Patrick G Hogan1, Ryan L Mork2,3,4, Ryley M Thompson1, Carol E Muenks1, Mary G Boyle1, Melanie L Sullivan1, John J Morelli1, Caroline V Williams1, Nataly Sanchez1, David A Hunstad1,5, Juliane Bubeck Wardenburg1, Sarah J Gehlert6, Carey-Ann D Burnham1,5,7,8, Andrey Rzhetsky9, Stephanie A Fritz1. 1. Department of Pediatrics, Washington University School of Medicine in St Louis, St Louis, Missouri. 2. Graduate Program in the Biophysical Sciences, University of Chicago, Chicago, Illinois. 3. Committee of Microbiology, University of Chicago, Chicago, Illinois. 4. Institute for Genomics and Systems Biology, University of Chicago, Chicago, Illinois. 5. Department of Molecular Microbiology, Washington University School of Medicine in St Louis, St Louis, Missouri. 6. Department of Surgery, Washington University School of Medicine in St Louis, St Louis, Missouri. 7. Department of Pathology and Immunology, Washington University School of Medicine in St Louis, St Louis, Missouri. 8. Department of Medicine, Washington University School of Medicine in St Louis, St Louis, Missouri. 9. Department of Human Genetics, University of Chicago, Chicago, Illinois.
Abstract
Importance: The longitudinal association among persistent Staphylococcus aureus colonization, household environmental contamination, and recurrent skin and soft tissue infection (SSTI) is largely unexplored to date. Objectives: To identify factors associated with persistent S aureus colonization and recurrent SSTI in households with children with community-associated methicillin-resistant S aureus (MRSA) SSTI. Design, Setting, and Participants: This 12-month prospective cohort study included 150 children with community-associated MRSA SSTI, 542 household contacts, and 154 pets enrolled from January 3, 2012, through October 20, 2015. A total of 5 quarterly home visits were made to 150 households in the St Louis, Missouri, region. Statistical analysis was performed from September 18, 2018, to January 7, 2020. Exposures: Covariates used in S aureus strain persistence and interval SSTI models included S aureus colonization and contamination measures, personal hygiene and sharing habits, health history, activities external to the home, and household characteristics (eg, cleanliness, crowding, home ownership, and pets). Serial samples to detect S aureus were collected from household members at 3 anatomic sites, from pets at 2 anatomic sites, and from environmental surfaces at 21 sites. Main Outcomes and Measures: Molecular epidemiologic findings of S aureus isolates were assessed via repetitive-sequence polymerase chain reaction. Individual persistent colonization was defined as colonization by an identical strain for 2 consecutive samplings. Longitudinal, multivariable generalized mixed-effects logistic regression models were used to assess factors associated with persistent S aureus personal colonization, environmental contamination, and interval SSTI. Results: Among 692 household members in 150 households, 326 (47%) were male and 366 (53%) were female, with a median age of 14.82 years (range, 0.05-82.25 years). Of 540 participants completing all 5 samplings, 213 (39%) were persistently colonized with S aureus, most often in the nares and with the strain infecting the index patient at enrollment. Nine pets (8%) were persistently colonized with S aureus. Participants reporting interval intranasal mupirocin application were less likely to experience persistent colonization (odds ratio [OR], 0.44; 95% credible interval [CrI], 0.30-0.66), whereas increasing strain-specific environmental contamination pressure was associated with increased individual persistent colonization (OR, 1.17; 95% CrI, 1.06-1.30). Strains with higher colonization pressure (OR, 1.47; 95% CrI, 1.25-1.71) and MRSA strains (OR, 1.57; 95% CrI, 1.16-2.19) were more likely to persist. Seventy-six index patients (53%) and 101 household contacts (19%) reported interval SSTIs. Individuals persistently colonized with MRSA (OR, 1.56; 95% CrI, 1.17-2.11), those with a history of SSTI (OR, 2.55; 95% CrI, 1.88-3.47), and index patients (OR, 1.54; 95% CrI, 1.07-2.23) were more likely to report an interval SSTI. Conclusions and Relevance: The study findings suggest that recurrent SSTI is associated with persistent MRSA colonization of household members and contamination of environmental surfaces. Future studies may elucidate the effectiveness of specific combinations of personal decolonization and environmental decontamination efforts in eradicating persistent strains and mitigating recurrent SSTIs.
Importance: The longitudinal association among persistent Staphylococcus aureus colonization, household environmental contamination, and recurrent skin and soft tissue infection (SSTI) is largely unexplored to date. Objectives: To identify factors associated with persistent S aureus colonization and recurrent SSTI in households with children with community-associated methicillin-resistant S aureus (MRSA) SSTI. Design, Setting, and Participants: This 12-month prospective cohort study included 150 children with community-associated MRSA SSTI, 542 household contacts, and 154 pets enrolled from January 3, 2012, through October 20, 2015. A total of 5 quarterly home visits were made to 150 households in the St Louis, Missouri, region. Statistical analysis was performed from September 18, 2018, to January 7, 2020. Exposures: Covariates used in S aureus strain persistence and interval SSTI models included S aureus colonization and contamination measures, personal hygiene and sharing habits, health history, activities external to the home, and household characteristics (eg, cleanliness, crowding, home ownership, and pets). Serial samples to detect S aureus were collected from household members at 3 anatomic sites, from pets at 2 anatomic sites, and from environmental surfaces at 21 sites. Main Outcomes and Measures: Molecular epidemiologic findings of S aureus isolates were assessed via repetitive-sequence polymerase chain reaction. Individual persistent colonization was defined as colonization by an identical strain for 2 consecutive samplings. Longitudinal, multivariable generalized mixed-effects logistic regression models were used to assess factors associated with persistent S aureus personal colonization, environmental contamination, and interval SSTI. Results: Among 692 household members in 150 households, 326 (47%) were male and 366 (53%) were female, with a median age of 14.82 years (range, 0.05-82.25 years). Of 540 participants completing all 5 samplings, 213 (39%) were persistently colonized with S aureus, most often in the nares and with the strain infecting the index patient at enrollment. Nine pets (8%) were persistently colonized with S aureus. Participants reporting interval intranasal mupirocin application were less likely to experience persistent colonization (odds ratio [OR], 0.44; 95% credible interval [CrI], 0.30-0.66), whereas increasing strain-specific environmental contamination pressure was associated with increased individual persistent colonization (OR, 1.17; 95% CrI, 1.06-1.30). Strains with higher colonization pressure (OR, 1.47; 95% CrI, 1.25-1.71) and MRSA strains (OR, 1.57; 95% CrI, 1.16-2.19) were more likely to persist. Seventy-six index patients (53%) and 101 household contacts (19%) reported interval SSTIs. Individuals persistently colonized with MRSA (OR, 1.56; 95% CrI, 1.17-2.11), those with a history of SSTI (OR, 2.55; 95% CrI, 1.88-3.47), and index patients (OR, 1.54; 95% CrI, 1.07-2.23) were more likely to report an interval SSTI. Conclusions and Relevance: The study findings suggest that recurrent SSTI is associated with persistent MRSA colonization of household members and contamination of environmental surfaces. Future studies may elucidate the effectiveness of specific combinations of personal decolonization and environmental decontamination efforts in eradicating persistent strains and mitigating recurrent SSTIs.
Authors: Patrick G Hogan; Ryan L Mork; Mary G Boyle; Carol E Muenks; John J Morelli; Ryley M Thompson; Melanie L Sullivan; Sarah J Gehlert; Jessica R Merlo; Matt G McKenzie; Juliane Bubeck Wardenburg; Andrey Rzhetsky; Carey-Ann D Burnham; Stephanie A Fritz Journal: J Infect Date: 2018-11-29 Impact factor: 6.072
Authors: Loren G Miller; Samantha J Eells; Alexis R Taylor; Michael Z David; Nancy Ortiz; Diana Zychowski; Neha Kumar; Denise Cruz; Susan Boyle-Vavra; Robert S Daum Journal: Clin Infect Dis Date: 2012-04-03 Impact factor: 9.079
Authors: Stephanie A Fritz; Bernard C Camins; Kimberly A Eisenstein; Joseph M Fritz; Emma K Epplin; Carey-Ann Burnham; Jonathan Dukes; Gregory A Storch Journal: Infect Control Hosp Epidemiol Date: 2011-09 Impact factor: 3.254
Authors: Loren G Miller; Samantha J Eells; Michael Z David; Nancy Ortiz; Alexis R Taylor; Neha Kumar; Denise Cruz; Susan Boyle-Vavra; Robert S Daum Journal: Clin Infect Dis Date: 2014-11-26 Impact factor: 9.079
Authors: Ryan L Mork; Patrick G Hogan; Carol E Muenks; Mary G Boyle; Ryley M Thompson; Melanie L Sullivan; John J Morelli; Jennifer Seigel; Rachel C Orscheln; Juliane Bubeck Wardenburg; Sarah J Gehlert; Carey-Ann D Burnham; Andrey Rzhetsky; Stephanie A Fritz Journal: Lancet Infect Dis Date: 2019-11-26 Impact factor: 25.071
Authors: Stephanie A Fritz; Patrick G Hogan; Lauren N Singh; Ryley M Thompson; Meghan A Wallace; Krista Whitney; Duha Al-Zubeidi; Carey-Ann D Burnham; Victoria J Fraser Journal: JAMA Pediatr Date: 2014-11 Impact factor: 16.193
Authors: Marcela Rodriguez; Patrick G Hogan; Sarah W Satola; Emily Crispell; Todd Wylie; Hongyu Gao; Erica Sodergren; George M Weinstock; Carey-Ann D Burnham; Stephanie A Fritz Journal: Medicine (Baltimore) Date: 2015-09 Impact factor: 1.817
Authors: Charles M Macal; Michael J North; Nicholson Collier; Vanja M Dukic; Duane T Wegener; Michael Z David; Robert S Daum; Philip Schumm; James A Evans; Jocelyn R Wilder; Loren G Miller; Samantha J Eells; Diane S Lauderdale Journal: J Transl Med Date: 2014-05-12 Impact factor: 5.531
Authors: Pauli Virtanen; Ralf Gommers; Travis E Oliphant; Matt Haberland; Tyler Reddy; David Cournapeau; Evgeni Burovski; Pearu Peterson; Warren Weckesser; Jonathan Bright; Stéfan J van der Walt; Matthew Brett; Joshua Wilson; K Jarrod Millman; Nikolay Mayorov; Andrew R J Nelson; Eric Jones; Robert Kern; Eric Larson; C J Carey; İlhan Polat; Yu Feng; Eric W Moore; Jake VanderPlas; Denis Laxalde; Josef Perktold; Robert Cimrman; Ian Henriksen; E A Quintero; Charles R Harris; Anne M Archibald; Antônio H Ribeiro; Fabian Pedregosa; Paul van Mulbregt Journal: Nat Methods Date: 2020-02-03 Impact factor: 28.547
Authors: Stephanie A Fritz; Todd N Wylie; Haley Gula; Patrick G Hogan; Mary G Boyle; Carol E Muenks; Melanie L Sullivan; Carey-Ann D Burnham; Kristine M Wylie Journal: Microbiol Spectr Date: 2022-04-06
Authors: Patrick G Hogan; Katelyn L Parrish; Ryan L Mork; Mary G Boyle; Carol E Muenks; Ryley M Thompson; John J Morelli; Melanie L Sullivan; David A Hunstad; Juliane Bubeck Wardenburg; Andrey Rzhetsky; Sarah J Gehlert; Carey-Ann D Burnham; Stephanie A Fritz Journal: Clin Infect Dis Date: 2021-12-06 Impact factor: 9.079