A Comparison of Pneumococcal Nasopharyngeal Carriage in Very Young Fijian Infants Born by Vaginal or Cesarean Delivery

Eleanor Frances Georgina Neal, Cattram Nguyen, Felista Tupou Ratu, Silivia Matanitobua, Eileen Margaret Dunne, Rita Reyburn, Mike Kama, Rachel Devi, Kylie M. Jenkins, Lisi Tikoduadua, Joseph Kado, Eric Rafai, Catherine Satzke, Edward Kim Mulholland, Fiona Mary Russell

Research output: Contribution to journalArticle

Abstract

Importance: Pneumococcal nasopharyngeal carriage is a prerequisite for pneumococcal disease. The main transmission route is from toddlers, who commonly carry pneumococci. However, neonatal pneumococcal disease case reports suggest that vertical pneumococcal transmission may also occur. Objective: To describe and compare pneumococcal nasopharyngeal carriage and density by infant mode of delivery in young Fijian infants. Design, Setting, and Participants: Annual cross-sectional surveys were performed in Suva, Fiji, before the introduction of 10-valent pneumococcal conjugate vaccine (PCV10), from September 14 to December 20, 2012, and after PCV10 was introduced, from July 11 to November 19, 2013; July 15 to December 9, 2014; and August 13 to November 19, 2015. Caregivers of 2006 infants aged 5 to 8 weeks participated in the surveys. Statistical analysis was performed from May 24, 2018, to August 12, 2019. Exposures: Caregivers provided data on infant mode of delivery and demographics via interviewer-led survey. Main Outcomes and Measures: Pneumococci in swab samples were detected and quantified by lytA quantitative polymerase chain reaction with molecular serotyping by microarray. Pneumococci were categorized as PCV10 or non-PCV10 serotypes. Results: Of the 2006 infants (976 girls and 1030 boys; mean [SD] age, 6.1 [0.02] weeks]), 1742 (86.8%) were born vaginally and 264 were born by cesarean delivery. Infants delivered vaginally, compared with those born by cesarean delivery, had a higher prevalence of overall pneumococcal nasopharyngeal carriage (470 of 1722 [27.3%; 95% CI, 25.2%-29.4%] vs 47 of 260 [18.1%; 95% CI, 13.6%-23.3%]; P = .002), PCV10 carriage (113 of 1698 [6.7%; 95% CI, 5.5%-7.9%] vs 8 of 256 [3.1%; 95% CI, 1.4%-6.1%]; P = .03), and non-PCV10 carriage (355 of 1698 [20.9%; 95% CI, 19.0%-22.9%] vs 38 of 256 [14.8%; 95% CI, 10.7%-19.8%]; P = .02), and had higher median densities of overall pneumococci (4.9 log10 genome equivalents [GE]/mL [interquartile range, 4.8-5.0 log10 GE/mL] vs 4.5 log10 GE/mL [interquartile range, 4.1-4.6 log10 GE/mL]; P = .01) and non-PCV10 pneumococci (4.9 log10 GE/mL [interquartile range, 4.7-5.0 log10 GE/mL] vs 4.4 log10 GE/mL [interquartile range, 4.0-4.7 log10 GE/mL]; P = .01). Vaginal delivery was associated with overall (adjusted odds ratio, 1.57 [95% CI, 1.10-2.23]; P = .01) and non-PCV10 (adjusted odds ratio, 1.49 [95% CI, 1.01-2.20]; P = .04]) pneumococcal nasopharyngeal carriage. Vaginal delivery was not associated with PCV10 carriage (adjusted odds ratio, 1.67 [95% CI, 0.80-3.51]; P = .17). After adjustment, vaginal delivery was not associated with density. Conclusions and Relevance: Pneumococcal nasopharyngeal carriage prevalence and density were higher in infants delivered vaginally compared with those delivered by cesarean birth. After adjustment, vaginal delivery was associated with pneumococcal carriage. Differences in carriage by mode of delivery may be due to differential exposure to the vaginal microbiota during delivery and the effect of intrapartum antibiotics during cesarean delivery on the infant microbiome. Our findings also raise the hypothesis that vertical transmission may contribute to pneumococcal acquisition.

Original languageEnglish
Pages (from-to)e1913650
JournalJAMA Network Open
Volume2
Issue number10
DOIs
Publication statusPublished - 2 Oct 2019

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Genome
Streptococcus pneumoniae
Microbiota
Odds Ratio
Caregivers
Infant, Newborn, Diseases
Fiji
Serotyping
10-valent pneumococcal conjugate vaccine
Cross-Sectional Studies
Demography
Outcome Assessment (Health Care)
Parturition
Interviews
Anti-Bacterial Agents
Polymerase Chain Reaction
Surveys and Questionnaires

Cite this

Neal, E. F. G., Nguyen, C., Ratu, F. T., Matanitobua, S., Dunne, E. M., Reyburn, R., ... Russell, F. M. (2019). A Comparison of Pneumococcal Nasopharyngeal Carriage in Very Young Fijian Infants Born by Vaginal or Cesarean Delivery. JAMA Network Open, 2(10), e1913650. https://doi.org/10.1001/jamanetworkopen.2019.13650
Neal, Eleanor Frances Georgina ; Nguyen, Cattram ; Ratu, Felista Tupou ; Matanitobua, Silivia ; Dunne, Eileen Margaret ; Reyburn, Rita ; Kama, Mike ; Devi, Rachel ; Jenkins, Kylie M. ; Tikoduadua, Lisi ; Kado, Joseph ; Rafai, Eric ; Satzke, Catherine ; Mulholland, Edward Kim ; Russell, Fiona Mary. / A Comparison of Pneumococcal Nasopharyngeal Carriage in Very Young Fijian Infants Born by Vaginal or Cesarean Delivery. In: JAMA Network Open. 2019 ; Vol. 2, No. 10. pp. e1913650.
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title = "A Comparison of Pneumococcal Nasopharyngeal Carriage in Very Young Fijian Infants Born by Vaginal or Cesarean Delivery",
abstract = "Importance: Pneumococcal nasopharyngeal carriage is a prerequisite for pneumococcal disease. The main transmission route is from toddlers, who commonly carry pneumococci. However, neonatal pneumococcal disease case reports suggest that vertical pneumococcal transmission may also occur. Objective: To describe and compare pneumococcal nasopharyngeal carriage and density by infant mode of delivery in young Fijian infants. Design, Setting, and Participants: Annual cross-sectional surveys were performed in Suva, Fiji, before the introduction of 10-valent pneumococcal conjugate vaccine (PCV10), from September 14 to December 20, 2012, and after PCV10 was introduced, from July 11 to November 19, 2013; July 15 to December 9, 2014; and August 13 to November 19, 2015. Caregivers of 2006 infants aged 5 to 8 weeks participated in the surveys. Statistical analysis was performed from May 24, 2018, to August 12, 2019. Exposures: Caregivers provided data on infant mode of delivery and demographics via interviewer-led survey. Main Outcomes and Measures: Pneumococci in swab samples were detected and quantified by lytA quantitative polymerase chain reaction with molecular serotyping by microarray. Pneumococci were categorized as PCV10 or non-PCV10 serotypes. Results: Of the 2006 infants (976 girls and 1030 boys; mean [SD] age, 6.1 [0.02] weeks]), 1742 (86.8{\%}) were born vaginally and 264 were born by cesarean delivery. Infants delivered vaginally, compared with those born by cesarean delivery, had a higher prevalence of overall pneumococcal nasopharyngeal carriage (470 of 1722 [27.3{\%}; 95{\%} CI, 25.2{\%}-29.4{\%}] vs 47 of 260 [18.1{\%}; 95{\%} CI, 13.6{\%}-23.3{\%}]; P = .002), PCV10 carriage (113 of 1698 [6.7{\%}; 95{\%} CI, 5.5{\%}-7.9{\%}] vs 8 of 256 [3.1{\%}; 95{\%} CI, 1.4{\%}-6.1{\%}]; P = .03), and non-PCV10 carriage (355 of 1698 [20.9{\%}; 95{\%} CI, 19.0{\%}-22.9{\%}] vs 38 of 256 [14.8{\%}; 95{\%} CI, 10.7{\%}-19.8{\%}]; P = .02), and had higher median densities of overall pneumococci (4.9 log10 genome equivalents [GE]/mL [interquartile range, 4.8-5.0 log10 GE/mL] vs 4.5 log10 GE/mL [interquartile range, 4.1-4.6 log10 GE/mL]; P = .01) and non-PCV10 pneumococci (4.9 log10 GE/mL [interquartile range, 4.7-5.0 log10 GE/mL] vs 4.4 log10 GE/mL [interquartile range, 4.0-4.7 log10 GE/mL]; P = .01). Vaginal delivery was associated with overall (adjusted odds ratio, 1.57 [95{\%} CI, 1.10-2.23]; P = .01) and non-PCV10 (adjusted odds ratio, 1.49 [95{\%} CI, 1.01-2.20]; P = .04]) pneumococcal nasopharyngeal carriage. Vaginal delivery was not associated with PCV10 carriage (adjusted odds ratio, 1.67 [95{\%} CI, 0.80-3.51]; P = .17). After adjustment, vaginal delivery was not associated with density. Conclusions and Relevance: Pneumococcal nasopharyngeal carriage prevalence and density were higher in infants delivered vaginally compared with those delivered by cesarean birth. After adjustment, vaginal delivery was associated with pneumococcal carriage. Differences in carriage by mode of delivery may be due to differential exposure to the vaginal microbiota during delivery and the effect of intrapartum antibiotics during cesarean delivery on the infant microbiome. Our findings also raise the hypothesis that vertical transmission may contribute to pneumococcal acquisition.",
author = "Neal, {Eleanor Frances Georgina} and Cattram Nguyen and Ratu, {Felista Tupou} and Silivia Matanitobua and Dunne, {Eileen Margaret} and Rita Reyburn and Mike Kama and Rachel Devi and Jenkins, {Kylie M.} and Lisi Tikoduadua and Joseph Kado and Eric Rafai and Catherine Satzke and Mulholland, {Edward Kim} and Russell, {Fiona Mary}",
year = "2019",
month = "10",
day = "2",
doi = "10.1001/jamanetworkopen.2019.13650",
language = "English",
volume = "2",
pages = "e1913650",
journal = "JAMA Network Open",
issn = "2574-3805",
publisher = "American Medical Association (AMA)",
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Neal, EFG, Nguyen, C, Ratu, FT, Matanitobua, S, Dunne, EM, Reyburn, R, Kama, M, Devi, R, Jenkins, KM, Tikoduadua, L, Kado, J, Rafai, E, Satzke, C, Mulholland, EK & Russell, FM 2019, 'A Comparison of Pneumococcal Nasopharyngeal Carriage in Very Young Fijian Infants Born by Vaginal or Cesarean Delivery' JAMA Network Open, vol. 2, no. 10, pp. e1913650. https://doi.org/10.1001/jamanetworkopen.2019.13650

A Comparison of Pneumococcal Nasopharyngeal Carriage in Very Young Fijian Infants Born by Vaginal or Cesarean Delivery. / Neal, Eleanor Frances Georgina; Nguyen, Cattram; Ratu, Felista Tupou; Matanitobua, Silivia; Dunne, Eileen Margaret; Reyburn, Rita; Kama, Mike; Devi, Rachel; Jenkins, Kylie M.; Tikoduadua, Lisi; Kado, Joseph; Rafai, Eric; Satzke, Catherine; Mulholland, Edward Kim; Russell, Fiona Mary.

In: JAMA Network Open, Vol. 2, No. 10, 02.10.2019, p. e1913650.

Research output: Contribution to journalArticle

TY - JOUR

T1 - A Comparison of Pneumococcal Nasopharyngeal Carriage in Very Young Fijian Infants Born by Vaginal or Cesarean Delivery

AU - Neal, Eleanor Frances Georgina

AU - Nguyen, Cattram

AU - Ratu, Felista Tupou

AU - Matanitobua, Silivia

AU - Dunne, Eileen Margaret

AU - Reyburn, Rita

AU - Kama, Mike

AU - Devi, Rachel

AU - Jenkins, Kylie M.

AU - Tikoduadua, Lisi

AU - Kado, Joseph

AU - Rafai, Eric

AU - Satzke, Catherine

AU - Mulholland, Edward Kim

AU - Russell, Fiona Mary

PY - 2019/10/2

Y1 - 2019/10/2

N2 - Importance: Pneumococcal nasopharyngeal carriage is a prerequisite for pneumococcal disease. The main transmission route is from toddlers, who commonly carry pneumococci. However, neonatal pneumococcal disease case reports suggest that vertical pneumococcal transmission may also occur. Objective: To describe and compare pneumococcal nasopharyngeal carriage and density by infant mode of delivery in young Fijian infants. Design, Setting, and Participants: Annual cross-sectional surveys were performed in Suva, Fiji, before the introduction of 10-valent pneumococcal conjugate vaccine (PCV10), from September 14 to December 20, 2012, and after PCV10 was introduced, from July 11 to November 19, 2013; July 15 to December 9, 2014; and August 13 to November 19, 2015. Caregivers of 2006 infants aged 5 to 8 weeks participated in the surveys. Statistical analysis was performed from May 24, 2018, to August 12, 2019. Exposures: Caregivers provided data on infant mode of delivery and demographics via interviewer-led survey. Main Outcomes and Measures: Pneumococci in swab samples were detected and quantified by lytA quantitative polymerase chain reaction with molecular serotyping by microarray. Pneumococci were categorized as PCV10 or non-PCV10 serotypes. Results: Of the 2006 infants (976 girls and 1030 boys; mean [SD] age, 6.1 [0.02] weeks]), 1742 (86.8%) were born vaginally and 264 were born by cesarean delivery. Infants delivered vaginally, compared with those born by cesarean delivery, had a higher prevalence of overall pneumococcal nasopharyngeal carriage (470 of 1722 [27.3%; 95% CI, 25.2%-29.4%] vs 47 of 260 [18.1%; 95% CI, 13.6%-23.3%]; P = .002), PCV10 carriage (113 of 1698 [6.7%; 95% CI, 5.5%-7.9%] vs 8 of 256 [3.1%; 95% CI, 1.4%-6.1%]; P = .03), and non-PCV10 carriage (355 of 1698 [20.9%; 95% CI, 19.0%-22.9%] vs 38 of 256 [14.8%; 95% CI, 10.7%-19.8%]; P = .02), and had higher median densities of overall pneumococci (4.9 log10 genome equivalents [GE]/mL [interquartile range, 4.8-5.0 log10 GE/mL] vs 4.5 log10 GE/mL [interquartile range, 4.1-4.6 log10 GE/mL]; P = .01) and non-PCV10 pneumococci (4.9 log10 GE/mL [interquartile range, 4.7-5.0 log10 GE/mL] vs 4.4 log10 GE/mL [interquartile range, 4.0-4.7 log10 GE/mL]; P = .01). Vaginal delivery was associated with overall (adjusted odds ratio, 1.57 [95% CI, 1.10-2.23]; P = .01) and non-PCV10 (adjusted odds ratio, 1.49 [95% CI, 1.01-2.20]; P = .04]) pneumococcal nasopharyngeal carriage. Vaginal delivery was not associated with PCV10 carriage (adjusted odds ratio, 1.67 [95% CI, 0.80-3.51]; P = .17). After adjustment, vaginal delivery was not associated with density. Conclusions and Relevance: Pneumococcal nasopharyngeal carriage prevalence and density were higher in infants delivered vaginally compared with those delivered by cesarean birth. After adjustment, vaginal delivery was associated with pneumococcal carriage. Differences in carriage by mode of delivery may be due to differential exposure to the vaginal microbiota during delivery and the effect of intrapartum antibiotics during cesarean delivery on the infant microbiome. Our findings also raise the hypothesis that vertical transmission may contribute to pneumococcal acquisition.

AB - Importance: Pneumococcal nasopharyngeal carriage is a prerequisite for pneumococcal disease. The main transmission route is from toddlers, who commonly carry pneumococci. However, neonatal pneumococcal disease case reports suggest that vertical pneumococcal transmission may also occur. Objective: To describe and compare pneumococcal nasopharyngeal carriage and density by infant mode of delivery in young Fijian infants. Design, Setting, and Participants: Annual cross-sectional surveys were performed in Suva, Fiji, before the introduction of 10-valent pneumococcal conjugate vaccine (PCV10), from September 14 to December 20, 2012, and after PCV10 was introduced, from July 11 to November 19, 2013; July 15 to December 9, 2014; and August 13 to November 19, 2015. Caregivers of 2006 infants aged 5 to 8 weeks participated in the surveys. Statistical analysis was performed from May 24, 2018, to August 12, 2019. Exposures: Caregivers provided data on infant mode of delivery and demographics via interviewer-led survey. Main Outcomes and Measures: Pneumococci in swab samples were detected and quantified by lytA quantitative polymerase chain reaction with molecular serotyping by microarray. Pneumococci were categorized as PCV10 or non-PCV10 serotypes. Results: Of the 2006 infants (976 girls and 1030 boys; mean [SD] age, 6.1 [0.02] weeks]), 1742 (86.8%) were born vaginally and 264 were born by cesarean delivery. Infants delivered vaginally, compared with those born by cesarean delivery, had a higher prevalence of overall pneumococcal nasopharyngeal carriage (470 of 1722 [27.3%; 95% CI, 25.2%-29.4%] vs 47 of 260 [18.1%; 95% CI, 13.6%-23.3%]; P = .002), PCV10 carriage (113 of 1698 [6.7%; 95% CI, 5.5%-7.9%] vs 8 of 256 [3.1%; 95% CI, 1.4%-6.1%]; P = .03), and non-PCV10 carriage (355 of 1698 [20.9%; 95% CI, 19.0%-22.9%] vs 38 of 256 [14.8%; 95% CI, 10.7%-19.8%]; P = .02), and had higher median densities of overall pneumococci (4.9 log10 genome equivalents [GE]/mL [interquartile range, 4.8-5.0 log10 GE/mL] vs 4.5 log10 GE/mL [interquartile range, 4.1-4.6 log10 GE/mL]; P = .01) and non-PCV10 pneumococci (4.9 log10 GE/mL [interquartile range, 4.7-5.0 log10 GE/mL] vs 4.4 log10 GE/mL [interquartile range, 4.0-4.7 log10 GE/mL]; P = .01). Vaginal delivery was associated with overall (adjusted odds ratio, 1.57 [95% CI, 1.10-2.23]; P = .01) and non-PCV10 (adjusted odds ratio, 1.49 [95% CI, 1.01-2.20]; P = .04]) pneumococcal nasopharyngeal carriage. Vaginal delivery was not associated with PCV10 carriage (adjusted odds ratio, 1.67 [95% CI, 0.80-3.51]; P = .17). After adjustment, vaginal delivery was not associated with density. Conclusions and Relevance: Pneumococcal nasopharyngeal carriage prevalence and density were higher in infants delivered vaginally compared with those delivered by cesarean birth. After adjustment, vaginal delivery was associated with pneumococcal carriage. Differences in carriage by mode of delivery may be due to differential exposure to the vaginal microbiota during delivery and the effect of intrapartum antibiotics during cesarean delivery on the infant microbiome. Our findings also raise the hypothesis that vertical transmission may contribute to pneumococcal acquisition.

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