Download Re-evaluating endoscopy-associated infection risk

American Journal of Infection Control 41 (2013) 734-6
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American Journal of Infection Control
American Journal of
Infection Control
journal homepage: www.ajicjournal.org
Commentary
Re-evaluating endoscopy-associated infection risk estimates and their
implications
Cori L. Ofstead MSPH a, *, Alexandra M. Dirlam Langlay PhD a, Natalie J. Mueller MPH a,
Pritish K. Tosh MD b, Harry P. Wetzler MD, MSPH a
a
b
Ofstead & Associates, Inc, Saint Paul, MN
Division of Infectious Diseases, Mayo Clinic, Rochester, MN
According to the Centers for Disease Control and Prevention
(CDC), approximately 11 million gastrointestinal endoscopies are
performed annually in the United States.1,2 The 2008 CDC/Healthcare Infection Control Practices Advisory Committee (HICPAC)
Guideline for Disinfection and Sterilization in Healthcare Facilities
states that contaminated endoscopes have been linked to more
health care-associated infections than any other medical device.3
Paradoxically, several guideline-issuing organizations assert that
the risk of endoscopy-associated infection (EAI) is only 1 in 1.8
million procedures.3-6
Recent audits have documented widespread lapses in infection
control involving medical equipment.7-11 Inspections of multiple
facilities determined that certain endoscopy equipment was not
properly reprocessed for up to several years.8,11-15 Direct observation in a multisite study revealed that endoscopes were virtually
never reprocessed in accordance with guidelines.7 The implications
of these lapses are unknown because no epidemiologic studies
have determined the risk of EAI associated with reprocessing
quality.
Research was conducted to evaluate the origins and accuracy of
the risk estimates after a single outbreak involved more cases of EAI
than would be expected in 1 year nationwide.15,16 This article
describes the methodology used to estimate risk and discusses the
patient safety implications of relying on the statistics appearing in
guidelines.
EVALUATING THE ORIGINS OF CURRENT EAI RISK ESTIMATES
How risk was calculated
The EAI risk estimate of “1 in 1.8 million procedures” first
appeared in a 1993 Technology Assessment Position Paper by the
American Society for Gastrointestinal Endoscopy (ASGE).17 ASGE
authors calculated risk by dividing a subset of EAIs (28) in the
* Address correspondence to Cori L. Ofstead, MSPH, Ofstead & Associates, Inc, 400
Selby Avenue, Suite V, Blair Arcade West, Saint Paul, MN 55102-4520.
E-mail address: [email protected] (C.L. Ofstead).
Conflicts of interest: None to report.
United States from 1988 to 1992 reported in 1 review article18 by
an estimated number of gastrointestinal endoscopies performed
during that time (40 million).17 This estimate is erroneous in part
because of mathematical errors (28 cases in 40 million procedures
represents a risk of 1 in 1.4 million procedures). There were also
substantially more transmission events documented in the review
than selected by the ASGE authors (145 rather than 28).18 When all
145 cases are used, the risk estimate is 1 in 276,000da 6-fold
increase over the stated risk.
In terms of the denominator for this calculation, there are large
discrepancies in the reported number of procedures performed
in the United States. For example, ASGE asserts that 34 million
gastrointestinal endoscopies are done annually,19 compared with
20 million stated in the 2011 Multisociety Guideline on Reprocessing
Flexible Gastrointestinal Endoscopes,4 11 million estimated using
CDC data,1,2 and 5 million reported in the CDC/HICPAC Guideline.3
Recent government data suggest that 11 million to 22 million
procedures are performed annually.1,2,20 Dividing minimal numbers
of published case reports by high procedural volumes results in very
low EAI risk estimates that are neither reliable nor representative
of actual infection risk.
Problems inherent in relying on published case reports
Recently, ASGE cited a 2006 article that used the same methodology to estimate an EAI risk of 1 in 10 million procedures
(35 EAIs in 340 million procedures).19,21 Although the newer risk
estimate suggests a considerable decrease in EAIs since the first
estimate was published in 1993, this method of estimating risk is
highly prone to reporting bias.22 This estimate likely exemplifies
decreasing numbers of published case reports rather than actual
reduction in risk. As an analogy, if case reports published in peerreviewed journals were used to determine risk of penicillinresistant Staphylococcus aureus infection during the last decade,
the risk would be almost zero. S aureus was universally penicillin
susceptible until the 1950s, when case reports of penicillin-resistant
S aureus were first published. By the 1970s, penicillin-resistant S
aureus was so prevalent that it was considered commonplace, and
case reports were rarely published.
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C.L. Ofstead et al. / American Journal of Infection Control 41 (2013) 734-6
At present, there is no incentive for practitioners to report EAIs
or other adverse events. A recent study found that complications
associated with outpatient endoscopy were rarely reported by
physicians.23 The authors of the original review cited by ASGE
stated that the cases included in their paper probably represented
only a small fraction of actual EAIs because reported incidents
frequently involved large outbreaks or unusual clusters of cases,
and most were due to bacterial infections that were easy to
recognize and had brief incubation periods.18 Because of the
substantial reporting bias, using published case reports to calculate
EAI risk is not methodologically sound.
REPROCESSING LAPSES AND ASSOCIATED OUTCOMES
Discordance between stated EAI risks and observed complications
Nearly all EAIs have resulted from failure to adequately clean
and disinfect endoscopes.4,6 Recent reports indicate reprocessing
lapses are ongoing and widespread.7,8,10,11 Although outcomes
of reprocessing lapses have been described on a case-by-case
basis,15,16,18,24 to our knowledge no epidemiologic data exist.
However, 3 recent studies have examined postendoscopy complications, with incidence rates ranging from 0.5% to 3.4%.23,25,26
Complications included fever, diarrhea, abdominal pain, and
other signs and symptoms that may indicate infection.23 These
findings suggest that the risk of EAI may be substantially higher
than current estimates. Furthermore, it is reasonable to assume
that the infection risk is greater when lapses occur than when
there is rigorous adherence to reprocessing protocols. For example, contaminated duodenoscopes have been associated with
outbreaks of multiple microorganisms, including Klebsiella pneumoniae carbapenemase-producing organisms, with multidrugresistant organism (MDRO) attack rates ranging from 8% to 41%
of exposed patients.15,16,27,28
Improper focus on bloodborne virus transmission
When reprocessing lapses are documented, patients are often
told there is little to no risk and no need for testing or followup.14,29,30 In rare instances when exposed patients are tested for
infections, institutions typically choose to test only for viral infections, such as HIV and hepatitis B and C, which are unlikely to be
transmitted by an endoscope.12,31-33 The focus on viral transmission
is improper because these viruses are less prevalent in the population,34-37 have shorter survival times outside the body,34,38,39
and are easier to kill with standard disinfectants3,38 than bacterial
pathogens, such as Clostridium difficile. Endoscopes are exposed to
very high numbers of enteric microbes during each procedure,3 and
Alfa et al found viable bacteria or fungi on 14% of patient-ready
endoscopes.40
Transmission and subsequent colonization with MDROs and
other enteric pathogens through a fecally contaminated endoscope
have not been assessed. Most MDROs become colonizers in the
gastrointestinal tract before causing infection elsewhere in the
body.41 As such, transmission and subsequent colonization are
clinically unapparent but of high consequence. Because the
gastrointestinal tract is a reservoir for pathogens, transmission of
MDROs between patients through a contaminated endoscope is not
only feasible but potentially quite common depending on the
colonization status of prior endoscopy patients, the quality of
reprocessing, and the degree of disruption of normal flora caused
by pre-endoscopy bowel preparation. The frequency of MDRO
colonization following endoscopy needs to be studied to accurately
evaluate risk and reframe the clinical consequences of improperly
reprocessed endoscopes.
735
CONCLUSION
Evidence indicates that current EAI risk estimates are inaccurate, outdated, based on flawed methodology, and can have
profound effects on patients. These extremely low risk estimates
are used to justify the lack of reporting, routine monitoring, patient
notification, and laboratory testing following a lapse. In 1993,
researchers recommended prospective studies involving both
patient monitoring and laboratory cultures be conducted to evaluate the risk of transmitting infections via contaminated endoscopes.18 Today, there remains a need for epidemiologic studies to
accurately estimate the risk of EAI and other complications.
Prospective studies should involve observation of reprocessing
practices, microbial testing, and outcomes assessment. The results
could be used to develop criteria for patient notification and
reporting of reprocessing lapses and assist decision makers in
determining what actions to take when a lapse occurs.
Acknowledgments
The authors thank Jeremy Ward for his thoughtful comments
and assistance editing this manuscript.
References
1. Centers for Disease Control and Prevention. National Hospital Discharge
Survey: 2009 table, procedures by selected patient characteristics. Available
from: http://www.cdc.gov/nchs/fastats/insurg.htm. Accessed June 15, 2012.
2. Cullen KA, Hall MJ, Golosinskiy A. Ambulatory surgery in the United States,
2006. Natl Health Stat Rep 2009;11:1-25.
3. Rutala WA, Weber DJ. In: Healthcare Infection Control Practices Advisory
Committee (HICPAC). Guideline for disinfection and sterilization in healthcare
facilities, Vol 2012. Washington [DC]: Department of Health and Human
Services; 2008.
4. Petersen BT, Chennat J, Cohen J, Cotton PB, Greenwald DA, Kowalski TE, et al.
Multisociety guideline on reprocessing flexible GI endoscopes: 2011. Infect
Control Hosp Epidemiol 2011;32:527-37.
5. ASGE Standards of Practice Committee, Banerjee S, Shen B, Nelson DB,
Lichtenstein DR, Baron TH, et al. Infection control during GI endoscopy. Gastrointest Endosc 2008;67:781-90.
6. Society of Gastroenterology Nurses and Associates Inc. SGNA Standards:
Standards of infection control in reprocessing of flexible gastrointestinal
endoscopes. Gastroenterol Nurs 2010;33:70-80.
7. Ofstead CL, Wetzler HP, Snyder AK, Horton RA. Endoscope reprocessing
methods: a prospective study on the impact of human factors and automation.
Gastroenterol Nurs 2010;33:304-11.
8. Schaefer MK, Jhung M, Dahl M, Schillie S, Simpson C, Llata E, et al. Infection
control assessment of ambulatory surgical centers. JAMA 2010;303:2273-9.
9. Tosh PK, Disbot M, Duffy JM, Boom ML, Heseltine G, Srinivasan A, et al.
Outbreak of Pseudomonas aeruginosa surgical site infections after arthroscopic
procedures: Texas, 2009. Infect Control Hosp Epidemiol 2011;32:1179-86.
10. VA Office of Inspector General. Follow-up colonoscope reprocessing at VA
medical facilities. Washington [DC]: Department of Veterans Affairs; 2009.
11. VA Office of Inspector General. Use and reprocessing of flexible fiberoptic
endoscopes at VA medical facilities. Washington [DC]: Department of Veterans
Affairs; 2009.
12. Holodniy M, Oda G, Schirmer PL, et al. Results from a large-scale epidemiologic
look-back investigation of improperly reprocessed endoscopy equipment.
Infect Control Hosp Epidemiol 2012;33:649-56.
13. New Jersey Ambulatory Surgery Center and Surgical Practice Transparency
Report. Pennington [NJ]: New Jersey Health Care Quality Institute; 2011. p. 35.
14. Ochsner Medical Center. Jefferson Highway Endoscopy Lab audit shows small
number of endoscopes did not complete high level disinfection process. New
Orleans [LA]: Ochsner Health System; April 19, 2011.
15. Sanderson R, Braithwaite L, Ball L, Ragan P, Eisenstein L. An outbreak of
carbapenem-resistant Klebsiella pneumoniae infections associated with endoscopic retrograde cholangiopancreatography (ERCP) procedures at a hospital.
Am J Infect Control 2010;38:e141.
16. DePasquale JM, Endimimani A, Forero S, Roberts D, Fiorella P, Pickens N, et al.
Outbreak of carbapenem-resistant Klebsiella pneumoniae infections in a longterm acute care hospital-Florida, 2008. 58th Annual EIS Conference. Atlanta
[GA]: CDC; 2009.
17. Kimmery MB, Burnett DA, Carr-Locke DL, DiMarino AJ, Jensen DM, Katon R,
et al. ASGE Technology assessment position paper: transmission of infection by
gastrointestinal endoscopy. Gastrointest Endosc 1993;39:885-8.
18. Spach DH, Silverstein FE, Stamm WE. Transmission of infection by gastrointestinal endoscopy and bronchoscopy. Ann Intern Med 1993;118:117-28.
736
C.L. Ofstead et al. / American Journal of Infection Control 41 (2013) 734-6
19. American Society for Gastrointestinal Endoscopy. Endoscope reprocessing and
infection control. 2010. Available from: http://www.asge.org/press/press.aspx?
id¼6858. Accessed May 23, 2012.
20. Sonnenberg A, Amorosi SL, Lacey MJ, Lieberman DA. Patterns of endoscopy in
the United States: analysis of data from the Centers for Medicare and Medicaid
Services and the National Endoscopic Database. Gastrointest Endosc 2008;67:
489-96.
21. Nelson DB, Muscarella LF. Current issues in endoscope reprocessing and
infection control during gastrointestinal endoscopy. World J Gastroenterol
2006;12:3953-64.
22. McGauran N, Wieseler B, Kreis J, Schuler YB, Kolsch H, Kaiser T. Reporting bias
in medical research: a narrative review. Trials 2010;11:37.
23. Leffler DA, Kheraj R, Garud S, Neeman N, Nathanson LA, Kelly CP, et al. The
incidence and cost of unexpected hospital use after scheduled outpatient
endoscopy. Arch Intern Med 2010;170:1752-7.
24. Nelson DB. Infectious disease complications of GI endoscopy: part II, exogenous
infections. Gastrointest Endosc 2003;57:695-711.
25. Quintero E, Castells A, Bujanda L, Cubiella J, Salas D, Lanas Á, et al. Colonoscopy
versus fecal immunochemical testing in colorectal cancer screening. N Engl J Med
2012;366:697-706.
26. Azrak MF, Huang Y-lA, Howard DH, Tangka F, Warren J, Klabunde C, et al. The
utilization and complication rates of outpatient colonoscopy performed at
ambulatory surgical centers versus hospitals 1992-2007. Chicago [IL]: Digestive
Disease Week; 2011.
27. Aumeran C, Poincloux L, Souweine B, Robin F, Laurichesse H, Baud O, et al.
Multidrug-resistant Klebsiella pneumoniae outbreak after endoscopic retrograde cholangiopancreatography. Endoscopy 2010;42:895-9.
28. Carbonne A, Thiolet JM, Fournier S, Fortineau N, Kassis-Chikhani N, Boytchev I,
et al. Control of a multi-hospital outbreak of KPC-producing Klebsiella pneumoniae type 2 in France, September to October 2009. Euro Surveill 2010;15:1-6.
29. Lerner M. HCMC tells 2,600 patients device wasn’t properly disinfected. Star
Tribune; June 22, 2010.
30. The Canadian Press. 9,000 B.C. patients warned of surgical tools. CBC News;
December 8, 2010.
31. Ciancio A, Manzini P, Castagno F, D’Antico S, Reynaudo P, Coucourde L, et al.
Digestive endoscopy is not a major risk factor for transmitting hepatitis C virus.
Ann Intern Med 2005;142:903-9.
32. Barrow B. Ochsner Health System notifies 222 patients of potential errors
sanitizing endoscopes. The Times-Picayune; April 19, 2011.
33. Barrow B. Tulane Medical Center alerts patients after medical gear improperly
sterilized. The Times-Picayune; March 10, 2011.
34. Weber DJ, Rutala WA, Miller MB, Huslage K, Sickbert-Bennett E. Role of hospital
surfaces in the transmission of emerging health care-associated pathogens:
norovirus, Clostridium difficile, and Acinetobacter species. Am J Infect Control
2010;38(5 Suppl 1):S25-33.
35. Cohen SH, Gerding DN, Johnson S, Kelly CP, Loo VG, McDonald LC, et al. Clinical
practice guidelines for Clostridium difficile infection in adults: 2010 update by the
society for healthcare epidemiology of America (SHEA) and the infectious diseases
society of America (IDSA). Infect Control Hosp Epidemiol 2010;31:431-55.
36. Centers for Disease Control and Prevention. HIV/AIDS statistics and surveillance:
basic statistics. Available from: http://www.cdc.gov/hiv/topics/surveillance/
basic.htm. Accessed September 27, 2012.
37. Centers for Disease Control and Prevention. Viral hepatitis statistics & surveillance.
Available from: http://www.cdc.gov/hepatitis/statistics/index.htm. Accessed
September 27, 2012.
38. Hota B. Contamination, disinfection, and cross-colonization: are hospital
surfaces reservoirs for nosocomial infection? Clin Infect Dis 2004;39:1182-9.
39. Kramer A, Schwebke I, Kampf G. How long do nosocomial pathogens persist on
inanimate surfaces? A systematic review. BMC Infect Dis 2006;6:130.
40. Alfa MJ, Sepehri S, Olson N, Wald A. Establishing a clinically relevant bioburden
benchmark: a quality indicator for adequate reprocessing and storage of
flexible gastrointestinal endoscopes. Am J Infect Control 2012;40:233-6.
41. Tosh PK, McDonald LC. Infection control in the multidrug-resistant era: tending
the human microbiome. Clin Infect Dis 2012;54:707-13.