Genomic Epidemiology of MRSA During Incarceration at a Large Inner-City Jail

Abstract

Background: Congregate settings, such as jails, may be a location where colonized detainees transmit methicillin-resistant Staphylococcus aureus (MRSA). We examined MRSA acquisition during incarceration and characterized the genomic epidemiology of MRSA entering the jail and isolated during incarceration.

Methods: Males incarcerated at the Cook County Jail were enrolled within 72 h of intake and MRSA surveillance cultures collected. Detainees in jail at Day 30 were re-cultured to determine MRSA acquisition. A survey was administered to identify acquisition predictors. Genomic sequencing of surveillance and clinical isolates was integrated with epidemiologic and jail location data to track MRSA transmission pathways.

Results: 800 males were enrolled; 19% MRSA colonized at intake. Of 184 who reached Day 30 visit, 12 acquired MRSA. Heroin use before entering (OR 3.67, P = .05) and sharing personal items during incarceration (OR = 4.92, P = .01) were predictors of acquisition. Sequenced clinical USA300 isolates (n = 112) were more genetically similar than diverse intake USA300 strains (P < .001), suggesting jail transmission. Four acquired colonization isolates were within 20 single-nucleotide variant (SNVs) of other isolates; 4 were within 20 SNVs of an intake isolate, 2 for an acquisition isolate, and 1 for a clinical isolate. Individuals with genetically similar isolates were more likely to have had overlapping stays in the same buildings.

Conclusion: There was a high MRSA burden entering jail. Genomic analysis of acquisition and clinical isolates suggests potential spread of incoming strains and networks of spread during incarceration, with spread often occurring among detainees housed in similar locations. Sharing personal items during incarceration is associated with MRSA acquisition and could be a focus for intervention.

Keywords: MRSA; Whole genome sequencing; jail.

Figure 1.

Whole-genome phylogeny of USA300 MRSA infection and colonization isolates in the jail. Recombination-masked whole-genome alignment was used to make a maximum likelihood phylogeny of intake colonization, jail-acquired colonization, and jail-onset infection collected from individuals in the jail and publically available genomes [23]. Tree is midpoint rooted. For samples in the current study, only a single isolate per individual was included, unless genomic analysis supported multiple isolates from an individual being associated with independent acquisition events (see Methods). Overall, jail isolates span the full diversity of the USA300 phylogeny, with intermixing of intake colonization, jail-acquired colonization, and jail-onset infection isolates. However, in the background of this diversity, clustering of isolates can be observed, particularly for jail-onset infections. Publicly available isolates span the diversity of the tree, but do not interrupt clusters of jail samples. Scale bar represents substitutions per site. One isolate with a long branch was removed for visualization purposes (see full USA300 tree in Supplementary Figure S8).

Figure 2.

Comparison of genetic diversity of intake colonization MRSA isolates versus jail-acquired colonization and jail-onset infection. To evaluate whether jail-acquired USA300 MRSA colonization and jail-onset USA300 MRSA infections were enriched for recent transmission events, their genetic diversity was compared to that of intake USA300 MRSA colonization by creating distributions of genetic distances to closest genetic neighbors (core genome size = 2.54 Mb). Closest-pair sources for intake USA300 MRSA colonization include other intake isolates (n = 100). Closest-pair sources for jail-acquired USA300 MRSA colonization (n = 9) and jail-onset USA300 MRSA infections (n = 113) included all isolate types (n = 239 sources including intake positive colonization, jail-onset infection, jail-acquired colonization, community-onset infection (n = 3), infections that occurred in 2015 but were in jail during the study period (n = 14)). Wilcoxon rank-sum test was used to make pairwise comparisons between the 3 sets—one-sided test for A and B, two-sided test for C. Comparisons are shown for (A) jail-onset infections versus intake colonization, (B) jail-acquired colonization versus intake colonization, and (C) jail-acquired colonization versus jail-onset infections. Histograms are overlapping, not stacked, and colors are blended in overlapping parts of distributions. Significance remained when controlling for the differences in number of possible pairs for intake colonization and jail-onset infections (see Supplementary Methods, Supplementary Figures S9).

Figure 3.

Individuals with closely related USA300 MRSA strains are more likely to reside in common jail locations and have longer length of stay. (A) Each square indicates the mean length of stay of unique individuals involved in a pair (y-axis) within the respective SNV distance range (x-axis). SNV distances ranges are inclusive. For A, B, and C, pairs involve a putative acquisition of USA300 MRSA (jail-acquired colonization or jail-onset infection) and a source. See distribution of length of stay in Supplementary Figure S11. (B) Each dot indicates the percentage of pairs related by the respective SNV distance that overlapped in the respective location (y-axis) in an epidemiologically relevant window. Sequential overlap indicates that 2 individuals were both in the same living unit at some point in their jail stay during an epidemiologically relevant window, but not necessarily at the same time. See Supplementary Figure 13 for results of permutation test. (C) Each dot indicates the mean time a pair of individuals related by the respective SNV distance overlapped in the jail, the same building, or the same living unit in an epidemiologically relevant window (see Supplementary Methods). See Supplementary Figure 14 to see the distribution of days overlapped in jail and in a particular building, and Supplementary Figure 15 for detailed results of permutation test. In panels B and C asterisks indicates significance by permutation test where 1 asterisk indicates significance at P < .05 and 2 asterisk indicates significance at P < .005.

Figure 4.

Overlap in buildings among individuals with closely related MRSA strains.Colors represent pairs of USA300 isolates (including a putative acquisition of colonization or infection and a source) genetically related at different SNV thresholds (ie, ≤10, ≤20, ≤40). Random (in gray) indicates all pairs of isolates and is shown to provide the baseline location sharing of pairs of individuals for each building regardless of genetic linkage. The x-axis indicates the different buildings male detainees could stay, labeled as cell-based (subscript c) or dorm-based building (subscript d). The y-axis indicates the percent of pairs that overlap in an epidemiologically relevant window in each building (See Supplementary Methods). Asterisks indicates significance by permutation test where 1 asterisk indicates significance at P < .05 and 2 asterisks indicates significance at P < .005 (see Supplementary Methods and Supplementary Figure S17 for results of permutation test).