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Letter to the Editor| Volume 86, ISSUE 3, P256-308, March 2023

Changes of Klebsiella pneumoniae infection and carbapenem resistance in ICU elderly infected patients before and after the COVID-19 pandemic in Zhengzhou, China

  • Author Footnotes
    1 These authors contributed equally to this work.
    Xianfei Ding
    Footnotes
    1 These authors contributed equally to this work.
    Affiliations
    General ICU, The First Affiliated Hospital of Zhengzhou University, Henan Key Laboratory of Critical Care Medicine, Zhengzhou Key Laboratory of Sepsis, Henan Engineering Research Center for Critical Care Medicine, Zhengzhou, Henan 450052, China
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  • Author Footnotes
    1 These authors contributed equally to this work.
    Huoyan Liang
    Footnotes
    1 These authors contributed equally to this work.
    Affiliations
    General ICU, The First Affiliated Hospital of Zhengzhou University, Henan Key Laboratory of Critical Care Medicine, Zhengzhou Key Laboratory of Sepsis, Henan Engineering Research Center for Critical Care Medicine, Zhengzhou, Henan 450052, China
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  • Author Footnotes
    1 These authors contributed equally to this work.
    Xueyan Qi
    Footnotes
    1 These authors contributed equally to this work.
    Affiliations
    General ICU, The First Affiliated Hospital of Zhengzhou University, Henan Key Laboratory of Critical Care Medicine, Zhengzhou Key Laboratory of Sepsis, Henan Engineering Research Center for Critical Care Medicine, Zhengzhou, Henan 450052, China
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  • Guiying Sun
    Affiliations
    Epidemiology and Statistics, College of Public Health, Zhengzhou University, Zhengzhou, Henan 450001, China
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  • Ming Cheng
    Affiliations
    Medical Information, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450052, China
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  • Min Feng
    Affiliations
    Department of Critical Care Medicine, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China
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  • Tongwen Sun
    Correspondence
    Corresponding author.
    Affiliations
    General ICU, The First Affiliated Hospital of Zhengzhou University, Henan Key Laboratory of Critical Care Medicine, Zhengzhou Key Laboratory of Sepsis, Henan Engineering Research Center for Critical Care Medicine, Zhengzhou, Henan 450052, China
    Search for articles by this author
  • Author Footnotes
    1 These authors contributed equally to this work.
Published:January 09, 2023DOI:https://doi.org/10.1016/j.jinf.2023.01.008
      Dear Editor,
      Recent articles suggested that Streptococcus pneumonia (S. pneumoniae), Haemophilus influenzae (H. influenzae) and Moraxella catarrhalis (M. catarrhalis) infections among children in Zhengzhou, China showed a decreasing trend during the COVID-19 pandemic.
      • 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-19pandemic, Henan, China.
      • Liang Y.
      • Qin X.
      • Hou G.
      • Zhang X.
      • Zhang W.
      Changes of Moraxella catarrhalis infection in children before and after the COVID-19 pandemic, Zhengzhou, China.
      Previous studies also reported changes in carbapenemase-producing Enterobacteriaceae and extended-spectrum beta-lactamase (ESBL) E. coli infections during the COVID-19 pandemic.
      • Lemenand O.
      • Coeffic T.
      • Thibaut S.
      • ColombCotinat M.
      • Caillon J.
      • Birgand G.
      • et al.
      Decreasing proportion of extended-spectrum beta-lactamaseamong E. coli infections during the COVID-19 pandemic in France.
      ,
      • Morris D.E.
      • Osman K.L.
      • Cleary D.W.
      • Clarke S.C.
      The characterization of Moraxella catarrhalis carried in the general population.
      However, Klebsiella pneumoniae (K. pneumoniae), especially carbapenem-resistance K. pneumonia (CRKP) infection, is the main cause of mortality among elderly in the ICU, and its’ impact during the COVID-19 pandemic has not been reported.
      K. pneumoniae is a Gram-negative pathogen associated with pneumonia, urinary tract infection, sepsis, wound infection, and meningitis.
      • Martin R.M.
      • Bachman M.A.
      Colonization, Infection, and the Accessory Genome of Klebsiella pneumoniae.
      K. pneumoniae naturally colonizes the nasopharyngeal and gastrointestinal tracts after infection. However, nasopharyngeal colonization was relatively low (maximum of 15%) compared with that of the gut (approximately 20%).
      • Gomez-Simmonds A.
      • Uhlemann A.C.
      Clinical implications of genomic adaptation and evolution of carbapenem-resistant Klebsiella pneumoniae.
      K. pneumoniae is usually susceptible to carbapenems, but more than 40% of clinical K. pneumoniae isolates collected from 30 medical centers in China were identified as CRKP in 2017. CRKP has emerged as a major worldwide human health threat, as CRKP infections are associated with high mortality and morbidity.
      • Hu Y.
      • Liu C.
      • Shen Z.
      • Zhou H.
      • Cao J.
      • Chen S.
      • et al.
      Prevalence, risk factors and molecular epidemiology of carbapenem-resistant Klebsiella pneumoniae in patients from Zhejiang, China, 2008-2018.
      Moreover, the morbidity and mortality rates for CRKP-infected patients in the ICU are much higher than the non-ICU patients. A previous study showed that nearly half of all K. pneumonia (45.7%) infections occurred in the elderly, and suggested that age is also an independent risk factor for CRKP, which may result from the decreased immune function of elderly patients.
      • Liu C.
      • Guo J.
      Hypervirulent Klebsiella pneumoniae (hypermucoviscous and aerobactin positive) infection over 6 years in the elderly in China: antimicrobial resistance patterns, molecular epidemiology and risk factor.
      Therefore, the prevention and control of K. pneumonia and CRKP infections in elderly ICU patients is a major public health concern worldwide.
      In this study, we assessed the positive rate, age, basic information and epidemic trend of K. pneumonia and CRKP infections in ICU elderly infected patients before and after the COVID-19 pandemic to provide a reference for hospital infection control and treatment of CRKP. The number of positive cases of K. pneumonia and CRKP infections among elderly (defined as more than 60 years old), in the stratified age groups of 60–70 years, 70–80 years and more than 80 years, were examined between January 1, 2018, and December 31, 2021, at the First Affiliated hospital of Zhengzhou University according to laboratory surveillance. The number of elderly with K. pneumonia and CRKP infections increased from 2018 to 2019, but showed a steady decline after the outbreak of COVID-19 in Zhengzhou, China. Additionally, K. pneumonia and CRKP infections showed an obvious seasonality from 2018 to 2019 before the COVID-19 pandemic, with the number of positive cases increasing in winter, but no seasonality was observed in 2020–2021 after the COVID-19 pandemic (Fig. 1A and 1C). Furthermore, the percentage of positive cases (positive cases/total cases) with K. pneumonia and CRKP infections showed an obvious seasonality from 2018 to 2019 before the pandemic, in which the percentage of positive cases was higher in winter, but the seasonality was inconspicuous from 2020 to 2021 after the COVID-19 pandemic (Fig. 1B and 1D). Interestingly, the number of positive cases of K. pneumonia and CRKP infections in 2021 was slightly lower than in 2020, which may be associated with the preventive and control measures of COVID-19 that resulted in a significant reduction in the number of elderly going to the hospital. Furthermore, both the number of positive cases of K. pneumonia and CRKP infections, as well as the percentage of positive cases of K. pneumonia infections rapidly increased owing to the COVID-19 outbreak in Zhengzhou from February to June 2021 (Fig. 1A–C). The percentage of positive cases of CRKP infections rapidly increased due to the COVID-19 outbreak in Zhengzhou between July and August 2021,and the large population mobility and increased transmissibility of COVID-19 may cause it's increased during the Chinese Spring Festival (Fig. 1D). Taken together, these results suggested that the COVID-19 pandemic could influence the infection status of K. pneumonia and CRKP infections.
      Fig 1
      Fig. 1(A) The number of positive infections of K. pneumoniae from January 2018 to December 2021. (B) The percentage of positive infections of K. pneumoniae from January 2018 to December 2021. (C) The number of positive infections of CRKP from January 2018 to December 2021. (D) The percentage of positive infections of CRKP from January 2018 to December 2021.
      Additionally, the number of elderly infected with K. pneumonia and CRKP in the ICU was the lowest in the >80 years age group, who only accounted for 23.3% and 24.5% of the total number of infected elderly ICU patients from 2018 to 2021, and was similar between the 60–70 years age group and the 70–80 years age group (Fig. 2A and 2C). However, among all age groups, the highest proportion of K. pneumonia and CRKP infections in the >80 years age group was 35.3% and 84%, respectively. Importantly, the number of infections showed a decreasing trend before and after the COVID-19 pandemic, particularly in the >80 years age group, but the percentage of positive cases showed an increasing trend in the elderly, especially, in the >80 years age group. This may like a report showed that although the number of positive cases with infections (i.e., the numerator) decreased, the extent of the decrease in the total number of tested patients (i.e., the denominator) was larger.
      • Hirabayashi A.
      • Kajihara T.
      • Yahara K.
      • Shibayama K.
      • Sugai M.
      Impact of the COVID-19 pandemic on the surveillance of antimicrobial resistance.
      Specifically, the decrease in the total number of tested patients would be because the increase in the number of new polymerase chain reaction-positive COVID-19 patients and hospitalized COVID-19 patients caused a decrease in the number of hospital admissions due to other diseases and increased the testing threshold due to the risk of transmission of COVID-19. Although the COVID-19 pandemic restrictions are completely lifted in some Chinese cities, the global pandemic continues and its prevention and control remains inadequate. Therefore, the long-term prevalence of K. pneumonia and CRKP infections in elderly ICU patients should be closely monitored. Moreover, ICU elderly infected patients, especially those >80 years old, should be aware of the risk of K. pneumoniae and CRKP infections.
      Fig 2
      Fig. 2(A) The number of positive infections of K. pneumoniae in different age groups from January 2018 to December 2021. (B) The percentage of positive infections of K. pneumoniae in different age groups from January 2018 to December 2021. (C) The number of positive infections of CRKP in different age groups from January 2018 to December 2021. (D) The percentage of positive infections of CRKP in different age groups from January 2018 to December 2021.
      In summary, this study suggested that K. pneumoniae and CRKP infections in ICU elderly infected patients had decreased during the COVID-19 pandemic. Monitoring epidemiological trends is important for preventing K. pneumoniae and CRKP infections in ICU elderly infected patients who are more than 80 years old.

      Declaration of Competing Interest

      None.

      Funding

      This study was supported by the Fund of National Natural Science Foundation of China (Grant No. U2004110, 82172129, 82202370);The central government guides local science and technology development funds (grant number Z20221343037); Medical Science and Technology Tackling Plan Provincial and Ministerial Major Projects of Henan Province (Grant No. SBGJ202101015); The Excellent Youth Science Foundation of Henan Province; The 2021 youth talent promotion project in Henan Province (Grant No.2021HYTP053), and 2021 joint construction project of Henan Medical Science and technology breakthrough plan (Grant No. LHGJ20210299).

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