Increased Proportions of Invasive Pneumococcal Disease Cases Among Adults Experiencing Homelessness Sets the Stage for New Serotype 4 Capsular-Switch Recombinants.

Abstract

The Centers for Disease Control and Prevention's Active Bacterial Core surveillance (ABCs) identified increased serotype 4 invasive pneumococcal disease (IPD), particularly among adults experiencing homelessness (AEH). We quantified increased proportions of IPD cases in AEH during 2016-2022. Employing genomic-based characterization of IPD isolates, we identified serotype-switch variants. Recombinational analyses were used to identify the genetic donor and recipient strain that generated a serotype 4 progeny strain. We performed phylogenetic analyses of the serotype 4 progeny and of the serotype 12F genetic recipient to determine genetic distances. We identified a cluster of 30 highly related (0-21 nucleotide differences) IPD isolates recovered during 2022-2023, corresponding to a serotype 4 capsular-switch variant. This strain arose through a multifragment recombination event between serotype 4/ST10172 and serotype 12F/ST220 parental strains. Twenty-five of the 30 cases occurred in Oregon. Of 29 cases with known residence status, 16 occurred in AEH. Variant emergence coincided with a 2.6-fold increase (57 to 148) of cases caused by the serotype 4/ST10172 donor lineage in 2022 compared to 2019 and its first appearance in Oregon. Most serotypes showed sequential increases of AEH IPD/all IPD ratios during 2016-2022 (eg, for all serotypes combined, 247/2198, 11.2% during 2022 compared to 405/5317, 7.6% for 2018-2019, P < .001). Serotypes 4 and 12F each caused more IPD than any other serotype in AEH during 2020-2022 (207 combined case isolates accounting for 38% of all IPD in AEH). Expansion and increased transmission of serotypes 4 and 12F among adults potentially led to recent genesis of an impactful hybrid serotype-switch variant.