Faeces Management Time to Address the Risks

Faeces Management Time to Address the Risks

Updated 20180412 1245! The Scoop on Poop: 21st Century Look at an 18th Century Problem Jim Gauthier MLT, CIC Senior Clinical Advisor Infection Prevention 1 Disclaimer

Jim is employed by Diversey. His expenses to attend this meeting (travel, accommodation, and salary) are paid by this company. 2 Objectives Review mode of transmission and portal of entry related to multi-drug resistant organisms (MDRO) Discuss areas in healthcare that need more attention Propose ideas for discussion

3 4 http://diseasedetectives.wikia.com/wiki/Chain_of_Transmission Infectious Agent Vancomycin Resistant Enterococci (VRE) Extended Spectrum Beta Lactamase (ESBL)

Carbapenemase-producing Enterobacteriaceae (CPE) Carbapenemase-producing Organisms (CPO) Clostridium difficile (CD) Not truly an MDRO 5 Infectious Agent Methicillin Resistant Staphylococcus aureus Yes, that bug (Boyce 2007) Ebola

Yes, I know it is not an MDRO by definition Norovirus Rotavirus 6 7 http://diseasedetectives.wikia.com/wiki/Chain_of_Transmission

Reservoir Feces feces fi siz/ [ces fi siz/ [fee-seez] noun (used with a plural verb ) 1. Waste matter discharged from the intestines through the anus; excrement. 2. Also, especially British, faeces. Origin 1425-75; late middle English from Latin faecs grounds, dregs, sediment *www.dictionary.com Dictionary.com unabridged V1.0.1

8 Reservoir Urine Colonization common Especially elderly patients Catheterized patients 9 Reservoir

Sputum Common in elderly, intubated (Garcia 2005) Not applicable to this presentation Sink Drains Beyond this presentation 10

11 http://diseasedetectives.wikia.com/wiki/Chain_of_Transmission Portal of Exit Defecation Formed, soft, loose www.continence.org.au (ODonnell 1990) Urination

12 13 http://diseasedetectives.wikia.com/wiki/Chain_of_Transmission Mode of Transmission Equipment Bedpans, commode buckets, urinals, High Touch surfaces (Overbed tables, bed rails), toilet high touch surfaces

Hands Staff Patients Sink Drains Aerosols 14 15

http://diseasedetectives.wikia.com/wiki/Chain_of_Transmission Portal of Entry Rectum, mouth, non-intact skin Fecal oral Who puts feces into the patients mouth or rectum? Rectum endoscopes, gloved hands Mouth endoscopes, hands 16

Portal of Entry Hepatitis A is usually spread through having oral contact with items contaminated with hepatitis A, for example, through ingesting food or drinks contaminated by infected feces ProMed 20180112 18 http://diseasedetectives.wikia.com/wiki/Chain_of_Transmission

Susceptible Host Our patients CDI Proton pump inhibitors, antibiotics, hemodialysis, HIV, numerous hospital admissions (Bengualid 2011) CRE International travel (Tngdn 2010) Unrecognized colonized patient (Borgia 2012) 19

Control Measures www.qualitysystems.com 20 Horizontal vs Vertical Infection Control Wenzel 2010 21

Horizontal Reduce rates of all infections for all pathogens Hand hygiene program Decolonization therapies (Chlorhexidine bathing) Board to ward (Nat Audit Office 2009) Antibiotic Stewardship Programs Cleaning and disinfection 22 Vertical

Focus on a single pathogen or anatomic site Pathogen specific MRSA VRE ESBL

CRE C. difficile Acinetobacter Candida auris 23 Semmelweis Death by Group A Streptococcal puerperal sepsis Screen for Group A only?

Only use an agent effective against gram positive cocci? Only wash hands if in morgue? 24 25 WARNING!! This patient has: Skin! Feces!

Mucous Membranes! PERFORM HAND HYGIENE AFTER CONTACT WITH THIS PATIENT OR THEIR ENVIRONMENT! 26 VRE in the Environment Grabsch 2006 Colonized and past colonized VRE patients Structured exam, hemodialysis sessions Chairs positive in 36% outpatient, 58% hemodialysis

Couch positive 48% OP, 42% radiology, 27 VRE How Much? Ray (2002) - 12 of 13 had greater than 4log VRE per gram (mean 7.5 log) Mayer (2003) - The mean density of these specimens was 7.5 log10 cfu/g of stool (range: 3.7-9.2 log) for the patients who were continent and 6.2 log10 cfu/g of stool (range: 3.48.9 log) for those who were incontinent

NDM-1 Environment Walsh 2011- New Delhi 12 of 171 seepage samples grew 2 of 50 water samples grew 11 species in which NDM-1 not previously reported Some resistance to meropenem seen in isolates 29 Survival - CRE Havill 2014

Looked at K. pneumoniae and C. freundii Water Trypticase Soy Broth K. pneumoniae 19 days 40 days

C. freundii 12 days 40 days Can be shed into the environment and survive Because in GI tract, could be shed with high inoculum 30

C. difficile Colonization Alasmari 2014 14% on admission Toxigenic, no relation to previous admission Galdys 2014 Review article Strong evidence suggests that CD-colonized individuals are a reservoir for CD infection Donskey 2015 Review article As above Sporicidal in all rooms has potential to reduce transmission

31 C. difficile Colonization Longtin 2016 4.8% of admission were carriers. Isolation of carriers reduced overall HAI with CD 32 MRSA diarrhea Stools for CD testing cultured for MRSA Case: Diarrhea and MRSA colonization of stool (pure to heavy

growth) Control: MRSA + patients, negative stool colonization with MRSA 10 surfaces in patients room cultured 33 MRSA diarrhea 59% of case surfaces contaminated 23% of control surfaces contaminated

Most commonly bedside rails, blood pressure cuffs, television remote controls, and toilet seats Specimens were found to contain approximately 107-109 colony-forming units (cfu) per gram of stool Boyce 2007 Ebola 2-4 litres of liquid stool per day Lyon 2014 35

36 Control Measures www.qualitysystems.com 37 Suggestions Clean! Nseir 2011

Acquisition if in bed from previous patient Siani 2011 Wipes moved spores around Issue with sporicidal claims

Sattar 2013 Need better control of wipe use and testing Loo 2015 Clean environment and patients hands

38 Suggestions Clean! Zoutman 2013 40% of ICPs felt hospital was NOT clean enough Frequent consultation between IPAC and Environmental Services before cleaning changes lower CDI rates 39

Suggestions Clean! Zoutman 2014 Less than 50% of EVS managers felt they had enough staff Over 1/3 did no auditing 40 The Patients Environment EVS Cleans 1x per day What happens the other

23.5 hrs? Patient Room Entries Between 5 AM and 8 PM, (ICU and Med/Surg Unit) Number of room entries = 5.5/hour (28 max) Number of different staff entering room = 3.5/hour (18 max) Number of people in room during waking hours

= 15 hrs * 5.5 /hr = 82.5 people Cohen 2012 Surface Contact Huslage and Rutala (2010) studied HTS in an ICU and a general med-surg unit. In the ICU (contacts per interaction): Bedrails = 7.8

Bed surface = 6 Supply cart = 4 Surface Contact In the Med-Surg unit (contact per interaction) Bedrails = 3.1

Over-bed table = 1.6 IV pump = 1.4 Bed surface = 1.3 Average surfaces per interaction: ICU = 44, Med-Surg = 15 More Math! Room entries per hour = 5.5 Bedrail contacts per hour = 17.1 (5.5 x 3.1) Bedrail contacts per 15 hour patient awake day = 256

Number of times per day bedrail is disinfected by EVS = 1 Probability of EVS disinfecting the bedrail = ~50% ?255? ICT Feb 2018 24 Hour ICU 1. 2. 3. 4. 5.

Patient (850) WOW (634) Bedrail (375) IV pump (326) Bed Surface (302) 6. Overbed Table (223) 7. Vitals Machines (213) 8. Wall Shelf (110) 9. Door (90)

10. In room Computer (78) Jinadatha BMC Infect Dis 2017 Math! Number of times per day bedrail is disinfected by the clinical staff = ? (probably zero) Probability of Clinical staff performing hand hygiene = 40% 6 Moments of Environmental Disinfection (6MED)

1. Before placing a food tray on an over-bed table 2. After any procedure involving feces or respiratory secretions within the patient bed space 3. Before/after any aseptic practice (wounds, lines, etc.) 4. After patient bathing (within bed space) 5. After assistance with productive cough or vomiting 6. Any time surfaces are visibly soiled It is everyones job to disinfect, but it is not everyones job to disinfect everything every time!

Why do We Need to do This? Bed Rail as HTS Bhalla (VRE), Boyce 1994 (VRE), Bonten (VRE), Ray (VRE), Duckro (VRE), Hayden (VRE), Mayer (VRE), Hota (VRE), Sehulster (HTS), Rock (KPC), Rosa (CR-Ab), Calfee (MRSA), Anderson (Bioburden), Sample (VRE), Hess (MDRO), Thom (MDR-Ab), Boyce 2007 (MRSA), Adams (Bio), Attaway (Bio), Choi (CR-Ab), Yui (CDI) Why do We Need to do This?

Overbed table as HTS: Bhalla (VRE, St. aureus, Gm neg bacilli, CD), Boyce 1994 (VRE), Boyce 2007 (MRSA), Hota (VRE) , Enfield (A. baumannii), Calfee (MRSA), Hess (MRSA, MDR-Ab), Dancer 2008 (bioburden) , Dancer 2009 (MSSA, MRSA), Adams (bioburden), Yui (CDI) Why do We Need to do This? Two body substances that are predominately organisms Feces 1x1012 per gram dry weight (Kelly) Saliva 1x108 per mL (Lamont)

Moment 1 Food Tray Overbed table listed as HTS or contaminated (see previous slide!) We all know what goes on an overbed table None of us eat in our bathrooms! Moment 2 Feces/Suctioning Mayer 2003 - VRE Continent average 3.2X107 colony-forming unit/g of stool (5x103-1.6x109)

1,600,000,000! Incontinent 1.6x106 colony-forming unit/g of stool (range: 2.3x103-7.9x108) 790,000,000! Moment 2 Feces/Suctioning Ray 2002 - VRE 13 patients (8 NH,5 Hosp) 12 had >4log VRE per g stool Mean of 7.5 log or ~32,000,000 per g stool! Boyce 2007 - MRSA

If present in 4+ -> 107-109 Colony-Forming Units (cfu) per gram of stool Moment 2 Feces/Suctioning Site Known + CD Patient After Routine Bedrails

After Terminal No Known + CD Patient After Routine After Terminal 50% 11.8%

7.4% 4.1% Bedside Table 57.1% 22.2% 7.5%

5.9% Bed Controls 42.9% 17.6% 3.7%

4.1% Yui 2017 Moment 2 Feces/Suctioning Rock: CRE spread linked to caring for a patient with trach or ET Morgan (2010): MDR-Ab: care or use of endotracheal tube or tracheostomy site Morgan (2012): the respiratory tract is often heavily colonized with MDR bacteria and contact with respiratory

equipment may pose a particular risk Moment 3 Wounds Rock CRE: factors associated with HCW contamination providing wound care (4 of 11 contacts resulted in contamination; P = .05) Morgan- MDR-Ab: wound dressing Sergent bioburden: contamination in the hospital environment is frequent during the dressing of colonized wounds with tissue loss

Moment 4 Basin Bathing Johnson basin mean aerobic colony count of 91657, median 1150. Reference (Shannon not available) that showed bath water had >105 cfu/mL Rose - Standard plate count bacteria ranged from 105 to 1010 (cfu) per 100 ml for shower and bath water, and an average of 104 to 106 cfu per 100 ml for total coliforms. Moment 5&6 - Visible In actuality Routine Practices!

Is This a New Idea? Choi (2010) A. baumanii Similarly, other HCWs such as medical technologists, radiological technologists, or physical therapists who care for patients in both ICUs could have been a source of transmission. Attaway (2012) Bioburden to keep the bacterial population in check on the bed rails likely would require bihourly cleaning Ali (2012) Staph

Regular wiping with antibacterial wipes could be a cost-effective means of maintaining low numbers of bacteria near to the patient Suggestion Family and Visitors Feel free to use our disinfectant wipe on hard surfaces around the patient (not a baby wipe) Dispose in the regular garbage Please do not flush!

Control Measures www.qualitysystems.com 64 Feces Receptacles No manual cleaning No emptying within patient area Use a machine to do the pan

Liners 65 Patient Hand Hygiene Savage 2011 36 hour observation session Patients: 151 opportunities Zero used soap or ABHR Visitors: 121 opportunities

4% soap or ABHR 66 67 Does it Work? Could not get MRSA rates down 4 full time and 4 part time attendants hired Met patients and visiting relatives at door Verbal and pamphlet

Encourage to clean hands at least twice per day Used 70% with 0.5% Chlorhexidine 68 Results Impressive MRSA Infections per 1000 Admissions MRSA BSI MRSA Resp Ratio MRSA BSI / MSSA BSI

MRSA Mortality 2002-3 10.6 2003-4 5.2 Reduction 51%

1.3 0.2 85% 4.9 1.5 69%

59% (13/22) 14% (2/14) 76% 0.7 0.2

71% 69 Projected Savings $688,843! May have prevented 51 infections MRSA infection ~ $14,360 MRSA BSI ~ $27,083 Staffing was $170,000

70 MRSA Infections per 1000 Patient Admissions 04-05 05-06 06-07 07-08

08-09 09-10 10-11 11-12 12-13 2.3

1.0 0.6 0.6 0.7 0.5

0.3 0.2 0 Personal Communication 2013 71 Patient Hand Hygiene Assessment on admission for capability of performing hand

hygiene Do you know what this is? Show me how to use it Signage if not able to do own HH 72 73 Hand Sanitizer Bottle Label

FOR PATIENT USE Keep on overbed table If necessary, please ask for assistance to use this product 74 Patient Moments Landers 2012 (review) 1. After using the toilet, bedpan, or commode 3. Before eating, drinking, taking medicine, or putting anything in your mouth

75 Patient Moments 4. When visibly dirty 5. Before touching any breaks in the skin (wounds, dressing, tubes) or any care procedure (dialysis, IV drug administration, injections) 7. After coughing, sneezing, or touching nose or mouth 76

Jims Additional Moments 1. Leaving a wheelchair - New pamphlet for patients 2. After pet therapy (Lefebvre 2006) 77 Control Measures

www.qualitysystems.com 78 Preventative Measures Palmore 2013 - CRE Patients use gloves and gowns Double clean Hand hygiene (staff) Chlorhexidine baths (ICU) Adherence monitoring

79 Guidelines ECDC 2011 80 ECDC Low Grade Evidence consistently supports the effectiveness of early, active surveillance for CPE carriage by rectal screening Additional precautions for the care of CPE-positive patients,

wearing disposable gloves and gown cohort nursing by a separate, dedicated team 81 ECDC Other Measures Long Term Healthcare Facilities Israel uses contact precautions if: Patient incontinent On antimicrobials

82 2013 83 PHE Early Screening Early Isolation Reinforce Strict Standard Precautions 84

PHE No words such as Bedpan Does have language for

Diarrhoea (around hand hygiene) Toilet (that patient will have a private en suite) Environment (cleaning) Commode (if no toilet) Disinfection (high touch, mattresses, endoscope, etc.) 85 86

CDC Hand Hygiene Contact Precautions (colonized or infected) Patient and staff cohorting Minimize use of invasive devices Antimicrobial Stewardship Screening 87 CDC LTC settings high risk residents

totally dependent upon healthcare personnel for activities of daily living ventilator-dependent incontinent of stool wounds whose drainage is difficult to control high-risk settings (e.g., ventilator unit) 88 CRE Guidelines Curran 2014

Confusion on terms like Standard Precautions Ensure guidelines writers understand the front line 89 Curran 2014 5 Fronts: SP for all and additional transmission based precautions for CRE Hand washing basins free of CRE Safe injection and endoscopy practices

Prepare for outbreaks Antimicrobial stewardship 90 Ebola Feces and vomit have virus (Shieffelin 2014, Chertow 2014) Dallas family

Wet Phase 2-4 litres of liquid stool per day No illness Dallas hospital 2 infected 91

So, What do I Suggest? Monitor, or know, how many patients are incontinent Or using briefs, diapers, assistive devices Cochard 2014 ESBL carriage nursing homes Significantly associated with Malignancy Urinary AND fecal incontinence 92

Suggestions When we publish, list how feces and urine is managed and by what percentage Brief/Incontinent product Toilet Commode AND Thermal disinfection Macerator Liner

93 Control Measures www.qualitysystems.com 94 Suggestions Manage feces and urine better than our great grandfathers

Mandate NO manual cleaning Thermal disinfection Macerators Liners Disposable

95 Suggestions Mandatory gown use for any contact or potential contact with feces All the time Horizontal program

Sporicidal agent for all terminal cleans of washrooms (Bengualid 2011, Galdys 2014) Use of UV for terminal clean of contact precaution room (Rutala, AHE conference 2016) 96 Suggestions Isolate patients with diarrhea Benjamin 2014 Any soiling of the environment with feces is an issue!

Spill clean up should include sporicide!?! 97 Suggestions Lids on toilets/hoppers Aerosols around toilets from flushing has been studied (Gerba 1975, Barker 2005, Johnson 2013) C. difficile was in droplets around toilets with no lids (Best 2012, Roberts 2008) C. difficile detected on 31.6% of air vents (Wei 2017)

Viral spread (Verani 2014) 98 Summary Its all about the poop Lets talk about this!! 99 Comments? Questions?

100 References Alasmari F, Sieler SM, Hink T, et al. Prevalence and risk factors for asymptomatic Clostridium difficile carriage. Clin Infect Dis 2014;59(2):216-22 American Practitioners in Infection Control and Epidemiology. http:// www.apic.org/For-Consumers/Monthly-alerts-for-consumers/Article?id=cre-the-night mare-bacteria . Accessed November 2, 2014

American Practitioners in Infection Control and Epidemiology. http:// www.apic.org/For-Media/News-Releases/Article?id=2122443e-6d22-46ae-aecc-e95 12e98e1cb Accessed November 10, 2014 Barker J, Jones MV. The potential spread of infection caused by aerosol contamination of surfaces after flushing a domestic toilet. J Appl Microbiol 2005;99:339-347 101 References

Benjamin A, Rogers BA, Havers SM, Harris-Brown TM, Paterson DL. Predictors of use of infection control precautions for multiresistant gram-negative bacilli in Australian hospitals: Analysis of a national survey. AJIC 2014;42:963-9 Best EL, Sandoe JAT, Wilcox MH. Potential for aerosolization of Clostridium difficile after flushing toilets: the role of toilet lids in reducing environmental contamination risk. J Hosp Infect 2012;80:1-5 Bengualid V, Umesh KC, Alapati J, Berger J. Clostridium difficile at a community hospital in the Bronx, New York: Incidence prevalence and risk factors from 2006 to 2008. AJIC 2011;39:183-7 Borgia S, Lastovetska O, Richardson D, Eshaghi A, et al. Outbreak of carbapenem-resistant

Enterobacteriaceae containing blaNDM-1, Ontario, Canada. Clin Infect Dis. 2012 102 Dec;55(11):e109-17. doi: 10.1093/cid/cis737. Epub 2012 Sep 20. References Boyce JM, Havill NL, Otter JA, Adams NMT. Widespread environmental contamination associated with patients with diarrhea and methicillin-resistant Staphylococcus aureus colonization of the gastrointestinal tract. ICHE2007;28(10):1142-7 Cartmill TDI, et al. Management and control of a large outbreak of diarrhoea due to Clostridium difficile. J Hosp Infect 1994;27:1-15

Center for Disease Control and Prevention. Guidance for control of carbapenem-resistant Enterobacteriaceae (CRE). 2012 http://www.cdc.gov/hai/organisms/cre/cre-toolkit/index.html Accessed November 10, 2014 Chertow DS, Kleine C, Edwards JK, Scaini R, et al. Ebola virus disease in West Africa clinical manifestations and management. NEJM 2014 Nov 5, 2014 103 References Cochard H, Aubier B, Quentin R, van der Mee-Marquet N. Extended-spectrum beta lactamase-producing Enterobacteriaceae in French nursing homes: an association between

high carriage rate among residents, environmental contamination, poor conformity with good hygiene practice, and putative resident-to-resident transmission. ICHE 2014;35(4):384-9 Curran ET, Otter JA. Outbreak column 15: Carbapenemase-producing Enterobacteriaceae. J Infect Prevent 2014;15:193-198 Donskey CJ, Kundrapu S, Deshpande A. Colonization versus carriage of Clostridium difficile. Infect Dis Clin N Am 2015;29:1328 European Centre for Disease Prevention and Control. Risk assessment on the spread of carbapenemase-producing Enterobacteriaceae (CPE) through patient transfer between healthcare facilities, with special emphasis on cross-border transfer. Stockholm: ECDC;2011 104

References Fekety R, et al. Studies on the epidemiology of antibiotic-associated Clostridium difficile colitis. Am J Clin Nutr 1980;33:2527-32 Gagn D, Bdard G, Maziade PJ. Systematic patients hand disinfection: impact on meticillin resistant Staphylococcus aureus infection rates in a community hospital. J Hosp Infect 2010;75:269-72 Galdys AL, Curry SR, Harrison LH. Asymptomatic Clostridium difficile colonization as a reservoir for Clostridium difficile infection. Expert Rev Anti Infect Ther 2014;12:96780 Garcia R. A review of the possible role of oral and dental colonization of the occurrence of health care-associated pneumonia: underappreciated risk and a call for interventions. Am J

Infect Control 2005;33(9):527-40 105 References Gerba CP, Wallis C, Melnick JL. Microbiological hazards of household toilets: droplet production and the fate of residual organisms. Appl Microbiol 1975;30(2):229-237 Grabsch EA, Burrell LJ, Padiglione A, OKeefe JM, et al. Risk of environmental and healthcare worker contamination with vancomycin resistant enterococci during outpatient procedures and hemodialysis. Infect Control Hosp Epidemiol 2006;27:287-93 Havill NL, Boyce JM, Otter JA. Extended survival of carbapenem-resistant Enterobacteriaceae

on dry surfaces. ICHE 2014;35(4)445-7 Johnson DL, Mead KR, Lynch RA, Hirst DVL. Lifting the lid on toilet plume aerosol: A literature review with suggestions for future research. AJIC 2013;41:254-8 Landers T, Abusalem S, Coty MB, Bingham J. Patient-centered hand hygiene: the next step in infection prevention. AJIC 2012;40:S11-S17 106 References Loo VG. Environmental interventions to control Clostridium difficile. Infect Dis Clin N Am 2015;29:8391

Longtin Y, et al. Effect of Detecting and Isolating Clostridium difficile Carriers at Hospital Admission on the Incidence of C difficile Infections. A Quasi-Experimental Controlled Study. JAMA Intern Med. doi:10.1001/jamainternmed.2016.0177. Published online April 25, 2016. Lyon GM, Mehta AK, Varkey JB, Brantly K, et al. Clinical care of two patients with Ebola virus disease in the United States. NEJM 2014 DOI: 10.1056/NEJMoa1409838 Mayer RA, et al. Role of fecal incontinence in contamination of the environment with vancomycin-resistant enterococci. Am J Infect Control 2003; 31:221-225. McCoubrey J, et al. Clostridium difficile in a geriatric unit: a prospective epidemiological study employing a novel S-layer typing method. J.Med Micro 2003;52:573-8 107

References National Audit Office. Reducing healthcare associated infections in hospitals in England. Report by the Comptroller and Auditor General. HC 560 Session 2008-2009; 2009. National Audit office; London, UK Nseir S, Blazejewski C, Lubret R, Wallet F, et al. Risk of acquiring multidrug-resistant gramnegative bacilli from prior room occupants in the intensive care unit. Clin Microbiol Infect 2011;17:12011208 ODonnell LJD, Virjee J, Heaton KW. Detection of pseudodiarrhea by simple clinical assessment of intestinal transit rate. BMJ 1990; 300(6772):439-40 Palmore TN, Henderson DK. Managing transmission for carbapenem-resistant Enterobacteriaceae in healthcare settings: a view from the trenches. Clin Infect Disease

2013;57(11):1593-9 Public Health England Working Group. Acute trust tooklit for the early detection, management 108 and control of carbapenemase producing Enterobacteriaceae. 2013 PHE: London. References Ray AJ, et al. Nosocomial transmission of vancomycin-resistant enterococci from surfaces. J Am Med Assoc 2002;287:1400-1401 Roberts K, Smith FC, Snelling AM, Kerr KG, et al. Aerial dissemination of Clostridium difficile spores. BMC Infect Dis 2008;8:7

Sattar S, Maillard JY. The crucial role of wiping in decontamination of high-touch environmental surfaces: Review of current status and directions for the future. Am J Infect Control 2013;41:S97S104 Savage J, Fuller C, Besser S, Stone S. Use of alcohol hand rub (AHR) at ward entrances and use of soap and AHR by patients and visitors: a study in 27 wards in 9 acute NHS trusts. J Infect Prev 2011;12:54-8 Schieffelin JS, Shaffer JG, Gova A, Gbaki M, et al. Clinical illness and outcomes in patients with Ebola in Sierra Leone. NEJM.org Oct 29 2014. DOI: 10.1056/NEJMoa1411680 109 References Siani G, Cooper C, Maillard JY. Efficacy of sporicidal wipes against Clostridium difficile.

Am J Infect Control 2011;39:212-8 Tngdn T, Cars O, Melhus A, Lwdin E. Foreign travel is a major risk factor for colonization with Escherichia coli producing CTX-M-type extended-spectrum betalactamases: a prospective study with Swedish volunteers. Antimicrob Agents Chemother 2010; 54:35648 Verani M, Bigazzi R, Carducci A. Viral contamination of aerosol and surfaces through toilet use in health care and other settings. AJIC 2014;42:758-62 Walsh TR, Weeks J, Livermore DM, Toleman MA. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. The Lancet Infect Dis 2011;11:355-62 110

References Wenzel RP, Edmond MB. Infection control: the case for horizontal rather than vertical interventional programs. Int J Infect Dis 2010;14(supp 4);S3-S5 Yui S, Ali S, Muzslay M, et al. Identification of Clostridium difficile reservoirs in the patient environment and efficacy of aerial hydrogen peroxide decontamination. ICHE 2017;38(12):1487-92 Zoutman DE, Ford BD, Sopha K. Working relationships of infection prevention and control programs and environmental services and associations with antibiotic-resistant organisms in Canadian acute care hospitals. AJIC 2014;42:349-52 Zoutman DE, Ford BD, Sopha K. Environmental cleaning resources and activities in Canadian acute care hospitals. AJIC 2014;42:490-494

111 References Ali S, et al. Effect of surface coating and finish upon the cleanability of bed rails and the spread of Staphylococcus aureus. J Hosp Infect 2012;80:192-8 Adams CE, et al. Examining the association between surface bioburden and frequently touched sites in the intensive care. J Hosp Infect 2017;95:76-80. Attaway HH, et al. Intrinsic bacterial burden associated with intensive care unit hospital beds: effects of disinfection on population recovery and mitigation of potential infection risk. AJIC 2012;40:907-12

Bhalla A, et al. Acquisition of nosocomial pathogens on hands after contact with environmental surfaces near hospitalized patients. ICHE 2004;25:164-167. Bonten MJM, et al. Epidemiology of colonisation of patients and environment with vancomycin-resistant enterococci. Lancet 1996;348:1615-1619. References Boyce JM, et al Outbreak of multidrug-resistant Enterococcus faecium with transferable vanB class vancomycin resistance. J Clin Microbiol 1994;32:1148-1153. Boyce JM, et al. Widespread environmental contamination associated with patients with diarrhea and methicillin-resistant Staphylococcus aureus colonization of the gastrointestinal tract. ICHE 2007;28(10):1142-7.

Calfee DP, et al. Strategies to prevent methicillin-resistant Staphylococcus aureus transmission and infection in acute care hospitals: 2014 Update ICHE 2014;35(S2):S108-132 Choi WS, et al. Acinetobacter baumanii in intensive care units and successful outbreak control program. J Korean Med Sci 2010;25:999-1004. References Cobley M, et al. Environmental contamination during tracheal suction. Anaesthesia 1991;46:957-61. Cohen, et. al., Frequency of patient contact with health care personnel and visitors: implications for infection prevention. Jt Comm J Qual Patient Safety, 2012; 38 (12): 560-565

Dancer SJ, et al. Monitoring environmental cleanliness on two surgical wards. Int J Environ Health Res 2008;18:357-364. Dancer SJ, et al. Measuring the effect of enhanced cleaning in a UK hospital: a prospective cross-over study. BMC Med 2009;7:28. Duckro AN, et al. Transfer of vancomycin-resistant enterococci via health care worker hands. Arch Intern Med 2005;165:302-307. References Enfield KB, et al. Control of simultaneous outbreaks of carbapenemase-producing Enterobacteriaceae and extensively drug-resistant Acinetobacter baumannii infection in an intensive care unit using interventions promoted in the Centers for Disease Control and

Prevention 2012 carbapenemase resistant Enterobacteriaceae toolkit. ICHE 2014;35:810817. Hayden MK, et al. Reduction in acquisition of vancomycin-resistant Enterococcus after enforcement of routine environmental cleaning measures. Clin Infect Dis 2006;42:1552-1560. Hess AS, et al. A randomized controlled trial of enhanced cleaning to reduce contamination of healthcare worker gowns and gloves with multidrug-resistant bacteria. ICHE 2013;34:487 493. References Hota B, et al. Interventional evaluation of environmental contamination by vancomycinresistant enterococci: failure of personnel, product, or procedure? J Hosp Infect 2009;71:123-31. Huslage, K et al. A Quantitative approach to defining hightouch surfaces in hospitals.

ICHE 2010;31(8):850-3 Johnson D, et al. Patients bath basins as potential sources of infection: a multicenter sampling study. Am J Crit Care 2009;18(1):31-40. Kelly CP, et al. Clostridium difficile colitis. NEJM 1944;330(4):257-62 Lamont RJ, Jenkinson H. In: Oral microbiology at a glance. Wiley-Blackwell 2010. West Sussex UK References Mayer RA, et al. Role of fecal incontinence in contamination of the environment with vancomycin-resistant enterococci. AJIC 2003; 31:221-225. Morgan DJ, et al. Frequent multidrug-resistant Acinetobacter baumannii

contamination of gloves, and hands of healthcare workers. ICHE 2010;31(7):716721. Morgan DJ, et al. Transfer of multidrug-resistant bacteria to healthcare workers gloves and gowns after patient contact increases with environmental contamination. Crit Care Med 2012;40(4):10451051. Otter JA, et al. The role played by contaminated surfaces in the transmission of nosocomial pathogens. ICHE 2011;32(7):687-99. References Ray AJ, et al. Nosocomial transmission of vancomycin-resistant enterococci from surfaces. JAMA 2002;287:1400-1401. Rock C, et al. Frequency of Klebsiella pneumoniae Carbapenemase

(KPC)producing and non-KPC producing Klebsiella species contamination of healthcare workers and the environment. ICHE 2014;35(4):426-9 Rose JB, et al. Pathogens in graywater from various household sources. Wat Res 1991;25(1):37-42. Sample ML, et al. An outbreak of vancomycin-resistant enterococci in a hematology-oncology unit: control by patient cohorting and terminal cleaning of the environment. ICHE 2002;23:468-470. References Sehulster LM, et al. Guidelines for environmental infection control in health-care

facilities. Recommendations from CDC and the Healthcare Infection Control Practices Advisory Committee (HICPAC). https://www.cdc.gov/infectioncontrol/pdf/guidelines/environmental-guidelines.pdf Accessed 20180131 Thom KA, et al. Environmental contamination because of multidrug-resistant Acinetobacter baumannii surrounding colonized or infected patients. AJIC 2011;39:711715. Yui S, et al. Identification of Clostridium difficile reservoirs in the patient environment and efficacy of aerial hydrogen peroxide decontamination. ICHE 2017;38(12):148792 References

Zelechowski GP. Suction collection and its relation to nosocomial infection. AJIC 1980;8(1):22-5 Jinadatha C, et al Interaction of healthcare worker hands and portable medical equipment: a sequence analysis to show potential transmission opportunities. BCM Infect Dis 2017;17:800

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