Usefulness of surveillance Cultures for Carbapenem-resistant Enterobacteriaceae, Carbapenem-resistant Pseudomonas aeruginosa and Vancomycin-resistant Enterococci in Hematopoietic Stem Cell Transplant Unit

doi:10.21203/rs.3.rs-109628/v1

Surveillance strategies to detect colonization is an important tool to prevent and control the spread of microorganisms especially among Hematopoietic Stem Cell Transplant (HSCT) patients. Colonization by Multidrug-resistant organisms (MDRO) has been evaluated as a risk factor for blood stream infection (BSI) in HSCT patients. The aim of this study was to evaluate the use of routine surveillance culture to screening colonization and infection by carbapenem-resistant Enterobacteriaceae (CRE), carbapenem-resistant Pseudomonas aeruginosa (CRPa) and vancomycin-resistant enterococci (VRE) in a HSCT unit.

Methods Surveillance cultures were collected from patients admitted to the HSCT unit over one-year, with swabs for cultures on admission and then weekly until discharge. We compared surveillance culture positivity for each site and agent, also clinical and epidemiological data according to the colonization status.

Results 200 HSCT patients underwent surveillance, with 1.323 samples collected. Infection due to MDRO occurred in 52 (21.5%) patients, among them 45 (86.5%) were blood stream infection (BSI) and 12 (23%) had positive surveillance culture before infection. 554 (41.8%) surveillance cultures were performed for CRPa, 413 (31.2%) for VRE, and 356 (27%) for CRE. Of these, 179 (13.5%) surveillance culture were positive, with greater positivity for oropharynx (6, 35.3%) CRPa, and rectal samples (16, 20.7%) for CRE. Being colonized by any MDRO, CRE (p <0.001) and CRPa (p = 0.027) was associated with a higher risk of infection in the bivariate analysis but being colonized was not associated with risk of death.

Conclusion Previous colonization by MDRO was a significant risk factor for infection by these pathogens, mainly colonization by CRE. Overall, rectal swab was the best site with the higher positivity, and the oropharynx was also an option for CRPa investigation. Feces culture showed low positivity and should be avoided. Although the impact of the strategy on the mortality of patients undergoing HSCT is not clear, VRE surveillance should be questioned in auto-HSCT patients as it has an additional cost and little impact on survival.

Applied & Industrial Microbiology

General Microbiology

Infectious Diseases

Hematopoietic Stem Cell Transplant infection

Hospital-acquired infection

Multidrug-resistant organisms

Surveillance Cultures

Blood Stream Infection

Infections are the major cause of death in Hematopoietic Stem Cell Transplant (HSCT) patients [1]. These patients are at high-risk for acquiring health care infections and the use of antibiotics during febrile neutropenia leads to a higher prevalence of multi drug resistant organisms (MDRO) in this population, [2] in addition to the risk of dissemination in the transplant unit.

A previous study in our hospital has identified previous gut colonization by MDRO, particularly by Gram Negative bacteria, as associated with blood stream infection (BSI) in patients undergoing HSCT [3].

Surveillance strategies to detect colonization have been considered important tools for preventing and controlling the spread of MDRO in the hospital setting [4, 5]. However, the cost effectiveness of this strategy in HSCT units and its impacts in patient’s outcome is still controversy [6–8].

The aim of this study was to evaluate the use of routine surveillance culture to track colonization and infection by carbapenem-resistant Enterobacteriaceae (CRE), carbapenem-resistant Pseudomonas aeruginosa (CRPa) and vancomycin-resistant enterococci (VRE) in a HSCT unit.

The Hospital das Clínicas of Faculdade de Medicina da Universidade de São Paulo (HCFMUSP) is a tertiary hospital, in São Paulo, Brazil, with 2,200 beds. The HSCT unit is a 23-bed unit with 4 beds designated to allogeneic and 18 to autologous transplant. The beds designated for the allogeneic transplant are individual bedrooms, with positive pressure air circulation with high-efficiency particle air filter, and the beds designated for the autologous transplant are shared bedrooms, with the maximum number of two beds per room.

Antibacterial prophylaxis was administered with levofloxacin on the first day of stem cell infusion and discontinued when recovery of neutropenia or if the patients developed febrile neutropenia. Antiviral prophylaxis, antifungal and anti-Pneumocystis were administered according to guidelines [1].

Surveillance cultures were collected from patients admitted to the HSCT unit over one-year (2012). Swabs were collected for cultures on admission and then weekly until discharge, from multiple sites: axilla, feces, oropharynx and/or rectum.

The culture swabs for CRE and CRPa were incubated overnight in liquid media and then plated in Agar MacConkey medium with a meropenem disk (Ferreira et al 2018), and surveillance cultures of feces samples for VRE, in medium with vancomycin 6 mg/L [9].

Colonization was defined as the presence of at least one positive surveillance culture for one of the studied microorganisms.

Identification of resistant bacteria was performed with VITEK 2 (Biomeurieaux, ‎Marcy-l'Étoile, France).

Clinical and epidemiological data were collected regarding sex, age, length of stay in BTM unit, diagnosis, use of antibiotics, infection, blood stream infection (BSI), and intra-hospital death. Infection was defined as CDC guidelines [10].

Statistical analysis

All data was stored in a database in Excel 97-2004 (Microsoft, Redmond, WA, United States). We compared surveillance culture positivity for each site and agent. Clinical and epidemiological data were analyzed according to the colonization status. All statistical analyses were performed using EpiInfo 7.0 (CDC, Atlanta, United States) Fisher's exact test or Chi-square test were used for categorical variables, as appropriate, and Mann–Whitney and Log-Rank testes for continuous variable. Univariate analysis and multivariate logistic regression analysis were performed (95% confidence interval). We considered a P value < 0.05 as statistically significant. A Kaplan–Meier curve was generated to compare survival among patients with and without BSI.

A total of 200 HSCT patients underwent surveillance, with 1.323 samples collected. The mean age was 45 years, 107 (53.5%) males and 17.7% of hospital death, and 59% patients performed Auto-transplantation as shown in Table 1.

Table 1

Characteristic of patients who underwent a surveillance culture, in HSCT ward, Hospital of Clinics, São Paulo
	N (%)
Total	200 (100)
Age mean (years)	45 y
Sex (Male)	107 (53.5)
Surveillance samples	1323 (100)
Allo-HSCT	82 (41)
LOS in days. Mean (range)	19.4 (1–66)
LOS in days until MDRO colonization. Mean (range) CRE CRPa VRE	16 (0–55) 18 (1–55) 20 (0–39) 10.5 (0–40)
LOS in days until MDRO infection Mean (range) CRE CRPa VRE*	23 (0–77) 26.7 (0–77) 21 (0–51) 19
Hospital Death	43 (17.7)
MDR- Multi-Drug Resistant Organism, Allo- allogenic, CRE – Carbapenem Resistant Enterobacteriaceae; CRPa - Carbapenem Resistant Pseudomonas aeruginosa; VRE – Vancomycin Resistant Enterococci. LOS- Length of Stay. *Only one case of VRE infection

We performed 554 (41.8%) surveillance cultures were performed for CRPa, 413 (31.2%) for VRE, and 356 (27%) for CRE. Of these, 179 (13.5%) surveillance culture were positive, with greater positivity for oropharynx (6, 35.3%) CRPa, and rectal samples (16, 20.7%) for CRE. Feces samples performed displayed only 12.6% of positivity, and CRE positivity was two times higher in rectal cultures. Infection due to MDRO occurred in 52 (21.5%) patients, among them 45 (86.5%) were bacteremia and 12 (23%) had positive surveillance culture before infection. Median detection time to positivity surveillance cultures until infection due to MDRO was 21.4 days for infection due CRE and 14.1 days for infection due CRPa (Table 2).

Table 2

Data from surveillance cultures, collected from inpatients at the HSCT ward, Hospital of Clinics, São Paulo
Survillance culture	Total (%)	Positive Samples	Positivity by site
Survillance culture	Total (%)	Positive Samples	Axilary (116)	Feces (1109)	Rectal (82)	Oropharynx (17)
Total Samples CRE (%) CRPa (%) VRE (%)	1324 (100) 356 (27) 554 (41.8) 413 (31.2)	179 (13.5) 85 (23.8) 41 (7.4) 53 (12.8)	16 (13.8) 62 (20.7) 28 (6.9) 50 (12.5)	140 (12.6) 62 (20.7) 28 (6.9) 50 (12.5)	17 (20.7) 13 (39.4) 1 (2.6) 3 (25)	6 (35.3) 5 (45.5) 1 (14.3) 3 (25)

CRE – Carbapenem Resistant Enterobacteriaceae; CRPa - Carbapenem Resistant Pseudomonas aeruginosa; VRE – Vancomycin Resistant Enterococci

The average LOS time for colonization and MDRO infection was 16 and 23 days respectively. Infection and colonization by VRE occurred earlier, when compared to other bacteria, however having VRE was not a risk factor for MDRO infection and death

Being colonized by any MDRO, CRE (p < 0.001) and CRPa (p = 0.027) was associated with a higher risk of infection in the bivariate analysis, and only colonization by CRE (p = 0.009) remained significant in the multivariate analysis (Table 3).

Risk for death was significantly higher among patients with any MDRO infection, including CRE and CRPa in the bivariate analysis (p < 0.001), whereas in the multivariate analysis, only CRPa infection (p = 0.028) remained significant (Tables 3 and 4).

Table 3.
Risk factors for death and infection - total and stratified by each agent in a bivariate analysis, in a HSCT ward, Hospital of Clinics, São Paulo

Death
Risk factor		Deaths/Patients with risk factor (%)			Deaths/Patients without risk factor (%)				OR					CI (95%)				P
Colonization by: any MDRO		20/94 (21.28)					22/145 (15.17)				1. 08					0.95	1.22			0. 22
CRE		12/50 (24)					30/189 (15.87)				1. 11					0.94	1.31			0. 18
CRPa		5/31 (16.13)					37/208 (17.79)				0. 98					0.83	1.16			0.82
VRE		7/47 (14.89)					35/192 (18.23)				0.96					0.84	1.10			0.59
Infection by: any MDRO		22/44 (50)					21/196 (10.71)				1. 79					1.32	2.41			<0.001
CRE		10/21 (47.62)					33/219 (15.07)				1.62					1.07	2.44			<0.001
CRPa		16/26 (61.54)					27/214 (12.62)				2. 27					1.39	3.70			<0.001
VRE		1/1 (100)					42/239 (17.57)				Undefined					Undefined	Undefined			0. 18
Infection
Risk factor		Infections/Pat. with risk factor (%)				Infections /Pat. without risk factor (%)				OR					CI (95%)				P
Colonization by: any MDRO		26/94 (27.66%)				17/145 (11.72%)					1.22					1.06	1.40			0.002
CRE		19/50 (38%)				24/189 (12.70%)					1.41					1.13	1.76			<0.001
CRPa		10/31 (32.26%)				33/208 (15.87%)					1.24					0.97	1.59			0.027
VRE		12/47 (25.53%)				31/192 (16.15%)					1.13					0.94	1.35			0.133
Infection by Carbapenem Resistant Enterobacteriaceae
Risk factor				Infection CRE/Pat. with risk factor (%)				Infection CRE/Pat. without risk factor(%)					OR			CI (95%)				P
Colonization by: any MDRO				13/94 (13.83%)				8/145 (5.52%)					1.10			1.002	1.20			0.027
CRE				10/50 (20%)				11/189 (5.82%)					1.18			1.02	1.36			0.004
CRPa				2/31 (6.45%)				19/208 (9.13%)					0.97			0.88	1.07			1.00
VRE			5/47 (10.64%)					16/192 (8.33%)					1.03			0.92	1.14			0.57
Infection by Carbapenem Resistant Pseudomonas aeruginosa
Risk factor	Infections CRPa/Patients with risk factor (%)						Infections CRPa/Patients without risk factor (%)					OR				CI (95%)				P
Colonization by: any MDRO			15/94 (15.96%)				10/145 (6.90%)					1.11				1.004	1.22			0.025
CRE			11/50 (22%)				14/189 (7.41%)					1.19				1.02	1.38			0.003
CRPa			9/31 (29.03%)				16/208 (7.69%)					1.30				1.03	1.63			0.002
VRE			7/47 (14.89%)				18/192 (9.38%)					1.06				0.94	1.21			0.29
Infection by Vancomycin Resistant Enterococci
Risk factor			Infections VRE/Patients with risk factor (%)				Infections VRE/Patients without risk factor (%)				OR					CI (95%)				P
Colonization by: Any MDRO			1/94 (1.06%)				0/145 (0%)				1.01					0.99	1.03			0.39
CRE			0/50 (0%)				1/189 (0.53%)				0.99					0.98	1.00			1.00
CRPa			1/31 (3.23%)				0/208 (0%)				1.03					0.97	1.10			0.13
VRE			1/47 (2.13%)				0/192 (0%)				1.02					0.98	1.07			0.19

CI – Confidence Interval; MDRO – Multi-Drug Resistant Organism (CRE. CRPa or VRE); CRE – Carbapenem Resistant Enterobacteriaceae; CRPa - Carbapenem Resistant Pseudomonas aeruginosa; VRE – Vancomycin Resistant Enterococci.

Table 4.

Variables associated with infection in a multiple logistic regression, BTM Unit, Hospital of Clinics, São Paulo
Infection
Colonization by:	OR	CI (95%)		P
CRE	4.54	1.46	14.13	0.009
CRPa	1.91	0.68	5.35	0.220
VRE	1.77	0.60	5.23	0.304
any MDRO	0.71	0.18	2.89	0.636

OR – Odds Ratio; CI – Confidence Interval; MDRO – Multi-Drug Resistant Organism (CRE. CRPa or VRE); CRE – Carbapenem Resistant Enterobacteriaceae; CRPa - Carbapenem Resistant Pseudomonas aeruginosa; VRE – Vancomycin Resistant Enterococci.

CRE infection occurred more significantly among CRE colonized (p = 0.004), and CRPa infection occurred more among CRPa colonized (p = 0.002). Having any MDRO was associated with a higher risk of infection in a bivariate analysis (Table 2).

Chance of Survival was significantly lower among patients with BSI, as demonstrated in the Kaplan Meier curve (P = 0.012), as well as among those infected with CRPa (0.0053).

The prevalence of colonization and type MDRO varies greatly according to the study centers, depending on epidemiology and local practices, such as the use of antibiotic prophylaxis, type of HSCT, among other factors [5–8]. In this study, the positivity of the surveillance culture was 13.5% lower than data from Europe [4, 11]. CRPa and VRE were the main MDRO, both colonizing 42% of patients with MDRO. The average length of hospital stays until the first positive culture varied according to the pathogen, the time for colonization with VRE was 10 days while for CRPa was much longer (20 days). Heidenreich et al diagnosed 27% of colonization by MDRO in the first 100 days after transplantation, with a predominance of CRPa (26.9%), with a pre-induction prevalence of 16% in German (11). Sadowska-Klasa in Poland obtained 42% colonization by MDRO during hospitalization, with an important predominance of VRE [4].

In this cohort, previous colonization by MDRO was a significant risk factor for infection by these pathogens, mainly colonization by CRE. A study at our center, in the 2014–2015 period, also reported that colonization by previous MDRO was associated with BSI (p < 0.001), with 20% of patients colonized by GNB-MDR developed BSI by these agents [3]. Other studies have also found similar findings [12, 13] Therefore, strategies for selective decolonization of the gastrointestinal tract (SDD) have been evaluated. A single center study demonstrated cost-effectiveness of SDD in CRE colonized patients in intensive care units [14]. However, a systematic review of 2019 still classifies the evidence indicating benefit in decolonization as limited and does not recommend this routine intervention, moreover. studies with immunocompromised patients are still extremely scarce in the literature [15].

Although, colonization is associated with a higher risk of infection, the impact of the strategy on the mortality of patients undergoing HSCT is not clear. We observed that infection by any MDRO, CRE and mainly by CRPa was associated with the risk of death; moreover, being colonized was not a risk factor for death. In other studies, a higher risk of death was observed in colonized patients. Sadowska-Klasa et al. [4] and Bilinski et al. [7] evaluated patients undergoing allogeneic HSCT and in both studies, colonization by MDRO had an impact on overall survival (OS) in 1 year. The relative high rate of Auto-HSCT in our series (59%) may explain our results.

In our study, we obtained a high prevalence of VRE colonization; which was the only MDRO that did not affect the risk of infection. Perhaps its lower virulence in relation to gram-negative bacillus (GNB) has influenced the lower impact of colonization by MDRO on hospital mortality in our population [16]. In contrast, a study conducted at the Mayo Clinic, with a 10-year series evaluated the influence of colonization by VRE on the prognosis of patients undergoing Allo-HSTC by AML. In multivariate analysis, colonization by VRE was an independent risk factor for VRE infection, but did not influence any other post-transplant outcome [8].

Corroborating this point, in a multicenter study carried out in Italy (52 centers), being colonized by resistant gram-negative bacteria significantly reduced 4-month survival. In addition, colonization by CRE and CRPa increased the risk of infection with these pathogens (p < 0.001) [16]. On the other hand, Heidenreich and colleagues [11] also found a similar risk of death regardless of the status of colonization by MDRO, even though CRE was the main colonizer in his studied population [11].

Our data corroborate the fact that the rectal swab is more sensitive than the culture of feces [18, 19], especially regarding VRE and CRE. Despite this, the use of rectal swab in HSCT patients should be used with care, to avoid skin or mucosal breakdown during severe neutropenia. In this scenario, the oropharyngeal swab may be an alternative, since it presented a high positivity for CRE and VRE. We observed that the type of surveillance culture site depends on the pathogen, feces culture showed low positivity and should be avoided; and VRE surveillance should be questioned in patients undergoing autologous transplantation because it has an additional cost and little impact on survival and development of bloodstream infection.

The present study, in addition to being carried out in a single center, has the disadvantage of being retrospective. However, it brings important reflections to the practice of screening MDR in TCTH patients. Firstly, being colonized by MDRO does not seem to be a sufficient factor to interfere in post-HSCT survival, especially VRE colonization and in auto-HSCT patients.

BSI - blood stream infection

CRE - carbapenem-resistant Enterobacteriaceae

CI – Confidence Interval

CRPa - carbapenem-resistant Pseudomonas aeruginosa

GNB – Gram-negative bacteria

HSCT - Hematopoietic Stem Cell Transplant

LOS - Length of stay

MDRO – Multi-drug-resistant organisms

VRE - vancomycin-resistant enterococci

Ethics approval

This study was evaluated and approved by the ethics committee of the Hospital of Clinics, São Paulo University. Protocol number: CAAE: 50237715.4.0000.0068

Consent for publication

All authors cited consented to the publication

Availability of data and materials

The datasets analyzed during the current study are available from the corresponding author on reasonable request.

Competing interests

There are no conflicts of interest involved

Funding

No funds were used in this paper

Authors' contributions

Elisa Teixeira Mendes: Literature review, statistical analysis and paper writing

Matias Salomão, Lísia Moura Tomishi, Maura Salaroli Oliveira, Fernanda Sapadão, Thais Guimarães, Vanderson Rocha: Data collection, database construction, literature review, statistical analysis

Mariana Graça, Flavia Rossi: Laboratory and microbiological work and analysis

Silvia Figueiredo Costa: study design, orientation and structuring of the research and review the manuscript.

Acknowledgements:

We thank our HSCT patients

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Usefulness of surveillance Cultures for Carbapenem-resistant Enterobacteriaceae, Carbapenem-resistant Pseudomonas aeruginosa and Vancomycin-resistant Enterococci in Hematopoietic Stem Cell Transplant Unit

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Abstract

Figures

Background

Methods

Results

Discussion

List Of Abbreviations

Declarations

References

Status:

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