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Bacterial resistance surveillance is a critical aspect of understanding the changes in drug-resistant bacteria and controlling their further spread. The surveillance results for non-duplicated clinical isolates collected from 71 hospitals in China by China Antimicrobial Surveillance Network (CHINET) in 2022 will be presented in this study (1). Species identification was conducted at each participating hospital and later verified by the central laboratory using matrix-assisted laser desorption ionisation-time of flight mass spectrometry (Bio-Mérieux, Marcy I'Etoile, France). Non-sterile body fluid samples containing coagulase-negative staphylococci andStreptococcus viridanswere excluded from this study.
Antimicrobial susceptibility testing was performed according to the Clinical and Laboratory Standards Institute (CLSI) (2), the European Committee on Antimicrobial Susceptibility Testing (3), and US Food and Drug Administration (4) 2022 breakpoints. Quality control for the drug susceptibility testing involved the use of standard strains, includingStaphylococcus aureusATCC 25923 and ATCC 29213,Escherichia coliATCC 25922,Pseudomonas aeruginosaATCC 27853,Streptococcus pneumoniaeATCC 49619,Enterococcus faecalisATCC 29212, andHaemophilus influenzaeATCC 49247.
A total of 339,513 clinical isolates were collected in 2022, with Gram-positive and Gram-negative bacteria accounting for 29.0% and 71.0% of the isolates, respectively. Inpatient and outpatient isolates accounted for 88.5% and 11.5%, respectively. The samples included 38.6% from respiratory secretions (e.g., sputum), 20.7% from urine, 14.4% from blood, 6.6% from wound pus, 6.6% from sterile body fluids (e.g., cerebrospinal fluid), 1.0% from genital secretions, 1.2% from feces, and 10.9% from other sources.Enterobacteralesaccounted for 43.7% of all isolates, with the three most common isolates beingE. coli(42.8%),Klebsiella pneumoniae(32.0%), andEnterobacter cloacae(6.4%). Non-fermentable sugar gram-negative bacilli accounted for 23.1% of isolates, with the top three isolates beingPseudomonasaeruginosa(34.8%),Acinetobacter baumannii(32.5%), andStenotrophomonas maltophilia(11.6%). The most common Gram-positive bacteria wereS.aureus(32.6%),E. faecalis(14.9%),E. faecium(12.4%), andS. pneumoniae(9.1%). The distribution of the main bacterial strains is shown inTable 1.
Organism No. of strains Percentage (%) E. coli 63,459 18.7 Klebsiellaspp. 54,785 16.1 S. aureus ss. aureus 32,159 9.5 Acinetobacterspp. 29,069 8.6 Enterococcusspp. 29,050 8.6 P. aeruginosa 27,257 8.0 Coagulase-negative Staphylococcus(from blood, CSF and other sterile body fluid) 16,186 4.8 H. influenzae 11,439 3.4 Enterobacterspp. 10,357 3.1 S. maltophilia 9,097 2.7 S. pneumoniae 8,964 2.6 β-hemolytic Streptococcus 7,201 2.1 Moraxella catarrhalis 6,588 1.9 Proteus spp. 5,994 1.8 Serratia spp. 3,821 1.1 S. viridans (from blood, CSF and other sterile body fluids) 3,840 1.1 Salmonellaspp. 3,621 1.1 Citrobacterspp. 3,100 0.9 Burkholderiaspp. 2,812 0.8 Morganellaspp. 1,637 0.5 Pseudomonasspp.(exceptP. aeruginosa) 1,118 0.3 Aeromonasspp. 1,111 0.3 Haemophilusspp.(exceptH. influenzae) 621 0.2 Achromobacter xylosoxidans ss. xylosoxidans 498 0.1 Raoultella ornitholytica 466 0.1 Elizabethkingia meningosepticum 437 0.1 Chryseobacterium indologenes 389 0.1 Haemophilus parainfluenzae 339 0.1 Neisseriaspp. 310 0.1 Providenciaspp. 358 0.1 Helicobacter nemestrinae 291 0.1 Ralstoniaspp. 276 0.1 Brucellaspp. 200 0.1 Listeriaspp. 137 0 Shigellaspp. 39 0 Others* 2,487 0.7 Total 339,513 100 *IncludingPantoeaspp.,Comamonasspp.,Chryseobacteriumspp.,Bordetellaspp.,Brevundimonasspp., andVibriospp., et al. Table 1.Distribution of bacterial species from major hospitals — China, 2022.
The detection rate of methicillin-resistantS. aureus(MRSA) was 28.7%, while the detection rate of methicillin-resistantS. epidermidis(MRSE) was 82.2%. Among methicillin-resistant strains (MRCNS) in otherStaphylococcusspp. (excludingS. pseudintermediusandS. schleiferi), the detection rate was 77.6%. The resistance rates of MRSA, MRSE, and MRCNS to macrolides, aminoglycosides, rifampicin, and quinolones were significantly higher than those of methicillin-susceptible strains (MSSA, MSSE, and MSCNS). However, the resistance rate to trimethoprim-sulfamethoxazole was lower in MRSA (6.4%) compared to MSSA (12.4%). Conversely, the resistance rate was significantly higher in MRSE (51.8%) compared to MRCNS (29.1%). Moreover, the resistance rate to clindamycin was lower in both MRSE and MRCNS (32.7% and 37.9%) compared to MRSA (53.6%). No strains ofStaphylococcusspp. exhibited resistance to vancomycin or norvancomycin, and only a few methicillin-resistant coagulase-negativeStaphylococcus spp. strains were resistant to teicoplanin or linezolid (Table 2).
Antimicrobial agent MRSA MSSA MRSE MSSE MRCNS MSCNS (n=9,116) (n=22,673) (n=5,353) (n=1,162) (n=6,433) (n=1,854) R S R S R S R S R S R S Penicillin G 100.0 0 87.5 12.5 100.0 0 71.8 28.2 100.0 0 66.0 34.0 Oxacillin 100.0 0 0 100.0 100.0 0 0 100.0 100.0 0 0 100.0 Gentamicin 14.6 83.7 5.9 91.1 20.2 69.3 2.8 92.5 22.2 67.2 1.0 97.6 Clindamycin 53.6 45.9 15.9 83.4 32.7 66.2 10.3 88.4 37.9 60.4 10.4 88.8 Erythromycin 73.4 25.8 44.8 53.8 75.1 23.5 64.8 34.8 85.5 13.5 54.3 44.3 Vancomycin 0 100.0 0 100.0 0 100.0 0 100.0 0 100.0 0 100.0 Norvancomycin 0 100.0 0 100.0 0 100.0 0 100.0 0 100.0 0 100.0 Teicoplanin 0.1 99.9 0 100.0 0.3 99.2 0.2 99.8 0.3 99.4 0.3 99.2 Linezolid 0 100.0 0 100.0 1.1 98.9 0.1 99.9 1.6 98.4 0 100.0 Tigecycline 0.2 99.8 0.1 99.9 0 100.0 0 99.9 0 100.0 0 100.0 Rifampin 3.7 93.9 0.6 98.6 8.5 90.9 1.0 99.0 10.0 89.4 0.5 99.3 Levofloxacin 23.8 75.3 8.3 91.0 53.1 44.5 14.9 83.5 65.8 32.5 4.6 94.6 Trimethoprim-sulfamethoxazole 6.4 93.6 12.4 87.6 51.8 48.1 26.9 72.7 29.1 70.7 6.5 93.5 Abbreviation: R=resistant; S=susceptible; MRSA=methicillin-resistantStaphylococcus aureus; MSSA=methicillin-sensitiveStaphylococcus aureus; MRSE=methicillin-resistantStaphylococcus epidermidis; MSSE=methicillin-sensitiveStaphylococcus epidermidis; MRCNS=methicillin-resistant coagulase-negativeStaphylococci; MSCNS=methicillin-sensitive coagulase-negativeStaphylococci. Table 2.Resistance and sensitivity rates ofStaphylococcusspp. to antimicrobial agents from major hospitals — China, 2022 (%).
E. faecalisexhibited significantly lower resistance rates to most tested antimicrobial agents compared toE.faecium. However,E. faeciumshowed higher resistance rates to ampicillin (90.8%) and nitrofurantoin (46.6%).E. faeciumhad lower resistance rates to ampicillin (2.4%), nitrofurantoin (1.6%), and fosfomycin (4.5%). Both species were highly susceptible (>99%) to tigecycline, while approximately 34.6% and 39.3% of strains were resistant to high concentrations of gentamicin. Some strains of bothE. faecalisandE. faeciumshowed resistance to vancomycin, teicoplanin, and linezolid. The prevalence of linezolid-resistant strains was higher inE. faecalis(3.5%) compared toE. faecium(0.6%), whereas vancomycin-resistant strains were more frequent inE. faecium(2.2%) than inE. faecalis(0.1%) (
Supplementary Table S1 ).Among the 7,222 strains ofStreptococcus pneumoniaeisolated from non-meningitis specimens of pediatric patients, the detection rates of penicillin-susceptibleS. pneumoniae(PSSP), penicillin-intermediateS. pneumoniae(PISP), and penicillin-resistantS. pneumoniae(PRSP) were 94.4%, 5.2%, and 0.3%, respectively. Similarly, among the 1,419 strains isolated from non-meningitis specimens of adult patients, the detection rates of PSSP, PISP, and PRSP were 95.4%, 3.4%, and 1.2%, respectively. Antimicrobial susceptibility testing revealed high rates of resistance to erythromycin, clindamycin, and trimethoprim-sulfamethoxazole (>54%) in both pediatric and adult strains. Levofloxacin and moxifloxacin resistance rates were lower in pediatric PSSP strains (0.1%–0.3%) compared to adult strains (2.3%–11.8%). No strains showed resistance to vancomycin or linezolid (
Supplementary Table S2 ).3,474 strains ofStreptococcus viridanswere isolated from sterile body fluid samples such as blood or cerebrospinal fluid. With the exception of S.viridans, which displayed a penicillin resistance rate of 6.8%, no penicillin-resistant strains were found in the other groups. The resistance rate to erythromycin and clindamycin exceeded 50% in all groups ofStreptococcusspp. Except for group B β-Streptococcus agalactiaeandS. viridans, which exhibited resistance rates of 43.4% and 12.3%, respectively, all other β-Streptococcushaemolyticusspp. displayed high susceptibility to levofloxacin, with resistance rates ranging from 0% to 2.3%. No strains resistant to vancomycin or linezolid were detected. (
Supplementary Table S3 ).The resistance rates ofE. colito ceftriaxone, cefuroxime, piperacillin, trimethoprim-sulfamethoxazole, ciprofloxacin, and levofloxacin were all above 50%. The resistance rates ofEnterobacteralesto the three carbapenems were generally low, except forKlebsiellaspp. which had resistance rates ranging from 20.4% to 21.9%. Most otherEnterobacteraleshad resistance rates of 12.5% or less.Enterobacteralesshowed higher susceptibility to amikacin, with resistance rates ranging from 1.5% to 13.7%. With the exception ofEnterobacteralesandCitrobacterspp., which had sensitivity rates of 72.4% and 82.6%, respectively, to ceftazidime-avibactam, otherEnterobacteraleswere sensitive to ceftazidime-avibactam with a range of 93.5%–97.4%. Most otherEnterobacteraleswere highly susceptible to tigecycline, mucin, and polymyxin B, with resistance rates ranging from 0.1% to 12.6% (Table 3).
Antimicrobial agent E. coli
(n=63,459)Klebsiellaspp. (n=54,785) Enterobacterspp. (n=10,357) Proteusspp.
(n=59,94)Serratiaspp. (n=3,821) Citrobacterspp. (n=3,100) Morganellaspp. (n=1,637) R S R S R S R S R S R S R S Amikacin 1.9 97.7 13.7 86.1 1.6 97.8 2.2 97.2 1.6 98.1 1.5 98.4 1.7 97.8 Gentamicin 34.5 64.6 25.1 73.9 13.4 84.6 19.8 63 8.2 91.1 13.0 85.8 18.3 76.7 Imipenem 1.9 97.9 20.4 78.6 9.7 88.6 11.5 65.6 5.7 91.0 7.5 91.3 23.0 40.8 Meropenem 2.0 97.9 21.9 77.7 9.7 89.5 1.0 98.5 5.1 94.5 7.9 91.7 1.9 97.5 Ertapenem 1.8 98.0 20.4 79.2 12.5 85.2 0.6 98.7 4.8 94.9 7.2 92.6 1.9 97.6 Cefepime 25.5 65.7 29.3 68.3 16.7 76.9 8.0 82.3 8.2 87.2 11.7 84.8 3.6 90.5 Ceftazidime 22.8 69.8 32.4 65.2 34.0 64.3 6.2 92.0 8.4 90.3 28.6 69.6 14.8 80.9 Ceftazidime-avibactam 6.5 93.5 6.2 93.8 27.6 72.4 2.7 97.3 7.1 92.9 17.4 82.6 2.6 97.4 Ceftriaxone 51.3 48.4 39.1 60.6 39.9 58.8 32.4 66.1 19.0 79.9 35.2 64.3 16.0 79.2 Cefoperazone-sulbactam 5.7 87.2 24.9 70.3 17.1 75 0.9 97.4 7.7 88.0 10.7 81.6 3.3 89.6 Cefoxitin 10.2 84.4 28.2 69.8 93.6 5.6 6.5 88.2 26.8 30.3 54.1 40.3 14.2 42.7 Cefuroxime 53.1 44.0 42.8 55.0 47.1 34.8 49.0 50.0 89.2 2.4 37.6 56.6 84.0 5.1 Cefazolin 57.7 42.4 49.2 50.9 93.8 6.1 54.8 45.2 98.3 1.7 66.9 33.1 98.2 1.8 Piperacillin 76.8 19.6 50.4 41.3 40.5 57.2 34.7 58.9 15.7 83.3 48.9 44.3 34.2 61.2 Piperacillin-tazobactam 8 88.5 29.2 65.9 27.5 68.3 1.8 97.3 7.9 89.8 22.1 69.8 7.2 89.1 Ampicillin-sulbactam 35.9 58.6 44.0 53.9 55.5 39.9 30.5 64.2 66.9 29.4 36.2 60.4 54.6 36.6 Ciprofloxacin 61.5 29.6 40.3 53.8 24.0 70.6 45.8 49.9 14.3 81.0 27.0 66.0 41.1 55.0 Levofloxacin 53.8 27.3 30.2 57.7 17.3 71.6 34.7 53.7 11.5 82.5 19.7 67.7 23.6 61.0 Trimethoprim-sulfamethoxazole 52.2 47.7 30.7 69.1 20.9 79.1 56.0 44.0 4.7 95.3 20.6 79.3 37.1 62.8 Tigecycline 0.1 99.4 2.6 92.1 1.9 95.1 12.6 25.0 0.5 94.7 0.6 96.8 9.6 69.3 Colistin 1.3 95.5 2.8 81.5 2.0 88.7 2.1 97.6 9.3 87.9 2.3 97.0 3.2 95.2 Polymyxin B 1.5 86.2 4.8 57.6 9.9 66.0 1.2 97.9 11.6 77.0 2.5 72.2 2.4 96.5 Abbreviation: R=resistant; S=susceptible. Table 3.Resistance and sensitivity rates ofEnterobacteralesto antimicrobial agents from major hospitals — China, 2022 (%) .
The rates of resistance ofPseudomonas aeruginosato imipenem and meropenem were 22.1% and 17.6%, respectively. For polymyxin B, colistin, amikacin, and ceftazidime-avibactam, the resistance rates were 0.5%, 1.7%, 3.5%, and 7.2%, respectively. The resistance rates ofPseudomonasaeruginosato piperacillin-tazobactam, cefoperazone-sulbactam, gentamicin, ciprofloxacin, levofloxacin, ceftazidime, cefepime, and piperacillin ranged from 7% to 20.1%. Similarly, resistance rates to imipenem and meropenem amongAcinetobacterspp. were 65.8% and 66.6%, with resistance rates of 1.6% to 2.3% for polymyxin B, colistin, and tigecycline. The resistance rates ofStenotrophomonas maltophiliato trimethoprim-sulfamethoxazole, minocycline, and levofloxacin were 6.4%, 1%, and 8.7%, respectively. ForBurkholderia cepacia, the resistance rates were 10.7%, 6.8%, 3.6%, and 4.3% to meropenem, ceftazidime, minocycline, and trimethoprim-sulfamethoxazole (
Supplementary Table S4 ).Among 11,439 strains ofHaemophilus influenzae, 76.7% were isolated from children, while 23.2% were from adults. The β-lactamase detection rates in pediatric and adult isolates were 70.3% and 56.2%, respectively. Most of theH. influenzaestrains showed high susceptibility to ceftriaxone, meropenem, levofloxacin, and chloramphenicol, with susceptibility rates ranging from 96.1% to 99.9%. However, pediatric isolates exhibited higher resistance than adult strains to ampicillin (76.5%vs. 63.1%), amoxicillin-clavulanic acid (14.0%vs. 4.8%), cefuroxime (53.9%vs. 27.4%), and trimethoprim-sulfamethoxazole (74.5%vs. 56.3%). Both pediatric and adult isolates showed similar resistance rates to ampicillin-sulbactam (34.5%vs. 34.6%) (
Supplementary Table S5 ). -
Currently, the production of Extended Spectrum Beta-Lactamases (ESBL) and carbapenemases is the most significant mechanism of resistance in Gram-negative bacteria, particularly inEnterobacterales. In this study, the prevalence of ceftriaxone or cefotaxime resistance inE. coli,K. pneumoniae, andP. mirabiliswas found to be 51%, 40.9%, and 36.6%, respectively. The widespread epidemic spread of ESBL-producing strains presents a major challenge for anti-infective therapy, forcing clinicians to resort to broad-spectrum antimicrobials like carbapenems (5-6). With the extensive use of carbapenems, the emergence of carbapenem-resistant Gram-negative bacteria under intense antimicrobial pressure has become a significant threat to global public health. Due to the frequent resistance of carbapenem-resistant Gram-negative bacilli to most commonly used antimicrobial agents, the selection of drugs for treating infections caused by these bacilli is limited, leading to high morbidity and mortality among affected patients (7).
Carbapenemase production is the predominant resistance mechanism inEnterobacteralesto carbapenems (8). Since various combinations of carbapenemase inhibitors exhibit different levels of inhibitory activity against different carbapenemases, this leads to divergent treatment regimens for infections caused by various drug-resistant bacteria (9). To address the significant challenges posed by carbapenem-resistant Gram-negative bacilli, Laboratories should perform susceptibility testing for effective antimicrobials (e.g., ceftazidime-avibactam, tigecycline, and polymyxin), carbapenemase phenotypic or genotypic testing, and combination drug susceptibility testing to support the development of accurate clinical anti-infective treatment regimens (10).
The mitigation of bacterial resistance represents a comprehensive endeavor, necessitating the implementation of traditional strategies. These include infection prevention and control, immunization, diminishing exposure to antimicrobial agents, reducing the misuse of these agents, and sustaining the research and development of novel antimicrobials. Crucially, establishing infrastructures to limit the epidemiological proliferation of drug-resistant bacteria is essential. This involves enhancing anti-infective treatment proficiency through education, standardizing antimicrobial susceptibility testing, and integrating various networks. These networks encompass the bacterial and fungal resistance surveillance network, the clinical usage surveillance network, and the hospital infection control network (11).
This study has two limitations. First, it was a passive surveillance study, mainly collecting results of routine antimicrobial susceptibility testing from different hospitals for analysis, and the types of antimicrobials tested were limited by the automated systems, which less often included new antimicrobials. Secondly, this study did not investigate the medical history to clarify whether it was the pathogen causing the infection or a colonising strain.
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The authors declare no competing interests.
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We would like to express our gratitude to the members of CHINET for their valuable contribution in collecting the isolates for this study.
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