Transmission of resistant Gram-negative bacteria to Healthcare Personnel Gowns and Gloves during Care of Residents in Community-based Nursing Facilities

Abstract

Objective:

To estimate the risk of transmission of antibiotic resistant Gram-negative bacteria (RGNB) to gowns and gloves worn by healthcare personnel (HCP) when providing care to residents of community-based nursing facilities in order to identify the types of care and resident characteristics associated with transmission.

Design:

Prospective observational study

Settings and participants:

Residents and HCP from 13 community-based nursing facilities in Maryland and Michigan

Methods:

Perianal swabs were collected from residents and cultured to detect RGNB. HCP wore gowns and gloves during usual care activities, and at the end of each interaction, these were swabbed in a standardized manner. Transmission of RGNB from a colonized resident to gowns and gloves was estimated. Odds ratios (OR) of transmission associated with type of care or resident characteristic were calculated.

Results:

403 residents and their HCP were enrolled. Nineteen percent of enrolled residents with a perianal swab (n=399) were colonized with at least one RGNB. RGNB transmission to either gloves or gowns occurred during 11% of the 584 interactions. Showering the resident, hygiene or toilet assistance, and wound dressing changes were associated with a high risk of transmission. Glucose monitoring and assistance with feeding or medication were associated with a low risk of transmission. Residents with a pressure ulcer were 3 times more likely to transmit RGNB than residents without one (OR=3.3, 95%CI 1.0–11.1).

Conclusions:

Results suggest that gowns and gloves use in community nursing facilities should be prioritized for certain residents and care interactions found to be high risk for transmission.

Introduction

Over half (57%) of nursing home residents are colonized with multi-drug resistant organisms (MDROs).¹ Methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci (VRE) and multi-drug resistant Gram negative bacteria (RGNB) are among the most common MDROs in nursing facilities.^1,2 Eleven to fifty-nine percent of nursing home residents are colonized with RGNB.^1,3 Furthermore, these bacteria have been shown to spread from patient-to-patient by healthcare personnel (HCP).^4–6

Contact Precautions are used for MDRO colonized patients in acute-care hospitals, while in nursing homes only Standard Precautions are used.^7–9 There are few evidence-based guidelines describing best practices for the prevention of the transmission of MDROs in nursing homes.

Our group recently reported that transmission of RGNB from colonized residents to HCP’s gloves and gowns occurs during specific high risk care activities in Veterans Affairs (VA) nursing homes.¹⁰ However, the majority of nursing homes in the United States are not part of the VA system and are known as community nursing facilities. In contrast to VA-nursing homes, residents living here are older and more likely to be women. They are less likely to be affiliated with acute-care hospitals responsible for the nursing homes’ infection prevention¹¹. Therefore, it is important to identify if the same risk factors are also observed in this related but different population.

This study examined care-specific transmission of RGNB to HCP’s gowns and gloves in community nursing homes. In addition, we aimed to identify resident characteristics associated with transmission of RGNB.

Methods

Study Design and study population

We present data collected as part of a multi-center, prospective, observational study reporting the frequency of, and risk factors for, the contamination of HCP’s gloves and gown when providing care to residents of community nursing homes. We previously reported data describing MRSA transmission in this population.⁹ This report describes transmission of RGNB in the same cohort. The protocol was approved by the Institutional Review Boards of the University of Maryland and the University of Michigan.⁹

Residents from 13 non-VA community-based nursing facilities in Maryland (n=10) and Michigan (n=3) were approached for enrollment.⁹ Eligible residents were enrolled with written informed consent from them (84%) or their legally authorized representative (16%). HCP were enrolled with verbal consent.⁹

Data Collection

A research coordinator recorded demographic and clinical characteristics from enrolled residents, including the Activities of Daily Living (ADL) score. The ADL score includes bed mobility, transfer, toilet use and eating. A total ADL score ranges between 0 through 16. A score of 0 represents an independent resident, in contrast to a score of 16 that represents a totally dependent resident¹². A perianal swab was collected only once from each participating resident at enrollment. As part of the study, we asked HCP to wear gown and gloves during usual care activities. The research coordinator observed and recorded the types of care delivered during each interaction (which may include one or more than one type of care). When the HCP were finished with their care activities, the coordinator swabbed their gloves and gown in a standardized manner before these were removed completely and the HCP interacted with a different resident. A single pair of gloves and gown were worn during each interaction.⁹

Laboratory analysis

Residents’ perianal swabs and HCP’s gown and gloves swabs were enriched by inoculating 100 μl of the E-swab liquid into 5 ml of BHI broth and incubated 24 hours at 35–37°C in ambient air. This was later cultured on each of the following plates: MacConkey agar supplemented with 1μg/ml of ciprofloxacin; MacConkey agar supplemented with 1μg/ml of ceftazidime; and MacConkey agar supplemented with 1μg/ml of imipenem. Plates were streaked for isolation and incubated aerobically at 37°C for 24 hours. Identification was confirmed using VITEK II system (BioMérieux Inc.; Hazelwood, MO, USA). The Kirby-Bauer test was used to confirm each organism’s susceptibility to antibiotics. Organisms were categorized as susceptible, intermediate or resistant based on the Clinical Laboratory Standards Institute’s (CLSI) breakpoints.¹³

Study definitions

RGNB were defined as any pathogenic Gram-negative bacteria categorized as intermediate or resistant based on the Kirby-Bauer test for at least one of the following antibiotics: ciprofloxacin, ceftazidime, or imipenem.¹³ Residents were considered colonized with RGNB if their perianal culture was positive for at least one RGNB. Transmission to gowns and/or gloves with RGNB was deemed to occur when at least one strain isolated from the HCP’s gown or gloves matched the genus, species, and antibiotic resistance pattern of the strain isolated from the respective RGNB colonized resident.¹⁰

Statistical analysis

Resident characteristics were described using proportions for categorical variables and median and range (min-max) for continuous variables. The overall crude transmission rate was estimated as the number of HCP’s interactions that led to RGNB transmission over the total number of HCP’s interactions. Overall transmission rate to HCP’s a) gown or gloves, b) gloves only, and c) gown only were estimated. Additionally, the crude rate of transmission by type of care was estimated as the total number of HCP’s interactions that led to transmission during a particular type of care over the total number of HCP’s interactions of this particular type of care. Logistic regression, using generalized estimating equations (GEE)¹⁴ to account for the correlation of repeated measures within resident, was used to estimate the odds ratio (OR) associated with each type of care and resident characteristics. The OR, for example, gives the odds of RGNB transmission to the HCP’s gloves or gown when a resident receives a particular type of care divided by the odds of RGNB transmission when the resident receives care other than the particular type of care being examined. Types of care or resident characteristics with an OR >1.0 and p<0.05 for specific were considered high risk. Additionally, types of care or resident characteristics with strong ORs above 2.5 even if not statistically significant were considered as high risk.

Results

Resident Characteristics

A perianal swab was collected from 399 (99%) of the 403 enrolled residents. Among the 399 residents, 221 residents were enrolled in Maryland and 178 in Michigan. No significant difference in median age or gender was observed between both states.

Among 399 residents, 74 (19%) were colonized with at least one RGNB on their perianal skin at enrollment (Table 1). Colonized residents were more likely to be receiving rehabilitation care than non-colonized residents (51% vs 37%, p=0.03). Colonized residents also had a higher median ADL score than non-colonized residents (9 vs 7, p<0.01).

Table 1.

Demographic and clinical characteristics of enrolled residents of community nursing facilities by colonization status as detected on perianal swab.

Characteristics	Enrolled residents(n=399)*		P value
	Colonized with RGNB n=74	Non-colonized with RGNB n=325
Age (yr)	80(47–98)	80(39–102)	0.84
Gender			0.66
Male	24(32)	97(30)
Female	50(68)	228(70)
Race/Ethnicity			<0.01
White	64(86)	245(76)
African American	9(12)	74(23)
Hispanic	1(1)	2(1)
Asians	0(0)	1(0)
Native Hawaiian/other Pacific Islander	0(0)	1(0)
Rehab	38(51)	121(37)	0.03
ADL score	9(0–16)	7(0–16)	<0.01
Recent acute care hospitalization (3 months)	41(55)	211(65)	0.30
Devices
Indwelling urinary catheter	7(10)	28(9)	0.80
External urinary catheter     Ostomy	1(1) 3(4)	0(0) 8(2)	0.04 0.45
Feeding tube	4(5)	12(4)	0.50
Any wounds (any skin break)	31(42)	110(34)	0.20
Antibiotics at enrollment	11(15)	46(14)	0.88
Secretions at enrollment
Diarrhea	2(3)	8(2)	0.91
Stool incontinence	15(20)	43(13)	0.12
Heavy wound secretions	0 (0)	1(0)	0.81
Heavy respiratory secretions	1(1)	0(0)	0.19

^*Enrolled residents with a perianal swab collected

RGNB: Resistant Gram Negative bacteria

N(%)/median(min-max)

Microbiological Characteristics

A total of 110 RGNB were isolated from the residents’ perianal swabs. Ninety-two of the 110 (84%) belonged to the Enterobacteriaceae family, 13 (12%) were Pseudomonas aeruginosa and 5 (4%) were Acinetobacter baumannii. Among the 92 isolates from Enterobacteriaceae family, 80 (87%) were resistant to ciprofloxacin, 21 (23%) were resistant to ceftazidime, and 28 (30%) were resistant to imipenem. Among the P. aeruginosa isolates (n=13), 13 (100%) were resistant to ciprofloxacin, 3 (23%) were resistant to ceftazidime, and 7 (55%) were resistant to imipenem.

Among the A. baumannii isolates (n=5), 5(100%) were resistant to ciprofloxacin, 4 (80%) were resistant to ceftazidime and 3 (60%) were resistant to imipenem. Similarly, among these 110 resistant isolates, 67 (61%) were resistant to only one of the analyzed antibiotics, while 39% were resistant to two or more antibiotics.

Gown and Glove Transmission with RGNB by Type of Care

We observed a median of 7 (interquartile range 6–9) interactions per RGNB colonized resident. Overall, either gowns or gloves were contaminated with RGNB during 11% of 584 interactions with RGNB colonized residents. Gloves were contaminated during 9% of 581 interactions (3 interactions were missing a glove specimen), while gowns were contaminated during 3% of 584 interactions. Seventy-three percent of the interactions had only one type of care during the interaction; 11%, two; 6% three and 10% four or more types of care. The risk of RGNB transmission to gloves or gowns by type of care did not differ significantly when the type of care occurred alone or in conjunction with other types of care (data not shown).

RGNB transmission from colonized residents to HCP varied by type of care activity from 0% to 22% for gowns and 0% to 33% for gloves (Figure 1). We identified showering, wound dressing change, diaper change, hygiene assistance (brushing teeth, combing hair), bathing, dressing, and transferring the resident as high risk activities for glove contamination (Table 2). Providing physical or occupational therapy, only giving medications, and glucose monitoring were considered low risk activities for glove contamination (OR< 1.0, p< 0.05; or no transmission observed). Showering, diaper change, toilet and hygiene assistance, bathing, dressing, and transferring the resident were identified as high risk activities for gown contamination. Glucose monitoring, giving medications, and feeding were also identified as low risk activities for gown contamination, as no transmissions occurred during these interactions (Table 2).

Figure 1.

Crude transmission risk of antibiotic resistant Gram-negative bacteria to healthcare personnel’s gloves and gowns during care interactions with resistant Gram-negative bacteria colonized residents of community nursing homes. The Y axis details the different types of care that were identified and analyzed. The X axis represents the percent of crude transmission detected. The blue bars represent transmission to gloves and the beige bars represent transmission to gowns.

Table 2.

Odds ratio^† of transmission of RGNB to healthcare personnel’s gowns or gloves by type of care given to R-GNB colonized residents in community nursing homes.

Type of care	# interactions	% care given with other care	Gloves		Gowns
			OR	p-value	OR	p-value
Showering	18	72	5.7	<0.01	15.4	<0.01
Dressing change	5	40	3.6	0.01	No transmission
Bathing	56	86	3.4	<0.01	2.7	0.12
Hygiene assistance	57	96	2.5	0.07	3.8	0.08
Diaper change	91	82	2.5	0.02	2.7	0.09
Transfer of resident	114	76	1.9	0.05	3.0	<0.01
Feeding	19	21	1.7	0.56	No transmission
Toilet assistance	58	64	1.6	0.27	3.4	<0.01
Dressing resident	98	90	1.5	0.25	2.5	0.10
Only feeding	15	0	1.2	0.89	No transmission
Changing linens	66	50	1.1	0.82	0.40	0.61
Any surveillance cultures	69	3	1.1	0.88	No transmission
Any device care or use	17	47	0.93	0.92	1.3	0.84
Physical exam	76	36	0.82	0.61	2.0	0.22
Any therapy	87	21	0.30	<0.01	No transmission
Any medications	104	16	0.15	<0.01	0.3	0.28
Only medications	87	0	0.09	<0.01	0.5	0.40
Glucose monitoring	11	64	No transmission		No transmission

^†Odds of transmission divided by odds of transmission if that type of care was not given, calculated using GEE to account for the correlation of repeated measurements obtained from a given resident.

Additionally, a random sample of 26 residents who were not found to be colonized by RGNB in the perianal culture (183 interactions) were also analyzed. Of the 183 HCP interactions, 23 (13%) glove swabs and 16 (9%) gown swabs were RGNB positive. Of the 26 non-colonized residents, fifteen (58%) had HCP’s interactions positive for RGNB.

Resident Characteristics that Increase Gown and Glove Transmission with RGNB

We also examined whether certain resident characteristics changed the risk of RGNB transmission. Having diarrhea was uncommon (3%) in this population, so we focused on stool incontinence (15%). No strong association between having stool incontinence and transmission of RGNB was observed. Although heavy wound secretions were rare (<1%), 23% of the enrolled population had a pressure ulcer. Among colonized residents, those with a pressure ulcer were 3 times more likely to transmit RGNB to HCP’s gowns than those residents without a pressure ulcer (OR=3.3, 95% CI 1.0–11.1). A weaker association was observed for transmission to gloves (OR=1.6, 95% CI 0.7–3.8). High risk types of care were also identified among residents with an unhealed pressure ulcer. Among this subpopulation, showering (OR=14.0, p=0.01), hygiene assistance (OR=8.4, p=0.03), transferring the resident (OR=2.5, p=0.01), diaper change (OR=2.9, p=0.08), and dressing (OR=2.6, p=0.09) were associated with higher RGNB transmission to HCP’s gowns.

Having an ostomy bag also had a strong association with transmission to HCP’s gowns (OR=5.4, 95%CI 1.8–16.1); however, this finding was driven by HCP’s interactions with a single nursing home resident with other risk factors (i.e. hemiplegia, currently on antibiotics, feeding tube.).

Due to the selective pressure of antibiotics on MDRO colonization¹⁵, we analyzed the association between the resident’s antibiotic use and RGNB transmission risk. Fifteen percent of our colonized population was receiving systemic antibiotics at the time of enrollment. Our residents received fluoroquinolones, cephalosporins, tetracyclines, sulfamethoxazole trimethoprim, amoxicillin, or glycopeptides. We found that residents using systemic antibiotics at enrollment did not have a significantly higher odds of gown or glove contamination compared to residents not on antibiotics at enrollment (OR=1.5, p=0.57 vs. OR 1.3, p=0.66 respectively).

Discussion

Overall 11% of the HCP’s interactions with a RGNB colonized resident resulted in the transmission of RGNB to HCP’s glove or gowns in community nursing homes. Showering, bathing, and dressing the resident, as well as diaper change, providing hygiene, and transferring the resident were identified as high risk types of care for HCP’s gown and glove contamination. Glucose monitoring and assistance with medications were also identified as low risk activities. Having an unhealed pressure ulcer increased the risk of RGNB transmission from the resident to HCP.

The observed high risk and low risk types of care were consistent with previously published results by our group about RGNB transmission to HCP’s gowns and gloves from RGNB colonized residents in VA nursing homes.¹⁰ These findings were also consistent with the high risk and low risk types of care associated with MRSA transmission in this same population.⁹

Pressure ulcers have been shown to be reservoirs of multidrug resistant Gram-negative bacteria.^16,17 Braga et al. isolated 72 Gram-negative isolates from infected or colonized pressure ulcers of 60 different patients. Seven percent of the isolates were resistant to fluoroquinolones, 76% were resistant to cephalosporins, 14% were resistant to carbapenems and 40% were multi-drug resistant.¹⁶ Furthermore, the presence of pressure ulcers has been described as a risk factor associated with RGNB colonization.¹⁸ Given this and the high dependency of those with pressure ulcers on HCP for care, it is not surprising that interacting with a resident with a pressure ulcer was associated with a higher transmission risk of RGNB. This finding is consistent with previously published results by our group about MRSA transmission to HCP’s gowns and gloves from MRSA colonized residents in this same population.⁹ Additionally, we observed similar high risk activities associated with transmission of RGNB and MRSA among this subpopulation.⁹

Although we observed a similar risk of transmission of RGNB to gloves associated with systemic antibiotic use, we were unable to replicate the positive association between systemic antibiotic use and transmission to gowns previously described in VA community living centers.¹⁰ Although both colonized populations had similar antibiotic use at enrollment, the current population received mostly broad spectrum antibiotics, which could have impacted both Gram negative and Gram positive bacteria colonization and, as a result, their transmission to HCP’s gowns and gloves. Topical antibiotic use was not recorded for the current study which could help explain this difference.

As observed in our prior studies, we detected transmission of RGNB to HCP’s gloves or gown from residents not detected to be colonized by RGNB in the perianal culture.^9,10,19 Other potential sources of RGNB exist that could explain these findings such as other body sites of RGNB colonization (e.g. skin or wounds) or the environment.^20–24 It is important to highlight that the definition of transmission of RGNB in residents not found to be colonized at the study baseline is less strict than among colonized residents, as there is no baseline isolate to match the HCP’s gown and glove’s isolate by antibiotic resistance and specific bacteria. All nursing homes should recognize the high prevalence of RGNB in their population and environment. Colonization of RGNB in nursing home residents has been described as high as fifty-nine percent ^1,3, highlighting the need of appropriate and effective guidelines for gown and gloves use that protect their HCP and their other residents.

This study is limited by the fact that our outcome, transmission to HCP’s gowns and gloves, acts as a surrogate for RGNB transmission to other nursing home residents. We are unable to estimate how often contamination of gowns and gloves results in transmission to other HCP or residents.^10,19 We did not perform molecular typing to compare the residents’ strains with the strains isolated from gowns and gloves. In earlier studies, we observed a high concordance (up to 89%) between antibiotic resistant strains from residents and those detected on gowns and gloves.^9,21 Our study is strengthened by its design, a multi-site prospective study, which is representative of community nursing facilities across the United States.

In contrast to other healthcare settings, nursing homes call for a balance between infection prevention and a home-like atmosphere. Nursing homes are also more limited in resources compared to acute care hospitals. Therefore, evidence-based guidelines tailored to this setting are important. This study provides evidence supporting the potential benefit of a care-based or resident-specific approach to reduce the transmission of MDROs in community nursing homes.