April 3, 2014 — In the June, 2001, issue of Infection Control and Hospital Epidemiology (“ICHE”), Sorin et al. (2001) reported that during a three-month period in 1998 as many as eighteen patients at a Flushing, New York, hospital were potentially infected or colonized with imipenem-resistant Pseudomonas aeruginosa (“IRPA”) following bronchoscopy.[1]

Imipemen is a carbapenem antibiotic to which superbugs, such as carbapenem-resistant Enterobacteriaceae (“CRE”), have developed a recent resistance. Click here to read more about the association of superbug infections and gastrointestinal (GI) endoscopy.

Three of these patients displayed clinical and radiographic evidence of infection requiring specific anti-pseudomonas therapy. One patient reportedly died as a result of this IRPA outbreak.[1]

An accompanying editorial discussing lessons to be learned from outbreaks associated with bronchoscopy was published in this same ICHE issue, in 2001.[2]

Several crucial infection control issues were addressed in Sorin et al.’s (2001) report. For example, these authors reported that the instructions provided by the manufacturer of an automated endoscope reprocessor (AER) were not always consistent with the bronchoscope manufacturers’ reprocessing instructions.

Moreover, Sorin et al. (2001) found that different brands of bronchoscopes connected differently to the AER, which could be a source of confusion for an inadequately trained staff member.

Due to the discrepancies in these reprocessing instructions, hospital staffers were reported to have improperly connected bronchoscopes to the AER, resulting in inadequate disinfection and disease transmission.

Unless specific precautions are taken, such as thorough review of the reprocessing instructions provided by both the AER and bronchoscope manufacturers to identify and resolve any inconsistencies, most endoscope and AER models would appear to be susceptible to this same type of confusion and user error.

As a result of their findings, Sorin et al. (2001) provide a number of recommendations when an AER is used to reprocess a bronchoscope (or other type of endoscope).[1]  These recommendations, which are intended to reduce the likelihood of user error, include:

  • color-coding the appropriate connectors for each endoscope manufacturer;
  • providing additional in-service training that highlights differences in the reprocessing instructions provided by different endoscope and AER manufacturers;  and
  • if feasible, purchasing and using endoscopes from one manufacturer.

A published reply

Responding to the report of this IRPA outbreak,[1] Muscarella (2002) wrote a reply,[3a] published one year later in the July, 2002, issue of ICHE, that discussed several implications of Sorin et al.’s (2001) investigation.

For instance, if as these authors conclude this IRPA outbreak was associated with improper connection of bronchoscopes to an AER, then their report has significant infection control implications applicable not only to reprocessing (both automated and manual) bronchoscopes but also GI endoscopes.

Featuring two valves and as many as four or five internal channels, each of which typically requires proper connection to an AER for adequate irrigation and complete disinfection, GI endoscopes are considerably more complex in design than bronchoscopes, which feature only a single channel and one (suction) valve.

Reports such as Sorin et al.’s (2001) that link patient infection to improper connection by staff of an AER to a bronchoscope would seem to raise concern that, due to their many more channels, connectors, and advanced complex internal design, GI endoscopes are particularly at risk for the type of user error and reprocessing mishap described by Sorin et al. (2001).

In addition, Sorin et al. (2001) reported that neither the source of the IRPA nor a patient-to-patient route of transmission was identified during their outbreak investigation.[1] Indeed, determination of both are crucial to the resolution of any outbreak and to the development and implementation of apt corrective actions necessary to prevent the outbreak’s recurrence.

Because Sorin et al. (2001) identified neither, the possibility remains that the environment (not necessarily a patient) was a source of this outbreak’s IRPA, prompting Muscarella (2002) reasonably to ask in a reply whether the IRPA could have originated from a wet surface within the hospital’s environment and have been transmitted to patients via the bronchoscope.[3a,4]

To be sure, several other outbreak investigations have associated P. aeruginosa infection with contaminated environmental surfaces within the healthcare setting, including the internal components of an AER, bronchoscopes, GI endoscopes, tap water, faucets and water taps, and wash basins.[5-18]

Sidebar:  One report by Kotsanas et al. (2013) describe an investigation that identified the likely source of a CRE outbreak in an intensive care unit (ICU) to be contaminated sinks.  Three clinical isolates of the CRE’s outbreak strain (i.e., Serratia marcescens that produces carbapenemases) were indistinguishable or closely related to four environmental isolates sampled from the grates and drains of several hand-washing sinks located in the ICU.

According to Kotsanas et al. (2013), first, CRE can be “hardy” environmental organisms that develop and grow in biofilms; and, second, their findings demonstrate the key role that bacterial contamination of the environment can play in the transmission of CRE in the healthcare setting.

Similarly, Starlander and Melhus (2012) reported that during a period of seven months, four patients in a neurosurgical ICU became infected or colonized by a multi-drug resistant strain of K. pneumoniae. The investigation revealed that the source of this outbreak was a contaminated sink. This outbreak was successfully controlled, in part, by replacing the sink and its plumbing.

And, Walsh and colleagues (2011) identified NDM-1-positive bacteria in samples of drinking water and waste seepage in Asia. In short, therefore, the type of CRE recently confirmed to be responsible for an outbreak at a hospital near Chicago, IL, in 2013 following ERCP — click here to read more about this outbreak — is not exclusively a patient-borne bacterium.

If the route of disease transmission reported by Sorin et al. (2001) were indeed patient-to-patient, then their conclusion that improper connection of the bronchoscope to an AER resulted in inadequate disinfection and patient infection certainly seems plausible and valid.

However, if instead the environment were the source of the IRPA, then Sorin et al.’s (2001) conclusion would be incomplete and potentially incorrect, and the IRPA outbreak they describe might have occurred even if hospital staff had properly connected the bronchoscope to the AER.[3a,4]

Endoscopes that are properly connected to an AER but terminally rinsed with contaminated water, inadequately dried before storage, or improperly handled before reuse can become re-contaminated with environmental organisms and transmit disease to the patient during endoscopy.

Therefore, it is important that outbreak investigations such as Sorin et al.’s (2001) that appear to lack the necessary data to conclude that an infected or colonized patient was the source of bacterial infections following endoscopy consider the possibility that bacteria from an environmental site within the hospital setting were transmitted to the patient via the endoscope.

Rebuttal to a reply 

In response to Muscarella’s (2002) reply,[3a] Segal-Maurer (one of the co-authors of the Sorin et al. [2001] report[1]) wrote a rebuttal that challenged Muscarella’s (2002) suggestion that the rinse water or some other environmental factor(s) unrelated to improper connection of the AER to the bronchoscope may have contributed to or have been the source of Sorin et al.’s (2001) reported IRPA outbreak.[3b]

As a result of this organism’s displayed resistance to the antibiotic imipenem,[1] Segal-Maurer concluded that the source of the IRPA outbreak could not have been the environment, but rather had to be an infected or colonized patient.

Dr. Segal-Maurer wrote:

Foremost, Dr. Muscarella fails to recognize an important infection control principle regarding antibiotic-resistant P. aeruginosa. It is widely recognized that such antibiotic-resistant organisms are not found in the general water supply (and thus distinguished from the usual P. aeruginosa found in tap water). IRPA is an organism exclusively associated with the presence of nosocomial infection or colonization.[3b] Dr. Segal-Maurer.

Dr. Segal-Maurer added that:

There are numerous reports in the literature of P. aeruginosa in the water supply leading to contamination or infection. These are all antibiotic-susceptible strains. The author (referring to Dr. Muscarella) needs to substantiate scientifically his implication that IRPA may be found in the general water supply.[3b] Dr. Segal-Maurer.

Alas, but are these comments indisputably correct?

Literature review 

The suggestion to substantiate scientifically the claim that IRPA can be found in the environment seemed worthy of investigation.  Therefore, the medical literature was reviewed to respond to and place in better perspective the significance of Sorin et al.’s (2001) report,[1,2] Muscarella’s reply,[3a] and Segal-Maurer’s rebuttal.[3b]

Several reports that discuss outbreaks of P. aeruginosa in critical care areas of the hospital unrelated to endoscopy were reviewed, although emphasis was placed on identifying reports that discuss P. aeruginosa outbreaks in the endoscopic setting.

This review investigated not only the antibiotic profile and source of the P. aeruginosa but also measures that effectively ended the reported outbreak.  Emphasis was also placed on reviewing investigations of outbreaks caused by strains of P. aeruginosa resistant to antibiotics, specifically imipenem.

In particular, this review investigated whether antibiotic-resistant P. aeruginosa, in general, and IRPA, in particular, are exclusively associated with infection or patient colonization, as suggested by Segal-Maurer,[3b] or whether these strains could also be found on an environmental surface acting as a source, as suggested by Muscarella (2002).[3a]

The results of this review would likely provide critical clinical information important to bacterial outbreak investigations in hospitals and endoscopic settings.

Antibiotic-resistant Pseudomonas in critical care areas

This review of the medical literature provided an interesting finding:  In addition to colonized and infected patients, the environment in critical care areas of a hospital, such as its intensive care unit (ICU), indeed was reported to be an important source of antibiotic-resistant P. aeruginosa.[5-8,13-16]

Several reports in particular discussed strains of P. aeruginosa resistant to several antibiotics although not specifically imipenem.[13-15] In these reports, environmental surfaces, including plumbing systems, sinks, sink and shower drains, and sink outlets in critical care areas of the hospital were determined to be the likely sources of antibiotic-resistant P. aeruginosa.

This review also identified several outbreak investigations that determined that the environment in critical care areas of the hospital was the source of strains of P. aeruginosa specifically resistant to imipenem (IRPA), the antibiotic described in Sorin et al.’s (2001) report.[1]

Environmental surfaces, including plumbing systems, sinks, sink and shower drains, and sink outlets in critical care areas of the hospital can be sources not only of carbapenem-resistant Enterobacteriaceae (CRE), but also of antibiotic-resistant P. aeruginosa. — Lawrence F Muscarella, PhD

For instance, a prospective study reported recovering an epidemic strain of IRPA in the sinks of the rooms of several mechanically ventilated patients in an ICU.[7] These colonized sinks were determined to be sources responsible for patient colonization and infection.

The report hypothesized that the sinks became contaminated with IRPA during the emptying of humidifier traps filled with condensed water, and, once the sinks were colonized, the patients were likely infected with IRPA via contact with healthcare staff’s hands or by equipment that had become contaminated during washing in these sinks.

This report stresses the importance of regularly cleaning and disinfecting sinks, to prevent the transmission of P. aeruginosa from colonized sinks to the patient via healthcare staff’s hands or equipment.

Similarly, a second report discussed an outbreak of IRPA in a neurosurgery ICU.[5] This organism was isolated from sinks and the tap water, which, according to this report, likely was its source. The outbreak ceased only after, among other measures, all of the ICU’s sinks were replaced.

This finding suggests that, in addition to the possibility of a patient-to-patient route of disease transmission, IRPA can be transmitted from the environment to patients via the hands of healthcare staff or nutritional solutions mixed with contaminated tap water. This report concluded that the tap water can play a crucial role in the spread of P. aeruginosa.

And a third report of an investigation of an outbreak of IRPA in an ICU isolated this organism from wash basins, water taps, and the tap water of the rooms of infected patients.[8] This report suggests that the tap water was likely the source of the outbreak and that the patients were probably contaminated with IRPA in part when crushed drugs suspended in tap water were administered to patients through gastric tubes.

The outbreak was terminated after weekly pasteurization of the ICU’s water taps (as well as use of sterile water for patients’ drugs and food).

Antibiotic-resistant Pseudomonas in the endoscopic setting

This review of the literature also yielded reports that discuss the antibiotic profile and source of P. aeruginosa associated with patient infection or colonization in the endoscopic setting, specifically following bronchoscopy and GI endoscopy.

The findings of these reports were similar to those in critical care areas of the hospital. In particular, several outbreak reports cite tap water or another environmental site in the endoscopic setting as the source of antibiotic-resistant (and -susceptible) P. aeruginosa.

Tap water or another environmental site in the endoscopic setting has been identified as the source of antibiotic-resistant (and -susceptible) P. aeruginosa. — Lawrence F Muscarella, PhD

For instance, one report investigated an outbreak following bronchoscopy that was caused by a resistant strain of P. aeruginosa.[10] After reprocessing, two bronchoscopes were found to be contaminated with P. aeruginosa (although with an antibiotic-susceptible strain).  This finding suggested a failure in the reprocessing of the facility’s bronchoscopes. An AER, which had not been maintained since its installation, was used to reprocess the bronchoscopes.

Although extensive environmental sampling failed to identify the outbreak’s exact source, the authors conclude that the source of the P. aeruginosa was the colonized AER, which during reprocessing re-contaminated bronchoscopes. The return of two bronchoscopes to their supplier for servicing and the replacement of several of the AER’s internal components were required to stop this outbreak.

The authors stress the importance of training, better supervision of reprocessing staff, and more frequent servicing and maintenance of AERs to prevent an outbreak.

A second investigation discussed an outbreak that reportedly started in a hospital’s endoscopy unit.[16] A colonoscope, a gastroscope, faucets of wash basins, and water taps were each contaminated with P. aeruginosa resistant to several antibiotics including imipenem. The possible transmission of this organism via the hands of healthcare staff is discussed.

The authors suggest that the faucets and water taps became contaminated and colonized with this organism when residues from drinking glasses were poured into the wash basins and splashed upwards.

The endoscopes were likely contaminated when removed wet from an AER, possibly during handling by staff. The implementation of patient isolation, strict glove usage, improved hand hygiene, drying the reprocessed endoscope before storage, and periodically replacing, cleaning and disinfecting the water taps successfully broke the chain of infection.

A third report investigated an outbreak of P. aeruginosa bacteremia following endoscopic retrograde cholangiopancreatography (“ERCP”).[17] Five epidemic strains of P. aeruginosa were identified.  Microbiologic sampling showed that endoscopes used during ERCP remained contaminated with an epidemic strain of P. aeruginosa after reprocessing in an AER.

One of the five outbreak strains (genotype B), of which there were four clonally related variants that displayed variable antibiotic resistance (more specific antibiotic-resistant data were not provided), was isolated from both the water used by the AER to rinse the endoscopes and the tap water in the endoscopy suite.

This report concluded that P. aeruginosa from the environment was transmitted via contaminated endoscopes to at least some of the bacteremic patients. This outbreak ended only after the ERCP channel and each of the endoscope’s other channels were thoroughly cleaned, disinfected, and terminally dried using 70% alcohol rinse followed by compressed air before storage.

Additionally, two reports that are frequently referenced in the medical literature whenever P. aeruginosa infections following endoscopy are discussed were also reviewed.[9,11]  Both investigated the source of P. aeruginosa infections following ERCP and traced their respective outbreaks to contaminated endoscopes, which were inadequately disinfected and dried by the hospitals’ AERs.

One of these reports cultured heavy colonization of P. aeruginosa from endoscopes as well as the AER’s detergent reservoir, among other sites.[9] P. aeruginosa was presumably transmitted from the AER to patients via the endoscope, which was contaminated during the AER’s terminal water rinse cycle.

In the other report, residual water contaminated with P. aeruginosa remained in the endoscope’s channels after the AER’s terminal water rinse cycle and was transmitted to patients during ERCP.[11] Both outbreaks ended once all of the endoscope’s channels were rinsed with 70% alcohol followed by forced air drying before storage.

In both reports, antibiotic susceptibility testing was performed on the outbreak strain of P. aeruginosa, but neither report published the data revealing the organism’s antibiotic profile.


Revealing an important conclusion with significant clinical implications to outbreak investigations, this literature review found that antibiotic-resistant P. aeruginosa is not exclusive to patient infection or colonization, as some have suggested.[3b]

Several investigations researching the cause of P. aeruginosa outbreaks, in both critical care areas within a hospital and the endoscopic setting, cite the facility’s tap water[5,8,16] and other environmental sites, including water faucets,[16] sinks,[5,7,14,15] an AER,[10] and water taps,[8,16] as the source of antibiotic-resistant P. aeruginosa.[5-17]

As a consequence of this review’s results, it is crucial that investigations of outbreaks caused by antibiotic-resistant  P. aeruginosa consider the environment (as well as other patients) as a potential source. Otherwise, erroneous conclusions about the outbreak’s true cause may be drawn and remedies for its prevention not provided, leading investigator’s astray and allowing the outbreak to spread.

Consider, for example, a bacterial outbreak that occurred in a hospital in Flushing (NY).[1,3a,3b] Investigators at this hospital ruled out the environment as a possible source because the outbreak strain of P. aeruginosa was resistant to the antibiotic imipenem.

As a result, as noted by Muscarella,[3a] the conclusion published by Sorin et al. (2001)[1] and Segal-Maurer (2002),[3b] which ignored the potential contribution of the environment and asserted improper connection of the bronchoscope to the AER by staff was responsible for the outbreak (i.e., cross-infection), may be incomplete.[3a]

In short, it is important to consider environmental surfaces—such as an AER’s internal components,[9,11] its bacterial water filters, and its filtered  rinse water[17]—as potential sources of antibiotic-resistant P. aeruginosa and other types of bacteria.

Also important to consider during an outbreak investigation, environmental surfaces in a healthcare setting can become colonized as a consequence of a bacterial outbreak, possibly from contact with the contaminated hands of healthcare staff.[5,7,16]

Once colonized, these contaminated environmental surfaces can themselves become sources of a second or subsequent outbreak, which can confound investigators and confuse determination of the outbreak’s original source. Specific tests that clarify whether a contaminated environmental surface was the cause or the consequence of a bacterial outbreak are important to perform.

In conclusion, because patients and environmental surfaces can both be sources of antibiotic-resistant P. aeruginosa, it is contraindicated during an outbreak investigation to rely on the antibiotic profile of P. aeruginosa (or another bacterium) to identify or exclude possible sources or causes of an outbreak.

Practices shown to prevent the transmission of P. aeruginosa from the environment to patients include more frequent hand-washing, use of disposable gloves between patient contacts, and regular cleaning and disinfection of sinks, their basins and their taps.[5,7,8] The practice of rinsing the endoscope’s channels terminally with 70% alcohol followed by forced air-drying is recommended to prevent bacterial colonization and transmission during endoscopy.

Manufacturers of flexible endoscopes can also contribute to reducing the risk of disease transmission by designing instruments that more effectively facilitate cleaning, high-level disinfection and drying.

In addition, manufacturers are encouraged to design AERs not only with a reliable filtration system that removes bacteria from the rinse water, but also with an effective auto-disinfection/sterilization cycle that prevents bacterial colonization of the AER’s internal components. Manufacturers are also encouraged to design AERs to facilitate drying of the endoscope using a 70% alcohol rinse followed by forced air.

Frequent review of the instructions and labeling of the endoscope and the AER is also recommended to understand the operation and limitations of both devices. Reconciliation of any apparent reprocessing differences provided by the endoscope and AER manufacturers may be necessary to prevent confusion and healthcare-associated infection.[1]

Inadequate training and supervision of reprocessing staff are of particular concern. A clear understanding by staff of the differences in the internal designs and reprocessing requirements of different endoscope models is crucial. More frequent servicing, repair and maintenance of both endoscopes and AERs may also be necessary to prevent bacterial outbreaks.


1.  Sorin M, Segal-Maurer S, Mariano N, et al. Infect Control Hosp Epidemiol 2001 Jun;22:409-13.

2. Weber DJ, Rutala WA. Infect Control Hosp Epidemiol  2001 Jun;22:403-8.

3a. Muscarella LF. Infect Control Hosp Epidemiol 2002 Jul;23(7):358-60.

3b. Segal-Maurer S. A reply. Infect Control Hosp Epidemiol 2002 Jul;23(7):360.

4. Muscarella LF. Infect Control Hosp Epidemiol 2000 Oct;21(10):628-9.

5. Bert F, Maubec E, et al. J Hosp Infect 1998;39:53-62.

6. Ferroni A, Nguyen L, et al. J Hosp Infect 1998;39:301-7.

7. Berthelot P, Grattard F, Mahul P, et al. Intensive Care Med 2001;27(3):503-12.

8. Bukholm G, Tannaes T, Kjelsberg ABB, et al. Infect Control Hosp Epidemiol 2002;23:441-6.

9. Alvarado C, Stolz SM, Maki DG.  Am J Med 1991 Sept 16;91(suppl 3B):272S-80S.

10. Schelenz S, French G. J Hosp Infect 2000;46:23-30.

11. Allen JI, Allen MO, Olson MM, et al. Gastroenterology 1987;92:759-63.

12. Kelly NM, Fitzgerald MX, Tempany E, et al. Lancet 1982 Sep25;2(8300):688-90.

13. Falkiner FR, Jacoby GA, Keane CT, et al. J Hosp Infect 1982 Sep;3(3):253-61.

14. Levin MH, Olson B, Nathan C, et al. J Clin Pathol 1984 Apr;37(4):424-7.

15. Gillespie TA, Johnson PRE, Notman AW, et al. Clin Microbiol Infect 2000;6:125-30.

16. Pitten FA, Panzig B, Schroder G, et al. J Hosp Infect 2001;47:125-30.

17. Struelens MJ, et al. Am J Med 1993 Nov;95:489-98.

18. Trautmann M, Muchalsky T, Wiedeck H, et al. Infect Control Hosp Epidemiol 2001;22(1):49-52.

19. Walsh TR et al. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: An environmental point prevalence study. Lancet Infect Dis 2011;11:355.

20. Starlander G, Melhus A. Minor outbreak of extended-spectrum β-lactamase-producing Klebsiella pneumoniae in an intensive care unit due to a contaminated sink. J Hosp Infect 2012 Oct;82(2):122-4.

Article by: Lawrence F Muscarella, PhD; posted 4/3/2014; updated 7/11/2016..


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