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Outbreak report: a nosocomial outbreak of vancomycin resistant enterococci in a solid organ transplant unit

Outbreak report: a nosocomial outbreak of vancomycin resistant enterococci in a solid organ... Background: Vancomycin resistant enterococci (VRE) are an emerging problem in health care settings. The purpose of the investigation was to assess the extent of the outbreak including environmental contamination and to limit further transmission. Methods: We used retrospective patient and laboratory data including pulse field gel electrophoresis (PFGE) typing and virulence and resistance gene analysis. For comparison of medians the Mann-Whitney and for comparison of proportions the Fisher exact tests were used. Results: PFGE typing of VRE strains of an outbreak of 15 VRE cases in a solid transplant unit revealed that nine of the cases belonged to one identical pattern (A), which was only found twice in the environment. Eleven further positive environmental samples showed a different, but identical PFGE pattern E. Only one patient was infected with this environmental strain. Two of nine (22.2%) PFGE A, but nine of eleven (81.2%) PFGE E samples were positive for gelatinase E (p = 0.01), which is described as enhancing biofilm production, suggesting a survival benefit for this strain on inanimate surfaces. Conclusion: Routine disinfection was not able to stop the cluster, but after repeated enforcement of the infection prevention and control (IPC) bundle such as training, strict adherence to hand hygiene and surface disinfection no further cases were observed. We conclude that certain VRE strains predominate in the environment whereas others predominate in humans. Enforcement of the IPC bundle is essential for controlling VRE outbreaks and reducing further transmission. Keywords: Solid organ transplant unit, Vancomycin resistant enterococci, Outbreak, Survival benefit, Infection control Background (EU/EEA). The proportion of VRE in Austria (4.3% in Vancomycin resistant enterococci (VRE) are important 2016) was below the EU population weighted mean of causes of morbidity and mortality especially in health 11.8% (95% confidence interval (CI) 11–13%) [2]. Mono- care settings where they easily disseminate [1]. Effective clonal and polyclonal outbreaks of VRE were described treatment is limited and thus VRE remain a major chal- worldwide; the largest reported outbreaks comprised up lenge for infection control. to 72 cases [3]. Vancomycin resistance of invasive Enterococcus fae- The most important transmission-routes of VRE are cium isolates ranges between 0 and 46.3% in countries still not fully understood, but cross contamination via of the European Union and European Economic Area the hands of health care workers’ (HCW) is believed to play a major role. HCW act as a vector between colo- nized or infected patients, inanimate surfaces and previ- * Correspondence: astrid.mayr@i-med.ac.at ously unaffected patients [4]. The reservoir for VRE is Department of Hygiene, Microbiology and Social Medicine, Division of believed to be the human intestine [5]. Hygiene and Medical Microbiology, Medical University of Innsbruck, Innsbruck, Schoepfstr. 41, 6020 Innsbruck, Austria Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 2 of 9 Known risk factors for acquisition of VRE include pre- four beds per room) and an adjacent intensive care unit vious use of antibiotics, prolonged hospital stay, under- (ICU) consisting of eight beds situated in three separate lying diseases, admission to high risk departments such rooms. Patients were transferred between the standard as oncology, hematology, transplant or intensive care care unit and the ICU depending on their medical con- units (ICU), the nurse to patient ratio, and occupancy to dition. The ICT consisted of one senior hospital hygiene a room where previously a patient harboring VRE was specialist and a local hygiene team. admitted [6]. The transmission in high risk wards via contaminated inanimate surfaces is believed to be im- Routine IPC protocol portant but it remains a challenge to quantify the attrib- The internal IPC protocol included the following recom- utable risk [6] of environmental contamination. mendations: 1) twice daily unsupervised routine disinfec- We describe an outbreak which was identified on 7th tion of inanimate surfaces of the patient close environment January 2017 after detection of five cases within 2 with an aldehyde-free-broad-spectrum disinfectant contain- months following the Orion statement [7]. ing quaternary ammonium compounds (QACs, 2% TPH The objective of this investigation was to assess the protect, Schülke & Mayr GmbH, Vienna, Austria) including extent of the outbreak including the environmental once daily patient charts, 2) terminal cleaning and disinfec- contamination, to limit further transmission and to tion of patient rooms with the above mentioned disinfect- evaluate the effectiveness of implemented control mea- ant and 3) hand hygiene (HH) based on the WHO sures. Further important objectives were to foster infec- approach “My Five Moments for Hand Hygiene” [8]using tion prevention and control (IPC) education by the alcohol-based detergents (Sterillium®, BODE Chemie infection control team (ICT) of the University Hospital GmbH, Hamburg, Germany). Surveillance of hand hygiene Innsbruck (LKI). compliance is conducted through bi-annual audits based on the protocol from the Robert Koch Institute [9], measur- Methods ing adherence to HH. The outcomes of the audits were cat- Study design egorized as sufficient or insufficient per unit but lacked a We used retrospective data analysis including PFGE typ- coding system to quantify the adherence to HH on an indi- ing, analysis of virulence and resistance genes and pa- vidual basis. Annual trainings of the IPC protocol through tient relevant data from the hospital records. verbal presentations and ward round sessions were rou- tinely conducted. Data on baseline IPC knowledge of HCW Participants were not routinely collected. IPC guidelines did not require Participants were patients admitted to the solid organ trans- pre-admission VRE screening of patients, unless 1) patients plant unit between 15th November 2016 and 30th June had a positive history of exposure in a high endemic coun- 2017 with laboratory confirmation of VRE. Colonization try, 2) were transferred from a long-term-care-facility or 3) was defined as laboratory confirmation of VRE in a sample were previously known having been infected or colonized of a patient from a non-sterile site without signs of infection with VRE. such as fever > = 38.5 °C. Infection was defined as laboratory According to the IPC protocol, each newly identified confirmation of VRE in a sample of a patient from a nor- patient either colonized or infected by VRE irrespective mally sterile site or signs of infection such as fever > = 38.5°. of the patient being part of an outbreak, triggered a rou- tine infection control response consisting of following Case definition measures: isolation precautions, defined as placement in We defined a VRE case as a patient admitted to the a single room, if possible, and, contact precautions de- transplant unit during the observation period with la- pending on the estimated potential for transmission in- boratory confirmation of VRE in at least one sample ir- cluding personal protective equipment. respective of the location or type of sampling. We defined a cluster case as a VRE case with the outbreak Intervention during the outbreak PFGE pattern A identified between December 2017 and During the outbreak the following additional measures June 2018 and admitted to the transplant unit. were implemented: Re-emphasizing strict adherence to HH and to environmental disinfection including un- Setting announced microbiological monitoring of the environ- The period of the outbreak lasted from 15 November ment and HCW’s hands, repeated sampling of stool or 2016 until 30 June 2017. rectal swabs of the VRE positive patients, newly admitted The LKI is a 1600-bed tertiary-care hospital with sev- patients and rectal screening of HCWs. Rectal swabbing eral departments including a solid organ transplant unit. of patients was implemented as precautionary measure The setting of the outbreak was the ward of the trans- to limit the extent of the outbreak. Self-administered plant unit consisting of 15 beds in seven rooms (one to rectal swabbing of HCWs was conducted on voluntary Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 3 of 9 basis upon the urgency of the situation. Thus informed Columbia agar containing 5% sheep blood (Becton, consent was not obtained. Dickenson and Company, Franklin Lakes, USA) for ap- Frequency of ward round training was increased. The proximately 5 seconds [14, 15]. Confirmation of VRE choice of HH antisepsis and environmental disinfection was conducted as described above. during the outbreak remained the same and compliance with HH was observed by the ICT. No additional decon- PFGE tamination procedures such as fogging or steaming were Molecular Typing was performed using pulse field gel implemented. electrophoresis (PFGE) according to the protocols pub- lished by the Centers for Disease Control and Prevention Culturing and typing [16]. Extracted bacterial DNA was restricted using Smal Patient samples enzyme. Strain typing was performed by manual PFGE We collected routine clinical samples and rectal screen- restriction pattern analysis [17] and by computational ing swabs from patients according to the IPC protocol analysis of band differences using GelJ Software Version (no informed consent was requested for rectal sam- 2[18]. Dendrogram analysis of PFGE patterns was per- pling), cultivated them on blood agar (Becton Dickinson, formed using Dice algorithm and Single Linkage cluster- Heidelberg, Germany) and selective ChromID VRE Agar ing. Genotypically related strains with similarity > 90% (Biomerieux, Marcy-l’Étoile, France) and incubated them were considered belonging to the same pattern. for 48 h at 37 °C under aerobic conditions. Suspect col- onies were identified by matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-- Genetic analysis TOF, Bruker, Bremen, Germany). Antibiotic susceptibility Vancomycin resistance genotypes were determined ac- testing was performed according to the European Com- cording to the protocol from Jayaratne et al. [19]. The mittee on Antimicrobial Susceptibility Testing (EUCAST enterococcal surface antigen was identified according to version 6.0, 2016) protocol [10]. Enterococci were classified the protocol by Toledo-Arana [20], the cytolysin activa- as VRE if the minimal inhibitory concentration of vanco- tor according to Vankerckhoven [21] and the gelatinase mycin was above 4 mg/L identified by E-Test (Biomerieux, E according to Hancock’s protocol [22]. Marcy-l’Étoile, France) [11]. Additional patient data such as diagnosis, duration of hospital stay, outcome, type and time of transplantation were obtained from the medical Infection related outcomes records of the LKI. Infection related outcomes, including colonization, in- fection and patient survival were assessed. Environmental samples The specimen processing and turn-around time were Unheralded sampling of environment was conducted ac- performed according to local laboratory protocol from cording to Galvins protocol (Galvin) using Columbia-III-Sheep blood agar 5% (Oxoid Limited, Basingstoke, UK) or Tryptic soy agar with neutralizers (VWR International, Radnor, USA) contact plates with a Sample size press on time of 10 seconds without any lateral move- The sample size was limited to the number of identified ment. Surfaces were selected at different locations close patients (n = 15). and distant from the respective patients [12] during three occasions: immediately after the alert of the cluster on 18 January, and twice after enforcement of control Statistical methods measures (30th January and 2nd February 2017, respect- Variables of interest were stored in excel database in- ively). Data recorded were date, type and location of cluding age, gender, number of isolates obtained includ- sampling, laboratory findings and PFGE results. Direct ing positives, date of available laboratory result, source unheralded observation of hygienic measures was con- and material of samples, length of hospital stay, previous ducted to identify potential gaps of adherence to infec- antibiotic treatment, previous confirmation of VRE in tion control measures. Patient close samples were any sample, diagnosis, other identified pathogens, and defined as samples obtained from the vicinity of patients patient outcome. such as the bedrail, bedframe, beside tables, clamps for Descriptive analysis was performed using Epi info ver- urine-bags, drug perfusors, stethoscope and bedside sion 7.2.2.2. (CDC Atlanta). For comparison of medians monitors [13]. the Mann-Whitney and for comparison of proportions Microbial monitoring of HCWs hands was performed the Fisher exact tests were used. A p-value of < 0.05 was by imprinting all fingertips including the thumb onto considered statistically significant. Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 4 of 9 Results additional patients (Fig. 1). Of these, ten patients (66.7%) Event description were males with a median age of 56.5 years (50– On 7th January 2017 the outbreak response team of the 71 years). The five female patients showed a median age LKI informed the transplant unit about a potential out- of 70 years (60–79 years) (p = 0.003) (Table 1). break of VRE. VRE was first isolated twice from blood cultures, five Analysis of historical data revealed that between May times from urine samples, four times from wound drainage 2012 and October 2016, a total of 53 VRE cases were and once each from a tissue, stool, and rectal swab and from identified at this unit. The median incidence was one a broncho-alveolar lavage sample. Three of the patients were (0–3) case per month and the annual median incidence classified as being colonized, the remaining twelve as being was 11 cases (6–16 cases) per year for the period 2013– infected with VRE. The median length of hospital stay was 2016. In comparison to previous years, the observed 24 days (10–112 days). All but one patient underwent trans- number of five VRE cases in a period of less than 2 plantation and received immunosuppression. Twelve pa- months clearly exceeded the expected value suggesting tients survived (80%) and three died (Table 1). In all patients an outbreak. Enterococcus faecium was identified, one patient harbored a tigecycline resistant, two a linezolid resistant and fourteen VRE cases teicoplanin resistant strains. After a period of 4 months without any detection of VRE from the transplant unit, the potential index case was confirmed on 15th November 2016. He was a PFGE patterns of cases 58 year old male suffering from IgA Nephritis who re- PFGE patterns were available for 13 of 15 patients (86.7%). ceived a kidney transplant on 12th November 2016, 3 Among those, five different PFGE patterns were identified days prior to the diagnosis of VRE in a single sample of and subsequently classified as patterns A to E. Nine of the a retroperitoneal surgical-site-drainage. The patient was thirteen cases (69.2%) were classified as PFGE pattern A classified as being infected. (further called cluster strain, Table 1,Fig. 2). Between 15th November 2016 and 30th June 2017, All 10 of the 15 patient isolates (66.7%) available for VRE was confirmed in at least one sample of 14 vancomycin resistance genotyping (vanR) revealed vanA, Fig. 1 Number of cases by PFGE pattern, week of diagnosis and main interventions (n = 15) Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 5 of 9 Table 1 Patient characteristics Categories N/total or median (mean; range) % Demographic characteristics Males 5/15 67 Age 59 yrs. (61.3 yrs.; 50–79 yrs) – Clinical findings Infected (versus colonized) 12/15 80 Deceased 3/15 20 Laboratory sampling Number of samples investigated per patient 24 (31; 8–105) – Number of positive samples per patient 2 (6.1; 1–52) – Laboratory findings PFGE pattern A (cluster strain) 9/13 69 PFGE pattern E (environmental strain) 1/13 8 other PFGE patterns 3/13 (one each) 23 irrespective of their PFGE pattern. The only patient iso- once on a patients chart after the first enforcement of late with pattern E, was not viable. control measures. All other eleven VRE positive environ- mental samples revealed one identical PFGE pattern E Cluster cases which was distinct from the patient cluster strain (Fig. 2). In total, 194 patient samples were obtained from cluster Pattern E was confirmed only in one patient, who was ad- cases, in 26 of them (13.4%) VRE was confirmed. The mitted 2 days prior to the first environmental sampling. median number of samples investigated per cluster case Eight of these positive non-cluster strains (PFGE E) were was 20 (12–34) and the median number of positive sam- identified during the first on-site visit. Six of them were ples was one (1–12). Five patients only had one sample determined in the patient close environment and two out- positive for VRE. The median duration of confirmation side patient rooms. During the third visit the environmen- between the first and the last positive sample was 4 days tal PFGE E strain was identified again three times. Once (1–33 days). The median interval between admission and from the patient close environment (urine clamp bag) of first isolation of VRE was 13 days (same day-22 days) the patient infected with PFGE E; and twice from a bed lo- (n = 14). One additional patient already tested positive cated in the corridor (Fig. 3). All tested environmental in another unit during the outbreak period, but the iso- strains were vanApositive. late was different from the cluster strain (PFGE C). One VRE positive hand sample of a HCW was not From all other cases no information of previous VRE available for PFGE typing. carriage was available as no routine VRE screening was conducted prior to this outbreak. VRE was first Virulence genes identified in following materials from the nine cluster Twenty three samples were available for virulence gene cases: Blood (n =1), (wound) drains (n = 4), rectal swab testing (13 environmental and 10 patient samples). (n =1), and urine (n =3). Two of nine (22.2%) PFGE A (six patient samples), but nine of 11 (81.2%) PFGE E (all environmental samples) VRE screening were positive for gelatinase E (p = 0.0123). The two gela- Pre-admission rectal screening was implemented after tinase E positive PFGE A samples were one human sam- the outbreak alert. Among 169 patients screened until ple from a patient already discharged at the time of the the end of 2017, only one was found to be VRE positive environmental sampling and one environmental sample (0.6%). from a urinary bag clamp obtained during the first on-site visit which could not be linked to a specific Environmental and hand samples patient. A total of 139 hand (n = 26; 18.7%) and environmental All investigated samples were positive for enterococcal (n = 113, 81.3%) samples were obtained during three un- surface protein and negative for cytolysin activator. heralded on-site visits; nearly half of them (n = 68, 48.9%) were obtained prior to the first enforcement of Control measures control measures. More samples taken prior to en- The first of the three unheralded on-site visit including hanced disinfection (n = 10; 14.7%) were positive for environmental and hand sampling was undertaken on VRE compared to post disinfection sampling (n =4; 18th January 2017. Lack of adherence to hand hygiene 5.6%) (p = 0.07). Among the thirteen VRE positive envir- was observed and therefore enforcement of control mea- onmental samples the cluster strain (PFGE A) was iden- sures was stressed by the infection control hygiene team. tified twice: once from a clamp of a urine-bag prior and At the time of this first visit, five patients were admitted Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 6 of 9 participation was voluntary. In the current IPC protocol HCW hand sampling but no rectal swabbing is included. During the last on-site visit on 2nd February, VRE was detected in four of 47 (8.51%) environmental samples. Three of those revealed PFGE E, all from patient-close sites of the patient infected with PFGE E, the cluster strain (PFGE A) was isolated from a patient chart. At the time of the third visit, five patients (two with PFGE A) were still admitted to the ward; four further cases, two with the cluster PFGE A were identified later. En- forcement of IPC measures was rigorously stressed again and four ward round sessions were conducted. Insuffi- cient adherence to HH according to the IPC protocol was documented during the first visit. During the second and third visit the adherence to HH was evaluated to be sufficient. The terminal cleaning was audited by the ICT and adherence was defined as sufficient already at the first visit. The effect of teaching was not measured. Discussion We describe an outbreak of fifteen VRE cases in a solid organ transplant unit in late 2016 and early 2017, of which nine patients revealed an identical PFGE pattern A, further called the cluster strain. During the first visit six VRE positive environmental samples were identified in the patient close environment which suggests lack of effective decontamination despite the audited terminal disinfection which was considered sufficient. Additionally, lack of adherence to strict hand hygiene was observed and compliance to HH was classi- fied as insufficient. The two positive samples identified from a laundry rack suggest cross-contamination via HCW hands, as all patients were immobile. The fact, that the majority of environmental strains were identical - although distinct from the outbreak strain - may sug- gest that also prior to the first sampling environmental contamination via HCW hands may have occurred. HH adherence during audits improved from insufficient dur- Fig. 2 Dendrogram of PFGE patterns of human (n = 13; pattern A = 9, ing the first visit to sufficient during the second and one each pattern B, C, D, E and environmental VRE strains (n =13; third visit. pattern E = 11, pattern A = 2) including 3 control strains Enforcement of ICP measures resulted in a decrease of the proportion of VRE contaminated environmental sam- ples, although it was not significant (Fig. 3). Nevertheless, (two with PFGE A, one each with PFGE B and E and reconfirmation of the non-cluster strain during the third one without a viable isolate) and six already discharged site visit may be due to recontamination and insufficient (five of whom with PFGE A and one with PFGE C). compliance to hand hygiene. In addition, the confirmation The second sampling on 30th January, performed after of the cluster strain on a patient chart after enforcement extended cleaning and disinfection procedures towards of control measures suggests the cross-contamination via patients’ distant zones did not detect any environmental HCW hands as well as ineffective decontamination of the contamination. Rectal screening targeting all staff was patient chart. Decontamination of patient charts is de- conducted the same day. The participation rate was 79% (94 scribed as effective measure to decrease horizontal trans- of 119), all samples remained negative. Non-participation fer of organisms and to prevent transmission of health was mainly due to absence; No consent was obtained as care associated infections [23, 24]. Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 7 of 9 Fig. 3 Number and results of hand and environmental samples by intervention (n = 139) We speculate that the lack of strict adherence to ad- The cluster strain PFGE A was identified only twice in equate hand hygiene might have led to contamination of the environment; all other environmental strains re- the environment. This is supported by the facts that firstly, vealed an identical PFGE E pattern. This PFGE E pattern contamination was observed in patient distant areas such was found only in one patient. The fact, that significantly as laundry racks and secondly, that contaminated patient more PFGE E compared to PFGE A strains were produ- charts are described being a result of lack of adherence to cing gelatinase E, which is described as enhancing bio- recommended HH [25]. This may have played an import- film production, suggests a survival benefit on inanimate ant role in triggering the outbreak. Tight working spaces in surfaces [33]. Accumulation of mobile genetic elements the ICU unit favor the patient-to-patient contact [26]and including plasmids, pathogenicity islands, resistance mayhaveresultedinahigher risk fortransmissionofVRE. transposons other fitness islands, phages and surface Hayden concludes that the role of environmental con- types [34, 35] may also have contributed to better sur- tamination in nosocomial cross-transmission of VRE is vival in the environment. still unresolved but enforcement of environmental de- The limitations of our study are that we used retro- contamination was both associated with reduction of spective data analysis which made selection of appropri- surface contamination and contamination of HCWs’ ate controls difficult. Also logistical reasons hindered us hands despite only moderate adherence to proper hand to conduct a case control study. Therefore we were nei- hygiene [27]. Proper environmental decontamination ther able to identify risk factors for acquisition of VRE may reduce the risk of VRE outbreaks in hospital set- nor to identify the source of infection. Furthermore, nei- tings as suggested in previous studies. Dancer et al. [28] ther retrospective data where patients were located suggest to focus more on patient close hand-touch sites within the ward at the time of admission nor informa- rather than on general surfaces and bathrooms. tion on staffing was available. A higher patient-staff ratio The observed higher median age of male VRE patients might have influenced the transmission risk. The only rather reflects the distribution of admitted patients than PFGE E strain from the patient could not be recovered being associated with VRE colonization or infection [29]. from the archived skim-milk stock and was hence also The pre-admission rectal screening implemented since not available for genotyping. the identification of the outbreak revealed less than one positive per hundred investigated patients. VRE screen- Conclusions ing in a tertiary hospital setting is suggested to decrease We conclude that enforcement of strict adherence to the the incidence in routine patient care and even more im- existing IPC protocol and assessment of adherence are es- portant in an outbreak situation [30–32]. Therefore we sential for controlling VRE outbreaks and reducing further speculate that most of the cluster cases acquired the transmission. We cannot exclude the role of other compo- VRE during the hospital stay. nents in the multi-modal IPC plan instituted which Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 8 of 9 ultimately may have played a role in the control of the out- 3. Ulrich N, Gastmeier P. Where is the difference between an epidemic and a high endemic level with respect to nosocomial infection control measures? break. Unheralded visits are useful tools to further improve An analysis based on the example of vancomycin-resistant enterococcus adherence to IPC protocols. Frequently touched surfaces faecium in hematology and oncology departments. GMS Hyg Infect such as patient charts are difficult to decontaminate and Control. 2017;12:Doc14. 4. Hayden MK, Blom DW, Lyle EA, Moore CG, Weinstein RA. Risk of hand therefore require particular attention. We conclude that this or glove contamination after contact with patients colonized with outbreak has resulted in better control of future VRE out- vancomycin-resistant enterococcus or the colonized patients’ breaks. HCWs reported a better understanding for the need environment. Infect Control Hosp Epidemiol. 2008;29(2):149–54. 5. Brodrick HJ, Raven KE, Harrison EM, Blane B, Reuter S, Torok ME, et al. of rigorous adherence to control measures. We expect fur- Whole-genome sequencing reveals transmission of vancomycin-resistant ther sporadic cases in future. enterococcus faecium in a healthcare network. Genome Med. 2016;8(1):4. 6. Huang SS, Datta R, Platt R. Risk of acquiring antibiotic-resistant bacteria from Abbreviations prior room occupants. Arch Intern Med. 2006;166(18):1945–51. CI: Confidence interval; EU/EEA: European Union and European Economic 7. Stone SP, Cooper BS, Kibbler CC, Cookson BD, Roberts JA, Medley GF, et al. area; HCW: Health care worker; HH: Hand hygiene; ICT: Infection control The ORION statement: guidelines for transparent reporting of outbreak team; ICU: Intensive care unit; IPC: Infection prevention and control; reports and intervention studies of nosocomial infection. 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Breakpoint tables for interpretation of MICs and zone from the corresponding author on reasonable request. diameters. Version 6.0, 2016. 11. Biomerieux. Gebrauchsfertige Teststreifen zur direkten Bestimmung der Authors’ contributions minimalen Hemmkonzentration [cited 2018 21 June]. Available from: http:// SE provided patient data regarding disease and transplant and reviewed the www.biomerieux.de/klinische-diagnostik/etestr. draft manuscript, MB and LK analyzed the patient samples and the 12. Galvin S, Dolan A, Cahill O, Daniels S, Humphreys H. Microbial monitoring of antimicrobial susceptibility testing, SF and WP conducted the molecular the hospital environment: why and how? J Hosp Infect. 2012;82(3):143–51. examinations. AM and GH conducted and analyzed the environmental 13. Wille I, Mayr A, Kreidl P, Bruhwasser C, Hinterberger G, Fritz A, et al. 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Surveillance of antimicrobial resistance in Europe, 2016 2017 [cited 24. Teng SO, Lee WS, Ou TY, Hsieh YC, Lee WC, Lin YC. Bacterial contamination of 2018 13 Mar]. Available from: https://ecdc.europa.eu/en/publications-data/ patients’ medical charts in a surgical ward and the intensive care unit: impact antimicrobial-resistance-surveillance-europe-2016. on nosocomial infections. J Microbiol Immunol Infect. 2009;42(1):86–91. Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 9 of 9 25. Russotto V, Cortegiani A, Raineri SM, Giarratano A. Bacterial contamination of inanimate surfaces and equipment in the intensive care unit. J Intensive Care. 2015;3:54. 26. Ulrich N, Vonberg RP, Gastmeier P. Outbreaks caused by vancomycin- resistant enterococcus faecium in hematology and oncology departments: a systematic review. Heliyon. 2017;3(12):e00473. 27. Hayden MK, Bonten MJ, Blom DW, Lyle EA, van de Vijver DA, Weinstein RA. Reduction in acquisition of vancomycin-resistant enterococcus after enforcement of routine environmental cleaning measures. Clin Infect Dis. 2006;42(11):1552–60. 28. Dancer SJ. The role of environmental cleaning in the control of hospital- acquired infection. J Hosp Infect. 2009;73(4):378–85. 29. Schold JD, Buccini LD, Goldfarb DA, Flechner SM, Hsich E, Mason D, et al. Patient participation in research among solid organ transplant recipients in the United States. Transplantation. 2011;91(12):1424–35. 30. Escaut L, Bouam S, Frank-Soltysiak M, Rudant E, Saliba F, Kassis N, et al. Eradication of an outbreak of vancomycin-resistant enterococcus (VRE): the cost of a failure in the systematic screening. Antimicrob Resist Infect Control. 2013;2(1):18. 31. Humphreys H. Controlling the spread of vancomycin-resistant enterococci. Is active screening worthwhile? J Hosp Infect. 2014;88(4):191–8. 32. Popiel KY, Miller MA. Evaluation of vancomycin-resistant enterococci (VRE)- associated morbidity following relaxation of VRE screening and isolation precautions in a tertiary care hospital. Infect Control Hosp Epidemiol. 2014; 35(7):818–25. 33. Banerjee T, Anupurba S. Prevalence of virulence factors and drug resistance in clinical isolates of enterococci: a study from North India. J Pathog 2015; 2015:692612. 34. Gaca AO, Gilmore MS. Killing of VRE enterococcus faecalis by commensal strains: evidence for evolution and accumulation of mobile elements in the absence of competition. Gut Microbes. 2016;7(1):90–6. 35. Hanczvikkel A, Toth A. Quantitative study about the role of environmental conditions in the survival capability of multidrug-resistant bacteria. J Infect Public Health. 2018; http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Antimicrobial Resistance and Infection Control Springer Journals

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Springer Journals
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Copyright © The Author(s). 2018
Subject
Biomedicine; Medical Microbiology; Drug Resistance; Infectious Diseases
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2047-2994
DOI
10.1186/s13756-018-0374-5
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Abstract

Background: Vancomycin resistant enterococci (VRE) are an emerging problem in health care settings. The purpose of the investigation was to assess the extent of the outbreak including environmental contamination and to limit further transmission. Methods: We used retrospective patient and laboratory data including pulse field gel electrophoresis (PFGE) typing and virulence and resistance gene analysis. For comparison of medians the Mann-Whitney and for comparison of proportions the Fisher exact tests were used. Results: PFGE typing of VRE strains of an outbreak of 15 VRE cases in a solid transplant unit revealed that nine of the cases belonged to one identical pattern (A), which was only found twice in the environment. Eleven further positive environmental samples showed a different, but identical PFGE pattern E. Only one patient was infected with this environmental strain. Two of nine (22.2%) PFGE A, but nine of eleven (81.2%) PFGE E samples were positive for gelatinase E (p = 0.01), which is described as enhancing biofilm production, suggesting a survival benefit for this strain on inanimate surfaces. Conclusion: Routine disinfection was not able to stop the cluster, but after repeated enforcement of the infection prevention and control (IPC) bundle such as training, strict adherence to hand hygiene and surface disinfection no further cases were observed. We conclude that certain VRE strains predominate in the environment whereas others predominate in humans. Enforcement of the IPC bundle is essential for controlling VRE outbreaks and reducing further transmission. Keywords: Solid organ transplant unit, Vancomycin resistant enterococci, Outbreak, Survival benefit, Infection control Background (EU/EEA). The proportion of VRE in Austria (4.3% in Vancomycin resistant enterococci (VRE) are important 2016) was below the EU population weighted mean of causes of morbidity and mortality especially in health 11.8% (95% confidence interval (CI) 11–13%) [2]. Mono- care settings where they easily disseminate [1]. Effective clonal and polyclonal outbreaks of VRE were described treatment is limited and thus VRE remain a major chal- worldwide; the largest reported outbreaks comprised up lenge for infection control. to 72 cases [3]. Vancomycin resistance of invasive Enterococcus fae- The most important transmission-routes of VRE are cium isolates ranges between 0 and 46.3% in countries still not fully understood, but cross contamination via of the European Union and European Economic Area the hands of health care workers’ (HCW) is believed to play a major role. HCW act as a vector between colo- nized or infected patients, inanimate surfaces and previ- * Correspondence: astrid.mayr@i-med.ac.at ously unaffected patients [4]. The reservoir for VRE is Department of Hygiene, Microbiology and Social Medicine, Division of believed to be the human intestine [5]. Hygiene and Medical Microbiology, Medical University of Innsbruck, Innsbruck, Schoepfstr. 41, 6020 Innsbruck, Austria Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 2 of 9 Known risk factors for acquisition of VRE include pre- four beds per room) and an adjacent intensive care unit vious use of antibiotics, prolonged hospital stay, under- (ICU) consisting of eight beds situated in three separate lying diseases, admission to high risk departments such rooms. Patients were transferred between the standard as oncology, hematology, transplant or intensive care care unit and the ICU depending on their medical con- units (ICU), the nurse to patient ratio, and occupancy to dition. The ICT consisted of one senior hospital hygiene a room where previously a patient harboring VRE was specialist and a local hygiene team. admitted [6]. The transmission in high risk wards via contaminated inanimate surfaces is believed to be im- Routine IPC protocol portant but it remains a challenge to quantify the attrib- The internal IPC protocol included the following recom- utable risk [6] of environmental contamination. mendations: 1) twice daily unsupervised routine disinfec- We describe an outbreak which was identified on 7th tion of inanimate surfaces of the patient close environment January 2017 after detection of five cases within 2 with an aldehyde-free-broad-spectrum disinfectant contain- months following the Orion statement [7]. ing quaternary ammonium compounds (QACs, 2% TPH The objective of this investigation was to assess the protect, Schülke & Mayr GmbH, Vienna, Austria) including extent of the outbreak including the environmental once daily patient charts, 2) terminal cleaning and disinfec- contamination, to limit further transmission and to tion of patient rooms with the above mentioned disinfect- evaluate the effectiveness of implemented control mea- ant and 3) hand hygiene (HH) based on the WHO sures. Further important objectives were to foster infec- approach “My Five Moments for Hand Hygiene” [8]using tion prevention and control (IPC) education by the alcohol-based detergents (Sterillium®, BODE Chemie infection control team (ICT) of the University Hospital GmbH, Hamburg, Germany). Surveillance of hand hygiene Innsbruck (LKI). compliance is conducted through bi-annual audits based on the protocol from the Robert Koch Institute [9], measur- Methods ing adherence to HH. The outcomes of the audits were cat- Study design egorized as sufficient or insufficient per unit but lacked a We used retrospective data analysis including PFGE typ- coding system to quantify the adherence to HH on an indi- ing, analysis of virulence and resistance genes and pa- vidual basis. Annual trainings of the IPC protocol through tient relevant data from the hospital records. verbal presentations and ward round sessions were rou- tinely conducted. Data on baseline IPC knowledge of HCW Participants were not routinely collected. IPC guidelines did not require Participants were patients admitted to the solid organ trans- pre-admission VRE screening of patients, unless 1) patients plant unit between 15th November 2016 and 30th June had a positive history of exposure in a high endemic coun- 2017 with laboratory confirmation of VRE. Colonization try, 2) were transferred from a long-term-care-facility or 3) was defined as laboratory confirmation of VRE in a sample were previously known having been infected or colonized of a patient from a non-sterile site without signs of infection with VRE. such as fever > = 38.5 °C. Infection was defined as laboratory According to the IPC protocol, each newly identified confirmation of VRE in a sample of a patient from a nor- patient either colonized or infected by VRE irrespective mally sterile site or signs of infection such as fever > = 38.5°. of the patient being part of an outbreak, triggered a rou- tine infection control response consisting of following Case definition measures: isolation precautions, defined as placement in We defined a VRE case as a patient admitted to the a single room, if possible, and, contact precautions de- transplant unit during the observation period with la- pending on the estimated potential for transmission in- boratory confirmation of VRE in at least one sample ir- cluding personal protective equipment. respective of the location or type of sampling. We defined a cluster case as a VRE case with the outbreak Intervention during the outbreak PFGE pattern A identified between December 2017 and During the outbreak the following additional measures June 2018 and admitted to the transplant unit. were implemented: Re-emphasizing strict adherence to HH and to environmental disinfection including un- Setting announced microbiological monitoring of the environ- The period of the outbreak lasted from 15 November ment and HCW’s hands, repeated sampling of stool or 2016 until 30 June 2017. rectal swabs of the VRE positive patients, newly admitted The LKI is a 1600-bed tertiary-care hospital with sev- patients and rectal screening of HCWs. Rectal swabbing eral departments including a solid organ transplant unit. of patients was implemented as precautionary measure The setting of the outbreak was the ward of the trans- to limit the extent of the outbreak. Self-administered plant unit consisting of 15 beds in seven rooms (one to rectal swabbing of HCWs was conducted on voluntary Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 3 of 9 basis upon the urgency of the situation. Thus informed Columbia agar containing 5% sheep blood (Becton, consent was not obtained. Dickenson and Company, Franklin Lakes, USA) for ap- Frequency of ward round training was increased. The proximately 5 seconds [14, 15]. Confirmation of VRE choice of HH antisepsis and environmental disinfection was conducted as described above. during the outbreak remained the same and compliance with HH was observed by the ICT. No additional decon- PFGE tamination procedures such as fogging or steaming were Molecular Typing was performed using pulse field gel implemented. electrophoresis (PFGE) according to the protocols pub- lished by the Centers for Disease Control and Prevention Culturing and typing [16]. Extracted bacterial DNA was restricted using Smal Patient samples enzyme. Strain typing was performed by manual PFGE We collected routine clinical samples and rectal screen- restriction pattern analysis [17] and by computational ing swabs from patients according to the IPC protocol analysis of band differences using GelJ Software Version (no informed consent was requested for rectal sam- 2[18]. Dendrogram analysis of PFGE patterns was per- pling), cultivated them on blood agar (Becton Dickinson, formed using Dice algorithm and Single Linkage cluster- Heidelberg, Germany) and selective ChromID VRE Agar ing. Genotypically related strains with similarity > 90% (Biomerieux, Marcy-l’Étoile, France) and incubated them were considered belonging to the same pattern. for 48 h at 37 °C under aerobic conditions. Suspect col- onies were identified by matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-- Genetic analysis TOF, Bruker, Bremen, Germany). Antibiotic susceptibility Vancomycin resistance genotypes were determined ac- testing was performed according to the European Com- cording to the protocol from Jayaratne et al. [19]. The mittee on Antimicrobial Susceptibility Testing (EUCAST enterococcal surface antigen was identified according to version 6.0, 2016) protocol [10]. Enterococci were classified the protocol by Toledo-Arana [20], the cytolysin activa- as VRE if the minimal inhibitory concentration of vanco- tor according to Vankerckhoven [21] and the gelatinase mycin was above 4 mg/L identified by E-Test (Biomerieux, E according to Hancock’s protocol [22]. Marcy-l’Étoile, France) [11]. Additional patient data such as diagnosis, duration of hospital stay, outcome, type and time of transplantation were obtained from the medical Infection related outcomes records of the LKI. Infection related outcomes, including colonization, in- fection and patient survival were assessed. Environmental samples The specimen processing and turn-around time were Unheralded sampling of environment was conducted ac- performed according to local laboratory protocol from cording to Galvins protocol (Galvin) using Columbia-III-Sheep blood agar 5% (Oxoid Limited, Basingstoke, UK) or Tryptic soy agar with neutralizers (VWR International, Radnor, USA) contact plates with a Sample size press on time of 10 seconds without any lateral move- The sample size was limited to the number of identified ment. Surfaces were selected at different locations close patients (n = 15). and distant from the respective patients [12] during three occasions: immediately after the alert of the cluster on 18 January, and twice after enforcement of control Statistical methods measures (30th January and 2nd February 2017, respect- Variables of interest were stored in excel database in- ively). Data recorded were date, type and location of cluding age, gender, number of isolates obtained includ- sampling, laboratory findings and PFGE results. Direct ing positives, date of available laboratory result, source unheralded observation of hygienic measures was con- and material of samples, length of hospital stay, previous ducted to identify potential gaps of adherence to infec- antibiotic treatment, previous confirmation of VRE in tion control measures. Patient close samples were any sample, diagnosis, other identified pathogens, and defined as samples obtained from the vicinity of patients patient outcome. such as the bedrail, bedframe, beside tables, clamps for Descriptive analysis was performed using Epi info ver- urine-bags, drug perfusors, stethoscope and bedside sion 7.2.2.2. (CDC Atlanta). For comparison of medians monitors [13]. the Mann-Whitney and for comparison of proportions Microbial monitoring of HCWs hands was performed the Fisher exact tests were used. A p-value of < 0.05 was by imprinting all fingertips including the thumb onto considered statistically significant. Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 4 of 9 Results additional patients (Fig. 1). Of these, ten patients (66.7%) Event description were males with a median age of 56.5 years (50– On 7th January 2017 the outbreak response team of the 71 years). The five female patients showed a median age LKI informed the transplant unit about a potential out- of 70 years (60–79 years) (p = 0.003) (Table 1). break of VRE. VRE was first isolated twice from blood cultures, five Analysis of historical data revealed that between May times from urine samples, four times from wound drainage 2012 and October 2016, a total of 53 VRE cases were and once each from a tissue, stool, and rectal swab and from identified at this unit. The median incidence was one a broncho-alveolar lavage sample. Three of the patients were (0–3) case per month and the annual median incidence classified as being colonized, the remaining twelve as being was 11 cases (6–16 cases) per year for the period 2013– infected with VRE. The median length of hospital stay was 2016. In comparison to previous years, the observed 24 days (10–112 days). All but one patient underwent trans- number of five VRE cases in a period of less than 2 plantation and received immunosuppression. Twelve pa- months clearly exceeded the expected value suggesting tients survived (80%) and three died (Table 1). In all patients an outbreak. Enterococcus faecium was identified, one patient harbored a tigecycline resistant, two a linezolid resistant and fourteen VRE cases teicoplanin resistant strains. After a period of 4 months without any detection of VRE from the transplant unit, the potential index case was confirmed on 15th November 2016. He was a PFGE patterns of cases 58 year old male suffering from IgA Nephritis who re- PFGE patterns were available for 13 of 15 patients (86.7%). ceived a kidney transplant on 12th November 2016, 3 Among those, five different PFGE patterns were identified days prior to the diagnosis of VRE in a single sample of and subsequently classified as patterns A to E. Nine of the a retroperitoneal surgical-site-drainage. The patient was thirteen cases (69.2%) were classified as PFGE pattern A classified as being infected. (further called cluster strain, Table 1,Fig. 2). Between 15th November 2016 and 30th June 2017, All 10 of the 15 patient isolates (66.7%) available for VRE was confirmed in at least one sample of 14 vancomycin resistance genotyping (vanR) revealed vanA, Fig. 1 Number of cases by PFGE pattern, week of diagnosis and main interventions (n = 15) Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 5 of 9 Table 1 Patient characteristics Categories N/total or median (mean; range) % Demographic characteristics Males 5/15 67 Age 59 yrs. (61.3 yrs.; 50–79 yrs) – Clinical findings Infected (versus colonized) 12/15 80 Deceased 3/15 20 Laboratory sampling Number of samples investigated per patient 24 (31; 8–105) – Number of positive samples per patient 2 (6.1; 1–52) – Laboratory findings PFGE pattern A (cluster strain) 9/13 69 PFGE pattern E (environmental strain) 1/13 8 other PFGE patterns 3/13 (one each) 23 irrespective of their PFGE pattern. The only patient iso- once on a patients chart after the first enforcement of late with pattern E, was not viable. control measures. All other eleven VRE positive environ- mental samples revealed one identical PFGE pattern E Cluster cases which was distinct from the patient cluster strain (Fig. 2). In total, 194 patient samples were obtained from cluster Pattern E was confirmed only in one patient, who was ad- cases, in 26 of them (13.4%) VRE was confirmed. The mitted 2 days prior to the first environmental sampling. median number of samples investigated per cluster case Eight of these positive non-cluster strains (PFGE E) were was 20 (12–34) and the median number of positive sam- identified during the first on-site visit. Six of them were ples was one (1–12). Five patients only had one sample determined in the patient close environment and two out- positive for VRE. The median duration of confirmation side patient rooms. During the third visit the environmen- between the first and the last positive sample was 4 days tal PFGE E strain was identified again three times. Once (1–33 days). The median interval between admission and from the patient close environment (urine clamp bag) of first isolation of VRE was 13 days (same day-22 days) the patient infected with PFGE E; and twice from a bed lo- (n = 14). One additional patient already tested positive cated in the corridor (Fig. 3). All tested environmental in another unit during the outbreak period, but the iso- strains were vanApositive. late was different from the cluster strain (PFGE C). One VRE positive hand sample of a HCW was not From all other cases no information of previous VRE available for PFGE typing. carriage was available as no routine VRE screening was conducted prior to this outbreak. VRE was first Virulence genes identified in following materials from the nine cluster Twenty three samples were available for virulence gene cases: Blood (n =1), (wound) drains (n = 4), rectal swab testing (13 environmental and 10 patient samples). (n =1), and urine (n =3). Two of nine (22.2%) PFGE A (six patient samples), but nine of 11 (81.2%) PFGE E (all environmental samples) VRE screening were positive for gelatinase E (p = 0.0123). The two gela- Pre-admission rectal screening was implemented after tinase E positive PFGE A samples were one human sam- the outbreak alert. Among 169 patients screened until ple from a patient already discharged at the time of the the end of 2017, only one was found to be VRE positive environmental sampling and one environmental sample (0.6%). from a urinary bag clamp obtained during the first on-site visit which could not be linked to a specific Environmental and hand samples patient. A total of 139 hand (n = 26; 18.7%) and environmental All investigated samples were positive for enterococcal (n = 113, 81.3%) samples were obtained during three un- surface protein and negative for cytolysin activator. heralded on-site visits; nearly half of them (n = 68, 48.9%) were obtained prior to the first enforcement of Control measures control measures. More samples taken prior to en- The first of the three unheralded on-site visit including hanced disinfection (n = 10; 14.7%) were positive for environmental and hand sampling was undertaken on VRE compared to post disinfection sampling (n =4; 18th January 2017. Lack of adherence to hand hygiene 5.6%) (p = 0.07). Among the thirteen VRE positive envir- was observed and therefore enforcement of control mea- onmental samples the cluster strain (PFGE A) was iden- sures was stressed by the infection control hygiene team. tified twice: once from a clamp of a urine-bag prior and At the time of this first visit, five patients were admitted Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 6 of 9 participation was voluntary. In the current IPC protocol HCW hand sampling but no rectal swabbing is included. During the last on-site visit on 2nd February, VRE was detected in four of 47 (8.51%) environmental samples. Three of those revealed PFGE E, all from patient-close sites of the patient infected with PFGE E, the cluster strain (PFGE A) was isolated from a patient chart. At the time of the third visit, five patients (two with PFGE A) were still admitted to the ward; four further cases, two with the cluster PFGE A were identified later. En- forcement of IPC measures was rigorously stressed again and four ward round sessions were conducted. Insuffi- cient adherence to HH according to the IPC protocol was documented during the first visit. During the second and third visit the adherence to HH was evaluated to be sufficient. The terminal cleaning was audited by the ICT and adherence was defined as sufficient already at the first visit. The effect of teaching was not measured. Discussion We describe an outbreak of fifteen VRE cases in a solid organ transplant unit in late 2016 and early 2017, of which nine patients revealed an identical PFGE pattern A, further called the cluster strain. During the first visit six VRE positive environmental samples were identified in the patient close environment which suggests lack of effective decontamination despite the audited terminal disinfection which was considered sufficient. Additionally, lack of adherence to strict hand hygiene was observed and compliance to HH was classi- fied as insufficient. The two positive samples identified from a laundry rack suggest cross-contamination via HCW hands, as all patients were immobile. The fact, that the majority of environmental strains were identical - although distinct from the outbreak strain - may sug- gest that also prior to the first sampling environmental contamination via HCW hands may have occurred. HH adherence during audits improved from insufficient dur- Fig. 2 Dendrogram of PFGE patterns of human (n = 13; pattern A = 9, ing the first visit to sufficient during the second and one each pattern B, C, D, E and environmental VRE strains (n =13; third visit. pattern E = 11, pattern A = 2) including 3 control strains Enforcement of ICP measures resulted in a decrease of the proportion of VRE contaminated environmental sam- ples, although it was not significant (Fig. 3). Nevertheless, (two with PFGE A, one each with PFGE B and E and reconfirmation of the non-cluster strain during the third one without a viable isolate) and six already discharged site visit may be due to recontamination and insufficient (five of whom with PFGE A and one with PFGE C). compliance to hand hygiene. In addition, the confirmation The second sampling on 30th January, performed after of the cluster strain on a patient chart after enforcement extended cleaning and disinfection procedures towards of control measures suggests the cross-contamination via patients’ distant zones did not detect any environmental HCW hands as well as ineffective decontamination of the contamination. Rectal screening targeting all staff was patient chart. Decontamination of patient charts is de- conducted the same day. The participation rate was 79% (94 scribed as effective measure to decrease horizontal trans- of 119), all samples remained negative. Non-participation fer of organisms and to prevent transmission of health was mainly due to absence; No consent was obtained as care associated infections [23, 24]. Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 7 of 9 Fig. 3 Number and results of hand and environmental samples by intervention (n = 139) We speculate that the lack of strict adherence to ad- The cluster strain PFGE A was identified only twice in equate hand hygiene might have led to contamination of the environment; all other environmental strains re- the environment. This is supported by the facts that firstly, vealed an identical PFGE E pattern. This PFGE E pattern contamination was observed in patient distant areas such was found only in one patient. The fact, that significantly as laundry racks and secondly, that contaminated patient more PFGE E compared to PFGE A strains were produ- charts are described being a result of lack of adherence to cing gelatinase E, which is described as enhancing bio- recommended HH [25]. This may have played an import- film production, suggests a survival benefit on inanimate ant role in triggering the outbreak. Tight working spaces in surfaces [33]. Accumulation of mobile genetic elements the ICU unit favor the patient-to-patient contact [26]and including plasmids, pathogenicity islands, resistance mayhaveresultedinahigher risk fortransmissionofVRE. transposons other fitness islands, phages and surface Hayden concludes that the role of environmental con- types [34, 35] may also have contributed to better sur- tamination in nosocomial cross-transmission of VRE is vival in the environment. still unresolved but enforcement of environmental de- The limitations of our study are that we used retro- contamination was both associated with reduction of spective data analysis which made selection of appropri- surface contamination and contamination of HCWs’ ate controls difficult. Also logistical reasons hindered us hands despite only moderate adherence to proper hand to conduct a case control study. Therefore we were nei- hygiene [27]. Proper environmental decontamination ther able to identify risk factors for acquisition of VRE may reduce the risk of VRE outbreaks in hospital set- nor to identify the source of infection. Furthermore, nei- tings as suggested in previous studies. Dancer et al. [28] ther retrospective data where patients were located suggest to focus more on patient close hand-touch sites within the ward at the time of admission nor informa- rather than on general surfaces and bathrooms. tion on staffing was available. A higher patient-staff ratio The observed higher median age of male VRE patients might have influenced the transmission risk. The only rather reflects the distribution of admitted patients than PFGE E strain from the patient could not be recovered being associated with VRE colonization or infection [29]. from the archived skim-milk stock and was hence also The pre-admission rectal screening implemented since not available for genotyping. the identification of the outbreak revealed less than one positive per hundred investigated patients. VRE screen- Conclusions ing in a tertiary hospital setting is suggested to decrease We conclude that enforcement of strict adherence to the the incidence in routine patient care and even more im- existing IPC protocol and assessment of adherence are es- portant in an outbreak situation [30–32]. Therefore we sential for controlling VRE outbreaks and reducing further speculate that most of the cluster cases acquired the transmission. We cannot exclude the role of other compo- VRE during the hospital stay. nents in the multi-modal IPC plan instituted which Kreidl et al. Antimicrobial Resistance and Infection Control (2018) 7:86 Page 8 of 9 ultimately may have played a role in the control of the out- 3. Ulrich N, Gastmeier P. Where is the difference between an epidemic and a high endemic level with respect to nosocomial infection control measures? break. Unheralded visits are useful tools to further improve An analysis based on the example of vancomycin-resistant enterococcus adherence to IPC protocols. Frequently touched surfaces faecium in hematology and oncology departments. GMS Hyg Infect such as patient charts are difficult to decontaminate and Control. 2017;12:Doc14. 4. Hayden MK, Blom DW, Lyle EA, Moore CG, Weinstein RA. Risk of hand therefore require particular attention. We conclude that this or glove contamination after contact with patients colonized with outbreak has resulted in better control of future VRE out- vancomycin-resistant enterococcus or the colonized patients’ breaks. HCWs reported a better understanding for the need environment. Infect Control Hosp Epidemiol. 2008;29(2):149–54. 5. Brodrick HJ, Raven KE, Harrison EM, Blane B, Reuter S, Torok ME, et al. of rigorous adherence to control measures. We expect fur- Whole-genome sequencing reveals transmission of vancomycin-resistant ther sporadic cases in future. enterococcus faecium in a healthcare network. Genome Med. 2016;8(1):4. 6. Huang SS, Datta R, Platt R. Risk of acquiring antibiotic-resistant bacteria from Abbreviations prior room occupants. Arch Intern Med. 2006;166(18):1945–51. CI: Confidence interval; EU/EEA: European Union and European Economic 7. Stone SP, Cooper BS, Kibbler CC, Cookson BD, Roberts JA, Medley GF, et al. area; HCW: Health care worker; HH: Hand hygiene; ICT: Infection control The ORION statement: guidelines for transparent reporting of outbreak team; ICU: Intensive care unit; IPC: Infection prevention and control; reports and intervention studies of nosocomial infection. J Antimicrob LKI: University Hospital Innsbruck (Landeskrankenhaus Innsbruck); PFGE: Pulse Chemother. 2007;59(5):833–40. filed gel electrophoresis; VRE: Vancomycin resistant enterococci 8. Organization WH. WHO Guidelines on Hand Hygiene in Health Care: First Global Patient Safety Challenge Clean Care is Safer Care 2009 [cited 2018 21 Acknowledgements June]. Available from: http://apps.who.int/iris/bitstream/handle/10665/ The authors want to thank the staff of the unit and laboratory and the ICT 44102/9789241597906_eng.pdf;jsessionid= for the good and transparent collaboration. 0353CC69A96F2B5A26F019487149B213?sequence=1. 9. Robert Koch Institute NRfSvnI. Hand-KISS 2017 [cited 2018 21 June]. Availability of data and materials Available from: http://www.nrz-hygiene.de/surveillance/kiss/hand-kiss/. The datasets used and/or analyzed during the current study are available 10. Testing TECoAS. Breakpoint tables for interpretation of MICs and zone from the corresponding author on reasonable request. diameters. Version 6.0, 2016. 11. Biomerieux. Gebrauchsfertige Teststreifen zur direkten Bestimmung der Authors’ contributions minimalen Hemmkonzentration [cited 2018 21 June]. Available from: http:// SE provided patient data regarding disease and transplant and reviewed the www.biomerieux.de/klinische-diagnostik/etestr. draft manuscript, MB and LK analyzed the patient samples and the 12. Galvin S, Dolan A, Cahill O, Daniels S, Humphreys H. Microbial monitoring of antimicrobial susceptibility testing, SF and WP conducted the molecular the hospital environment: why and how? J Hosp Infect. 2012;82(3):143–51. examinations. AM and GH conducted and analyzed the environmental 13. Wille I, Mayr A, Kreidl P, Bruhwasser C, Hinterberger G, Fritz A, et al. Cross- sampling, AO, CLF and DO reviewed the manuscript, PK analyzed and sectional point prevalence survey to study the environmental interpreted the data and drafted the manuscript. All authors read and contamination of nosocomial pathogens in intensive care units under real- approved the final manuscript. life conditions. J Hosp Infect. 2018;98(1):90–5. 14. Bruhwasser C, Hinterberger G, Mutschlechner W, Kaltseis J, Lass-Florl C, Mayr Ethics approval and consent to participate A. A point prevalence survey on hand hygiene, with a special focus on The Ethics Committee of the Medical University of Innsbruck confirms that Candida species. Am J Infect Control. 2016;44(1):71–3. for retrospective observational studies no ethics committee approval is 15. Creamer E, Dorrian S, Dolan A, Sherlock O, Fitzgerald-Hughes D, Thomas T, required by Austrian law. et al. When are the hands of healthcare workers positive for methicillin- resistant Staphylococcus aureus? J Hosp Infect. 2010;75(2):107–11. 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Journal

Antimicrobial Resistance and Infection ControlSpringer Journals

Published: Jul 18, 2018

Keywords: Solid organ transplant unit; Vancomycin resistant enterococci; Outbreak; Survival benefit; Infection control

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