Strong Homology Between Colonizing and Bloodstream Carbapenem-Resistant Acinetobacter Spp.: Implications for Empiric Antibiotic Therapy in Hematological Patients

Jia Li; Wenjing Guo; Jieru Wang; Xiaomeng Feng; Qingsong Lin; Yizhou Zheng; Fengkui Zhang; Yingchang Mi; Xiaofan Zhu; Erlie Jiang; Zhijian Xiao; Jianxiang Wang; Sizhou Feng

doi:10.2147/IDR.S458427

Strong Homology Between Colonizing and Bloodstream Carbapenem-Resistant Acinetobacter Spp.: Implications for Empiric Antibiotic Therapy in Hematological Patients

Infect Drug Resist. 2024 May 9:17:1827-1838. doi: 10.2147/IDR.S458427. eCollection 2024.

Authors

Jia Li^{1

2}, Wenjing Guo^{1

2}, Jieru Wang^{1

2}, Xiaomeng Feng^{1

2}, Qingsong Lin^#^{1

2}, Yizhou Zheng^{1

2}, Fengkui Zhang^{1

2}, Yingchang Mi^{1

2}, Xiaofan Zhu^{1

2}, Erlie Jiang^{1

2}, Zhijian Xiao^{1

2}, Jianxiang Wang^{1

2}, Sizhou Feng^#^{1

2}

Affiliations

¹ State Key Laboratory of Experimental Hematology, National Clinical Research Center for Blood Diseases, Haihe Laboratory of Cell Ecosystem, Institute of Hematology & Blood Diseases Hospital, Chinese Academy of Medical Sciences & Peking Union Medical College, Tianjin, 300020, People's Republic of China.
² Tianjin Institutes of Health Science, Tianjin, 301600, People's Republic of China.

^# Contributed equally.

Abstract

Objective: This study aimed to assess the impact of colonization status on the outcomes of Acinetobacter spp. bloodstream infection (BSI) and investigate the homology and within-host evolution between colonizing and bloodstream carbapenem-resistant Acinetobacter spp. (CRA) to inform antibiotic therapeutic decisions.

Methods: We analyzed clinical outcomes of 46 hematological patients with Acinetobacter spp. BSI and performed whole-genome sequencing on the remaining CRA isolates.

Results: Among the patients, 39.1% (n=18) had prior Acinetobacter spp. colonization. Colonized patients had higher rates of polymicrobial BSI (50.0% vs 21.4%, P=0.044) and CRA BSI (72.2% vs 17.9%, P<0.001), resulting in elevated inflammatory markers and increased 30-day mortality. Each of the eight pairs of the remaining respiratory colonizing and bloodstream CRA strains belonged to the same genomospecies. Each pair exhibited definitive agreement in at least 21 of the 22 most representative antibiotic susceptibility tests. The minimum spanning tree based on multilocus sequence typing (MLST) and phylogenetic trees based on MLST and single nucleotide polymorphism (SNP) all indicated that each pair shared the same minimum branch. Very few non-synonymous SNPs in genic regions were identified during the transition from respiratory colonization to bloodstream infection, with minimal changes in virulence genes. Homology analysis suggested that CRA BSI originated from colonizing isolates in the respiratory tract.

Conclusion: Strict infection control measures are needed to manage Acinetobacter spp. colonisation in hematological patients. Appropriate empirical therapy can be administered for suspected CRA BSI based on the antimicrobial minimum inhibitory concentration of CRA colonising the respiratory tract.

Keywords: Acinetobacter; bloodstream infections; carbapenem-resistant; colonization; homology; therapy.

Grants and funding

This work was supported by the Chinese Academy of Medical Sciences Innovation Fund for Medical Sciences (grant numbers 2021-I2M-1-017, 2021-I2M-C&T-B-080), and the Tianjin Municipal Science and Technology Commission Grant (grant number 21JCZDJC01170).