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Non-slip socks: a potential reservoir for transmitting multidrug-resistant organisms in hospitals?
Journal of Hospital Infection xxx (2016) 1e3 Available online at www.sciencedirect.com
Journal of Hospital Infection journal homepage: www.elsevierhealth.com/journals/jhin
Short report
Non-slip socks: a potential reservoir for transmitting multidrug-resistant organisms in hospitals? N. Mahida, T. Boswell* Department of Clinical Microbiology, Nottingham University Hospitals NHS Trust, Nottingham, UK
A R T I C L E
I N F O
Article history: Received 24 May 2016 Accepted 16 June 2016 Available online xxx Keywords: Fall Multidrug-resistant organisms Non-slip sock Meticillin-resistant Staphylococcus aureus Vancomycin-resistant enterococci
S U M M A R Y
Non-slip socks are increasingly used to prevent falls in hospitals. Patients use them to walk to various parts of the hospital and also wear them in bed. Fifty-four pairs of socks and 35 environmental floor samples were obtained from seven wards in a tertiary referral hospital. Vancomycin-resistant enterococci (VRE) were detected from 46 (85%) socks and meticillin-resistant Staphylococcus aureus (MRSA) from five (9%). Environmental sampling cultured VRE from 24 (69%) floor samples and MRSA from six (17%) floor samples. Clostridium difficile was not detected from any sample. Non-slip socks may become contaminated with multidrug-resistant pathogens and may form a potential route for cross-transmission. ª 2016 Published by Elsevier Ltd on behalf of The Healthcare Infection Society.
Introduction Falls and fall-related injuries occur frequently within acute healthcare settings. People aged 65 years have the highest risk of falling, with 30% of people aged >65 years, and 50% of people aged >80 years, falling at least once a year.1 National guidelines recommend that a multi-factorial, falls risk assessment should be considered for all patients aged 65 years who are admitted to hospital, including an assessment of footwear.1 In response to patients admitted with unsuitable or inappropriate footwear, our hospital, like many other * Corresponding author. Address: Department of Clinical Microbiology, Nottingham University Hospitals NHS Trust, QMC Campus, Derby Road, Nottingham NG7 2UH, UK. Tel.: þ44 (0)115 9249924x61161; fax: þ44 (0)115 970 9767. E-mail address: [email protected] (T. Boswell).
healthcare organizations, has introduced non-slip socks to reduce falls.2,3 These socks are worn by elderly patients who are admitted to acute medical wards, who are able to walk, but who are at risk of falling through the lack of appropriate footwear. Non-slip socks are single-use medical device items but the frequency with which they should be changed is unclear. Hence patients may wear these socks for a short period of hours or possibly several days. In addition, investigators noted that patients not only use them to walk to various parts of the hospital during the inpatient journey e including toilets, radiology departments, coffee shops, restaurants e but also wear them in bed. These socks are made of cotton and polyester, terrycloth lined, with treads added to improve underfoot traction. This study evaluates whether non-slip socks may be become contaminated with multidrug-resistant organisms (MDROs)
http://dx.doi.org/10.1016/j.jhin.2016.06.018 0195-6701/ª 2016 Published by Elsevier Ltd on behalf of The Healthcare Infection Society. Please cite this article in press as: Mahida N, Boswell T, Non-slip socks: a potential reservoir for transmitting multidrug-resistant organisms in hospitals?, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.06.018
2
N. Mahida, T. Boswell / Journal of Hospital Infection xxx (2016) 1e3
found on the floor and potentially lead to cross-transmission of pathogens to patients.
Methods Non-slip socks (Medline Industries, Knutsford, UK) were collected from seven wards across two hospital sites in a tertiary referral centre. Socks were anonymously collected from patients by offering a new pair of non-slip socks in exchange for the in-use pair. Each pair of socks was placed in a sterile bag and transported to the laboratory. Socks were processed on the same day by selecting one sock from the pair and cutting it into four quarters. One-quarter (which formed the sole of the sock) was placed in a sterile container and 100 mL of braineheart infusion broth (BHI; Oxoid, Basingstoke, UK) added. Fifteen pairs of unused (new) socks were also processed using the same method, with 10 pairs interspersed between the used/dirty socks. On each ward where socks were collected, five floor areas (two ward corridors, three toilets) were sampled using a Polywipe sponge (Medical Wire and Equipment, Corsham, UK). Washed microfibre mop heads for cleaning floors, which are normally re-used after high temperature laundering, were also collected. These were sampled by cutting a 5 cm by 5 cm section from the centre of the mop head as well as fibres from the edge of the mop. Sponges and the two samples from each mop head were placed in sterile containers and 100 mL of BHI broth added. Following overnight immersion of the samples in broths, 10 mL loops were used to inoculate vancomycin-resistant enterococci agar (VRE Oxoid, UK), meticillin-resistant Staphylococcus aureus agar (MRSA; E&O, Bonnybridge, UK) and Braziers agar (E&O, UK) used for detecting Clostridium difficile. After incubation, bacterial colonies of interest were identified using Vitek-2 (bioMe ´rieux, Basingstoke, UK), and where appropriate also underwent sensitivity testing by disc diffusion.4 The hospital patient administration system was interrogated to determine whether there were any patients with MDROs on the ward at the time of sample collection.
Results Fifty-four pairs of socks and 35 environmental floor samples were collected. VRE were detected from 85% of socks with Enterococcus faecium cultured in 44 samples and E. faecalis in two samples (Table I). VRE were also abundant on the floor with E. faecium found in 21 samples, E. gallinarum in two, and E. faecalis in one (Table I). Substantial levels of MRSA were also detected from socks (9%) and floor (17%) samples. Clostridium difficile was not detected from any socks or floor samples. Fifteen pairs of unused (new) socks and 20 samples from 10 laundered mop heads did not culture VRE, MRSA, or C. difficile.
Discussion Hospital floors are known to be reservoirs of potentially pathogenic bacteria, and the recovery of VRE from 69% of floor samples is somewhat surprising, especially in the absence of any specific known clinical problems or outbreaks. Previous
Table I Recovery of multidrug-resistant organisms from socks and floor samples; and numbers of patients known to have carriage from hospital administration system
Used socks (54 samples) Floor (35 samples) Patients with carriage on hospital system
Vancomycinresistant enterococci
Meticillinresistant Staphylococcus aureus
Clostridium difficile
46 (85%)
5 (9%)
0
24 (69%)
6 (17%)
0
3
2
4
studies have demonstrated that even after cleaning floors using a disinfectant, which achieves a 94e99% reduction in bacterial numbers, contamination returns to the same levels within a few hours.5,6 In the past, most authorities have agreed that the risk of cross-transmission of pathogens from these surfaces is low.5,7,8 However, the introduction of non-slip socks into the healthcare environment is relatively new and their effect on healthcare-associated pathogens has not been previously considered. High levels of contamination with VRE (85%) and MRSA (17%) were detected from socks which are often used by patients to walk to numerous areas within the hospital and also worn while in bed. It is therefore possible that MDROs are gathered by non-slip socks from the floor, with subsequent transmission on to hospital bedsheets and the patient. Mops and clean pairs of socks were also sampled, which excluded contamination during laundering of mop heads or manufacture of these socks. In addition, interspersing clean socks with dirty socks during laboratory processing also confirmed that there was no cross-contamination in the methodology. There are several limitations to this study. It was carried out in one centre with a small number of samples. The length of time the socks were worn by patients was not recorded, which could affect the likelihood of contamination. The use of a hospital administration system is an imperfect indicator of colonization with these organisms and hence the true rates of patient carriage may be higher. The range of pathogens considered was limited and did not assess for contamination with carbapenemase-producing Enterobacteriaceae or multiresistant acinetobacter. However, clinical infections due to these organisms at our centre are low, compared to MRSA, VRE, and C. difficile. In addition, there was no comparison to patient’s slippers or bare feet walking, hence it remains unclear whether the materials from which the socks are made promote contamination. Finally, BHI broth was used to enrich low levels of bacteria and hence it was not possible to assess for the exact levels of contamination on the socks or the floor. Non-slip socks are single-use items and should be discarded following usage. However, single-use is a vague term in the context of non-slip socks because patients wear them continuously. Hence, it is possible for patients to wear the same pair of socks for a few hours, few days or even weeks while in hospital. In this context it is probably more accurate to describe them as being for single patient use.
Please cite this article in press as: Mahida N, Boswell T, Non-slip socks: a potential reservoir for transmitting multidrug-resistant organisms in hospitals?, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.06.018
N. Mahida, T. Boswell / Journal of Hospital Infection xxx (2016) 1e3 In conclusion, this study demonstrates that non-slip socks may become contaminated with MDROs and could lead to transmission of healthcare-associated pathogens. Although the study has not demonstrated direct transmission of pathogens from the floor to the patient, it suggests a potential route that thus far has not been considered. Conflict of interest statement None declared. Funding sources None.
References 1. National Institute for Health and Clinical Excellence. Falls: assessment and prevention of falls in older people. London: NICE; 2013. Available from: https://www.nice.org.uk/guidance/cg161 [last accessed June 2016].
3
2. Ford S. Trust introduces red socks to identify falls risk patients. Nursing Times, May 10th, 2013. Available from: http://www. nursingtimes.net/nursing-practice/specialisms/older-people/trustintroduces-red-socks-to-identify-falls-risk-patients/5058445.article [last accessed June 2016]. 3. Sinha SK, Detsky AS. Measure, promote, and reward mobility to prevent falls in older patients. JAMA 2012;308:2573e2574. 4. Howe RA, Andrews JM; BSAC Working Party on Susceptibility Testing. BSAC standardized disc susceptibility testing method (version 11). J Antimicrob Chemother 2012;67:2783e2784. 5. Dancer SJ. Mopping up hospital infection. J Hosp Infect 1999;43:85e100. 6. Ayliffe GAJ, Collins DM, Lowbury EJL. Cleaning and disinfection of hospital floors. Br Med J 1966;2:442e445. 7. Ayliffe GA. Role of the environment of the operating suite in surgical wound infection. Rev Infect Dis 1991;13:S800eS804. 8. Maki DG, Alvarado CJ, Hassemer CA, Zilz MA. Relation of the inanimate hospital environment to endemic nosocomial infection. N Engl J Med 1982;307:1562e1566.
Please cite this article in press as: Mahida N, Boswell T, Non-slip socks: a potential reservoir for transmitting multidrug-resistant organisms in hospitals?, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.06.018
Journal of Hospital Infection journal homepage: www.elsevierhealth.com/journals/jhin
Short report
Non-slip socks: a potential reservoir for transmitting multidrug-resistant organisms in hospitals? N. Mahida, T. Boswell* Department of Clinical Microbiology, Nottingham University Hospitals NHS Trust, Nottingham, UK
A R T I C L E
I N F O
Article history: Received 24 May 2016 Accepted 16 June 2016 Available online xxx Keywords: Fall Multidrug-resistant organisms Non-slip sock Meticillin-resistant Staphylococcus aureus Vancomycin-resistant enterococci
S U M M A R Y
Non-slip socks are increasingly used to prevent falls in hospitals. Patients use them to walk to various parts of the hospital and also wear them in bed. Fifty-four pairs of socks and 35 environmental floor samples were obtained from seven wards in a tertiary referral hospital. Vancomycin-resistant enterococci (VRE) were detected from 46 (85%) socks and meticillin-resistant Staphylococcus aureus (MRSA) from five (9%). Environmental sampling cultured VRE from 24 (69%) floor samples and MRSA from six (17%) floor samples. Clostridium difficile was not detected from any sample. Non-slip socks may become contaminated with multidrug-resistant pathogens and may form a potential route for cross-transmission. ª 2016 Published by Elsevier Ltd on behalf of The Healthcare Infection Society.
Introduction Falls and fall-related injuries occur frequently within acute healthcare settings. People aged 65 years have the highest risk of falling, with 30% of people aged >65 years, and 50% of people aged >80 years, falling at least once a year.1 National guidelines recommend that a multi-factorial, falls risk assessment should be considered for all patients aged 65 years who are admitted to hospital, including an assessment of footwear.1 In response to patients admitted with unsuitable or inappropriate footwear, our hospital, like many other * Corresponding author. Address: Department of Clinical Microbiology, Nottingham University Hospitals NHS Trust, QMC Campus, Derby Road, Nottingham NG7 2UH, UK. Tel.: þ44 (0)115 9249924x61161; fax: þ44 (0)115 970 9767. E-mail address: [email protected] (T. Boswell).
healthcare organizations, has introduced non-slip socks to reduce falls.2,3 These socks are worn by elderly patients who are admitted to acute medical wards, who are able to walk, but who are at risk of falling through the lack of appropriate footwear. Non-slip socks are single-use medical device items but the frequency with which they should be changed is unclear. Hence patients may wear these socks for a short period of hours or possibly several days. In addition, investigators noted that patients not only use them to walk to various parts of the hospital during the inpatient journey e including toilets, radiology departments, coffee shops, restaurants e but also wear them in bed. These socks are made of cotton and polyester, terrycloth lined, with treads added to improve underfoot traction. This study evaluates whether non-slip socks may be become contaminated with multidrug-resistant organisms (MDROs)
http://dx.doi.org/10.1016/j.jhin.2016.06.018 0195-6701/ª 2016 Published by Elsevier Ltd on behalf of The Healthcare Infection Society. Please cite this article in press as: Mahida N, Boswell T, Non-slip socks: a potential reservoir for transmitting multidrug-resistant organisms in hospitals?, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.06.018
2
N. Mahida, T. Boswell / Journal of Hospital Infection xxx (2016) 1e3
found on the floor and potentially lead to cross-transmission of pathogens to patients.
Methods Non-slip socks (Medline Industries, Knutsford, UK) were collected from seven wards across two hospital sites in a tertiary referral centre. Socks were anonymously collected from patients by offering a new pair of non-slip socks in exchange for the in-use pair. Each pair of socks was placed in a sterile bag and transported to the laboratory. Socks were processed on the same day by selecting one sock from the pair and cutting it into four quarters. One-quarter (which formed the sole of the sock) was placed in a sterile container and 100 mL of braineheart infusion broth (BHI; Oxoid, Basingstoke, UK) added. Fifteen pairs of unused (new) socks were also processed using the same method, with 10 pairs interspersed between the used/dirty socks. On each ward where socks were collected, five floor areas (two ward corridors, three toilets) were sampled using a Polywipe sponge (Medical Wire and Equipment, Corsham, UK). Washed microfibre mop heads for cleaning floors, which are normally re-used after high temperature laundering, were also collected. These were sampled by cutting a 5 cm by 5 cm section from the centre of the mop head as well as fibres from the edge of the mop. Sponges and the two samples from each mop head were placed in sterile containers and 100 mL of BHI broth added. Following overnight immersion of the samples in broths, 10 mL loops were used to inoculate vancomycin-resistant enterococci agar (VRE Oxoid, UK), meticillin-resistant Staphylococcus aureus agar (MRSA; E&O, Bonnybridge, UK) and Braziers agar (E&O, UK) used for detecting Clostridium difficile. After incubation, bacterial colonies of interest were identified using Vitek-2 (bioMe ´rieux, Basingstoke, UK), and where appropriate also underwent sensitivity testing by disc diffusion.4 The hospital patient administration system was interrogated to determine whether there were any patients with MDROs on the ward at the time of sample collection.
Results Fifty-four pairs of socks and 35 environmental floor samples were collected. VRE were detected from 85% of socks with Enterococcus faecium cultured in 44 samples and E. faecalis in two samples (Table I). VRE were also abundant on the floor with E. faecium found in 21 samples, E. gallinarum in two, and E. faecalis in one (Table I). Substantial levels of MRSA were also detected from socks (9%) and floor (17%) samples. Clostridium difficile was not detected from any socks or floor samples. Fifteen pairs of unused (new) socks and 20 samples from 10 laundered mop heads did not culture VRE, MRSA, or C. difficile.
Discussion Hospital floors are known to be reservoirs of potentially pathogenic bacteria, and the recovery of VRE from 69% of floor samples is somewhat surprising, especially in the absence of any specific known clinical problems or outbreaks. Previous
Table I Recovery of multidrug-resistant organisms from socks and floor samples; and numbers of patients known to have carriage from hospital administration system
Used socks (54 samples) Floor (35 samples) Patients with carriage on hospital system
Vancomycinresistant enterococci
Meticillinresistant Staphylococcus aureus
Clostridium difficile
46 (85%)
5 (9%)
0
24 (69%)
6 (17%)
0
3
2
4
studies have demonstrated that even after cleaning floors using a disinfectant, which achieves a 94e99% reduction in bacterial numbers, contamination returns to the same levels within a few hours.5,6 In the past, most authorities have agreed that the risk of cross-transmission of pathogens from these surfaces is low.5,7,8 However, the introduction of non-slip socks into the healthcare environment is relatively new and their effect on healthcare-associated pathogens has not been previously considered. High levels of contamination with VRE (85%) and MRSA (17%) were detected from socks which are often used by patients to walk to numerous areas within the hospital and also worn while in bed. It is therefore possible that MDROs are gathered by non-slip socks from the floor, with subsequent transmission on to hospital bedsheets and the patient. Mops and clean pairs of socks were also sampled, which excluded contamination during laundering of mop heads or manufacture of these socks. In addition, interspersing clean socks with dirty socks during laboratory processing also confirmed that there was no cross-contamination in the methodology. There are several limitations to this study. It was carried out in one centre with a small number of samples. The length of time the socks were worn by patients was not recorded, which could affect the likelihood of contamination. The use of a hospital administration system is an imperfect indicator of colonization with these organisms and hence the true rates of patient carriage may be higher. The range of pathogens considered was limited and did not assess for contamination with carbapenemase-producing Enterobacteriaceae or multiresistant acinetobacter. However, clinical infections due to these organisms at our centre are low, compared to MRSA, VRE, and C. difficile. In addition, there was no comparison to patient’s slippers or bare feet walking, hence it remains unclear whether the materials from which the socks are made promote contamination. Finally, BHI broth was used to enrich low levels of bacteria and hence it was not possible to assess for the exact levels of contamination on the socks or the floor. Non-slip socks are single-use items and should be discarded following usage. However, single-use is a vague term in the context of non-slip socks because patients wear them continuously. Hence, it is possible for patients to wear the same pair of socks for a few hours, few days or even weeks while in hospital. In this context it is probably more accurate to describe them as being for single patient use.
Please cite this article in press as: Mahida N, Boswell T, Non-slip socks: a potential reservoir for transmitting multidrug-resistant organisms in hospitals?, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.06.018
N. Mahida, T. Boswell / Journal of Hospital Infection xxx (2016) 1e3 In conclusion, this study demonstrates that non-slip socks may become contaminated with MDROs and could lead to transmission of healthcare-associated pathogens. Although the study has not demonstrated direct transmission of pathogens from the floor to the patient, it suggests a potential route that thus far has not been considered. Conflict of interest statement None declared. Funding sources None.
References 1. National Institute for Health and Clinical Excellence. Falls: assessment and prevention of falls in older people. London: NICE; 2013. Available from: https://www.nice.org.uk/guidance/cg161 [last accessed June 2016].
3
2. Ford S. Trust introduces red socks to identify falls risk patients. Nursing Times, May 10th, 2013. Available from: http://www. nursingtimes.net/nursing-practice/specialisms/older-people/trustintroduces-red-socks-to-identify-falls-risk-patients/5058445.article [last accessed June 2016]. 3. Sinha SK, Detsky AS. Measure, promote, and reward mobility to prevent falls in older patients. JAMA 2012;308:2573e2574. 4. Howe RA, Andrews JM; BSAC Working Party on Susceptibility Testing. BSAC standardized disc susceptibility testing method (version 11). J Antimicrob Chemother 2012;67:2783e2784. 5. Dancer SJ. Mopping up hospital infection. J Hosp Infect 1999;43:85e100. 6. Ayliffe GAJ, Collins DM, Lowbury EJL. Cleaning and disinfection of hospital floors. Br Med J 1966;2:442e445. 7. Ayliffe GA. Role of the environment of the operating suite in surgical wound infection. Rev Infect Dis 1991;13:S800eS804. 8. Maki DG, Alvarado CJ, Hassemer CA, Zilz MA. Relation of the inanimate hospital environment to endemic nosocomial infection. N Engl J Med 1982;307:1562e1566.
Please cite this article in press as: Mahida N, Boswell T, Non-slip socks: a potential reservoir for transmitting multidrug-resistant organisms in hospitals?, Journal of Hospital Infection (2016), http://dx.doi.org/10.1016/j.jhin.2016.06.018