Expansion of healthcare-associated hypervirulent KPC-2-producing Klebsiella pneumoniae ST11/KL64 beyond hospital settings

Fernanda Esposito; Brenda Cardoso; Fábio P Sellera; Elder Sano; Danny Fuentes-Castillo; Herrison Fontana; Bruna Fuga; Quézia Moura; Maria I Z Sato; Carlos J Brandão; Nilton Lincopan

doi:10.1016/j.onehlt.2023.100594

Expansion of healthcare-associated hypervirulent KPC-2-producing Klebsiella pneumoniae ST11/KL64 beyond hospital settings

One Health. 2023 Jun 26:17:100594. doi: 10.1016/j.onehlt.2023.100594. eCollection 2023 Dec.

Authors

Fernanda Esposito^{1

2}, Brenda Cardoso^{2

3}, Fábio P Sellera^{2

4

5}, Elder Sano^{2

3}, Danny Fuentes-Castillo^{2

6}, Herrison Fontana^{1

2}, Bruna Fuga^{1

2

3}, Quézia Moura⁷, Maria I Z Sato⁸, Carlos J Brandão⁸, Nilton Lincopan^{1

2

3}

Affiliations

¹ Department of Clinical Analysis, School of Pharmacy, University of São Paulo, São Paulo, Brazil.
² One Health Brazilian Resistance Project (OneBR), Brazil.
³ Department of Microbiology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, Brazil.
⁴ Department of Internal Medicine, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, Brazil.
⁵ School of Veterinary Medicine, Metropolitan University of Santos, Santos, Brazil.
⁶ Departamento de Patología y Medicina Preventiva, Facultad de Ciencias Veterinarias, Universidad de Concepción, Chillán, Chile.
⁷ Federal Institute of Education Science and Technology of Espírito Santo, Vila Velha, Brazil.
⁸ Environmental Company of São Paulo State (CETESB), São Paulo, Brazil.

Abstract

The spread of carbapenemase-producing Klebsiella pneumoniae beyond hospital settings is a global critical issue within a public health and One Health perspective. Another worrisome concern is the convergence of virulence and resistance in healthcare-associated lineages of K. pneumoniae leading to unfavorable clinical outcomes. During a surveillance study of WHO critical priority pathogens circulating in an impacted urban river in São Paulo, Brazil, we isolate two hypermucoviscous and multidrug-resistant K. pneumoniae strains (PINH-4250 and PINH-4900) from two different locations near to medical centers. Genomic investigation revealed that both strains belonged to the global high-risk sequence type (ST) ST11, carrying the bla_KPC-2 carbapenemase gene, besides other medically important antimicrobial resistance determinants. A broad virulome was predicted and associated with hypervirulent behavior in the Galleria mellonella infection model. Comparative phylogenomic analysis of PINH-4250 and PINH-4900 along to an international collection of publicly available genomes of K. pneumoniae ST11 revealed that both environmental strains were closely related to hospital-associated K. pneumoniae strains recovered from clinical samples between 2006 and 2018, in São Paulo city. Our findings support that healthcare-associated KPC-2-positive K. pneumoniae of ST11 clone has successfully expanded beyond hospital settings. In summary, aquatic environments can become potential sources of international clones of K. pneumoniae displaying carbapenem resistance and hypervirulent behaviors, which is a critical issue within a One Health perspective.

Keywords: Carbapenems; Enterobacterales; Environmental dissemination; Genomic surveillance; One Health; Resistome; Virulome; WHO critical priority pathogens.