Longitudinal, strain-specific Staphylococcus aureus introduction and transmission events in households of children with community-associated meticillin-resistant S aureus skin and soft tissue infection: a prospective cohort study

Abstract

Background: Devising effective, targeted approaches to prevent recurrent meticillin-resistant Staphylococcus aureus (MRSA) skin and soft tissue infection requires an understanding of factors driving MRSA acquisition. We comprehensively defined household longitudinal, strain-level S aureus transmission dynamics in households of children with community-associated MRSA skin and soft tissue infection.

Methods: From 2012-15, otherwise healthy paediatric patients with culture-confirmed, community-onset MRSA infections were recruited for the Household Observation of MRSA in the Environment (HOME) prospective cohort study from hospitals and community practices in metropolitan St Louis (MO, USA). Children with health-care-related risk factors were excluded, as determined by evidence of recent hospital admission, an invasive medical device, or residence in a long-term care facility. Household contacts (individuals sleeping in the home ≥four nights per week) and indoor dogs and cats were also enrolled. A baseline visit took place at the index patient's primary home, followed by four quarterly visits over 12 months. At each visit, interviews were done and serial cultures were collected, to detect S aureus from three anatomic sites of household members, two anatomic sites on dogs and cats, and 21 environmental surfaces. Molecular typing was done by repetitive-sequence PCR to define distinct S aureus strains within each household. Longitudinal, multivariable generalised mixed-effects logistic regression models identified factors associated with S aureus acquisition.

Findings: Across household members, pets, and environmental surfaces, 1267 strain acquisition events were observed. Acquisitions were driven equally by 510 introductions of novel strains into households and 602 transmissions within households, each associated with distinct factors. Frequent handwashing decreased the likelihood of novel strain introduction into the household (odds ratio [OR] 0·86, credible interval [CrI] 0·74-1·01). Transmission recipients were less likely to own their homes (OR 0·77, CrI 0·63-0·94) and were more likely to share bedrooms with strain-colonised individuals (OR 1·33, CrI 1·12-1·58), live in homes with higher environmental S aureus contamination burden (OR 3·97, CrI 1·96-8·20), and report interval skin and soft tissue infection (OR 1·32, CrI 1·07-1·64). Transmission sources were more likely to share bath towels (OR 1·25, CrI 1·01-1·57). Pets were often transmission recipients, but rarely the sole transmission source.

Interpretation: The household environment plays a key role in transmission, a factor associated with skin and soft tissue infection. Future interventions should inclusively target household members and the environment, focusing on straightforward changes in hand hygiene and household sharing behaviours.

Funding: National Institutes of Health, Agency for Healthcare Research and Quality, Children's Discovery Institute, Burroughs Wellcome Foundation, Defense Advanced Research Projects Agency.

Figure 1.. Flow diagram of S. aureus strain acquisitions.

Across household members, pets, and environmental surfaces, a total of 1267 strain acquisition events were observed. Of these, 510 were novel strain introduction events, 602 were transmission events, and 155 were indeterminate events (present in the household previously but not at the immediately preceding sampling; it is unclear whether these represented transmissions or re-introductions). For these 602 transmission events, there were 749 paths from potential transmission sources to household members. Each individual or pet who became colonized with a strain not present at the prior sampling counted for one acquisition, while one acquisition for the environment was counted when a strain not found anywhere in the environment at the prior sampling appeared on ≥1 environmental sites.

Figure 2.. Longitudinal strain dynamics in exemplar households.

“X” denotes a reported interval SSTI, “A” denotes interval oral or IV antibiotics, and “D” represents interval decolonization (nasal mupirocin, bleach baths, or chlorhexidine body washes). For households A and B, the index patient’s enrollment infection isolate, MRSA_1, is indicated with red hash marks; the red box around this cell signifies an infection (with MRSA_1) prior to the infection prompting enrollment. Household A. The Index patient experienced an SSTI 3 months prior to the infection that prompted enrollment. Between the 3-month and 6-month follow-up visits, the Index patient experienced a recurrent SSTI caused by MRSA_1 (the enrollment infection strain), denoted by a red box around the cell; for this infection, the Index patient received systemic antibiotics and subsequently performed decolonization. Example introduction events occurred at the 3-month follow-up visit: novel strain MSSA_7 appeared on Half-sister 3, Dog 1, and electronic and bathroom environmental surfaces; novel strain MSSA_6 appeared on electronic, bathroom, and kitchen environmental surfaces. Example transmission events occurred between the enrollment and 3-month follow-up visits in which strain MSSA_2 was transmitted from potential sources Half-sister 2 or bathroom environmental surfaces to recipients Dad, Mom, Half-sister 1, and the kitchen. Household B. The Index patient experienced an SSTI one year prior to the infection that prompted enrollment. Example introduction events occurred at the 3-month follow-up visit: novel strain MSSA_1 appeared on Index patient and Half-sister 2; novel strain MSSA_3 appeared on Half-sister 1; novel strain MSSA_5 appeared on kitchen environmental surfaces. Example transmission events occurred between the enrollment and 3-month follow-up visits in which strain MRSA_2 was transmitted from potential sources Half-sister 3 or electronic or bathroom environmental surfaces to the kitchen. Subsequently, between the 3-month and 6-month visits, this strain was transmitted from the potential source kitchen to recipients Index patient, Dad, Mom, and electronics.

Figure 2.. Longitudinal strain dynamics in exemplar households.

“X” denotes a reported interval SSTI, “A” denotes interval oral or IV antibiotics, and “D” represents interval decolonization (nasal mupirocin, bleach baths, or chlorhexidine body washes). For households A and B, the index patient’s enrollment infection isolate, MRSA_1, is indicated with red hash marks; the red box around this cell signifies an infection (with MRSA_1) prior to the infection prompting enrollment. Household A. The Index patient experienced an SSTI 3 months prior to the infection that prompted enrollment. Between the 3-month and 6-month follow-up visits, the Index patient experienced a recurrent SSTI caused by MRSA_1 (the enrollment infection strain), denoted by a red box around the cell; for this infection, the Index patient received systemic antibiotics and subsequently performed decolonization. Example introduction events occurred at the 3-month follow-up visit: novel strain MSSA_7 appeared on Half-sister 3, Dog 1, and electronic and bathroom environmental surfaces; novel strain MSSA_6 appeared on electronic, bathroom, and kitchen environmental surfaces. Example transmission events occurred between the enrollment and 3-month follow-up visits in which strain MSSA_2 was transmitted from potential sources Half-sister 2 or bathroom environmental surfaces to recipients Dad, Mom, Half-sister 1, and the kitchen. Household B. The Index patient experienced an SSTI one year prior to the infection that prompted enrollment. Example introduction events occurred at the 3-month follow-up visit: novel strain MSSA_1 appeared on Index patient and Half-sister 2; novel strain MSSA_3 appeared on Half-sister 1; novel strain MSSA_5 appeared on kitchen environmental surfaces. Example transmission events occurred between the enrollment and 3-month follow-up visits in which strain MRSA_2 was transmitted from potential sources Half-sister 3 or electronic or bathroom environmental surfaces to the kitchen. Subsequently, between the 3-month and 6-month visits, this strain was transmitted from the potential source kitchen to recipients Index patient, Dad, Mom, and electronics.