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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 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: 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 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 studies865 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 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 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 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 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 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 β-lactamase producers, and there is little evidence to suggest that carriers of carbapenemase-producing 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 2006Error: Reference source not found and 2012Error: Reference source not found 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 2006Error: Reference source not found and 2012Error: Reference source not found 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 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 Error: Reference source not found 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 1995 42, 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 1999 46 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 nosocomially-acquired 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 (