Multiple Clusters of Hepatitis Virus Infections Associated With Anesthesia for Outpatient Endoscopy Procedures

GASTROENTEROLOGY 2010;139:163 170 Multiple Clusters of Hepatitis Virus Infections Associated With Anesthesia for Outpatient Endoscopy Procedures BRUCE GUTELIUS,*, JOSEPH F. PERZ, MONICA M. PARKER, RENEE HALLACK, RACHEL STRICOF, ERNEST J. CLEMENT, YULIN LIN, # GUO-LIANG XIA, # AMADO PUNSALANG, ANTONELLA ERAMO, MARCI LAYTON, and SHARON BALTER *Centers for Disease Control and Prevention, Atlanta, Georgia; New York City Department of Health and Mental Hygiene, New York, New York; Centers for Disease Control and Prevention, Division of Healthcare Quality Promotion, Atlanta, Georgia; New York State Department of Health, Wadsworth Center, Division of Infectious Diseases, Albany, New York; New York State Department of Health, Bureau of Healthcare-Associated Infections, Albany, New York; # Centers for Disease Control and Prevention, Division of Viral Hepatitis, Atlanta, Georgia BACKGROUND & AIMS: Hepatitis B virus (HBV) and hepatitis C virus (HCV) can be transmitted during administration of intravenous anesthesia when medication vials are used for multiple patients using incorrect technique. We investigated an outbreak of acute HBV and HCV infections among patients who received anesthesia during endoscopy procedures from the same anesthesiologist (anesthesiologist 1), in 2 different gastroenterology clinics. METHODS: Chart reviews, patient interviews, clinic site visits and infection control assessments, and molecular sequencing of patient isolates were performed. Patients treated by anesthesiologist 1 on specific procedure days were offered testing for blood-borne pathogens. Endoscopy and anesthesia procedures were reviewed; HCV quasispecies analysis was performed. RE- SULTS: Six cases of outbreak-associated HCV infection and 6 cases of outbreak-associated HBV infection were identified in clinic 1. One outbreak-associated HCV infection was identified in clinic 2. HCV quasispecies sequences from the patients were nearly identical (96.9% 100%) to those from source patients with chronic viral hepatitis. All affected patients in both clinics received propofol from anesthesiologist 1, who inappropriately used a single-patient-use vial of propofol for multiple patients. Reuse of syringes to redose patients, with resulting contamination of medication vials used for subsequent patients, likely resulted in viral transmission. CONCLUSIONS: Twelve persons acquired HBV and HCV infections (6 hepatitis C, 5 hepatitis B, and 1 coinfection) in 2 separate offices as a result of receiving anesthesia from anesthesiologist 1. Gastroenterologists are urged to review carefully the injection, medication handling, and other infection control practices of all staff under their supervision, including providers of anesthesia services. Keywords: Hepatitis; Outbreak; Infection Control. In March 2007, a report was made to the New York City Department of Health and Mental Hygiene (DOHMH) by a patient claiming to have been infected with hepatitis C virus (HCV) as a result of an outpatient procedure. This patient had no other risk factors for infection and had tested negative for HCV antibodies 1 week before an esophagoduodenoscopy performed in 2006. The patient subsequently experienced symptomatic HCV infection diagnosed 3 months after the esophagoduodenoscopy was performed. Given the presentation within the expected incubation period and a documented HCV seroconversion, the DOHMH initiated an investigation to determine whether the infection occurred as a result of medical procedures performed at the physician s office and, if so, to assess modes of transmission, prevent additional transmission, and identify other persons at risk who needed testing. Material and Methods Medical Office Investigation The DOHMH investigated the medical office at which the index patient s procedure had been performed (clinic 1). All staff were interviewed to assess opportunities for hepatitis B virus (HBV) and HCV transmission. Endoscopy procedures, anesthesia practices, and endoscope reprocessing were observed to evaluate infection control. Blood samples were taken from consenting staff and tested for HBV, HCV, and human immunodeficiency virus (HIV). These same methods were used to investigate a second gastroenterologist s office (clinic 2) when the investigation identified a case of HCV infection that appeared to have occurred during a procedure performed there in 2005. Patients were assigned numbers indicating the clinic in which their procedures had been performed and the order in which their procedures were performed. Thus, the index patient is designated as patient 1.7 because a procedure was performed in clinic 1 and was the Abbreviations used in this paper: DOHMH, New York City Department of Health and Mental Hygiene; E1-HVR1, hypervariable region 1 of the E2 gene; HBV, hepatitis B virus; HCV, hepatitis C virus; HIV, human immunodeficiency virus; IV, intravenous. 2010 by the AGA Institute 0016-5085/$36.00 doi:10.1053/j.gastro.2010.03.053

164 GUTELIUS ET AL GASTROENTEROLOGY Vol. 139, No. 1 seventh procedure performed in the clinic during the time frame of interest. Epidemiologic Investigation Patient data from procedure logs of clinic 1 were matched to the DOHMH registry of patients with HBV and HCV infections to identify patients with previously reported HBV or HCV infections who had procedures performed the day before, of, or after the index patient s procedure or that of another case. Procedures were not performed every day in clinic 1; therefore, the procedure days before and after the index patient s occurred during a 6-day period. Procedures were performed on days 1, 5, and 6 during this time. Previously reported HBV and HCV infections were also discovered among patients who had procedures performed on day 6; therefore, the investigation expanded to include day 8. Medical record review was completed for patients who had procedures performed on those days, and an attempt was made to interview and draw blood on all patients. A standardized interview questionnaire was used. The investigation of clinic 1 indicated that incorrect infection control practices by anesthesiologist 1 might have led to blood-borne pathogen transmission. Anesthesiologist 1 worked in New York City during the period of December 1, 2003, to May 1, 2007, exclusively providing care in outpatient clinics. Notification letters were mailed to all 4490 patients who received anesthesia from anesthesiologist 1 at any of the 12 clinics in which anesthesiologist 1 worked during that time. Patients were advised to get tested for HBV, HCV, and HIV. Outbreak-associated HBV and HCV cases were defined as HBV or HCV infection among patients who had received anesthesia from anesthesiologist 1 in New York City during the period of December 1, 2003 to May 1, 2007, and for whom one or more of the following applied: (1) no lifetime history of major HBV or HCV infection risk factors (ie, intravenous [IV] drug use, chronic hemodialysis [ 5 years], receipt of a blood transfusion [before 1972 for HBV or before 1992 for HCV], or organ transplantation), with an initial diagnosis of HBV or HCV infection occurring after receiving anesthesia; (2) documented HBV or HCV seroconversion 6 months after receiving anesthesia, with no major HBV or HCV infection risk factors during that time; or (3) presentation with signs or symptoms of HBV or HCV infection (alanine transaminase 2.5 times upper limit of normal or jaundice) within 2 26 weeks of receiving anesthesia, with no major HBV or HCV risk factors during that time. Cases were defined as confirmed if HCV NS5b region analysis indicated 95% RNA sequence homology with hepatitis C virus, or HBV molecular analysis indicated 95% DNA sequence homology with hepatitis B virus, from at least 1 possible source patient. Cases were defined as probable if a possible source patient had been identified, but HCV RNA or HBV DNA could not be obtained from enough patients because of low viral load or lack of specimen at the time of this investigation. Laboratory Investigation Serologic testing for HBV and HCV was performed by the DOHMH Public Health Laboratory. Serum samples were tested for hepatitis B surface antigen (Abbott Laboratories, Abbott Park, IL), total antibodies to the hepatitis B core antigen (Abbott Laboratories), and antibodies to HCV (Abbott Laboratories). Serum samples that were positive for antibodies to HCV were confirmed with recombinant immunoblot assay testing (3.0 SIA; Chiron Healthcare, Ireland [Distributed by Ortho-Clinical Diagnostics, Raritan, NJ]). Results of serologic or RNA tests performed by licensed clinical laboratories were also accepted. Serum samples from possible source patients and patients with outbreak-associated HCV were sent to the New York State Department of Health Wadsworth Center laboratories for genotyping. Phylogenetic analyses were conducted by using MEGA version 3.1 (Center for Evolutionary Medicine and Informatics, Tempe, AZ). Specimens that demonstrated 95% nucleotide sequence homology were sent to the Centers for Disease Control and Prevention for additional analyses of NS5b sequences and hypervariable region 1 of the E2 gene (E1- HVR1) quasispecies (the population of related HCV variants that occur within HCV-infected individuals). All laboratory investigations were performed using established methods and rigorous quality control procedures, as described previously. 1 5 The E1-HVR1 quasispecies were isolated and amplified by the end-point limiting-dilution real-time polymerase chain reaction assay, and approximately 65 end-point clones (291 nucleotides) were sequenced from each sample. 1 NS5b consensus and E1-HVR1 quasispecies sequences from the patients specimens were compared with each other and with sequences from randomly selected HCV-infected persons from the Third National Health and Nutrition Examination Survey, a representative sample of the noninstitutionalized civilian population of the United States. 2,6 Pair-wise analysis of nucleotides sequences and construction of the phylogenetic tree to evaluate genetic relatedness were performed. 1 Results Medical Office Investigation None of the staff in clinics 1 or 2 had evidence of current hepatitis B or C infection. Endoscopy technique and endoscope reprocessing were correctly performed in both offices. Observation and interview of anesthesiologist 1, who worked in both offices, revealed improper practices including the reuse of a single-patient-use 100-mL vial of propofol for multiple patients. Propofol was drawn into a needleless syringe through a vented

July 2010 HEPATITIS ASSOCIATED WITH ANESTHESIA 165 Figure 1. Suspected mechanism of HBV and HCV transmission. spike and administered through 6 inches of extension tubing attached to an angiocatheter (Figure 1). Anesthesiologist 1 reported that it was possible a second dose of medication could be given to the same patient with the same syringe used to give the first dose. Epidemiologic Investigation: Outbreak- Associated HBV and HCV Infections At clinic 1, a total of 37 (73%) of 51 patients who had had procedures performed on days 1, 5, 6, and 8 agreed to testing for HBV, HCV, and HIV. Six cases of outbreak-associated HCV infection and 6 cases of outbreak-associated HBV infection were identified among 12 of these patients, with all outbreak-associated cases occurring among the 25 patients who had received anesthesia for procedures during investigation days 5 and 6 in 2006 (Table 1). Four of the case-patients clearly had symptomatic infections, which led to their diagnoses (2 HCV patients, 1 HBV patient, and the 1 patient who contracted both HCV and HBV). The other patients had vague symptoms or were diagnosed as a result of liver function test elevations, routine screening, or testing prompted by our investigation. No outbreak-associated cases of HIV infection were identified. Of the 6 outbreak-associated HCV cases in clinic 1, 4 occurred among patients who had procedures performed on investigation day 5, immediately after a patient with chronic HCV infection had undergone a colonoscopy (Table 1). HCV genotype 1b was recovered from the patient with chronic HCV infection, patient 1.3, and from patients 1.5, 1.6, and 1.7 (Table 1). Patient 1.4 had a low viral load at the time of investigation, although previous testing indicated infection with HCV genotype 1b. Patient 1.6 had antibody evidence of chronic HCV exposure dating back to 1998 but had never had a detectable HCV viral load. Approximately 2 months after the procedure on day 5, this patient presented with symptomatic HCV infection and a detectable HCV viral load; quasispecies analysis revealed HCV from the cases was highly genetically related to HCV from the source patient (Figure 2). Two additional outbreak-associated HCV cases at clinic 1 occurred among patients (patients 1.17 and 1.20)

166 GUTELIUS ET AL GASTROENTEROLOGY Vol. 139, No. 1 Table 1. Procedures Performed, Biopsy Equipment Used, and Anesthesia Administered for Patients With Outbreak-Associated Hepatitis B and C in Clinics 1 and 2 Clinic 1 Clinic 2 Day 5: 2006 Day 6: 2006 Day 1: 2005 Patient No. a 1.3 1.4 1.5 1.6 1.7 1.10 1.11 1.12 1.14 1.16 1.17 1.18 1.20 1.25 2.3 2.4 Procedure time 1:30 PM 1:59 PM 2:27 PM 2:43 PM 3:05 PM 3:55 PM 4:32 PM 7:49 AM 8:53 AM 9:41 AM 10:04 AM 10:41 AM 11:17 AM 1:13 PM 9:06 AM 9:34 AM HBV status Neg Neg Neg Neg Neg eag Pos Pos Pos Neg Pos Pos Neg Pos Neg Neg HCV status Chronic Pos Pos Pos Pos Neg Neg Neg Neg Chronic Pos Neg Pos Neg Chronic Pos HCV genotype 1b 1b 1b 1b 1b n/a n/a n/a n/a 1a Unk n/a 1a n/a 1a 1a Case status b Source C C C C Source B B B Source B&C B C B Source C Procedure type Colon Colon EGD EGD EGD Colon EGD Colon Colon Colon Colon Sig Colon EGD Colon Colon Scope number 93 49 63 64 63 93 63 93 L-1 93 49 7 93 64 Unk Unk Biopsy equipment Forceps Snare Forceps Forceps Forceps Forceps Forceps Snare Snare Snare Forceps None Snare Forceps Snare None Propofol Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Pentothal Yes Yes Yes Yes No No No Yes Yes Yes Yes Yes Yes Yes Yes Yes Lidocaine No No No Yes No No Yes No No No No No No Yes No No B, outbreak-associated case of hepatitis B infection; C, outbreak-associated case of hepatitis C infection; Colon, colonoscopy; EGD, esophagogastroduodenoscopy; Sig, sigmoidoscopy; Pos, positive; Neg, negative; Unk, unknown; eag, hepatitis B e antigen positive. a Consecutive patients not listed here tested negative for outbreak-associated hepatitis B and C. b Source, source patient. whose procedures were performed during day 6, after another patient with chronic HCV infection (patient 1.16) had undergone a colonoscopy (Table 1). Patient 1.16 refused to give a blood sample for this investigation but was known to be infected with HCV genotype 1a. HCV genotype 1a was recovered from patient 1.20. Patient 1.17 did not have sufficient viral load for genotype determination. Of the 6 cases of outbreak-associated HBV identified at clinic 1, all occurred on procedure days 5 and 6. Patient 1.10 had a procedure on day 5 and was known to be HBV e antigen positive. The subsequent patient on day 5 and 5 patients on day 6 all had probable outbreak-associated HBV infections. Patient 1.17 was coinfected with HBV and HCV. Open medications, including single-patientdose propofol, were stored overnight and reused the following day in this office; therefore, a single medication vial could have been the source of exposure for patients who had procedures on different days. Table 1 indicates that patients 1.3 1.7 did not all have the same type of procedure performed. Different endoscopes (with different serial numbers) were used for source and case patients who did have the same procedures. Table 1 also demonstrates that the biopsy equipment used was not the same for all patients and that the only anesthesia medication that all of the source and case patients had in common was propofol. Receiving propofol from anesthesiologist 1 during days 5 and 6 was the only common characteristic among all of the source patients and all of the case patients with outbreak-associated HBV or HCV (Table 1). These findings, together with results of HCV genetic testing (see Laboratory Investigation section) and anesthesiologist 1 s report of using single-patient-use vials for multiple patients and possibly reusing syringes for the same patient, prompted us to conduct a broader public health patient notification. Patients tested as part of this effort included 9 patients who had procedures performed in clinic 2 on 1 date ( Day 1 ) in 2005. One case of outbreak-associated HCV infection was identified among these patients in clinic 2 (Table 1; patient 2.4). This patient was infected with HCV genotype 1a and received propofol from anesthesiologist 1 during a colonoscopy performed 30 minutes after a patient with chronic HCV genotype 1a (patient 2.3) had a colonoscopy performed and received propofol from anesthesiologist 1 (Table 1). Patient 2.4 had no lifetime history of major risk factors for HCV infection and had documented HCV seroconversion within 6 months of this procedure. No biopsy was performed for patient 2.4, and there was no evidence that the same endoscope was used for the source patient because all staff reported colonoscopes were rotated between procedures (Table 1). Both patients received propofol and pentothal anesthetic. Individual patients were more commonly redosed with propofol than pentothal, suggesting again that syringe reuse and contamination of

July 2010 HEPATITIS ASSOCIATED WITH ANESTHESIA 167 Figure 2. Phylogenetic consensus tree of hepatitis C virus E1-HVR1 sequences identified from selected Third National Health and Nutrition Examination participants and 4 case patients from clinic 1, days 5 and 6, 2006. a shared propofol vial was a more likely mode of HCV transmission from patient 2.3 to patient 2.4 than either a shared endoscope or biopsy equipment. Laboratory Investigation In clinic 1, serum samples from patients 1.3, 1.5, 1.6, and 1.7 underwent HCV sequence analysis, which classified them as genotype 1b. The NS5b consensus sequences from patients 1.3, 1.5, 1.6, and 1.7 created a distinct phylogenic subcluster (data not shown). Consensus sequences from patients 1.5, 1.6, and 1.7 were identical to one another in the approximately 300-nucleotide region examined and shared 98% nucleotide identity with patient 1.3. Among patients known to be infected with genotype 1a HCV, an NS5b polymerase chain reaction product was obtained for patient 1.20 but could not be compared with HCV from patient 1.16, who refused to give a serum sample. Genetic relatedness of HCV from patients 1.3, 1.5, 1.6, and 1.7 was confirmed by E1-HVR1 quasispecies sequences analysis. The 4 patients had distinct E1-HVR1 quasispecies sequences. These sequences clustered as a group and were significantly different from other genotype 1b quasispecies sequences from Third National Health and Nutrition Examination Survey III participants (P.01; Figure 2). E1-HVR1 nucleotide sequences from patient 1.3 had 99.7% to 100% maximum nucleotide identity to sequences from patients 1.5, 1.6, and 1.7. These results indicated that HCV from these 4 clinic 1 patients was highly genetically related and that patient 1.3 was the source patient for the HCV transmitted on day 5. Molecular sequencing and quasispecies results also confirmed that patient 2.3 was the source for HCV transmitted to patient 2.4. HCV NS5b sequences from patients 2.3 and 2.4 in clinic 2 belonged to genotype 1a and were 98% identical. These patients had E1-HVR1 quasispecies sequences that formed a distinct cluster with 96.9% maximum nucleotide identity (Figure 3). Genetic testing was also attempted for patients with outbreakassociated HBV on days 5 and 6 in clinic 1 but could not be completed because none of the patients had detectable HBV DNA in their serum samples. Discussion Our investigation of a single acute hepatitis C case led to the identification of patient-to-patient transmission of HBV and HCV infections in 2 separate gastroenterology offices. The only common exposure among all infected patients in both offices was receiving propofol from one contract anesthesiologist; incorrect anesthesia practices involved the reuse of syringes and single-patient-dose propofol vials for multiple patients. Multiple patients were identified as infected with HCV strains that were highly genetically related to viruses from chronically infected source patients. Infected patients were not exposed to common endoscopes or biopsy equipment in a

168 GUTELIUS ET AL GASTROENTEROLOGY Vol. 139, No. 1 Figure 3. Phylogenetic consensus tree of hepatitis C virus E1-HVR1 sequences identified from selected Third National Health and Nutrition Examination participants and 2 case patients from clinic 2, day 1, 2005. manner that can explain transmission. In contrast, all infected patients received propofol from a single anesthesiologist, who inappropriately used single-patient-use propofol vials for multiple patients and reported possibly reusing syringes to redose individual patients. This practice can lead to contamination of an entire vial of propofol used for multiple patients and is the most likely cause of HBV and HCV transmission during this outbreak. Our findings are consistent with other investigations of HBV and HCV infection in health care settings. 3 5,7 21 These studies have consistently demonstrated that contamination of anesthesia or other IV medications was far more likely to be responsible for transmission of HBV or HCV than the equipment used in the patients medical procedures. 22 25 Propofol in particular has been cited in previous outbreaks, and efforts are needed to better educate the health care community on the importance of strict adherence to aseptic technique when using it. 26 Our investigation is unique in that it involved 2 separate clusters of transmission in 2 independent gastroenterology offices. If not for the investigation of the index case, which was prompted by a patient s self-report, it is likely that most of the other outbreak associated infections that occurred in the first office would not have been recognized. Likewise, viral transmission in the second medical office would not have been suspected in the absence of the notification letters. These findings highlight the fact that many instances of health care-related HBV and HCV transmission probably go undetected. 25 The true magnitude of this problem is therefore unknown. These findings increase concerns regarding infection control practices and use of shared medication vials for anesthesia administration to multiple patients, especially in outpatient settings, where infection control oversight is limited and procedures such as colonoscopies are increasingly performed. The highest prevalence of HCV infection in the United States is among persons who are now aged 50 59 years, 6 all of whom should currently be receiving screening colonoscopies, an important preventive care practice targeting persons 50 years. Thus, the potential risk for HCV transmission during these procedures will likely increase unless adherence to safe injection practices is consistent. Because most new HCV infections are asymptomatic, these outbreaks are extremely difficult to detect and rely on astute patients and clinicians to detect them. Many more may go undetected. To address this concern, the New York State Department of Health updated its blood-borne pathogen transmission prevention and barrier precautions training, mandatory for licensed health care providers, to include

July 2010 HEPATITIS ASSOCIATED WITH ANESTHESIA 169 provisions related to injection safety. In addition, beginning in 2009, all outpatient practices in New York State that perform procedures involving moderate or deep sedation or general anesthesia will be required to obtain accreditation. 27 Gastroenterologists are urged to carefully review the injection, medication handling, and other infection control practices of all staff under their supervision, including providers of anesthesia services. 28,29 Gastroenterologists should insist on the use of single-patient-use medication vials for anesthesia and strict adherence to infection control guidelines to prevent outbreaks such as the ones we describe. While outbreaks such as this one can happen in any office in which multipatient vials are used, and gastroenterology practices are at risk for such outbreaks, given that colonoscopies are commonly-performed outpatient procedures requiring sedation, clinicians can play a key role in helping to recognize and contain health care-associated viral hepatitis infections. Physicans diagnosing patients with acute viral hepatitis should report these cases to their local health department and carefully consider the role of health care exposures, especially among persons who do not report traditional risk factors for infection. In particular, potential clusters involving 2 or more cases with a common health care procedure during the likely exposure period should immediately be reported to public health authories. Likewise, a single case of acute hepatitis B or C (or documented seroconversion) occurring in a cancer, dialysis, or transplant patient; long-term care resident; or routine blood donor represents a red flag for medical transmission that should be reported. Outbreaks similar to the one described here would not have been possible if intravenous anesthesia medications were not administered from a single vial to multiple patients. For this reason, we advocate eliminating use of all multipatient vials for anesthesia medications to the greatest extent possible and educating clinicians on the risks associated with their use. This can be accomplished by more clearly labeling medications (eg, propofol) as single-patient-use only and improving pricing of unit dose single-patient-use medications to encourage their use. Together, increased education and policies that promote single-patient-use medication vials for IV anesthesia should reduce the risk for health care-associated HBV and HCV transmission. References 1. Ramachandran S, Xia G, Ganova-Raeva LM, et al. Endpoint limiting-dilution real-time PCR assay for evaluation of hepatitis C virus. J Virol Methods 2008;151:217 224. 2. Nainan OV, Alter MJ, Kruszon-Moran D, et al. Hepatitis C virus genotypes and viral concentrations in participants of a general population survey in the United States. Gastroenterology 2006; 131:478 484. 3. Patel PR, Larson KA, Castel AD, et al. Hepatitis C virus infections from a contaminated radiopharmaceutical used in myocardial perfusion studies. JAMA 2006;296:2005 2011. 4. Cody SH, Nainan OV, Garfein RS, et al. Hepatitis C virus transmission from an anesthesiologist to a patient. Arch Intern Med 2002;162:345 350. 5. Thompson ND, Hellinger WC, Kay RS, et al. Healthcare-associated hepatitis C virus transmission among patients in an abdominal organ transplant center. Transpl Infect Dis 2009;11: 324 329. 6. Armstrong GL, Wasley A, Simard EP, et al. The prevalence of hepatitis C virus infection in the United States, 1999 through 2002. Ann Intern Med 2006;144:705 714. 7. Centers for Disease Control and Prevention. Transmission of hepatitis B and C viruses in outpatient settings New York, Oklahoma, and Nebraska, 2000 2002. MMWR Morb Mortal Wkly Rep 2003;52:901 906. 8. Samandari T, Malakmadze N, Balter S, et al. A large outbreak of hepatitis B virus infections associated with frequent injections at a physician s office. Infect Control Hosp Epidemiol 2005;26: 745 750. 9. Bruguera M, Saiz JC, Franco S, et al. Outbreak of nosocomial hepatitis C virus infection resolved by genetic analysis of HCV RNA. J Clin Microbiol 2002;40:4363 4366. 10. Comstock RD, Mallonee S, Fox JL, et al. A large nosocomial outbreak of hepatitis C and hepatitis B among patients receiving pain remediation treatments. Infect Control Hosp Epidemiol 2004;25:576 583. 11. Germain JM, Carbonne A, Thiers V, et al. Patient-to-patient transmission of hepatitis C virus through the use of multidose vials during general anesthesia. Infect Control Hosp Epidemiol 2005; 26:789 792. 12. Kidd-Ljunggren K, Broman E, Ekvall H, et al. Nosocomial transmission of hepatitis B virus infection through multiple-dose vials. J Hosp Infect 1999;43:57 62. 13. Macedo de Oliveira A, White K, Leschinsky D, et al. An outbreak of hepatitis C virus infections among outpatients at a hematology/ oncology clinic. Ann Intern Med 2005;142:898 902. 14. Krause G, Trepka MJ, Whisenhunt RS, et al. Nosocomial transmission of hepatitis C virus associated with the use of multidose saline vials. Infect Control Hosp Epidemiol 2003;24: 122 127. 15. Massari M, Petrosillo N, Ippolito G, et al. Transmission of hepatitis C virus in a gynecological surgery setting. J Clin Microbiol 2001;39:2860 2863. 16. Oren I, Hershow RC, Ben-Porath E, et al. A common-source outbreak of fulminant hepatitis B in a hospital. Ann Intern Med 1989;110:691 698. 17. Carbonne A, Thiers V. Nosocomial transmission of hepatitis C from patient to patient in general anesthesia in the northern inter-region in 2001 2002. Ann Fr Anesth Reanim 2004;23: 550 553. 18. Fisker N, Carlsen NL, Kolmos HJ, et al. Identifying a hepatitis B outbreak by molecular surveillance: a case study. BMJ 2006; 332:343 345. 19. Lagging LM, Aneman C, Nenonen N, et al. Nosocomial transmission of HCV in a cardiology ward during the window phase of infection: an epidemiological and molecular investigation. Scand J Infect Dis 2002;34:580 582. 20. Centers for Disease Control and Prevention. Acute hepatitis C virus infections attributed to unsafe injection practices at an endoscopy clinic Nevada, 2007. MMWR Morb Mortal Wkly Rep 2008;57:513 517. 21. Bronowicki JP, Venard V, Botte C, et al. Patient-to-patient transmission of hepatitis C virus during colonoscopy. N Engl J Med 1997;337:237 240.

170 GUTELIUS ET AL GASTROENTEROLOGY Vol. 139, No. 1 22. Alter MJ. Healthcare should not be a vehicle for transmission of hepatitis C virus. J Hepatol 2008;48:2 4. 23. Patel PR, Srinivasan A, Perz JF. Developing a broader approach to management of infection control breaches in health care settings. Am J Infect Control 2008;685 687. 24. Katzenstein TL, Jorgensen LB, Permin H, et al. Nosocomial HIVtransmission in an outpatient clinic detected by epidemiological and phylogenetic analyses. AIDS 1999;13:1737 1744. 25. Thompson ND, Perz JF, Moorman AC, et al. Nonhospital health care-associated hepatitis B and C virus transmission: United States, 1998 2008. Ann Intern Med 2009;150:33 39. 26. Bennett SN, McNeil MM, Bland LA, et al. Postoperative infections traced to contamination of an intravenous anesthetic, propofol. N Engl J Med 1995;333:147 154. 27. New York State Department of Health. Health care professionals and patient safety: office-based surgery. Available at: http:// www.health.state.ny.us/professionals/office-based_surgery/. Accessed June 19, 2009. 28. The Centers for Disease Control and Prevention (CDC). Injection safety Web site. Available at: http://www.cdc.gov/ncidod/dhqp/ injectionsafety.html. Accessed February 6, 2009. 29. Perz JF, Thompson ND, Schaefer MK, et al. US outbreak investigations highlight the need for safe injection practices and basic infection control. Clin Liver Dis 2010;14:137 151. Received September 11, 2009. Accepted May 22, 2010. Reprint requests Address requests for reprints to: Sharon Balter, MD, New York City Department of Health and Mental Hygiene, 125 Worth St, CN 22A, New York, New York 10013. e-mail: sbalter@health. nyc.gov; fax: (212) 788-4278. Acknowledgments The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention. This work was presented at the Epidemic Intelligence Service Conference, April 16, 2008, in Atlanta, GA. Conflicts of interest The authors disclose no conflicts. Funding Primary support for this investigation was provided by the New York City Department of Health and Mental Hygiene, additional support was provided by the Emerging Infections Program Cooperative Agreement number 5U50/CC1223667 from the Centers for Disease Control and Prevention, and staff were funded by their primary institutions.