Serious pseudomonas infections associated with endoscopic retrograde cholangiopancreatography

Serious Pseudomonas Infections Associated with Endoscopic Retrograde Cholangiopancreatography

DAVID C. CLASSEN, M.D. JAY A. JACOBSON, M.D. JOHN P. BURKE, M.D. JULIE T. JACOBSON, M.T., A.S.C.P. R. SCOTT EVANS, Ph.D. Salt Lake City, Utah

From the Division of Infectious Diseases, LDS Hospital, and University of Utah School of Medicine, Salt Lake City, Utah. Requests for reprints should be addressed to Dr. David C. Classen, Division of Infectious Diseases, LDS Hospital, 8th Avenue and C Streets, Salt Lake City, Utah 84143. Manuscript submitted September 23, 1987, and accepted in revised form December 28, 1987.

590

March

1988

The American

Journal

After observing a single case of Pseudomonas aeruginosa bacteremia following endoscopic retrograde cholangiopancreatography (ERCP), six other P. aeruginosa infections that were temporally related to ERCP were retrospectively found over one year (August 1985 through July 1988) at LDS Hospital. In all seven patients, infection developed within five days after an ERCP. Five patients had bacteremia and two had cholangitis. All five of the Pseudomonas isolates available for testing were serotype 010. Cultures from the ERCP endoscope and several other endoscopes also yielded P. aeruginosa serotype 10, as did environmental cultures from equipment used to clean endoscopes. Among 187 ERCPs performed during the outbreak period, no other patient acquired P. aeruginosa infection. Each of the patients in the outbreak received the first scheduled ERCP of the day. The mean duration between the cleaning of the ERCP endoscope and its subsequent use was significantly longer in cases than in matched controls, a factor that may have permitted contaminating organisms to achieve high inocula in the inadequately cleaned endoscope. Epidemic control measures included improved disinfection of endoscopes, ongoing surveillance, and appropriate antimicrobial prophylaxis. This experience suggests that exogenous infection with Pseudomonas is associated with ERCP, that protracted and insidious outbreaks may occur, and that the occurrence of even a single case of Pseudomonas infection after ERCP should stimulate an epidemiologic investigation. Endoscopic examinations using fiberoptic technology have revolutionized the management of gastrointestinal disorders. These procedures permit direct visualization, photography, roentgenography, biopsy, and lesion removal in the esophagus, stomach, duodenum, and colon [l-4]. When performed by experienced physicians, endoscopic procedures are usually safe, well tolerated, and increasingly performed in outpatient settings. Serious complications including viscus perforation and infection are infrequent [5-81. Endoscopic retrograde cholangiopancreatography (ERCP) is one of the most invasive endoscopic procedures and carries added risks of peritonitis, cholangitis, and bacteremia. ERCP involves cannulation and contrast injection of the common bile duct for roentgenographic evaluation of diseases of the biliary tract. However, several reports have revealed a low rate (2 to 8 percent) of infectious complications of ERCP [9- 131. A variety of bacterial species including Pseudomonas aeruginosa has been found in ERCP-associated infections. Moreover, there have been several reports of ERCP-related infections attributed to irregularities in endoscope disinfection [ 14- 161.

of Medicine

Volume

84

ERCP-ASSOCIATED

OF THE

ET AL

strength 2 percent alkaline glutaraldehyde (Cidex) was usually performed only at the end of each day, and not routinely between patients. These procedures had been changed to allow high-level disinfection of endoscopes between patients in accordance with CDC and ASGE guidelines.

Recently, we identified an occult epidemic of seven serious infections due to a single serotype of P. aeruginosa that occurred over a one-year period. Our experience in the context of earlier reports represents recognition of a significant clinical problem with important implications for endoscopists, endoscopic technicians, and hospital infection control personnel. BACKGROUND

INFECTIONS-CLASSEN

MATERIALS

OUTBREAK

Physical Facilities. The site of the outbreak was a 520bed teaching hospital associated with the University of Utah School of Medicine in Salt Lake City, Utah. The endoscopy suite was relocated in August 1985 in a recently completed new hospital wing. The endoscopy suite included a waiting room, four examination rooms (one with roentgenographic equipment), and an endoscope cleaning and storage room. Three nurse technicians and one secretary were employed in the suite in which nearly 4,000 endoscopic procedures were performed each year by a total of IO gastroenterologists. The majority of these procedures were done on outpatients. A total of 13 endoscopes were used in the suite including gastro-, duodeno-, colono-, and sigmoidoscopes. There was one ERCP endoscope (Olympus model JFIT- 10). Four gastroenteroiogists had privileges to perform ERCPs. Disinfection Procedures. All gastrointestinal endoscopes were disinfected according to American Society for Gastrointestinal Endoscopy (ASGE) and Centers for Disease Control (CDC) guidelines for high-level disinfection [ 17,181. Between uses, the endoscopes were cleaned by washing the exterior of the endoscope with 70 percent isopropyl alcohol. The air/water and suction/biopsy channels were all flushed with detergent soap; however, only the biopsy channel was completely brushed on a routine basis. Then the endoscopes were disinfected for at least 30 minutes by soaking for 15 minutes each, first in a I:16 dilution of 2 percent glutaraldehyde and 79 percent phenol (Sporocidin) and finally the endoscopes were soaked in tap water that was changed daily but not between washings. Each lumen of the endoscope was also flushed and soaked with the disinfecting solutions by use of an all-channel lumen irrigator. There were only two all-channel lumen irrigators, one for use with the disinfecting solution and one for use with the tap water. The irrigators were cleaned at the end of each day by washing with tap water. After the soaking process was completed, the exterior was then wiped dry and the endoscope was reused. At the end of each day, endoscopes were again washed and disinfected, the exteriors were dried, and the endoscopes were suspended in a storage cabinet until the next day’s use. Endoscopes were not washed or disinfected again before subsequent use, regardless of the duration since the last use. Endoscopes were not routinely gas sterilized. Each of the three nurse technicians performed the washing and disinfecting procedure. Before August 1985, a more limited endoscope cleaning and disinfection procedure had been used. This procedure involved detergent and tap water washing followed by flushing of the endoscope lumens with 70 percent isopropyl alcohol between patients. High-level disinfection with full

March

AND

METHODS

In July 1986, we detected a case of P. aeruginosa bacteremia in a patient with no apparent risk factors for Pseudomonas infection. Clinical infection occurred within 48 hours after an ERCP that had disclosed no abnormalities. A second ERCP in this patient one week later revealed evidence of severe destructive cholangitis. This prompted us to review the records of all patients that underwent ERCP within the past year and were then subsequently hospitalized. We identified six other patients who had serious P. aeruginosa infections temporally related to ERCP. We then reviewed the records of all patients receiving ERCPs during the last three years (July 1983 through July 1986) for other cases of Pseudomonas infections. We also reviewed the results of all cultures from biliary tract or gallbladder studies during those three years. Because of a suspected common source for the seven cases, we began extensive culturing of possible sources in the endoscopy suite including the endoscope (exterior, nozzles, flushed inner channels), lens cleaning bottles, a water pik used for lumen flushing, glutaraldehyde phenate disinfectant (Sporocidin) and water soaking baths, and the allchannel lumen flushing equipment (syringe, tubing, adapter). Samples were also obtained from ethylene oxide-sterilized endoscopes after various stages of the disinfecting procedure. In additon, specimens were obtained for culture from ERCP endoscopes that had been cleaned, disinfected, and suspended overnight. All cultures were done by flushing of the inner channels of the endoscope with 10 ml of trypticase soy broth. The broth was incubated at 37’C for 24 hours and then plated on blood and MacConkey agar plates. Isolated organisms were identified using Micro Scan Plates (American Hospital Supply Corp.). Antimicrobial susceptibilities were determined with minimal inhibitory concentration (MIC) sensitivity plates (American Hospital Supply Corp.). Serotyping of P. aeruginosa isolates was done in the Hospital Infections Laboratory, CDC. Statistical evaluation was done using the Student t test (two-tailed). RESULTS Clinical Features of the Cases. The outbreak occurred over the period August 1985 through July 1986 (Figure 1). For the investigation, a case was defined as P. aeruginosa bacteremia or cholangitis within 10 days of ERCP without any other apparent source for P. aeruginosa. Seven patients had serious Pseudomonas infections within one week after an ERCP (Table I). Five patients had P. aeruginosa isolated from blood cultures and three had P. aeruginosa isolated from biliary tract specimens collected at operation (one patient had Pseudomonas isolated from both blood and biliary sources). All five bacteremic pa-

1988

The

American

Journal

of Medicine

Volume

84

591

ERCP-ASSOCIATED

INFECTIONS-CLASSEN

ET AL

Number 3 of Cases 2 1 0

JJASONDJFYAYJJASOND Figure 1. Occurrence of P. aeruginosa infections following ERCP by month 1985 through 1986.

Month

receive an ERCP that day. Three patients were the first of two cases and one patient was the first of three cases. All five patients who had ERCPs on the same day as those of the infected cases were found to have abnormal findings, but a review of the records of these five cases showed no evidence of any serious complications after their ERCPs. Of 167 ERCPs performed during the outbreak year, 127 ERCPs were the first and only cases; 40 ERCPs were done as either the second or third case of the day. However, the P. aeruginosa infection rate was not statistically different in first cases versus second or third cases. A review of personnel associated with each infected case revealed no clear relation between a particular physician or technician and the cases. One physician had three cases, one had two cases, and two physicians had one case each. Intervals Between Uses of ERCP Endoscopes. The relation between the scheduling of ERCP procedures and the occurrence of P. aeruginosa infection suggested the possible importance of long storage times of ERCP endoscopes between disinfection of the instrument and its next use. Therefore, we attempted to determine the number of hours that had elapsed from disinfection to that of the use of the endoscope in each of the seven infected cases (taking into account weekends and frequent weekdays with no use of the ERCP endoscope). Six of the seven patients underwent ERCP with an endoscope that had not been disinfected in more than 48 hours, and only one patient underwent ERCPwith an endoscope that had been disinfected within 24 hours (Table II). The mean interval before ERCP endoscope use in the infected cases was 85.7 hours versus 45.6 hours in all 120 noninfected first cases of the day over the 12 months of the outbreak (p < 0.05). Relation of Cases to Biliary Tract Cultures. We reviewed the results of all cultures from biliary tract sources done at our hospital over the last three years (July 1983 through July 1986). Cultures were obtained from the gallbladder or biliary tract in approximately 30 percent of all biliary tract-related operations. During the outbreak year, a total of 130 cultures from the biliary tract were

tients had a positive blood culture result obtained within 72 hours after an ERCP. Six patients had one or more biliary tract abnormalities detected by ERCP. The findings included common duct stones (Patients 4 and 5), malignant stricture (Patient l), benign stricture (Patient 7), extrahepatic obstruction (Patient 2), and severe pancreatitis/pseudocyst (Patient 3). Five patients had fever to 39.5’C within 24 hours after the procedure and six underwent a definitive drainage procedure within one week after the ERCP. Four patients had operative procedures and two patients underwent percutaneous transhepatic drainage. Six patients had received prophylactic antimicrobial drugs before the ERCP. However, none of the patients received an agent with activity against P. aeruginosa. All seven patients were hospitalized within five days after ERCP at our hospital and were treated with appropriate antibiotic therapy when the cultures became positive. However, five of the seven patients subsequently died (two died within four weeks after the ERCP). The other two patients experienced long hospitalizations. In one of the five, mortality appeared to be directly related to the ERCP-associated infection. In addition, two of the surviving patients had morbidity directly related to their infection. A review of the patient records of the other 160 ERCPs done during the outbreak year (July 1985 to August 1986) revealed only four patients with a positive culture of biliary tract or gallbladder. No patient was found to have bacteremia. Organisms included Escherichia coli, Klebsiella, and enterococci. All four patients received drainage procedures and survived. Daily Schedule of ERCP. ERCPs were performed five days a week with zero to three procedures scheduled each day. ERCPs were scheduled as the first endoscopic procedures of the day and all ERCPs were completed before any other procedures were undertaken in the endoscopy suite. Review of the daily schedule of ERCPs showed that each of the seven patients in whom serious Pseudomonas infections developed had been either the first or the only patient to have an ERCP performed that day. Three of the seven patients were the only ones to

592

March

1988

The American

Journal

of Medicine

Volume

84

ERCP-ASSOCIATED

done among 400 biliary tract operations. Approximately 53 percent of these culture results were positive; frequent isolates included E. coli, Klebsiella species, streptococci, and anaerobes. P. aeruginosa accounted for 4.2 percent (three of 70) of all positive biliary cultures and occurred only in patients who had undergone ERCP. There were 290 cultures obtained from gallbladder or biliary tract sources over the two years before the outbreak; 124 cultures were positive, but no culture was positive for P. aeruginosa. Cultures of Endoscopes. All the endoscopes were contaminated with multiple organisms (Table III). The most frequently recovered organism was P. aeruginosa, but other species including E. coli, Klebsiella, Serratia, and Staphylococcus epidermidis were also found. In addition, we subjected an ERCP endoscope to ethylene oxide sterilization, then subjected it to the routine cleaning and disinfection procedure. This endoscope was culture-negative but, after overnight storage, a repeat culture from it was positive for P. aeruginosa. Cultures of Disinfection Equipment. All cultures obtained from equipment used in the cleaning and disinfection process were positive for P. aeruginosa except the disinfecting bath (Sporocidin) (Table Ill). P. aeruginosa was not the only contaminating organism found; Serratia and E. coli were also isolated. The water storage bottle used to flush the endoscope lens during the ERCP procedure was also contaminated with P. aeruginosa. Serotyping of Isolates. All P. aeruginosa isolates obtained from clinical and envrionmental sources had similar antimicrobial susceptibilities both by disk testing and broth dilution testing. However, recoverable isolates from five of the patients and all the environmental sources were available for sterotyping. The isolates from all five patients as well as the ERCP endoscope, the tap water basin, and the lens bottle were all serotype 010. P. aeruginosa serotype 04 was also isolated but from the tap water basin only. Control Measures. We instituted several measures to control the outbreak. The measures were targeted toward more effective methods for decontamination of endoscopes and other endoscopy suite equipment, developing a system for ongoing random culturing of endoscopes and other endoscopy equipment to detect contamination, and ongoing surveillance of biliary cultures of patients undergoing post-ERCP surgical drainage procedures. We also recommended antibiotic prophylaxis in high-risk ERCP patients to include coverage for P. aeruginosa. Specifically, we instituted daily sterilization of lens cleaner storage bottles, flushing of the all-channel irrigator apparatus with glutaraldehyde phenate disinfectant (Sporocidin) between patients, addition of chlorine (200 parts per million) to the tap water bath, and frequent (three times daily) changing of the tap water bath. We also instituted alcohol flushing of all endoscopes prior to compressed air drying to ensure

TABLE I

Diagnosis Biliary obstruction Ascending cholangitis Pancreatitisi pseudocyst Cholelithiasis Biliary obstruction Ascending cholangitis Biliary stricture

2 3 4 5 6 7

ET AL

Relevant Features of Seven Cases of P. aeruginosa Infection Following ERCP

Patient

1

INFECTIONS-CLASSEN

TABLE II

Source

Isolate

Outcome

Blood

P. aeruginosa

Death

Blood, bile duct Bile duct

P. aeruginosa

Death

P. aeruginosa

Alive

Gallbladder Blood

P. aeruginosa P. aeruginosa

Alive Death

Blood

P. aeruginosa

Death

Blood

P. aeruginosa

Death

interval of Time Between Disinfection and Subsequent Use of the ERCP Endoscope in the Outbreak Cases

PallentNumber

Time(hours)

1

30 66 160 56 72 74 142 85.7 45.6

2 3 4 5 6 7 Case mean Control mean *Two-tailed

Student

TABLE III

t test.

Organisms Isolated from Equipment Environmental Cultures Equipment

EndoscoQes ERCP endoscope Sigmoidoscope Gastroscope Colonoscope 1 Colonoscope

p <0.05*

2

and

Isolate

P. aeruginosa P. aeruginosa P. aeruginosa P. aeruginosa S. epidermidis Klebsiella pneumonia, Serratia marcescens

Disinfecting equipment Sporocidin Tap water All-channel Endoscope

wash basin basin water irrigator syringe lens cleaner bottle

None P. aeruginosa P. aeruginosa P. aeruginosa

complete drying of all endoscopic inner channels to prevent retained moisture that might allow for bacterial survival and growth. Subsequently, we have not detected a single case of P. aeruginosa infection among more than 200 patients undergoing ERCP.

March 1988

The American Journal of Medicine

Volume 84

593

ERCP-ASSOCIATED

INFECTIONS-CLASSEN

ET AL

identified. The hospital infection control system at our hospital utilizes computer-directed surveillance [25]. This system is used by a cadre of infection control practitioners. However, most procedures, including ERCP, were not routinely entered into the data base of this computerized surveillance system and, therefore, a link between ERCP and the P. aeruginosa infections was not made. In addition, the P. aeruginosa infections also escaped detection because the monthly and yearly percentages of bacteremias caused by P. aeruginosa were not significantly different in the outbreak period versus the previous year. Overall, the rate of P. aeruginosa bacteremia was 8.4 percent (nine of 107) of all bacteremias in the outbreak year versus 6.4 percent (five of 81) of all bacteremias in the previous year, which is not significantly different. However, in the two years before the outbreak, there was not a single positive culture for P. aeruginosa for bile cultures, yet in the outbreak year there were three positive cultures from bile. Although not statistically significant, this difference could have suggested a problem. Therefore, without the awareness of a clinical association between ERCP and P. aeruginosa infections, a serious outbreak can occur that might escape attention even with a vigilant infection control system. Although the current report appears to be the longest and most serious ERCP-related outbreak, it does not represent the first association of P. aeruginosa with ERCP. Bilbao et al [I l] speculated on the relation of ERCPassociated infection to endogenous flora and did recognize that P. aeruginosa was a common contaminant of ERCP endoscopes. However, they did not suspect it to be a potential pathogen. Low et al [ 121, in a prospective assessment of infectious complications of ERCP in 10 1 consecutive patients, found P. aeruginosa in 14 of 101 common bile duct aspirates just after duct injection, but accompanying blood culture results in all patients were negative. Although P. aeruginosa was not isolated from environmental cultures, it was thought to originate from the tap water used to clean the endoscopes. In 198 1, Doherty et al [ 141 reported the first case of P. aeruginosa bacteremia closely associated with a contaminated endoscope. Unfortunately, the isolate was not serotyped. In 1983, a prospective evaluation of infectious complications of ERCP was performed by Dutta et al [ 131 in which only three patients had a positive blood culture after an ERCP but none was positive for P. aeruginosa. Two outbreaks were reported in the British literature by Cryan et al [ 151 and by Earnshaw et al [ 161. Both reported P. aeruginosa bacteremia traced to ERCP endoscopes, with three cases in the former and five cases in the latter study. The problems were resolved when endoscope disinfection procedures were improved. Both studies pointed to P. aeruginosa serotype 010 as the agent. Finally, Vennes [8] at the University of Minnesota de-

COMMENTS

Fiberoptic endoscopy has become an increasingly common medical procedure, often performed in outpatient settings. Although infectious complications are unusual, contaminated endoscopes have been the sources for nosocomial transmission of bacterial agents including Pseudomonas, Klebsiella, Serratia, Salmonella, and Mycobacterium tuberculosis [7,8,1 g-211. In recognition of these risks, rigorous guidelines have been established for cleaning and disinfecting endoscopes. Transient bacteremia may also occur in 2 to 8 percent of all gastrointestinal endoscopies but usually without serious complications [5,8,22,23]. ERCP has rapidly become a standard technique since its introduction in 1968. More than 10,000 procedures were performed in 1985 in the United States alone, most in outpatients. Infectious complications are not as well described in relation to ERCP as to other forms of gastrointestinal endoscopy. Bilbao et al [ 1 l] reviewed complications in more than 10,000 ERCPs. Complications were seen only with successful cannulation of the common bile duct. The overall complication rate was quite low (3 percent). Complications included pancreatitis, cholangitis, drug reactions, pseudocyst, and instrumental injury. Death occurred in 0.2 percent, with infection as the major cause. The major infectious complication, cholangitis, was seen in fewer than 1 percent and bacteremia was seen in fewer than 2 percent [l I]. The lower rate of infectious complications with ERCP was thought to be related to the smaller and more flexible nature of the ERCP endoscope, which could cause less abrasion and injury to mucosa. When infectious complications occur, the responsible microorganisms have usually been those of the gastrointestinal tract, i.e., E. coli, Klebsiella, streptococci, and anaerobes [24]. Although infectious complications of ERCP are rare, our outbreak illustrates that these infections can be devastating. Furthermore, the current outbreak emphasizes three important features of ERCP-associated infections: first, a serious and insidious outbreak occurred over a year-long period and escaped early detection; second, P. aeruginosa serotype 0 IO appears to be an important nosocomial pathogen in high-risk ERCP patients; and third, the concurrence of multiple factors precipitated the outbreak. The index case in our outbreak was discovered almost one year after the occurrence of the first case. The apparent random distribution of cases over the year and our lack of appreciation of an association between ERCP and serious P. aeruginosa infections contributed to the occult nature of this outbreak. The endoscopists had attributed the P. aeruginosa infections in each case to other potential nosocomial sources related to inpatient hospitalization, although in no case was another source 594

March

1988

The American

Journal

of Medicine

Volume

84

ERCP-ASSOCIATED

scribed an outbreak of serious P. aeruginosa infections related to a contaminated ERCP endoscope associated with the use of a new automated device for endoscope washing. P. aeurginosa serotype 0 10 was implicated. The outbreak resolved with improved cleaning procedures, specifically improved drying of endoscope inner channels PI. Limited information exists to permit correlation of serotypes of P. aeruginosa with epidemiologic features or virulence factors. However, P. aeruginosa serotype 010 probably shares the capacity of all Pseudomonas strains to survive and grow in water and to develop resistance to some disinfectants [27]. The organism persisted in our endoscopy suite for at least one year. The ERCP endoscope contains many difficult-to-clean channels that may have acted as a moist potential reservoir in which the organism could multiply. We discovered another Pseudomonas serotype (04) on our endoscopes and yet it did not cause disease in our outbreak. Obviously, serotype 0 IO can cause serious disease in high-risk patients, but it is not yet clear if this serotype has any increased virulence or particular capacity to multiply in environmental reservoirs. Although the persistently contaminated ERCP endoscope offered the potential for a much larger outbreak, we cannot explain the wide dispersion of cases given the fact that about half of all ERCPs performed at our hospital reveal markedly altered biliary tract anatomy that should have placed those patients at high risk for infectious complications. Therefore, it is likely that each case resulted from the combined effects of multiple factors rather than a single definable cause. There were also multiple reasons for contamination of the endoscopes: persistently moist inner lumen channels, persistently contaminated tap water bath, contaminated all-channel irrigators, and finally a contaminated lens cleaner system. The lens cleaner bottle and the all-channel irrigators were sources for long-term contamination with P. aeruginosa. Another evident problem was the method by which endoscopes were cleaned at the end of each day. All endoscopes contain inner channels that are difficult to completely clean and dry, and some channels cannot be mechanically brushed and thus may harbor organic debris. The ERCP endoscope (Olympus JFIT-IO) contains three channels: the suction/biopsy, air/water, and elevator cable channels. The first two channels can both be completely flushed but only the suction/biopsy channel can be mechanically brushed throughout its length. The elevator cable channel is partially blinded and thus cannot be flushed or brushed adequately. Each of the patients in whom P. aeruginosa infection developed was the first patient of the day to undergo ERCP. It seems likely that some channels of the ERCP endoscope were not completely dry and that overnight or extended storage allowed the contaminating P. aeruginMarch

INFECTIONS-CLASSEN

ET AL

osa to multiply to a high inoculum. This situation would only exist for the first patient of the day and when the inoculum could have been diluted by the subsequent washing. Indeed, we established this possible sequence by determining that a cleaned and disinfected culturenegative endoscope was culture-positive after overnight storage. Thus, the incompletely dried endoscope may have allowed low inocula of Pseudomonas that survived disinfection to multiply during overnight storage. Allen et al [26] have also suggested this possibiity by finding that the critical step in disinfection may be the complete drying of the endoscope after washing. Another possible reason for the timing of our outbreak may have been the changes made in the cleaning and disinfection procedure. Paradoxically, the month of the first case in our epidemic, a more rigorous endoscope cleaning procedure had been adopted in accordance with guidelines of the CDC and ASGE. These procedures involved high-level disinfection between patients. The new procedures included cleaning of the endoscope at the end of each day with a solution of a 1: 16 dilution of 2 percent glutaraldehyde and 79 percent phenol (Sporocidin), which is a less concentrated disinfectant than the full-strength 2 percent alkalinized glutaraldehyde (Cidex) that was used previously. Although full-strength Cidex is more concentrated than the solution of Sporocidin used, many consider them to be equally efficacious when used properly for high-level disinfection [28,29]. However, full-strength Cidex is potentially more irritating to personnel and patients and therefore less attractive as a disinfectant. In summary, our outbreak in the context of serious recent outbreaks should emphasize the importance of this clinical problem not only as a serious and often occult nosocomially transmitted infection but also as a warning to all those involved in endoscopy that continued vigilance is necessary to recognize this problem and to prevent its occurrence. Clearly, the mere observation of disinfection procedures is not adequate to prevent this problem from occurring. This experience should serve to emphasize an important clinical association. As intravenous drug abuse and puncture wounds of the foot are associated with Pseudomonas osteomyelitis of the clavicle and heel, respectively, ERCP is associated with serious P. aeruginosa infections of the biliary tract and bacteremia. Moreover, the occurrence of even a single case of P. aeruginosa infection following ERCP should lead to an epidemiologic investigation. ACKNOWLEDGMENT

We are indebted to Lane Stevens, B.S., Elaine Hillas, B.S., M.T., Carol Ross, L.P.N., and Sharon Smith, A.S., for help in preparation of this document. We can also wish to thank Shelley Woodmansee, L.P.N., for help in obtaining cultures from the endoscopy suite and Anita Highsmith, MS., Hospital Infections Branch, CDC, Atlanta, Georgia, for Pseudomonas serotyping. 1988

The American

Journal

of Medicine

Volume

84

595

ERCP-ASSOCIATED

INFECTIONS-CLASSEN

ET AL

REFERENCES

4. 5.

6.

7.

8. 9.

10. 11.

12.

13.

14.

15.

596

Colcher H: Current concepts: gastrointestinal endoscopy. N Engl J Med 1975; 293: 1129-1131. Katen RM, Smith FW: Pandendoscopy in early diagnosis of acute upper gastrointestinal bleeding. Gastroenterology 1973; 65: 726-734. Gibb SP, Tarshis A: Diagnostic endoscopy of the upper gastrointestinal tract. Current Concepts of Gastroenterol0gy 1982; 7: 3-7. Forrest JA, Finlayson NDC, Shearman DJC: Endoscopy in gastrointestinal bleeding. Lancet 1974; II: 394-397. Silver SE, Nebel 0, Rogers G, Sugawa L, Mendeston P: Endoscopic complications: results of a 1974 American Society for Gastrointestinal Endoscopy survey. JAMA 1976; 235: 926-930. Shorum PJ, Eykyn SJ, Cotton PB: Gastrointestinal instrumentation, bacteremia and endocarditis. Gut 1963; 24: 1078-1093. Colin-Jones DG, Cockel R, Schiller KFR: Current endoscopic practice in the United Kingdom. Clin Gastroenterol 1986; 7: 775-786. Vennes JA: Infectious complications of gastrointestinal endoscopy. Dig Dis Sci 1961; 26 (July suppl):6OS-64s. Kasugai T, Kino N, Kobashis H: Endoscopic pancreatography l&l 1. Gastroenterology 1972; 63: 217-234. lngelfinger FJ: Endoscopic pancreatocholangiography: progress and problem. N Engl J Med 1972; 287: 879-660. Bilbao MK, Dotter CT, Lee TG, Katon RM: Complications of endoscopic retrograde cholangiopancreatography (ERCP): a study of 10,000 cases. Gastroenterology 1976; 70: 3 14-320. Low DE, Micflikier AB, Kennedy JK, Striver HG: Infectious complications of endoscopic retrograde cholangiopancreatography: a prospective assessment. Arch Intern Med 1980; 140: 1076-1077. Dutta SK, Cox M, Williams RB, Eisenstat TE, Standiform HC: Prospective evaluation of the risk of bacteremia and the role of antibiotics in ERCP. J Clin Gastroenterol 1963; 5: 325-329. Doherty DE, Falko JM, Lefkovitz N, Rogers J, Fromkes J: Pseudomonas aeruginosa sepsis following retrograde cholangiopancreatography. Dig Dis Sciences 1962; 27:169-170. Cryan EM, Falkiner FR, Mulvihill TE, Keane CT, Keeling PWN: Pseudomonas aeruginosa cross infection following endoscopic retrograde cholangiopancreatography. J Hosp Infect 1964; 5: 371-376.

March

1966

The American

Journal

of Medicine

Volume

16.

17.

18.

19.

20.

21.

22. 23.

24.

25.

26.

27.

28.

29.

64

Earnshaw JJ, Clark AW, Thon BT: Outbreak of Pseudomonas aeruginosa following endoscopic retrograde cholangiopancreatography. J Hosp Infect 1965; 6: 95-97. Simmons BP, Hooton TM, Mallison GF, et al: Cleaning, disinfection, and sterilization of hospital equipment: guidelines for the prevention and control of nosocomial infections. Centers for Disease Control, July 1962. Ad Hoc Committee on Infection Control in the Handling of Endoscopic Equipment: Guidelines for cleaning and disinfection of flexible fiberoptic endoscopes used in gastrointestinal endoscopy. AORN J 1976; 26: 907-910. Hawkey PM, Davies AJ, Viant AC, Lush CJ, Mortensen NJ: Contamination of endoscopes by Salmonella species. J Hosp Infect 1961;,2: 373-376. Bond WW, Moncada RE: Viral hepatitis B infection risk in flexible fiberoptic endoscopy. Gastrointest Endosc 1976; 24: 225-230. Webb SF, Vail-Spinosa A: Outbreak of Serratia marcescens associated with flexible fiberoptic bronchoscope. Chest 1974; 68: 703-708. Libermann TR: Bacteremia and fiberoptic endoscopy. Gastrointest Endosc 1976; 23: 36-37. Everett ED, Hirschmann JV: Transient bacteremia and endocarditis prophylaxis. A review. Medicine (Baltimore) 1977; 56: 61-77. Claesson BE: Microflora of the gallbladder related to duration of acute cholecystitis. Surg Gynecol Obstet 1966; 102: 531-535. Evans RS, Larsen RA, Burke JP, et al: Computer surveillance of hospital-acquired infections and antibiotic use. JAMA 1966; 256: 1007-1011. Allen JI, Allen MO, Olson MM, et al: Pseudomonas infection of the biliary system resulting from use of a contaminated endoscope. Gastroenterology 1967; 92: 759-763. Vasil ML: Pseudomonas aeruginosa: biology, mechanisms of virulence, epidemiology. J Pediatr 1966; 106: 600805. Matteucci DJ, Organ CH, Dykstra M, Zalasney B, Jenkens H: Efficacy of a simplified lower gastrointestinal flexible endoscope cleaning method. Dis Colon Rectum 1965; 26: 653-657. Favero MS: Sterilization, disinfection and antisepsis in the hospital. In: Lennette EH, Balows A, Hausler WJ, Shadomy HJ, eds. Manual of clinical microbiology, 4th ed. Washington: American Society of Microbiology, 1965; 129-138.