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Practical toolkit for monitoring endoscope reprocessing effectiveness: Identification of viable bacteria on gastroscopes, colonoscopes, and bronchoscopes
ARTICLE IN PRESS American Journal of Infection Control ■■ (2016) ■■-■■
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
j o u r n a l h o m e p a g e : w w w. a j i c j o u r n a l . o r g
Original Research Article
Practical toolkit for monitoring endoscope reprocessing effectiveness: Identification of viable bacteria on gastroscopes, colonoscopes, and bronchoscopes Cori L. Ofstead MSPH a,*, Evan M. Doyle BS a, John E. Eiland MS, RN a, Miriam R. Amelang BA a, Harry P. Wetzler MD, MSPH a, Dawn M. England MPH, CPHQ b, Kristin M. Mascotti MD, CPE c, Michael J. Shaw MD d a
Ofstead & Associates, Inc, St Paul, MN Department of Infection Prevention, University of Minnesota Health, Minneapolis, MN c Department of Clinical Quality Improvement, University of Minnesota Health, Minneapolis, MN d Division of Gastroenterology, Department of Medicine, University of Minnesota Medical School, Minneapolis, MN b
Key Words: High-level disinfection Microbial cultures Stenotrophomonas maltophilia
Background: Experts have recommended microbiologic surveillance by external reference laboratories for certain flexible endoscopes. There is currently insufficient evidence on the feasibility and utility of cultures. Researchers evaluated a preassembled toolkit for collecting and processing samples from endoscopes. Methods: A pilot study was performed in a large academic medical center. A toolkit was used to aseptically sample biopsy ports and suction/biopsy channels of 5 gastroscopes, 5 colonoscopes, and 5 bronchoscopes after full reprocessing. Blinded specimens were packaged and transported on icepacks to a reference laboratory that used standard methodologies for microbial cultures. Results: The laboratory detected bacteria in samples from 60% of patient-ready endoscopes, including gram-positive and gram-negative species. Viable microbes (<10 CFU) were recovered from 2 gastroscopes, 3 colonoscopes, and 4 bronchoscopes. Stenotrophomonas maltophilia and Delftia acidovorans were recovered from all 3 endoscope types. Subsequent environmental testing detected S maltophilia in the reprocessing rinse water. Conclusions: A preassembled toolkit facilitated the aseptic collection of samples for culturing by a reference laboratory that detected viable microbes on fully reprocessed endoscopes. Speciation allowed identification of potential pathogens and a possible common contamination source, demonstrating that microbial cultures may have value even when colony counts are low. © 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
* Address correspondence to Cori L. Ofstead, MSPH, 400 Selby Ave, Suite V, Blair Arcade West, St Paul, MN 55102. This work was supported in part by STERIS Corporation, which provided funding and materials to Ofstead & Associates, Inc, for this study. STERIS did not have access to the data and was not involved in the preparation of this manuscript. Additional research support was provided by University of Minnesota Health and Ofstead & Associates, Inc. No monetary compensation was received by the physicians or staff at University of Minnesota or their departments for participating in the research or writing of the manuscript. Conflicts of Interest: CLO is employed by Ofstead & Associates, Inc, which has received research funding and speaking honoraria related to infection prevention from STERIS Corporation, 3M Company, Medivators, HealthMark Industries, Boston Scientific, invendo medical, and Advanced Sterilization Products. EMD, JEE, MRA, and HPW are employed by Ofstead & Associates, Inc.
Gastrointestinal endoscopes can harbor organic residue and viable microbes despite reprocessing in accordance with current guidelines.1-4 Although the risk of infection associated with contaminated endoscopes is unknown,5 high attack rates and patient deaths have been documented in recent endoscopy-associated outbreaks of multidrug-resistant organisms.3,4,6 In the wake of these outbreaks, the US Food and Drug Administration recommended that health care facilities perform routine microbial cultures on samples from duodenoscopes to mitigate pathogen transmission.7 In March 2015, the US Centers for Disease Control and Prevention released interim guidance for conducting duodenoscope cultures.8 The American Society for Microbiology has recommended that cultures be performed by external reference laboratories because they may be better equipped than internal clinical labs in health care facilities to successfully conduct cultures.9
0196-6553/© 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2016.01.017
ARTICLE IN PRESS 2
C.L. Ofstead et al. / American Journal of Infection Control ■■ (2016) ■■-■■
To support the implementation of these recommendations in the field, we evaluated the clinical feasibility and value of using a preassembled toolkit to aseptically collect samples from colonoscopes, gastroscopes, and bronchoscopes for microbial cultures conducted by an offsite reference laboratory. METHODS Setting This study was conducted in the Endoscopy Department at the University of Minnesota Medical Center (Minneapolis, MN), where both gastrointestinal and respiratory endoscopes are reprocessed. The University of Minnesota Institutional Review Board granted a waiver for this study because it did not involve human subjects. During the study period, procedures in this institution were performed using Olympus gastroscopes (models GIFXP190N and GIFHQ190), colonoscopes (models CFHQ190L and PCFH190L), and bronchoscopes (models BF1TH190 and BFH190) (Olympus America, Center Valley, PA).
Table 1 Sampling kit contents Material 120-mL bottle sterile water Remel BactiSwab #1275* 60-mL sterile syringe 5-cm long × 0.8-0.9-cm diameter flexible connection tubing 120-mL sterile urine cup Styrofoam transportation container Cold packs Paraffin film strips
Quantity 1 3 3 3 3 1 2 3
*Remel Inc, Lenexa, KS.
pling was performed by 2 researchers with prior experience as operating room nurses, with assistance from other members of the research team. Researchers wore impermeable gowns, face shields, masks, shoe covers, and hair covers. Sterile gloves were worn while handling endoscopes and collecting samples. After sampling each endoscope, environment surfaces were disinfected, disposable pads were changed, and researchers performed hand hygiene and personal protective changes.
Reprocessing steps Sampling Reprocessing began with bedside precleaning immediately after case completion. A trained technician used a precleaning kit (Compliance Endokit; EndoChoice Inc, Alpharetta, GA) to wipe the external surfaces of the endoscopes with disposable sponges and flush detergent through the suction/biopsy (SB) channels in the procedure room. The endoscopes were then transported to a dedicated reprocessing room for leak testing, cleaning, and high-level disinfection (HLD). The external surfaces were wiped and the channels were brushed before the endoscope was placed in an automated endoscope reprocessor (AER) (MEDIVATORS Advantage Plus Endoscope Reprocessing System; MEDIVATORS, Inc, Minneapolis, MN). The AER performed automated cleaning (Intercept Detergent; MEDIVATORS, Inc) and HLD with peracetic acid (Rapicide PA 30°C High-Level Disinfectant; MEDIVATORS, Inc, Minneapolis, MN). The high-level disinfectant’s minimum effective concentration was verified at the end of each cycle in accordance with the AER manufacturer’s instructions. Following HLD, the AER flushed 10 mL isopropyl alcohol through the channels and purged them with forced air to aid the drying process. Disinfected endoscopes were wiped down with a lint-free towel and stored vertically. Researchers observed reprocessing practices and used a checklist to document adherence with reprocessing policies. Toolkit A preassembled sampling toolkit was used with a detailed protocol for aseptic collection and packaging to assess contamination levels on patient-ready endoscopes. The contents of the sampling kit were selected by researchers in collaboration with personnel from the reference laboratory (Biotest Laboratories, Inc, Brooklyn Park, MN). Decisions about the sampling kits’ contents were based on scientific literature and researchers’ previous experience with sampling and conducting cultures (Table 1).1,10-12 The sampling kits were assembled by the laboratory and each kit contained enough materials to collect samples from 3 endoscopes. Aseptic technique Samples were collected in a dedicated procedure room that had been thoroughly cleaned before study initiation. All surfaces used for endoscope sampling were disinfected using CaviWipes (Metrex Research LLC, Orange, CA) and draped with disposable pads. Sam-
Reprocessing personnel identified a convenience sample of patient-ready endoscopes for this pilot study. Researchers sampled biopsy ports and SB channels on 5 gastroscopes, 5 colonoscopes, and 5 bronchoscopes reprocessed in the endoscopy unit. Positive and negative controls were used to verify the effectiveness of aseptic technique and the sensitivity of culturing methods. Sterile water and a swab of an autoclaved wire cutter served as negative controls. For the positive controls, channel effluent and a biopsy port swab were taken from a clinically used gastroscope before manual cleaning. To evaluate the potential influence of the toolkit on workflow and efficiency, each sampling event was timed with a stopwatch. Biopsy ports were sampled for culturable microbes using a sterile sample collection and transport device (BactiSwab Gel Collection and Transport Systems; Remel Inc, Lenexa, KS), which consists of a rayon swab with a plastic shaft placed into a polypropylene tube containing a nonnutritive, charcoal-based media designed to maintain specimen viability during transport. Researchers swabbed inside the biopsy port for 30 seconds before inserting the swab into its tube and securing it in accordance with the manufacturer’s instructions for use. The SB channel was sampled using a flush-only method previously described by Alfa et al.10 A sterile 60-mL syringe was used to draw up 30 mL sterile water, followed by 20 mL air. The syringe was connected to the biopsy port using the connection tubing. The sterile water was injected through the SB lumen, followed by an air flush, and collected in a sterile urine cup at the distal end. The urine cup was capped and sealed with a plastic paraffin film (Parafilm; Bemis Company, Inc, Oshkosh, WI). The samples were labeled using a predetermined blinding protocol and packaged in sealed biohazard bags, which were placed in transportation coolers containing cold packs. Coolers were delivered to the reference laboratory within 3 hours of sample collection. Cultures The reference laboratory extracted samples from the swabs in 100 mL sterile buffered water with 0.02% polysorbate 80, which was mechanically shaken for 30 minutes. The extract was filtered through 0.45 μm nitrocellulose filters. The filters were rinsed with an additional 100 mL sterile buffered water with 0.02% polysorbate 80 and plated on tryptic soy agar.
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The channel effluent samples were filtered through 0.22 μm nitrocellulose filters. The filters were rinsed with an additional 100 mL sterile buffered water with 0.02% polysorbate 80 and plated on trypic soy agar. All tryptic soy agar plates were incubated aerobically for 3-5 days in an incubator maintained at 30°C-35°C. Longer incubation times were used as necessary to foster growth of slowly growing colonies. Growth was quantified and reported in colony forming units. Following colony isolation, Gram stains were conducted and speciation was performed using matrix-assisted laser desorption ionization-time of flight mass spectroscopy with ribosomal protein analysis. This method involves matching the peptide mass fingerprint of the unknown sample to the fingerprint for a known sample. It is relatively quick and economical, and is considered useful for environment and clinical samples. The main limitation of matrixassisted laser desorption ionization-time of flight mass spectroscopy is that the system can only identify microbes when there is a known reference sample in the database.
Table 2 Time required for sampling the biopsy port and suction/biopsy channel of each endoscope Endoscope
RESULTS Patient-ready endoscopes had been stored for a maximum of 4 days (range, 0-4 days) before sampling. The average time required for researchers to collect samples from the biopsy port and SB channel was 2 minutes, 43 seconds (range, 1:37-9:13) (Table 2). Neither of the negative controls yielded any microbial growth. Gram-positive and gram-negative bacteria (Neisseria flavescens/ perflava, N perflava, and Rothia mucilaginosa) were found in samples from the biopsy port (86 CFU) and the SB channel (2,366 CFU) of the positive control. The laboratory detected growth on 9 of the 15 patient-ready endoscopes tested (60%), including 2 gastroscopes, 3 colonoscopes, and 4 bronchoscopes (Table 3). Biopsy ports and SB channels both yielded positive growth in 33% of samples. Samples with growth yielded low quantities (< 10 CFU) of gram-positive and gram-negative bacteria. Species found on patient-ready endoscopes included Cupriavidus metallidurans, Delftia acidovorans, N flavescens, R mucilaginosa, Staphylococcus epidermidis, and Stenotrophomonas maltophilia. Two species of gram-negative bacteria, D acidovorans and Stenotrophomonas maltophilia, were recovered from all 3 endoscope types (ie, bronchoscopes, gastroscopes, and colonoscopes). Table 4 provides additional information about these microbes.
Sampling time, min:sec
Gastroscope 1 Gastroscope 2* Gastroscope 3 Gastroscope 4 Gastroscope 5 Colonoscope 1 Colonoscope 2 Colonoscope 3 Colonoscope 4 Colonoscope 5 Bronchoscope 1 Bronchoscope 2 Bronchoscope 3 Bronchoscope 4 Bronchoscope 5 Range (min, max) Mean Median
1:58 9:13 2:43 2:06 2:06 1:55 1:37 4:12 2:01 2:00 1:47 3:37 1:38 1:51 2:01 1:37, 9:13 2:43 2:01
*The first endoscope sampled during this study.
DISCUSSION The sample collection protocol and preassembled toolkit facilitated aseptic collection of samples for microbial cultures and speciation conducted at an offsite reference laboratory. There was a brief learning curve associated with using the toolkit, and sampling required less time as researchers gained experience. The average time required to collect samples (<3 minutes) suggests that a preassembled sampling toolkit could be incorporated into routine practice in reprocessing units without significantly hindering workflow or efficiency. There was no growth on the samples from the negative controls, which verifies that samples were not contaminated. Low quantities of viable microbes were detected in samples obtained from gastroscopes, colonoscopes, and bronchoscopes. Laboratory per-
Table 3 Culture results by endoscope Endoscope Gastroscope 1 Gastroscope 2 Gastroscope 3 Gastroscope 4 Gastroscope 5 Colonoscope 1* Colonoscope 2 Colonoscope 3 Colonoscope 4 Colonoscope 5* Bronchoscope 1 Bronchoscope 2 Bronchoscope 3† Bronchoscope 4† Bronchoscope 5 Positive control‡ Negative controls
3
Biopsy port, CFU
Suction/biopsy channel, CFU
Species identification
0 0 0 0 5 0 0 0 0 5 0 1 0 1 1 86 0§
0 0 0 2 0 0 0 2 4 0 0 1 2 0 0 2,366 0‖
NA NA NA Neisseria flavescens, Cupriavidus metallidurans Delftia acidovorans, Stenotrophomonas maltophilia NA NA Cupriavidus metallidurans, Delftia acidovorans Neisseria flavescens, Cupriavidus metallidurans Delftia acidovorans, Stenotrophomonas maltophilia, Cupriavidus metallidurans NA Delftia acidovorans, Rothia mucilaginosa Stenotrophomonas maltophilia Staphylococcus epidermidis Staphylococcus epidermidis Rothia mucilaginosa, Neisseria flavescens/perflava. Neisseria perflava NA
NA, not applicable. *Pediatric endoscope. † Used in the intensive care unit. ‡ Clinically used gastroscope (precleaned at bedside). §Sterile wire cutter. ‖ Sterile water.
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Table 4 Characteristics of bacteria identified on patient-ready endoscopes Microbes identified
Categorization
Cupriavidus metallidurans Delftia acidovorans (also known as Pseudomonas acidovorans) Neisseria flavescens
Gram negative Gram negative, nonfermentative Gram negative
Rothia mucilaginosa (also known as Micrococcus mucilaginosa) Staphylococcus epidermidis Stenotrophomonas maltophilia (previously classified as Pseudomonas)
Gram positive Gram positive Gram negative, nonfermentative
sonnel performed Gram staining and speciation on all samples with growth. This provided valuable information because 2 gramnegative, nonfermentative organisms (Stenotrophomonas maltophilia and D acidovorans) were found on all 3 endoscope types. These organisms were not recovered from the positive control (a gastroscope sampled before manual cleaning), which suggested the possibility of a common contamination source encountered after manual cleaning. According to guidelines published by the Gastroenterological Society of Australia and the European Society of Gastroenterology and the European Society of Gastroenterology Endoscopy Nurses and Associates, the growth of indicator species such as Pseudomonas or other nonfermentative gram-negative bacteria is concerning and should prompt immediate action.13,14 In response to these results, study site personnel obtained samples from environment surfaces in the reprocessing suite. These samples were cultured by the institution’s clinical laboratory, which identified Stenotrophomonas maltophilia in samples of AER rinse water. In response, the AERs were disinfected and their filters were changed. A schedule for conducting routine microbial cultures of AERs is under development. Instances of pathogen transmission associated with contaminated duodenoscopes used in endoscopic retrograde cholangiopancreatography procedures have been well documented. 3,4,6,15-17 In several of these incidents, pathogens were cultured from elevator wire channels of duodenoscopes4,6 or infection transmission was attributed to improperly cleaned elevator mechanisms.4,17 Outbreaks have also been associated with endoscopes that do not have elevator wire channels, including gastroscopes, cystoscopes, and bronchoscopes.18-20 Persistent bacteria on a gastroscope was genetically tied to an outbreak of extended-spectrum β-lactamase-producing Pseudomonas aeruginosa, during which 4 patients contracted the outbreak strain. 18 A bronchoscope-associated outbreak of carbapenem-resistant Klebsiella pneumoniae occurred in the intensive care unit of a German hospital. The outbreak strain was recovered from a bronchoscope that had been used on 2 infected patients. Three subsequent patients became infected with carbapenem-resistant K pneumoniae after undergoing bronchoscopies with this device, despite reprocessing in accordance with guidelines. 19 In New Mexico, an improperly reprocessed cystoscope was implicated in an outbreak of P aeruginosa infections. Environmental sampling identified P aeruginosa on a brush used to clean the cystoscope channel, in water used for rinsing the endoscope, and in 3 samples of sterile water flushed through the cystoscope channel. The strain was genetically matched to P aeruginosa cultured from patients who had previously undergone cystoscopy procedures at the facility.20 In the present study, viable microbes were recovered from 60% of endoscopes. Bacteria were found in samples from all 3 types of endoscopes (ie, colonoscopes, gastroscopes, and bronchoscopes). These endoscopes harbored viable microbes despite being stored for brief periods (0-4 days) that were shorter than the maximum
Other characteristics Environmental/aquatic, rarely pathogenic Environmental, rarely pathogenic Host-associated, commensal flora of upper respiratory tract, infections reported in immunocompromised patients Host-associated, normal microflora of upper respiratory system, opportunistic pathogen, infections reported in immunocompromised patients Host-associated, normal microflora of skin and mucous membranes Environmental/aquatic, biofilm-forming bacterium, opportunistic pathogen, infections reported in immunocompromised patients, multidrug resistant
storage times recommended by current reprocessing guidelines.21,22 Reprocessing included bedside precleaning with enzymatic detergent, leak testing, manual brushing, automated cleaning and HLD in an AER, and an alcohol flush followed by an air purge in the AER to aid in drying the endoscopes. The findings from this study are similar to previous research1,2 and indicate that current reprocessing methods do not reliably eliminate residual contamination and viable microbes from colonoscopes, gastroscopes, or bronchoscopes. This pilot study has several limitations. Sample collection occurred at a single site, and findings may not be generalizable to the larger field. A flush-only method was employed to collect channel samples, which is less rigorous than methods employed in past studies.1,11,17 However, Alfa et al10 found that a flush-only method was adequate because more than 85% of viable microbes and organic debris were recovered during an initial round of harvesting. Microbial samples were stored in a transportation container with cold packs for up to 3 hours before delivery to the reference laboratory, which could have affected sample viability. CONCLUSIONS The findings of this pilot study demonstrate the feasibility and value of using a preassembled culturing toolkit to identify bacterial contamination on patient-ready endoscopes. The external reference laboratory detected viable microbes in samples collected from gastroscopes, colonoscopes, and bronchoscopes that were fully reprocessed. Speciation led to identification of a possible common contamination source in the reprocessing room, demonstrating that cultures may have value even when colony counts are low. The identification of a waterborne pathogen (Stenotrophomonas maltophilia) in samples from endoscopes and AER rinse water also prompted reconsideration of endoscope drying practices in this facility, which have since been revised to provide more thorough drying. Additional research is needed to determine whether a similar toolkit could be implemented successfully in other settings to support routine surveillance of endoscope reprocessing effectiveness. Acknowledgments The authors thank the leadership of University of Minnesota Health and staff in the Endoscopy Department who provided researchers with laboratory space and logistical support during this study. The authors also thank Catherine Rocco, MSN, RN, CNOR, for her assistance with sample collection; Otis Heymann, BA, and Ellen Johnson, BAS, for providing editorial assistance; and Lisa Mattson, MBA, for handling logistics related to the study. Andrew Streifel, MPH, provided expertise regarding waterborne pathogens and handled the environment cultures. The authors especially thank the employees at the study site who coordinated the identification of study endoscopes, accommodated our presence in the unit, and rereprocessed the endoscopes after we obtained samples.
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References 1. Ofstead CL, Wetzler HP, Doyle EM, Rocco CK, Visrodia KH, Baron TH, et al. Persistent contamination on colonoscopes and gastroscopes detected by biologic cultures and rapid indicators despite reprocessing performed in accordance with guidelines. Am J Infect Control 2015;43:794-801. 2. Alfa MJ, Sepehri S, Olson N, Wald A. Establishing a clinically relevant bioburden benchmark: a quality indicator for adequate reprocessing and storage of flexible gastrointestinal endoscopes. Am J Infect Control 2012;40:233-6. 3. Epstein L, Hunter JC, Arwady MA, Tsai V, Stein L, Gribogiannis M, et al. New Delhi metallo-beta-lactamase-producing carbapenem-resistant Escherichia coli associated with exposure to duodenoscopes. JAMA 2014;312:1447-55. 4. Wendorf KA, Kay M, Baliga C, Weissman SJ, Gluck M, Verma P, et al. Endoscopic retrograde cholangiopancreatography–associated AmpC Escherichia coli outbreak. Infect Control Hosp Epidemiol 2015;36:634-42. 5. Ofstead CL, Dirlam Langlay AM, Mueller NJ, Tosh PK, Wetzler HP. Re-evaluating endoscopy-associated infection risk estimates and their implications. Am J Infect Control 2013;41:734-6. 6. Smith ZL, Oh YS, Saeian K, Edmiston CE Jr, Khan AH, Massey BT, et al. Transmission of carbapenem-resistant enterobacteriaceae during ERCP: time to revisit the current reprocessing guidelines. Gastrointest Endosc 2015;81:1041-5. 7. U.S. Food and Drug Administration. Supplemental measures to enhance duodenoscope reprocessing: FDA safety communication. FDA Safety Communications. Available from: http://www.fda.gov/MedicalDevices/ Safety/AlertsandNotices/ucm454766.htm. Accessed August 4, 2015. 8. Centers for Disease Control and Prevention. Interim duodenoscope surveillance protocol—interim protocol for healthcare facilities regarding surveillance for bacterial contamination of duodenoscopes after reprocessing. Available from: http://www.cdc.gov/hai/organisms/cre/cre-duodenoscope-surveillance-protocol .html. Accessed April 3, 2015. 9. Sharp SE. On the question of culturing of duodenoscopes. American Society for Microbiology. Available from: https://www.asm.org/index.php/component/ content/article/98-policy/issues/93456-lp-4-15. Accessed April 9, 2015. 10. Alfa MJ, Fatima I, Olson N. Validation of adenosine triphosphate to audit manual cleaning of flexible endoscope channels. Am J Infect Control 2013;41:245-8. 11. Visrodia KH, Ofstead CL, Yellin HL, Wetzler HP, Tosh PK, Baron TH. The use of rapid indicators for the detection of organic residues on clinically used
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gastrointestinal endoscopes with and without visually apparent debris. Infect Control Hosp Epidemiol 2014;35:987-94. Fushimi R, Takashina M, Yoshikawa H, Kobayashi H, Okubo T, Nakata S, et al. Comparison of adenosine triphosphate, microbiological load, and residual protein as indicators for assessing the cleanliness of flexible gastrointestinal endoscopes. Am J Infect Control 2013;41:161-4. Gastroenterological Society of Australia. Infection Control in Endoscopy. Clinical Update. 3rd ed. Victoria, Australia: Digestive Health Foundation; 2011. Beilenhoff U, Neumann CS, Rey JF, Biering H, Blum R, Schmidt V, et al. ESGESGENA guideline for quality assurance in reprocessing: microbiological surveillance testing in endoscopy. Endoscopy 2007;39:175-81. Carbonne A, Thiolet JM, Fournier S, Fortineau N, Kassis-Chikhani N, Boytchev I, et al. Control of a multi-hospital outbreak of KPC-producing Klebsiella pneumoniae type 2 in France, September to October 2009. Euro Surveill 2010;15:1-6. Kovaleva J, Meessen NE, Peters FT, Been MH, Arends JP, Borgers RP, et al. Is bacteriologic surveillance in endoscope reprocessing stringent enough? Endoscopy 2009;41:913-6. Aumeran C, Poincloux L, Souweine B, Robin F, Laurichesse H, Baud O, et al. Multidrug-resistant Klebsiella pneumoniae outbreak after endoscopic retrograde cholangiopancreatography. Endoscopy 2010;42:895-9. Bajolet O, Ciocan D, Vallet C, de Champs C, Vernet-Garnier V, Guillard T, et al. Gastroscopy-associated transmission of extended-spectrum beta-lactamase-producing Pseudomonas aeruginosa. J Hosp Infect 2013;83: 341-3. Zweigner J, Gastmeier P, Kola A, Klefisch FR, Schweizer C, Hummel M. A carbapenem-resistant Klebsiella pneumoniae outbreak following bronchoscopy. Am J Infect Control 2014;42:936-7. Wendelboe AM, Baumbach J, Blossom DB, Frank P, Srinivasan A, Sewell CM. Outbreak of cystoscopy related infections with Pseudomonas aeruginosa: New Mexico, 2007. J Urol 2008;180:588-92, discussion 592. Association of periOperative Registered Nurses. Recommended practices for cleaning and processing flexible endoscopes and endoscope accessories. AORN J 2003;77,434-84. Petersen BT, Chennat J, Cohen J, Cotton PB, Greenwald DA, Kowalski TE, et al. Multisociety Guideline on Reprocessing Flexible GI endoscopes: 2011. Infect Control Hosp Epidemiol 2011;32:527-37.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
j o u r n a l h o m e p a g e : w w w. a j i c j o u r n a l . o r g
Original Research Article
Practical toolkit for monitoring endoscope reprocessing effectiveness: Identification of viable bacteria on gastroscopes, colonoscopes, and bronchoscopes Cori L. Ofstead MSPH a,*, Evan M. Doyle BS a, John E. Eiland MS, RN a, Miriam R. Amelang BA a, Harry P. Wetzler MD, MSPH a, Dawn M. England MPH, CPHQ b, Kristin M. Mascotti MD, CPE c, Michael J. Shaw MD d a
Ofstead & Associates, Inc, St Paul, MN Department of Infection Prevention, University of Minnesota Health, Minneapolis, MN c Department of Clinical Quality Improvement, University of Minnesota Health, Minneapolis, MN d Division of Gastroenterology, Department of Medicine, University of Minnesota Medical School, Minneapolis, MN b
Key Words: High-level disinfection Microbial cultures Stenotrophomonas maltophilia
Background: Experts have recommended microbiologic surveillance by external reference laboratories for certain flexible endoscopes. There is currently insufficient evidence on the feasibility and utility of cultures. Researchers evaluated a preassembled toolkit for collecting and processing samples from endoscopes. Methods: A pilot study was performed in a large academic medical center. A toolkit was used to aseptically sample biopsy ports and suction/biopsy channels of 5 gastroscopes, 5 colonoscopes, and 5 bronchoscopes after full reprocessing. Blinded specimens were packaged and transported on icepacks to a reference laboratory that used standard methodologies for microbial cultures. Results: The laboratory detected bacteria in samples from 60% of patient-ready endoscopes, including gram-positive and gram-negative species. Viable microbes (<10 CFU) were recovered from 2 gastroscopes, 3 colonoscopes, and 4 bronchoscopes. Stenotrophomonas maltophilia and Delftia acidovorans were recovered from all 3 endoscope types. Subsequent environmental testing detected S maltophilia in the reprocessing rinse water. Conclusions: A preassembled toolkit facilitated the aseptic collection of samples for culturing by a reference laboratory that detected viable microbes on fully reprocessed endoscopes. Speciation allowed identification of potential pathogens and a possible common contamination source, demonstrating that microbial cultures may have value even when colony counts are low. © 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
* Address correspondence to Cori L. Ofstead, MSPH, 400 Selby Ave, Suite V, Blair Arcade West, St Paul, MN 55102. This work was supported in part by STERIS Corporation, which provided funding and materials to Ofstead & Associates, Inc, for this study. STERIS did not have access to the data and was not involved in the preparation of this manuscript. Additional research support was provided by University of Minnesota Health and Ofstead & Associates, Inc. No monetary compensation was received by the physicians or staff at University of Minnesota or their departments for participating in the research or writing of the manuscript. Conflicts of Interest: CLO is employed by Ofstead & Associates, Inc, which has received research funding and speaking honoraria related to infection prevention from STERIS Corporation, 3M Company, Medivators, HealthMark Industries, Boston Scientific, invendo medical, and Advanced Sterilization Products. EMD, JEE, MRA, and HPW are employed by Ofstead & Associates, Inc.
Gastrointestinal endoscopes can harbor organic residue and viable microbes despite reprocessing in accordance with current guidelines.1-4 Although the risk of infection associated with contaminated endoscopes is unknown,5 high attack rates and patient deaths have been documented in recent endoscopy-associated outbreaks of multidrug-resistant organisms.3,4,6 In the wake of these outbreaks, the US Food and Drug Administration recommended that health care facilities perform routine microbial cultures on samples from duodenoscopes to mitigate pathogen transmission.7 In March 2015, the US Centers for Disease Control and Prevention released interim guidance for conducting duodenoscope cultures.8 The American Society for Microbiology has recommended that cultures be performed by external reference laboratories because they may be better equipped than internal clinical labs in health care facilities to successfully conduct cultures.9
0196-6553/© 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2016.01.017
ARTICLE IN PRESS 2
C.L. Ofstead et al. / American Journal of Infection Control ■■ (2016) ■■-■■
To support the implementation of these recommendations in the field, we evaluated the clinical feasibility and value of using a preassembled toolkit to aseptically collect samples from colonoscopes, gastroscopes, and bronchoscopes for microbial cultures conducted by an offsite reference laboratory. METHODS Setting This study was conducted in the Endoscopy Department at the University of Minnesota Medical Center (Minneapolis, MN), where both gastrointestinal and respiratory endoscopes are reprocessed. The University of Minnesota Institutional Review Board granted a waiver for this study because it did not involve human subjects. During the study period, procedures in this institution were performed using Olympus gastroscopes (models GIFXP190N and GIFHQ190), colonoscopes (models CFHQ190L and PCFH190L), and bronchoscopes (models BF1TH190 and BFH190) (Olympus America, Center Valley, PA).
Table 1 Sampling kit contents Material 120-mL bottle sterile water Remel BactiSwab #1275* 60-mL sterile syringe 5-cm long × 0.8-0.9-cm diameter flexible connection tubing 120-mL sterile urine cup Styrofoam transportation container Cold packs Paraffin film strips
Quantity 1 3 3 3 3 1 2 3
*Remel Inc, Lenexa, KS.
pling was performed by 2 researchers with prior experience as operating room nurses, with assistance from other members of the research team. Researchers wore impermeable gowns, face shields, masks, shoe covers, and hair covers. Sterile gloves were worn while handling endoscopes and collecting samples. After sampling each endoscope, environment surfaces were disinfected, disposable pads were changed, and researchers performed hand hygiene and personal protective changes.
Reprocessing steps Sampling Reprocessing began with bedside precleaning immediately after case completion. A trained technician used a precleaning kit (Compliance Endokit; EndoChoice Inc, Alpharetta, GA) to wipe the external surfaces of the endoscopes with disposable sponges and flush detergent through the suction/biopsy (SB) channels in the procedure room. The endoscopes were then transported to a dedicated reprocessing room for leak testing, cleaning, and high-level disinfection (HLD). The external surfaces were wiped and the channels were brushed before the endoscope was placed in an automated endoscope reprocessor (AER) (MEDIVATORS Advantage Plus Endoscope Reprocessing System; MEDIVATORS, Inc, Minneapolis, MN). The AER performed automated cleaning (Intercept Detergent; MEDIVATORS, Inc) and HLD with peracetic acid (Rapicide PA 30°C High-Level Disinfectant; MEDIVATORS, Inc, Minneapolis, MN). The high-level disinfectant’s minimum effective concentration was verified at the end of each cycle in accordance with the AER manufacturer’s instructions. Following HLD, the AER flushed 10 mL isopropyl alcohol through the channels and purged them with forced air to aid the drying process. Disinfected endoscopes were wiped down with a lint-free towel and stored vertically. Researchers observed reprocessing practices and used a checklist to document adherence with reprocessing policies. Toolkit A preassembled sampling toolkit was used with a detailed protocol for aseptic collection and packaging to assess contamination levels on patient-ready endoscopes. The contents of the sampling kit were selected by researchers in collaboration with personnel from the reference laboratory (Biotest Laboratories, Inc, Brooklyn Park, MN). Decisions about the sampling kits’ contents were based on scientific literature and researchers’ previous experience with sampling and conducting cultures (Table 1).1,10-12 The sampling kits were assembled by the laboratory and each kit contained enough materials to collect samples from 3 endoscopes. Aseptic technique Samples were collected in a dedicated procedure room that had been thoroughly cleaned before study initiation. All surfaces used for endoscope sampling were disinfected using CaviWipes (Metrex Research LLC, Orange, CA) and draped with disposable pads. Sam-
Reprocessing personnel identified a convenience sample of patient-ready endoscopes for this pilot study. Researchers sampled biopsy ports and SB channels on 5 gastroscopes, 5 colonoscopes, and 5 bronchoscopes reprocessed in the endoscopy unit. Positive and negative controls were used to verify the effectiveness of aseptic technique and the sensitivity of culturing methods. Sterile water and a swab of an autoclaved wire cutter served as negative controls. For the positive controls, channel effluent and a biopsy port swab were taken from a clinically used gastroscope before manual cleaning. To evaluate the potential influence of the toolkit on workflow and efficiency, each sampling event was timed with a stopwatch. Biopsy ports were sampled for culturable microbes using a sterile sample collection and transport device (BactiSwab Gel Collection and Transport Systems; Remel Inc, Lenexa, KS), which consists of a rayon swab with a plastic shaft placed into a polypropylene tube containing a nonnutritive, charcoal-based media designed to maintain specimen viability during transport. Researchers swabbed inside the biopsy port for 30 seconds before inserting the swab into its tube and securing it in accordance with the manufacturer’s instructions for use. The SB channel was sampled using a flush-only method previously described by Alfa et al.10 A sterile 60-mL syringe was used to draw up 30 mL sterile water, followed by 20 mL air. The syringe was connected to the biopsy port using the connection tubing. The sterile water was injected through the SB lumen, followed by an air flush, and collected in a sterile urine cup at the distal end. The urine cup was capped and sealed with a plastic paraffin film (Parafilm; Bemis Company, Inc, Oshkosh, WI). The samples were labeled using a predetermined blinding protocol and packaged in sealed biohazard bags, which were placed in transportation coolers containing cold packs. Coolers were delivered to the reference laboratory within 3 hours of sample collection. Cultures The reference laboratory extracted samples from the swabs in 100 mL sterile buffered water with 0.02% polysorbate 80, which was mechanically shaken for 30 minutes. The extract was filtered through 0.45 μm nitrocellulose filters. The filters were rinsed with an additional 100 mL sterile buffered water with 0.02% polysorbate 80 and plated on tryptic soy agar.
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The channel effluent samples were filtered through 0.22 μm nitrocellulose filters. The filters were rinsed with an additional 100 mL sterile buffered water with 0.02% polysorbate 80 and plated on trypic soy agar. All tryptic soy agar plates were incubated aerobically for 3-5 days in an incubator maintained at 30°C-35°C. Longer incubation times were used as necessary to foster growth of slowly growing colonies. Growth was quantified and reported in colony forming units. Following colony isolation, Gram stains were conducted and speciation was performed using matrix-assisted laser desorption ionization-time of flight mass spectroscopy with ribosomal protein analysis. This method involves matching the peptide mass fingerprint of the unknown sample to the fingerprint for a known sample. It is relatively quick and economical, and is considered useful for environment and clinical samples. The main limitation of matrixassisted laser desorption ionization-time of flight mass spectroscopy is that the system can only identify microbes when there is a known reference sample in the database.
Table 2 Time required for sampling the biopsy port and suction/biopsy channel of each endoscope Endoscope
RESULTS Patient-ready endoscopes had been stored for a maximum of 4 days (range, 0-4 days) before sampling. The average time required for researchers to collect samples from the biopsy port and SB channel was 2 minutes, 43 seconds (range, 1:37-9:13) (Table 2). Neither of the negative controls yielded any microbial growth. Gram-positive and gram-negative bacteria (Neisseria flavescens/ perflava, N perflava, and Rothia mucilaginosa) were found in samples from the biopsy port (86 CFU) and the SB channel (2,366 CFU) of the positive control. The laboratory detected growth on 9 of the 15 patient-ready endoscopes tested (60%), including 2 gastroscopes, 3 colonoscopes, and 4 bronchoscopes (Table 3). Biopsy ports and SB channels both yielded positive growth in 33% of samples. Samples with growth yielded low quantities (< 10 CFU) of gram-positive and gram-negative bacteria. Species found on patient-ready endoscopes included Cupriavidus metallidurans, Delftia acidovorans, N flavescens, R mucilaginosa, Staphylococcus epidermidis, and Stenotrophomonas maltophilia. Two species of gram-negative bacteria, D acidovorans and Stenotrophomonas maltophilia, were recovered from all 3 endoscope types (ie, bronchoscopes, gastroscopes, and colonoscopes). Table 4 provides additional information about these microbes.
Sampling time, min:sec
Gastroscope 1 Gastroscope 2* Gastroscope 3 Gastroscope 4 Gastroscope 5 Colonoscope 1 Colonoscope 2 Colonoscope 3 Colonoscope 4 Colonoscope 5 Bronchoscope 1 Bronchoscope 2 Bronchoscope 3 Bronchoscope 4 Bronchoscope 5 Range (min, max) Mean Median
1:58 9:13 2:43 2:06 2:06 1:55 1:37 4:12 2:01 2:00 1:47 3:37 1:38 1:51 2:01 1:37, 9:13 2:43 2:01
*The first endoscope sampled during this study.
DISCUSSION The sample collection protocol and preassembled toolkit facilitated aseptic collection of samples for microbial cultures and speciation conducted at an offsite reference laboratory. There was a brief learning curve associated with using the toolkit, and sampling required less time as researchers gained experience. The average time required to collect samples (<3 minutes) suggests that a preassembled sampling toolkit could be incorporated into routine practice in reprocessing units without significantly hindering workflow or efficiency. There was no growth on the samples from the negative controls, which verifies that samples were not contaminated. Low quantities of viable microbes were detected in samples obtained from gastroscopes, colonoscopes, and bronchoscopes. Laboratory per-
Table 3 Culture results by endoscope Endoscope Gastroscope 1 Gastroscope 2 Gastroscope 3 Gastroscope 4 Gastroscope 5 Colonoscope 1* Colonoscope 2 Colonoscope 3 Colonoscope 4 Colonoscope 5* Bronchoscope 1 Bronchoscope 2 Bronchoscope 3† Bronchoscope 4† Bronchoscope 5 Positive control‡ Negative controls
3
Biopsy port, CFU
Suction/biopsy channel, CFU
Species identification
0 0 0 0 5 0 0 0 0 5 0 1 0 1 1 86 0§
0 0 0 2 0 0 0 2 4 0 0 1 2 0 0 2,366 0‖
NA NA NA Neisseria flavescens, Cupriavidus metallidurans Delftia acidovorans, Stenotrophomonas maltophilia NA NA Cupriavidus metallidurans, Delftia acidovorans Neisseria flavescens, Cupriavidus metallidurans Delftia acidovorans, Stenotrophomonas maltophilia, Cupriavidus metallidurans NA Delftia acidovorans, Rothia mucilaginosa Stenotrophomonas maltophilia Staphylococcus epidermidis Staphylococcus epidermidis Rothia mucilaginosa, Neisseria flavescens/perflava. Neisseria perflava NA
NA, not applicable. *Pediatric endoscope. † Used in the intensive care unit. ‡ Clinically used gastroscope (precleaned at bedside). §Sterile wire cutter. ‖ Sterile water.
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Table 4 Characteristics of bacteria identified on patient-ready endoscopes Microbes identified
Categorization
Cupriavidus metallidurans Delftia acidovorans (also known as Pseudomonas acidovorans) Neisseria flavescens
Gram negative Gram negative, nonfermentative Gram negative
Rothia mucilaginosa (also known as Micrococcus mucilaginosa) Staphylococcus epidermidis Stenotrophomonas maltophilia (previously classified as Pseudomonas)
Gram positive Gram positive Gram negative, nonfermentative
sonnel performed Gram staining and speciation on all samples with growth. This provided valuable information because 2 gramnegative, nonfermentative organisms (Stenotrophomonas maltophilia and D acidovorans) were found on all 3 endoscope types. These organisms were not recovered from the positive control (a gastroscope sampled before manual cleaning), which suggested the possibility of a common contamination source encountered after manual cleaning. According to guidelines published by the Gastroenterological Society of Australia and the European Society of Gastroenterology and the European Society of Gastroenterology Endoscopy Nurses and Associates, the growth of indicator species such as Pseudomonas or other nonfermentative gram-negative bacteria is concerning and should prompt immediate action.13,14 In response to these results, study site personnel obtained samples from environment surfaces in the reprocessing suite. These samples were cultured by the institution’s clinical laboratory, which identified Stenotrophomonas maltophilia in samples of AER rinse water. In response, the AERs were disinfected and their filters were changed. A schedule for conducting routine microbial cultures of AERs is under development. Instances of pathogen transmission associated with contaminated duodenoscopes used in endoscopic retrograde cholangiopancreatography procedures have been well documented. 3,4,6,15-17 In several of these incidents, pathogens were cultured from elevator wire channels of duodenoscopes4,6 or infection transmission was attributed to improperly cleaned elevator mechanisms.4,17 Outbreaks have also been associated with endoscopes that do not have elevator wire channels, including gastroscopes, cystoscopes, and bronchoscopes.18-20 Persistent bacteria on a gastroscope was genetically tied to an outbreak of extended-spectrum β-lactamase-producing Pseudomonas aeruginosa, during which 4 patients contracted the outbreak strain. 18 A bronchoscope-associated outbreak of carbapenem-resistant Klebsiella pneumoniae occurred in the intensive care unit of a German hospital. The outbreak strain was recovered from a bronchoscope that had been used on 2 infected patients. Three subsequent patients became infected with carbapenem-resistant K pneumoniae after undergoing bronchoscopies with this device, despite reprocessing in accordance with guidelines. 19 In New Mexico, an improperly reprocessed cystoscope was implicated in an outbreak of P aeruginosa infections. Environmental sampling identified P aeruginosa on a brush used to clean the cystoscope channel, in water used for rinsing the endoscope, and in 3 samples of sterile water flushed through the cystoscope channel. The strain was genetically matched to P aeruginosa cultured from patients who had previously undergone cystoscopy procedures at the facility.20 In the present study, viable microbes were recovered from 60% of endoscopes. Bacteria were found in samples from all 3 types of endoscopes (ie, colonoscopes, gastroscopes, and bronchoscopes). These endoscopes harbored viable microbes despite being stored for brief periods (0-4 days) that were shorter than the maximum
Other characteristics Environmental/aquatic, rarely pathogenic Environmental, rarely pathogenic Host-associated, commensal flora of upper respiratory tract, infections reported in immunocompromised patients Host-associated, normal microflora of upper respiratory system, opportunistic pathogen, infections reported in immunocompromised patients Host-associated, normal microflora of skin and mucous membranes Environmental/aquatic, biofilm-forming bacterium, opportunistic pathogen, infections reported in immunocompromised patients, multidrug resistant
storage times recommended by current reprocessing guidelines.21,22 Reprocessing included bedside precleaning with enzymatic detergent, leak testing, manual brushing, automated cleaning and HLD in an AER, and an alcohol flush followed by an air purge in the AER to aid in drying the endoscopes. The findings from this study are similar to previous research1,2 and indicate that current reprocessing methods do not reliably eliminate residual contamination and viable microbes from colonoscopes, gastroscopes, or bronchoscopes. This pilot study has several limitations. Sample collection occurred at a single site, and findings may not be generalizable to the larger field. A flush-only method was employed to collect channel samples, which is less rigorous than methods employed in past studies.1,11,17 However, Alfa et al10 found that a flush-only method was adequate because more than 85% of viable microbes and organic debris were recovered during an initial round of harvesting. Microbial samples were stored in a transportation container with cold packs for up to 3 hours before delivery to the reference laboratory, which could have affected sample viability. CONCLUSIONS The findings of this pilot study demonstrate the feasibility and value of using a preassembled culturing toolkit to identify bacterial contamination on patient-ready endoscopes. The external reference laboratory detected viable microbes in samples collected from gastroscopes, colonoscopes, and bronchoscopes that were fully reprocessed. Speciation led to identification of a possible common contamination source in the reprocessing room, demonstrating that cultures may have value even when colony counts are low. The identification of a waterborne pathogen (Stenotrophomonas maltophilia) in samples from endoscopes and AER rinse water also prompted reconsideration of endoscope drying practices in this facility, which have since been revised to provide more thorough drying. Additional research is needed to determine whether a similar toolkit could be implemented successfully in other settings to support routine surveillance of endoscope reprocessing effectiveness. Acknowledgments The authors thank the leadership of University of Minnesota Health and staff in the Endoscopy Department who provided researchers with laboratory space and logistical support during this study. The authors also thank Catherine Rocco, MSN, RN, CNOR, for her assistance with sample collection; Otis Heymann, BA, and Ellen Johnson, BAS, for providing editorial assistance; and Lisa Mattson, MBA, for handling logistics related to the study. Andrew Streifel, MPH, provided expertise regarding waterborne pathogens and handled the environment cultures. The authors especially thank the employees at the study site who coordinated the identification of study endoscopes, accommodated our presence in the unit, and rereprocessed the endoscopes after we obtained samples.
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