicz W, et al. Surveillance of pneumococcal diseases in Central and Eastern Europe. Hum Vaccin Immunother. 2016 Aug 02;12(8):2124–34.CrossRefPubMedPubMedCentral Ceyhan M, Dagan R, Sayiner A, Chernyshova L, Dinleyici EC, Hryniewicz W, et al. Surveillance of pneumococcal diseases in Central and Eastern Europe. Hum Vaccin Immunother. 2016 Aug 02;12(8):2124–34.CrossRefPubMedPubMedCentral
7.
go back to reference Griffin MR, Mitchel E, Moore MR, Whitney CG, Grijalva CG. Centers for Disease C, et al. Declines in pneumonia hospitalizations of children aged <2 years associated with the use of pneumococcal conjugate vaccines - Tennessee, 1998-2012. MMWR Morb Mortal Wkly Rep. 2014 Nov 07;63(44):995–8.PubMedPubMedCentral Griffin MR, Mitchel E, Moore MR, Whitney CG, Grijalva CG. Centers for Disease C, et al. Declines in pneumonia hospitalizations of children aged <2 years associated with the use of pneumococcal conjugate vaccines - Tennessee, 1998-2012. MMWR Morb Mortal Wkly Rep. 2014 Nov 07;63(44):995–8.PubMedPubMedCentral
8.
go back to reference Von Gottberg A, De Gouveia L, Tempia S, Quan V, Meiring S, Von Mollendorf C, et al. Effects of vaccination on invasive pneumococcal disease in South Africa. New England Journal of Medicine. 2014;371(20):1889–99.CrossRef Von Gottberg A, De Gouveia L, Tempia S, Quan V, Meiring S, Von Mollendorf C, et al. Effects of vaccination on invasive pneumococcal disease in South Africa. New England Journal of Medicine. 2014;371(20):1889–99.CrossRef
9.
go back to reference Brandileone MC, Zanella RC, Almeida SC, Brandao AP, Ribeiro AF, Carvalhanas TM, et al. Effect of 10-valent pneumococcal conjugate vaccine on nasopharyngeal carriage of Streptococcus pneumoniae and Haemophilus influenzae among children in Sao Paulo. Brazil. Vaccine. 2016 Nov 04;34(46):5604–11.CrossRefPubMed Brandileone MC, Zanella RC, Almeida SC, Brandao AP, Ribeiro AF, Carvalhanas TM, et al. Effect of 10-valent pneumococcal conjugate vaccine on nasopharyngeal carriage of Streptococcus pneumoniae and Haemophilus influenzae among children in Sao Paulo. Brazil. Vaccine. 2016 Nov 04;34(46):5604–11.CrossRefPubMed
10.
go back to reference Biesbroek G, Wang X, Keijser BJ, Eijkemans RM, Trzcinski K, Rots NY, et al. Seven-valent pneumococcal conjugate vaccine and nasopharyngeal microbiota in healthy children. Emerg Infect Dis. 2014 Feb;20(2):201–10.CrossRefPubMedPubMedCentral Biesbroek G, Wang X, Keijser BJ, Eijkemans RM, Trzcinski K, Rots NY, et al. Seven-valent pneumococcal conjugate vaccine and nasopharyngeal microbiota in healthy children. Emerg Infect Dis. 2014 Feb;20(2):201–10.CrossRefPubMedPubMedCentral
11.
go back to reference Loughlin AM, Hsu K, Silverio AL, Marchant CD, Pelton SI. Direct and indirect effects of PCV13 on nasopharyngeal carriage of PCV13 unique pneumococcal serotypes in Massachusetts' children. Pediatr Infect Dis J. 2014 May;33(5):504–10.CrossRefPubMed Loughlin AM, Hsu K, Silverio AL, Marchant CD, Pelton SI. Direct and indirect effects of PCV13 on nasopharyngeal carriage of PCV13 unique pneumococcal serotypes in Massachusetts' children. Pediatr Infect Dis J. 2014 May;33(5):504–10.CrossRefPubMed
12.
go back to reference Desai AP, Sharma D, Crispell EK, Baughman W, Thomas S, Tunali A, et al. Decline in Pneumococcal Nasopharyngeal Carriage of Vaccine Serotypes After the Introduction of the 13-Valent Pneumococcal Conjugate Vaccine in Children in Atlanta. Georgia. Pediatr Infect Dis J. 2015 Nov;34(11):1168–74.CrossRefPubMed Desai AP, Sharma D, Crispell EK, Baughman W, Thomas S, Tunali A, et al. Decline in Pneumococcal Nasopharyngeal Carriage of Vaccine Serotypes After the Introduction of the 13-Valent Pneumococcal Conjugate Vaccine in Children in Atlanta. Georgia. Pediatr Infect Dis J. 2015 Nov;34(11):1168–74.CrossRefPubMed
13.
go back to reference Simell B, Auranen K, Kayhty H, Goldblatt D, Dagan R, O'Brien KL, et al. The fundamental link between pneumococcal carriage and disease. Expert Rev Vaccines. 2012 Jul;11(7):841–55.CrossRefPubMed Simell B, Auranen K, Kayhty H, Goldblatt D, Dagan R, O'Brien KL, et al. The fundamental link between pneumococcal carriage and disease. Expert Rev Vaccines. 2012 Jul;11(7):841–55.CrossRefPubMed
14.
go back to reference Hammitt LL, Bruden DL, Butler JC, Baggett HC, Hurlburt DA, Reasonover A, et al. Indirect effect of conjugate vaccine on adult carriage of Streptococcus pneumoniae: an explanation of trends in invasive pneumococcal disease. J Infect Dis. 2006 Jun 01;193(11):1487–94.CrossRefPubMed Hammitt LL, Bruden DL, Butler JC, Baggett HC, Hurlburt DA, Reasonover A, et al. Indirect effect of conjugate vaccine on adult carriage of Streptococcus pneumoniae: an explanation of trends in invasive pneumococcal disease. J Infect Dis. 2006 Jun 01;193(11):1487–94.CrossRefPubMed
15.
go back to reference Devine VT, Jefferies JM, Clarke SC, Faust SN. Nasopharyngeal Bacterial Carriage in the Conjugate Vaccine Era with a Focus on Pneumococci. J Immunol Res. 2015;2015:394368.CrossRefPubMedPubMedCentral Devine VT, Jefferies JM, Clarke SC, Faust SN. Nasopharyngeal Bacterial Carriage in the Conjugate Vaccine Era with a Focus on Pneumococci. J Immunol Res. 2015;2015:394368.CrossRefPubMedPubMedCentral
16.
go back to reference Owais A, Tikmani SS, Sultana S, Zaman U, Ahmed I, Allana S, et al. Incidence of pneumonia, bacteremia, and invasive pneumococcal disease in Pakistani children. Trop Med Int Health. 2010 Sep;15(9):1029–36.PubMed Owais A, Tikmani SS, Sultana S, Zaman U, Ahmed I, Allana S, et al. Incidence of pneumonia, bacteremia, and invasive pneumococcal disease in Pakistani children. Trop Med Int Health. 2010 Sep;15(9):1029–36.PubMed
17.
go back to reference WHO. Pakistan: WHO and UNICEF estimates of immunization coverage: 2015 revision; 2015 Contract No.: Document Number|. WHO. Pakistan: WHO and UNICEF estimates of immunization coverage: 2015 revision; 2015 Contract No.: Document Number|.
18.
go back to reference O'Brien KL, Nohynek H. World Health Organization Pneumococcal Vaccine Trials Carraige Working G. Report from a WHO working group: standard method for detecting upper respiratory carriage of Streptococcus pneumoniae. Pediatr Infect Dis J. 2003 Feb;22(2):133–40.CrossRefPubMed O'Brien KL, Nohynek H. World Health Organization Pneumococcal Vaccine Trials Carraige Working G. Report from a WHO working group: standard method for detecting upper respiratory carriage of Streptococcus pneumoniae. Pediatr Infect Dis J. 2003 Feb;22(2):133–40.CrossRefPubMed
19.
go back to reference Jin P, Xiao M, Kong F, Oftadeh S, Zhou F, Liu C, et al. Simple, accurate, serotype-specific PCR assay to differentiate Streptococcus pneumoniae serotypes 6A, 6B, and 6C. J Clin Microbiol. 2009 Aug;47(8):2470–4.CrossRefPubMedPubMedCentral Jin P, Xiao M, Kong F, Oftadeh S, Zhou F, Liu C, et al. Simple, accurate, serotype-specific PCR assay to differentiate Streptococcus pneumoniae serotypes 6A, 6B, and 6C. J Clin Microbiol. 2009 Aug;47(8):2470–4.CrossRefPubMedPubMedCentral
20.
go back to reference Jin P, Kong F, Xiao M, Oftadeh S, Zhou F, Liu C, et al. First report of putative Streptococcus pneumoniae serotype 6D among nasopharyngeal isolates from Fijian children. J Infect Dis. 2009 Nov 01;200(9):1375–80.CrossRefPubMed Jin P, Kong F, Xiao M, Oftadeh S, Zhou F, Liu C, et al. First report of putative Streptococcus pneumoniae serotype 6D among nasopharyngeal isolates from Fijian children. J Infect Dis. 2009 Nov 01;200(9):1375–80.CrossRefPubMed
21.
go back to reference Adegbola RA, DeAntonio R, Hill PC, Roca A, Usuf E, Hoet B, et al. 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(8):e103293.CrossRefPubMedPubMedCentral Adegbola RA, DeAntonio R, Hill PC, Roca A, Usuf E, Hoet B, et al. 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(8):e103293.CrossRefPubMedPubMedCentral
22.
go back to reference Mastro TD, Nomani NK, Ishaq Z, Ghafoor A, Shaukat NF, Esko E, et al. Use of nasopharyngeal isolates of Streptococcus pneumoniae and Haemophilus influenzae from children in Pakistan for surveillance for antimicrobial resistance. Pediatr Infect Dis J. 1993 Oct;12(10):824–30.CrossRefPubMed Mastro TD, Nomani NK, Ishaq Z, Ghafoor A, Shaukat NF, Esko E, et al. Use of nasopharyngeal isolates of Streptococcus pneumoniae and Haemophilus influenzae from children in Pakistan for surveillance for antimicrobial resistance. Pediatr Infect Dis J. 1993 Oct;12(10):824–30.CrossRefPubMed
23.
go back to reference Nisar MI, Jehan F, Akhund T, Shakoor S, Qureshi S, Zaidi A. Nasopharyngeal carriage of streptococcus pneumoniae in children under 5 years of age before introduction of pneumococcal vaccine (PCV 10) in urban and rural Sindh. International Journal of Infectious Diseases. 2016;45:423.CrossRef Nisar MI, Jehan F, Akhund T, Shakoor S, Qureshi S, Zaidi A. Nasopharyngeal carriage of streptococcus pneumoniae in children under 5 years of age before introduction of pneumococcal vaccine (PCV 10) in urban and rural Sindh. International Journal of Infectious Diseases. 2016;45:423.CrossRef
24.
go back to reference Cheung YB, Zaman SM, Nsekpong ED, Van Beneden CA, Adegbola RA, Greenwood B, et al. Nasopharyngeal carriage of Streptococcus pneumoniae in Gambian children who participated in a 9-valent pneumococcal conjugate vaccine trial and in their younger siblings. Pediatr Infect Dis J. 2009 Nov;28(11):990–5.CrossRefPubMed Cheung YB, Zaman SM, Nsekpong ED, Van Beneden CA, Adegbola RA, Greenwood B, et al. Nasopharyngeal carriage of Streptococcus pneumoniae in Gambian children who participated in a 9-valent pneumococcal conjugate vaccine trial and in their younger siblings. Pediatr Infect Dis J. 2009 Nov;28(11):990–5.CrossRefPubMed
25.
go back to reference Roca A, Dione MM, Bojang A, Townend J, Egere U, Darboe O, et al. Nasopharyngeal carriage of pneumococci four years after community-wide vaccination with PCV-7 in The Gambia: long-term evaluation of a cluster randomized trial. PLoS One. 2013;8(9):e72198.CrossRefPubMedPubMedCentral Roca A, Dione MM, Bojang A, Townend J, Egere U, Darboe O, et al. Nasopharyngeal carriage of pneumococci four years after community-wide vaccination with PCV-7 in The Gambia: long-term evaluation of a cluster randomized trial. PLoS One. 2013;8(9):e72198.CrossRefPubMedPubMedCentral
26.
go back to reference Hill PC, Townend J, Antonio M, Akisanya B, Ebruke C, Lahai G, et al. Transmission of Streptococcus pneumoniae in rural Gambian villages: a longitudinal study. Clin Infect Dis. 2010 Jun 01;50(11):1468–76.CrossRefPubMed Hill PC, Townend J, Antonio M, Akisanya B, Ebruke C, Lahai G, et al. Transmission of Streptococcus pneumoniae in rural Gambian villages: a longitudinal study. Clin Infect Dis. 2010 Jun 01;50(11):1468–76.CrossRefPubMed
27.
go back to reference Coles CL, Kanungo R, Rahmathullah L, Thulasiraj RD, Katz J, Santosham M, et al. Pneumococcal nasopharyngeal colonization in young South Indian infants. Pediatr Infect Dis J. 2001 Mar;20(3):289–95.CrossRefPubMed Coles CL, Kanungo R, Rahmathullah L, Thulasiraj RD, Katz J, Santosham M, et al. Pneumococcal nasopharyngeal colonization in young South Indian infants. Pediatr Infect Dis J. 2001 Mar;20(3):289–95.CrossRefPubMed
28.
go back to reference Wattal C, Oberoi JK, Pruthi PK, Gupta S. Nasopharyngeal carriage of Streptococcus pneumoniae. Indian J Pediatr. 2007 Oct;74(10):905–7.CrossRefPubMed Wattal C, Oberoi JK, Pruthi PK, Gupta S. Nasopharyngeal carriage of Streptococcus pneumoniae. Indian J Pediatr. 2007 Oct;74(10):905–7.CrossRefPubMed
29.
go back to reference Miller E, Andrews NJ, Waight PA, Slack MP, George RC. Effectiveness of the new serotypes in the 13-valent pneumococcal conjugate vaccine. Vaccine. 2011 Nov 15;29(49):9127–31.CrossRefPubMed Miller E, Andrews NJ, Waight PA, Slack MP, George RC. Effectiveness of the new serotypes in the 13-valent pneumococcal conjugate vaccine. Vaccine. 2011 Nov 15;29(49):9127–31.CrossRefPubMed
30.
go back to reference Uruena A, Pippo T, Betelu MS, Virgilio F, Giglio N, Gentile A, et al. Cost-effectiveness analysis of the 10- and 13-valent pneumococcal conjugate vaccines in Argentina. Vaccine. 2011 Jul 12;29(31):4963–72.CrossRefPubMed Uruena A, Pippo T, Betelu MS, Virgilio F, Giglio N, Gentile A, et al. Cost-effectiveness analysis of the 10- and 13-valent pneumococcal conjugate vaccines in Argentina. Vaccine. 2011 Jul 12;29(31):4963–72.CrossRefPubMed
31.
go back to reference Mauffrey F, Fournier Ãr, Demczuk W, Martin I, Mulvey M, Martineau C, et al. Comparison of sequential multiplex PCR, sequetyping and whole genome sequencing for serotyping of Streptococcus pneumoniae. PLoS One. 2017;12(12):e0189163. Mauffrey F, Fournier Ãr, Demczuk W, Martin I, Mulvey M, Martineau C, et al. Comparison of sequential multiplex PCR, sequetyping and whole genome sequencing for serotyping of Streptococcus pneumoniae. PLoS One. 2017;12(12):e0189163.
32.
go back to reference Roca A, Bottomley C, Hill PC, Bojang A, Egere U, Antonio M, et al. Effect of age and vaccination with a pneumococcal conjugate vaccine on the density of pneumococcal nasopharyngeal carriage. Clin Infect Dis. 2012 Sep;55(6):816–24.CrossRefPubMedPubMedCentral Roca A, Bottomley C, Hill PC, Bojang A, Egere U, Antonio M, et al. Effect of age and vaccination with a pneumococcal conjugate vaccine on the density of pneumococcal nasopharyngeal carriage. Clin Infect Dis. 2012 Sep;55(6):816–24.CrossRefPubMedPubMedCentral
Metadata
Title
Nasopharyngeal carriage of Streptococcus pneumoniae in children under 5 years of age before introduction of pneumococcal vaccine (PCV10) in urban and rural districts in Pakistan
Authors
Muhammad Imran Nisar
Kanwal Nayani
Tauseef Akhund
Atif Riaz
Omar Irfan
Sadia Shakoor
Sehrish Muneer
Sana Muslim
Aneeta Hotwani
Furqan Kabir
Cynthia Whitney
Lindsay Kim
Velusamy Srinivasan
Asad Ali
Anita K. M. Zaidi
Fyezah Jehan
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2018
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-018-3608-5

Other articles of this Issue 1/2018

BMC Infectious Diseases 1/2018 Go to the issue