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Outbreak investigation of Serratia marcescens neurosurgical site infections associated with a contaminated shaving razors

Outbreak investigation of Serratia marcescens neurosurgical site infections associated with a... Background: Surgical site infection (SSI) is the most common healthcare-associated infection. We report an outbreak of neurosurgical site infections caused by Serratia marcescens after craniotomy in a tertiary care hospital. Methods: Between August 6 and 21, 2018, five cases of early-onset SSI caused by S. marcescens after craniotomy were recorded in a 1786-bed tertiary care hospital. Cultures were collected from potential environmental sources and healthcare workers. Whole-genome sequencing (WGS) was used to investigate the genetic relationships among S. marcescens isolates. Results: The outbreak involved five patients; S. marcescens was isolated from the cerebrospinal fluid, pus, tissue, and blood samples from these patients. S. marcescens was also isolated from shaving razors and brushes. All S. marcescens isolates from the infected patients and razors showed the same resistance patterns on antibiotic- susceptibility tests. WGS revealed close clustering among four of five isolates from the patients and among three of four isolates from the razors. No additional patient developed S. marcescens infection after we stopped using the razors for scalp shaving. Conclusions: We report an outbreak of neurosurgical site infections after craniotomy, which was associated with shaving razors contaminated by S. marcescens. Shaving scalps with razors should be avoided to prevent SSI. Keywords: Surgical site infection, Serratia marcescens, Disease outbreak, Whole-genome sequencing * Correspondence: molder@unitel.co.kr Center for Infection Control and Prevention, Seoul National University Hospital, Seoul, South Korea Department of Internal Medicine, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul 03080, South Korea Full list of author information is available at the end of the article © The Author(s). 2020 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://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data. Kim et al. Antimicrobial Resistance and Infection Control (2020) 9:64 Page 2 of 7 Background Molecular biological analysis (microbiological A recent prevalence study found surgical site infections investigation/genotyping) (SSIs) to be the most common healthcare-associated in- Whole-genome sequencing (WGS) was performed with fection (HAI), accounting for 31% of all HAIs among nine S. marcescens isolates, including five strains from hospitalized patients [1, 2]. SSI, a serious complication patients with SSI and four from razors. Genomic DNA of surgery, is associated with significant morbidity, mor- extracted using a QIAamp DNA Mini Kit (QIAGEN, tality, and health care costs [3, 4]. Serratia marcescens is Hilden, Germany) was quantified using a Qubit®2.0 in- a gram-negative bacteria widely distributed in the envir- strument (Life Technologies, Burlington, Canada), and onment. It is a well-known etiologic agent of HAIs, in- sequencing libraries were generated using an Illumina cluding bacteremia, urinary tract infection, meningitis, TruSeq DNA PCR-Free Kit (15036187; Illumina). Briefly, pneumonia, and SSIs [5–7]. the samples were normalized to 1 μg DNA and sheared We report an outbreak of neurosurgical site infections by sonication with a Covaris S220. AMPure XP beads by S. marcescens after craniotomy in a tertiary care hos- were used for cleanup and size selection, and adapters pital. We describe the outbreak investigation and the were then ligated. The fragment sizes for all libraries measures taken to control it. were measured using a 2100 Bioanalyzer (Agilent Tech- nologies, Palo Alto, CA, USA), and quantitative polymer- Methods ase chain reaction (qPCR) was performed on a Background and epidemiological investigation LightCycler® 480 System (Roche, CA, USA) with a KAPA The outbreak occurred in a 1,786-bed tertiary care hos- Library Quantification Kit (KK4854, KAPA Biosystems). pital in Seoul, South Korea. Between August 6 and 21, Whole-genome sequencing was performed on an Illu- 2018, five cases of early-onset SSI caused by S. marcescens mina Nextseq500 instrument with 300-cycle reagent. To after craniotomy were confirmed using the 2018 National filter adapter and low quality sequences, all reads were Healthcare Safety Network surveillance definitions [8]. trimmed using fastp (version 0.13.1) with default param- The Infection Control Team has performed surveil- eters [9]. Kraken2, a taxonomic classification system lance of SSIs after craniotomy since 2007 and observed a using exact k-mer matches [10], was used to detect the significant increase in the number of patients with reference genome and S. marcescens subsp. marcescens neurosurgical site infection. S. marcescens had hitherto Db11 was found to have the closest genome to those of been an uncommon pathogen causing SSI, and the inci- the isolates. The trimmed reads were mapped to the ref- dence of neurosurgical site infection by S. marcescens erence sequence using BWA-mem [11], and single nu- significantly increased during the outbreak. As soon as cleotide polymorphisms (SNPs) were detected using an SSI outbreak was suspected, the team monitored the SAMtools and bcftools [12] using default parameters ex- practices and interviewed personnel in the operating cept the following: minimum mapping quality score 30, room, neurosurgical ward, and barbershop. Based on in- minimum base quality score 20, and ploidy 1. For com- formation from observation and interviews, environmen- parison, using the same process, we processed two S. tal samples were obtained for culture. A total of 22 marcescens genome data, PRJEB28358 and PRJEB27112, samples were collected from water sources, scrub sinks, publically available in the European Nucleotide Archive surfaces, and shaving razors in the operation room. An- (ENA) database consisting of 19 and 17 isolates, derived other 296 samples were collected from surgical instru- from the outbreaks in Germany and India, respectively ments, and 39 nasal samples were collected from [13, 14]. The core regions were defined as the genomic doctors, nurses, and other healthcare workers who were positions having depths from all 47 isolates ranging be- associated with neurosurgical operations and the hos- tween mean depth ± 2 standard deviations. Phylogenetic pital barbershop. An additional 30 samples were col- analysis was conducted using MEGA-X (version 10.0.5) lected from the equipment used for preoperative [15] with SNPs only in core regions. The distances between shaving, including razors, brushes, solid soap for shaving, isolates were computed with the maximum composite like- and other tools in the barbershop. lihood method [16], and the phylogenetic tree was built by All environmental samples were immersed in 3 mL an unweighted pair group with arithmetic mean (UPGMA) brain heart infusion (BHI) broth and cultured aerobically method. The test of phylogeny was performed using the for 24 h at 35 °C ± 2 °C. The BHI was inoculated onto bootstrap test (number of bootstrap = 100). blood agar plates and MacConkey agar and incubated for 24 h at 35 °C ± 2 °C. Bacteria were identified using Statistical analysis matrix-assisted laser desorption/ionization-time of flight The prevalence of SSI in the pre-outbreak and outbreak (MALDI-TOF), and antimicrobial susceptibility tests periods was compared by chi-square tests using IBM were performed using either VITEK 2 or Microscan SPSS Statistics for Windows, version 23.0 (IBM Corp., Walkaway 96 plus instruments. Armonk, NY). Kim et al. Antimicrobial Resistance and Infection Control (2020) 9:64 Page 3 of 7 Results surgery. Microorganisms other than S. marcescens were Outbreak investigation detected in 53 samples collected from environment and Surveillance of SSIs following craniotomy since 2007 re- healthcare workers. (Table 2) All patients were treated vealed a prevalence of 1.82% (165/9,058) until July 2018. with antibiotics, and some underwent wound debride- Between August 6 and 21, 2018, five cases (11.63%) out ment and/or external ventricular drainage. of 43 patients who underwent craniotomy developed neurosurgical SSI due to S. marcescens. The prevalence Implementation of infection control measures of neurosurgical site infection increased significantly Upon detection of S. marcescens on the razors, we compared to that in the pre-outbreak period (p = 0.003). stopped using the razors for scalp shaving in the barber- Between January 2014 and July 2018, the prevalence of shop, ward, and operating room. Contamination of oper- SSI following craniotomy was 1.03% (45/4,384). During ating rooms, instruments, or specific procedures such as this period, the most common etiologic microorganism wound dressing, and bacterial colonization among health was Staphylococcus aureus (22.2%), followed by care workers were checked while investigating the out- coagulase-negative staphylococcus (21.6%). S. marcescens break, but there was no common source of S. marcescens accounted for 8.3% of etiologic microorganisms. Consid- infection other than brushes and razors in the barber- ering the significant increase in the prevalence of SSI shop. We recommended that trained doctors or nurses and proportion of S. marcescens, we decided to start an shave scalps using disposable clippers for surgery when outbreak investigation. Between August 6 and 21, 2018, shaving was necessary. Infection Control team nurses there was another case of SSI after craniotomy which performed rounds frequently to enforce standardized was attributed to Staphylococcus aureus. Four cases of skin preparation procedures and the use of clippers. SSI were monomicrobial infections caused by S. marces- After implementation of these infection control mea- cens, and one case was a polymicrobial infection caused sures, no further patients developed S. marcescens by S. marcescens and Klebsiella aerogenes. infections. The epidemiological and clinical characteristics of the patients are summarized in Table 1. S. marcescens was Antibiotic susceptibility and molecular biological analysis isolated from cerebrospinal fluid (three patients), pus The S. marcescens isolates from infected patients and ra- (four patients), tissue (one patient), and blood (one pa- zors shared the same resistance pattern in antibiotic- tient). Three of the five patients (60%) were female, and susceptibility testing. The isolates were resistant to the mean age of the patients was 39 years (range 11–76 amoxicillin/clavulanic acid and nitrofurantoin and sus- years). The mean interval between surgery and positive ceptible to piperacillin/tazobactam, ceftriaxone, cefe- culture was 7.2 days (range 3–11 days). These patients pime, ertapenem, imipenem, meropenem, gentamicin, were located in different wards and their operations ciprofloxacin, and trimethoprim/sulfamethoxazole. were performed by different surgeons. All patients had WGS was performed for nine S. marcescens isolates, undergone preoperative scalp shaving at the barbershop five strains from patients with SSI, and four from razors. in the study hospital. Among the 387 surveillance sam- The mean sequencing depth of the nine isolates in this ples (22 from the water sink and surface of operating study was 220× (185–244×) and the number of SNPs in rooms, 296 from surgical instruments, 30 from the the core regions was 142,316 on average. With WGS barbershop, and 39 from healthcare workers), S. marces- data of 36 S. marcescens isolates derived from the out- cens was isolated from two shaving brushes and four ra- breaks in Germany and India, a total 420,357 bp of core zors that had been used to shave patients’ hair before regions with SNPs were used to build the phylogenetic Table 1 Epidemiological and clinical characteristics of outbreak patients with SSI caused by Serratia marcescens after craniotomy Patient Age/sex Date of surgery Date of isolation Operative procedures Isolates Scalp shaving Management of surgical using razors site infection 1 76/female 8/6/2018 8/9/2018 Craniotomy, Occipital artery to CSF, Blood Yes Antibiotics, EVD posterior inferior cerebellar artery bypass 2 66/female 8/6/2018 8/13/2018 Craniotomy, tumor removal CSF, Pus Yes Antibiotics, EVD 3 11/female 8/6/2018 8/14/2018 Craniotomy, Encephaloduroarterio Wound, Pus Yes Antibiotics, wound synangiosis debridement 4 14/male 8/10/2018 8/21/2018 Craniotomy, Encephaloduroarterio Pus Yes Antibiotics, wound synangiosis debridement 5 29/male 8/21/2018 8/28/2018 Craniotomy, tumor removal CSF, Pus, Tissue Yes Antibiotics, EVD CSF, cerebrospinal fluid; EVD, extraventricular drain Kim et al. Antimicrobial Resistance and Infection Control (2020) 9:64 Page 4 of 7 Table 2 Surveillance cultures from environmental samples and healthcare workers Environment Healthcare Total workers (n = 387) Surface of sink, Surgical instruments Tools for shaving or in the barbershop (n = 39) operating room (n = 296) (n = 30) (n = 22) Positive culture (%) 7 (31.8) 10 (3.4) 25 (83.3) 17 (43.6) 59 (15.2) S. aureus, n (%) 2 (6.7) 2 (5.1) 4 (1.0) CNS, n (%) 2 (9.1) 9 (3.1) 6 (20.0) 17 (4.4) Bacillus spp., n (%) 5 (22.7) 1 (3.3) 6 (1.6) Enterococcus spp., n (%) 1 (3.3) 1 (0.3) Micrococcus spp., n (%) 1 (0.3) 1 (0.3) Klebsiella spp., n (%) 14 (35.9) 14 (3.6) Enterobacter spp., n (%) 3 (10.0) 3 (0.7) Raoultella spp. n (%) 3 (10.0) 3 (0.7) Escherichia spp. n (%) 1 (2.6) 1 (0.3) Pseudomonas spp.,, n (%) 3 (10.0) 3 (0.7) S. marcescens, n (%) 6 (20.0) 6 (1.6) CNS Coagulase negative staphylococcus, 13 Klebsiella aerogenes and 1 Klebsiella pneumoniae Fig. 1 The Phylogenetic tree of S. marcescens isolates across three outbreaks in Korea, India, and Germany. An UPGMA phylogenetic tree of S. marcescens isolates from the three outbreaks was generated using the 420,357 core SNP positions detected. The tree reveals the tight clustering of isolates from four patients and three razors in Korea (blue). The other brackets (orange for India, green for Cologne in Germany) annotate clusters described in the previous studies, and all clusters have the same isolates as observed in this study. The small box shows an ~ 100 times enlarged subtree of the clustered isolates. The scale bar and branch lengths are in the units of the number of base substitutions per site. The percentage of replicate trees in which the associated taxa clustered tighter in the bootstrap test (100 replicates) is shown close to the branches in the small box Kim et al. Antimicrobial Resistance and Infection Control (2020) 9:64 Page 5 of 7 tree. Phylogenetic analysis using WGS revealed close clus- razors to shave scalps and recommended disposable clip- tering between four of five patient isolates and three of pers if scalp shaving was necessary. Following the imple- four razor isolates (Fig. 1). S. marcescens isolated from pa- mentation of these recommendations, no further patients tients and razors were expected to be of the same strain, have developed SSI by S. marcescens. but there was a considerable distance genetically between Typing methods for discriminating different bacterial iso- the strains isolated from patient 3, razor 1, and others. lates of the same species are essential tools in outbreak in- vestigation. A typing method must have the discriminatory Discussion power to distinguish related and unrelated isolates. These Neurosurgical site infection occurs in 2.2–4.7% of pa- methods are classified as phenotypic or molecular. Pheno- tients after craniotomy [17]. SSI after craniotomy has typic methods include antibiograms, serotyping, and bio- been associated with increased morbidity, risk of reoper- typing, while molecular methods include pulse-field gel ation, neurological sequelae, and mortality. A meta- electrophoresis, multi-locus sequencing typing, and variable analysis revealed that the risk factors for SSI included number tandem repeat typing. Following improvements in CSF leakage, CSF drainage, operation duration, venous sequencing technologies, whole-genome sequencing sinus entry, and American Society of Anesthesiologists (WGS) is a highly discriminative tool that has become the score [18]. In the current report, we found that contami- gold standard for bacterial typing, as it can define the nated brushes and razors were the sources of the out- complete genomic structure of a pathogen [26, 27]. In this break and that the inadequate shaving technique might study, we applied WGS to investigate the relatedness of S. cause serious neurosurgical site infections. marcescens isolates, finding close genetic relationships be- It is common practice to shave a patient’shairaround tween four patient and three razor isolates. The strain iso- the surgical area. Hair removal has benefits for surgical lated from patient 3 did not show close genetic similarity wound visualization, dressing application, and avoidance with the other strains; therefore the S. marcescens infection of potential annoyance due to hair. Furthermore, many in patient 3 should be considered as irrelevant to the S. surgeons believe that hair removal is helpful for the pre- marcescens outbreak. vention of SSI. However, the results of randomized con- We obtained nasal samples rather than samples from trolled trials revealed no differences in SSIs between the hands for bacterial culture. Considering that bacterial patients with and without hair removal before surgery colonizations in the hand sample is a more meaningful in- [19]. In the context of neurosurgery, the prevalence of dicator of SSI than that in nasal sample, it would be better SSIs also does not differ with scalp shaving [20–23]. Toki- to consider hands as a site of surveillance culture. mura et al. conducted a retrospective study of 632 patients The epidemiological and microbiological evidence in- who underwent cranial surgery without head shaving, of dicated that contaminated razors and brushes in the which only 7 (1.1%) developed postoperative infections barbershop were the sources of the outbreak. The out- [20]. Horgan et al. and Ratanalert et al. conducted ran- break ended after stopping preoperative shaving in the domized studies with 20 patients and 225 procedures re- barbershop and instead using disposable surgical clip- spectively [22, 23]. In Horgans’ trial, 10 patients had been pers. Several studies have also reported outbreaks associ- assigned to the non-shaved group, and there was no infec- ated with contaminated razors or brushes [28, 29]. The tion in both groups. In Ratanalert’s trial, 89 procedures findings of the present report have implications for clini- had been allocated to the non-shaved group, and the rates cians and infection preventionists. First, inadequate of SSI were 3.37 and 5.88%, respectively. (p >0.05) Fur- shaving technique may cause severe SSIs. Second, the ther, a systematic review including 18 studies on the effect use of razors to shave scalps is not recommended be- of preoperative scalp shaving on SSI showed that pre- cause it is associated with an increased incidence of SSI. operative scalp shaving was unnecessary for the asepsis of Third, regular surveillance for SSIs may be beneficial for surgical sites [21]. However, as those studies are under- early outbreak detection. Infection control practitioners powered, more research is needed to obtain conclusive can play an important role in screening and preventing evidence. Moreover, the guidelines from the Centers for outbreaks of SSI based on the prevalence of SSI and the Diseases Control and Prevention and the World Health distribution of pathogens. Organization recommend that hair not be removed unless it interferes with the surgical procedure [24, 25]. If it is ne- Conclusions cessary to remove hair, clipping rather than shaving is rec- We reported an outbreak of neurosurgical site infections ommended in light of infection control [19]. In the associated with shaving razors contaminated by S. mar- present study hospital, scalp shaving was performed by cescens. To prevent SSIs, razors should not be used to barbers in the barbershop. Shaving razors were reused be- shave scalps. As recommended in several guidelines, tween patients, which eventually resulted in an outbreak proper hair removal using disposal clippers before sur- of SSI. The infection control team prohibited the use of gery is important for the prevention of SSIs. Kim et al. Antimicrobial Resistance and Infection Control (2020) 9:64 Page 6 of 7 Abbreviations 6. Cilli F, Nazli-Zeka A, Arda B, Sipahi OR, Aksit-Barik S, Kepeli N, Ozinel MA, SSI: Surgical site infection; WGS: Whole-genome sequencing; HAI: Healthcare- Gulay Z, Ulusoy S. Serratia marcescens sepsis outbreak caused by associated infection; BHI: Brain heart infusion contaminated propofol. Am J Infect Control. 2019;47(5):582–4. 7. Redondo-Bravo L, Gutiérrez-González E, San Juan-Sanz I, Fernández-Jiménez I, Ruiz-Carrascoso G, Gallego-Lombardo S, Sánchez-García L, Elorza- Acknowledgements Fernández D, Pellicer-Martínez A, Omeñaca F. Serratia marcescens outbreak We thank our colleagues of infection control team and department of in a neonatology unit of a Spanish tertiary hospital: risk factors and control neurosurgery in Seoul National University Hospital. measures. Am J Infect Control. 2019;47(3):271–9. Authors’ contributions 8. Centers for Disease Control and Prevention. 2019 Patient Safety Component EJK and NJK designed the study and wrote the manuscript. WSJ, KIJ and CKK Manual. http://www.cdc.gov/nhsn/validation. Accessed 20 Sept 2019. contributed to patients’ medical care. SJK and YRO collected the data. PGC, 9. Chen S, Zhou Y, Chen Y, Gu J. Fastp: an ultra-fast all-in-one FASTQ WBP, EHC and MDO analyzed and interpreted the data. All authors read and preprocessor. Bioinformatics. 2018;34(17):i884–90. approved the final manuscript. 10. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with kraken 2. Genome Biol. 2019;20(1):257. 11. Yao C, Liu X, Tang Z. Prognostic role of neutrophil-lymphocyte ratio and Author’s information platelet-lymphocyte ratio for hospital mortality in patients with AECOPD. Int This study was presented at the slide session of surgical site infection in the J Chron Obstruct Pulmon Dis. 2017;12:2285–90. 5th International Conference on Prevention & Infection Control (ICPIC 2019), 10–13 September 2019, Geneva, Switzerland [abstract no. ICPIC19-ABS-1470]. 12. Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics. 2011;27(21):2987–93. Funding 13. Rohit A, Suresh Kumar D, Dhinakaran I, Joy J, Vijay Kumar D, Kumar Not applicable. Ballamoole K, Karunasagar I, Karola P, Dag H. Whole-genome-based analysis reveals multiclone Serratia marcescens outbreaks in a non-neonatal Availability of data and materials intensive care unit setting in a tertiary care hospital in India. 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Outbreak investigation of Serratia marcescens neurosurgical site infections associated with a contaminated shaving razors

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Abstract

Background: Surgical site infection (SSI) is the most common healthcare-associated infection. We report an outbreak of neurosurgical site infections caused by Serratia marcescens after craniotomy in a tertiary care hospital. Methods: Between August 6 and 21, 2018, five cases of early-onset SSI caused by S. marcescens after craniotomy were recorded in a 1786-bed tertiary care hospital. Cultures were collected from potential environmental sources and healthcare workers. Whole-genome sequencing (WGS) was used to investigate the genetic relationships among S. marcescens isolates. Results: The outbreak involved five patients; S. marcescens was isolated from the cerebrospinal fluid, pus, tissue, and blood samples from these patients. S. marcescens was also isolated from shaving razors and brushes. All S. marcescens isolates from the infected patients and razors showed the same resistance patterns on antibiotic- susceptibility tests. WGS revealed close clustering among four of five isolates from the patients and among three of four isolates from the razors. No additional patient developed S. marcescens infection after we stopped using the razors for scalp shaving. Conclusions: We report an outbreak of neurosurgical site infections after craniotomy, which was associated with shaving razors contaminated by S. marcescens. Shaving scalps with razors should be avoided to prevent SSI. Keywords: Surgical site infection, Serratia marcescens, Disease outbreak, Whole-genome sequencing * Correspondence: molder@unitel.co.kr Center for Infection Control and Prevention, Seoul National University Hospital, Seoul, South Korea Department of Internal Medicine, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul 03080, South Korea Full list of author information is available at the end of the article © The Author(s). 2020 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://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data. Kim et al. Antimicrobial Resistance and Infection Control (2020) 9:64 Page 2 of 7 Background Molecular biological analysis (microbiological A recent prevalence study found surgical site infections investigation/genotyping) (SSIs) to be the most common healthcare-associated in- Whole-genome sequencing (WGS) was performed with fection (HAI), accounting for 31% of all HAIs among nine S. marcescens isolates, including five strains from hospitalized patients [1, 2]. SSI, a serious complication patients with SSI and four from razors. Genomic DNA of surgery, is associated with significant morbidity, mor- extracted using a QIAamp DNA Mini Kit (QIAGEN, tality, and health care costs [3, 4]. Serratia marcescens is Hilden, Germany) was quantified using a Qubit®2.0 in- a gram-negative bacteria widely distributed in the envir- strument (Life Technologies, Burlington, Canada), and onment. It is a well-known etiologic agent of HAIs, in- sequencing libraries were generated using an Illumina cluding bacteremia, urinary tract infection, meningitis, TruSeq DNA PCR-Free Kit (15036187; Illumina). Briefly, pneumonia, and SSIs [5–7]. the samples were normalized to 1 μg DNA and sheared We report an outbreak of neurosurgical site infections by sonication with a Covaris S220. AMPure XP beads by S. marcescens after craniotomy in a tertiary care hos- were used for cleanup and size selection, and adapters pital. We describe the outbreak investigation and the were then ligated. The fragment sizes for all libraries measures taken to control it. were measured using a 2100 Bioanalyzer (Agilent Tech- nologies, Palo Alto, CA, USA), and quantitative polymer- Methods ase chain reaction (qPCR) was performed on a Background and epidemiological investigation LightCycler® 480 System (Roche, CA, USA) with a KAPA The outbreak occurred in a 1,786-bed tertiary care hos- Library Quantification Kit (KK4854, KAPA Biosystems). pital in Seoul, South Korea. Between August 6 and 21, Whole-genome sequencing was performed on an Illu- 2018, five cases of early-onset SSI caused by S. marcescens mina Nextseq500 instrument with 300-cycle reagent. To after craniotomy were confirmed using the 2018 National filter adapter and low quality sequences, all reads were Healthcare Safety Network surveillance definitions [8]. trimmed using fastp (version 0.13.1) with default param- The Infection Control Team has performed surveil- eters [9]. Kraken2, a taxonomic classification system lance of SSIs after craniotomy since 2007 and observed a using exact k-mer matches [10], was used to detect the significant increase in the number of patients with reference genome and S. marcescens subsp. marcescens neurosurgical site infection. S. marcescens had hitherto Db11 was found to have the closest genome to those of been an uncommon pathogen causing SSI, and the inci- the isolates. The trimmed reads were mapped to the ref- dence of neurosurgical site infection by S. marcescens erence sequence using BWA-mem [11], and single nu- significantly increased during the outbreak. As soon as cleotide polymorphisms (SNPs) were detected using an SSI outbreak was suspected, the team monitored the SAMtools and bcftools [12] using default parameters ex- practices and interviewed personnel in the operating cept the following: minimum mapping quality score 30, room, neurosurgical ward, and barbershop. Based on in- minimum base quality score 20, and ploidy 1. For com- formation from observation and interviews, environmen- parison, using the same process, we processed two S. tal samples were obtained for culture. A total of 22 marcescens genome data, PRJEB28358 and PRJEB27112, samples were collected from water sources, scrub sinks, publically available in the European Nucleotide Archive surfaces, and shaving razors in the operation room. An- (ENA) database consisting of 19 and 17 isolates, derived other 296 samples were collected from surgical instru- from the outbreaks in Germany and India, respectively ments, and 39 nasal samples were collected from [13, 14]. The core regions were defined as the genomic doctors, nurses, and other healthcare workers who were positions having depths from all 47 isolates ranging be- associated with neurosurgical operations and the hos- tween mean depth ± 2 standard deviations. Phylogenetic pital barbershop. An additional 30 samples were col- analysis was conducted using MEGA-X (version 10.0.5) lected from the equipment used for preoperative [15] with SNPs only in core regions. The distances between shaving, including razors, brushes, solid soap for shaving, isolates were computed with the maximum composite like- and other tools in the barbershop. lihood method [16], and the phylogenetic tree was built by All environmental samples were immersed in 3 mL an unweighted pair group with arithmetic mean (UPGMA) brain heart infusion (BHI) broth and cultured aerobically method. The test of phylogeny was performed using the for 24 h at 35 °C ± 2 °C. The BHI was inoculated onto bootstrap test (number of bootstrap = 100). blood agar plates and MacConkey agar and incubated for 24 h at 35 °C ± 2 °C. Bacteria were identified using Statistical analysis matrix-assisted laser desorption/ionization-time of flight The prevalence of SSI in the pre-outbreak and outbreak (MALDI-TOF), and antimicrobial susceptibility tests periods was compared by chi-square tests using IBM were performed using either VITEK 2 or Microscan SPSS Statistics for Windows, version 23.0 (IBM Corp., Walkaway 96 plus instruments. Armonk, NY). Kim et al. Antimicrobial Resistance and Infection Control (2020) 9:64 Page 3 of 7 Results surgery. Microorganisms other than S. marcescens were Outbreak investigation detected in 53 samples collected from environment and Surveillance of SSIs following craniotomy since 2007 re- healthcare workers. (Table 2) All patients were treated vealed a prevalence of 1.82% (165/9,058) until July 2018. with antibiotics, and some underwent wound debride- Between August 6 and 21, 2018, five cases (11.63%) out ment and/or external ventricular drainage. of 43 patients who underwent craniotomy developed neurosurgical SSI due to S. marcescens. The prevalence Implementation of infection control measures of neurosurgical site infection increased significantly Upon detection of S. marcescens on the razors, we compared to that in the pre-outbreak period (p = 0.003). stopped using the razors for scalp shaving in the barber- Between January 2014 and July 2018, the prevalence of shop, ward, and operating room. Contamination of oper- SSI following craniotomy was 1.03% (45/4,384). During ating rooms, instruments, or specific procedures such as this period, the most common etiologic microorganism wound dressing, and bacterial colonization among health was Staphylococcus aureus (22.2%), followed by care workers were checked while investigating the out- coagulase-negative staphylococcus (21.6%). S. marcescens break, but there was no common source of S. marcescens accounted for 8.3% of etiologic microorganisms. Consid- infection other than brushes and razors in the barber- ering the significant increase in the prevalence of SSI shop. We recommended that trained doctors or nurses and proportion of S. marcescens, we decided to start an shave scalps using disposable clippers for surgery when outbreak investigation. Between August 6 and 21, 2018, shaving was necessary. Infection Control team nurses there was another case of SSI after craniotomy which performed rounds frequently to enforce standardized was attributed to Staphylococcus aureus. Four cases of skin preparation procedures and the use of clippers. SSI were monomicrobial infections caused by S. marces- After implementation of these infection control mea- cens, and one case was a polymicrobial infection caused sures, no further patients developed S. marcescens by S. marcescens and Klebsiella aerogenes. infections. The epidemiological and clinical characteristics of the patients are summarized in Table 1. S. marcescens was Antibiotic susceptibility and molecular biological analysis isolated from cerebrospinal fluid (three patients), pus The S. marcescens isolates from infected patients and ra- (four patients), tissue (one patient), and blood (one pa- zors shared the same resistance pattern in antibiotic- tient). Three of the five patients (60%) were female, and susceptibility testing. The isolates were resistant to the mean age of the patients was 39 years (range 11–76 amoxicillin/clavulanic acid and nitrofurantoin and sus- years). The mean interval between surgery and positive ceptible to piperacillin/tazobactam, ceftriaxone, cefe- culture was 7.2 days (range 3–11 days). These patients pime, ertapenem, imipenem, meropenem, gentamicin, were located in different wards and their operations ciprofloxacin, and trimethoprim/sulfamethoxazole. were performed by different surgeons. All patients had WGS was performed for nine S. marcescens isolates, undergone preoperative scalp shaving at the barbershop five strains from patients with SSI, and four from razors. in the study hospital. Among the 387 surveillance sam- The mean sequencing depth of the nine isolates in this ples (22 from the water sink and surface of operating study was 220× (185–244×) and the number of SNPs in rooms, 296 from surgical instruments, 30 from the the core regions was 142,316 on average. With WGS barbershop, and 39 from healthcare workers), S. marces- data of 36 S. marcescens isolates derived from the out- cens was isolated from two shaving brushes and four ra- breaks in Germany and India, a total 420,357 bp of core zors that had been used to shave patients’ hair before regions with SNPs were used to build the phylogenetic Table 1 Epidemiological and clinical characteristics of outbreak patients with SSI caused by Serratia marcescens after craniotomy Patient Age/sex Date of surgery Date of isolation Operative procedures Isolates Scalp shaving Management of surgical using razors site infection 1 76/female 8/6/2018 8/9/2018 Craniotomy, Occipital artery to CSF, Blood Yes Antibiotics, EVD posterior inferior cerebellar artery bypass 2 66/female 8/6/2018 8/13/2018 Craniotomy, tumor removal CSF, Pus Yes Antibiotics, EVD 3 11/female 8/6/2018 8/14/2018 Craniotomy, Encephaloduroarterio Wound, Pus Yes Antibiotics, wound synangiosis debridement 4 14/male 8/10/2018 8/21/2018 Craniotomy, Encephaloduroarterio Pus Yes Antibiotics, wound synangiosis debridement 5 29/male 8/21/2018 8/28/2018 Craniotomy, tumor removal CSF, Pus, Tissue Yes Antibiotics, EVD CSF, cerebrospinal fluid; EVD, extraventricular drain Kim et al. Antimicrobial Resistance and Infection Control (2020) 9:64 Page 4 of 7 Table 2 Surveillance cultures from environmental samples and healthcare workers Environment Healthcare Total workers (n = 387) Surface of sink, Surgical instruments Tools for shaving or in the barbershop (n = 39) operating room (n = 296) (n = 30) (n = 22) Positive culture (%) 7 (31.8) 10 (3.4) 25 (83.3) 17 (43.6) 59 (15.2) S. aureus, n (%) 2 (6.7) 2 (5.1) 4 (1.0) CNS, n (%) 2 (9.1) 9 (3.1) 6 (20.0) 17 (4.4) Bacillus spp., n (%) 5 (22.7) 1 (3.3) 6 (1.6) Enterococcus spp., n (%) 1 (3.3) 1 (0.3) Micrococcus spp., n (%) 1 (0.3) 1 (0.3) Klebsiella spp., n (%) 14 (35.9) 14 (3.6) Enterobacter spp., n (%) 3 (10.0) 3 (0.7) Raoultella spp. n (%) 3 (10.0) 3 (0.7) Escherichia spp. n (%) 1 (2.6) 1 (0.3) Pseudomonas spp.,, n (%) 3 (10.0) 3 (0.7) S. marcescens, n (%) 6 (20.0) 6 (1.6) CNS Coagulase negative staphylococcus, 13 Klebsiella aerogenes and 1 Klebsiella pneumoniae Fig. 1 The Phylogenetic tree of S. marcescens isolates across three outbreaks in Korea, India, and Germany. An UPGMA phylogenetic tree of S. marcescens isolates from the three outbreaks was generated using the 420,357 core SNP positions detected. The tree reveals the tight clustering of isolates from four patients and three razors in Korea (blue). The other brackets (orange for India, green for Cologne in Germany) annotate clusters described in the previous studies, and all clusters have the same isolates as observed in this study. The small box shows an ~ 100 times enlarged subtree of the clustered isolates. The scale bar and branch lengths are in the units of the number of base substitutions per site. The percentage of replicate trees in which the associated taxa clustered tighter in the bootstrap test (100 replicates) is shown close to the branches in the small box Kim et al. Antimicrobial Resistance and Infection Control (2020) 9:64 Page 5 of 7 tree. Phylogenetic analysis using WGS revealed close clus- razors to shave scalps and recommended disposable clip- tering between four of five patient isolates and three of pers if scalp shaving was necessary. Following the imple- four razor isolates (Fig. 1). S. marcescens isolated from pa- mentation of these recommendations, no further patients tients and razors were expected to be of the same strain, have developed SSI by S. marcescens. but there was a considerable distance genetically between Typing methods for discriminating different bacterial iso- the strains isolated from patient 3, razor 1, and others. lates of the same species are essential tools in outbreak in- vestigation. A typing method must have the discriminatory Discussion power to distinguish related and unrelated isolates. These Neurosurgical site infection occurs in 2.2–4.7% of pa- methods are classified as phenotypic or molecular. Pheno- tients after craniotomy [17]. SSI after craniotomy has typic methods include antibiograms, serotyping, and bio- been associated with increased morbidity, risk of reoper- typing, while molecular methods include pulse-field gel ation, neurological sequelae, and mortality. A meta- electrophoresis, multi-locus sequencing typing, and variable analysis revealed that the risk factors for SSI included number tandem repeat typing. Following improvements in CSF leakage, CSF drainage, operation duration, venous sequencing technologies, whole-genome sequencing sinus entry, and American Society of Anesthesiologists (WGS) is a highly discriminative tool that has become the score [18]. In the current report, we found that contami- gold standard for bacterial typing, as it can define the nated brushes and razors were the sources of the out- complete genomic structure of a pathogen [26, 27]. In this break and that the inadequate shaving technique might study, we applied WGS to investigate the relatedness of S. cause serious neurosurgical site infections. marcescens isolates, finding close genetic relationships be- It is common practice to shave a patient’shairaround tween four patient and three razor isolates. The strain iso- the surgical area. Hair removal has benefits for surgical lated from patient 3 did not show close genetic similarity wound visualization, dressing application, and avoidance with the other strains; therefore the S. marcescens infection of potential annoyance due to hair. Furthermore, many in patient 3 should be considered as irrelevant to the S. surgeons believe that hair removal is helpful for the pre- marcescens outbreak. vention of SSI. However, the results of randomized con- We obtained nasal samples rather than samples from trolled trials revealed no differences in SSIs between the hands for bacterial culture. Considering that bacterial patients with and without hair removal before surgery colonizations in the hand sample is a more meaningful in- [19]. In the context of neurosurgery, the prevalence of dicator of SSI than that in nasal sample, it would be better SSIs also does not differ with scalp shaving [20–23]. Toki- to consider hands as a site of surveillance culture. mura et al. conducted a retrospective study of 632 patients The epidemiological and microbiological evidence in- who underwent cranial surgery without head shaving, of dicated that contaminated razors and brushes in the which only 7 (1.1%) developed postoperative infections barbershop were the sources of the outbreak. The out- [20]. Horgan et al. and Ratanalert et al. conducted ran- break ended after stopping preoperative shaving in the domized studies with 20 patients and 225 procedures re- barbershop and instead using disposable surgical clip- spectively [22, 23]. In Horgans’ trial, 10 patients had been pers. Several studies have also reported outbreaks associ- assigned to the non-shaved group, and there was no infec- ated with contaminated razors or brushes [28, 29]. The tion in both groups. In Ratanalert’s trial, 89 procedures findings of the present report have implications for clini- had been allocated to the non-shaved group, and the rates cians and infection preventionists. First, inadequate of SSI were 3.37 and 5.88%, respectively. (p >0.05) Fur- shaving technique may cause severe SSIs. Second, the ther, a systematic review including 18 studies on the effect use of razors to shave scalps is not recommended be- of preoperative scalp shaving on SSI showed that pre- cause it is associated with an increased incidence of SSI. operative scalp shaving was unnecessary for the asepsis of Third, regular surveillance for SSIs may be beneficial for surgical sites [21]. However, as those studies are under- early outbreak detection. Infection control practitioners powered, more research is needed to obtain conclusive can play an important role in screening and preventing evidence. Moreover, the guidelines from the Centers for outbreaks of SSI based on the prevalence of SSI and the Diseases Control and Prevention and the World Health distribution of pathogens. Organization recommend that hair not be removed unless it interferes with the surgical procedure [24, 25]. If it is ne- Conclusions cessary to remove hair, clipping rather than shaving is rec- We reported an outbreak of neurosurgical site infections ommended in light of infection control [19]. In the associated with shaving razors contaminated by S. mar- present study hospital, scalp shaving was performed by cescens. To prevent SSIs, razors should not be used to barbers in the barbershop. Shaving razors were reused be- shave scalps. As recommended in several guidelines, tween patients, which eventually resulted in an outbreak proper hair removal using disposal clippers before sur- of SSI. The infection control team prohibited the use of gery is important for the prevention of SSIs. Kim et al. Antimicrobial Resistance and Infection Control (2020) 9:64 Page 6 of 7 Abbreviations 6. Cilli F, Nazli-Zeka A, Arda B, Sipahi OR, Aksit-Barik S, Kepeli N, Ozinel MA, SSI: Surgical site infection; WGS: Whole-genome sequencing; HAI: Healthcare- Gulay Z, Ulusoy S. Serratia marcescens sepsis outbreak caused by associated infection; BHI: Brain heart infusion contaminated propofol. Am J Infect Control. 2019;47(5):582–4. 7. Redondo-Bravo L, Gutiérrez-González E, San Juan-Sanz I, Fernández-Jiménez I, Ruiz-Carrascoso G, Gallego-Lombardo S, Sánchez-García L, Elorza- Acknowledgements Fernández D, Pellicer-Martínez A, Omeñaca F. Serratia marcescens outbreak We thank our colleagues of infection control team and department of in a neonatology unit of a Spanish tertiary hospital: risk factors and control neurosurgery in Seoul National University Hospital. measures. Am J Infect Control. 2019;47(3):271–9. Authors’ contributions 8. Centers for Disease Control and Prevention. 2019 Patient Safety Component EJK and NJK designed the study and wrote the manuscript. WSJ, KIJ and CKK Manual. http://www.cdc.gov/nhsn/validation. Accessed 20 Sept 2019. contributed to patients’ medical care. SJK and YRO collected the data. PGC, 9. Chen S, Zhou Y, Chen Y, Gu J. Fastp: an ultra-fast all-in-one FASTQ WBP, EHC and MDO analyzed and interpreted the data. All authors read and preprocessor. Bioinformatics. 2018;34(17):i884–90. approved the final manuscript. 10. Wood DE, Lu J, Langmead B. Improved metagenomic analysis with kraken 2. Genome Biol. 2019;20(1):257. 11. Yao C, Liu X, Tang Z. Prognostic role of neutrophil-lymphocyte ratio and Author’s information platelet-lymphocyte ratio for hospital mortality in patients with AECOPD. Int This study was presented at the slide session of surgical site infection in the J Chron Obstruct Pulmon Dis. 2017;12:2285–90. 5th International Conference on Prevention & Infection Control (ICPIC 2019), 10–13 September 2019, Geneva, Switzerland [abstract no. ICPIC19-ABS-1470]. 12. Li H. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics. 2011;27(21):2987–93. Funding 13. Rohit A, Suresh Kumar D, Dhinakaran I, Joy J, Vijay Kumar D, Kumar Not applicable. Ballamoole K, Karunasagar I, Karola P, Dag H. Whole-genome-based analysis reveals multiclone Serratia marcescens outbreaks in a non-neonatal Availability of data and materials intensive care unit setting in a tertiary care hospital in India. J Med WGS data were deposited at Short Read Archive (assessment number Microbiol. 2019;68(4):616–21. PRJNA609822). Other data generated or analyzed during this study are 14. Rossen JWA, Dombrecht J, Vanfleteren D, De Bruyne K, van Belkum A, included in this published article. Rosema S, Lokate M, Bathoorn E, Reuter S, Grundmann H, et al. Epidemiological typing of serratia marcescens isolates by whole-genome Ethics approval and consent to participate multilocus sequence typing. J Clin Microbiol. 2019;57(4). https://doi.org/10. This study was approved by the Institutional Review Board of the study 1128/JCM.01652-18. hospitals (IRB No. H-1906-146-1043). 15. Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. Consent for publication 2018;35(6):1547–9. Not applicable. 16. Tamura K, Nei M, Kumar S. Prospects for inferring very large phylogenies by using the neighbor-joining method. 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