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Deja vu: nosocomial hepatitis B virus transmission and fingerstick monitoring
Deja Vu: Nosocomial Hepatitis B Virus Transmission and Fingerstick Monitoring John M. Quale, MD, David Landman, MD, Barbara Wallace, MD, Elaine Atwood, RN, Virginia Ditore, RN, Gerald Fruchter, MD PURPOSE: Three patients with acute hepatitis B virus infection were identified who had been hospitalized on the same medical ward during a 19-day period several months earlier. An investigation was undertaken to determine if nosocomial transmission had occurred. SUBJECTS AND METHODS: A cohort study of patients admitted to the medical ward during the 19-day period in 1995 was conducted. In addition, we reviewed medical charts and laboratory records of all patients with acute hepatitis B virus infection who had been admitted to the hospital from 1992 through October 1996 to identify other cases with possible nosocomial acquisition. RESULTS: The 3 patients who had developed acute hepatitis B infection 2 to 5 months after hospitalization on the same medical ward had diabetes mellitus but no identified risk factors for hepatitis B infection. A source patient with diabetes mellitus and hepatitis B “e” antigenemia also was present on the same medical ward at the same time; all 4 patients were infected with
the same viral subtype (adw2). Diabetes mellitus and fingerstick monitoring were associated with illness (P ,0.001). Through the review of medical charts and laboratory records, 11 additional cases of suspected nosocomial acquisition via fingersticks were identified in 1996, including two clusters involving an unusual subtype of hepatitis B virus (adw4). The fingerstick device employed had a reusable base onto which disposable lancet caps were inserted. There was ample opportunity for cross-contamination among patients because deficiencies in infection control practices, particularly failure to change gloves between patients, were reported by nurses and patients with diabetes mellitus. CONCLUSION: Transmission during fingerstick procedures was the most likely cause of these cases of nosocomial hepatitis B infection. Contamination probably occurred when healthcare workers failed to change gloves between patients undergoing fingerstick monitoring, although other means of contamination cannot be ruled out. Am J Med. 1998;105:296 –301. q1998 by Excerpta Medica, Inc.
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wards, two surgical wards, and coronary care, medical intensive care, and surgical intensive care areas. In early 1996, 3 patients with diabetes mellitus and acute hepatitis B virus infection were identified (cases 1, 2, and 3), none of whom had risk factors for hepatitis B virus. The 3 patients were hospitalized on the same medical ward in December 1995 (primary outbreak). Further investigation revealed another diabetic patient hospitalized on the same ward in December 1995 who had been diagnosed 2 months earlier with acute hepatitis B infection. This last patient was considered the source (source 1) for the 3 cases.
osocomial transmission of hepatitis B virus continues to be a problem in health-care facilities. Transmission has been linked to infected healthcare workers (1– 6), contamination of multi-use vials (7– 10), and medical devices, including gastrointestinal endoscopes (11), acupuncture needles (12), jet injectors (13), and fingerstick instruments (14,15). In the last example, reuse of the platform of a spring-loaded fingerstick device was determined to be the mechanism of transmission. Because of these reports, the use of these devices was discontinued at our hospital in 1993 and replaced by a spring-loaded device with a disposable finger guard.
PATIENTS AND METHODS Background The involved hospital is a 324-bed teaching, tertiary-care facility. The hospital has four acute-care general medical From the Department of Veterans Affairs Medical Center (JMQ, DL, EA, VD, GF), Brooklyn, New York, and Epidemic Intelligence Service (BW), Bureau of Communicable Disease Control, New York State Department of Health, Albany, New York, Epidemiology Program Office, Centers for Disease Control and Prevention (BW), Atlanta, Georgia. Requests for reprints should be addressed to David Landman, MD, Box 77 Division of Infectious Diseases, SUNY Health Science Center at Brooklyn, 450 Clarkson Avenue, Brooklyn, New York 11203. Manuscript submitted October 2, 1997 and accepted in revised form June 1, 1998. 296
q1998 by Excerpta Medica, Inc. All rights reserved.
Cohort Study The first part of this study examined the primary outbreak period, which was defined as the 19-day period of hospitalization of source 1 on medical ward A. A retrospective cohort study was performed by reviewing the medical records of all patients present on the ward during the outbreak period. Data extracted from the patients’ medical charts included demographic information, major diagnoses, risk factors for hepatitis B infection, and the number and type of percutaneous exposures (ie, subcutaneous, intramuscular, and intravenous injections, placement of intravenous lines, phlebotomy, and capillary blood sampling). The outcome of all involved patients during the subsequent 6 months was determined. All available patients were interviewed using a standard questionnaire on risk factors for hepatitis B infection and 0002-9343/98/$19.00 PII S0002-9343(98)00256-3
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potential events that could lead to transmission during their hospitalization. All available patients also underwent serological testing for hepatitis B virus. A case was defined as acute hepatitis B infection 6 weeks to 6 months after admission to the ward during source 1’s hospitalization. Cases were considered to have acute hepatitis B infection if anti-hepatitis B core IgM (anti-HBc IgM) was present. Acute hepatitis B infection also was considered if seroconversion from hepatitis B surface antigen (HBsAg) negative to positive occurred within a 6-month period, or if acute hepatitis developed, HBsAg was positive, and testing for anti-HBc IgM was not performed.
Surveillance Study In the second part of this study, we reviewed all episodes of hepatitis B infection at our facility to determine the extent of possible nosocomial transmission in patients with diabetes mellitus. Medical records from all patients with an ICD-9 discharge diagnosis of hepatitis B from 1992 through October 1996 were reviewed. Laboratory records also were reviewed to identify additional patients with acute hepatitis B infection. Patients who developed acute hepatitis B infection within 6 months after being hospitalized were interviewed, if available. Lastly, the nursing staff of the medical and surgical wards were given anonymous questionnaires concerning capillary blood sampling. Questions regarding the frequency of compliance (both practiced and observed) to infection control practices and of contamination of the devices were included. Serum specimens were tested for HBsAg and anti-HBc by enzyme immunoassay (Abbott Laboratories, Abbott Park, Illinois). Subtyping of HBsAg was performed using enzyme immunoassay by the Seattle-King County Public Health Laboratory.
Statistics Categorical data were analyzed using Fisher’s exact test. Student’s t test was used to compare means; results are given as mean 6 standard deviation (SD). A two-tailed P value of #0.05 was considered significant.
RESULTS Cohort Study Seventy-two patients were present on medical ward A during the 19-day primary outbreak period. Twenty-one patients (including 5 with diabetes) had died during the 6-month follow-up period, and 7 patients were lost to follow-up. Eight patients (including 1 with diabetes) were presumed to be immune (preexisting anti-HBc) before the outbreak period. Another 11 patients (including 4 with diabetes) without baseline serological information were found to be positive for anti-HBc and negative for HBsAg during the follow-up period and without symptoms of acute hepatitis; these 11 patients also were as-
Table 1. Comparison of Hepatitis B Cases and Seronegative Cohort Patients Hospitalized during the Primary Outbreak Period Cases (n 5 3)
Seronegative Cohort (n 5 20) P Value
Age (years) 64 6 10 62 6 15 Length of exposure 6.3 6 2.1 6.6 6 3.7 to source (days) Male 3 19 Intravenous catheter 2 16 placement Receipt of subcutaneous heparin 0 4 Intramuscular injection 0 4 Diagnosis of diabetes 3 0 mellitus Fingersticks performed 3 0 Receipt of insulin 2 0
.0.2 .0.2 .0.2 .0.2 .0.2 .0.2 ,0.001 ,0.001 50.01
Plus-minus values are mean 6 SD.
sumed to be immune during the outbreak period. One diabetic patient was found to be HBsAg positive, but the levels of antigen were too low for subtyping. This patient did not have evidence of acute infection and was not considered an acute case. Of the remaining 24 patients, 1 was the presumed source (source 1) and 3 were cases. The remaining 20 patients were all seronegative for hepatitis B virus. Having diabetes mellitus (and events associated with diabetes) was highly associated with the development of hepatitis B infection (Table 1). One of the cases did not receive insulin injections during the hospital stay. All 3 cases developed acute icteric hepatitis and became seropositive for HBsAg and anti-HBc IgM. The same viral subtype (adw2) of hepatitis B virus was present in the source and the 3 cases. The source patient developed acute hepatitis B infection 2 months before hospital admission, and subsequently developed chronic hepatitis B infection with persistent surface and “e” antigenemia. During the outbreak period, 13 different nurses shared fingerstick responsibilities for the source and cases. Results of screening for HBsAg were negative for 11 of these 13 nurses; 2 were unavailable for testing. Source 1 underwent 61 fingerstick procedures during the hospitalization. Case 1 was hospitalized for the first 7 days of the outbreak period and underwent 25 fingersticks. While several nurses performed the fingersticks, for 22 of the 25 instances, the same nurse performed the fingerstick on both the source and case 1. Case 2 was hospitalized on days 7 to 19 of the outbreak period and underwent 27 fingersticks. For 22 of these, the same nurse performed a fingerstick on the source patient. Case 3 was hospitalized during days 5 to 8 of the outbreak; each of the 10 fingersticks on this case were done by a nurse who also performed a fingerstick on the source patient. The 3 cases October 1998
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were hospitalized in close proximity to the source patient. Of the 3 cases, 1 shared the room with, 1 had an adjoining room to, and 1 had a room across the hall from the source patient.
Surveillance Study There was a marked increase in the number of patients with an ICD-9 discharge diagnosis of acute hepatitis B infection in 1996, particularly in patients with diabetes mellitus (Figure 1). Of the 10 patients with acute hepatitis B infection without diabetes mellitus identified from 1992 through 1996, 2 had had a prior hospitalization within 6 months of the diagnosis of acute hepatitis B infection. In contrast, 12 of the 14 patients with diabetes mellitus had been recently hospitalized (P 5 0.006). Review of serological records identified a total of 17 patients who were diagnosed with acute hepatitis B infection in the first 10 months of 1996. For 3 cases, other risk factors were present and nosocomial transmission was not considered likely. Three cases were identified in the primary outbreak described above. The remaining 11 cases were reviewed further (Figure 2). Ten of these 11 developed anti-HBc IgM and the 11th seroconverted from HBsAg negative to positive. Case 4 was a 67-year-old patient admitted to surgical ward B in November 1995. A source patient (source 2) known to be HBsAg-positive (and subsequently found to be hepatitis “e” antigen positive) was also on the surgical ward (Figure 2). Both patients had diabetes mellitus and underwent fingerstick monitoring. Case 4 developed acute hepatitis B virus infection in January 1996; he denied having risk factors for hepatitis B virus. Both source 2 and case 4 were found to have hepatitis B virus subtype adw2. Case 5 was a 54-year-old patient admitted to medical ward C for 4 days in January 1996. The same source patient (source 2) also was on medical unit C during that admission (Figure 2). Both patients underwent fingerstick monitoring. Case 5 developed acute hepatitis B infection in July 1996. He also denied risk factors for hepatitis B virus. Case 5 subsequently became HBsAg negative, and his hepatitis B virus subtype could not be determined. Case 6 was a 73-year-old patient with diabetes mellitus admitted to medical ward C for 9 days in May 1996 (Figure 2). Case 6 had fingerstick monitoring performed, denied having risk factors for hepatitis B infection, and developed acute hepatitis B (with subtype adw2) infection in October 1996. All of the patients on the medical ward during the 9-day period in May were reviewed, and a source could not be identified. Six of the patients (cases 7 through 12) who developed acute hepatitis B infection in June and July 1996 had been hospitalized on medical ward D between March 20 and
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Figure 1. Distribution of patients with ICD-9 discharge diagnosis of acute hepatitis B virus infection, January 1992 through October 1996. Solid bars 5 patients without diabetes mellitus; hatched bars 5 patients with diabetes mellitus.
April 12, 1996 (Figure 2). Patients 7 through 10 and 12 all underwent fingerstick monitoring during their hospitalizations. Patient 11 had diabetes mellitus, but his medical record did not contain documentation of fingerstick monitoring. This patient subsequently died and hence could not be interviewed. Patients 7 to 11 all had hepatitis B virus subtype adw4. Patient 12 was unavailable for interview and his hepatitis B virus subtype was unknown. Of the 6 patients in this cluster, 2 received insulin and 2 received subcutaneous heparin during the hospitalization. Three of the 6 patients were confined to the hospital or an affiliated skilled nursing facility for at least 5 months before the onset of acute hepatitis B infection. Review of all of the patients hospitalized on medical ward D during the common exposure period revealed one potential
Figure 2. Distribution of cases by ward. Open bars 5 period of presumed nosocomial exposure to hepatitis B virus. Closed bars 5 period with active hepatitis B infection. adw2, adw4 5 subtype of hepatitis B virus.
Nosocomial Hepatitis B Virus Transmission/Quale et al
source, a patient known to have chronic hepatitis B infection. However, only one fingerstick was documented during his eight-day hospitalization on Medical Ward D. The patient subsequently died, and further testing of his hepatitis B virus isolate was not possible. Two patients (cases 13 and 14) were hospitalized on surgical ward E in March and April 1996 and developed acute hepatitis B infection in June and August 1996 (Figure 2). Both had diabetes mellitus and underwent fingerstick monitoring during their hospitalizations. Both patients had been hospitalized in close proximity at one end of the ward and were found to have hepatitis B virus subtype adw4. Patient 14 was on maintenance hemodialysis and had been hospitalized on four other wards during the 6 months before the onset of hepatitis. No obvious source patient could be identified during the period of exposure on surgical ward E. Since the same (and relatively rare) hepatitis B virus subtype was present in all of the tested patients from medical ward D and surgical ward E, and the time period of exposure was similar, an attempt was made to identify patients present on both of these wards during the exposure periods. Three patients were discovered to be present on both wards. Two patients had normal liver function tests, had no obvious risk factors for hepatitis B infection, did not have diabetes mellitus, and did not undergo fingerstick monitoring. The third patient had end-stage renal disease, AIDS, and hepatitis C virus infection with persistently abnormal liver function tests. He was admitted for a bleeding and infected vascular graft, which required removal on the second hospital day. No evidence of fingerstick monitoring was found in the medical record. This patient previously tested positive for antiHBc but negative for HBsAg and anti-HBs. He subsequently died, and his serum was not available for further testing.
Infection Control Practices The fingerstick instrument used at the hospital was a penlike device with a reusable base containing a plunger. Before each fingerstick, the plunger was reset, and an unused lancet was attached to the base and the protective tip was removed from the lancet. After completing the capillary blood sampling, the lancet was removed and discarded. The reusable base was shared between patients and was not routinely disinfected between patients. A small plastic box was used to carry the clean lancet caps to the patients’ bedside. The nursing staff typically performed fingersticks by starting at one end of the ward and proceeding from room to room measuring blood glucose levels. Results of the patient interviews revealed several deficiencies in infection control practices. Three of the 20 diabetic patients interviewed recalled that nurses did not
consistently change gloves between patients undergoing fingersticks and 1 recalled blood contaminating the gloves and glucose monitoring devices. Of the 33 patients without diabetes mellitus interviewed (including the 20 controls and 13 immune patients from the retrospective cohort study), 1 patient remembered that nurses did not change gloves consistently between patients undergoing fingersticks, and 1 patient recalled seeing blood on the nurse’s gloves or monitoring equipment. Forty-five nurses completed the anonymous questionnaire, representing 36% of the nursing staff employed on the involved wards. Questionnaires from 42 respondents who performed fingerstick monitoring were reviewed in further detail. When performing the fingerstick tests, 98% of the nurses stated they always wore gloves, 76% stated they always changed gloves between patients, and 59% always washed hands between patients. Nurses observed frequent or occasional blood contamination of gloves (78% of respondents), the lancet device (61%) or plunger (32%), or the glucometer (48%). One third of respondents recalled placing or seeing used lancet caps in the plastic box containing unused lancets.
DISCUSSION Despite the development of an effective vaccine and the implementation of universal precautions, outbreaks of hepatitis B virus continue to be reported from health-care facilities. The extremely high viral concentrations in the blood of an asymptomatic or unrecognized carrier, particularly in those who are hepatitis B “e” antigen positive, facilitates transmission. Contamination of reusable medication vials (7–10) or percutaneous medical devices (12– 15) with miniscule amounts of serum or blood may lead to outbreaks. Spring-loaded fingerstick devices have been implicated in the transmission of hepatitis B virus among patients with diabetes mellitus (14,15). In these reports, reuse of a disposable finger guard was a risk factor for nosocomial transmission. Because of these reports, our hospital began using a device with a disposable lancet cap in 1993. Despite this change, nosocomial transmission of hepatitis B virus occurred in patients who had received fingersticks. Of the 14 cases in this report, most were middleaged or elderly patients with diabetes mellitus and had no identifiable risk factors for hepatitis B infection. In three instances, patients were hospitalized on a ward with another patient known to be positive for HBsAg of the same subtype. One viral subtype identified in this study, adw2, is common to North America (16). However, the second subtype (adw4) recovered in at least 7 of the patients in this study, is more prevalent in French Polynesia and Ar-
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gentina, and is rare in the United States, Europe, and Africa (16,17). Both subtypes have been reported in outbreaks of hepatitis B virus in patients requiring hemodialysis (7). Because five different wards and two different hepatitis B virus strains were ultimately involved, transmission from an infected health-care worker appears unlikely. Contamination of a reusable medication vial also seems unlikely, because only some of the patients received insulin or subcutaneous heparin. Our evidence indicates that cross contamination occurred during the fingerstick procedure. There are two possible mechanisms to explain how contaminated blood was transferred from patient to patient. First, some of the nurses surveyed acknowledged placing used lancet caps back in the plastic box with sterile caps. It has been reported that lancet caps frequently become contaminated with blood (18), and cross contamination may have occurred in the lancet box. A more plausible explanation is that contaminated gloves served as vehicles of transmission. Patients and nurses noted that gloves were not always changed between patients. Therefore, before use, lancet caps may have been contaminated by blood on a glove. Alternatively, blood from contaminated gloves may have been introduced directly into the fingerstick wounds of subsequent patients. Because there was immediate feedback to the nursing staff about the mode of transmission, we were unable to study actual compliance to infection control practices. We suspect that many health-care workers view gloves mainly as a form of personal protection, and lose sight of their role in infection control. Changing of soiled gloves occurred in only 15% of the patient interactions in one report involving a long-term care facility (19). Reuse of contaminated gloves has been associated with a nosocomial outbreak of Acinetobacter calcoaceticus (20), and has been suggested as the mode of transmission of hepatitis B virus in a dialysis unit (7). Precisely why there was a sudden increase in nosocomial transmission of hepatitis B virus in 1996 is not clear. There were no staffing changes, and the procedure for fingerstick monitoring had remained constant since 1993. The sudden increase may have resulted from an increasing number of days of hospitalization of highly infectious patients with diabetes mellitus. For example, 1 such patient identified in this report (source 2) was hospitalized for 8 days in 1994, 107 days in 1995, and for 87 days in 1996. A long hospitalization in a highly infectious patient, especially if the infection was unrecognized, would increase the likelihood that a human error involving that patient would occur. In response to this outbreak, we have implemented several corrective measures. Appropriate educational feedback has been given to the nursing staff, particularly regarding the changing of gloves and handwashing be-
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tween patients. We have begun using a totally disposable fingerstick device. Each patient requiring fingerstick monitoring receives their own supply of disposable fingerstick devices; the plastic box used by the nurses to carry the lancets has been eliminated. These measures should reduce the likelihood of cross contamination and subsequent nosocomial transmission. We have continued to review all cases of acute hepatitis B virus at our medical center. Since these changes were implemented, we have identified an additional two cases of acute hepatitis B infection in which nosocomial transmission via fingerstick monitoring is suspected. Both of these cases are undergoing review. Further follow-up will determine if these measures have successfully terminated this outbreak.
ACKNOWLEDGMENT The authors thank the Seattle-King County Public Health Laboratory for their assistance in this investigation.
REFERENCES 1. Harpaz R, Von Seidlein L, Averhoff FM, et al. Transmission of hepatitis B virus to multiple patients from a surgeon without evidence of inadequate infection control. NEJM. 1996;334:549 –554. 2. Welch J, Webster M, Tilzey AJ, et al. Hepatitis B infections after gynecological surgery. Lancet. 1989;1:205–206. 3. Rimland D, Parkin WE, Miller GB, Schrack WD. Hepatitis B outbreak traced to an oral surgeon. NEJM. 1977;296:953–958. 4. Hadler SC, Sorley DL, Acree KH, et al. An outbreak of hepatitis B in a dental practice. Ann Intern Med. 1981;95:133–138. 5. Garibaldi RA, Rasmussen CM, Holmes AW, Gregg MB. Hospitalacquired serum hepatitis. Report of an outbreak. JAMA. 1972;219: 1577–1580. 6. Snydman DR, Hindman SH, Wineland MD, et al. Nosocomial viral hepatitis B. A cluster among staff with subsequent transmission to patients. Ann Intern Med. 1976;85:573–577. 7. Centers for Disease Control. Outbreaks of hepatitis B virus infection among hemodialysis patients—California, Nebraska, and Texas, 1994. MMWR. 1996;45:285–289. 8. Oren I, Hershow RC, Ben-Proath E, et al. A common-source outbreak of fulminant hepatitis B in a hospital. Ann Intern Med. 1989; 110:691– 698. 9. Alter MJ, Ahtone J, Maynard JE. Hepatitis B virus transmission associated with a multiple-dose vial in a hemodialysis unit. Ann Intern Med. 1993;99:330 –333. 10. Carl M, Francis DP, Maynard JE. A common-source outbreak of hepatitis B in a hemodialysis unit. Dial Transplant. 1983;12:222– 229. 11. Birnie GG, Quigley EM, Clements GB, et al. Endoscopic transmission of hepatitis B virus. Gut. 1983;24:171–174. 12. Kent GP, Brondum J, Keenlyside RA, et al. A large outbreak of acupuncture-associated hepatitis B. Am J Epidemiol. 1988;127:591–598. 13. Canter J, Mackey K, Good LS, et al. An outbreak of hepatitis B associated with jet injections in a weight reduction clinic. Arch Intern Med. 1990;150:1923–1927. 14. Polish LB, Shapiro CN, Bauer F, et al. Nosocomial transmission of hepatitis B virus associated with the use of a spring-loaded fingerstick device. NEJM. 1992;326:721–725. 15. Douvin C, Simon D, Zinelabidine H, et al. An outbreak of hepatitis
Nosocomial Hepatitis B Virus Transmission/Quale et al B in an endocrinology unit traced to a capillary-blood-sampling device. NEJM. 1990;322:57. 16. Swenson PD, Riess JT, Krueger LE. Determination of HBsAg subtypes in different high risk populations using monoclonal antibodies. J Virolog Meth. 1991;33:27–38. 17. Courouce-Pauty AM, Plancon A, Soulier JP. Distribution of HBsAg subtypes in the world. Vox Sang. 1983;44:197–211.
18. Shier N, Warren J, Torabi M, Hongen R. Contamination of a finger-stick device. NEJM. 1993;328:969 –970. 19. Centers for Disease Control. Handwashing and glove use in a longterm-care facility—Maryland, 1992. MMWR. 1993;42:672– 675. 20. Patterson JE, Vecchio J, Pantelick, et al. Association of contaminated gloves with transmission of Acinetobacter calcoaceticus var. anitratus in an intensive care unit. Am J Med. 1991;91:479 – 483.
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the same viral subtype (adw2). Diabetes mellitus and fingerstick monitoring were associated with illness (P ,0.001). Through the review of medical charts and laboratory records, 11 additional cases of suspected nosocomial acquisition via fingersticks were identified in 1996, including two clusters involving an unusual subtype of hepatitis B virus (adw4). The fingerstick device employed had a reusable base onto which disposable lancet caps were inserted. There was ample opportunity for cross-contamination among patients because deficiencies in infection control practices, particularly failure to change gloves between patients, were reported by nurses and patients with diabetes mellitus. CONCLUSION: Transmission during fingerstick procedures was the most likely cause of these cases of nosocomial hepatitis B infection. Contamination probably occurred when healthcare workers failed to change gloves between patients undergoing fingerstick monitoring, although other means of contamination cannot be ruled out. Am J Med. 1998;105:296 –301. q1998 by Excerpta Medica, Inc.
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wards, two surgical wards, and coronary care, medical intensive care, and surgical intensive care areas. In early 1996, 3 patients with diabetes mellitus and acute hepatitis B virus infection were identified (cases 1, 2, and 3), none of whom had risk factors for hepatitis B virus. The 3 patients were hospitalized on the same medical ward in December 1995 (primary outbreak). Further investigation revealed another diabetic patient hospitalized on the same ward in December 1995 who had been diagnosed 2 months earlier with acute hepatitis B infection. This last patient was considered the source (source 1) for the 3 cases.
osocomial transmission of hepatitis B virus continues to be a problem in health-care facilities. Transmission has been linked to infected healthcare workers (1– 6), contamination of multi-use vials (7– 10), and medical devices, including gastrointestinal endoscopes (11), acupuncture needles (12), jet injectors (13), and fingerstick instruments (14,15). In the last example, reuse of the platform of a spring-loaded fingerstick device was determined to be the mechanism of transmission. Because of these reports, the use of these devices was discontinued at our hospital in 1993 and replaced by a spring-loaded device with a disposable finger guard.
PATIENTS AND METHODS Background The involved hospital is a 324-bed teaching, tertiary-care facility. The hospital has four acute-care general medical From the Department of Veterans Affairs Medical Center (JMQ, DL, EA, VD, GF), Brooklyn, New York, and Epidemic Intelligence Service (BW), Bureau of Communicable Disease Control, New York State Department of Health, Albany, New York, Epidemiology Program Office, Centers for Disease Control and Prevention (BW), Atlanta, Georgia. Requests for reprints should be addressed to David Landman, MD, Box 77 Division of Infectious Diseases, SUNY Health Science Center at Brooklyn, 450 Clarkson Avenue, Brooklyn, New York 11203. Manuscript submitted October 2, 1997 and accepted in revised form June 1, 1998. 296
q1998 by Excerpta Medica, Inc. All rights reserved.
Cohort Study The first part of this study examined the primary outbreak period, which was defined as the 19-day period of hospitalization of source 1 on medical ward A. A retrospective cohort study was performed by reviewing the medical records of all patients present on the ward during the outbreak period. Data extracted from the patients’ medical charts included demographic information, major diagnoses, risk factors for hepatitis B infection, and the number and type of percutaneous exposures (ie, subcutaneous, intramuscular, and intravenous injections, placement of intravenous lines, phlebotomy, and capillary blood sampling). The outcome of all involved patients during the subsequent 6 months was determined. All available patients were interviewed using a standard questionnaire on risk factors for hepatitis B infection and 0002-9343/98/$19.00 PII S0002-9343(98)00256-3
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potential events that could lead to transmission during their hospitalization. All available patients also underwent serological testing for hepatitis B virus. A case was defined as acute hepatitis B infection 6 weeks to 6 months after admission to the ward during source 1’s hospitalization. Cases were considered to have acute hepatitis B infection if anti-hepatitis B core IgM (anti-HBc IgM) was present. Acute hepatitis B infection also was considered if seroconversion from hepatitis B surface antigen (HBsAg) negative to positive occurred within a 6-month period, or if acute hepatitis developed, HBsAg was positive, and testing for anti-HBc IgM was not performed.
Surveillance Study In the second part of this study, we reviewed all episodes of hepatitis B infection at our facility to determine the extent of possible nosocomial transmission in patients with diabetes mellitus. Medical records from all patients with an ICD-9 discharge diagnosis of hepatitis B from 1992 through October 1996 were reviewed. Laboratory records also were reviewed to identify additional patients with acute hepatitis B infection. Patients who developed acute hepatitis B infection within 6 months after being hospitalized were interviewed, if available. Lastly, the nursing staff of the medical and surgical wards were given anonymous questionnaires concerning capillary blood sampling. Questions regarding the frequency of compliance (both practiced and observed) to infection control practices and of contamination of the devices were included. Serum specimens were tested for HBsAg and anti-HBc by enzyme immunoassay (Abbott Laboratories, Abbott Park, Illinois). Subtyping of HBsAg was performed using enzyme immunoassay by the Seattle-King County Public Health Laboratory.
Statistics Categorical data were analyzed using Fisher’s exact test. Student’s t test was used to compare means; results are given as mean 6 standard deviation (SD). A two-tailed P value of #0.05 was considered significant.
RESULTS Cohort Study Seventy-two patients were present on medical ward A during the 19-day primary outbreak period. Twenty-one patients (including 5 with diabetes) had died during the 6-month follow-up period, and 7 patients were lost to follow-up. Eight patients (including 1 with diabetes) were presumed to be immune (preexisting anti-HBc) before the outbreak period. Another 11 patients (including 4 with diabetes) without baseline serological information were found to be positive for anti-HBc and negative for HBsAg during the follow-up period and without symptoms of acute hepatitis; these 11 patients also were as-
Table 1. Comparison of Hepatitis B Cases and Seronegative Cohort Patients Hospitalized during the Primary Outbreak Period Cases (n 5 3)
Seronegative Cohort (n 5 20) P Value
Age (years) 64 6 10 62 6 15 Length of exposure 6.3 6 2.1 6.6 6 3.7 to source (days) Male 3 19 Intravenous catheter 2 16 placement Receipt of subcutaneous heparin 0 4 Intramuscular injection 0 4 Diagnosis of diabetes 3 0 mellitus Fingersticks performed 3 0 Receipt of insulin 2 0
.0.2 .0.2 .0.2 .0.2 .0.2 .0.2 ,0.001 ,0.001 50.01
Plus-minus values are mean 6 SD.
sumed to be immune during the outbreak period. One diabetic patient was found to be HBsAg positive, but the levels of antigen were too low for subtyping. This patient did not have evidence of acute infection and was not considered an acute case. Of the remaining 24 patients, 1 was the presumed source (source 1) and 3 were cases. The remaining 20 patients were all seronegative for hepatitis B virus. Having diabetes mellitus (and events associated with diabetes) was highly associated with the development of hepatitis B infection (Table 1). One of the cases did not receive insulin injections during the hospital stay. All 3 cases developed acute icteric hepatitis and became seropositive for HBsAg and anti-HBc IgM. The same viral subtype (adw2) of hepatitis B virus was present in the source and the 3 cases. The source patient developed acute hepatitis B infection 2 months before hospital admission, and subsequently developed chronic hepatitis B infection with persistent surface and “e” antigenemia. During the outbreak period, 13 different nurses shared fingerstick responsibilities for the source and cases. Results of screening for HBsAg were negative for 11 of these 13 nurses; 2 were unavailable for testing. Source 1 underwent 61 fingerstick procedures during the hospitalization. Case 1 was hospitalized for the first 7 days of the outbreak period and underwent 25 fingersticks. While several nurses performed the fingersticks, for 22 of the 25 instances, the same nurse performed the fingerstick on both the source and case 1. Case 2 was hospitalized on days 7 to 19 of the outbreak period and underwent 27 fingersticks. For 22 of these, the same nurse performed a fingerstick on the source patient. Case 3 was hospitalized during days 5 to 8 of the outbreak; each of the 10 fingersticks on this case were done by a nurse who also performed a fingerstick on the source patient. The 3 cases October 1998
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were hospitalized in close proximity to the source patient. Of the 3 cases, 1 shared the room with, 1 had an adjoining room to, and 1 had a room across the hall from the source patient.
Surveillance Study There was a marked increase in the number of patients with an ICD-9 discharge diagnosis of acute hepatitis B infection in 1996, particularly in patients with diabetes mellitus (Figure 1). Of the 10 patients with acute hepatitis B infection without diabetes mellitus identified from 1992 through 1996, 2 had had a prior hospitalization within 6 months of the diagnosis of acute hepatitis B infection. In contrast, 12 of the 14 patients with diabetes mellitus had been recently hospitalized (P 5 0.006). Review of serological records identified a total of 17 patients who were diagnosed with acute hepatitis B infection in the first 10 months of 1996. For 3 cases, other risk factors were present and nosocomial transmission was not considered likely. Three cases were identified in the primary outbreak described above. The remaining 11 cases were reviewed further (Figure 2). Ten of these 11 developed anti-HBc IgM and the 11th seroconverted from HBsAg negative to positive. Case 4 was a 67-year-old patient admitted to surgical ward B in November 1995. A source patient (source 2) known to be HBsAg-positive (and subsequently found to be hepatitis “e” antigen positive) was also on the surgical ward (Figure 2). Both patients had diabetes mellitus and underwent fingerstick monitoring. Case 4 developed acute hepatitis B virus infection in January 1996; he denied having risk factors for hepatitis B virus. Both source 2 and case 4 were found to have hepatitis B virus subtype adw2. Case 5 was a 54-year-old patient admitted to medical ward C for 4 days in January 1996. The same source patient (source 2) also was on medical unit C during that admission (Figure 2). Both patients underwent fingerstick monitoring. Case 5 developed acute hepatitis B infection in July 1996. He also denied risk factors for hepatitis B virus. Case 5 subsequently became HBsAg negative, and his hepatitis B virus subtype could not be determined. Case 6 was a 73-year-old patient with diabetes mellitus admitted to medical ward C for 9 days in May 1996 (Figure 2). Case 6 had fingerstick monitoring performed, denied having risk factors for hepatitis B infection, and developed acute hepatitis B (with subtype adw2) infection in October 1996. All of the patients on the medical ward during the 9-day period in May were reviewed, and a source could not be identified. Six of the patients (cases 7 through 12) who developed acute hepatitis B infection in June and July 1996 had been hospitalized on medical ward D between March 20 and
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Figure 1. Distribution of patients with ICD-9 discharge diagnosis of acute hepatitis B virus infection, January 1992 through October 1996. Solid bars 5 patients without diabetes mellitus; hatched bars 5 patients with diabetes mellitus.
April 12, 1996 (Figure 2). Patients 7 through 10 and 12 all underwent fingerstick monitoring during their hospitalizations. Patient 11 had diabetes mellitus, but his medical record did not contain documentation of fingerstick monitoring. This patient subsequently died and hence could not be interviewed. Patients 7 to 11 all had hepatitis B virus subtype adw4. Patient 12 was unavailable for interview and his hepatitis B virus subtype was unknown. Of the 6 patients in this cluster, 2 received insulin and 2 received subcutaneous heparin during the hospitalization. Three of the 6 patients were confined to the hospital or an affiliated skilled nursing facility for at least 5 months before the onset of acute hepatitis B infection. Review of all of the patients hospitalized on medical ward D during the common exposure period revealed one potential
Figure 2. Distribution of cases by ward. Open bars 5 period of presumed nosocomial exposure to hepatitis B virus. Closed bars 5 period with active hepatitis B infection. adw2, adw4 5 subtype of hepatitis B virus.
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source, a patient known to have chronic hepatitis B infection. However, only one fingerstick was documented during his eight-day hospitalization on Medical Ward D. The patient subsequently died, and further testing of his hepatitis B virus isolate was not possible. Two patients (cases 13 and 14) were hospitalized on surgical ward E in March and April 1996 and developed acute hepatitis B infection in June and August 1996 (Figure 2). Both had diabetes mellitus and underwent fingerstick monitoring during their hospitalizations. Both patients had been hospitalized in close proximity at one end of the ward and were found to have hepatitis B virus subtype adw4. Patient 14 was on maintenance hemodialysis and had been hospitalized on four other wards during the 6 months before the onset of hepatitis. No obvious source patient could be identified during the period of exposure on surgical ward E. Since the same (and relatively rare) hepatitis B virus subtype was present in all of the tested patients from medical ward D and surgical ward E, and the time period of exposure was similar, an attempt was made to identify patients present on both of these wards during the exposure periods. Three patients were discovered to be present on both wards. Two patients had normal liver function tests, had no obvious risk factors for hepatitis B infection, did not have diabetes mellitus, and did not undergo fingerstick monitoring. The third patient had end-stage renal disease, AIDS, and hepatitis C virus infection with persistently abnormal liver function tests. He was admitted for a bleeding and infected vascular graft, which required removal on the second hospital day. No evidence of fingerstick monitoring was found in the medical record. This patient previously tested positive for antiHBc but negative for HBsAg and anti-HBs. He subsequently died, and his serum was not available for further testing.
Infection Control Practices The fingerstick instrument used at the hospital was a penlike device with a reusable base containing a plunger. Before each fingerstick, the plunger was reset, and an unused lancet was attached to the base and the protective tip was removed from the lancet. After completing the capillary blood sampling, the lancet was removed and discarded. The reusable base was shared between patients and was not routinely disinfected between patients. A small plastic box was used to carry the clean lancet caps to the patients’ bedside. The nursing staff typically performed fingersticks by starting at one end of the ward and proceeding from room to room measuring blood glucose levels. Results of the patient interviews revealed several deficiencies in infection control practices. Three of the 20 diabetic patients interviewed recalled that nurses did not
consistently change gloves between patients undergoing fingersticks and 1 recalled blood contaminating the gloves and glucose monitoring devices. Of the 33 patients without diabetes mellitus interviewed (including the 20 controls and 13 immune patients from the retrospective cohort study), 1 patient remembered that nurses did not change gloves consistently between patients undergoing fingersticks, and 1 patient recalled seeing blood on the nurse’s gloves or monitoring equipment. Forty-five nurses completed the anonymous questionnaire, representing 36% of the nursing staff employed on the involved wards. Questionnaires from 42 respondents who performed fingerstick monitoring were reviewed in further detail. When performing the fingerstick tests, 98% of the nurses stated they always wore gloves, 76% stated they always changed gloves between patients, and 59% always washed hands between patients. Nurses observed frequent or occasional blood contamination of gloves (78% of respondents), the lancet device (61%) or plunger (32%), or the glucometer (48%). One third of respondents recalled placing or seeing used lancet caps in the plastic box containing unused lancets.
DISCUSSION Despite the development of an effective vaccine and the implementation of universal precautions, outbreaks of hepatitis B virus continue to be reported from health-care facilities. The extremely high viral concentrations in the blood of an asymptomatic or unrecognized carrier, particularly in those who are hepatitis B “e” antigen positive, facilitates transmission. Contamination of reusable medication vials (7–10) or percutaneous medical devices (12– 15) with miniscule amounts of serum or blood may lead to outbreaks. Spring-loaded fingerstick devices have been implicated in the transmission of hepatitis B virus among patients with diabetes mellitus (14,15). In these reports, reuse of a disposable finger guard was a risk factor for nosocomial transmission. Because of these reports, our hospital began using a device with a disposable lancet cap in 1993. Despite this change, nosocomial transmission of hepatitis B virus occurred in patients who had received fingersticks. Of the 14 cases in this report, most were middleaged or elderly patients with diabetes mellitus and had no identifiable risk factors for hepatitis B infection. In three instances, patients were hospitalized on a ward with another patient known to be positive for HBsAg of the same subtype. One viral subtype identified in this study, adw2, is common to North America (16). However, the second subtype (adw4) recovered in at least 7 of the patients in this study, is more prevalent in French Polynesia and Ar-
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gentina, and is rare in the United States, Europe, and Africa (16,17). Both subtypes have been reported in outbreaks of hepatitis B virus in patients requiring hemodialysis (7). Because five different wards and two different hepatitis B virus strains were ultimately involved, transmission from an infected health-care worker appears unlikely. Contamination of a reusable medication vial also seems unlikely, because only some of the patients received insulin or subcutaneous heparin. Our evidence indicates that cross contamination occurred during the fingerstick procedure. There are two possible mechanisms to explain how contaminated blood was transferred from patient to patient. First, some of the nurses surveyed acknowledged placing used lancet caps back in the plastic box with sterile caps. It has been reported that lancet caps frequently become contaminated with blood (18), and cross contamination may have occurred in the lancet box. A more plausible explanation is that contaminated gloves served as vehicles of transmission. Patients and nurses noted that gloves were not always changed between patients. Therefore, before use, lancet caps may have been contaminated by blood on a glove. Alternatively, blood from contaminated gloves may have been introduced directly into the fingerstick wounds of subsequent patients. Because there was immediate feedback to the nursing staff about the mode of transmission, we were unable to study actual compliance to infection control practices. We suspect that many health-care workers view gloves mainly as a form of personal protection, and lose sight of their role in infection control. Changing of soiled gloves occurred in only 15% of the patient interactions in one report involving a long-term care facility (19). Reuse of contaminated gloves has been associated with a nosocomial outbreak of Acinetobacter calcoaceticus (20), and has been suggested as the mode of transmission of hepatitis B virus in a dialysis unit (7). Precisely why there was a sudden increase in nosocomial transmission of hepatitis B virus in 1996 is not clear. There were no staffing changes, and the procedure for fingerstick monitoring had remained constant since 1993. The sudden increase may have resulted from an increasing number of days of hospitalization of highly infectious patients with diabetes mellitus. For example, 1 such patient identified in this report (source 2) was hospitalized for 8 days in 1994, 107 days in 1995, and for 87 days in 1996. A long hospitalization in a highly infectious patient, especially if the infection was unrecognized, would increase the likelihood that a human error involving that patient would occur. In response to this outbreak, we have implemented several corrective measures. Appropriate educational feedback has been given to the nursing staff, particularly regarding the changing of gloves and handwashing be-
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tween patients. We have begun using a totally disposable fingerstick device. Each patient requiring fingerstick monitoring receives their own supply of disposable fingerstick devices; the plastic box used by the nurses to carry the lancets has been eliminated. These measures should reduce the likelihood of cross contamination and subsequent nosocomial transmission. We have continued to review all cases of acute hepatitis B virus at our medical center. Since these changes were implemented, we have identified an additional two cases of acute hepatitis B infection in which nosocomial transmission via fingerstick monitoring is suspected. Both of these cases are undergoing review. Further follow-up will determine if these measures have successfully terminated this outbreak.
ACKNOWLEDGMENT The authors thank the Seattle-King County Public Health Laboratory for their assistance in this investigation.
REFERENCES 1. Harpaz R, Von Seidlein L, Averhoff FM, et al. Transmission of hepatitis B virus to multiple patients from a surgeon without evidence of inadequate infection control. NEJM. 1996;334:549 –554. 2. Welch J, Webster M, Tilzey AJ, et al. Hepatitis B infections after gynecological surgery. Lancet. 1989;1:205–206. 3. Rimland D, Parkin WE, Miller GB, Schrack WD. Hepatitis B outbreak traced to an oral surgeon. NEJM. 1977;296:953–958. 4. Hadler SC, Sorley DL, Acree KH, et al. An outbreak of hepatitis B in a dental practice. Ann Intern Med. 1981;95:133–138. 5. Garibaldi RA, Rasmussen CM, Holmes AW, Gregg MB. Hospitalacquired serum hepatitis. Report of an outbreak. JAMA. 1972;219: 1577–1580. 6. Snydman DR, Hindman SH, Wineland MD, et al. Nosocomial viral hepatitis B. A cluster among staff with subsequent transmission to patients. Ann Intern Med. 1976;85:573–577. 7. Centers for Disease Control. Outbreaks of hepatitis B virus infection among hemodialysis patients—California, Nebraska, and Texas, 1994. MMWR. 1996;45:285–289. 8. Oren I, Hershow RC, Ben-Proath E, et al. A common-source outbreak of fulminant hepatitis B in a hospital. Ann Intern Med. 1989; 110:691– 698. 9. Alter MJ, Ahtone J, Maynard JE. Hepatitis B virus transmission associated with a multiple-dose vial in a hemodialysis unit. Ann Intern Med. 1993;99:330 –333. 10. Carl M, Francis DP, Maynard JE. A common-source outbreak of hepatitis B in a hemodialysis unit. Dial Transplant. 1983;12:222– 229. 11. Birnie GG, Quigley EM, Clements GB, et al. Endoscopic transmission of hepatitis B virus. Gut. 1983;24:171–174. 12. Kent GP, Brondum J, Keenlyside RA, et al. A large outbreak of acupuncture-associated hepatitis B. Am J Epidemiol. 1988;127:591–598. 13. Canter J, Mackey K, Good LS, et al. An outbreak of hepatitis B associated with jet injections in a weight reduction clinic. Arch Intern Med. 1990;150:1923–1927. 14. Polish LB, Shapiro CN, Bauer F, et al. Nosocomial transmission of hepatitis B virus associated with the use of a spring-loaded fingerstick device. NEJM. 1992;326:721–725. 15. Douvin C, Simon D, Zinelabidine H, et al. An outbreak of hepatitis
Nosocomial Hepatitis B Virus Transmission/Quale et al B in an endocrinology unit traced to a capillary-blood-sampling device. NEJM. 1990;322:57. 16. Swenson PD, Riess JT, Krueger LE. Determination of HBsAg subtypes in different high risk populations using monoclonal antibodies. J Virolog Meth. 1991;33:27–38. 17. Courouce-Pauty AM, Plancon A, Soulier JP. Distribution of HBsAg subtypes in the world. Vox Sang. 1983;44:197–211.
18. Shier N, Warren J, Torabi M, Hongen R. Contamination of a finger-stick device. NEJM. 1993;328:969 –970. 19. Centers for Disease Control. Handwashing and glove use in a longterm-care facility—Maryland, 1992. MMWR. 1993;42:672– 675. 20. Patterson JE, Vecchio J, Pantelick, et al. Association of contaminated gloves with transmission of Acinetobacter calcoaceticus var. anitratus in an intensive care unit. Am J Med. 1991;91:479 – 483.
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