Gastroscopy-associated transmission of extended-spectrum beta-lactamase-producing Pseudomonas aeruginosa

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Journal of Hospital Infection xxx (2012) 1e3 Available online at www.sciencedirect.com

Journal of Hospital Infection journal homepage: www.elsevierhealth.com/journals/jhin

Short report

Gastroscopy-associated transmission of extended-spectrum beta-lactamase-producing Pseudomonas aeruginosa O. Bajolet a, d, *, D. Ciocan a, C. Vallet a, C. de Champs b, d, V. Vernet-Garnier b, d, T. Guillard b, d, L. Brasme b, G. Thiefin c, d, G. Cadiot c, d, F. Bureau-Chalot a a

Equipe Ope´rationnelle d’Hygie`ne, CHU de Reims, Reims, France Laboratoire de Bacte´riologie-Virologie-Hygie`ne, CHU de Reims, Reims, France c Service d’He´pato-Gastro-Ente´rologie et de Cance´rologie Digestive, CHU de Reims, Reims, France d UFR Me´decine, Universite´ de Reims, Reims, France b

A R T I C L E

I N F O

Article history: Received 4 April 2012 Accepted 24 October 2012 Available online xxx Keywords: Pseudomonas aeruginosa Cross-infection Gastrointestinal endoscopy

S U M M A R Y

An unusual multi-drug-resistant Pseudomonas aeruginosa (MDR-PA) was isolated in four patients whilst hospitalized in a French teaching hospital between May and August 2011. All four patients had undergone an oesophago-gastro-duodenoscopy with the same gastroscope over a five-month period. This endoscope was associated with a culture positive for the MDR-PA. Observations of endoscope reprocessing identified deviations from the agreed processes: insufficient initial cleaning, shortening of the immersion time and brushing time, insufficient channel flushing, and inadequate drying prior to storage. Since withdrawing the gastroscope and institution of strict adherence to the agreed processes, no other MDR-PA cases have been isolated. ª 2012 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved.

Introduction

Methods

Patient-to-patient transmission of pathogens during endoscopy has been extremely rare since the publication of endoscope reprocessing guidelines.1,2 Nosocomial transmission of multi-drug-resistant Pseudomonas aeruginosa (MDR-PA) following endoscopic retrograde cholangiopancreatography has been described previously.3,4 This paper reports an outbreak of an MDR-PA related to a contaminated gastroscope.

A 54-year-old patient was admitted to an intensive care unit (ICU) with pneumonia in July 2011. An extended-spectrum b-lactamase (ESBL)-producing MDR-PA was isolated from his bronchoalveolar lavage. The microbiology database identified another ESBL-producing P. aeruginosa isolate from a patient with a psoas haematoma, admitted to another ICU in May 2011. Being an uncommon strain at the hospital, a retrospective review of medical records was undertaken. During the investigation, the MDR-PA was isolated from two further patients. Review of the notes for these four cases revealed the only common source to be endoscopic procedures performed over a five-month period with the same gastroscope on the same ward. This gastroscope was withdrawn from use on 29 July 2011 and an audit of endoscope reprocessing was undertaken.

* Corresponding author. Address: Equipe Ope ´rationnelle d’Hygie `ne Hospitalie `re, CHU de Reims, 45 rue Cognacq Jay, 51092 Reims Cedex, France. Tel.: þ33 3 26 78 37 03; fax: þ33 3 26 78 85 66. E-mail address: [email protected] (O. Bajolet).

0195-6701/$ e see front matter ª 2012 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jhin.2012.10.016 Please cite this article in press as: Bajolet O, et al., Gastroscopy-associated transmission of extended-spectrum beta-lactamase-producing Pseudomonas aeruginosa, Journal of Hospital Infection (2012), http://dx.doi.org/10.1016/j.jhin.2012.10.016

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O. Bajolet et al. / Journal of Hospital Infection xxx (2012) 1e3

Gastrointestinal endoscope reprocessing was performed in accordance with French guidelines.5 Endoscopes were cleaned manually by trained staff, followed by reprocessing in a washerdisinfector. The disinfectant used was peracetic acid, and drying was performed with medical air under pressure. Endoscopes were stored between sterile sheets in a horizontal position. Environmental investigations included microbiological testing of water used during reprocessing, tap water used for pre-cleaning, and water used in the washer-disinfector. Endoscope sampling was performed by flushing a sterile solution through the lumen, and passing the fluid collected through a membrane filter; this was subsequently incubated on trypticase soy agar for three days.6 According to the antibiotic resistance phenotype, the genes blaTEM, blaSHV and blaCTx-M were characterized by polymerase chain reaction using specific primers and DNA sequencing as reported previously.7 P. aeruginosa isolates were genotyped by random amplification of polymorphic DNA (RAPD) from the Ready-To-Go RAPD analysis kit, in accordance with the manufacturer’s instructions (GE Healthcare Life Sciences, Chalfont St Giles, UK) using two primers: [5’-d(AAGAGCCCGT)-3’] and [5’-d(AACGCGCAAC)-3’].

MW

1

2

3

4

G

ATCC 27853

Results From May to August 2011, four patients were identified with an MDR-PA. Patient characteristics and sources of the strain are shown in Table I. All patients had received wide-spectrum antimicrobial therapy during their hospitalization. Three of the patients died due to gastrointestinal bleeding (Cases 1, 2 and 3). No deaths were related to the MDR-PA. Review of the patients’ notes revealed that they had all undergone gastroscopy with the same endoscope. This device was new and available for use from January 2011. No damage was noticed at commissioning and microbiological sampling was negative. No subsequent damage was reported. The MDR-PA strain was isolated from this endoscope (>100 colony-forming units/100 mL of wash solution). Other microbiological tests (other gastrointestinal endoscopes, tap water, water from automated reprocessor unit) were negative. All strains were resistant to b-lactams, fluoroquinolones and rifampicin, and were susceptible to aminoglycosides (except Case 2) and colistin. The presence of the blaSHV-2a gene was identified in each strain by polymerase chain reaction and

Figure 1. Random amplified polymorphic DNA analysis of patients (Cases 1, 2, 3 and 4) and gastroscope multi-drug-resistant Pseudomonas aeruginosa isolates (G). MW, molecular weight. ATCC 27853: P. aeruginosa reference strain. Primer 5’-d(AACGCGCAAC)-3’.

sequencing. All P. aeruginosa strains were identical by RAPD (Figure 1). Examination of the maintenance records for the washerdisinfector showed that the cleaning solutions and the filters had been changed in accordance with recommendations. Microbiological analysis of water used in the washer-disinfector was negative. However, observation of gastrointestinal endoscope reprocessing identified deviation from agreed processes, including initial manual cleaning. Also, the time dedicated to brushing and flushing of the channels was less than 10 min, and suction cylinders used for manual cleaning of the channels were not sterilized every day but were only disinfected. A single-diameter channel cleaning brush was used for all gastrointestinal endoscopes. This is not appropriate to clean endoscope channels of different diameters (Figure 2). Cleaning

Table I Characteristics of patients colonized or infected with extended-spectrum b-lactamase (ESBL)-producing Pseudomonas aeruginosa from May to August 2011 Case

Age (years)

Comorbidities

1

65

2

54

3

87

4

30

B-type haemophilia Sigmoid fistula Chronic pancreatitis Kidney failure Oesophagitis Acute kidney failure Hodgkin’s disease Tracheo-oesophageal fistula

ESBL-producing P. aeruginosa Date

Source

Infection

Gastroscopy Date

Invasive procedure

18/05/11

Psoas haematoma

Yes

21/04/11

Gastric biopsy

8/07/11

BAL

Yes

Gastric biopsy

13/08/11

Urine

No

24/02/11 18/03/11 22/07/11

24/08/11

Tracheal aspiration

Yes

24/06/11

e e

BAL, bronchoalveolar lavage. Please cite this article in press as: Bajolet O, et al., Gastroscopy-associated transmission of extended-spectrum beta-lactamase-producing Pseudomonas aeruginosa, Journal of Hospital Infection (2012), http://dx.doi.org/10.1016/j.jhin.2012.10.016

O. Bajolet et al. / Journal of Hospital Infection xxx (2012) 1e3

Figure 2. Importance of brush diameter for effective cleaning of endoscope channel (photograph provided by LTA Medical, Montreuil, France). (a) Diameter of the brush is correct for the channel size, and effective cleaning is ensured. (b) Diameter of the brush is too big, so brush fibres are compacted in the channel and are not effective. (c) Diameter of the brush is too small, so brush fibres do not touch the channel.

personnel noticed that channel cleaning brushes were collapsing inside the channels of some of the endoscopes. Drying after reprocessing and before storage was not sufficient as endoscopes were still wet at the time of investigation at the end of the cleaning process. The manufacturer’s check of the contaminated gastroscope identified wear of adhesive at the distal sheath. The distal sheath was removed. Consequently, the following measures were taken in August and September 2011: compliance with the recommended times for manual cleaning processes (10 min), use of brushes appropriate for the size of each endoscope channel, sterilization of suction cylinders after each use, and quarterly microbiological testing of endoscopes. An endoscope cupboard was acquired in September 2011 to store the endoscopes in a vertical position, facilitating drying. Following these measures, no other MDR-PA have been isolated. In total, 182 patients underwent an endoscopy with the contaminated gastroscope. Patients were not called back for follow-up evaluation, as neither treatment strategies nor specific precautions exist for colonization with MDR-PA.

Discussion This outbreak of an ESBL-producing P. aeruginosa was related to a gastroscope, which is an uncommon reservoir. The relationship between the gastroscope and the four patients affected was facilitated by the unusual resistance of the strain. A recent outbreak with a Klebsiella pneumonia-producing KPC-2 b-lactamase related to a contaminated duodenoscope was identified in France because of the scarcity of the strain.8 Exposure to contaminated equipment can be prevented through better reprocessing practices and adherence to decontamination guidelines. Previous reports have shown that deficiencies in endoscope reprocessing can lead to contamination with P. aeruginosa, which may lead to the development of biofilm. Deviations from agreed processes during manual cleaning, inappropriate size of endoscope cleaning brushes,

3

inadequate drying before storage and a minor defect in the sheath may have contributed to the development and persistence of bacterial biofilm in this case. It is noted that French guidelines do not recommend a flush with 70e90% ethyl or isopropyl alcohol before drying.5 According to US and other European guidelines, however, flushing with 70e90% alcohol or isopropyl alcohol is recommended for drying endoscope channels at the end of a clinic session.9,10 The usefulness of routine microbiological testing of endoscopes with standard microbiological techniques has not been established.10 In France, microbiological testing of endoscopes is recommended once per year. Since this outbreak, as the MDR-PA was cultured from the endoscope, quarterly microbiological testing has been implemented. Since withdrawing the gastroscope and instituting strict adherence to agreed decontamination processes, no other MDR-PA cases have been observed. Conflict of interest statement None declared. Funding sources None.

References 1. Nelson DB. Infectious disease complications of GI endoscopy. Part II: exogenous infections. Gastrointest Endosc 2003;57: 695e711. 2. Seoane-Vasquez E, Rodriguez-Monguio R. Endoscopy-related infection: relic of the past? Curr Opin Infect Dis 2008;21:362e366. 3. Fraser TG, Reiner S, Malczynski M, Yarnold PR, Warren J, Noskin GA. Multidrug-resistant Pseudomonas aeruginosa cholangitis after endoscopic retrograde cholangiopancreatography: failure of routine endoscope cultures to prevent an outbreak. Infect Control Hosp Epidemiol 2004;25:856e859. 4. Kovaleva J, Meessen NE, Peters FT, et al. Is bacteriologic surveillance in endoscope reprocessing stringent enough? Endoscopy 2009;41:913e916. 5. DHOS/DGS. Circulaire DHOS/E2/DGS/SD5C/2003/N 591 du 17/12/ 2003 relative aux modalite´s de traitement manuel pour la de´sinfection des endoscopes non autoclavables dans les lieux de soins. Paris: Ministe `re de la sante ´; 2003. 6. DHOS/DGS-CTINILS. Ele´ments d’assurance qualite´ en hygie`ne relatifs au controˆle microbiologique des endoscopes et a` la trac¸abilite´ en endoscopie. Paris: Ministe `re de la sante ´; 2007. 7. Brasme L, Nordmann P, Fidel F, et al. Incidence of class A extended-spectrum beta-lactamases in Champagne-Ardenne (France): a 1 year prospective study. J Antimicrob Chemother 2007;60:956e964. 8. Naas T, Cuzon G, Babics A, et al. Endoscopy-associated transmission of carbapenem-resistant Klebsiella pneumoniae producing KPC-2 beta-lactamase. J Antimicrob Chemother 2010;65: 1305e1306. 9. Beilenhoff U, Neumann CS, Rey JF, et al. ESGE-ESGENA guideline: cleaning and disinfection in gastrointestinal endoscopy update 2008. Endoscopy 2008;40:939e957. 10. Petersen BT, Chennat J, Cohen J, et al. Multisociety guideline on reprocessing flexible GI endoscopes: 2011. Infect Control Hosp Epidemiol 2011;32:527e538.

Please cite this article in press as: Bajolet O, et al., Gastroscopy-associated transmission of extended-spectrum beta-lactamase-producing Pseudomonas aeruginosa, Journal of Hospital Infection (2012), http://dx.doi.org/10.1016/j.jhin.2012.10.016

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