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Letter to the Editor| Volume 86, ISSUE 2, P154-225, February 2023

Changes of coagulase-negative Staphylococci infections in children before and after the COVID-19 pandemic in Zhengzhou, China

  • Lifeng Li
    Correspondence
    Corresponding authors.
    Affiliations
    Henan International Joint Laboratory of Children's Infectious Diseases, Department of Neonatology, Henan Children's Hospital, Zhengzhou Children's Hospital, Children's Hospital Affiliated to Zhengzhou University, Zhengzhou, China
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  • Jiayue Ma
    Affiliations
    Henan International Joint Laboratory of Children's Infectious Diseases, Department of Neonatology, Henan Children's Hospital, Zhengzhou Children's Hospital, Children's Hospital Affiliated to Zhengzhou University, Zhengzhou, China
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  • Pengbo Guo
    Affiliations
    Henan International Joint Laboratory of Children's Infectious Diseases, Department of Neonatology, Henan Children's Hospital, Zhengzhou Children's Hospital, Children's Hospital Affiliated to Zhengzhou University, Zhengzhou, China
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  • Kaijie Gao
    Affiliations
    Zhengzhou Key Laboratory of Children's Infection and Immunity, Department of Laboratory Medicine, Henan Children's Hospital, Zhengzhou Children's Hospital, Children's Hospital Affiliated to Zhengzhou University, Zhengzhou, China
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  • Junmei Yang
    Affiliations
    Zhengzhou Key Laboratory of Children's Infection and Immunity, Department of Laboratory Medicine, Henan Children's Hospital, Zhengzhou Children's Hospital, Children's Hospital Affiliated to Zhengzhou University, Zhengzhou, China
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  • Huiqing Sun
    Correspondence
    Corresponding authors.
    Affiliations
    Henan International Joint Laboratory of Children's Infectious Diseases, Department of Neonatology, Henan Children's Hospital, Zhengzhou Children's Hospital, Children's Hospital Affiliated to Zhengzhou University, Zhengzhou, China
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Published:December 11, 2022DOI:https://doi.org/10.1016/j.jinf.2022.12.006
      Dear editor,
      We read with great interest the findings of Li et al.
      • Li Y.
      • Guo Y.
      • Duan Y.
      Changes in Streptococcus pneumoniae infection in children before and after the COVID-19 pandemic in Zhengzhou, China.
      and Zhou et al.
      • Zhou J.
      • Zhao P.
      • Nie M.
      • Gao K.
      • Yang J.
      • Sun J.
      Changes of Haemophilus influenzae infection in children before and after the COVID-19 pandemic, Henan, China.
      published in the Journal of infection, which reported a decline in Streptococcus pneumoniae and Haemophilus influenzae infections in children under the influence of COVID-19 pandemic. Li et al.
      • Li L.
      • Song C.
      • Li P.
      • Li Y.
      Changes of Escherichia coli infection in children before and after the COVID-19 pandemic in Zhengzhou, China.
      found that COVID-19 had a greater impact on Escherichia coli isolated from children with respiratory infections than children with digestive system infections. Decreased carbapenemase-producing Enterobacteriaceae incidence after COVID-19 pandemic was also reported by Duverger et al.
      • Duverger C.
      • Monteil C.
      • Souyri V.
      • Fournier S.
      Decrease of carbapenemase-producing Enterobacteriaceae incidence during the first year of the COVID-19 pandemic.
      However, there is no report focusing on the prevalence of coagulase-negative Staphylococci infections in children before and after COVID-19.
      Coagulase-positive Staphylococci (CoPS) and coagulase-negative Staphylococci (CoNS) are two major types of the genus Staphylococci, which has become a serious challenge to the global public health system due to increasing antibiotic resistance.
      • Michels R.
      • Last K.
      • Becker S.L.
      • Papan C.
      Update on coagulase-negative staphylococci-what the clinician should know.
      For a long time, studies have mainly focused on CoPS such as Staphylococcus aureus, while few research has focused on CoNS. People start to pay attention to CoNS with the increasing detection rates of CoNS in clinical practice e.g., blood cultures or other sterile samples.
      • Michels R.
      • Last K.
      • Becker S.L.
      • Papan C.
      Update on coagulase-negative staphylococci-what the clinician should know.
      ,
      • Becker K.
      • Both A.
      • Weißelberg S.
      • Heilmann C.
      • Rohde H.
      Emergence of coagulase-negative staphylococci.
      CoNS consists of a heterogeneous and ever-increasing group of species that colonize the skin and mucosa of their hosts, which could also cause invasive diseases including bloodstream infection, urinary tract infection, and endocarditis.
      • Becker K.
      • Both A.
      • Weißelberg S.
      • Heilmann C.
      • Rohde H.
      Emergence of coagulase-negative staphylococci.
      Common CoNS species include Staphylococcus epidermidis, Staphylococcus haemolyticus, Staphylococcus capitis, Staphylococcus hominis, etc.
      • Ye Y.
      • Tian Y.
      • Kong Y.
      • Ma J.
      • Shi G.
      Trends of antimicrobial susceptibility in clinically significant coagulase-negative staphylococci isolated from cerebrospinal fluid cultures in neurosurgical adults: a nine-year analysis.
      The COVID-19 pandemic has significantly changed human lifestyles worldwide. Infection prevention and control measures (hand hygiene, wearing masks and limitation of gatherings) were taken to control the spread of SARS-CoV-2. These management measures could also reduce the transmission of many other pathogens.
      • Li Y.
      • Guo Y.
      • Duan Y.
      Changes in Streptococcus pneumoniae infection in children before and after the COVID-19 pandemic in Zhengzhou, China.
      • Zhou J.
      • Zhao P.
      • Nie M.
      • Gao K.
      • Yang J.
      • Sun J.
      Changes of Haemophilus influenzae infection in children before and after the COVID-19 pandemic, Henan, China.
      • Li L.
      • Song C.
      • Li P.
      • Li Y.
      Changes of Escherichia coli infection in children before and after the COVID-19 pandemic in Zhengzhou, China.
      • Duverger C.
      • Monteil C.
      • Souyri V.
      • Fournier S.
      Decrease of carbapenemase-producing Enterobacteriaceae incidence during the first year of the COVID-19 pandemic.
      ,
      • Meyer Sauteur P.M.
      • Beeton M.L.
      • Uldum S.A.
      • et al.
      Mycoplasma pneumoniae detections before and during the COVID-19 pandemic: results of a global survey, 2017 to 2021.
      Therefore, analysis of the prevalence trend of CoNS infection in children before and after the COVID-19 pandemic would be important for the prevention and control of related infectious diseases.
      To evaluate the impact of COVID-19 on the epidemiological characteristics of CoNS infection in children, laboratory data were collected and analyzed for children with blood culture records in Henan Children's hospital from January 2018 to November 2022. The total numbers of blood culture cases, the total positive numbers and the total positive rates were analyzed (Fig. 1). A total of 98, 245 children were included (n = 22, 196 in 2018, n = 23, 047 in 2019, n = 15, 216 in 2020, n = 19,735 in 2021 and n = 18, 051 in 2022) (Fig. 1A). The total number of blood culture positive cases was 1, 410 (n = 421 in 2018, n = 353 in 2019, n = 223 in 2020, n = 195 in 2021 and n = 218 in 2022). Significant decrease in the total cases was found in 2020 (the first year of COVID-19 pandemic), which increased in 2021 and 2022, whereas the cases were still lower than that in 2018 and 2019. The positive cases and the total positive rates showed a decreasing trend from 2018 to 2021 (Fig. 1B). In 2022, there was a slight increase in the positive rates, but it was still lower than that before COVID-19. These results indicated significant impact of COVID-19 pandemic on the epidemiological characteristics of children with bloodstream infection.
      Fig 1
      Fig. 1The total number of cases and the number of positive cases (A), and the positive rates (B) in children with blood cultures from 2018–2022.
      Then, the culture-positive cases were analyzed to reveal the pathogen distribution with special focus on the epidemic trend of CoNS infection in children before and after the COVID-19 epidemic. The pathogens mainly included S. epidermidis, S. hominis, S. capitis, S. haemolyticus, S. aureus, E. coli, Enterococcus faecium, S. pneumoniae, Klebsiella pneumoniae, and Pseudomonas aeruginosa (Table 1). These pathogens accounted for more than 55% of the total pathogens detected. Among these pathogens, S. epidermidis and S. hominis accounted for a higher proportion. The positive cases (108 in 2018 and 15 in 2022) and the positive rates (25.65% in 2018 and 6.88% in 2022) of S. epidermidis showed continuous decrease before and after the COVID-19 pandemic (Fig. 2A). The positive cases (76 in 2018 and 16 in 2021) and the positive rates (18.05% in 2018 and 8.21% in 2021) of S. hominis decreased from 2018 to 2021, which increased slightly in 2022 (28 and 12.84%) (Fig. 2B). The proportion of S. haemolyticus and S. capitis was low, but reduced infection rates were indicated in 2020. E. coli also showed decreased positive rates from 2019 to 2022. The other pathogen showed no significant increase or decrease in the years analyzed. The main strains of CoNS were analyzed together (Fig. 2C), and the positive rates decreased from 2018 to 2022. In addition, all Staphylococcus detected were analyzed, which showed a decline trend from 2018 to 2021, but increased slightly in 2022 (Fig. 2D). According to the above analysis, significant effect of COVID-19 on the prevalence of CoNS infections especially S. epidermidis and S. hominis were indicated.
      Table 1The pathogen distribution in culture-positive children from 2018 to 2022.
      Pathogen2018 (n = 421)2019 (n = 353)2020 (n = 223)2021 (n = 195)2022 (n = 218)
      Staphylococcus epidermidis108 (25.65%)65 (18.41%)34 (15.25%)18 (9.23%)15 (6.88%)
      Staphylococcus hominis76 (18.05%)53 (15.01%)28 (12.56%)16 (8.21%)28 (12.84%)
      Staphylococcus haemolyticus16 (3.80%)11 (3.12%)3 (1.35%)8 (4.10%)4 (1.83%)
      Staphylococcus capitis5 (1.19%)7 (1.98%)4 (1.79%)6 (3.08%)3 (1.38%)
      Staphylococcus aureus16 (3.80%)27 (7.65%)26 (11.66%)18 (9.23%)31 (14.22%)
      Streptococcus pneumoniae25 (5.94%)23 (6.52%)9 (4.04%)16 (8.21%)11 (5.05%)
      Enterococcus faecium9 (2.14%)9 (2.55%)6 (2.69%)7 (3.59%)6 (2.75%)
      Pseudomonas aeruginosa8 (1.90%)7 (1.98%)2 (0.90%)5 (2.56%)5 (2.29%)
      E. coli21 (4.99%)42 (11.90%)24 (10.76%)16 (8.21%)16 (7.34%)
      Other pathogens137 (32.54%)109 (30.88%)87 (39.01%)85 (43.59%)99 (45.41%)
      Fig 2
      Fig. 2The number of cases and the positive rates of Staphylococcus epidermidis (A), Staphylococcus hominis (B), main coagulase-negative staphylococci (C), and total strains of the genus staphylococci (D) isolated from the blood of children from 2018–2022.
      In summary, our data indicated that the epidemiological characteristics of children with blood infections including total culture cases, the culture-positive cases, the positive rates and pathogen distribution were affected by COVID-19. The prevalence of CoNS infections especially S. epidermidis and S. hominis decreased gradually during the COVID-19 pandemic. As the COVID-19 pandemic eased, the infection of some pathogens may recover or increase. Hence, continuous surveillance with large samples is required to obtain the epidemiological features and provide evidence for the prevention and control of related infectious diseases.

      Declaration of Competing Interest

      The authors declare no conflict of interests.

      Acknowledgments

      This work was supported by grants from the National Natural Science Foundation of China (31900116) and the Medical Science and Technology Projects of Henan Province (LHGJ20190955).

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