Molecular and clinical epidemiology of carbapenem resistant Acinetobacter baumannii ST2 in Oceania: a multicountry cohort study

Sakiusa C Baleivanualala; Lupeoletalalelei Isaia; Swastika V Devi; Benjamin Howden; Claire L Gorrie; Silivia Matanitobua; Sajnel Sharma; Donald Wilson; Silpa Kumar; Komal Maharaj; Scott Beatson; Lusiana V Boseiwaqa; Kristin Dyet; John A Crump; Philip C Hill; James E Ussher

doi:10.1016/j.lanwpc.2023.100896

Molecular and clinical epidemiology of carbapenem resistant Acinetobacter baumannii ST2 in Oceania: a multicountry cohort study

Lancet Reg Health West Pac. 2023 Sep 22:40:100896. doi: 10.1016/j.lanwpc.2023.100896. eCollection 2023 Nov.

Authors

Sakiusa C Baleivanualala^{1

2

3}, Lupeoletalalelei Isaia^{1

3

4}, Swastika V Devi², Benjamin Howden^{5

6}, Claire L Gorrie^{5

6}, Silivia Matanitobua⁷, Sajnel Sharma⁸, Donald Wilson², Silpa Kumar⁸, Komal Maharaj⁸, Scott Beatson⁹, Lusiana V Boseiwaqa⁸, Kristin Dyet¹⁰, John A Crump¹¹, Philip C Hill^{3

11}, James E Ussher^{1

3

12}

Affiliations

¹ Department of Microbiology and Immunology, School of Biomedical Sciences, University of Otago, Dunedin 9054, New Zealand.
² College of Medicine, Nursing and Health Science, Fiji National University, Suva, Fiji.
³ Maurice Wilkins Centre for Molecular Biodiscovery, University of Auckland, Auckland 92019, New Zealand.
⁴ Tupua Tamasese Mea'ole Hospital, Apia, Samoa.
⁵ Microbiological Diagnostic Unit, Peter Doherty Institute for Infection & Immunity, University of Melbourne, Melbourne, Victoria 3000, Australia.
⁶ Department of Microbiology & Immunology, Peter Doherty Institute for Infection & Immunity, University of Melbourne, Melbourne, Victoria 3000, Australia.
⁷ Fiji Centre for Disease Control, Tamavua, Suva, Fiji.
⁸ Colonial War Memorial Hospital, Suva, Fiji.
⁹ Australian Infectious Diseases Research Centre, University of Queensland, Brisbane, Queensland 4072, Australia.
¹⁰ Institute of Environmental Science and Research Ltd., Porirua 5022, New Zealand.
¹¹ Otago Global Health Institute, University of Otago, Dunedin 9054, New Zealand.
¹² Southern Community Laboratories, Dunedin Hospital, Dunedin 9016, New Zealand.

Abstract

Background: Carbapenem resistant Acinetobacter baumannii (CRAb) is categorised by the World Health Organization (WHO) as a pathogen of critical concern. However, little is known about CRAb transmission within the Oceania region. This study addresses this knowledge gap by using molecular epidemiology to characterise the phylogenetic relationships of CRAb isolated in hospitals in Fiji, Samoa, and other countries within the Oceania region including Australia and New Zealand, and India from South Asia.

Methods: In this multicountry cohort study, we analysed clinical isolates of CRAb collected from the Colonial War Memorial Hospital (CWMH) in Fiji from January through December 2019 (n = 64) and Tupua Tamasese Mea'ole Hospital (TTMH) in Samoa from November 2017 through June 2021 (n = 32). All isolates were characterised using mass spectrometry, antimicrobial susceptibility testing, and whole-genome sequencing. For CWMH, data were collected on clinical and demographic characteristics of patients with CRAb, duration of hospital stay, mortality and assessing the appropriateness of meropenem use from the treated patients who had CRAb infections. To provide a broader geographical context, CRAb strains from Fiji and Samoa were compared with CRAb sequences from Australia collected in 2016-2018 (n = 22), New Zealand in 2018-2021 (n = 13), and India in 2019 (n = 58), a country which has close medical links with Fiji. Phylogenetic relationships of all these CRAb isolates were determined using differences in core genome SNPs.

Findings: Of CRAb isolates, 49 (77%) of 64 from Fiji and all 32 (100%) from Samoa belonged to CRAb sequence type 2 (ST2). All ST2 isolates from both countries harboured bla_OXA-23, bla_OXA-66 and ampC-₂ genes, mediating resistance to β-lactam antimicrobials, including cephalosporins and carbapenems. The bla_OXA-23 gene was associated with two copies of ISAba1 insertion element, forming the composite transposon Tn2006, on the chromosome. Two distinct clusters (group 1 and group 2) of CRAb ST2 were detected in Fiji. The first group shared common ancestral linkage to all CRAb ST2 collected from Fiji's historic outbreak in 2016/2017, Samoa, Australia and 54% of total New Zealand isolates; they formed a single cluster with a median (range) SNP difference of 13 (0-102). The second group shared common ancestral linkage to 3% of the total CRAb ST2 isolated from India. Fifty eight of the 64 patients with CRAb infections at the CWMH had their first positive CRAb sample collected 72 h or more following admission. Meropenem use was deemed inappropriate in 15 (48%) of the 31 patients that received treatment with meropenem in Fiji. Other strains of CRAb ST1, ST25, ST107, and ST1112 were also detected in Fiji.

Interpretation: We identified unrecognised outbreaks of CRAb ST2 in Fiji and Samoa that linked to strains in other parts of Oceania and South Asia. The existence of Tn2006, containing the bla_OXA-23 and ISAba1 insertion element, within CRAb ST2 from Fiji and Samoa indicates the potential for high mobility and dissemination. This raises concerns about unmitigated prolonged outbreaks of CRAb ST2 in the two major hospitals in Fiji and Samoa. Given the magnitude of this problem, there is a need to re-evaluate the current strategies used for infection prevention and control, antimicrobial stewardship, and public health measures locally and internationally. Moreover, a collaborative approach to AMR surveillance within the Oceania region with technical, management and budgetary support systems is required to prevent introduction and control transmission of these highly problematic strains within the island nation health systems.

Funding: This project was funded by an Otago Global Health Institute seed grant and Maurice Wilkins Centre of Research Excellence (CoREs) grant (SC0000169653, RO0000002300).

Keywords: Acinetobacter baumannii; Carbapenem resistance; Oceania; Sequence type 2; blaOXA-23.