The ‘bed location lottery’: the MDRO status of the prior bed occupant affects the risk of acquisition Jon Otter, PhD Scientific Director, Healthcare, Bioquell Research Fellow, Centre for Clinical Infection and Diagnostics Research (CIDR), King’s College London / Guy’s and St. Thomas’ Hospital NHS Foundation Trust Visiting Professor, Tokyo Healthcare University jon.otter@bioquell.com

Sites contaminated with MRSA Broth enrichment Direct plating French et al. J Hosp Infect 2004;57:31-37. 2

Surface survival 1400 Otter and French. J Clin Microbiol 2009;47:205-207. Wagenvoort et al. J Hosp Infect 2011;77:282-283.

(8 rooms; 2 four-bed bays previously occupied by MRSA patients) Conventional terminal cleaning 26% reduction 90% of 124 sites 66% of 124 sites Percentage of MRSA swabs positive (8 rooms; 2 four-bed bays previously occupied by MRSA patients) Before cleaning After cleaning French et al. J Hosp Infect 2004;57:31-37.

Contaminated sites after cleaning Broth enrichment Direct plating French et al. J Hosp Infect 2004;57:31-37.

Conventional terminal decontamination

Multiple rounds of bleach disinfection 140 samples from 9 rooms after 2xbleach 5705 samples from 312 rooms after 4xbleach 26.6% of rooms remained contaminated with either MRSA or A. baumannii following 4 rounds of bleach disinfection Manian et al. Infect Control Hosp Epidemiol 2011;32:667-672.

Implications of sub-optimal terminal disinfection Room can be contaminated with >1 strain of the same pathogen; a “build up” over time. Average of 2.3 MRSA antibiograms in each patient room.1 ~30% of MRSA environmental isolates are not closely related to patient isolates.2,3 Pathogens can be cultured from empty rooms. 5% of 638 empty rooms contaminated with VRE.4 French et al. J Hosp Infect 2004;57:31-37. Sexton et al. J Hosp Infect 2006;62:187-194. Boyce et al. Infect Control Hosp Epidemiol 2007;28:1142-1147. Drees et al. Clin Infect Dis 2008;46:678-685.

‘The bed location lottery’ Patient infected or colonised with a pathogen (e.g. C. difficile, MRSA, VRE, A. baumannii or P. aeruginosa) Patient is discharged and the room is cleaned / disinfected; surfaces in the room remain contaminated with the pathogen The next room occupant is at an increased risk of acquiring the pathogen

Independent predictors of VRE acquisition The VRE ‘bed location lottery’ Setting & design: 14-month prospective study on 2 ICUs, Boston, USA. Methods: All patients were screened on admission and twice weekly, and the environment was screened weekly for VRE. The 50 patients who acquired VRE were compared with the 588 who did not. Independent predictors of VRE acquisition VRE colonised prior room occupant VRE colonised occupant in the prior 2 weeks Hazard ratio Drees et al. Clin Infect Dis 2008;46:678-685.

Percentage of patients acquiring The MRSA & VRE ‘bed location lottery’ Setting & design: 20-month retrospective cohort study on 8 ICUs, Boston, USA. Methods: Admission and weekly screening for MRSA and VRE. Evaluated the rate of acquisition in 11,528 occupants admitted into rooms where the prior room occupant was known to be infected or colonised with MRSA (n=1454) or VRE (n=1291). Adjusted odds ratio 1.4, p=0.02 Adjusted odds ratio 1.4, p=0.04 VRE colonised prior room occupant Percentage of patients acquiring VRE colonised occupant in the prior 2 weeks Huang et al. Arch Intern Med 2006;166:1945-51.

Percentage of patients with CDI The C. difficile ‘bed location lottery’ Setting & design: 18-month retrospective cohort study on an ICU, Ann Arbor, Michigan, USA. Methods: 134 cases of C. difficile infection occured among 48 hours after ICU admission or with 30 days of discharge in 1,844 patients admitted to the ICU during the study. Hazard ratio 2.35, p=0.01 Percentage of patients with CDI Shaughnessy et al. Infect Control Hosp Epidemiol 2011;32:201-206.

The C. difficile ‘bed location lottery’ Kaplan-Meier analysis, which accounts for time at risk of CDI, also showed a significant difference (p=0.008) Shaughnessy et al. Infect Control Hosp Epidemiol 2011;32:201-206.

The Gram-negative ‘bed location lottery’ Setting & design: 12-month prospective cohort study on an ICU, Lille, France. Methods: Admission and weekly screening was performed for MDROs. 511 patients were admitted; risk factors were examined for the patients that acquired MDR P. aeruginosa (n=82) and A. baumannii (n=57). Adjusted odds ratio 2.3, p=0.012 Percentage of patients acquiring Adjusted odds ratio 4.2, p<0.001 Nseir et al. Clin Microbiol Infect 2011;17:1201-1208.

Prior room occupancy Study Nosocomial pathogen Likelihood of patient acquiring HCAI based on prior room occupancy (comparing a previously ‘positive’ room with a previously ‘negative’ room) Martinez 20031 VRE – cultured within room 2.6x Huang 20062 VRE – prior room occupant 1.6x MRSA – prior room occupant 1.3x Drees 20083 1.9x 2.2x VRE – prior room occupant in previous two weeks 2.0x Shaughnessy 20114 C. difficile – prior room occupant 2.4x Nseir 20105 A. baumannii – prior room occupant 3.4x P. aeruginosa – prior room occupant 1.7x 1. Martinez et al. Arch Intern Med 2003; 163: 1905-12. 2. Huang et al. Arch Intern Med 2006;166:1945-1951. 3. Drees et al. Clin Infect Dis 2008; 46: 678-85. 4. Shaughnessy et al. Infect Control Hosp Epidemiol 2011;32:201-206. 5. Nseir et al. Clin Microbiol Infect 2011; 17: 1201-1208.

Limitations of prior room occupancy studies Could certain bed locations be inherently more risky for acquisition? Sicker patients are placed under the watchful eye of the nursing staff Physical problems with the bed space (e.g. too small, poor ventilation) Prior room occupancy studies are required for other organisms and in other settings: Norovirus All studies performed in ICU settings – general ward, community settings? Most studies performed in the USA All studies performed in single room units – open ward examining bed location? Only one study has included microbiological culture; no study has performed molecular typing to link the isolates.

Hydrogen peroxide vapour (HPV) Effect of cleaning Effect of HPV 90% of 124 sites (8 rooms; 2 four-bed bays previously occupied by MRSA patients) 26% reduction 72% of 85 sites (4 rooms; 2 bathrooms previously occupied by MRSA patients) 66% of 124 sites Percentage of MRSA swabs positive 98% reduction 1% of 85 sites* Before cleaning After cleaning Before HPV After HPV * 1 swab out of 85 on enrichment only French et al. J Hosp Infect 2004;57:31-37.

Residual contamination 140 samples from 9 rooms after 2xbleach 5705 samples from 312 rooms after 4xbleach 2680 sites from 134 rooms after HPV 26.6% of rooms remained contaminated with either MRSA or A. baumannii following 4 rounds of bleach disinfection Manian et al. Infect Control Hosp Epidemiol 2011;32:667-672.

Mitigating the risk from the prior occupant HPV units Non-HPV units Pre- intervention Intervention RR P Total number of rooms sampled 170 397 156 316 Rooms contaminated with any MDRO 21.2% 13.9% 0.65 0.03 23.7% 28.5% 1.20 0.32 Multiple MDROs 4.7% 0.8% 0.16 <0.01 2.6% 3.2% 1.23 1.00 MDRO matches the current room occupant 8.2% 9.3% 1.13 0.75 9.6% 10.1% 1.05 MDRO differs from the current room occupant 8.8% 3.3% 0.37 0.01 11.5% 12.3% 1.07 0.88 Contaminated empty rooms 4.1% 1.3% 0.31 0.05 6.0% 1.88 0.27 Passaretti et al. ICAAC/IDSA 2008.

Taking the lottery out of the room 66% reduction MDRO standard No MDRO MDRO HPV Passaretti et al. ICAAC/IDSA 2008.

Taking the lottery out of the room Acquisition rate of MDROs depending on the status of the prior room occupant (number of patients that acquired on the top of each bar) -standard % change -77% -54% -65% -38% -66% p <0.001 0.28 0.18 0.17 Passaretti et al. ICAAC/IDSA 2008.

Taking the lottery out of the room Baseline: Sept 2003 – Apr 2005 Conventional cleaning / disinfection using a QAC Intervention: Sept 2006 – Apr 2008 Enhanced cleaning (black-light, ‘bucket method’, education) 3.0% of patients acquired MRSA 50% reduction p<0.001 1.5% of patients acquired MRSA 3.0% of patients acquired VRE 27% reduction p<0.001 2.2% of patients acquired VRE Datta et al. Arch Intern Med 2011;171:491-494.

Taking the lottery out of the room Baseline: Sept 2003 – Apr 2005 Conventional cleaning / disinfection using a QAC Intervention: Sept 2006 – Apr 2008 Enhanced cleaning (black-light, ‘bucket method’, education) Acquisition rates by status of the prior room occupant Acquisition rates by status of the prior room occupant MRSA+ 3.9% acquired MRSA- 2.9% acquired MRSA+ 1.5% acquired MRSA- 1.5% acquired -26% P=0.03 ±0% P=0.79 VRE+ 4.5% acquired VRE- 2.8% acquired VRE+ 3.5% acquired VRE- 2.0% acquired -61% P=0.01 -43% P=0.01 Limitations: No environmental sampling Datta et al. Arch Intern Med 2011;171:491-494.

Infected and Colonised Transmission routes The Environment Source Control Daily Cleaning Terminal Cleaning Infected and Colonised Screening Hand Hygiene Healthcare Workers Hospital Acquired Infections Isolation

Increased risk from the prior room occupant Otter et al. Infect Control Hospital Epidemiol 2011;32:687-699.

How much does environmental contamination contribute to transmission? % admissions with positive prior room occupant OR % infections attributable to the prior room occupant Shaughnessy C. difficile1 5 2.4 3 Nseir A. baumannii2 10 3.4 7 Huang VRE3 13 1.6 Huang MRSA3 14 1.3 Nseir P. aeruginosa2 17 1.7 Drees VRE4 22 2.2 12 Drees VRE (2 weeks)4 43 2.0 Note, these estimates exclude indirect environmental contamination due to the acquisition of hand contamination. Shaughnessy et al. Infect Control Hosp Epidemiol 2011;32:201-206. Nseir et al. Clin Microbiol Infect 2011; 17: 1201-1208. Huang et al. Arch Intern Med 2006; 166: 1945-51. Drees et al. Clin Infect Dis 2008; 46: 678-85.

Implications of the bed space lottery We can now begin to estimate the % of transmission related directly to environmental contamination. Improving terminal disinfection can mitigate the increased risk from the prior room or bed space occupant. The impact of improving terminal disinfection is likely to depend on the organism and setting. Further work is required to evaluate indirect environmental transmission routes. French et al. J Hosp Infect 2004;57:31-37. Sexton et al. J Hosp Infect 2006;62:187-194. Boyce et al. Infect Control Hosp Epidemiol 2007;28:1142-1147. Drees et al. Clin Infect Dis 2008;46:678-685.