Serotype distribution and antimicrobial resistance of pediatric <i>Streptococcus pneumoniae</i> isolated from inpatients and outpatients at Beijing Children's Hospital

Lyu, Shuang; Shi, Wei; Dong, Fang; Xu, Bao Ping; Liu, Gang; Wang, Quan; Yao, Kai Hu; Yang, Yong Hong

doi:10.1016/j.bjid.2024.103734

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Original Article • Braz J Infect Dis 28 (2) • 2024 • https://doi.org/10.1016/j.bjid.2024.103734 copy

Serotype distribution and antimicrobial resistance of pediatric Streptococcus pneumoniae isolated from inpatients and outpatients at Beijing Children's Hospital

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

Background

Understanding the epidemiology of Streptococcus pneumoniae (S. pneumoniae) isolates is important for pneumonia treatment and prevention. This research aimed to explore the epidemiological characteristics of S. pneumoniae isolated from pediatric inpatients and outpatients during the same period.

Methods

S. pneumoniae were isolated from unsterile samples of inpatients and outpatients younger than five years old between March 2013 and February 2014. The serotypes were determined using diagnostic pneumococcal antisera. The resistance of each strain to 13 antibiotics was tested using either the E-test or the disc diffusion method. The Sequence Types (STs) were analyzed via Multilocus Sequence Typing (MLST).

Results

The dominant serotypes obtained from inpatients were 19F (32.9 %), 19A (20.7 %), 23F (10.7 %), 6A (10.0 %), and 14 (8.6 %), while those from outpatients were 19F (13.6 %), 23F (12.9 %), 6A (10.0 %), 6B (10.0 %), and 19A (7.9 %). The coverage rates of 13-valent Pneumococcal Conjugate Vaccine (PCV) formulations were high in both groups. The nonsusceptibility to penicillin, cefuroxime, imipenem, erythromycin, and trimethoprim-sulfamethoxazole among the inpatient isolates was 7.1 %, 92.8 %, 65.7 %, 100 %, and 85.0 %, respectively, while that among the outpatient isolates was 0.7 %, 50.0 %, 38.6 %, 96.4 %, and 65.7 %, respectively. There were 45 and 81 STs detected from the pneumococci isolated from inpatients and outpatients, respectively. CC271 was common among both inpatients and outpatients (43.6 % and 14.3 %).

Conclusions

Pneumococcal vaccine-related serotypes are prevalent among both inpatients and outpatients, especially among inpatients, who exhibit more severe antibiotic resistance. Therefore, universal immunization with PCV13 would decrease the hospitalization rate due to S. pneumoniae and the antibiotic resistance rate of S. pneumoniae.

Keywords
Streptococcus pneumoniae; Serotype distribution; Antibiotic resistance; Multilocus sequence typing; Inpatients and outpatients

Serotype	Inpatient isolates (n = 140)	Outpatient isolates (n = 140)
19F	46 (32.9 %)	19 (13.6 %)
23F	15 (10.7 %)	18 (12.9 %)
14	12 (8.6 %)	5 (3.6 %)
6B	4 (2.9 %)	14 (10.0 %)
9V	1 (0.7 %)	0
18C	0	1 (0.7 %)
7F	1 (0.7 %)	1 (0.7 %)
19A	29 (20.7 %)	11 (7.9 %)
6A	14 (10.0 %)	14 (10.0 %)
3	1 (0.7 %)	3 (2.1 %)
15B	9 (6.4 %)	5 (3.6 %)
34	0	7 (5.0 %)
Others	7 (5.0 %)^a a The other types include serotypes 15C (3), 6C (2), 42 (1), and 15F (1).	34 (24.3 %)^b b The other types include serotypes 6C (5), 23A (5), 15C (4), 42 (4), 15A (4), 29 (3), 13 (2), 20 (1), 23B (1), 24 (1), 31 (1), 19B (1), 11B (1), and 7C (1).
PCV7^c c The serotypes included in PCV7 are 4, 6B, 9 V, 14, 18C, 19F and 23F.	78 (55.7 %)	57 (40.7 %)
PCV10^d d The serotypes included in PCV10 are PCV7 plus serotypes 1, 5 and 7F.	79 (56.4 %)	58 (41.4 %)
PCV13^e e The serotypes included in PCV13 are PCV10 plus serotypes 3, 6A and 19A.	123 (87.9 %)	86 (61.4 %)
PCV20^f f The serotypes included in PCV20 are PCV13 plus serotypes 8, 10A, 11A, 12 F, 15B, 22 F, and 33 F.	133 (95.0 %)	99 (70.7 %)

Antimicrobial^a a Breakpoints were based on the 2015 criteria of the CLSI. The breakpoint of penicillin was based on the parenteral nonmeningitis (intermediate [4 mg/L], resistant [≥ 8 mg/L]), and oral nonmeningitis (intermediate [0.12‒1 mg/L], resistant [≥ 2 mg/L]). The breakpoint of ceftriaxone was based on only parenteral nonmeningitis (intermediate [2 mg/L], resistant [≥ 4 mg/L]). The breakpoint of amoxicillin-clavulanic acid was based on nonmeningitis (intermediate [2 mg/L], resistant [≥ 4 mg/L]). The breakpoint of cefuroxime was based on parenteral nonmeningitis (intermediate [2 mg/L], resistant [≥ 4 mg/L]). The breakpoint of cefaclor was (intermediate [2 mg/L], resistant [≥ 4 mg/L]). The breakpoint of vancomycin was defined as susceptibility ≤ 1 mg/L. The breakpoint of linezolid was defined as susceptibility ≤ 2 mg/L. The breakpoint of erythromycin was (intermediate [0.5 mg/L], resistant [≥ 1 mg/L]). The breakpoint of levofloxacin was (intermediate [14‒16 mg/L], resistant [≤ 13 mg/L]). The breakpoint of tetracycline was (intermediate [25‒27 mg/L], resistant [≤ 24 mg/L]). The breakpoint of chloramphenicol was defined as resistant [≤ 20 mg/L]. The breakpoint of trimethoprim-sulfamethoxazole was (intermediate [16‒18 mg/L], resistant [≤ 15 mg/L]).	Inpatient isolates (n = 140)	Outpatient solates (n = 140)
Penicillin
Parenteral nonmeningitis
R%	2.1	0.7
I%	5	0
Oral nonmeningitis
R%	40.0	20.7
I%	54.3	38.6
MIC range (mg/L)	0.016‒12	0.004‒6
MIC₅₀ (mg/L)	1	0.5
MIC₉₀ (mg/L)	2	1.5
Amoxicillin-clavulanic acid
R%	0.7	0
I%	6.4	0.7
MIC range (mg/L)	0.016‒12	0.016‒3
MIC₅₀ (mg/L)	1	0.38
MIC₉₀ (mg/L)	2	1.5
Cefuroxime
R%	87.1	43.6
I%	5.7	6.4
MIC range (mg/L)	0.023‒48	0.016‒12
MIC₅₀ (mg/L)	3	0.5
MIC₉₀ (mg/L)	8	4
Cefaclor
R%	90.7	51.4
I%	2.9	2.1
MIC range (mg/L)	0.19->256	0.125->256
MIC₅₀ (mg/L)	24	3
MIC₉₀ (mg/L)	64	96
Ceftriaxone
R%	1.4	0.7
I%	17.9	10.7
MIC range (mg/L)	0.012‒4	0.006‒3
MIC₅₀ (mg/L)	0.75	0.38
MIC₉₀ (mg/L)	1.5	1.5
Imipenem
R%	0.7	0
I%	65	38.6
MIC range (mg/L)	0.008‒2	0.004‒0.38
MIC₅₀ (mg/L)	0.19	0.094
MIC₉₀ (mg/L)	0.25	0.25
Vancomycin
MIC range (mg/L)	0.19‒0.5	0.25‒1
MIC₅₀ (mg/L)	0.5	0.5
MIC₉₀ (mg/L)	0.5	0.5
Linezolid
MIC range (mg/L)	0.38‒2	0.25‒2
MIC₅₀ (mg/L)	0.75	1
MIC₉₀ (mg/L)	1	1.5
Levofloxacin
MIC range (mg/L)	0.38‒2	0.38‒2
MIC₅₀ (mg/L)	0.75	0.75
MIC₉₀ (mg/L)	1	1
Erythromycin
R%	100	96.4
MIC range (mg/L)	4‒>256	0.094‒256
MIC₅₀ (mg/L)	>256	>256
MIC₉₀ (mg/L)	>256	>256
Tetracycline
R%	92.9	93.6
I%	4.2	1.4
Chloramphenicol
R%	4.3	10.7
Trimethoprim-sulfamethoxazole
R%	85	65.7
I%	2.1	11.4

Class of antibiotic	Resistance pattern^a a The breakpoint of penicillin was based on the parenteral nonmeningitis.	Inpatient isolates (n = 140)	Outpatients’ isolates (n = 140)
5	Macrolides/ β-lactams/ Tetracyclines/ Chloramphenicols/ Sulfonamides	3 (2.1 %)	7 (5.0)
4	Macrolides/ Tetracyclines/ Chloramphenicols/ Sulfonamides	1 (0.7 %)	5 (3.6 %)
	Macrolides / β-lactams/ Tetracyclines/ Sulfonamides	109 (77.9 %)	52 (37.1 %)
	Macrolides/ β-lactams/ Tetracyclines/ Chloramphenicols	1 (0.7 %)	0
	Macrolides/ β-lactams/ Sulfonamides/ Chloramphenicols	1 (0.7 %)	0
3	Macrolides/ β-lactams/ Tetracyclines	7 (5.0 %)	9 (6.4 %)
	Macrolides/ β-lactams/ Sulfonamides	3 (2.1 %)	3 (2.1 %)
	Macrolides/tetracyclines/sulfonamides	4 (2.9 %)	40 (28.6 %)
	Macrolides/ Tetracyclines/ Chloramphenicols	0	3 (2.1 %)
Total	‒	129 (92.1 %)	119 (85.0 %)

MLST	Inpatient isolates (n = 140)	Outpatient isolates (n = 140)
271	34 (24.3 %)	11 (7.9 %)
320	27 (19.3 %)	9 (6.4 %)
81	10 (7.1 %)	12 (8.6 %)
876	10 (7.1 %)	3 (2.1 %)
3397	8 (5.7 %)	6 (4.3 %)
Others	51 (36.4 %)	99 (70.7 %)

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E-mail: bjid@bjid.org.br

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[1] ⁎ Corresponding authors. yyh628628@sina.com (K.H. Yao), yaokaihu@bch.com.cn (Y.H. Yang)