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Background Methicillin resistant Staphylococcus aureus (MRSA) is a major burden for hospitals globally. However, in the Netherlands, the MRSA prevalence is relatively low due to the ‘search and destroy’ policy. Routine multiple‑locus variable‑number of tandem repeat analysis (MLVA) of MRSA isolates supports outbreak detection. However, whole genome multiple locus sequence typing (wgMLST ) is superior to MLVA in identifying (pseudo‑)outbreaks with MRSA. The present study describes a pseudo‑ outbreak of MRSA at the bacteriology laboratory of a large Dutch teaching hospital. Methods All staff members of the bacteriology laboratory of the Elisabeth‑ TweeSteden hospital were screened for MRSA carriage, after a laboratory contamination with MRSA was suspected. Clonal relatedness between the index isolate and the MRSA isolates from laboratory staff members and all previous MRSA isolates from the Elisabeth‑ Twe‑ eSteden hospital with the same MLVA‑type as the index case was examined based on wgMLST using whole genome sequencing. Results One of the staff members was identified as the probable source of the laboratory contamination, because of carriage of a MRSA possessing the same MLVA‑type as the index case. Eleven other isolates with the same molecular characteristics were found in the database, of which seven were retrospectively suspected of contamination. Clonal relatedness was found between ten isolates, including the isolate found in the staff member and the MRSA found in the index patient with a maximum of eleven alleles difference. All isolates were epidemiologically linked through the laboratory staff member, who had worked on all these cultures. Conclusions The present study describes a MRSA pseudo‑ outbreak over a 2.5‑ year period due to laboratory contam‑ ination caused by a MRSA carrying laboratory staff member involving nine patients. In case of unexpected bacterio ‑ logical findings, the possibility of a laboratory contamination should be considered. Keywords MRSA, Pseudo‑ outbreak, Contamination, wgMLST *Correspondence: Present Address: Reinier de Graaf Hospital, Delft, The Netherlands Karlijn M. G. Houkes firstname.lastname@example.org Microvida, Laboratory of Medical Microbiology and Immunology, Elisabeth‑ TweeSteden Hospital, Tilburg, The Netherlands Department of Infection Prevention, Amphia Hospital, Breda, The Netherlands Department of Infection Prevention, Elisabeth‑ TweeSteden Hospital, Tilburg, the Netherlands © The Author(s) 2023. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Houkes et al. Antimicrobial Resistance & Infection Control (2023) 12:1 Page 2 of 7 abroad, professional contact with livestock, intensive Introduction contact with a MRSA carrier or a stay in a refugee center Staphylococcus aureus is a major human pathogen and an in the last two months . In case of a high or interme- important cause of nosocomial and community-acquired diate risk, swabs are taken to test for MRSA carriage . infections . Since the 1960s, methicillin resistant S. This screening is part of the ‘search and destroy’ policy aureus (MRSA) strains have emerged. These strains har - in the Netherlands and is followed by strict isolation and bor a mecA gene making them resistant to almost all treatment of MRSA carriers [11, 12]. β-lactam antibiotics [2, 3]. In the Netherlands, the preva- lence of MRSA carriage is low, ranging from 0.03% to Routine microbiology methods regarding MRSA 0.17% . Despite this low MRSA prevalence in the Neth- For MRSA carriage screening swabs of the anterior erlands, nosocomial outbreaks do occur . To detect the nares, throat, perineum and, if present, catheters, source and route of transmission in hospital outbreaks, drains and cutaneous lesions were collected using epidemiological investigation can be combined with eSwab medium (Copan, Murrieta, USA) . The swabs molecular typing of the bacterial isolates. Molecular typ- were inoculated on a chromogenic MRSA2 Brilliance ing of S. aureus can be done using Staphylococcal protein agar (Oxoid Ltd., Basingstoke, UK), on which MRSA A (spa) typing, pulsed-field gel electrophoresis, multiple isolates appear as blue colonies after overnight incuba- loci variable number tandem repeat analysis (MLVA), or tion at 35 ± 1 °C, and on a blood agar plate as growth whole genome multi-locus sequence typing (wgMLST) control. The remaining eSwab medium was added to . The latter has the highest discriminatory power due Mueller Hinton Broth (BD Diagnostics, Sparks, USA) to the many alleles included in the analysis to identify or supplemented with 6.5% sodium chloride. After over- dismiss clonal relatedness. night incubation at 35 ± 1 °C, the broth was inoculated In March 2019, an unexpected MRSA finding in a on a chromogenic MRSA2 Brilliance agar. Species patient led to the suspicion of a laboratory contamina- determination of presumptive MRSA colonies was tion. This patient had a S. aureus infection of a prosthetic performed by matrix-assisted laser desorption/ioniza- joint of the knee. The infection was diagnosed based on tion time-of-flight (MALDI-TOF) mass spectrometry methicillin sensitive S. aureus (MSSA) in five of eight tis - (Bruker Daltonics, Leipzig Germany). Antibiotic sus- sue cultures of the knee. Unexpectedly, MRSA colonies ceptibility testing was performed of S. aureus isolates were found in one of the eight cultures. To verify this using either BD Phoenix 100 system (BD Diagnostics, finding, all original tissue samples were cultured again Sparks, USA) or disc diffusion (BD Diagnostics, Sparks, and swabs originating from the patient’s anterior nares, USA) according to EUCAST . An in-house real- throat and perineum were cultured to test for MRSA time PCR was performed on isolates with a cefoxitin carriage. In none of these cultures, MRSA was found, MIC values > 4 mg/L or cefoxitin (30 μg) disc diffusion suggesting that the previously cultured MRSA was a diameter < 22 mm to confirm the MRSA identifica - laboratory contamination rather than an actual MRSA tion, detecting the Sa442 DNA fragment , S. aureus infection. For this reason, contact investigation was not nuclease (nuc) , Panton-Valentine leukocidine performed for the patient’s contacts and infection con- (PVL) , and methicillin resistance genes MecA and trol measures were lifted. Multiple studies have described MecC [17, 18]. Additionally, in selected samples (e.g., in laboratory contamination of clinical specimens though case of limited patient isolation capacity) direct molec- various causes [8–10]. The objective of the present study ular screening for MRSA presence can be performed was to determine the source and the extent of this MRSA using the Xpert MRSA NxG detection kit (Cepheid, contamination. Whole genome multiple locus sequence Sunnyvale, USA). For each patient where MRSA was typing (wgMLST) was performed to identify a pseudo- cultured, the isolate was sent to the National Institute outbreak of MRSA due to laboratory contamination. for Public Health and the Environment (RIVM) for fur- ther genotyping by MLVA as described by Schouls et al. Methods . Setting and routine microbiology methods regarding MRSA Setting Source and extent of laboratory contamination The Elisabeth-TweeSteden hospital, Tilburg, the Neth - Source of laboratory contamination erlands is a teaching hospital with 796 beds. Around Laboratory staff members were screened for MRSA car - 85 new cases of MRSA carriage or infection are identi- riage by sampling of the anterior nares, throat and peri- fied each year. Upon hospital admission, all patients are neum. These samples were cultured as described above. screened for risk factors for MRSA carriage using a ques- tionnaire. Such risk factors are recent hospital admission Houkes et al. Antimicrobial Resistance & Infection Control (2023) 12:1 Page 3 of 7 Extend of laboratory contamination Technician 2, who worked on all these cultures. Msta04, The laboratory data system was searched for all MRSA Msta05, Msta07, and Msta08 were not suspect for labo- isolates cultured in the Elisabeth-TweeSteden hospital ratory contamination, since these isolates were found in from January 2008 until May 2019 with the same MLVA- multiple samples (Table 1). There was no sufficient data type as the index MRSA isolate. For each of the detected to determine the likelihood of contamination of Msta12. MRSA isolates with an identical MLVA-type, the likeli- There is an epidemiological relationship between the hood of (laboratory) contamination (likely or unlikely) patient C and E since patient E is the partner of patient C. was determined. Contamination with a MRSA isolate No epidemiological link was detected between any of the was deemed likely if the MRSA isolate was only cultured other patients. once and not in any other sample of the same patient. Whole genome sequencing and wgMLST Whole genome sequencing (WGS) and wgMLST Whole genome sequence data was generated for all iso- The MRSA index isolate, the MRSA isolates from the lab - lates described in Table 1 and the ATCC43300 reference oratory staff members, the MRSA isolates detected in the strain. All assembled genomes met the quality criteria laboratory data system and the control strain ATCC43300 (Additional file 1: Table S1). WgMLST revealed two clus- were selected for WGS. WGS was performed using Nex- ters (Fig. 1). The cluster indicated in red in Fig. 1 consists tera XT chemistry on a Miseq sequencer (Illumina, San of Msta03, detected in technician 2, Msta01, Msta05, Diego, CA, USA). After error-correction and de novo Msta06, Msta07, Msta09, Msta10, Msta11, Msta13 genome assembly on CLC genomics workbench 20.0.4 and Msta14. The number of alleles difference between (Qiagen, Germantown, MD, USA), the number of allelic these 10 isolates ranged from 0 to 11 alleles, indicating differences between the MRSA isolates was determined that they belong to the same genetic cluster (Additional using the wgMLST tools of Ridom SeqSphere + ver- file 2: Table S2). Within this cluster, 8 isolates (Msta01, sion 7.7.5 (Ridom GmbH, Munich, Germany). A total of Msta03, Msta06, Msta09, Msta10, Msta11, Msta13 and 2574 alleles were included in the pairwise comparison, Msta14) were suspected of laboratory contamination. in which missing values were ignored. For data visuali- However, Msta05 and Msta07 were not suspected of zation, a neighbor-joining tree was created. A maximum laboratory contamination. The timeline of the identified allelic difference of 24 alleles was used to identify clusters pseudo-outbreak cluster revealed that, chronologically, . the outbreak starts with Msta05 (Fig. 2). The second clus - ter is indicated in blue in Fig. 1 and consists of Msta04, Results Msta08 and Msta12 with a difference ranging from 16 to Source of laboratory contamination 19 alleles (Additional file 2: Table S2). None of these iso- All 23 laboratory staff members working in the bacte - lates was suspected of laboratory contamination and epi- riology department were screened for MRSA carriage. demiological links were absent in this cluster. The isolates Three cultures from two staff members were positive for in the second cluster differed at least 275 alleles from the MRSA. Strain Msta02 was cultured from the perineum of first identified cluster containing both Msta01 (index iso - technician 1 and belonged to the MLVA type MT0398- late) and Msta03 found in technician 2. MC0398. Strain Msta03 was cultured from the anterior nares and throat of technician 2 and belonged to MLVA- Discussion type MT0489-MC0022, identical to the MLVA-type of This report describes a MRSA pseudo-outbreak due to the index MRSA isolate Msta01 (Table 1). a laboratory contamination by a MRSA carrying labora- tory staff member involving nine patients over a period Extent of laboratory contamination of 2.5 years. The pseudo-outbreak cluster was identi - Between January 2008 and May 2019, MLVA-typing was fied by wgMLST and had a maximum allelic difference performed on 1037 MRSA isolates. Among those, 12 of 11 alleles. A previous wgMLST cluster analysis study isolates belonged to the MLVA-type MT0489-MC0022 found a relatedness threshold of < 24 alleles for S. aureus (including Msta01) and carried a MecA gene. All 12 iso- . However, all difference > 5 alleles should be inter- lates were found between November 2016 and March preted with caution and in relation to the presence or 2019 (Table 1) (Fig. 2). Seven of the twelve isolates were absence of an epidemiological link . Moreover, the suspect for contamination based on the selection criteria determination of the relatedness threshold of wgMLST (MRSA detected in only 1 sample), namely Msta01 (index is complicated by the evolution rate of active growing patient), Msta06, Msta09, Msta10, Msta11, Msta13, of isolates, which is 1 mutation per 6 weeks in the case and Msta14 (Table 1). All these isolates were epidemio- of MRSA . In the present study, two clusters were logically linked through the laboratory staff member identified. One is the pseudo-outbreak cluster in which Houkes et al. Antimicrobial Resistance & Infection Control (2023) 12:1 Page 4 of 7 ‑ ‑ ‑ ‑ ‑ ‑ ‑ ‑ ‑ ‑ ‑ ‑ ‑ ‑ Table 1 Data of all MRSA isolates found in the Elisabeth TweeSteden hospital laboratory belonging to MLVA type MT0489MC0022 from 2008mid 2019 and the MRSA isolates found by screening the technicians Isolate ID Patient/ Sampling date Material Clinical Carriage screening Direct PCR Subsequent Risk factors for Suspect of MLVA type Technician MRSA cultures of sample screening MRSA carriage contamination infection culture Nose Throat Perineum Msta01 Patient A (index) Mar 2019 Synovial fluid / No – – – ‑ N/P None Yes MT0489MC0022 tissue knee Msta02 Technician 1 May 2019 Perineum No – – + N/P + None N/A MT0489MC0022 Msta03 Technician 2 May 2019 Nose, throat No + + – N/P + None N/A MT0398MC0398 Msta04 Patient B Nov 2016 Nose No + – – + + Hospital abroad No MT0489MC0022 Msta05 Patient C Jan 2017 Wound swab Yes + + + N/P + None No MT0489MC0022 Msta06 Patient D Apr 2017 Throat No – + – – – Hospital abroad Yes MT0489MC0022 Msta07 Patient E May 2017 Skin swab Yes + + + N/P – Partner of patient No MT0489MC0022 Msta08 Patient F Aug 2017 Throat No N/P + + N/P – Roommate MRSA No MT0489MC0022 positive Msta09 Patient G Sept 2017 Nose No + – – N/P – Unknown Yes MT0489MC0022 Msta10 Patient H Oct 2017 Perineum No – – + N/P – Contact MRSA Yes MT0489MC0022 positive person Msta11 Patient I Dec 2017 CAPD dialysate No – – – N/P N/P None Yes MT0489MC0022 Msta12 Patient J Mar 2018 Skin swab No N/P N/P N/P N/P N/P None ND MT0489MC0022 Msta13 Patient K Apr 2018 Ascites No – – – N/P – None Yes MT0489MC0022 Msta14 Patient L Feb 2019 Perineum No – – + – – None Yes MT0489MC0022 CAPD continue ambulante peritoneaal dialyse; ND not determined; N/P not performed; N/A not applicable Houkes et al. Antimicrobial Resistance & Infection Control (2023) 12:1 Page 5 of 7 Fig. 1 Neighbor‑joining tree of MRSA isolates based on wgMLST. The horizontal distance corresponds to the absolute number of allelic differences between isolates. Details of the isolates are depicted in Table 1. The pseudo‑ outbreak cluster is indicated in red with a maximum allelic difference of 11 alleles. The isolates in blue do have the same MLVA characteristics, but form a separate cluster. Green indicates the MRSA isolates with other MLVA characteristics, including control strain ATCC43300. The number of allelic differences (or range) between clusters are indicated in black and within clusters in red or blue corresponding to the cluster color Fig. 2 Timeline of the pseudo‑ outbreak cluster due to laboratory contamination. The MRSA isolates belonging to the cluster are indicated with a diamond shape on the point in time when the isolate was first cultured. The MRSA isolate found in the staff member with the same MLVA type is indicated in red the most divergent samples within the cluster were iso- that all nine MRSA isolates do belong to the pseudo-out- lated 17 months apart, which could explain the increased break. The other cluster consisting of three MRSA iso - number of allelic differences. The two isolates isolated in lates without an epidemiological link, are not part of an the last three months of the pseudo-outbreak differ only (pseudo-)outbreak based on this analysis. Although these 1 allele from the isolate found in the staff member. Fur - isolates had the same MLVA-typing, based on wgMLST thermore, all isolates in this cluster had an epidemiologi- these three isolates were clearly distinct from the isolates cal link through the MRSA carrying staff member. Based belonging to the pseudo-outbreak cluster. This illustrates on wgMLST and their epidemiological link, it is likely the added value of wgMLST compared to MLVA-typing. Houkes et al. Antimicrobial Resistance & Infection Control (2023) 12:1 Page 6 of 7 Chronologically, the first isolate of the pseudo-out - Conclusion break cluster was not suspected of contamination, since A pseudo-outbreak of MRSA was identified involving nine the MRSA carriage in this patient was confirmed by mul - patients caused by MRSA carriage of a laboratory staff tiple cultures making laboratory contamination highly member who contaminated clinical specimens. Clonal unlikely. The laboratory staff member may have been relatedness between the samples suspected of contamina- infected with Msta03 during culturing of Msta05 in Janu- tion could be confirmed by wgMLST, showing the added ary 2017. It is only after January 2017 that we observed value over MLVA-typing. This pseudo-outbreak empha - an increase of MRSA isolates in the Elisabeth-TweeSt- sizes the importance of critical and continuous evaluation eden hospital with MLVA MT0489-MC0022. The only of microbiology laboratory procedures to minimize the MRSA isolate with the same MLVA-type isolated before possibility of laboratory contamination and to maximize 2017 (Msta04) did not belong to the same cluster accord- early detection of false-positive culture results. ing to the WgMLST analysis. The MRSA carrying staff member had no risk factors for MRSA carriage. Although Supplementary Information we have no definite proof, it seems most likely that the The online version contains supplementary material available at https:// doi. org/ 10. 1186/ s13756‑ 022‑ 01207‑7. laboratory staff member was infected during laboratory activities. Infections acquired during laboratory work Additional file 1. Supplementary table 1. Quality control values of with various other bacteria have been described, but whole genome sequencing. MRSA is not recognized as a pathogen that presents a Additional file 2. Supplementary table 2. Distance matrix of the risk of laboratory infection . An increased incidence wgMLST analysis of the MRSA strains from the laboratory database with MLVA type complex MC0022, MLVA type MT0489 and MLVA profile 18‑05‑ for Staphylococcus aureus carriage was found in a Dutch 03‑01‑01‑13‑01‑05 and the two medical microbiology technicians tested cross-sectional study among laboratory staff members, positive for MRSA in the pseudo‑ outbreak investigation. The colors of the but observed a MRSA prevalence comparable to that of isolate IDs and the colored absolute number of allelic differences cor ‑ respond to the cluster they belong to as depicted in Figure 1. the general population . In the present study, two of the 23 laboratory staff members working at the bacteri - ology department were MRSA carriers (8.9%) (unrelated Acknowledgements We acknowledge the contribution of the laboratory staff members of the strains). This is more than could be expected based on bacteriology department of the Elisabeth‑ TweeSteden hospital. We would also the general Dutch population where the MRSA preva- like to acknowledge the contribution of the Microvida sequencing team for lence is < 1% [4, 12]. However, more research is needed to performing the whole genome sequencing. determine whether there is an increased risk for MRSA Author contributions carriage among laboratory staff members. J.V. set up the study. K.G., A.O. and A.B. performed investigation and manage‑ Although pseudo-outbreaks due to laboratory contam- ment of the outbreak. K.H., J.S. and J.V. analyzed the data. V.W. and K.C. critically reviewed the analysis. K.H. wrote the main manuscript with the contributions ination of clinical specimens have been reported [7–10], from all coauthors. All authors read and approved the final manuscript. to the best of our knowledge, no pseudo-outbreak due to MRSA carriage of a laboratory staff member has been Funding This research did not receive any specific grant from funding agencies in the described before. This may be due to reporting bias, but public, commercial, or not‑for ‑profit sectors. also due to a lack of awareness recognizing such pseudo- outbreaks. At the time the current pseudo-outbreak Availability of data and materials Genomic sequences are available under the NCBI BioProject accession num‑ due to laboratory contamination was detected, clinical ber PRJEB58118. specimens were inoculated manually. It is likely that con- tamination occurred during inoculation or handling the Declarations culture plate after initial incubation. Automated speci- men processing could minimize the risk of contamina- Ethics approval and consent to participate The data of patients used in this study were part of routine clinical practices in tion. To enable early detection of pseudo-outbreaks, Elisabeth‑ TweeSteden hospital and their anonymous use is beyond the scope whole genome sequencing of newly identified MRSA iso - of the Medical Research Involving Human Subjects Act. lates could be performed routinely in search for clusters Consent for publication within the laboratory specific database. We recommend Not applicable. to further investigate clusters without an epidemiologi- cal link and to consider screening laboratory employees Competing interests The authors declare that they have no competing interests. when laboratory contamination is suspected. Further investigation into MSSA and MRSA carrying laboratory staff members using wgMLST could provide more evi - Received: 22 July 2022 Accepted: 21 December 2022 dence on the possible relationship between MSSA and MRSA carriage and microbiological laboratory work. Houkes et al. 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Schouls LM, Spalburg EC, van Luit M, Huijsdens XW, Pluister GN, van Learn more biomedcentral.com/submissions Santen‑ Verheuvel MG, et al. Multiple‑locus variable number tandem repeat analysis of Staphylococcus aureus: comparison with pulsed‑field
Antimicrobial Resistance & Infection Control – Springer Journals
Published: Jan 5, 2023
Keywords: MRSA; Pseudo-outbreak; Contamination; wgMLST
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