Dynamics of Streptococcus pneumoniae serotype structure in children for the period 2016–2022
- Authors: Protasova I.N.1, Feldblium I.V.2, Bakhareva N.V.3, Zinovieva L.V.4, Sidorenko S.V.5
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Affiliations:
- Professor V.F. Voino-Yasenetsky Krasnoyarsk State Medical University
- Perm State Medical University named after Academician E.A. Wagner
- Krasnoyarsk Regional Center for AIDS Prevention and Control
- Krasnoyarsk City Children’s Hospital No. 8
- Children’s Scientific and Clinical Center for Infectious Diseases
- Issue: Vol 29, No 2 (2024)
- Pages: 108-117
- Section: Original study articles
- Submitted: 28.02.2024
- Accepted: 04.04.2024
- Published: 10.06.2024
- URL: https://rjeid.com/1560-9529/article/view/627518
- DOI: https://doi.org/10.17816/EID627518
- ID: 627518
Cite item
Abstract
BACKGROUND: The need for microbiological monitoring of the distribution of pneumococcal serotypes is associated with changes that occur during routine immunization of children with pneumococcal vaccines.
AIM: To characterize the changes in the serotype structure of Streptococcus pneumoniae obtained from healthy preschool children between 2016 and 2022.
MATERIALS AND METHODS: In total, 1250 healthy children aged <6 years attending kindergartens were examined in multicenter studies (2016–2018 and 2020–2022). Nasopharyngeal pneumococcal isolates (n=265) were obtained using the culture method. S. pneumoniae serotype was determined using polymerase chain reaction.
RESULTS: Between 2016 and 2018, the prevalence of pneumococcal carriage decreased from 27.3 to 17.3%, and by 2022, it increased to 25.6%. Moreover, the correspondence of S. pneumoniae serotypes to the antigenic composition of the 13-valent pneumococcal vaccine decreased from 48.8 to 9.4% and the composition of the 20-valent vaccine from 75.6 to 39.1%. The proportion of “non-vaccine” types of pneumococcus increased from 22% in 2016 to 61% in 2022. Among the “non-vaccine” serotypes/groups, 15AF, 6CD, 23A, and 35F/47F were predominant, and new variants were also discovered: 23B and 35B. The serotypes included in the 13-valent conjugate vaccine were detected among unvaccinated children and were represented by variants 19F, 6A and 6B, 23F. Throughout the observation period, pneumococci of serotypes/groups 15BC, 11AD, and 10A were detected with high frequency.
CONCLUSIONS: Because of the elimination of a significant part of S. pneumoniae “vaccine” serotypes in 2016–2022, the concordance of circulating variants with the antigenic composition of pneumococcal conjugate vaccines significantly decreased. In addition, the new types detected with high frequency are not included in existing pneumococcal vaccines, which necessitates the creation of new immunobiological drugs for pneumococcal infection prevention.
Keywords
Full Text
BACKGROUND
Pneumococcal infection represents a group of ubiquitous anthroponotic diseases with aerosol transmission of the causative agent, Streptococcus pneumoniae. The clinical manifestations of these diseases range from asymptomatic to invasive, generalized forms of infection, which may be highly fatal, particularly in cases of meningitis and bacteremia [1].
Currently, there are over 100 serovariants of S. pneumoniae, differing in the chemical structure of the polysaccharide capsular antigen. The spectrum of epidemiologically relevant serotypes is characterized by variability [2]. A significant factor contributing to the prevalence and etiological significance of certain serotypes is immunization of children within the national schedule of preventive vaccinations with conjugate vaccines containing polysaccharides of S. pneumoniae capsule. These polysaccharides play an important role in colonization, virulence, and induction of serotype-specific immune response in the human body [3–6]. The 13-valent conjugate vaccine (PCV13) has been used in the Russian Federation since 2015 as a component of the national schedule of preventive vaccinations and the schedule of preventive vaccinations for epidemic indications. The vaccine contains capsular polysaccharides of pneumococci of the following serotypes: 1, 3, 4, 5, 6A, 6B, 7F, 9V, 14, 18C, 19A, 19F, and 23F. Each of these serotypes was individually conjugated to the carrier protein CRM197 [7]. Given the prolonged use of PCV13 for routine immunization of both children and adults at risk, it seems reasonable to suggest significant changes in the serotype composition of pneumococci over the past period.
AIM
To assess the prevalence and serotypes of S. pneumoniae isolates obtained from preschool children, the primary reservoir for the pathogen, over a period from 2016 to 2022.
MATERIALS AND METHODS
Study design
The SAPIENS [8] international, multicenter, prospective study examined 1,250 healthy children from organized groups in Krasnoyarsk (nursery schools) aged up to 6 years. The children were selected randomly, with a sampling error of 2.75% and 95% confidence level.
Nasopharyngeal swabs were performed once using probe-tampons with Amies liquid transport medium. S. pneumoniae was cultured on Colombian agar with addition of ram’s blood (5%), nalidixic acid, and colistin (ready-to-use agar, Sredoff LLC) under capnophilic conditions using Campylogas generator bags. Pneumococci were identified using a combination of cultural properties, tests with optochin and bile, and polymerase chain reaction (PCR) of cpsA and lytA genes [9]. Serotypes were determined using multiplex PCR [10].
Eligibility criteria
Inclusion criteria: permanent attendance of a child in an organized group (nursery school), age 0–6 years, informed consent signed by a parent or legal guardian, and no signs of infectious diseases at the time of examination.
Non-inclusion criteria: failure to meet the above age criteria and refusal of parents or guardians to sign the informed consent form.
Exclusion criteria: signs of acute infectious disease at the time of examination.
Study duration
The first phase of the study was conducted between 2020 and 2022, while the second phase was conducted in 2022.
Ethical review
The study was approved by the Ethics Committee of the Krasnoyarsk State Medical University named after Professor V.F. Voyno-Yasenetsky (Protocol No. 69/2016 dated April 28, 2016) and the Independent Interdisciplinary Committee for Ethical Review of Clinical Trials (Protocol No. 1 dated January 17, 2020).
Statistical analysis
Statistical analysis of the obtained results was performed using the STATISTICA10.0.1011 software package. Qualitative attributes were calculated as percentages, whereas quantitative data were calculated as mean values and standard deviations. Distribution of the attributes was evaluated using the Shapiro–Wilk test. If the normality of distribution was confirmed, the Student’s t-test was used to compare the groups. If normality was not confirmed, the Mann–Whitney test (for quantitative attributes) or the chi-square test (χ2; for qualitative attributes) was used. The level of statistical significance of the differences was considered to be p < 0.05.
RESULTS
Participant characteristics
The mean age of the subjects was 4.12 ± 0.97 years. When the subjects were divided into groups according to the study periods (years), the children examined in 2022 were found to be younger than those examined earlier (Table 1). Additionally, an increase in the number and proportion of children vaccinated in accordance with the schedule was noted during the analyzed period, accompanied by a simultaneous decrease in the proportion of non-vaccinated and once-vaccinated children. Accordingly, in 2022, the majority of children (68.8%) received three doses of the pneumococcal vaccine in accordance with the national immunization schedule, and the percentage of non-vaccinated children was 4.8% (see Table 1).
Table 1. Characteristics of examined children by age, gender, vaccination status, and prevalence of Streptococcus pneumoniae carriage
Parameter | 2016 | 2017 | 2018 | 2022 | Significance of differences |
Number examined | 150 | 450 | 400 | 250 | – |
Mean age | 4.25 ± 1.00 | 4.09 ± 0.96 | 4.19 ± 0.87 | 3.78 ± 1.06 | p4,1 = 0.0000 p4,2 = 0.0000 p4,3 = 0.0000 |
Gender, n/% | Male: 84/56 Female: 66/44 | Male: 244/54.22 Female: 206/45.78 | Male: 215/53.75 Female: 185/46.25 | Male: 133/53.20 Female: 117/46.80 | Not found |
Triple-vaccinated, n/% | 1/0.67 | 6/1.33 | 12/3.00 | 172/68.80 | p4,1 = 0.0000 p4,2 = 0.0000 p4,3 = 0.0000 |
Double-vaccinated, n/% | 2/1.33 | 26/5.78 | 25/6.25 | 51/20.40 | p2,1 = 0.0250 p3,1 = 0.0170 p4,1 = 0.0000 p4,2 = 0.0000 p4,3 = 0.0000 |
Once-vaccinated, n/% | 35/23.33 | 120/26.67 | 131/32.75 | 15/6.00 | p4,1 = 0.0000 p4,2 = 0.0000 p4,3 = 0.0000 |
Non-vaccinated, n/% | 112/74.67 | 298/66.22 | 232/58.00 | 12/4.80 | p3,1 = 0.0003 p4,1 = 0.0000 p4,2 = 0.0000 p4,3 = 0.0000 |
S. pneumoniae culture isolated, n/% | 41/27.33 | 91/20.22 | 69/17.25 | 64/25.60 | p3,1 = 0.0080 p4,3 = 0.0100 |
Primary findings
The prevalence of pneumococcal carriage, having decreased by 10% by 2018, increased by 8.3% by 2022, amounting to 25.6% (see Table 1).
Analysis of compliance of circulating S. pneumoniae serotypes with the antigen composition of pneumococcal vaccines showed that in 2022, only 9.4% of isolated cultures belonged to the serotypes included in PCV13, used for routine immunization of infants and toddlers (Table 2). Additionally, a progressive reduction in serotype overlap between PCV20 and PPSV23 (the 23-valent pneumococcal polysaccharide vaccine recommended for children over 2 years of age and adults) was observed, accompanied by a simultaneous increase in the proportion of S. pneumoniae variants not included in available vaccines, commonly referred to as “non-vaccine” (see Table 2).
Table 2. Correspondence of isolated Streptococcus pneumoniae cultures to the serotype composition of pneumococcal vaccines
Serotypes | 2016 | 2017 | 2018 | 2022 | Significance of differences |
Vaccine serotypes, n/%: PCV13 | 20/48.78 | 37/41.11 | 31/44.93 | 6/9.38 | p4,1 = 0.0000 p4,2 = 0.0000 p4,3 = 0.0000 |
PCV15 | 20/48.78 | 39/43.33 | 33/47.83 | 8/12.50 | p4,1 = 0.0000 p4,2 = 0.0000 p4,3 = 0.0000 |
PCV20 | 31/75.61 | 67/74.44 | 45/65.21 | 25/39.06 | p4,1 = 0.0002 p4,2 = 0.0000 p4,3 = 0.0025 |
PPSV23 | 32/78.05 | 70/77.77 | 45/65.21 | 25/39.06 | p4,1 = 0.0000 p4,2 = 0.0000 p4,3 = 0.0025 |
Non-vaccine serotypes, n/% | 9/21.95 | 21/23.08 | 24/34.78 | 39/60.94 | p4,1 = 0.0000 p4,2 = 0.0000 p4,3 = 0.0025 |
A detailed analysis of S. pneumoniae serotypes revealed that during the period between 2016 and 2018, the most prevalent variants were the vaccine serotypes such as 19F, 6A, 6B, and 23F. However, in 2022, these serotypes were only identified in single cases (Fig. 1). The circulation of pneumococci belonging to serogroups 11 and 15 (11AD and 15BC), as well as serotype 10A, was observed throughout the analyzed period. Remarkably, a significant increase in the proportion of non-vaccine serotypes/serogroups, including 15AF, 6CD, 23A, and 35F/47F and the emergence of novel variants, such as 23B and 35B, was revealed in 2022 (see Fig. 1).
Fig. 1. Dynamics of Streptococcus pneumoniae serotype distribution in healthy preschool children in 2016–2022. *Н/т — strains which serotype has not been determined (not included in the standard serotyping scheme).
A study of S. pneumoniae serotypes by vaccination status showed that serotypes included in PCV13 were detected in 5.8% of triple-vaccinated children. The most frequently detected serotypes were 6A, 6B, and 19A (Table 3). In nearly half of the cases (45.5%), the carriers of PCV13 serotypes did not comply with the recommended schedule of vaccination and revaccination, including late start of vaccination and non-compliance with the recommended intervals between vaccinations. The serotypes included in PCV15 and PCV20, as well as the non-vaccine serotypes, were primarily detected in the 2022 cohort (see Table 3). The overall frequency of their detection in triple-vaccinated children was 22.5%.
No PCV13 serotypes were identified in double-vaccinated children. PCV20 serotypes were detected in 13.5% of cases, along with non-vaccine serotypes (see Table 3).
Table 3. Distribution of Streptococcus pneumoniae serotypes in children by vaccination status (%)
Streptococcus pneumoniae serotype | Triple-vaccinated | Double-vaccinated | Once-vaccinated | Non-vaccinated | ||||||||||||
2016 n=1 | 2017 n=6 | 2018 n=12 | 2022 n=172 | 2016 n=2 | 2017 n=26 | 2018 n=25 | 2022 n=51 | 2016 n=35 | 2017 n=120 | 2018 n=131 | 2022 n=15 | 2016 n=112 | 2017 n=298 | 2018 n=232 | 2022 n=12 | |
PCV13 serotypes | ||||||||||||||||
23F | – | – | – | – | – | – | – | – | – | – | 0.8 | – | 3.6 | 1.7 | 2.6 | – |
6AB | – | 16.7 | 16.7 | 1.7 | – | – | – | – | – | 1.6 | 0.8 | – | 2.7 | 2.7 | 4.3 | – |
19F | – | – | – | 0.6 | – | – | – | – | 5.7 | – | 0.8 | – | 8.9 | 4.0 | 2.2 | – |
18ABCF | – | 16.7 | – | – | – | – | – | – | – | – | 1.5 | – | – | 0.7 | 0.4 | – |
14 | – | – | – | – | – | – | – | – | – | – | – | – | – | – | 0.4 | – |
9AV | – | – | – | – | – | – | – | – | – | – | – | – | – | 0.3 | – | – |
19A | – | 16.7 | – | 1.2 | – | – | – | – | – | – | – | – | – | 1.3 | – | – |
3 | – | – | – | – | – | – | – | – | – | – | – | – | 0.9 | – | 0.4 | – |
Total | 0.0 | 50.1 | 16.7 | 3.5 | 0.0 | 0.0 | 0.0 | 0.0 | 5.7 | 1.6 | 3.9 | 0.0 | 16.1 | 10.7 | 10.3 | 0.0 |
Additional PCV15 serotypes | ||||||||||||||||
22AF | – | – | – | 0.6 | – | – | – | – | – | 0.8 | – | – | – | – | 0.4 | – |
33AF/37 | – | – | – | 0.6 | – | – | – | – | – | 0.8 | – | – | – | – | 0.4 | – |
Total | 0.0 | 0.0 | 0.0 | 1.2 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 1.6 | 0.0 | 0.0 | 0.0 | 0.0 | 0.8 | 0.0 |
Additional PCV20 serotypes | ||||||||||||||||
15BC | – | – | – | 1.7 | – | – | 4.0 | 2.0 | – | 4.2 | 2.3 | – | 3.6 | 3.0 | 1.3 | – |
11AD | – | – | – | 4.7 | – | – | 4.0 | – | 5.7 | 1.6 | 0.8 | – | 0.9 | 3.0 | 1.3 | 8.3 |
8 | – | – | – | – | – | – | – | – | – | – | – | – | – | 0.3 | – | – |
10А | – | – | – | 0.6 | – | – | – | 3.9 | – | – | – | – | 3.6 | 0.7 | – | 8.3 |
Total | 0.0 | 0.0 | 0.0 | 7.0 | 0.0 | 0.0 | 8.0 | 5.9 | 5.7 | 5.8 | 3.1 | 0.0 | 8.1 | 7.0 | 2.6 | 16.6 |
Additional PPSV23 serotypes | ||||||||||||||||
9LN | – | – | – | – | – | – | – | – | – | – | – | – | – | – | – | – |
17F | – | – | – | – | – | – | – | – | – | – | – | – | 0.9 | 1.0 | – | – |
Total | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.0 | 0.9 | 1.0 | 0.0 | 0.0 |
Non-vaccine serotypes | ||||||||||||||||
15AF | – | – | – | 4.7 | – | 3.8 | – | 5.9 | – | 0.8 | – | – | – | 0.3 | 0.4 | 16.6 |
23A | – | – | – | 3.5 | – | – | – | – | – | – | – | – | – | 0.3 | 1.3 | – |
24ABF | – | – | – | – | – | – | – | – | 2.9 | – | – | – | 0.9 | – | – | – |
34 | – | – | – | – | – | – | – | – | – | 3.3 | – | 6.7 | – | – | – | – |
35AC/42 | – | – | – | – | – | – | – | – | 2.9 | – | 0.8 | – | 0.9 | – | – | – |
35F/47F | – | – | – | 2.3 | – | 3.8 | – | 2.0 | – | 0.8 | – | 6.7 | – | – | – | – |
39 | – | 16.7 | – | – | – | – | – | 3.9 | – | – | – | – | – | – | – | – |
23B | – | – | – | 0.6 | – | – | – | – | – | – | – | – | – | – | – | – |
6CD | – | – | – | 0.6 | – | – | – | – | 2.9 | 1.6 | 0.8 | – | 1.8 | 0.7 | 2.2 | – |
35B | – | – | – | 1.7 | – | – | – | – | – | - | – | – | – | – | – | – |
Non-typeable | – | – | 8.3 | 2.3 | – | – | – | 2.0 | – | – | 3.8 | 6.7 | 1.8 | 2.0 | 3.0 | – |
Total | 0.0 | 16.7 | 8.3 | 15.7 | 0.0 | 7.6 | 0.0 | 13.8 | 8.7 | 6.7 | 5.4 | 20.1 | 5.4 | 3.3 | 6.9 | 16.6 |
In the cohort of once-vaccinated children, the prevalence of PCV13 serotypes was 3%, the main serotypes of S. pneumoniae were 6A, 6B, and 19F. Furthermore, additional types included in PCV15 and PCV20, as well as non-vaccine types, were identified in 12% of cases (see Table 3).
The highest detection rate for PCV13 serotypes (11.3%) was observed in the group of non-vaccinated children, with a notable diversity of serotypes compared to other groups. Additional and non-vaccine types of pneumococcus were detected in 12.4% of cases, with the highest diversity observed in this group (see Table 3).
Notably, 4 of 13 serotypes included in PCV13 (serotypes 1, 4, 5, and 7F) were not detected in the examined children. Additionally, the serotypes/serogroups included in PCV15 (22AF and 33AF/37), as well as PCV23 (9LN and 17F), were rarely detected. Conversely, there was a high detection rate of non-vaccine S. pneumoniae serovariants, including 15AF, 23A, 34, 35F/47F, and 6CD.
DISCUSSION
Summary of the primary study results
Over the period between 2016 and 2022, changes in the serotype structure of S. pneumoniae were observed among healthy, organized bacterial carriers under 6 years of age. There was a significant decrease in the proportion of serovariants included in available pneumococcal vaccines (PCV13, PCV15, PCV20, and PPSV23), with a simultaneous increase in the proportion of non-vaccine isolates. The prevalence of pneumococcal carriage exhibited a decrease from 27.3% to 17.3% between 2016 and 2018, followed by an increase to 25.6% by 2022.
Discussion of the primary study results
Microbiological monitoring of the prevalence and serotype spectrum of circulating S. pneumoniae strains is needed both for predicting the effectiveness of immunization and for monitoring the ongoing “serotype substitution” [11]. A typical example of “serotype substitution” is the increase in the incidence of invasive forms of pneumococcal infection caused by serotype 19A in children vaccinated with PCV7 and PCV10 [12]. Moreover, the release of PCV13 resulted in the global dissemination of non-PCV13 pneumococcal serovariants, including 22F, 12F, 33F, 24F, 15C, 15B, 23B, 10A, and 38 [13]. Recent studies conducted in Asian countries revealed the prevalence of non-PCV13 and non-vaccine types of S. pneumoniae in invasive (22F, 11A, 10A, 34, 23A, and 35B) [14] and non-invasive (15BC, 11AD, 10A, 23A, 34, 15AF, 21, 35B, 31, and 33FA/37) [4, 15] clinical forms of pneumococcal infection.
The studies conducted in various regions of the Russian Federation showed that the main serotypes/serogroups of S. pneumoniae in nasopharyngeal carriage in children were 15AF, 6, 11AD, 23A, 9LN, and 16F in recent years [16, 17]. The proportion of children with PCV13 serotypes decreased from 59.2% in 2016–2018 to 24.8% in 2020–2023, and the proportion with PCV20 decreased from 73.7% to 46.4%, respectively [16].
Our data indicate a significant decline in concordance of detected S. pneumoniae serotypes with the antigenic composition of PCV13, from 48.8% in 2016 [15] to 9.4% in 2022. Moreover, the most frequent non-PCV13 serotypes/serogroups among healthy organized children in Krasnoyarsk were 15BC, 11AD, and 10A. The main non-vaccine serotypes were 15AF, 6CD, 23A, and 35F/47F. The primary reservoir for non-PCV13 and non-vaccine types was children who received three doses in accordance with the national immunization schedule.
The serotype concordance of detected S. pneumoniae isolates with the PCV20 composition decreased by 36.5% (from 75.6% in 2016 to 39.1% in 2022).
CONCLUSION
Thus, the obtained data show that the circulating serotypes of S. pneumoniae do not correspond to the antigenic composition of the currently available pneumococcal conjugate vaccines in most cases. This discrepancy may result in increased incidence of various clinical forms of infection caused by non-vaccine pneumococcal serovariants. For more complete information, monitoring of serotypes and epidemic clones of S. pneumoniae is needed both at the regional and national levels.
ADDITIONAL INFORMATION
Funding source. The research was carried out as part of a multicenter international prospective epidemiological study of the characteristics of pneumococcal infection “SAPIENs” (2016–2018 and 2020–2022), sponsored by the Rostropovich–Vishnevskaya foundation “For the health of children”.
Competing interests. The authors declare that they have no competing interests.
Authors’ contribution. All authors made a substantial contribution to the conception of the article, acquisition, analysis, interpretation of the research data, drafting and revising the work, final approval of the version to be published and agree to be accountable for all aspects of the work. I.N. Protasova — microbiological research, data analysis, writing the text; I.V. Feldblium — concept of the study, editing; N.V. Bakhareva — organizing the collection material, data analysis, editing; L.V. Zinovieva — data collection; S.V. Sidorenko — study concept and design.
About the authors
Irina N. Protasova
Professor V.F. Voino-Yasenetsky Krasnoyarsk State Medical University
Author for correspondence.
Email: ovsyanka802@gmail.com
ORCID iD: 0000-0001-6521-8615
SPIN-code: 4599-4410
MD, Dr. Sci. (Medicine)
Russian Federation, KrasnoyarskIrina V. Feldblium
Perm State Medical University named after Academician E.A. Wagner
Email: irinablum@mail.ru
ORCID iD: 0000-0003-4398-5703
SPIN-code: 3394-9879
MD, Dr. Sci. (Medicine), Professor
Russian Federation, PermNatalia V. Bakhareva
Krasnoyarsk Regional Center for AIDS Prevention and Control
Email: bakhareva@kraszdrav.ru
ORCID iD: 0000-0003-2868-1509
Russian Federation, Krasnoyarsk
Ludmila V. Zinovieva
Krasnoyarsk City Children’s Hospital No. 8
Email: Lzinovieva@gdb8.ru
ORCID iD: 0009-0005-5176-6190
Russian Federation, Krasnoyarsk
Sergey V. Sidorenko
Children’s Scientific and Clinical Center for Infectious Diseases
Email: sidorserg@yandex.ru
ORCID iD: 0000-0003-3550-7875
SPIN-code: 7738-7060
Russian Federation, Saint Petersburg
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