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Clinical case study
Investigating the failure of repeated standard cleaning and
disinfection of a Pseudomonas aeruginosaeinfected pancreatic and
biliary endoscope
Lijun Qiu a
, Zhihui Zhou b
, Qifang Liu a
, Yuhua Ni a
, Feng Zhao c
, Hao Cheng MD d,
*
a
Endoscopy Center, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, P.R. China
b
Infection Department, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, P.R. China
c
Clinical Laboratory Department, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, P.R. China
d
Dermatology and Venerology Department, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, P.R. China
Key Words:
Pseudomonas aeruginosa
Endoscope
Disinfection
Digestive endoscopy is an important technique for the diagnosis and treatment of digestive system
disease. To assure medical safety, a digestive endoscope must be cleaned and disinfected before its use in
an operation on the next patient. The most common treatment procedure on a digestive endoscope is
high-level disinfection. The potential risk associated with digestive endoscopes is always the focus of
endoscopic management in clinical practice. In this study, a polluted pancreatic and biliary endoscope
after surgery was cleaned and disinfected multiple times with the standard procedure but still tested
positive for Pseudomonas aeruginosa culture, which is very rare and has not been reported in China or
abroad.
Copyright Ó 2015 by the Association for Professionals in Infection Control and Epidemiology, Inc.
Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
Digestive endoscopy is an important technique for the diagnosis
and treatment of digestive system disease. Similar to many other
high-precision medical devices, a digestive endoscope is a device
with a complex structure, special building materials, and reus-
ability. To assure medical safety, a digestive endoscope must be
cleaned and disinfected before its use in an operation on the next
patient. The most common treatment procedure on a digestive
endoscope is high-level disinfection. According to current literature
reports, digestive endoscopic examinationerelated pathogen
spread is caused by the following: incompliance of the guidelines
for endoscope cleaning and disinfection procedure; use of a
defective device; or biofilm formation on endoscope tubes leading
to failure of the cleaning and disinfection. The potential risk asso-
ciated with digestive endoscopes is always the focus of endoscopic
management in clinical practice. In this study, a polluted pancreatic
and biliary endoscope after surgery was cleaned and disinfected
multiple times with the standard procedure but still tested positive
for Pseudomonas aeruginosa culture, which has never been reported
in China or abroad.
CASE REPORT
Case 1
An 82-year-old man was admitted to the hospital because of
epigastric pain for 2 days. The physical examination results showed
a temperature of 36.8C, pulse of 96 beats per minute, respiration of
18 breaths per minute, blood pressure (BP) of 102/60 mm Hg,
complete blood count (CBC) of 17.9  109
/L, no clear yellow stain or
bleeding spot on the systemic skin mucous membrane, no
enlargement for either cervical or supraclavicular lymph nodes,
positive Murphy sign, soft abdomen, and active bowel sounds.
Abdominal B ultrasound suggested acute cholecystitis, calculus
incarcerated in the neck of the gallbladder, multiple gallbladder
stones, and the upper section with common bile duct stones
accompanied by extrahepatic biliary dilatation. The patient was
diagnosed with acute obstructive suppurative cholangitis and was
given emergent endoscopic retrograde cholangiopancreatography
(ERCP) and endoscopic retrograde biliary drainage. The patient
started to have a fever on day 3 after the surgery, with a maximum
* Address correspondence to Hao Cheng, MD, 3 Qingchun East Rd, 310016
Hangzhou, Zhejiang Province, China.
E-mail address: hz_chenghao@126.com (H. Cheng).
Funding/Support: Supported by the Medical Science Research Foundation of
Zhejiang Province (grant no. 2010KYA112).
Conflicts of interest: None to report.
Contents lists available at ScienceDirect
American Journal of Infection Control
journal homepage: www.ajicjournal.org
American Journal of
Infection Control
0196-6553/Copyright Ó 2015 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. This is an open access article under the
CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
http://dx.doi.org/10.1016/j.ajic.2015.04.204
American Journal of Infection Control 43 (2015) e43-e46
body temperature of 39C. Bile culture for P aeruginosa tested
positive. Blood culture for both Klebsiella pneumoniae and Escher-
ichia coli also tested positive.
Case 2
An 80-year-old man was previously admitted to the hospital in
January when he was 79 because his skin and sclera turned yellow
accompanied with weight loss. The physical examination results
showed a temperature of 36.7C, a pulse of 70 beats per minute,
respiration of 18 breaths per minute, BP of 106/58 mm Hg, and CBC
of 3.5  109
/L. The sclera and systemic skin clearly exhibited a
yellow stain. The superficial lymph nodes, heart, and lungs were
normal. The abdomen was soft without tenderness or rebound
pain. The Murphy sign was negative, and bowel sounds were
normal. An upper abdominal noncontrast enhanced computed to-
mography scan and magnetic resonance cholangiopancreatography
showed a widespread expansion of the intra- and extrahepatic bile
duct, a common bile duct obstruction, and a dilated pancreatic duct.
In addition, the ultrasound result from another facility suggested
the following: a low echo occupied the low part of the common bile
duct; cancer; chronic schistosomiasis; dilatation in the common
bile duct, intrahepatic bile duct, and main pancreatic duct; multiple
gallbladder stones; biliary sludge; and a filled spleen. The patient
was diagnosed with common bile duct obstruction and possible
pancreatic head cancer or ampullary cancer. The patient was given
ERCP, endoscopic sphincterotomy, and endoscopic biliary stent
implantation (2 days after the previous patient). The patient
developed a fever on day 2 after the surgery, with a maximum body
temperature of 39.2C. Bile culture of P aeruginosa tested positive.
Blood culture of both K pneumoniae and E coli tested positive.
Case 3
A 40-year-old man was admitted to the hospital because of
recurrent fever and abdominal pain for 20 days and exacerbated
conditions for 4 days. The physical examination showed the
following: temperature of 37.5C, pulse of 98 beats per minute,
respiration of 19 breaths per minute, BP of 91/53 mm Hg, and CBC
of 12.0  109
/L. No skin superficial lymph node enlargement was
observed. The abdomen was soft without intestinal or gastric
peristalsis. The left lower abdomen showed tenderness without
rebound pain or muscle tension. The Murphy sign was negative,
and bowel sounds were normal. The patient was given an auxiliary
examination of the abdomen and Bartholin, Urethral, and Skene
glands; the result showed multiple small stones in the gallbladder,
cholecystitis, hepatic adipose infiltration, and a lower left abdom-
inal cystic mass with possible abscess. High-sensitivity C-reactive
protein tested at 81.7 mg/L. The patient was diagnosed with gall-
bladder stones and common bile duct stones. ERCP was performed
to remove the stones, and nasobiliary drainage was given (3 days
after the ERCP operation on the previous patient). This patient
developed a fever on day 4 after the surgery, with a maximum body
temperature of 39C. Bile culture of P aeruginosa tested positive.
Blood culture tested negative.
Treatment and monitoring of endoscope
Preventive monitoring and investigation on multidrug-resistant
bacteria infection by the department of infectious disease discov-
ered that the infection of 3 patients occurred after ERCP surgery. The
entire process of ERCP in the endoscopy center was investigated
immediately. The procedures, including patient documentation,
operation environment, the device, and endoscopic-related
equipment, were inspected. Compliance with the cleaning and
disinfection technical standard for endoscope operations, such as
the rinse of the lifting clamp channel of the pancreatic and biliary
endoscope and infection control chain inside the hospital, was also
investigated. The results revealed that the same pancreatic and
biliary endoscope was used in operations on the 3 patients
sequentially. This pancreatic and biliary endoscope was suspended
immediately, and biologic inspection was performed on the device.
Bacteria culture of P aeruginosa tested positive. Pulsed-field gel
electrophoresis revealed a high homology between the P aeruginosa
from the endoscope and those from the 3 patients (Fig 1.). This
endoscope was again cleaned and disinfected in compliance with
the standard protocol followed by a biologic inspection. The P aer-
uginosa culture still tested positive. This endoscope was cleaned and
disinfected using the standard procedure for a third and fourth time.
In addition, various high-level disinfectants were used in the im-
mersion disinfection process, including 2% glutaraldehyde,
o-Phthalaldehyde (made in China), o-Phthalaldehyde (imported),
and 24% glutaraldehyde (imported). Biologic inspection was carried
out again after each disinfection procedure, and the P aeruginosa
culture still tested positive. The endoscope was cleaned with the
standard procedure for the fifth time and soaked in 2% glutaralde-
hyde for 13 hours to sterilize. Biologic inspection was performed
again and the P aeruginosa culture still tested positive, but the colony
count decreased by 50% when compared with the previous samples.
The endoscope was sent to the Olympus endoscopic repair station at
Shanghai, China. After being sterilized with epoxyethane, the entire
endoscopic channel of the endoscope was dismantled and sent to
the Laboratoire Biotech-Germande (Marseille, France) for exami-
nation. Microbiologic analysis was performed on the sample
retrieved from the 4 tubes of the endoscope, and the report showed
that the level of polymorphic nonpathogenic bacteria was higher
than the allowed interference level in the standard guideline rec-
ommended by the hospital Committee of Technical Infection. The
endoscope was cleaned and disinfected with a standard procedure
and stored for 24 hours. Samples taken from the endoscope still
tested positive with polymorphic nonpathogenic bacteria. In addi-
tion, the number of bacteria at the biopsy-suction tube and lifting
clamp tube was higher than the allowed interference level in the
standard guideline recommended by the hospital Committee of
Technical Infection. Measurement of the protein and total organic
carbon contents excluded the possible existence of bacterial biofilm
in the various tubes. In the end, the repair center replaced the in-
ternal tubes of the endoscope on dismantlement of various com-
ponents. The endoscope was then cleaned and disinfected with the
standard protocol at the hospital endoscopy center and sent for
biologic inspection. The bacteria culture this time was negative after
2 tests.
DISCUSSION
The completeness of endoscope cleaning and disinfection is
crucial for medical safety and is highly regarded by hospital and
endoscope management staff nationwide. The Chinese Department
of Health published Guidelines for Cleaning and Disinfecting Endo-
scopes (2004 version), in which rule 34 in chapter 5 stated that after
cleaning and disinfecting with the standard procedure, gastroin-
testinal endoscopy, pancreatic and biliary endoscope require a
quarterly biologic inspection. In our hospital a standard precleaning,
cleaning, and disinfection of the endoscope is managed under World
Gastroenterology Organization (WGO/OMGE)-Organization Mon-
diale de Gastroenterologie (OMGE)/the World Organization of
Digestive Endoscopy (OMED) Practice Guideline Endoscope Disinfec-
tion (2005 version). Considering the narrow lifting clamp tube and
complex structure of the pancreatic and biliary endoscope, it is
harder to clean and disinfect than other endoscopes. Since 2011,
L. Qiu et al. / American Journal of Infection Control 43 (2015) e43-e46
e44
the endoscopy center of our hospital has adopted a policy that
biologic inspections for pancreatic and biliary endoscope be per-
formed every 4 weeks based on the recommendation from the
Gastroenterological Society of Australia in Guidelines Infection
Control in Endoscopy (3rd ed). In this report, a pancreatic and biliary
endoscope in our hospital was used in an ERCP operation on a
patient with bile duct infection. After standard cleaning and disin-
fection, the endoscope was used for ERCP operations on another 2
patients and resulted in the P aeruginosa infection of these 2 pa-
tients. Even though a previous study reported that the probability of
pathogen spread during endoscopic examination operation was 1 in
1.8 million,1
some other studies have suggested that with the
compliance of infection control guidelines, the endoscope prepared
for patients still showed a 2% bacterial infection rate.2
The infection
risk was hard to evaluate for various reasons. The blood culture and
bile culture of the 3 patients reported in this study were not
completely the same, which suggested a potential source of
endogenous infection. However, the 3 cases showed a surprisingly
similar bile culture result and bacteria homology, which indicated
the relevance between the P aeruginosa infection and the endoscope
used in the process. The standard cleaning and disinfection pro-
cedures on the endoscope plus a standard cleaning and sterilizing
procedure were performed, but the biologic inspection result still
came back positive for P aeruginosa. However, the biofilm tested
negative. The bacteria culture tested negative until the endoscope
was dismantled and replaced with new internal tubes. All the 3
patients were under the treatment with antibiotics before and after
the endoscopic examination for cholecystitis and were given naso-
biliary drainage. Therefore, no special treatment for P aeruginosa
infection was given. Case patients 1 and 3 recovered afterward. Case
patient 2 went to a local hospital for further treatment after the
infection was under control.
The failed cleaning and disinfection for this endoscope might be
the result of the following. P aeruginosa could have developed a
resistance to disinfectants, especially aldehyde disinfectants. Even
though no direct evidence was found in this study, a previous study
suggested that atypical mycobacteria showed complete resistance
to glutaraldehyde.3
Also, this endoscope was used for 6 years, and
its inner tubes might have been damaged and left with a rough or
uneven surface and cracks. During the ERCP operation on patients
with bile duct infection, bacteria easily accumulated in the irregular
connections, cracks, or ruptures of the internal channel surface and
were hard to clean up.4
The final explanation is formation of biofilm.
Biofilms consist of substrates from different types of bacteria and
extracellular polysaccharides secreted by the bacteria that are
attached to the surface of the endoscope. With the growth of bac-
teria in the biofilm-covered channels, even though the standard
cleaning and disinfection procedure is executed, the damaged
channel with bacteria attached would potentially prevent the
disinfectant from killing the bacteria. The infecting bacteria in this
study were P aeruginosa, which is a typical biologic organism that
can easily develop biofilms. In addition, this type of biofilm is very
difficult to remove from the channel components and damaged
endoscopic tubes, therefore increasing the infection risk to the next
patient even after a standard cleaning and disinfection procedure.
The examination of the biofilm was based on stochastic selection of
the remaining samples for endoscopic biologic inspection, which
indicated the possibility of missed detections. Therefore, even
though no biofilm was detected during the biologic inspection
process in this study, it was still difficult to exclude the possibility of
biofilm formation. It is necessary to improve the standard cleaning
and disinfection methods for P aeruginosaeinfected endoscopes.
For example, an automatic endoscope washer with an ultrasonic
oscillation function and the application of detergent with good
biofilm removing efficiency could more effectively remove the
attached bacteria.5
In this case, cross-infection and in-hospital
infection could be reduced, and medical safety could eventually
be assured.
Fig 1. Pulsed-field gel electrophoresis revealed a high homology between the Pseu-
domonas aeruginosa from the endoscope (307) and those from the bile cultures of the 3
patients (309, 310, 305).
L. Qiu et al. / American Journal of Infection Control 43 (2015) e43-e46 e45
CONCLUSION
ERCP is the endoscopic operation with the highest postsurgical
infection rate.6-10
According to the endoscopic treatment experi-
ences of the authors of this report, after an endoscopic examination
or treatment was performed on a patient with a high infection risk,
a biologic inspection after the standard cleaning and disinfection of
the endoscope is very critical. It is recommended to perform an
immediate bacteria culture after any endoscopic operation on a
patient with a suspected bile duct infection. In addition, biologic
inspection is still necessary even after cleaning and disinfection.
The endoscope should only be used again on the confirmation of a
negative bacteria culture result.
References
1. Srinivasan A. Epidemiology and prevention of infections related to endoscopy.
Curr Infect Dis Rep 2003;5:467-72.
2. Ishino Y, Ido K, Sugano K. Improvement of the automatic endoscopic reproc-
essor: self-cleaning disinfecting connectors between endoscope and reproc-
essor. Endoscopy 2003;35:469-71.
3. Lee JH, Rhee PL, Kim JH, Kim JJ, Paik SW, Rhee JC, et al. Efficacy of elec-
trolyzed acid water in reprocessing patient-used flexible upper endoscopes:
comparison with 2% alkaline glutaraldehyde. J Gastroenterol Hepatol 2004;
19:897-903.
4. Nelson DB, Jarvis WR, Rutala WA, Foxx-Orenstein AE, Isenberg G, Dash GP, et al.
Multi-society guideline for reprocessing flexible gastrointestinal endoscopes.
Dis Colon Rectum 2004;47:413-20.
5. Vickery K, Pajkos A, Cossart Y. Removal of biofilm from endoscopes:
evaluation of detergent efficiency. Am J Infect Control 2004;32:
170-6.
6. Doherty DE, Falko JM, Lefkovitz N, Rogers J, Fromkes J. Pseudomonas aerugi-
nosa sepsis following retrograde cholangiopancreatography (ERCP). Dig Dis Sci
1982;27:169-70.
7. Allen JI, Allen MO, Olson MM, Gerding DN, Shanholtzer CJ, Meier PB, et al.
Pseudomonas infection of the biliary system resulting from use of a contami-
nated endoscope. Gastroenterology 1987;92:759-63.
8. Classen DC, Jacobson JA, Burke JP, Jacobson JT, Evans RS. Serious Pseudomonas
infections associated with endoscopic retrograde cholangiopancreatography.
Am J Med 1988;84:590-6.
9. Siegman-Igra Y, Isakov A, Inbar G, Cahaner J. Pseudomonas aeruginosa
septicemia following endoscopic retrograde cholangiopancreato-
graphy with a contaminated endoscope. Scand J Infect Dis 1987;19:
527-30.
10. Godiwala T, Andry M, Agrawal N, Ertan A. Consecutive Serratia marcescens
infections following endoscopic retrograde cholangiopancreatography. Gas-
trointest Endosc 1988;34:345-7.
L. Qiu et al. / American Journal of Infection Control 43 (2015) e43-e46
e46

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2015 infeccao endoscopia

  • 1. Clinical case study Investigating the failure of repeated standard cleaning and disinfection of a Pseudomonas aeruginosaeinfected pancreatic and biliary endoscope Lijun Qiu a , Zhihui Zhou b , Qifang Liu a , Yuhua Ni a , Feng Zhao c , Hao Cheng MD d, * a Endoscopy Center, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, P.R. China b Infection Department, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, P.R. China c Clinical Laboratory Department, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, P.R. China d Dermatology and Venerology Department, Sir Run Run Shaw Hospital, School of Medicine, Zhejiang University, Hangzhou, P.R. China Key Words: Pseudomonas aeruginosa Endoscope Disinfection Digestive endoscopy is an important technique for the diagnosis and treatment of digestive system disease. To assure medical safety, a digestive endoscope must be cleaned and disinfected before its use in an operation on the next patient. The most common treatment procedure on a digestive endoscope is high-level disinfection. The potential risk associated with digestive endoscopes is always the focus of endoscopic management in clinical practice. In this study, a polluted pancreatic and biliary endoscope after surgery was cleaned and disinfected multiple times with the standard procedure but still tested positive for Pseudomonas aeruginosa culture, which is very rare and has not been reported in China or abroad. Copyright Ó 2015 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/). Digestive endoscopy is an important technique for the diagnosis and treatment of digestive system disease. Similar to many other high-precision medical devices, a digestive endoscope is a device with a complex structure, special building materials, and reus- ability. To assure medical safety, a digestive endoscope must be cleaned and disinfected before its use in an operation on the next patient. The most common treatment procedure on a digestive endoscope is high-level disinfection. According to current literature reports, digestive endoscopic examinationerelated pathogen spread is caused by the following: incompliance of the guidelines for endoscope cleaning and disinfection procedure; use of a defective device; or biofilm formation on endoscope tubes leading to failure of the cleaning and disinfection. The potential risk asso- ciated with digestive endoscopes is always the focus of endoscopic management in clinical practice. In this study, a polluted pancreatic and biliary endoscope after surgery was cleaned and disinfected multiple times with the standard procedure but still tested positive for Pseudomonas aeruginosa culture, which has never been reported in China or abroad. CASE REPORT Case 1 An 82-year-old man was admitted to the hospital because of epigastric pain for 2 days. The physical examination results showed a temperature of 36.8C, pulse of 96 beats per minute, respiration of 18 breaths per minute, blood pressure (BP) of 102/60 mm Hg, complete blood count (CBC) of 17.9 109 /L, no clear yellow stain or bleeding spot on the systemic skin mucous membrane, no enlargement for either cervical or supraclavicular lymph nodes, positive Murphy sign, soft abdomen, and active bowel sounds. Abdominal B ultrasound suggested acute cholecystitis, calculus incarcerated in the neck of the gallbladder, multiple gallbladder stones, and the upper section with common bile duct stones accompanied by extrahepatic biliary dilatation. The patient was diagnosed with acute obstructive suppurative cholangitis and was given emergent endoscopic retrograde cholangiopancreatography (ERCP) and endoscopic retrograde biliary drainage. The patient started to have a fever on day 3 after the surgery, with a maximum * Address correspondence to Hao Cheng, MD, 3 Qingchun East Rd, 310016 Hangzhou, Zhejiang Province, China. E-mail address: hz_chenghao@126.com (H. Cheng). Funding/Support: Supported by the Medical Science Research Foundation of Zhejiang Province (grant no. 2010KYA112). Conflicts of interest: None to report. Contents lists available at ScienceDirect American Journal of Infection Control journal homepage: www.ajicjournal.org American Journal of Infection Control 0196-6553/Copyright Ó 2015 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). http://dx.doi.org/10.1016/j.ajic.2015.04.204 American Journal of Infection Control 43 (2015) e43-e46
  • 2. body temperature of 39C. Bile culture for P aeruginosa tested positive. Blood culture for both Klebsiella pneumoniae and Escher- ichia coli also tested positive. Case 2 An 80-year-old man was previously admitted to the hospital in January when he was 79 because his skin and sclera turned yellow accompanied with weight loss. The physical examination results showed a temperature of 36.7C, a pulse of 70 beats per minute, respiration of 18 breaths per minute, BP of 106/58 mm Hg, and CBC of 3.5 109 /L. The sclera and systemic skin clearly exhibited a yellow stain. The superficial lymph nodes, heart, and lungs were normal. The abdomen was soft without tenderness or rebound pain. The Murphy sign was negative, and bowel sounds were normal. An upper abdominal noncontrast enhanced computed to- mography scan and magnetic resonance cholangiopancreatography showed a widespread expansion of the intra- and extrahepatic bile duct, a common bile duct obstruction, and a dilated pancreatic duct. In addition, the ultrasound result from another facility suggested the following: a low echo occupied the low part of the common bile duct; cancer; chronic schistosomiasis; dilatation in the common bile duct, intrahepatic bile duct, and main pancreatic duct; multiple gallbladder stones; biliary sludge; and a filled spleen. The patient was diagnosed with common bile duct obstruction and possible pancreatic head cancer or ampullary cancer. The patient was given ERCP, endoscopic sphincterotomy, and endoscopic biliary stent implantation (2 days after the previous patient). The patient developed a fever on day 2 after the surgery, with a maximum body temperature of 39.2C. Bile culture of P aeruginosa tested positive. Blood culture of both K pneumoniae and E coli tested positive. Case 3 A 40-year-old man was admitted to the hospital because of recurrent fever and abdominal pain for 20 days and exacerbated conditions for 4 days. The physical examination showed the following: temperature of 37.5C, pulse of 98 beats per minute, respiration of 19 breaths per minute, BP of 91/53 mm Hg, and CBC of 12.0 109 /L. No skin superficial lymph node enlargement was observed. The abdomen was soft without intestinal or gastric peristalsis. The left lower abdomen showed tenderness without rebound pain or muscle tension. The Murphy sign was negative, and bowel sounds were normal. The patient was given an auxiliary examination of the abdomen and Bartholin, Urethral, and Skene glands; the result showed multiple small stones in the gallbladder, cholecystitis, hepatic adipose infiltration, and a lower left abdom- inal cystic mass with possible abscess. High-sensitivity C-reactive protein tested at 81.7 mg/L. The patient was diagnosed with gall- bladder stones and common bile duct stones. ERCP was performed to remove the stones, and nasobiliary drainage was given (3 days after the ERCP operation on the previous patient). This patient developed a fever on day 4 after the surgery, with a maximum body temperature of 39C. Bile culture of P aeruginosa tested positive. Blood culture tested negative. Treatment and monitoring of endoscope Preventive monitoring and investigation on multidrug-resistant bacteria infection by the department of infectious disease discov- ered that the infection of 3 patients occurred after ERCP surgery. The entire process of ERCP in the endoscopy center was investigated immediately. The procedures, including patient documentation, operation environment, the device, and endoscopic-related equipment, were inspected. Compliance with the cleaning and disinfection technical standard for endoscope operations, such as the rinse of the lifting clamp channel of the pancreatic and biliary endoscope and infection control chain inside the hospital, was also investigated. The results revealed that the same pancreatic and biliary endoscope was used in operations on the 3 patients sequentially. This pancreatic and biliary endoscope was suspended immediately, and biologic inspection was performed on the device. Bacteria culture of P aeruginosa tested positive. Pulsed-field gel electrophoresis revealed a high homology between the P aeruginosa from the endoscope and those from the 3 patients (Fig 1.). This endoscope was again cleaned and disinfected in compliance with the standard protocol followed by a biologic inspection. The P aer- uginosa culture still tested positive. This endoscope was cleaned and disinfected using the standard procedure for a third and fourth time. In addition, various high-level disinfectants were used in the im- mersion disinfection process, including 2% glutaraldehyde, o-Phthalaldehyde (made in China), o-Phthalaldehyde (imported), and 24% glutaraldehyde (imported). Biologic inspection was carried out again after each disinfection procedure, and the P aeruginosa culture still tested positive. The endoscope was cleaned with the standard procedure for the fifth time and soaked in 2% glutaralde- hyde for 13 hours to sterilize. Biologic inspection was performed again and the P aeruginosa culture still tested positive, but the colony count decreased by 50% when compared with the previous samples. The endoscope was sent to the Olympus endoscopic repair station at Shanghai, China. After being sterilized with epoxyethane, the entire endoscopic channel of the endoscope was dismantled and sent to the Laboratoire Biotech-Germande (Marseille, France) for exami- nation. Microbiologic analysis was performed on the sample retrieved from the 4 tubes of the endoscope, and the report showed that the level of polymorphic nonpathogenic bacteria was higher than the allowed interference level in the standard guideline rec- ommended by the hospital Committee of Technical Infection. The endoscope was cleaned and disinfected with a standard procedure and stored for 24 hours. Samples taken from the endoscope still tested positive with polymorphic nonpathogenic bacteria. In addi- tion, the number of bacteria at the biopsy-suction tube and lifting clamp tube was higher than the allowed interference level in the standard guideline recommended by the hospital Committee of Technical Infection. Measurement of the protein and total organic carbon contents excluded the possible existence of bacterial biofilm in the various tubes. In the end, the repair center replaced the in- ternal tubes of the endoscope on dismantlement of various com- ponents. The endoscope was then cleaned and disinfected with the standard protocol at the hospital endoscopy center and sent for biologic inspection. The bacteria culture this time was negative after 2 tests. DISCUSSION The completeness of endoscope cleaning and disinfection is crucial for medical safety and is highly regarded by hospital and endoscope management staff nationwide. The Chinese Department of Health published Guidelines for Cleaning and Disinfecting Endo- scopes (2004 version), in which rule 34 in chapter 5 stated that after cleaning and disinfecting with the standard procedure, gastroin- testinal endoscopy, pancreatic and biliary endoscope require a quarterly biologic inspection. In our hospital a standard precleaning, cleaning, and disinfection of the endoscope is managed under World Gastroenterology Organization (WGO/OMGE)-Organization Mon- diale de Gastroenterologie (OMGE)/the World Organization of Digestive Endoscopy (OMED) Practice Guideline Endoscope Disinfec- tion (2005 version). Considering the narrow lifting clamp tube and complex structure of the pancreatic and biliary endoscope, it is harder to clean and disinfect than other endoscopes. Since 2011, L. Qiu et al. / American Journal of Infection Control 43 (2015) e43-e46 e44
  • 3. the endoscopy center of our hospital has adopted a policy that biologic inspections for pancreatic and biliary endoscope be per- formed every 4 weeks based on the recommendation from the Gastroenterological Society of Australia in Guidelines Infection Control in Endoscopy (3rd ed). In this report, a pancreatic and biliary endoscope in our hospital was used in an ERCP operation on a patient with bile duct infection. After standard cleaning and disin- fection, the endoscope was used for ERCP operations on another 2 patients and resulted in the P aeruginosa infection of these 2 pa- tients. Even though a previous study reported that the probability of pathogen spread during endoscopic examination operation was 1 in 1.8 million,1 some other studies have suggested that with the compliance of infection control guidelines, the endoscope prepared for patients still showed a 2% bacterial infection rate.2 The infection risk was hard to evaluate for various reasons. The blood culture and bile culture of the 3 patients reported in this study were not completely the same, which suggested a potential source of endogenous infection. However, the 3 cases showed a surprisingly similar bile culture result and bacteria homology, which indicated the relevance between the P aeruginosa infection and the endoscope used in the process. The standard cleaning and disinfection pro- cedures on the endoscope plus a standard cleaning and sterilizing procedure were performed, but the biologic inspection result still came back positive for P aeruginosa. However, the biofilm tested negative. The bacteria culture tested negative until the endoscope was dismantled and replaced with new internal tubes. All the 3 patients were under the treatment with antibiotics before and after the endoscopic examination for cholecystitis and were given naso- biliary drainage. Therefore, no special treatment for P aeruginosa infection was given. Case patients 1 and 3 recovered afterward. Case patient 2 went to a local hospital for further treatment after the infection was under control. The failed cleaning and disinfection for this endoscope might be the result of the following. P aeruginosa could have developed a resistance to disinfectants, especially aldehyde disinfectants. Even though no direct evidence was found in this study, a previous study suggested that atypical mycobacteria showed complete resistance to glutaraldehyde.3 Also, this endoscope was used for 6 years, and its inner tubes might have been damaged and left with a rough or uneven surface and cracks. During the ERCP operation on patients with bile duct infection, bacteria easily accumulated in the irregular connections, cracks, or ruptures of the internal channel surface and were hard to clean up.4 The final explanation is formation of biofilm. Biofilms consist of substrates from different types of bacteria and extracellular polysaccharides secreted by the bacteria that are attached to the surface of the endoscope. With the growth of bac- teria in the biofilm-covered channels, even though the standard cleaning and disinfection procedure is executed, the damaged channel with bacteria attached would potentially prevent the disinfectant from killing the bacteria. The infecting bacteria in this study were P aeruginosa, which is a typical biologic organism that can easily develop biofilms. In addition, this type of biofilm is very difficult to remove from the channel components and damaged endoscopic tubes, therefore increasing the infection risk to the next patient even after a standard cleaning and disinfection procedure. The examination of the biofilm was based on stochastic selection of the remaining samples for endoscopic biologic inspection, which indicated the possibility of missed detections. Therefore, even though no biofilm was detected during the biologic inspection process in this study, it was still difficult to exclude the possibility of biofilm formation. It is necessary to improve the standard cleaning and disinfection methods for P aeruginosaeinfected endoscopes. For example, an automatic endoscope washer with an ultrasonic oscillation function and the application of detergent with good biofilm removing efficiency could more effectively remove the attached bacteria.5 In this case, cross-infection and in-hospital infection could be reduced, and medical safety could eventually be assured. Fig 1. Pulsed-field gel electrophoresis revealed a high homology between the Pseu- domonas aeruginosa from the endoscope (307) and those from the bile cultures of the 3 patients (309, 310, 305). L. Qiu et al. / American Journal of Infection Control 43 (2015) e43-e46 e45
  • 4. CONCLUSION ERCP is the endoscopic operation with the highest postsurgical infection rate.6-10 According to the endoscopic treatment experi- ences of the authors of this report, after an endoscopic examination or treatment was performed on a patient with a high infection risk, a biologic inspection after the standard cleaning and disinfection of the endoscope is very critical. It is recommended to perform an immediate bacteria culture after any endoscopic operation on a patient with a suspected bile duct infection. In addition, biologic inspection is still necessary even after cleaning and disinfection. The endoscope should only be used again on the confirmation of a negative bacteria culture result. References 1. Srinivasan A. Epidemiology and prevention of infections related to endoscopy. Curr Infect Dis Rep 2003;5:467-72. 2. Ishino Y, Ido K, Sugano K. Improvement of the automatic endoscopic reproc- essor: self-cleaning disinfecting connectors between endoscope and reproc- essor. Endoscopy 2003;35:469-71. 3. Lee JH, Rhee PL, Kim JH, Kim JJ, Paik SW, Rhee JC, et al. Efficacy of elec- trolyzed acid water in reprocessing patient-used flexible upper endoscopes: comparison with 2% alkaline glutaraldehyde. J Gastroenterol Hepatol 2004; 19:897-903. 4. Nelson DB, Jarvis WR, Rutala WA, Foxx-Orenstein AE, Isenberg G, Dash GP, et al. Multi-society guideline for reprocessing flexible gastrointestinal endoscopes. Dis Colon Rectum 2004;47:413-20. 5. Vickery K, Pajkos A, Cossart Y. Removal of biofilm from endoscopes: evaluation of detergent efficiency. Am J Infect Control 2004;32: 170-6. 6. Doherty DE, Falko JM, Lefkovitz N, Rogers J, Fromkes J. Pseudomonas aerugi- nosa sepsis following retrograde cholangiopancreatography (ERCP). Dig Dis Sci 1982;27:169-70. 7. Allen JI, Allen MO, Olson MM, Gerding DN, Shanholtzer CJ, Meier PB, et al. Pseudomonas infection of the biliary system resulting from use of a contami- nated endoscope. Gastroenterology 1987;92:759-63. 8. Classen DC, Jacobson JA, Burke JP, Jacobson JT, Evans RS. Serious Pseudomonas infections associated with endoscopic retrograde cholangiopancreatography. Am J Med 1988;84:590-6. 9. Siegman-Igra Y, Isakov A, Inbar G, Cahaner J. Pseudomonas aeruginosa septicemia following endoscopic retrograde cholangiopancreato- graphy with a contaminated endoscope. Scand J Infect Dis 1987;19: 527-30. 10. Godiwala T, Andry M, Agrawal N, Ertan A. Consecutive Serratia marcescens infections following endoscopic retrograde cholangiopancreatography. Gas- trointest Endosc 1988;34:345-7. L. Qiu et al. / American Journal of Infection Control 43 (2015) e43-e46 e46