Download Unusual implication of biopsy forceps in outbreaks of Pseudomonas

Journal of Hospital Infection (2005) 61, 20–26
www.elsevierhealth.com/journals/jhin
Unusual implication of biopsy forceps in outbreaks
of Pseudomonas aeruginosa infections and
pseudo-infections related to bronchoscopy
P. Cornea,*, S. Godreuilb, H. Jean-Pierreb, O. Jonqueta, J. Camposb,
E. Jumas-Bilakc, Sylvie Parerd, H. Marchandinb
a
Service de Réanimation Médicale Assistance Respiratoire, Hôpital Gui de Chauliac, 80 avenue Augustin
Fliche, 34295 Montpellier, France
b
Laboratoire de Bactériologie, Hôpital Arnaud de Villeneuve, Montpellier, France
c
Laboratoire de Bactériologie, Faculté de Pharmacie, Montpellier, France
d
Unité d’Hygiène Hospitalière et de Prévention, Hôpital Saint-Eloi, Montpellier, France
Received 7 May 2004; accepted 27 January 2005
KEYWORDS
Bronchoscope;
Pseudomonas
aeruginosa; Pulsedfield gel
electrophoresis;
Outbreak; Biopsy
forceps
Summary Between January and April 2003, a sudden increase in positive
respiratory tract specimens for Pseudomonas aeruginosa was observed in an
intensive care unit of the University Teaching Hospital of Montpellier, France.
Most of the strains were cultured from bronchoalveolar lavage fluid samples,
suggesting that bronchoscopic procedures could be implicated. The relationships between isolates were investigated by antibiotyping and pulsed-field gel
electrophoresis. Both phenotypic and molecular markers allowed identification of two consecutive nosocomial outbreaks of respiratory infections
related to two different bronchoscopes. These two outbreaks implicated nine
and seven patients, respectively. Four of these 16 patients had true infections
and recovered with antibiotic therapy. Inspection of both bronchoscopes
revealed a damaged internal channel caused by defective biopsy forceps.
These defects led to improper cleaning and disinfection of the bronchoscopes
despite adherence to all current reprocessing procedures. The two outbreaks
were controlled after replacing the inner channels of the bronchoscopes and
switching from use of re-usable to disposable biopsy forceps. These outbreaks
emphasize the need to establish surveillance procedures for detecting
contamination of bronchoscopes, and the importance of recording each
endoscopic procedure to facilitate further investigations if needed.
Q 2005 The Hospital Infection Society. Published by Elsevier Ltd. All rights
reserved.
* Corresponding author. Tel.: C33 4 67 33 77 36; fax: C33 4 67 33 67 31.
E-mail address: [email protected]
0195-6701/$ - see front matter Q 2005 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.jhin.2005.01.024
P. aeruginosa outbreaks and bronchoscopy
21
Introduction
Pulsed-field gel electrophoresis (PFGE)
Contaminated endoscopes are the most common
cause of device-related nosocomial outbreaks.1 In
most cases, implicated micro-organisms are
environmental bacteria, particularly Pseudomonas
aeruginosa2–4 and mycobacteria.5,6 The outcome of
bronchoscopy-related infections can be dramatic,
particularly in critically ill patients. Moreover,
contamination of bronchoscopes can lead to
unnecessary diagnostic and therapeutic interventions. Most outbreaks have resulted from
inadequate cleaning and disinfection procedures.7
Less frequently, defective bronchoscopes have
been incriminated despite adequate reprocessing.3
As infections related to bronchoscopy are uncommon, there are no formal recommendations for any
type of surveillance for these procedures.8 The lack
of surveillance system can result in delays in the
initiation of outbreak investigation.8
Between January and April 2003, an increasing
number of P. aeruginosa isolates were recovered
from respiratory tract specimens in an intensive
care unit (ICU) of the University Teaching Hospital
of Montpellier, France. Most of the strains were
cultured from samples in patients who underwent
bronchoscopy. This report describes the epidemiological investigations undertaken to prove that this
increase was associated with the spread of
P. aeruginosa clones and to search for the common
source of infection.
Genomic DNAs were prepared by a method
described previously.10 P. aeruginosa DNAs were
digested with 40 U of the the restriction enzyme
SpeI (New England Biolabs, Hertfordshire, UK) for
6 h at 37 8C. PFGE was performed with a CHEF-DR III
apparatus (Bio-Rad, Hercules, CA, USA) in a 1%
agarose gel in Tris-borate-EDTA buffer at 8 8C for
40 h. SpeI digests were run at 4.5 V/cm with pulses
from 40 to 5 s. PFGE patterns were compared by
visual inspection and interpreted according to the
criteria of Tenover et al.11
Materials and methods
Bacterial strains and antibiotic susceptibility
profiles
P. aeruginosa strains recovered from sputum and
bronchoalveolar lavage (BAL) samples in patients
hospitalized in an ICU of the University Teaching
Hospital of Montpellier, France between January
and April 2003 were collected. The two bronchoscopes, designated A and B, used in this ICU during
the same period were investigated for bacterial
culture after flushing the biopsy port into a sterile
cup with 40 mL of sterile saline that mimicked BAL,
swabbing the biopsy port-cap and the suction port
of the bronchoscopes, and sampling tap water and
cleaning solutions. The isolates were identified by
conventional phenotypic methods. Antibiotic susceptibility was tested by disk diffusion assay on
Mueller–Hinton agar, and interpreted according to
the recommendations of the Antibiogram Committee of the French Microbiology Society.9
Clinical data and outcomes
Medical records were reviewed to determine
whether patients who had undergone a bronchoscopy had transient colonization or true infection.
Patients were considered to be colonized on the
basis of clinical and radiological data, and if
subsequent sputum analysis did not reveal the
same bacteria as BAL samples. In contrast, infection was defined: (i) on the basis of clinical data,
particularly signs of respiratory tract infection with
fever and purulent sputum; (ii) on radiographic
appearance of a new and persistent pulmonary
infiltrate; (iii) on isolation of the same bacterial
species from sputum with a bacterial count O107
colony forming units/mL; and (iv) if PFGE patterns
of strains from BAL and sputum samples were
indistinguishable. Respiratory infections were considered to be potentially attributable to bronchoscopy if they occurred within 14 days of
bronchoscopic procedures.
Bronchoscope cleaning procedures
Bronchoscopes were cleaned by trained personnel
in accordance with national guidelines.12 Briefly,
after leak testing, instruments were soaked twice
(10 and 5 min, respectively) in detergent (Aniosyme
Pla, Anios, Lille, France) and cleaned manually by
wiping the outer surface and brushing the internal
channel and suction ports. Bronchoscopes subsequently underwent complete immersion in a
solution of peracetic acid (Anioxyde 1000, Anios)
for 20 min. Finally, bronchoscopes were rinsed with
sterile water, dried with forced air and stored.
Results
Between January and April 2003, the frequency of
isolation of P. aeruginosa from BAL samples
22
increased dramatically (Figure 1). During this
period, 61 bronchoscopic procedures were performed in 36 patients with two different bronchoscopes (bronchoscopes A and B). All patients were
mechanically ventilated, and evaluation of pneumonia and bronchial aspiration were the main
indications for bronchoscopy. Thirty-six BAL specimens were obtained for bacterial culture and 20
samples yielded growth of 22 P. aeruginosa isolates. Six different antibiotypes, named 1 to 6, were
detected among these 22 P. aeruginosa strains
(Table I), and two main clusters of isolates were
detected according to their antibiotype and their
date of isolation.
Between 4 and 17 January 2003, eight
P. aeruginosa strains were isolated from BAL
samples collected with bronchoscope A in patients
1–8 (P1–P8). In five of these eight BAL specimens,
organisms other than P. aeruginosa were recovered, including Staphylococcus aureus in two
patients (P1 and P6) and Streptococcus pneumoniae
in two other patients (P5 and P8). These eight
P. aeruginosa isolates were only resistant to
imipenem (antibiotype 1) and displayed the same
pulsotype A (Table I and Figure 2). Investigation of
bronchoscope A after flushing with sterile saline
yielded the growth of a P. aeruginosa isolate (strain
10) showing antibiotype 1 and pulsotype A. However, the index case and the mechanism of
contamination of bronchoscope A remained
unknown. Two patients (P6 and P10) were con-
Figure 1 Number of Pseudomonas aeruginosa isolates
recovered monthly from bronchoalveolar lavage samples
in the intensive care unit between November 2002 and
June 2003. Striped bars, number of strains unrelated to
the outbreaks determined by pulsed-field gel electrophoresis analysis; open bars, number of strains from
outbreak 1 with pulsotype A; solid bars, number of strains
from outbreak 2 with pulsotype D.
P. Corne et al.
sidered to have been infected during bronchoscopy.
Indeed, these two patients presented clinical and
radiological signs of pneumonia and had subsequent
respiratory tract culture (strains 7 and 14) that grew
P. aeruginosa with antibiotype 1 and pulsotype A.
Between 1 February and 1 April 2003, 14 clinical
isolates were recovered in 12 BAL samples from 10
ICU patients (Table I). P. aeruginosa was recovered
in pure culture in nine of the 12 BAL specimens,
with coagulase-negative staphylococci in two
samples and S. aureus in one specimen. Ten of
the 14 isolates displayed a similar antibiotype
(antibiotype 6) and the same pulsotype (pulsotype
D) (Table I and Figure 2). The P. aeruginosa strain
recovered from bronchoscope B after flushing with
sterile saline (strain 28) showed the same phenotypic and genotypic characteristics. For P12,
P. aeruginosa had been isolated from sputum
samples before undergoing bronchoscopy, and this
patient was considered to be the source of
contamination of bronchoscope B. Two patients
(P15 and P17) presented with bronchitis after
bronchoscopic procedures, and were considered
to be infected by the P. aeruginosa strain recovered
from bronchoscope B. For three patients (P9, P11
and P18) who underwent bronchoscopy with
bronchoscope B, P. aeruginosa strains recovered
from BAL samples showed different antibiotypes
and unrelated pulsotypes.
The four patients infected during bronchoscopic
procedures (P6, P10, P15 and P17) recovered under
antibiotic therapy. Three patients (P10, P15 and
P17) received piperacillin/tazobactam for eight to
14 days. P6 had one recurrence of P. aeruginosa
pneumonia and received cefepime and ofloxacin for
14 days and ticarcillin/clavulanate for 21 days with
tobramycin for the first seven days.
In the ICU, written bronchoscope reprocessing
protocols were reviewed, and reprocessing procedures were observed during unannounced visits.
No significant breaches in reprocessing procedures
were observed and re-usable biopsy forceps were
sterilized correctly between patients. Moreover,
bronchoscopes A (model BF type P15, Pentax; date
of manufacturing: 1999) and B (model BF type 18P,
Pentax; date of manufacturing: 2001) had been
regularly serviced and maintained, and the last
maintenance service was in December 2002 for both
bronchoscopes. These two bronchoscopes were
removed from the ICU on 21 January and 2 April
2003, respectively. Inspection by the manufacturer
revealed large breaches in the internal channel of
both bronchoscopes due to defective biopsy forceps. After April 2003, the rate of recovery of
P. aeruginosa from BAL specimens returned to
baseline level (Figure 1).
Straina
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
Patient (P) or
bronchoscope
Bronchoscope
used
Date of isolation
(day/month)
Sample
Bacterial
count
(CFU/mL)
Antibiotypeb
Infection (I) or
contamination (C)
Pulsotypec
P1
P2
P3
P4
P5
P6
P6
P7
P8
Bronchoscope A
P9
P9
P9
P10
P11
P12
P12
P13
P14
P12
P15
P16
P17
P17
P15
P18
P19
Bronchoscope B
A
A
A
A
A
A
–
A
A
–
B
B
B
–
B
B
B
B
B
B
B
B
B
–
–
B
B
–
04/01
07/01
08/01
08/01
10/01
12/01
13/01
15/01
17/01
21/01
01/02
01/02
01/02
03/02
14/02
21/02
04/03
14/03
16/03
17/03
18/03
20/3
21/03
24/03
24/03
31/03
01/04
02/04
BAL
BAL
BAL
BAL
BAL
BAL
Sputum
BAL
BAL
–
BAL
BAL
BAL
Sputum
BAL
BAL
BAL
BAL
BAL
BAL
BAL
BAL
BAL
Sputum
Sputum
BAL
BAL
–
O106
9!103
2!104
–
3!104
102
O107
O104
104
–
–
–
–
108
O104
104
105
2!104
103
O104
60
3!102
5!103
O107
O107
O106
6!104
–
1
1
1
1
1
1
1
1
1
1
2
3
4
1
5
6
6
6
6
6
6
6
6
6
6
2
6
6
C
C
C
C
C
I
I
C
C
–
C
C
C
I
C
I
I
C
C
I
I
C
I
I
I
C
C
–
A
A
A
A
A
A
A
A
A
A
B
B
B1
A
C
D
D
D
D
D
D
D
D
D
D
E
D
D
23
–, not determined; CFU, colony forming unit; BAL, bronchoalveolar lavage; bold type, strains isolated from bronchoscopes.
a
Presented by chronological date of isolation.
b
Determined by pattern of susceptibility to the following antibiotics: ticarcillin; ticarcillin/clavulanate; piperacillin; piperacillin/tazobactam; imipenem; cefotaxime; ceztazidime;
cefepime; gentamicin; tobramycin; netilmicin; amikacin; colistin; pefloxacin; and ciprofloxacin. Antibiotype 1, resistance to imipenem only; antibiotype 2, wild-type phenotype;
antibiotype 3, resistance to ticarcillin and intermediate susceptibility to ticarcillin/clavulanate, aztreonam, gentamicin and netilmicin; antibiotype 4, multi-resistance; antibiotype 5,
intermediate susceptibility to cefepime and resistance to all aminoglycosides tested; antibiotype 6, resistance to ticarcillin, ticarcillin/clavulanate and aztreonam and intermediate
susceptibility to cefepime and pefloxacin.
c
Identical pulsed-field gel electrophoresis (PFGE) patterns were assigned the same annotation, related pulsotypes were noted A, A1, etc. and unrelated PFGE patterns were noted
pulsotype A, B, etc.
P. aeruginosa outbreaks and bronchoscopy
Table I Data for strains of Pseudomonas aeruginosa recovered from bronchoalveolar lavage (BAL) and corresponding sputum samples between January and April
2003 in the intensive care unit
24
P. Corne et al.
Figure 2 Pulsed-field gel electrophoresis profiles of selected strains of Pseudomonas aeruginosa. Lane M, concatemer
of phage lambda DNA (48.5 kb) as molecular weight marker. Bold type, strains isolated from bronchoscopes. (a) Lanes I
and II, strains isolated from bronchoalveolar lavage samples in November 2002 and December 2002, respectively, before
first outbreak and showing two unrelated pulsotypes (U); lanes 1, 6, 7, 9 and 10, corresponding strains in Table I with
identical pulsotype A. (b) Lanes 16, 18, 19, 21, 23, 24, 26 and 27, corresponding strains in Table I with identical pulsotype
D characteristic of the second outbreak; lane 25, strain 25 with unrelated pulsotype E.
Discussion
The increasing number of P. aeruginosa isolates
recovered from BAL specimens in the ICU over a
three-month period was investigated by both
phenotyping and genotyping methods. Usually, the
antibiotype is considered to be an epidemiological
marker with low discriminatory power for
P. aeruginosa typing due to the capacity of this
bacteria to gradually and progressively develop its
resistance to antibiotics. However, some outbreaks
of P. aeruginosa infections, related or not to
bronchoscopy, are still detected on the basis of an
unusual antibiotype of the epidemic cluster,13,14 as
was the case in the first outbreak reported here.
Indeed, eight P. aeruginosa strains isolated from
BAL samples during January 2003 only displayed
resistance to imipenem, suggesting a mechanism of
resistance due to decreased penetration through
the outer membrane. Since this pattern of isolated
resistance to imipenem is rarely observed in our
institution, these strains were suspected to be
clonaly related. In contrast, the antibiotype of
P. aeruginosa strains involved in the second outbreak was more usual in our institution, and the
increasing number of P. aeruginosa isolates recovered from BAL specimens was the warning to
activate investigations. Further investigations
were conducted by macrorestriction analysis of
SpeI-digested DNA, which is considered to be
the most discriminatory molecular method for
P. aeruginosa typing.15 Finally, two successive
P. aeruginosa outbreaks implicating nine and
seven patients, respectively, were identified after
PFGE analysis and each epidemic cluster could be
linked to a contaminated bronchoscope.
Previously reported outbreaks of P. aeruginosa
infections related to bronchoscopy have been
attributed to inappropriate handling methods for
disinfection,7,16,17 and to contamination13,18 or
improper connection to an automated washerdisinfector.2 More recently, two large outbreaks
of P. aeruginosa infections and contamination
implicated manufacturing defects in bronchoscopes
for the first time. Both outbreaks were attributed to
a loose biopsy-port cap in the bronchoscopes,
P. aeruginosa outbreaks and bronchoscopy
resulting in inadequate disinfection of the bronchoscopes.3,4 In our institution, an automated endoscope washer is not used for bronchoscopes.
Cleaning and disinfection procedures are manual
and are performed in accordance with national
guidelines.12 Although reprocessing procedures
were shown to be performed correctly in the ICU,
bacteriological investigations of the bronchoscopes
yielded a pure culture of P. aeruginosa after saline
flushes. In contrast, no bacterial growth was
obtained from the biopsy port-cap and the port of
the bronchoscopes, tap water or cleaning solutions,
suggesting that they were not implicated in the
spread of P. aeruginosa. This observation contrasted with previous studies showing that saline
flushes are less sensitive than brush cultures of
bronchoscope lumens for detection of contamination,19 and demonstrated that saline flushes
remain useful to search for bronchoscope contamination. Finally, inspection of both bronchoscopes
by the manufacturer revealed a defect in the
internal channel caused by defective biopsy forceps. These defects were not detected by leak
tests. The biopsy forceps had defective closing that
was not visually detectable, probably due to
repeated use and decontamination. These damaged
inner channels probably sheltered organisms and
led to improper cleaning and disinfection of the
bronchoscopes despite adherence to all current
reprocessing standards. The two outbreaks were
controlled after replacing the inner channels of the
bronchoscopes. Since these outbreaks, disposable
biopsy forceps have been used in the ICU. At
present, in France, the use of disposable biopsy
forceps is obligatory in gastrointestinal endoscopy
because of the risk of prions.20 On the other hand,
there are no recommendations for biopsy forceps in
bronchoscopy. Based on the outbreaks reported
herein, the use of disposable biopsy forceps also
seems to be necessary for bronchoscopy.
There are no formal recommendations for
surveillance of bronchoscopic procedures.21 The
two outbreaks reported here emphasize the importance of monitoring microbiology results for all
procedures. This type of surveillance can be
performed manually or by automated computer
system, and identifies an increase in the recovery of
organisms in specimens taken during procedures.8
Moreover, the investigation of suspected outbreaks
is considerably facilitated by the record of each
bronchoscopic procedure, including the patient’s
name, the date of the procedure and the serial
number of the endoscope used. Another type of
surveillance procedure is periodic examination of
endoscopic equipment for contamination. This type
of surveillance procedure is already performed by
25
30% of bronchoscopists with varied frequencies.22
Although this approach of surveillance is attractive,
there are no standard culture methods, no standard
for how often the cultures should be performed,
and no consensus regarding what threshold of
various types of bacteria is considered to be
problematic. This area requires more investigation.7,8 Consequently, periodic surveillance cultures of bronchoscopes is not formally
recommended.7,23
Reports of outbreaks related to bronchoscopy for
which no procedural breaches could be identified
are very rare, as are nosocomial infections involving
bronchoscopy accessories. We presented here two
successive outbreaks of P. aeruginosa infections
and pseudo-infections attributed to defective
bronchoscopes. For the first time, these defects
were attributed to defective re-usable biopsy
forceps, and this accessory should be considered
as an additional potential source of cross-infection
during bronchoscopy. Contamination of the endoscopes was controlled after replacing the inner
channels and establishing the use of disposable
biopsy forceps despite their cost. These outbreaks
emphasize the need for surveillance procedures for
detecting contamination of bronchoscopes, and the
importance of recording each endoscopic procedure to facilitate epidemiological investigations
in case of suspected outbreaks.
Acknowledgements
The authors are grateful to Pr Philippe Van de Perre
for critical reading of the manuscript.
References
1. Spach DA, Silverstein FE, Stamm WE. Transmission of
infection by gastrointestinal endoscopy and bronchoscopy.
Ann Intern Med 1993;118:117—128.
2. Sorin M, Segal-Maurer S, Mariano N, Urban C, Combest A,
Rahal JJ. Nosocomial transmission of imipenem-resistant
Pseudomonas aeruginosa following bronchoscopy associated
with improper connection to the Steris System 1 processor.
Infect Control Hosp Epidemiol 2001;22:409—413.
3. Kirschke DL, Jones TF, Craig AS, et al. Pseudomonas
aeruginosa and Serratia marcescens contamination associated with a manufacturing defect in bronchoscopes. N Engl
J Med 2003;348:214—220.
4. Srinivasan A, Wolfenden LL, Song X, et al. An outbreak of
Pseudomonas aeruginosa infections associated with flexible
bronchoscopes. N Engl J Med 2003;348:221—227.
5. Kressel AB, Kidd F. Pseudo-outbreak of Mycobacterium
chelonae and Methylobacterium mesophilicum caused by
contamination of an automated endoscopy washer. Infect
Control Hosp Epidemiol 2001;22:414—418.
26
6. Ramsey AH, Oemig TV, Davis JP, Massey JP, Török TJ. An
outbreak of bronchoscopy-related Mycobacterium tuberculosis infections due to lack of bronchoscope leak testing.
Chest 2002;121:976—981.
7. Culver DA, Gordon SM, Mehta AC. Infection control in the
bronchoscopy suite. A review of outbreaks and guidelines for
prevention. Am J Respir Crit Care Med 2003;167:
1050—1056.
8. Srinivasan A. Epidemiology and prevention of infections
related to endoscopy. Curr Infect Dis Rep 2003;5:467—472.
9. Soussy CJ, Carret G, Cavallo JD, et al. Antibiogram
Committee of the French Microbiology Society. Report
2000–2001. Pathol Biol (Paris) 2001;48:832—871.
10. Gouby A, Neuwirth C, Bourg G, et al. Epidemiological study
by pulsed-field gel electrophoresis of an outbreak of
extended-spectrum b-lactamase-producing Klebsiella pneumoniae in a geriatric hospital. J Clin Microbiol 1994;32:
301—305.
11. Tenover FC, Arbeit RD, Goering RV, et al. Interpreting
chromosomal DNA restriction patterns produced by pulsedfield gel electrophoresis: criteria for bacterial strain typing.
J Clin Microbiol 1995;33:2233—2239.
12. Ministère de la Santé, de la famille et des personnes
handicapées. Circulaire DHOS/E 2/DGS/SD 5 C n82003-591
du 17 décembre 2003 relative aux modalités de traitement
manuel pour la désinfection des endoscopes non autoclavables dans les lieux de soins Bull Officiel 2004; 1:11.
13. Schelenz S, French G. An outbreak of multidrug-resistant
Pseudomonas aeruginosa infection associated with contamination of bronchoscopes and an endoscope washer–disinfector. J Hosp Infect 2000;46:23—30.
14. Denton M, Kerr K, Mooney L, et al. Transmission of colistinresistant Pseudomonas aeruginosa between patients attending a pediatric cystic fibrosis center. Pediatr Pulmonol 2002;
34:257—261.
P. Corne et al.
15. Grundmann H, Schneider C, Hartung D, Daschner FD, Pitt TL.
Discriminatory power of three DNA-based typing techniques
for Pseudomonas aeruginosa. J Clin Microbiol 1995;33:
528—534.
16. Kolmos HJ, Lerche A, Kristoffersen K, Rosdahl VT. Pseudooutbreak of Pseudomonas aeruginosa in HIV-infected
patients undergoing fiberoptic bronchoscopy. Scand
J Infect Dis 1994;26:653—657.
17. Silva CV, Magalhaes VD, Pereira CR, Kawagoe JY, Ikura C,
Ganc AJ. Pseudo-outbreak of Pseudomonas aeruginosa and
Serratia marcescens related to bronchoscopes. Infect Control Hosp Epidemiol 2003;24:195—197.
18. Blanc DS, Parret T, Janin B, Raselli P, Francioli P. Nosocomial
infections and pseudoinfections from contaminated
bronchoscopes: two-year follow up using molecular markers.
Infect Control Hosp Epidemiol 1997;18:134—136.
19. Rutala WA, Weber DJ. Disinfection of endoscopes: review of
new chemical sterilants used for high-level disinfection.
Infect Control Hosp Epidemiol 1999;20:69—76.
20. Ministère de l’emploi et de la solidarité. Décision du 18 juin
portant sur l’interdiction de réutilisation des pinces à biopsie
endoscopique digestive. J Officiel 2001;150:10403.
21. British Thoracic Society Bronchoscopy Guidelines Committee, a Subcommittee of Standards of Care Committee of
British Thoracic Society. British Thoracic Society guidelines on
diagnostic flexible bronchoscopy. Thorax 2001;56(Suppl. 1):
1—21.
22. Srinivasan A, Wolfenden LL, Song X, Perl TM, Haponik EF.
Bronchoscope reprocessing and infection prevention and
control: bronchoscopy-specific guidelines are needed. Chest
2004;125:307—314.
23. Rutala WA, Weber DJ. Reprocessing endoscopes: United
States perspective. J Hosp Infect 2004;56(Suppl. 2):
S27—S39.