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Risks associated with spread of antibiotic resistant strains in the
“healthy” community and in the home – a review of the published
data
Sally F Bloomfield, April 2013
Introduction
In addition to assessing potential risks of spread of infections in home and everyday life
settings, there is a further aspect that needs to be considered. Tackling antibiotic resistance
is now a global priority, and there is increasing awareness that hygiene measures are a
central part of reducing the spread of drug-resistant organisms.1
Currently, the focus is on preventing nosocomial infections arising from spread of resistant
superbugs in hospitals, but it is increasingly recognised that this is just as much a home and
community problem. In the community, otherwise healthy people can become persistent
skin carriers of MRSA, or faecal carriers of enterobacteria strains which carry multi-antibiotic
resistance factors (e.g NDM-1 or ESBL-producing strains) Because these people are healthy
i.e. there is no evidence of clinical disease, the risks are not apparent until they are, for
example, admitted to hospital, when they can become “self infected” with their own resistant
organisms following a surgical procedure, and then spread it to other patients. It is thought
that the major source of nosocomial pathogens is the patient’s endogenous flora.2
Sometimes these infections occur in the community, as happened in 2005 when a young
soldier acquired what should have been an easily treatable skin infection from a PVLproducing strain of MRSA, but subsequently died.3 As persistent nasal, skin or bowel
carriage in the healthy population spreads “silently” with and between communities and
across the world, risks from drug resistant strains in both hospitals and the community
increases.
This means that hygiene measures in home and everyday life settings are important in the
fight against antibiotic resistance, not just because they reduce the need for antibiotic
prescribing (i.e. reduce the number of infections requiring antibiotic treatment) they can also
reduce the spread of resistant strains in the healthy community, reducing not only the spread
infections with drug resistant strains, but also the rate of carriage in the healthy population
The following is a review of the increasing amount of data from various studies which
examine:
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

The extent to which antibiotic resistant strains are found in the community, and the
rate of spread of these strains
The extent to which (and the routes through which) these organisms are spread in
home and community environments
The extent to which resistant strains are circulating between the community and
hospital
It should be noted that a significant part of these studies have been published since around
2009/2010. MRSA in the home and community has also been reviewed in earlier IFH
reports in 20064 and 20125.
Note: this review is a summary of the published data accumulated by IFH over the past 15
years. It does not represent a systematic search of the literature.
1. Increasing spread of resistant strains in the healthy community
The following focuses on some of the most recent prevalence-based studies which illustrate
the extent to which antibiotic resistant strains are spreading in the healthy community
1.1 Studies involving ESBL-producing and multidrug resistant strains
A number of studies relate to ESBL-producing and multidrug resistant gram –ve strains:
In a 2006 paper Woodford et al.6 concluded that Whereas strains were unrecorded in the UK
prior to 2000, the data published by suggest that the ESBL-producing E. coli strains have
“now become widely disseminated through the UK”. In their 2005 report, Livermore and
Hawkey7 suggest that the implications of gut carriage as reported in 2004 UK and Spanish
studies8<9) is that CTM-X producing E. coli strains have now entered via the food chain into
the healthy community producing a reservoir of colonised healthy individuals,
Some more recent studies are as follows
In a 2008 report10 Canton et al discuss how extended-spectrum b-lactamases (ESBLs)
represent a major threat among resistant bacterial isolates. The first types described were
derivatives of the TEM-1, TEM-2 and SHV-1 enzymes during the 1980s in Europe, mainly in
Klebsiella pneumoniae associated with nosocomial outbreaks. Nowadays, they are mostly
found among Escherichia coli isolates in community-acquired infections, with an increasing
occurrence of CTX-M enzymes. The prevalence of ESBLs in Europe is higher than in the
USA but lower than in Asia and South America. However, important differences among
European countries have been observed. Spread of mobile genetic elements, mainly
epidemic plasmids, and the dispersion of specific clones have been responsible for the
increase in ESBL-producing isolates, such as those with TEM-4, TEM-24, TEM-52, SHV-12,
CTX-M-9, CTX-M-14, CTX-M-3, CTX-M-15 and CTX-M-32 enzymes.
Vidal-Navarro et al 201011 report a study which revealed the wide dissemination of MDR
bacteria, including carbapenemase producers, in a French hospital during a non-outbreak
situation. To determine the prevalence of multidrug-resistant (MDR) Gram-negative bacilli
and extended spectrum b-lactamase (ESBL)-producing isolates in stool specimens obtained
from patients hospitalized for acute diarrhoea in a French university hospital. Methods:
Bacteria in stool specimens were screened for ESBL production on Drigalski agar
supplemented with ceftazidime, ESBL CHROMagarw and CTX CHROMagarw media and
confirmed by the double-disc synergy test. Genetic detection was performed by PCR and
sequencing with bacterial DNA extracted from isolates. Results: The presence of MDR
bacteria was markedly high (96 of 303 patients, 31.7%). The majority of MDR bacteria were
Enterobacter cloacae (44, 38%) and Escherichia coli (32, 28%). Moreover, the prevalence of
ESBL and CTX-M producers among all included patients was 15.8% and 5.9%, respectively.
The clone E. coli O25b:H4-ST131 was detected in 63% of CTX-M strains. Surprisingly, 16
carbapenemases (5.3% of patients) were isolated.
D’Andrea et al (2011)12 report on the first detection of the NDM-1 carbapenemase in Italy, in
E. coli isolated in October 2009. Prolonged colonization and relapsing infection by NDM-1positive E. coli were observed in a patient (index case) with an indirect epidemiological link
with areas of endemicity. Transient colonization was apparently observed in another patient
linked with the index case. All patients admitted to the bone marrow transplantation unit
(BMTU) of Modena University Hospital are routinely screened for intestinal colonization by
antibiotic resistant enterics. The first NDM-1-positive Escherichia coli isolate (CVB-1) was
detected from the fecal swab of an inpatient (patient 1, index case) of the same unit in
October 2009. The isolate exhibited a multidrug-resistant (MDR) phenotype to
aminoglycosides, fluoroquinolones, and lactams, including carbapenems, and was found to
produce metallo-_- lactamase (MBL) activity (specific imipenemase activity, 128 g protein,
inhibited _90% by EDTA) and to carry the blaNDM-1 gene along with several other
resistance determinants (see below). The patient, with a history of acute myeloid leukemia,
had been admitted for fever and pancytopenia (but with no obvious signs of infection) and
treated with piperacillin-tazobactam and teicoplanin; oral vancomycin and intravenous
metronidazole were also administered due to a previous positivity for Clostridium difficile.
Tigecycline was added following the detection of fecal carriage of MDR E. coli, but
subsequent fecal swabs collected during the admission period continued to yield E. coli
showing the same MDR phenotype as CVB-1. Similar NDM-1-positive E. coli isolates were
cultured again from this patient in February and June 2010, from exudates of a relapsing toe
In a 2012 review, Van der bij et al13 review how international travel and tourism are
important modes for acquisition and spread of antimicrobial-resistant Enterobacteriaceae,
especially CTX-M-producing Escherichia coli. Infections with KPC-, VIM-, OXA-48- and
NDM-producing Enterobacteriaceae in developed countries have been associated with
visiting and being hospitalised in endemic areas such as the USA, Greece and Israel for
KPCs, Greece for VIMs, Turkey for OXA-48, and the Indian subcontinent for NDMs. For
effective public and patient health interventions, it is important to understand the role of
international travel in the spread of antimicrobial-resistant Enterobacteriaceae. They
conclude that “We urgently need well-designed studies to evaluate the transmission potential
and risks for colonisation and infections due to multiresistant Enterobacteriaceae in travellers
who have recently visited or have been hospitalised in endemic areas. The emergence of
CTX-M-, KPC- and NDM-producing bacteria is a good example of the role that globalisation
plays in the rapid dissemination of new antibiotic resistance mechanisms”.
In 2012 Wickramasinghe et al14 published a study of the proportion of E. coli carrying
specific CTX-M extended-spectrum b-lactamase (ESBL) genotypes in a community
population of East and North Birmingham. In 2010, general practice and outpatient stool
samples from 732 individuals were screened for ESBL-producing E. coli and isolates from
people were assigned to ‘Europe’, ‘Middle East/South Asia’ (MESA) or ‘uncategorised’
groups. Prevalence of CTX-M carriage in the sample population was 11.3%. There was a
statistically significant difference (P,0.001) between carriage in the Europe group (8.1%) and
the MESA group (22.8%). There was also a higher rate of carriage of CTX-M-15-producing
E. coli (P,0.001) in MESA subjects. The authors state” the findings also raise the concern
that the pattern and routes of spread of CTX-M-15 may be replicated in the future by
broader-spectrum b-lactamases, such as New Delhi metallo-b-lactamase (‘NDM-1’)”.
From a study carried out in 2006 Nicolas-Chanoine et al (2012)15 report a 10-fold increase
in the rate of healthy subjects with ESBL-producing E. coli faecal carriage over a 5-year
period suggests wide dissemination of these isolates in the Parisian community. In 2006,
0.6% of healthy subjects living in the Paris area had extended-spectrum β-lactamase
(ESBL)-producing Escherichia coli in their gut. To assess the evolution of this rate, a study
identical to that of 2006 was conducted in 2011. Healthy adults who visited the IPC check-up
centre in February–March 2011 and agreed to participate, provided stools and answered a
questionnaire on the visit day. Stools were analysed to detect ESBL producers and to isolate
the dominant E. coli population. ESBLs were molecularly characterised. For the subjects
harbouring ESBL-producing E. coli, the phylogenetic group and sequence type (ST) were
determined for both ESBL-producing and dominant E. coli isolates. PFGE profiles were also
determined when two types of isolates had the same ST. Results Among the 345 subjects
included, 21 (6%) had ESBL-producing E. coli faecal carriage. None of the previously
published risk factors was identified. CTX-M accounted for 86% and SHV-12 for 14%.
Dominant and ESBL-producing E. coli were similarly distributed into phylogenetic groups (A,
52%–48%; B1, 5%; B2, 24%–14%; and D, 19%–33%). Dominant and ESBL-producing E.
coli displayed a polyclonal structure (18 STs each). However, ST10 and ST131 were
identified in dominant and ESBL-producing E. coli isolates from different subjects. Most
(20/21) ESBL producers were subdominant and belonged (16/21) to STs different from that
of the corresponding dominant E. coli.
Kaame et al 201316 carried out a study to determine the prevalence of extended-spectrum
beta-lactamase (ESBL)-producing Enterobacteriaceae in faeces from healthy Swedish
preschool children and to establish whether transmission took place between children in
preschools. Diapers from children attending preschools in Uppsala city were collected during
September to October 2010, and the faeces was cultured. Antibiotic profiles and carriage of
CTX-M, TEM, SHV and AmpC type enzymes were determined. PCR-positive isolates were
further characterized by sequencing and epidemiological typing. Statistics on antibiotic use
and ESBL producers in paediatric patients at Uppsala University Hospital were extracted for
comparison. A total of 313 stool specimens were obtained, representing 24.5% of all
preschool children in Uppsala city. The carriage rate of ESBL-producing Enterobacteriaceae
was 2.9% among these healthy children. The corresponding figure for patients in the same
age group was 8.4%. E. coli with CTX-M type enzymes predominated, and only one E. coli
isolate carried genes-encoding CMY. CTX-M-producing E. coli isolates with identical
genotypes were found in children with no familial relation at two different preschools.
Conclusion: Using diapers, the prevalence of ESBL-producing Enterobacteriaceae in
children was quickly established, and, most likely, a transmission of ESBL-producing E. coli
was for the first time documented between children at the same preschool.
A 2013 study by Lohr et al in Norway demonstrates how infants may become long-term
faecal carriers of ESBL-producing Klebsiella pneumoniae after colonization during
hospitalization in the neonatal period.17 The median carriage time after discharge from
hospital was 12.5 months.
To study acquisition of faecal colonization with ESBL-producing Enterobacteriaceaeduring
travel Östholm-Balkhed et al 201318 carried out an observational study of individuals
attending vaccination clinics in south-east Sweden, in which submission of faecal samples
and questionnaires before and after travelling outside Scandinavia was requested. Of 262
individuals, 2.4% were colonized before travel. Among 226 evaluable participants, ESBL-PE
was detected in the post-travel samples from 68 (30%) travellers. The most important risk
factor in the final model was the geographic area visited: Indian subcontinent, Asia and
Africa north of the equator. The most common species and ESBL-encoding gene were
Escherichia coli (90%) and CTX-M (73%), respectively. The authors concluded that
acquisition of multiresistant ESBL-PE among the faecal flora during international travel is
common and that the geographical area visited has the highest impact on acquisition
1.2 Studies involving MRSA
A whole number of studies document the increase in carriage of MRSA, particularly
community strains of MRSA, in the community.19 Although further systematic review work is
required to identify the latest data, the following is an assessment of carriage of MRSA in the
community taken from appendix section 1.3.1.1 the IFH 20125 review, together with some
more recent data:
Establishing the prevalence of MRSA circulating in the general community is difficult and can
vary significantly from one location to another.20 In the US, a 2006 assessment concluded
that “MRSA colonisation rates in the community are still low, but are thought to be
increasing.21,22 Graham et al. 23 reported an analysis of 2001-2002 data from the National
Health and Nutrition Examination Survey (NHANES) documenting colonisation with S.
aureus in a non-institutionalized US population. From a total of 9622 participants, it was
found that 31.6% were colonised with S. aureus, of which 2.5% were colonised with MRSA.
Of persons with MRSA, half were identified as strains containing the SCCmec type IV gene
(most usually associated with CA-MRSA), whilst the other half were strains containing the
SCCmec type II gene (most usually associated with HCA-MRSA). Other US studies such as
the study of Shopsin et al 2000 suggest sporadic distribution of CA-MRSA, with carriage
rates ranging from 8-20% in Baltimore, Atlanta and Minnesota, and up to 28-35% for an
apparently healthy population in New York.24
In the UK, a 1007 study indicated that the proportion of the general population carrying
antibiotic resistant strains of S. aureus is somewhere between 0.5-1.5%, the majority being
carriers of HCA-MRSA who are >65 years of age and/or have had recent association with a
healthcare setting.25 Although cases of CA-MRSA and PVL-producing MRSA have been
reported, indications are that the prevalence of MRSA and PVL-producing strains circulating
in the community is small.26 Although CA-MRSA strains are now a major problem in the
US,27 they are still relatively uncommon in Europe, and there is thus still an opportunity to
avoid the problem escalating to a similar same scale. CA-MRSA strains are reported not
only in UK, France, Switzerland, Germany, Greece, Ireland, Nordic countries, Netherlands
and Latvia.28 The burden of MRSA infections across Europe is reviewed in a 2010 survey by
Kock et al.29 who estimate that the proportion of CA-MRSA with respect to total MRSA
ranges between 1% and 2% in Spain and Germany and 29–56% in Denmark and Sweden.
Among outpatients with S. aureus infections, MRSA accounted for 6% in the Ligurian region
in Italy, 14% in Germany, 18% in France and 30% in Greece.
A report by Zafar et al. (2007) suggests that frequency of CA-MRSA colonisation among
household members of patients with CA-MRSA infections is higher than among the general
population. Among colonised household members, only half of MRSA strains were related to
the patients' infective isolate. Within the same household, multiple strains of CA-MRSA may
be present.30
More recently, Casper et al 201331 carried out a study to compare the prevalence of nasal S
aureus carriage and antibiotic resistance, including meticillin-resistant S aureus (MRSA), in
healthy patients across nine European countries. Nasal swabs were obtained from 32 206
patients recruited by family doctors in Austria, Belgium, Croatia, France, Hungary, Spain,
Sweden, the Netherlands, and the UK. Eligible patients were aged 4 years or older (≥18
years in the UK) and presented with a non-infectious disorder. S aureus was isolated from
6956 (21·6%) of 32 206 patients swabbed. The adjusted S aureus prevalence for patients
older than 18 years ranged from 12·1% (Hungary) to 29·4% (Sweden). Except for penicillin,
the highest recorded resistance rate was to azithromycin (from 1·6% in Sweden to 16·9% in
France). In total, 91 MRSA strains were isolated, and the highest MRSA prevalence was
reported in Belgium (2·1%). 53 different spa types were detected—the most prevalent were
t002 (n=9) and t008 (n=8). Overall the workers concluded that, generally, the prevalence of
resistance, including that of MRSA, was low. They found that the MRSA strains recorded
showed genotypic heterogeneity, both within and between countries.
2. Transmission of antibiotic resistant strains in the home and community
The following are studies in which the spread of antibiotic resistant strains in the home and
community has been identified. This includes studies where a family or family members
have become infected, and those where colonisation only has been detected.
2.1 Studies involving ESBL producing and multidrug resistant strains
Gottesman et al 200832 documented transmission of carbapenemase-producing Klebsiella
pneumoniae within a household, the source being a debilitated patient who returned home
after a long hospitalization. A 73-year-old man had a urologic procedure (transurethral
resection of the bladder neck) in a community hospital in early October 2007. He was initially
evaluated on September 23, 2007, at an outpatient clinic where a routine urine sample was
obtained for culture. Carbapenemase-producing K. pneumoniae was cultured. Identification
and susceptibility testing of the isolate were completed by using the VITEK 2 system
(bioMérieux, Marcy l'Etoile, France). K. pneumoniae carbapenemase was confirmed by
using the modified Hodge test. Two repeat urine cultures grew the same organism; however,
a stool culture was negative for carbapenemase-producing K. pneumoniae. The medical
history of the patient included treatment with high-intensity focused ultrasound in May 2007,
followed by transurethral resection of prostate in June 2007 which was performed in 2
different private hospitals, each requiring 24-hour hospitalization. No carbapenemaseproducing K. pneumoniae was documented in these hospitals. Two months before detection
of carbapenemase-producing K. pneumoniae, the patient received a 1-week course of oral
amoxicillin-clavulanate for presumed urinary tract infection, although urine culture obtained
on July 29, 2007 was sterile. Because the circumstances of strain acquisition and patient
characteristics were not typical for epidemiology of carbapenemase-producing K.
pneumoniae, he was further questioned about possible contacts of relevance. The patient
disclosed that his wife, who had amyotrophic lateral sclerosis that required mechanical
ventilation, had been hospitalized in a tertiary hospital in the Tel Aviv area for 9 weeks until
July 2007. After discharge, she has been staying at home where she was cared for by her
son, sister, and nurses; the patient stated that he had limited contact with his wife (he did not
participate in her care). The infection control unit of the tertiary hospital was contacted, and
the name of the wife was identified in the hospital registry. Carbapenemase-producing K.
pneumoniae was isolated from her urine on June 8, 2007. Despite limited contact, the
patient probably acquired carbapenemase-producing K. pneumoniae from his wife, who was
a documented carrier of this organism. Because his early urine cultures (taken after his wife
was discharged from hospital) were sterile, it was assumed that transmission of the
organism occurred at their home. They could not rule out that the strain was transferred by
an intermediary, such as the couple's son. It is unlikely that the organism was acquired at
the hospitals from which no case of carbapenemase-producing K. pneumoniae was
reported. Also, the patient had 2 negative urine cultures. Carbapenemase-producing K.
pneumoniae is a recent addition to the pool of multidrug-resistant nosocomial pathogens.
The strain can colonize the urinary, intestinal, and respiratory tracts, as well as wounds;
bloodstream infection is associated with higher death rates than infection at other sites.
Hand carriage is probably the biggest factor in transmission of extended-spectrum βlactamase producers, and there is little evidence to suggest that carriers of carbapenemaseproducing K. pneumoniae would be different. Environmental contamination plays a limited
role in transmission of the organism.
As stated previously, a 2013 study by Löhr et al in Norway demonstrates how infants may
be long-term faecal carriers of ESBL-producing Klebsiella pneumoniae after colonization
during hospitalization in the neonatal period.33 In this study, resistant K. pneumoniae were
detected in faecal samples from 20% of household contacts in 9/28 (32%) of households,
indicating that faecal ESBL carriage in otherwise healthy infants can be a reservoir for intrahousehold spread.
Cotter et al 201234 report a case of ESBL-producing E. coli bloodstream infection in a
healthcare worker associated with subsequent isolation of an indistinguishable strain from
one causing a urinary tract infection in his spouse.
As stated above, Kaame et al 201335 carried out a study to determine the prevalence of
ESBL-producing Enterobacteriaceae in faeces from healthy Swedish preschool children and
to establish whether transmission took place between children in preschools. Diapers from
children attending preschools in Uppsala city were collected during September to October
2010, and the faeces was cultured. A total of 313 stool specimens were obtained,
representing 24.5% of all preschool children in Uppsala city. The carriage rate of ESBLproducing Enterobacteriaceae was 2.9% among these healthy children. The corresponding
figure for patients in the same age group was 8.4%. E. coli with CTX-M type enzymes
predominated, and only one E. coli isolate carried genes-encoding CMY. CTX-M-producing
E. coli isolates with identical genotypes were found in children with no familial relation at two
different preschools. The authors concluded that the in this study, transmission of ESBLproducing E. coli was for the first time documented between children at the same preschool.
Poirel et al 201136 reported community acquisition of an NDM-1 producer. This case
involved a patient who, when hospitalized in France in early 2010, was found to be colonized
on her skin by an NDM-1-producing Escherichia coli. Although the patient had been living in
Darjeeling, India, there was no prior history of hospitalization in that country. The source of
colonization of this patient was not identified, but recent reports have demonstrated the
extensive isolation of NDM-1 from tap and environmental water in New Delhi, leading us to
speculate that exposure to contaminated water may account for this case. We report here on
the long-term follow-up of this patient over a period of 13 months, from initial hospitalization
until her death. Screening of this patient using rectal swabs yielded regular positive samples.
The patient had received two courses of antibiotics comprising co-amoxiclav (3 g daily) for
10 days at the time of identification of the colonization in March 2010 and then gentamicin
(250 mg daily) in an attempt to treat a urinary tract infection just prior to her demise. In our
view, those courses of antibiotic treatment are unlikely to have generated sufficient selective
pressure to account for the persistence of the NDM-1-positive E. coli in the intestinal flora of
the patient for >1 year. Indeed, such long-term persistence of E. coli in the environment and
in the intestinal flora is already known. The case reported here indicates the long-term
persistence of NDM-1-positive bacteria in the intestinal flora. This sustained level of carriage
may be considered as a further risk factor for the dissemination of NDM-1 producers, taking
into account that up to 108 E. coli per gram of faeces are commonly found in humans. This
observation also further underlines the urgent need to screen for carriers worldwide and the
fact that colonized patients should be kept in strict isolation during their entire hospital stay.
2.2 Studies of household and community spread involving MRSA
Household transmission of MRSA is most recently reviewed in a 2012 report by Davis et al.37
It is also reviewed in the IFH 20064 and 20125 reports. Some of the individual studies are
reviewed as follows:
2.2.1 Studies involving person to person spread
In recent years, a wide range of laboratory and field studies have been carried out that
focussed specifically on the spread of MRSA in a domestic setting. These include studies
which suggest person to person transmission either directly or via hands and surfaces. It
also includes studies show that, in situations where good hygiene practice is not observed,
S. aureus (including MRSA) are readily transferred in the home during normal daily activities
via hands, cleaning cloths, hand contact surfaces, clothing, linens and sometimes also via
the airborne route such that family members are regularly exposed.
The following examples are taken the IFH 20064 and 20125 reviews:
The potential for transmission to other family members where there is a family member in
the home carrying MRSA, is borne out by a number of investigations of health care workers
In studies of HCWs colonised with MRSA, the HCW was treated to eradicate the organism,
but subsequently became recolonised. In each case, MRSA was isolated from
environmental surfaces in the home of the HCW, including door handles, a computer desk
shelf and computer joystick, linens, furniture, and in some cases also from other family
members and family pets. The studies include
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Masterton et al. 199538 reported a UK outbreak of MRSA, where a nurse was found
to be colonised. The patient’s parents and fiancée, who shared the same house,
were also colonised with the same strain. The family was treated with antimicrobials
but this failed to eradicate the organism. Investigation of the home revealed MRSA
on door handles, a computer desk shelf and computer joystick in the patient’s
bedroom, but not elsewhere. The home was thoroughly vacuumed and damp dusted
and all pillows and bedding were replaced. After subsequent antimicrobial treatment,
three subsequent consecutive weekly cultures from the throat, both nostrils, groin
and armpit did not yield MRSA.
Allen et al. 199739 investigated a UK nurse who became colonised with MRSA.
Tests showed that carriage (nose, throat, armpit and perineum) was eliminated by
antimicrobial treatment, but each time the MRSA colonisation returned. During this
period both her son (probably due to storage of family toothbrushes in close
proximity) and husband also became colonised. Sampling showed MRSA
contamination on the three-piece suite, bedroom mattress, duvet, pillows and padded
headboard, living room carpets, dining room, hall and three bedrooms, living room
rug, dining chairs, kitchen stools, two items of clothing and a spare sofa bed in the
son’s bedroom. The problem was finally terminated after a co-ordinated commercial
cleaning of the house, thermal disinfection of all linen and replacement of soft
furnishings. Two weeks later repeat environmental samples were all negative for
MRSA and monthly screens of the nurse for six months, were also all negative.
Cefai et al. 1994 56 68 reported a case of two UK nurses (married to each other, one
of them caring for an infected patient) who were found to be nasal MRSA carriers.
Weekly checks for three weeks following antimicrobial treatment showed no MRSA.
Six months after the first isolation, a second patient was found to be colonised with
the organism. Repeat screening showed the same staff nurse and his wife were
colonised. At this time MRSA was isolated from a nose swab taken from the dog.
Kniehl et al. (2005)40 described a recent study in Germany, of healthcare workers
(HCWs) who had close and regular contact with MRSA-colonised patients. MRSA
was identified from nasal swabs of 87 workers treated with topical antimicrobials.
They were advised to disinfect their bathrooms and personal hygiene articles, and
wash bed linen and pillows. Seventy-three (84%) of HCWs lost their carrier status
when tested after three days, and this was maintained after further sampling over
three months. In 11 cases MRSA was detected, but only in "later" swabs, indicating
recolonisation. In eight of these 11 cases, screening identified colonisation of close
household contacts. Environmental sampling detected contamination in seven of the
eight home environments. Contaminated surfaces included pillows, bed linen,
brushes, cosmetics and hand contact surfaces, as well as household dust. When
eradication treatment was applied to household contacts and surfaces were cleaned
and disinfected, carriage cleared in most cases within a few weeks. However, when

home environments were heavily contaminated, despite adequate medical treatment,
eradication took up to two years.
de Boer et al 2006 studied use of gaseous ozone for eradication of methicillinresistant Staphylococcus aureus from the home environment of a colonized hospital
employee.41
A number of other individual cases are reported where family members in the home of
an infected person have been found to be colonised with MRSA (Hollis et al. 199542,
Hollyoak et al. 199543, L’Heriteau et al. 199944, Shahin et al. 199945).
 The potential for intrafamilial transmission is demonstrated by the case study
reported by Hollis et al. who found that following the identification of an index case (a
sibling infected with MRSA), two other siblings in the home and the mother became
infected or colonised. The study suggested that transmission of the MRSA strain
occurred at least three times within this family, and that at least one family member
was colonised with the same strain for up to seven months or more.
 A study by Mitsuda et al 199946 shows how HCWs may become a source of MRSA
infection for their own families as well as for patients.
 A study by Calfee et al. (2003)47 suggested that MRSA colonisation occurs
frequently amongst home and community contacts of patients with nosocomiallyacquired MRSA. MRSA was isolated from 14.5% of 172 individuals who were the
household/community contacts of 88 MRSA colonised patients discharged from a
hospital in Virginia, USA. Household contacts who had close contact with the patient
were 7.5 times more likely to be colonised than those who had less frequent contact
(53% vs. 7%). In each case, analysis of antimicrobial susceptibility and DNA patterns
suggested that the MRSA isolated from the household contact was identical, or
closely related, to that carried by the index patient indicating person-to-person
spread.
 Most recently, a study of the impact of hygiene on transmission of what was likely to
be an outbreak of CA-MRSA in a community setting has been reported. Turabelidze
et al. 200648 carried out a case-control study, involving 55 culture-confirmed cases of
MRSA in a prison in the USA to examine risk factors for MRSA infection with a focus
on personal hygiene factors. An interviewer collected information about relevant
medical history, personal hygiene factors (including hand washing, shower, laundry
practices, and sharing personal items), use of gymnasium and barbershop, and
attendance of educational classes. The risk for MRSA infection increased with lower
frequency of hand washing per day and showers per week. Inmates who washed
their hands ≤six times per day had an increased risk for infection compared with that
of inmates who washed their hands >12 times per day. Inmates who took seven
showers per week had an increased risk for infection compared to that of inmates
who took >14 showers per week. In addition patients were also less likely than
controls to wash personal items (80.0% vs. 88.8%) or bed linens (26.7% vs. 52.5%)
themselves instead of using the prison laundry. When personal hygiene factors were
examined for cases and controls, patients were more likely than controls to share
personal products (e.g., cosmetic items, lotion, bedding, toothpaste, headphones),
especially nail clippers (26.7% vs. 10%) and shampoo (13.3% vs. 1.3%), with other
inmates. To evaluate an overall effect of personal hygiene practice on MRSA
infection, a composite hygiene score was created on the basis of the sum of scores
of three individual hygiene practices, including frequency of hand washing per day,
frequency of a shower per week, and number of personal items shared with other
inmates. A significantly higher proportion of case-patients than controls had lower
hygiene scores (<six) (46.7% vs. 20.0%).
 In a study by Nguyen et al 2005, sharing of towels and soap was identified as
significant risk factors in recurrent outbreaks of CA-MRSA in a football team in the
USA.49
Other studies which indicate household person to person transmission, including very recent
studies, are as follows:
 A 2007 report by Robotham et al illustrates how infected patients discharged from
hospitals may continue to carry MRSA, even after their infection has healed, and pass it
on to healthy family members who become colonised, thereby spreading the organism
into the community and then back into hospitals.50
 Lis et al. 2009 evaluated the airborne Staphylococcus genus features in homes in which
inhabitants have had contact with the hospital environment and found a higher
prevalence of methicillin-resistant (MR) strains among the species isolated (40% of S.
epidermidis, 40% of S. hominis, and 60% of S. cohnii spp cohnii) was found in homes of
persons who had contact with a hospital environment compared with the reference
homes (only 12% of S. hominis).51
 Lautenbach et al 201052 identified eight consecutive patients who presented with a skin
or soft tissue infection due to MRSA. Of seven household members of these cases, three
were colonised with MRSA. The mean duration of MRSA colonisation in index cases was
33 days (range 14–104), while mean duration of colonisation in household cases was 54
days (range 12–95). There was a borderline significant association between having a
concurrent colonised household member and a longer duration of colonisation (mean 44
days vs. 26 days, P=0.08).
 Heelan et al 201153 report a case of four siblings, three brothers whose atopic dermatitis
was complicated by cutaneous lesions and furunculosis, while their 21-month-old sister
had a fatal PVL positive staphylococcal pneumonia.
 Uhlemann et al 201154 carried out a case-control study which showed that household
environmental contamination with community-acquired MRSA USA300 was associated
with re-infection of index case patients,uhlemann 61 suggesting that contamination of the
household also has consequences for clinical disease. The study was a communitybased, case-control study investigating socio-demographic risk factors and infectious
reservoirs associated with MRSA infections. Case patients presented with CA-MRSA
infections to a New York hospital. Age-matched controls without infections were randomly
selected from the hospital’s Dental Clinic patient population. During a home visit, case
and control subjects completed a questionnaire, nasal swabs were collected from index
respondents and household members and standardised environmental surfaces were
swabbed. Genotyping was performed on S. aureus isolates. They enrolled 95 case and
95 control subjects. Cases more frequently reported diabetes mellitus and a higher
number of skin infections among household members. Among case households, 53
(56%) were environmentally contaminated with S. aureus, compared to 36 (38%) control
households (p = .02). MRSA was detected on fomites in 30 (32%) case households and 5
(5%; p,.001) control households. More case patients, 20 (21%) were nasally colonised
with MRSA than were control indexes, 2 (2%; p,.001). In a subgroup analysis, the clinical
isolate (predominantly USA300), was more commonly detected on environmental
surfaces in case households with recurrent MRSA infections (16/36, 44%) than those
without (14/58, 24%, p = .04). The authors concluded that the higher frequency of
environmental contamination of case households with S. aureus in general, and MRSA in
particular, implicates this as a potential reservoir for recolonisation and increased risk of
infection. Environmental colonisation may contribute to the community spread of epidemic
strains such as USA300.
 Miller et al 201255 carried out a study to investigate the epidemiologic characteristics of
S. aureus household transmission. They performed a cross-sectional study of adults and
children with S. aureus skin infections and their household contacts in Los Angeles and
Chicago. Subjects were surveyed for S. aureus colonisation of the nares, oropharynx,
and inguinal region and risk factors for S. aureus disease. All isolates underwent genetic
typing. Results We enrolled 1162 persons (350 index patients and 812 household
members). The most common infection isolate characteristic was ST8/SCCmec IV, PVL1
MRSA (USA300) (53%). S. aureus colonised 40% (137/350) of index patients and 50%
(405/812) of household contacts. A nares-only survey would have missed 48% of S.
aureus and 51% of MRSA colonised persons. Sixty-five percent of households had .1 S.
aureus genetic background identified and 26% of MRSA isolates in household contacts
were discordant with the index patients’ infecting MRSA strain type. Factors
independently associated with the index strain type colonising household contacts were
recent skin infection, recent cephalexin use, and USA300 genetic background. The
authors concluded that, Conclusions In the study population, USA300 MRSA appeared
more transmissible among household members compared with other S. aureus genetic
backgrounds. Strain distribution was complex; .1 S. aureus genetic background was
present in many households. S. aureus decolonisation strategies may need to address
extra-nasal colonisation and the consequences of eradicating S. aureus genetic
backgrounds infrequently associated with infection.
A number of recent studies have examined the extent to which MRSA strains may be found
in home and community settings:
 Scott et al 2008 studied 35 homes of healthcare and non–healthcare workers, each with
a child in diapers and a cat or dog, was recruited from the Boston area between January
and April 2006. In each home, 32 surfaces were sampled in kitchens, bathrooms, and
living areas. S. aureus was found in 34 of the 35 homes (97%) and was isolated from all
surfaces in 1 or more homes, with the exception of the kitchen chopping board and the
child training potty. MRSA was isolated from 9 of 35 homes (26%) and was found on
kitchen and bathroom sinks, countertops, kitchen faucet handle, kitchen drain, dish
sponge/cloth, dish towel, tub, infant high chair tray, and pet food dish. A positive
correlation was indicated for the presence of a cat and isolation of MRSA from surfaces.56
 Roberts et al (2011)57 studied the presence of MRSA on 509 frequently touched
nonhospital environmental surfaces at university, student homes and local community
sites. Twenty-four isolates from 21 (4.1%, n = 509) surfaces were MRSA positive and
included ten (11.8%, n = 85) student house samples, eight (2.7%, n = 294) university
samples and three (2.3%, n = 130) community samples. MRSA-positive university
samples were isolated from the bathroom, floors, ATM keypads, elevator buttons, locker
handles, but not computer keyboards. Two university ATM keypads were sampled nine
times over a 6-month time period. During that time, one keypad was positive 3 (33%, n =
9) times for S. aureus including twice for MRSA and MSSA, while the other was positive 4
(44%, n = 9) for S. aureus including once with MRSA and three times with MSSA. Genetic
relatedness of S aureus USA300 (strain ST8) isolates collected from domestic and public
surfaces on a university campus suggests transfer between the community and the
household.
Davis et al37 cite a number of further, mostly recent, studies which indicate transmission of
MRSA in the home (Lucet et al 200958, Mollima et al 201059, Eveillard et al 200460, Faires et
al 200961, Huang et al 200762, Johanson 200763, Zafar et al 200764, Fritz et al 201265, Nerby
et al 201166). From their assessment of the data, they make a number of observations:
 Whereas hospital and public community settings are characterised by transient contact
by a diverse population, households have high-intensity contact between the same
individuals. As a result, transmission dynamics within households might differ from those
of public settings.
 Rates of transmission between positive case patients and household members range
from less than 10% to 43%. However, molecular characterisation of isolates is
important, because studies reported lower rates of transmission when household
members were assessed for strains related to the one identified in the index patient than
when assessed for colonisation with any strain.





The number of household contacts may affect transmission rates Nerby et al 2011
report that 25% of households had at least one contact colonised with MRSA and 9%
had more than one contact colonised. Some, but not all, studies noted that households in
which transmission occurs have a higher than average number of human occupants
suggesting that people in large households might have direct contact more frequently,
increasing the likelihood of transmission.
Crowding, residence in subsidised housing or shelter, and residence in regions with high
rates of incarceration are risk factors for MRSA skin and soft-tissue infections.
Duration of human colonisation might be important for household transmission because
long colonisation time might increase the number of opportunities for a transfer event.
They assessed that colonisation lasts from 2 weeks to months in index patients, with
much the same time for household contacts, but with a wide range
A study of patients colonised with MRSA67 suggested carriers had intermittent negative
results 26% of the time and intermittent carriers more frequently developed clinical
MRSA infection during the study than did other carrier types,81 which emphasises the
importance of longitudinal monitoring and of reexposure from household sources.
An estimated 20% of people are persistent carriers who remain positive for MRSA for
months or years. Even after decolonisation treatment, these people might be recolonised
preferentially with the previously persistent strain if exposed to multiple strains.85 This
effect makes decontamination of the home particularly crucial for strategies to decolonise
persistent carriers.
2.2.2 Domestic animals as sources of S. aureus exposure in the home
Domestic pets can also be a source of S. aureus, including MRSA and PVL-producing
strains. Although little information is available on the prevalence of MRSA in the domestic
animals, isolation from household pets has been documented. The following is taken from
appendix section of the 2012 IFH review5:






Cefai et al. (1994)68 reported persistent carriage of MRSA in a health-care worker where
the source or colonisation/recolonisation was identified as a domestic dog.
Manian et al. (2003)69 described two dog owners suffering from persistent MRSA
infection, who suffered from relapses whenever they returned home from the hospital.
Further investigation revealed that their dog was carrying the same strain of MRSA.
van Duijkeren et al. (2004)70 isolated MRSA from the nose of a healthy dog, the owner
of which worked in a Dutch nursing home and was colonised with MRSA. Typing of the
staphylococcal chromosome showed that the MRSA strains were identical.
Rankin et al. (2005)71 carried out a study to determine the presence of S. aureus PVL
toxin genes in MRSA strains isolated from companion animals. Eleven MRSA isolates
from 23 animals were found to be positive for the PVL toxin genes as well as for
methicillin resistance (mecA) genes.
Enoch et al. (2005)72 reported a pet therapy dog that acquired MRSA in a UK hospital
after visiting care-of-elderly wards. The dog and owner were asymptomatic and had no
observable source of MRSA. Two other pet therapy dogs, screened before visiting the
hospital, were found to be MRSA negative. Further investigations suggested that the dog
was colonised by contact with a human carrier.
A colonisation prevalence of study in clinically normal dogs by Vengust et al. in 2006 in
Ontario, Canada reported that at present Methicillin-resistant Staphylococcus
intermedius (MRSI) is not considered to be a significant zoonotic concern; however, it
may become an important pathogen in dogs. Although Methicillin-resistant coagulase
negative staphylococci mostly cause disease in compromised human or animal hosts,
these bacteria can serve as reservoirs of resistance determinants in the community,
which could lead to the emergence of novel MRSA strains.73

Sing et al. (2008) reported transmission of PVL-positive MRSA between a symptomatic
woman and both her asymptomatic family and their healthy pet cat. This case illustrates
that MRSA transmission also occurs between humans and cats and that pets should be
considered as possible household reservoirs of MRSA that can cause infection or
reinfection in humans.74
Transmission of S. aureus (including MRSA) between humans and cats and dogs is further
reviewed by Oehler et al. (2009).75 Several workers have noted that MRSA in pets is closely
linked to MRSA in humans and concluded that that the source of MRSA in pets or other
animals may often be colonised or infected humans, although this is by no means proven.76
A one day survey conducted at a veterinary hospital in February 2004 by Loeffler et al.
200577 identified MRSA carriage in 17.9% of veterinary staff, 9% of dogs, and 10% of
environmental sites. CA-MRSA has also been identified in livestock animals (particularly
pigs), veterinarians, and animal farm workers. Angelo et al. (2009) reported a case of
infection in a pig-farm worker in an animal farming area in Italy. The infection was caused by
MRSA of swine origin, ST398.78 Veterinary staff and owners of MRSA-infected pets are high
risk groups for MRSA carriage despite not having direct hospital links. As part of a UK-wide
case-control study investigating risk factors for MRSA infection in dogs and cats between
2005 and 2008, 608 veterinary staff and pet owners in contact with 106 MRSA and 91
methicillin-susceptible S. aureus (MSSA)-infected pets were screened for S. aureus nasal
carriage. This study indicated for the first time an occupational risk for MRSA carriage in
small animal general practitioners.79
In a 2011 review, Kassem et al conclude that, besides humans, perhaps the most important
community reservoirs of staphylococci are pets and livestock.80. He cites evidence showing
that MRSA has been isolated from pigs, horses, dogs, cats, cattle, sheep, chinchillas, and
parrots. Targeted sampling suggests that up to 8% of dogs, 12% of horses, 15% of
lactating cows, 14.3% of broiler farms, and 68% of fattening pig farms were potentially
positive for MRSA. In many cases, MRSA clones from animals were shared by their owners
and/or handlers, suggesting the possibility for MRSA transmission between animals and
humans
In their 2011 review Davis et al37 cite a number of further recent studies which indicate the
role of pets in transmission of MRSA in the home (Baptiste 200581 Weese et al 2006
82
..Faires et al 200983, Ferierra 201184, Morris et al 201085. Loeffi 201086 ,Weese et al 2010
87
, Heller et al 2011 88, Walther et al 2012.89
From their assessment of the data, Davis et al make a number of observations:



Prevalences of S aureus and MRSA in people tend to equal or surpass
prevalences in pets. Prevalence of MRSA in 122 households with 242 people
living with pets (132 dogs and 161 cats) was 3.3% for people, 1.5% for dogs, and
0ｷ0% for cats, whereas the prevalence of meticillin-susceptible S aureus was
27.7% for people, 14.4% for dogs, and 4.3% for cats.
Strain relatedness between staphylococcal isolates from people and animals
within households tends to be similar to those between human household
members. Although discovery of related strains in both people and animals
suggests that transmission has occurred, it does not show the direction of
movement (from people to animals, vice versa, or from a common source).
in addition to contact with veterinary clinics, surgery, and antimicrobial use, risk
factors for pet colonisation with S aureus include contact with children and licking
behaviours.106 Interactions between children and pets within households might



involve direct face-to-face contact through licking and biting, or indirect contact
through shared environments.
As in people, non-nasal anatomical sites—such as the mouth, perineum, and
inguinal skin—are often colonised or contaminated with S aureus in dogs and
cats. A positive dorsal fur site100 is probably a result of contamination from
human hand or mouth contact; such contamination might be important for
transmission but might not be indicative of pet colonisation status.
Several studies have estimated transmission rates between people and pets. In
households with an MRSA positive pet, the prevalence of human carriage was
27%. (Faires 2009).
In a case-control study of 49 MRSA-positive people with skin and soft-tissue
infection and 50 MRSA negative controls, colonisation with an identical MRSA
strain occurred in four in-contact pets (two dogs, a cat, and a hamster), but in
none of the pets from control households.84 The low transmission rates might be a result
of the methods; pets were sampled by nasal swab only.
Pets other than dogs and cats might also be important for transmission. Davis et al
37 cite studies showing that clinical S aureus isolates, including MRSA, have been
identified in parrots and other birds, rabbits, hamsters and guinea pigs, rats, small
ruminants, iguanas, a turtle, and bats.
Medhus et al 2012 report isolation of MRSA with the novel mecC gene variant from a cat
suffering from chronic conjunctivitis.90
2.2.3 Food as a source of MRSA transmission in the home
Van loo et al.91 found 36 S. aureus strains in 79 meat samples (including 2 samples
containing MRSA). Furthermore, low amounts of S. aureus are regularly found in meat sold
to consumers demonstrating that MRSA has entered the food chain. Persoons et al92 in
2009 confirmed the presence of MRSA in broiler chickens indicating that MRSA may persist
in farm environments. Van Loo et al. concluded that the contamination of food products may
be a potential threat for the acquisition of MRSA by those who handle the food.
3. The revolving door – the cycling of antibiotic resistant strains between homes and
healthcare settings
A few studies have looked specifically at issues related to the cycling of antibiotic resistant
strains between home and healthcare settings:
Otter and French 200893 identified probable community-associated (CA-MRSA) infection in
65 patients with evidence of injecting drug use or alcohol abuse between 2000 and 2006.
Only 18 (27.7%) of the infections were defined as community-acquired. However, patients in
this group often have previous hospital admissions for other reasons and their infections
may originally have been acquired in the community. A further 26 (40%) were communityonset infections following a previous hospitalisation, many of which were related to IDU or
alcohol abuse.
Milstone et al 201194 carried out a study to determine whether MRSA colonization outside
hospital is a predictor of subsequent infection in hospitalized children. Children admitted to a
pediatric intensive care unit between March 2007 and March 2010 were included in the
study. Anterior naris swabs were cultured to identify children with MRSA colonization at
admission. MRSA admission prevalence among 3140 children was 4.9%. Overall, 56
children (1.8%) developed an MRSA infection, including 13 (8.5%) colonized on admission
and 43 (1.4%) not colonized on admission (relative risk [RR], 5.9; 95% confidence interval
[CI], 3.4–10.1). Of those, 10 children (0.3%) developed an MRSA infection during their
hospitalization, including 3 of 153 children (1.9%) colonized on admission and 7 of 2987
children (0.2%) not colonized on admission (RR, 8.4; 95% CI, 2.7–25.8). African-Americans
and those with public health insurance were more likely to get a subsequent infection (P <
.01 and P = .03, respectively).
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