mrsa infections: the roles of people, pets and the home...mrsa infections: the roles of people, pets...

MRSA Infections: The roles of people, pets and the home Delaware Healthy Homes Summit Children’s Health & the Indoor Environment March 12, 2014

Meghan F. Davis, DVM MPH PhD

Johns Hopkins Bloomberg School of Public Health

[email protected]

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mailto:[email protected]

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About this Lecture and Lecturer

• Dr. Meghan Davis

• Veterinarian – Dairy/Mixed animal practice (PA)

– Companion animal practice (PA & MD)

– Rabies clinics (MD)

• Hopkins Postdoc in Environmental Health

– Zoonotic disease research

– Focus on household bacterial exposures

– One health approach

• This lecture: Zoonoses in the Household

Outline

• The home environment & infectious disease – Zoonoses & pets

– Children in the home

• The importance of staphylococcal bacteria

• Pets and Environmental Transmission of Staphylococci study

• Broader implications of pets in the home

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What is a zoonosis?

• Zoo- animal + -nosis disease

• Disease transmitted to humans from animals (usually vertebrates)

• May have animal reservoir

• May be novel “emergence”

What is a zoonosis?

• Zoo- animal + -nosis disease

• Disease transmitted to humans from animals (usually vertebrates)

• May have animal reservoir

• May be novel “emergence”

Many diseases we call zoonoses

actually impact both people

and animals and can be

transmitted in both directions

(from animals to people

and from people to animals)

One Health: the Venn diagram

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Household pets

• Pet species – Dogs, cats

– “Pocket pets” – rodents, rabbits, etc.

– Reptiles – turtles, lizards, snakes, etc.

– Birds – parrots, etc.

– Horses

• High level of contact with humans

& their environments

The household: a community nexus

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The household: a community nexus

9 Davis et al., The role of the household in transmission of methicillin-resistant S. aureus and other staphylococci. The Lancet Infectious Diseases 2012, in press.

Household Contamination Sites

10 Davis et al., The role of the household in transmission of methicillin-resistant S. aureus and other staphylococci. The Lancet Infectious Diseases 2012, in press.

The Importance of Transmission Dynamics

Davis et al., The role of the household in transmission of methicillin-resistant S. aureus and other staphylococci. The Lancet Infectious Diseases 2012

Conventional clinical approaches focus on short-term clearance following treatment in the index patient only

Transmission dynamics: consider the household as a unit

Davis et al., The role of the household in transmission of methicillin-resistant S. aureus and other staphylococci. The Lancet Infectious Diseases 2012

Why staphylococci matter

• Share the genes for antimicrobial

resistance + the staphylococcal

chromosomal cassette (SCCmec, methicillin resistance)

• Induce toxic effects (e.g. toxic shock syndrome, enterotoxin)

• Survive on environmental surfaces

13 Background

Staphylococci: the usual suspects

• S. aureus, incl. methicillin-resistant strains (MRSA) – Primary pathogens of people, can colonize pets & cause pet infections

– Livestock and horses have animal-adapted strains (e.g. ST398, USA500)

• S. pseudintermedius, incl. methicillin-resistant strains (MRSP) – Primary pathogen of pets, esp. dogs, can colonize people & cause rare

human infections

• S. schleiferi, subsp. coagulans & subsp. schleiferi – Emerging pathogen of pets, esp. dogs, can colonize people & cause rare

human infections

These are coagulase-positive staphylococci (CPS)*

* except S. schleiferi subsp. schleiferi

14 Background

MRSA Epidemiology

• Increases in MRSA nasal colonization rates based on U.S. population estimates between 2001 and 2004

– By 2003-04 (NHANES), almost 20% of cases were associated with strain types associated with community disease

• Increases since 1990s and 2000s appear to be due to rise in community-associated (CA-)MRSA

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Image source: Microbiology Online

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PETS AND ENVIRONMENTAL TRANSMISSION OF STAPHYLOCOCCI STUDY (P.E.T.S.)

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Goals: (1) To identify the roles of animals and

the environment as reservoirs of MRSA in households, related to human colonization and infection

(2) To evaluate animal health impacts from exposure to people with MRSA

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Nested Study Design

• “Epidemiology and Prevention of MRSA in the Community” aka CURE

– Registered randomized controlled trial (NCT00966446)

– Enrollment: 223 index patients (people) with recent MRSA infection and their household members

– Randomization to treatment protocol for people (two decolonization treatment options, education control)

• PETS study nested in CURE trial – 95 households (43% of CURE)

– 184 pets in 67 households

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3 months

Figure: Amy Brazil Methods

PETS Household Enrollment

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We are here

PETS Overview

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Household and pet-related environments (aim of PETS study)

Pets of all species (aim of PETS study)

People living in the house (aim of CURE study)

Inclusion criteria: MRSA-exposed populations

Methods

PETS Overview: workflow

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Conducted surveys of household & pet characteristics

Collected samples from home surfaces, pets & beds Performed laboratory

testing of samples: • Culture-dependent with molecular ID (PCR) • Culture-independent (microbiome, Illumina MiSeq)

Methods

nuc mecA/C

R primer F primer with barcode

16S V4~254 bp

Household Enrollment: most households were urban

PETS study, n (%)

Baseline Follow-up

Households enrolled 96* 65

Enrollment center HUP CHOP Philly community hospitals (2) Hershey Medical Center

18 (19%) 35 (36%) 21 (22%) 22 (23%)

10 (15%) 24 (37%) 13 (20%) 18 (28%)

Randomization Education Unsupervised decolonization Supervised decolonization

33 (35%) 29 (31%) 33 (35%)

26 (40%) 18 (28%) 21 (32%)

Home location Urban Suburban Rural (ag and non-ag)

64 (67%) 19 (20%) 13 (13%)

37 (57%) 17 (26%) 11 (17%)

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* one house did not complete CURE baseline enrollment

Household Enrollment: many households had children

• Enrollment: 398 at baseline, 263 at follow-up

• On average 4.3 people per household (range 1-11)

• Child index patient: 44% baseline, 46% at follow-up – CHOP and HMC enrollment centers

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Pet Enrollment: most households had pets

PETS study

Baseline Follow-up

Households enrolled, N 95 65

Homes with pets, N (%) 67 (71%) 44 (68%)

Pets enrolled, N 184 1303

Dogs, N (%) 71 (39%) 38 (29%)

Cats, N (%) 68 (37%) 50 (38%)

Pocket pets, N (%)1 11 (6%) 9 (7%)

Reptiles, N (%)2 21 (11%) 18 (14%)

Freshwater fish tanks, N (%) 11 (6%) 13 (10%)

Birds (parrots), N (%) 2 (1%) 2 (2%)

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1 Chinchillas, hamsters, rat, sugar glider, ferret, rabbit 2 Turtles (primarily aquatic), lizards, snake

3 113 continuing pets, 17 new pets at follow-up (10 cats, 3 reptiles, 3 fish, and a hamster)

Results

Over half of pets lick people or share beds with them

Baseline

Pets enrolled, N 184

Female, N (%) 103 (56%)

Spayed/Neutered, N (%) 55 (30%)

Median age (in months) 44

Ever go outside, N (%)2 37 (20%)

Veterinary contact in past year, N (%) 55 (30%)

Abx use in past year, N (%) 10 (5%)

Ever lick people, N (%) 79 (43%)

Ever share a bed with people, N (%) 76 (41%)

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63% of pets lick, share beds, or both

CULTURE-DEPENDENT RESULTS

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Household environments are contaminated with MRSA

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PETS study

MRSA MSSA MSSP

Baseline visit, n=96* 60 (63%) 20 (21%) 4 (4%)

Common room, n=96* 53 (55%) 16 (17%) 3 (3%)

Bedroom (index pt), n=92 53 (58%) 13 (14%) 2 (2%)

Based on screening one isolate per visit for each location group (common room, bedroom) *95 homes concurrently enrolled in CURE and eligible for longitudinal study All homes with S. pseudintermedius had pets

Environmental MRSA contamination was associated significantly with the proportion of people who were MRSA-positive at the time of sampling. This association was non-significant with MRSA-positive pets.

Results

Household environments are contaminated with MRSA

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PETS study

MRSA MSSA MSSP

Baseline visit, n=96 60 (63%) 20 (21%) 4 (4%)

Common room, n=96 53 (55%) 16 (17%) 3 (3%)


Follow-up visit, n=65 33 (50%) 13 (20%) 3 (5%)

Common room, n=65 27 (42%) 9 (14%) 2 (3%)


21/65 (33%) homes were MRSA-positive at both visits. Randomization to a treatment group lowered odds for common room contamination with MRSA at both visits, but this estimate of association was non-significant.

Results

Mouth

Perineum

Inguinal Region

Dorsum Nares

Pet Sampling

Figure: Sally Ann Iverson

Methods

Most sensitive!

Dogs carry S. pseudintermedius more often than S. aureus

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PETS study - baseline prevalence, n (%)

MRSA MSSA MSSP1

Pets overall, n=179* 13 (7%) 14 (8%) 31 (18%)

Dogs, n=71 5 (7%) 9 (13%) 27 (38%)1

Cats, n=63* 7 (11%) 4 (6%) 2 (3%)

Pocket pets, rabbit, ferret, n=11 0 (0%) 0 (0%) 0 (0%)

Reptiles, n=21 0 (0%) 1 (5%) 1 (5%)

Freshwater fish tanks, n=11 1 (9%) 0 (0%) 1 (9%)

Birds (parrots), n=2 0 (0%) 0 (0%) 0 (0%)

Based on screening one isolate per pet per visit Single S. schleiferi isolate identified (dog) 1Additional single MRSP isolate identified * Five cats enrolled but not sampled, results based on prevalence among sampled pets

Results

Can’t completely ignore exotic species

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PETS study prevalence, n (%)

MRSA MSSA MSSP1

Pets overall, n=179* 13 (7%) 14 (8%) 31 (18%)

Dogs, n=71 5 (7%) 9 (13%) 27 (38%)1

Cats, n=63* 7 (11%) 4 (6%) 2 (3%)


Reptiles, n=21 0 (0%) 1 (5%) 1 (5%)


Birds (parrots), n=2 0 (0%) 0 (0%) 0 (0%)

First report of MRSA-positive fish tank

Contaminated homes are associated with pet MRSA

MRSA

• Pets with owner-reported history of pet antimicrobial use in the past year was associated with 7-fold increase in odds for MRSA positivity (p<0.01).

• Contact with veterinary hospitals in the past year was not statistically significantly associated with MRSA positivity.

• Positive home environments were associated with a 9-fold increase in odds for MRSA positivity (p=0.04)

• Proportion of positive humans in the household with a non-significant 9-fold increase in odds for MRSA positivity (p=0.17).

Logistic regression modeling, controlled for clustering at the household level

Bivariate ORs reported; these remained generally consistent in multivariate models

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Pets may be persistently positive for staphylococci

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PETS study, three-month prevalence, n (%)

MRSA MSSA MSSP1

Pets overall, n=128* 7 (5%) 12 (9%) 19 (15%)

Dogs, n=38 4 (11%) 5 (13%) 18 (45%)

Cats, n=48* 3 (6%) 7 (15%) 1 (2%)


Reptiles, n=18 0 (0%) 0 (0%) 0 (0%)


Birds (parrots), n=2 0 (0%) 0 (0%) 0 (0%)

Persistently positive pets (from 111 pets sampled longitudinally): MRSA, 3%: 2 cats, 1 dog MSSA, 3%: 2 cats, 1 dog MSSP, 10%: 10 dogs, 1 cat MRSP, 1%: 1 dog

Results

Clinical significance: cases of MRSA in person and pet

• Case in owner: Male Caucasian, 31 years old – Neck abscess in June 2012

– Drained, treated successfully with IV clindamycin and oral trimethoprim-sulfadimethoxazole

• Case in dog: FS Italian Mastiff, 23 months old – Cruciate surgery on the day after baseline visit (July 2012)

– Only dog to have surgery between baseline and follow-up visits

– Developed MRSA post-surgical infection two weeks after procedure

– Treated successfully with clindamycin

• Pet’s bed the only site positive

for MRSA at baseline visit

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Cases developed within one month of each other

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Molecular typing links MRSA strains

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PFGE, DICE coefficient ≥85%

Antimicrobial susceptibility changes over time

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Person treated with SXT

Dog treated with CLI MRSA

isolates

Conclusions from PETS study

• Positive home environments were associated with risk for both positive people and positive pets.

• Pets may be more likely to carry veterinary staphylococcal bacteria than a human pathogenic bacterium like MRSA, and this varies by species of pet.

• Dogs were more likely to carry Staphylococcus pseudintermedius

• Cats were more likely to carry Staphylococcus aureus

• Case report illustrates clinical significance and transmission dynamics within a household involving both people and a dog.

• Case report also suggests response to selective pressure from antimicrobial use in either a person or a pet.

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Selected other zoonoses/anthroponoses

• Bacteria • Salmonella associated with reptiles - does cause disease in reptiles!

• Campylobacter, E. coli, etc.

• Parasites • Hookworms and roundworms – puppies and kittens

• Cryptosporidium parvum – HIV+ and immunosuppressed at risk

• Toxoplasma gondii – cat feces and gardening a source for pregnant women

• Viruses • Influenza A – variable risk, hard to quantify

• Rabies virus - household pets required to be vaccinated

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Source: Centers for Disease Control and Prevention, November 2010

Pathogen characteristics that influence infectious disease transmission

• Physical structure – Size, shape, etc.

• Survival/growth in environment or reservoir – Inoculating dose

• Lifecycle characteristics (complexity) – Important for vector-borne diseases (host, vector, infectious agent)

• Antigen – Structures (epitopes) on pathogen that induce immune response

• Physiologic barrier (host)

Vectors

• GENERAL: Indirect pathway of transmission, e.g. fomite

• SPECIFIC: arthropod or other insect host which either serves as a mechanical or biological route of disease transmission

– Mechanical: Flies carry bacteria on legs

– Biological: Mosquitoes are part of the malaria parasite lifecycle

Pests

– Sources of discomfort • lice, fleas, mites, bedbugs, spiders

– Vectors of disease

Mosquitoes Malaria, yellow fever, dengue fever, filariasis, encephalitis, West Nile Virus

Flies Typhoid fever, cholera, dysentery, parasitic worm infections

Cockroaches Allergic reactions, asthma attacks, skin irritations

Body lice Typhus fever, trench fever

Rat fleas Plague

Ticks Rocky Mountain spotted fever, Lyme disease, anaplasmosis, erlichiosis

Household pets and vectors

• Mechanical vector for pests – Ticks (Lyme disease, other tick-borne diseases)

• Amplifying host – Fleas

• Treatment may lead to increase in household pesticide use

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Product Active Ingredient Product type

Revolution Selamectin Prescription drug

K9 Advantix II Imidacloprid & Permethrin Insecticide

Vectra 3D Dinotefuran & Permethrin Insecticide

Please note that permethrins are toxic to cats; ivermectins are toxic to collie-type dogs

Potential human health hazards from pesticides

• Carcinogens or potentially carcinogenic – 60% of all herbicides

– 90% of all fungicides

– 30% of insecticides

• Endocrine disruptors – Feminization of males

– Birth defects

– Impaired fertility

• Immune system disruptors – infectious disease incidence increases, contact dermatitis seen

Animal-associated bioaerosols

• Allergens / dander

• Culturable microbes • Specific pathogens, e.g. MRSA

• Microbial products • Endotoxin (LPS)

• Superantigens

• Bacterial cell wall components (peptidoglycan, lipoteichoic acid)

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But it’s not all bad!

• Pets may contribute to household microbial diversity / microbial sharing among household members

– PETS study findings corroborate the literature

• A diversity of microbial exposures in early childhood may protect against development of asthma and other allergic disorders

Health benefits of pet ownership

• Mental health / Mood improvements

• Increased fitness – Walking the dog leads to more routine owner exercise

Image source: Wikimedia

Take home messages

• Researchers: be aware of the influence of household pets – Particularly on infectious disease

– Also on other correlated household environmental exposures, such as pesticides and endotoxin

• Clinicians: consider pets and the home environment with cases of recurrent infection with potentially zoonotic disease agents

• Public health practitioners: ask about pet ownership when investigating outbreaks

• Community nurses: evaluate the whole household

• Engineers: design homes with pets and infectious diseases in mind

• All: consider that pets may be a sentinel for home-based exposures (toxicant or infectious agent)

– Birds and amphibians are particularly sensitive to toxicants

Thank you!

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CURE: Ebbing Lautenbach, Irving Nachamkin, Pam Tolomeo, and the field and laboratory team, especially John, Grace and Robin PETS: Sally Ann Iverson, Amy Brazil, Aimee Vasse, Rachael Joseph, Patrick Baron, Elana Youssef, Jackie Ferguson JHSPH: John Groopman, Peter Lees, Ken Nelson, & Ellen Silbergeld; with thanks to David Sack & his lab group and the EHS department Penn: Daniel Morris, Shelley Rankin, Elizabeth Grice, Ana Misic PETS Funding: Johns Hopkins Center for a Livable Future, Morris Animal Foundation, & the American College of Veterinary Dermatology; T32 training grant

Still scratching your head? [email protected]

Culture-Dependent Methods

Salt broth enrichment

Antimicrobial broth enrichment

Columbia CNA Blood Agar (staph-selective)

Baird-Parker Agar (CPS)

Environmental Sampling Animal Sampling

Antimicrobial Susceptibility Testing

PCR (nuc, mecA/C) &

or

or PFGE & whole genome analysis (subset – pending)

Davis et al., Dry collection and culture methods for recovery of methicillin-susceptible and methicillin-resistant Staphylococcus aureus strains from indoor home environments. Applied & Environmental Microbiology 2012.

Companion Animal Results: Baseline visit

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PETS study prevalence, n (%)

MRSA MSSA MSSP1

Pets overall, n=179* 13 (7%) 14 (8%) 31 (18%)

Dogs, n=71 5 (7%) 9 (13%) 27 (38%)1

Cats, n=63* 7 (11%) 4 (6%) 2 (3%)


Reptiles, n=21 0 (0%) 1 (5%) 1 (5%)


Birds (parrots), n=2 0 (0%) 0 (0%) 0 (0%)

Based on screening one isolate per pet per visit Single S. schleiferi isolate identified (dog) 1Additional single MRSP isolate identified * Five cats enrolled but not sampled, results based on prevalence among sampled pets

Companion Animal Risk Factor Analysis

MSSP

• Dogs were 19 times more likely than cats to be positive for S. pseudintermedius (p=0.001).

• Owner-reported history of licking by pet was associated with a 4-fold increase in odds of S. pseudintermedius positivity (p<0.001), but this was largely explained by pet species (dog).

• Residence in suburban or rural area was associated with 4-fold increase in odds for pet S. pseudintermedius positivity (p<0.01).

Logistic regression modeling, controlled for clustering at the household level

Bivariate ORs reported; these remained generally consistent in multivariate models

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Companion Animal Results: Follow-up visit

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PETS study

MRSA MSSA MSSP1

Pets overall, n=128* 7 (5%) 12 (9%) 19 (15%)

Dogs, n=38 4 (11%) 5 (13%) 18 (45%)

Cats, n=48* 3 (6%) 7 (15%) 1 (2%)


Reptiles, n=18 0 (0%) 0 (0%) 0 (0%)


Birds (parrots), n=2 0 (0%) 0 (0%) 0 (0%)

Based on screening one isolate per pet per visit, n=130 1Additional single MRSP isolate identified (same pet positive at baseline) *Two cats surveyed but not sampled, results based on prevalence among sampled pets

Companion Animal Results: Follow-up visit

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PETS study

MRSA MSSA MSSP1

Pets overall, n=128* 7 (5%) 12 (9%) 19 (15%)

Dogs, n=38 4 (11%) 5 (13%) 18 (45%)

Cats, n=48* 3 (6%) 7 (15%) 1 (2%)


Reptiles, n=18 0 (0%) 0 (0%) 0 (0%)


Birds (parrots), n=2 0 (0%) 0 (0%) 0 (0%)

Persistently positive pets (from 111 pets sampled longitudinally): MRSA, 3%: 2 cats, 1 dog MSSA, 3%: 2 cats, 1 dog MSSP, 10%: 10 dogs, 1 cat MRSP, 1%: 1 dog

Effect of Baseline Characteristics and Household Randomization to Treatment on Pet MRSA Status at Follow-up

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Bivariate OR [95% CI] Multivariate OR [95% CI]

Pet Positive at Baseline 15 [2.4, 89] 23 [1.8, 303]

Environment Positive at Baseline

3.8 [0.42, 35] 2.0 [0.12, 34]

Proportion of MRSA-positive People at Baseline

3.6 [0.37, 34] 7.0 [ 0.19, 254]

Randomization to Treatment Group

2.4 [0.40, 14] 3.5 [0.43, 28]

Baseline Follow-up

~3 months Decolonization treatment of people (2/3 of homes)

Effect of Baseline Characteristics and Household Randomization to Treatment on Pet MRSA Status at Follow-up

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Bivariate OR [95% CI] Multivariate OR [95% CI]

Pet Positive at Baseline 15 [2.4, 89] 23 [1.8, 303]

Environment Positive at Baseline

3.8 [0.42, 35] 2.0 [0.12, 34]

Proportion of MRSA-positive People at Baseline

3.6 [0.37, 34] 7.0 [ 0.19, 254]

Randomization to Treatment Group

2.4 [0.40, 14] 3.5 [0.43, 28]

Household randomization to treatment of people did not decrease odds of pet MRSA positivity at the follow-up visit.

True colonization?

• Pets with persistent positivity: 15/113 (13%) – MRSA: 2 cats, 1 dog – MSSA: 2 cats, 1 dog – MSSP: 1 cat, 7 dogs – MRSP, 1 dog

• 3 dogs had MSSP-positive skin lesions at both visits

• Pets with mixed/shifting patterns over time: 6/113 (5%) – MRSA to MSSA: 1 cat, 1 dog – MRSA to MSSP: 2 dogs – MSSS to MRSA: 1 dog

• This dog also had MSSP-positive FAD at baseline visit – MSSP to MSSA: 1 dog

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Clinical implications: susceptibility

Baseline visit Follow-up visit

Pets Env Pets Env

MRSA 38% 58% 86% 44%

MSSA 21% 6% 9% 37%

MRSP* 100% - - -

MSSP 0% 0% 0% 0%

MSSS* 0% - - -

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Prevalence of multidrug resistance

*Single isolate from pet

PETS Enrollment & Microbiome Study

PETS study Microbiome sub-study

Baseline Follow-up Baseline Follow-up

Households enrolled, N 95 65 25 21

Homes with pets, N (%) 67 (71%) 44 (68%) 22 (88%) 18 (86%)

Pets enrolled, N 184 1303 63 434

Dogs, N (%) 71 (39%) 38 (29%) 36 (57%) 19 (44%)

Cats, N (%) 68 (37%) 50 (38%) 20 (32%) 18 (42%)

Pocket pets, N (%)1 11 (6%) 9 (7%) 7 (11%) 6 (14%)

Reptiles, N (%)2 21 (11%) 18 (14%) excluded excluded

Freshwater fish tanks, N (%) 11 (6%) 13 (10%) excluded excluded

Birds (parrots), N (%) 2 (1%) 2 (2%) excluded excluded

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1 Chinchillas, hamsters, rat, sugar glider, ferret, rabbit 2 Turtles (primarily aquatic), lizards, snake

3 113 continuing pets, 17 new pets at follow-up (10 cats, 3 reptiles, 3 fish, and a hamster) 4 38 continuing pets, 5 new pets at follow-up

Preliminary PCR Results: Baseline visit

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PETS study Microbiome sub-study

MRSA MSSA MSSP1 MRSA MSSA MSSP1

Pets overall, N (%) 13 (7%) 14 (8%) 27 (15%) 5 (8%) 4 (6%) 16 (25%)

Dogs 4 (6%) 9 (13%) 23 (32%)1

3 (8%) 2 (6%) 16 (44%)

Cats 8 (12%) 4 (6%) 2 (3%) 2 (10%) 2 (10%) 0 (0%)

Pocket pets 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%) 0 (0%)

Reptiles 0 (0%) 1 (5%) 1 (5%) excluded excluded excluded

Freshwater fish tanks 1 (9%) 0 (0%) 1 (9%) excluded excluded excluded

Birds (parrots) 0 (0%) 0 (0%) 0 (0%) excluded excluded excluded

Based on screening one isolate per pet per visit (**underestimate of prevalence) Single S. schleiferi isolate identified in an mbiome-sampled dog 1Additional single MRSP isolate in an mbiome-sampled dog

Future Directions

• Planned completion of genetic analysis – Finish PCR speciation (all isolates at nares/mouth mbiome sites) – PFGE typing to evaluate clonality within households (incl. people and

environmental surfaces) and within pets over time – Movement of genes, e.g. for antimicrobial resistance (including

SCCmec), between microbes within households and over time

• Molecular epidemiology / multilevel modeling – Pets: do certain characteristics or behaviors predict MRSA positivity? – RCT: do environmental contamination and pet colonization with MRSA

(independently or interactively) predict re-colonization of people after successful decolonization treatment?

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