Abstract

Unrecognized transmission of pathogens in healthcare settings can lead to colonization and infection of both patients and healthcare personnel. The use of personal protective equipment (PPE) is an important strategy to protect healthcare personnel from contamination and to prevent the spread of pathogens to subsequent patients. However, optimal PPE use is difficult, and healthcare personnel may alter delivery of care because of the PPE. Here, we summarize recent research from the Prevention Epicenters Program on healthcare personnel contamination and improvement of the routine use of PPE as well as Ebola-specific PPE. Future efforts to optimize the use of PPE should include increasing adherence to protocols for PPE use, improving PPE design, and further research into the risks, benefits, and best practices of PPE use.

Every day, people touch and carry a range of potential pathogens, some of which will ultimately cause infections. This includes healthcare personnel (HCP) and patients in healthcare settings where there are frequent opportunities for close contact that can lead to transmission of organisms between HCP and patients. Unrecognized transmission of pathogens can lead to colonization and infection of both patients and HCP. While many pathogens can lead to harm to patients, a few also pose a high risk to HCP. Personal protective equipment (PPE) is an important component in infection control strategies to protect HCP. By preventing contamination of HCP hands and garments, PPE is intended to prevent infections in the individual HCP, as well as secondary spread to other HCP and to patients. Understanding how and where HCP contamination occurs is important for improving PPE and infection control practices for both routine and specialized patient care. The 2014–2016 Ebola outbreak brought to light important gaps in HCP use of PPE and implementation of strategies for preventing patient-to-HCP transmission. Recent studies on Ebola-specific PPE and routine healthcare PPE, as described in the Centers for Disease Control and Prevention (CDC) guidelines [1–3], have shown that optimal use is difficult, HCP may alter healthcare delivery when utilizing PPE, and self-contamination occurs during the use of PPE, potentially endangering HCP and patients. Furthermore, strategies to address these challenges often lack strong evidence for effectiveness [4]. To increase our knowledge and facilitate improved design and use of PPE, the CDC expanded research and innovation funding through the CDC Prevention Epicenters Program beginning in 2015. The 2015 Prevention Epicenters investments focused on contact transmission and optimizing PPE use for preventing transmission in healthcare settings.

The CDC Prevention Epicenters Program is a unique collaborative research partnership among public health and academic medical centers in the United States that perform research and innovation in the prevention of healthcare-associated infections and antibiotic resistance. This supplement to Clinical Infectious Diseases provides insights from the recent work of the Prevention Epicenters Program for improving routine use of PPE and Ebola-specific PPE and for preventing contact transmission of pathogens to better protect patients and HCP. Although settings, equipment, and instructions for donning and doffing of routine PPE differ from Ebola-specific practices, insights gained from one scenario can be applied to the other. In this article, we discuss the recent work of the Prevention Epicenters, summarize the findings of their work presented in this supplement, and describe future directions for improving PPE and its use in healthcare settings.

CONTACT TRANSMISSION AND THE ROLE OF HCP

Transmission of microbes between patients and HCP during routine care is common, regardless of whether the patient is actively infected or asymptomatically colonized. HCP can be contaminated during direct contact with patient skin or bodily fluids (direct contact transmission) or by contact with the patient’s environment (indirect contact transmission). The hands of HCP are frequently contaminated and are sources of transmission to others and to the environment. HCP clothing, including white coats, can also become contaminated and serve as a reservoir for pathogens. Standard precautions, including hand hygiene and the use of PPE, are the cornerstone to preventing transmission, based on the potential for exposure to blood, body fluids, or infectious material. Additional contact precautions are applied when a patient has a documented or suspected diagnosis with which contact with the patient, their body fluids, or their environment presents a substantial transmission risk [3].

Many factors related to the patient and HCP affect the risk for HCP contamination. Patient factors associated with pathogen shedding include their microbial burden, antibiotic exposures, and patient conditions, such as open wounds and bowel incontinence [5–7]. The type of HCP interactions with patients [5, 8] and their environment [9–11] also influence the risk for contamination. Several Prevention Epicenters studies aimed to better identify HCP-to-patient interactions that resulted in contamination. Epicenters investigators found that that high-risk HCP-to-patient interactions involve direct contact with the patient or bodily fluids and include activities such as touching endotracheal tubes, changing wound dressings, and assisting with bathing, whereas low-risk interactions involve minimal patient contact, for example, glucose monitoring and medication assistance [12–14]. Understanding when HCP are at highest risk for contamination can help inform control strategies, including PPE.

PPE FOR PREVENTING CONTAMINATION

Preventing exposures to infectious material in the healthcare setting is a fundamental part of protecting HCP and patients. Traditionally, a hierarchy of controls (Figure 1) has been used to determine how to implement feasible and effective control solutions to occupational hazards. The hierarchy ranks controls according to their effectiveness, leading with elimination of a hazard as the most potentially effective control, and ending with PPE, whose effectiveness relies on consistent and correct use. In healthcare settings, elimination of an infectious disease from a facility is typically not possible, as patients with infections require medical care. Preventing the transmission of infectious agents that are spread by contact primarily involves the use of engineering controls (such as maintaining private patient isolation rooms), administrative controls (such as limiting patient movement out of isolation rooms to medical necessity only), and PPE. Because other control solutions cannot completely eliminate the risk for exposure to infectious diseases in healthcare settings, PPE remains an important tool in a comprehensive strategy for preventing the transmission of pathogens from patients to HCP.

Hierarchy of controls for occupational hazards [15]. Abbreviation: PPE, personal protective equipment.
Figure 1.

Hierarchy of controls for occupational hazards [15]. Abbreviation: PPE, personal protective equipment.

IMPROVING ROUTINE PPE USE

HCP contamination can occur due to failure to use PPE, PPE malfunction, incorrect use of PPE, and self-contamination during care and in the doffing process. When immediate health consequences of contamination are not apparent for either patients or HCP, HCP may not recognize the importance of work practices, including correct and consistent PPE use. One study that used video monitoring showed that adherence to correct PPE use was 34% with variability by provider type [16]. Even when HCP wear PPE, incorrect use occurs, which can provide a false sense of security and lead to self-contamination and transmission events. Understanding the types of errors that occur in using PPE is one step toward identifying solutions. Investigators performed 325 HCP observations of adherence to contact and droplet precautions and observed 283 failures. Of these failures, 102 were deviations from safe operating practices or procedures, such as entering a room without donning PPE or not donning the gown completely; 44 process or procedural mistakes, such as being interrupted while doffing PPE, were identified; and 37 slips or lapses, such as unintentional self-contact without awareness, were identified [17]. Unfortunately, such failures can result in pathogen transmission. One study showed that 37% of HCP hands were contaminated after doffing contaminated gloves, but contamination varied based on the doffing technique [18]. Another study of glove and gown removal simulations showed that self-contamination of skin or clothing occurred in 46% of simulations, which would have gone unrecognized in real-world settings [19].

Prevention Epicenters investigators and others have noted that PPE design may affect errors in PPE use, and some have suggested that use of human factors engineering could help address some of these issues [20]. HCP describe a tension between doffing safely and doffing expediently and that PPE design can provide both barriers to or be facilitators of appropriate use [21]. Prevention Epicenters investigators and others are evaluating different designs of PPE, such as features to facilitate doffing gloves, designs that allow for easy removal around the neck, improved fasteners to facilitate donning and doffing, and color coding to aid in recognition of potentially contaminated areas [21–23].

Several retrospective studies have reported an association of contact precautions with patient adverse events, including depression, anxiety, anger, fear, loneliness, and other noninfectious adverse effects [24]. However, many of these studies were not designed to adequately address concerns that patients in contact precautions might have a greater severity of illness, and a prospective multicenter randomized controlled study did not demonstrate adverse events for patients cared for by HCP in gloves and gowns [25]. Nevertheless, the effect of contact precautions on HCP workflow has been documented with HCP entering isolation patient rooms less often [26]. Prevention Epicenters investigators found that job activities contribute to PPE errors and that HCP movement patterns, time with patients, care activities, and use of equipment vary by type of HCP and will require multiple solutions to improve PPE use based on the activities performed [27]. Ultimately, a better understanding of how contact precautions and PPE affect patient care activities can lead to strategies to mitigate unintended consequences.

Additional HCP-level interventions aimed at reducing HCP risk of contamination are being evaluated. Some institutions have implemented a policy of bare-below-the-elbows, which advocates for HCP to wear short sleeve shirts and avoid wearing white coats, hand and wrist jewelry, and neckties [28]. In a randomized controlled study that involved simulated patient care interactions with a surrogate marker, HCP in the short-sleeved group had less contamination than HCP in the long-sleeved group [29]. Separately, a recent clinical trial of antimicrobial-impregnated textiles, such as HCP scrubs, showed that antimicrobial-impregnated scrubs were not effective at reducing HCP contamination, despite having shown early promise [30]. The effect of additional strategies to reduce the risk of HCP contamination warrants further investigation.

The burden of contact precautions on HCP and healthcare facilities, potential adverse effects of contact precautions on patient care, and the existence of additional strategies to reduce the risk for transmission have led some to question the use of contact precautions for endemic pathogens, such as methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant enterococcus [31]. Although PPE is the most recognizable element of contact precautions, CDC recommendations for the use of contact precautions include engineering, administrative, and PPE controls [3]. While the recommendation to use contact precautions to prevent disease transmission is based on sound rationale and evidence, the impact on disease transmission is unclear, in part, because the optimal methods for evaluating the effect of contact precautions on transmission rates are not established. Due to this limitation, single-center quasiexperimental studies that evaluate the noninferiority of discontinuing contact precautions are unable to adequately establish its effect [32]. These studies may underestimate the impact of contact precautions by not including effects on colonization or downstream adverse events, such as postdischarge infections, which are more common than hospital-onset infections [33]. Notably, hospital-onset and healthcare-associated MRSA bloodstream infections have declined in the United States from 2012–2017, suggesting that current strategies, which include contact precautions, have been effective in reducing MRSA infections [33, 34]. Regardless, conducting research aimed at establishing methodology to evaluate the effectiveness of contact precautions to prevent transmission could help optimize implementation of contact precautions in the future.

IMPROVING EBOLA-SPECIFIC PPE USE

Errors in routine PPE use and patient care practices generally do not result in recognized harm to HCP; however, patient care for individuals infected with pathogens such as hemorrhagic fever viruses is much less forgiving. Successful PPE use and adherence to correct infection control practices require extensive, comprehensive training and demonstrated competency in donning, performing care activities, and doffing. It is recommended that a trained observer supervise Ebola-specific PPE donning and doffing to prevent unrecognized mistakes. However, even with guidance on the sequence of donning and doffing and training for HCP using Ebola-specific PPE, research from the Prevention Epicenters and others has shown that HCP actions still cause self-contamination in simulated environments [35–37]. Human factors engineering methodology can be utilized to identify doffing activities where self-contamination is more likely to occur; quantify the risk associated with those failures; and describe the mental, physical, and temporal load of each task [38, 39]. A challenge for the field will be to reconcile differences in the results from individual facilities by finding commonalities in errors and identifying solutions that are applicable to other sites.

Human factors engineering has been used to describe reasons for PPE use errors and identify methods to reduce self-contamination while doffing PPE, such as optimizing PPE design, improving hand hygiene while doffing, and designing the built environment to facilitate successful doffing. Although glove decontamination prior to doffing decreases the concentration of bacteria on inner gloves, self-contamination still occurs [40]. Research evaluating methods of decontaminating hands (eg, wipes or spray) may help facilities compare methods [41], but facilities also need to consider occupational health hazards, such as adverse respiratory effects and falls. Prevention Epicenter investigators identified significant variation in hand hygiene technique, duration, and thoroughness at 4 Ebola treatment centers and showed that simple techniques, such as singing a song to help estimate time while performing hand hygiene, improved adherence and duration [42].

For HCP who care for patients with Ebola, Prevention Epicenters investigators identified 5 key features of the built environment that improve safety during doffing of complex PPE ensembles: the doffing area facilitates communication, the environment indicates zones of contamination; the doffing area provides stabilization to aid balance, the doffing area nudges automatic safe choices, and the environment provides situational awareness [43]. Investigators also implemented an optimized doffing area design in a simulated environment that included simple interventions such as a chair or grab bar for balance, demarcating zones of contamination on the floor, and use of a mirror to reduce risky behaviors while doffing [44]. Similarly, other Prevention Epicenters investigators showed that an intervention package that addresses PPE selection, teamwork building, doffing protocols, the built environment, and training all can effectively reduce self-contamination [45].

The Prevention Epicenters research provides an evidence base for how improving usability and effectiveness of PPE can better protect HCP. There is further need to be able to quantify transmission risk. Research in transmission dynamics and PPE efficacy to date has relied on the use of benign surrogate markers. These markers are a valuable tool to qualify and quantify the potential risk of pathogen transmission for research and for training [19]. Numerous studies that evaluated PPE use have used a range of fluorescent markers (liquid, lotions, or powder) with ultraviolet light either alone or in combination with other surrogates, such as bacteria, bacterial spores, nonenveloped bacteriophages (MS2), enveloped bacteriophages (ɸ6), cauliflower mosaic virus DNA, and polystyrene latex spheres PolyStyrene Latex (PSL). For instance, Epicenters investigators evaluated the use of PSLs in combination with fluorescent markers in order to quantify potential inhalational exposures [46]. Further developing appropriate surrogates, standardizing methods for applying surrogates to simulate real-life contamination, comparing various surrogates to each other, and, importantly, correlating them with pathogenic organisms are needed to move the field forward.

FUTURE DIRECTIONS

Based on the results of the Prevention Epicenters Program and related research, efforts to improve the use of PPE for contact precautions should include methods to improve adherence to recommended protocols for PPE use, improved PPE design that facilitates donning, patient care activities, and doffing, as well as further research into the risks, benefits, and best practices of PPE use.

First, improving adherence to recommended protocols for PPE use should involve HCP education, training, demonstrations of competency, monitoring, and creating a patient care environment that facilitates the appropriate use of PPE. HCP should be educated about the importance of transmission in healthcare settings, the role of HCP contamination in transmission events, and methods for reducing that risk. Furthermore, schools for healthcare providers (eg, medical and nursing schools) are critical places for early career engagement and instruction in transmission dynamics and the importance and use of PPE for creating a safe work environment.

Second, PPE design for both routine and specialized use should help HCP provide optimal care for patients, rather than diverting their attention during patient care while attempting to remember multiple steps and awkward actions needed for safe PPE use. Multidisciplinary partnerships, including industry partners, human factors engineers, healthcare epidemiologists, and HCP, can provide the diverse expertise for evaluating and improving PPE design and finding effective solutions to improve performance and usability in healthcare settings.

Third, our understanding of transmission events in healthcare settings is limited, and further research that links transmission risk to best practices in patient care, including PPE use, is needed. Common transmission events are unrecognized because acquisition of pathogens by HCP or patients is usually not clinically apparent or has delayed clinical manifestation (eg, after the patient is discharged from a facility). More detailed studies in real-world and simulated environments, including the use of surrogate markers, will be valuable in describing transmission dynamics, the role of HCP self-contamination in the spread of pathogens, and the effectiveness of different PPE strategies and care processes in preventing transmission. Specifically, assessing the contribution of PPE among multiple concurrent infection control interventions is an ongoing challenge. Mathematical modeling can be used to predict the effect of individual components of bundled interventions [47], but these models depend on appropriately detailed data points to parameterize important variables. The marriage of modeling with observational data collection might be an avenue whereby interventions could be evaluated. Sequencing of isolates to verify transmission events would give greater clarity to when transmission events are occurring and potentially aid in identifying the source of patient or HCP acquisition. Furthermore, a better understanding of the contribution of colonization status, shedding, and high-risk patient–HCP interactions could provide important insights for optimizing PPE use and design for all types of healthcare delivery.

All healthcare settings can benefit from improvements in PPE use and design. Postacute care settings, such as nursing homes and high-acuity skilled nursing facilities, have high rates of multidrug-resistant organism (MDRO) colonization and transmission [48] that can affect the regional control of MDROs [49–51]. Due to the higher prevalence of MDRO colonization, patient care workflow processes, communal living, and other factors, these settings need tailored approaches to prevent transmission, including strategies such as using PPE based on resident risk factors rather than pathogen-specific indications [52].

In summary, PPE plays an important role in preventing pathogen transmission in healthcare settings, but its optimal design and use need to be informed by dedicated research to achieve the reliability and effectiveness needed to protect patients and HCP. Current Prevention Epicenters projects on PPE explore improvements in the use and refinements in the design of PPE and foster innovation and research to reduce the risk of transmission of infectious diseases between HCP and patients.

Notes

Acknowledgments. The authors thank Melissa Kornfeld, Karima Hunter, Tiffanee Woodard, and John Jernigan for their continued support of the Prevention Epicenters Program and this supplement.

Disclaimer. The findings and conclusions in this article are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention.

Supplement sponsorship. This article appears as part of the supplement “Personal Protective Equipment for Preventing Contact Transmission of Pathogens: Innovations from CDC’s Prevention Epicenters Program,” sponsored by the CDC’s Prevention Epicenters Program.

Potential conflicts of interest. All authors report no potential conflicts. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.

References

1.

Centers for Disease Control and Prevention
.
Guidance on personal protective equipment (PPE) to be used by healthcare workers during management of patients with confirmed Ebola or persons under investigation (PUIs) for Ebola who are clinically unstable or have bleeding, vomiting, or diarrhea in U.S. hospitals, including procedures for donning and doffing PPE
. Available at: https://www.cdc.gov/vhf/ebola/healthcare-us/ppe/guidance.html. Accessed
2 May 2019
.

2.

Centers for Disease Control and Prevention
.
For U.S. healthcare settings: donning and doffing personal protective equipment (PPE) for evaluating persons under investigation (PUIs) for Ebola who are clinically stable and do not have bleeding, vomiting, or diarrhea. https://www.cdc.gov/vhf/ebola/healthcare-us/ppe/guidance-clinically-stable-puis.html
. Accessed
2 May 2019
.

3.

Siegel
JD
,
Rhinehart
E
,
Jackson
M
,
Chiarello
L
,
and the Healthcare Infection Control Practices Advisory Committee
.
2007 Guideline for isolation precautions: preventing transmission of infectious agents in healthcare settings
. Available at: https://www.cdc.gov/infectioncontrol/guidelines/isolation/index.html. Accessed
2 May 2019
.

4.

Verbeek
JH
,
Ijaz
S
,
Mischke
C
, et al.
Personal protective equipment for preventing highly infectious diseases due to exposure to contaminated body fluids in healthcare staff
.
Cochrane Database Syst Rev
2016
;
4
:
CD011621
.

5.

Alhmidi
H
,
Cadnum
JL
,
Koganti
S
, et al.
Shedding of methicillin-resistant Staphylococcus aureus by colonized patients during procedures and patient care activities
.
Infect Control Hosp Epidemiol
2019
;
40
:
328
32
.

6.

Jackson
SS
,
Harris
AD
,
Magder
LS
, et al. ;
Bacterial burden is associated with increased transmission to health care workers from patients colonized with vancomycin-resistant Enterococcus
.
Am J Infect Control
2019
;
47
:
13
7
.

7.

Livorsi
DJ
,
Arif
S
, Garry P, et al.
Methicillin-resistant Staphylococcus aureus (MRSA) nasal real-time PCR: a predictive tool for contamination of the hospital environment
.
Infect Control Hosp Epidemiol
2015
;
36
:
34
9
.

8.

Jackson
SS
,
Thom
KA
,
Magder
LS
, et al. ;
Patient contact is the main risk factor for vancomycin-resistant Enterococcus contamination of healthcare workers’ gloves and gowns in the intensive care unit
.
Infect Control Hosp Epidemiol
2018
;
39
:
1063
7
.

9.

Phan
LT
,
Maita
D
,
Mortiz
D
,
Bleasdale
SC
,
Jones
RM
.
Environmental contact and self-contact patterns of healthcare personnel: implications for infection prevention and control
.
Clin Infect Dis
2019
; 69(S3):S178–84.

10.

Phan
L
,
Su
YM
,
Weber
R
,
Fritzen-Pedicini
C
,
Edomwande
O
,
Jones
RM
;
Environmental and body contamination from cleaning vomitus in a health care setting: a simulation study
.
Am J Infect Control
2018
;
46
:
397
401
.

11.

Hajar
Z
,
Mana
TSC
,
Cadnum
JL
,
Donskey
CJ
.
Dispersal of gram-negative bacilli from contaminated sink drains to cover gowns and hands during hand washing
.
Infect Control Hosp Epidemiol
2019
; 40:
460
2
.

12.

Blanco
N
,
Pineles
L
,
Lydecker
AD
, et al.
Transmission of resistant gram-negative bacteria to health care worker gowns and gloves during care of nursing home residents in Veterans Affairs community living centers
.
Antimicrob Agents Chemother
2017
;
61:e00790-17
.

13.

Pineles
L
,
Morgan
DJ
,
Lydecker
A
, et al.
Transmission of methicillin-resistant Staphylococcus aureus to health care worker gowns and gloves during care of residents in Veterans Affairs nursing homes
.
Am J Infect Control
2017
;
45
:
947
53
.

14.

O’Hara
LM
,
Calfee
DP
,
Miller
LG
, et al.
Optimizing contact precautions to curb the spread of antibiotic-resistant bacteria in hospitals: a multicenter cohort study to identify patient characteristics and healthcare personnel interactions associated with transmission of MRSA
.
Clin Infect Dis
2019
; 69(S3):S171–7.

15.

Centers for Disease Control and Prevention
.
Hierarchy of controls
. Available at: https://www.cdc.gov/niosh/topics/hierarchy/default.html. Accessed
2 May 2019
.

16.

Katanami
Y
,
Hayakawa
K
,
Shimazaki
T
, et al.
Adherence to contact precautions by different types of healthcare workers through video monitoring in a tertiary hospital
.
J Hosp Infect
2018
;
100
:
70
5
.

17.

Krein
SL
,
Mayer
J
,
Harrod
M
, et al.
Identification and characterization of failures in infectious agent transmission precaution practices in hospitals: a qualitative study
.
JAMA Intern Med
2018
;
178
:
1051
7
.

18.

Alhmidi
H
,
Gonzalez-Orta
M
,
Cadnum
JL
, et al.
Contamination of health care personnel during removal of contaminated gloves
.
Am J Infect Control
2019
;
47
:
850
2
.

19.

Tomas
ME
,
Kundrapu
S
,
Thota
P
, et al.
Contamination of health care personnel during removal of personal protective equipment
.
JAMA Intern Med
2015
;
175
:
1904
10
.

20.

Salehi
H
,
Pennathur
PR
,
Da Silva
JP
,
Herwaldt
LA
.
Examining health care personal protective equipment use through a human factors engineering and product design lens
.
Am J Infect Control
2019
;
47
:
595
8
.

21.

Baloh
J
,
Reisinger
HS
,
Dukes
K
, et al.
Healthcare workers’ strategies for doffing personal protective equipment
.
Clin Infect Dis
2019
; 69(S3):S192–8.

22.

Mana
TSC
,
Tomas
ME
,
Cadnum
JL
,
Jencson
AL
,
Piedrahita
CT
,
Donskey
CJ
.
A randomized trial of two cover gowns comparing contamination of healthcare personnel during removal of personal protective equipment
.
Infect Control Hosp Epidemiol
2018
;
39
:
97
100
.

23.

Drews
FA
,
Mulvey
D
,
Stratford
K
,
Samore
M
.
Evaluation of a redesigned personal protective equipment gown
.
Clin Infect Dis
2019
; 69(S3):S199–205.

24.

Abad
C
,
Fearday
A
,
Safdar
N
.
Adverse effects of isolation in hospitalised patients: a systematic review
.
J Hosp Infect
2010
;
76
:
97
102
.

25.

Croft
LD
,
Harris
AD
,
Pineles
L
, et al. ;
Benefits of Universal Glove and Gown Primary Investigators
.
The effect of universal glove and gown use on adverse events in intensive care unit patients
.
Clin Infect Dis
2015
;
61
:
545
53
.

26.

Morgan
DJ
,
Pineles
L
,
Shardell
M
, et al.
The effect of contact precautions on healthcare worker activity in acute care hospitals
.
Infect Control Hosp Epidemiol
2013
;
34
:
69
73
.

27.

Harrod
M
,
Petersen
L
,
Westen
LE
,
Gregory
L
,
Krein
SL
.
Understanding workflow and personal protective equipment challenges across different healthcare personnel roles
.
Clin Infect Dis
2019
; 69(S3):S185–91.

28.

Bearman
G
,
Bryant
K
,
Leekha
S
, et al.
Healthcare personnel attire in non-operating-room settings
.
Infect Control Hosp Epidemiol
2014
;
35
:
107
21
.

29.

John
AR
,
Alhmidi
H
,
Gonzalez-Orta
MI
,
Cadnum
JL
,
Donskey
CJ
.
A randomized trial to determine whether wearing short-sleeved white coats reduces the risk for pathogen transmission
.
Infect Control Hosp Epidemiol
2018
;
39
:
233
4
.

30.

Anderson
DJ
,
Addison
R
,
Lokhnygina
Y
, et al. ;
The antimicrobial scrub contamination and transmission (ASCOT) trial: a three-arm, blinded, randomized controlled trial with crossover design to determine the efficacy of antimicrobial-impregnated scrubs in preventing healthcare provider contamination
.
Infect Control Hosp Epidemiol
2017
;
38
:
1147
54
.

31.

Morgan
DJ
,
Wenzel
RP
,
Bearman
G
.
Contact precautions for endemic MRSA and VRE: time to retire legal mandates
.
JAMA
2017
;
318
:
329
30
.

32.

Rubin
MA
,
Samore
MH
,
Harris
AD
.
The importance of contact precautions for endemic methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococci
.
JAMA
2018
;
319
:
863
4
.

33.

Kourtis
AP
,
Hatfield
K
,
Baggs
J
, et al. ;
Emerging Infections Program MRSA Author Group
.
Vital signs: epidemiology and recent trends in methicillin-resistant and in methicillin-susceptible Staphylococcus aureus bloodstream infections–United States
.
MMWR Morb Mortal Wkly Rep
2019
;
68
:
214
9
.

34.

Jones
M
,
Jernigan
JA
,
Evans
ME
,
Roselle
GA
,
Hatfield
KM
,
Samore
MH
.
Vital signs: trends in Staphylococcus aureus infections in Veterans Affairs medical centers–United States, 2005–2017
.
MMWR Morb Mortal Wkly Rep
2019
;
68
:
220
4
.

35.

Kwon
JH
,
Burnham
CD
,
Reske
KA
, et al.
Assessment of healthcare worker protocol deviations and self-contamination during personal protective equipment donning and doffing
.
Infect Control Hosp Epidemiol
2017
;
38
:
1077
83
.

36.

Casanova
LM
,
Erukunuakpor
K
,
Kraft
CS
, et al. ;
Assessing viral transfer during doffing of Ebola-level personal protective equipment in a biocontainment unit
.
Clin Infect Dis
2018
;
66
:
945
9
.

37.

Mumma
JM
,
Durso
FT
,
Ferguson
AN
, et al. ;
Human factors risk analyses of a doffing protocol for Ebola-level personal protective equipment: mapping errors to contamination
.
Clin Infect Dis
2018
;
66
:
950
8
.

38.

Gurses
AP
,
Dietz
AS
,
Nowakowski
E
, et al. ;
Human factors-based risk analysis to improve the safety of doffing enhanced personal protective equipment
.
Infect Control Hosp Epidemiol
2019
;
40
:
178
86
.

39.

Mumma
JM
,
Durso
FT
,
Casanova
L
, et al.
Common behaviors and faults when doffing personal protective equipment for patients with serious communicable diseases
.
Clin Infect Dis
2019
; 69(S3):S214–20.

40.

Kpadeh-Rogers
Z
,
Robinson
GL
,
Alserehi
H
, et al.
Effect of glove decontamination on bacterial contamination of healthcare personnel hands
.
Clin Infect Dis
2019
; 69(S3):S224–7.

41.

Robinson
GL
,
Hitchcock
S
,
Kpadeh-Rogers
Z
, et al.
Preventing viral contamination—effects of wipe and spray-based decontamination of gloves and gowns
.
Clin Infect Dis
2019
; 69(S3):S228–30.

42.

Mumma
JM
,
Durso
FT
,
Casanova
L
, et al.
Variability in duration and thoroughness of hand hygiene in biocontainment units
.
Clin Infect Dis
2019
;
2019
.

43.

DuBose
JR
,
Matić
Z
,
Sala
MFW
, et al. ;
Design strategies to improve healthcare worker safety in biocontainment units: learning from Ebola preparedness
.
Infect Control Hosp Epidemiol
2018
;
39
:
961
7
.

44.

Wong
MF
,
Matic
Z
,
Campiglia
GC
, et al.
Design strategies to reduce risk during doffing of high-level personal protective equipment in biocontainment units
.
Clin Infect Dis
2019
;
69(S3):S241–7
.

45.

Andonian
J
,
Kazi
S
,
Therkorn
J
, et al.
Effect of an intervention package and teamwork training to prevent healthcare personnel self-contamination during personal protective equipment doffing
.
Clin Infect Dis
2019
; 69(S3):S248–55.

46.

Therkorn
J
,
Drewry
D
,
Andonian
J
, et al.
Development and comparison of complementary methods to study potential skin and inhalational exposure to pathogens during personal protective equipment doffing
.
Clin Infect Dis
2019
; 69(S3):S231–40.

47.

Toth
D
,
Khader
K
,
Beams
A
,
Samore
M
.
Model-based assessment of the effect of contact precautions applied to surveillance-detected carriers of carbapenemase–producing Enterobacteriaceae in long-term acute-care hospitals
.
Clin Infect Dis
2019
; 69(S3):S206–13.

48.

McKinnell
JA
,
Singh
RD
,
Miller
LG
, et al.
The SHIELD Orange County Project–multi drug-resistant organism (MDRO) prevalence in 21 nursing homes and long term acute care facilities in Southern California
.
Clin Infect Dis
2019
. doi:10.193/cid/ciz119

49.

Slayton
RB
,
Toth
D
,
Lee
BY
, et al.
Vital signs: estimated effects of a coordinated approach for action to reduce antibiotic-resistant infections in health care facilities–United States
.
MMWR Morb Mortal Wkly Rep
2015
;
64
:
826
31
.

50.

Toth
DJA
,
Khader
K
,
Slayton
RB
, et al.
The potential for interventions in a long-term acute care hospital to reduce transmission of carbapenem-resistant Enterobacteriaceae in affiliated healthcare facilities
.
Clin Infect Dis
2017
;
65
:
581
7
.

51.

Paul
P
,
Slayton
RB
,
Kallen
AJ
,
Walters
MS
,
Jernigan
JA
.
Modeling regional transmission and containment of a healthcare-associated multidrug-resistant organism
.
Clin Infect Dis
2019
. doi:10.1093/cid/ciz248

52.

Dumyati
G
,
Stone
ND
,
Nace
DA
,
Crnich
CJ
,
Jump
RL
.
Challenges and strategies for prevention of multidrug-resistant organism transmission in nursing homes
.
Curr Infect Dis Rep
2017
;
19
:
18
.

This work is written by (a) US Government employee(s) and is in the public domain in the US. This Open Access article contains public sector information licensed under the Open Government Licence v2.0 (http://www.nationalarchives.gov.uk/doc/open-government-licence/version/2/).