American Journal of Infection Control 42 (2014) e7-e10
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Major article
Outbreak of hepatitis C among patients admitted to the Department of Gynecology, Obstetrics, and Oncology Marta Rorat MD *, Tomasz Jurek PhD, Lukasz Szleszkowski PhD, Andrzej Gladysz PhD Department of Forensic Medicine, Wroclaw Medical University, Wroclaw, Poland
Key Words: Safety Infection control Equipment contamination Adverse event
Background: In Poland, nosocomial infections account for 32% of all patients’ claims against public hospitals, with hepatitis B virus and hepatitis C virus (HCV) being the most common causes. We present a major nosocomial outbreak of the HCV infection in the Department of Gynecology, Obstetrics, and Oncology and the results of detailed sanitary and epidemiologic research. Methods: A retrospective analysis of medicolegal opinions issued at the request of the civil court regarding the suspicion of HCV nosocomial infections was conducted. Results: The detailed medical data analysis proved 26 patients aged 19 to 72 years with recent HCV hepatitis hospitalized on the same gynecology ward. Twenty women were operated on for neoplasm. The State Sanitary Inspection’s investigation revealed a number of malpractices: incorrect sterilization procedures, insufficient hygiene habits of health care workers, poor condition of premises, and equipment being in poor condition. Numerous cases of staff breaking basic sanitary rules and hygiene standards and a lack of crucial procedures were discovered. The high number of women infected and the multiple errors recognized led to closure of the ward. Conclusion: Outbreaks of HCV hepatitis may be the result of ineffective infection control systems and remains a significant public health problem. Asymptomatic HCV nosocomial infections might go unnoticed or concealed and underreported. Auditing medical centers and health care workers for compliance with sanitary and epidemiologic requirements is an essential need. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Despite the introduction of multiple procedures minimizing the risk of the nosocomial hepatitis C virus (HCV) infection (blood donor screening in particular), local outbreaks are still being observed. The risk of acquiring HCV hepatitis is highest among hemodialysis patients or those treated for hematologic malignancies.1,2 Because HCV is most commonly transmitted via the parenteral route, blood transfusions, fluid infusions, injections, and invasive medical and surgical interventions using contaminated specimens and equipment is a major source of hospital infections. Some studies show the correlation between the risk of HCV infection and the duration of previous hospital admissions as well as the type and number of invasive medical procedures the patient has undergone.3 HCV transmission has also been documented to result from contact with infected health care workers, eg, during surgery. In these cases, the risk of infection depends on the viral status of the
* Address correspondence to Marta Rorat, MD, Mikulicza-Radeckiego 4, 50-345 Wroclaw, Poland. E-mail address: [email protected] (M. Rorat). Conflicts of interest: None to report.
source person and the type and duration of exposure-prone procedures.4 The nosocomial spread of the HCV infection is usually difficult to prove because the majority of patients do not present any symptoms of acute hepatitis. The detection of the disease is accidental and predominantly delayed for many years. In addition, other sources of infectiondintravenous drug use and perinatal or sexual transmissiondcannot be ruled out definitively. Nosocomial HCV infections do not just have significant medical implications but legal ones as well. In Poland, nosocomial infections account for 32% of all patients’ claims against public hospitals, with hepatitis B virus and HCV being the most common cause, especially on gynecology and obstetrics wards.5 In the following study, we present a major nosocomial outbreak of HCV infection in the Department of Gynecology, Obstetrics, and Oncology, discovered as a result of thorough research. MATERIALS AND METHODS A retrospective analysis of 26 medicolegal opinions issued at the request of the civil court regarding the suspicion of hepatitis C
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2013.07.016
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nosocomial infections was conducted. An epidemiologic investigation was performed to identify the cases, the source of infection/ contamination, and the route of the spreading of the virus. All the patients in question were diagnosed with a HCV infection between May and November 2003. All cases of infection were confirmed using polymerase chain reaction. The study protocol comprised the following: age, data included in medical records (diagnosis, all procedures performed, medical history), and results of the epidemiologic investigation conducted by the sanitary-epidemiologic services as well as testimonies provided by patients during court proceedings on the alleged malpractice. In our study, we have focused on the clinical course and evidence of HCV infection: signs, symptoms, laboratory selected, serology, and molecular tests results. The second point of interest was the condition of the ward where all the patients were hospitalized, particularly in terms of its sanitary and epidemiologic aspects. Proximate cause between infection and hospitalization was established on the basis of the highest risk and probability in accordance with the principles of opinions issued in civil cases. RESULTS In 2003, several women were hospitalized because of acute hepatitis in one of the infectious disease departments in Poland. Medical interviews revealed that all infected patients were previously admitted to the Department of Gynecology, Obstetrics, and Oncology. The detailed investigation and medical data analysis (clinical course, evolution of liver enzymes, and serologic and molecular HCV test results) proved 26 patients aged 19 to 72 years with recent HCV hepatitis hospitalized on the same gynecology ward during the infection’s incubation period (6 weeks to 6 months). In few patients, the disease was detected through the symptoms, eg, jaundice, weakness, fatigue, dyspepsia. Some women with chronic diseases were admitted to this ward several times. In these cases, aminotranspherase activity was determined each time so the dynamic of changes could be observed. The diagnostic criteria of acute hepatitis included the following: clinical course (symptoms, time of their appearance), high aminotranspherase activity or its increase, seroconversion (in a few cases, the primary serologic status was known), and HCV RNA detection. Twenty women were operated on for neoplasms: 15 had a laparotomy (genital removal); 5 had a mastectomy. In 2 cases, curettage was performed because of fetal death and diagnosis of an endometrial pathology; in 1 case, a hysteroscopy was carried out. In 3 patients, no invasive procedures were ordered during the period of hospitalization. Other procedures performed included the following: routine gynecologic examination, cytology, colposcopy, transvaginal ultrasound, blood sample collections, injections, fluid infusions, chemotherapy, and blood transfusions. The State Sanitary Inspection’s investigation revealed a number of malpractices, which finally led to the closure of the ward. The list of failures included incorrect sterilization procedures (Table 1), insufficient hygiene habits of health care workers (Table 2), poor condition of premises, and equipment being in poor condition (Table 3). The investigation revealed numerous cases of basic sanitary rules and hygienic standards being flouted as well as a lack of crucial procedures. The most significant sterilization errors related to the use of old, damaged, or prohibited sterilization packaging systems without adequate control, particularly biologic indicators. In addition, the sterilization unit, transport of contaminated and decontaminated tools, and procedures to prepare equipment for sterilization did not comply with recognized standards. Poor hygiene habits of health care workers such as washing hands, neonates, and instruments in the same washbasin or pouring bodily fluids down the toilet were
Table 1 Failings in sterilization procedures Incorrect transportation of contaminated equipment and sterile supplies Incorrect packaging material for the sterilization Using decommissioned sterilization equipment (eg, Schimmelbusch container: to multiple sterilizations) Using a dry air sterilizer Medical instrument sterilization without tray No control of packaging seals Using expired biologic tests No procedures for dealing with air becoming contaminated with contagious agents Paper packaging wet, too small, and broken Using the wrong sterilization indicator tapes
Table 2 Poor hygiene habits of health care workers Lack of compliance with proper hand hygiene (eg, washing hands, instruments, and newborns in the same washbasin: no separate handwashing sink) Medical equipment dried with hand towels Inappropriate management of sharps waste Using nonsterile materials (swabs), instruments, and equipment Lack of compliance with sanitary regulations when handling sterilized packages Lack of differentiation between behavior in sterile and nonsterile areas Incorrect disposal of biologic material (eg, pouring bodily fluids down the toilet) Using inappropriate disinfectant liquids Inappropriate frequency of thorough cleaning of operating theaters Using wicker baskets for dirty clothes and linen Lack of regular bed linen changes
noticed. A lack of proper cleaning (including insufficient cleaning equipment) and disinfection was reported. The condition of the premises was also very poor: the equipment obsolete and requiring replacement. DISCUSSION Health care-associated infections caused by medical interventions are quite rare. Epidemics called “nosocomial outbreaks” can occur in any medical department.6,7 HCV infections are predominantly reported in hemodialysis units.8 It is well-known that HCV has a significant impact on the morbidity of patients undergoing dialysis. Despite anti-HCV screening of blood products, HCV infections still occur in this group of patients because of nosocomial spread, although this is less common.9 HCV transmission may occur because of the reuse of dialysis filters, internal contamination of hemodialysis machines, and contamination of the environment but also because of a lack of standard precautions. Molecular and epidemiologic analysis shows that patient-to-patient transmission is the most common way of HCV being transmitted in this group of patients.8 Multiple intravenous procedures other than hemodialysis also carry a risk of HCV nosocomial spread. De Lédinghen et al described a large outbreak of HCV in 43 patients with a medical history of sclerotherapy of varicose veins performed by the same physician. The HCV transmission was connected with use of multidose vials.10 This method of transmitting bloodborne viruses (hepatitis B virus, HCV), which is also attributed to unsafe injection practices in nosocomial outbreaks, has been previously identified by many researchers.11-14 Nosocomial infections on gynecology wards are not particularly common. Bacterial infections are observed far more frequently than viral infections.7 Only a few HCV epidemics, including 3 because of anti-D immunoglobulin, 1 because of propofol administration, and 1 during ancillary procedures for assisted conception were described in the publications available.15-19 The 3 main ways of transmitting HCVdprimary medication contamination, patient to
M. Rorat et al. / American Journal of Infection Control 42 (2014) e7-e10 Table 3 Premises and equipment Poor condition of premises: dirty walls, damaged leather on gynecologic chairs No separation of sterile and nonsterile areas Cleaning irregularities (eg, insufficient number of mops dedicated to operating theaters; no single contact mops policy, lack of chemical reagents) Lack of washing stations for medical tools and equipment Lack of protective clothing Inappropriate “birth tract” cleansing techniques No dedicated wheelchair to carry patients to operating theaters Lack of appropriate taps meeting sanitary requirements
patient, and health care worker to patientdhave been discussed in the literature.14-19 Fortunately, the risk of hepatitis C being transmitted from an infected gynecologist to patients during medical care is marginal. Ross et al estimated this at 0.04%.14 In addition, blood transfusion became a practically safe procedure as a result of pooled nucleic acid amplification techniques and anti-HCV screening of blood donors. Cases of transfusion-acquired HCV infection only occur occasionally.20 To recognize a nosocomial outbreak, improve health safety, and prevent further incidents, a detailed investigation needs to be carried out. A sanitary and epidemiologic inspection was carried out as part of our study. The control protocol comprises multiple allegations concerning hygiene, sanitation procedures, and technical condition of equipment and facilities. Such significant negligence should not occur in any medical institution, especially one caring for oncologic patients. The key issue was lack of knowledge or ignorance of the risk of hospital-acquired infections among health care workersda typical human factor. They did not know or were not familiar with the protection procedures and were not aware of the need to obey them. The most significant malpractices concerned sterilization procedures in various stages: preparation, sterilization, packaging, segregation, and storage. No putative source of HCV infection was discovered in this epidemic, although analysis showed that 77% of patients were operated on for a gynecologic disorder. This suggests that the nosocomial spread might have been related to surgical or anesthetic procedures connected with the contamination of equipment or medication vials. Outbreaks with a similar route of transmission have been described, eg, Massari et al18 or Tallis et al.21 The medical history analysis also revealed that endoscopy procedures (colposcopy, hysteroscopy) were performed numerous times. According to the literature, some researchers conclude that these procedures are a potential source of nosocomial infections.22,23 Others prove that strict adherence to standard safety procedures eliminates the HCV transmission risk.24 Of course, in such cases, it is often difficult to determine whether the transmission resulted from contamination of medication vials or inadequate disinfection of endoscopes, especially when the investigation is conducted a long time after the outbreak.24 The investigation carried out revealed a lack of suitable sterilization standards in the gynecology department, which has been identified as one of the most important risk factors of HCV transmission. Sterilization procedures change constantly. New technologies, equipment, and control systems are always being introduced. The goal is the prevention of patient-to-patient infections. However, such actions will not prevent pathogens spreading if standard precautions such as hand hygiene, use of gloves and disposable equipment, or safe injection practices are not implemented.25 In the outbreak presented, the high number of infected women and multiple recognized errors eventually led to ward closure. Major refurbishment of the ward was then carried out, and all required procedures were implemented to improve patients’ safety. This
e9
epidemic highlighted the underreported and neglected problem of nosocomial infections in Polish hospitals. This was an incentive to increase awareness among health care workers, create appropriate procedures, and better control systems to protect against pathogens spreading. In all cases, the patients analyzed filed complaints against the hospital with the civil court. The subject of the claim was compensation for damage to health, psychologic trauma, medical expenses, inability to work, and poor prognosis for the future. The medicolegal opinions commissioned by the court and analyzed in our study focused on determining the existence of the HCV infection, the time the infection occurred, and the causal relationship with hospitalization. In accordance with the existing principles of judicial opinion delivery, both the time of development and the source of the infection were determined. We analyzed not only the defendant hospital’s malpractices but also other possible sources of infection. We used the theory of adequate causal link, which allows for determining the most likely source of infection. In all cases analyzed, both the temporal relationship with the development of the disease and the scale of the sanitary irregularities pointed to the defendant hospital. The courts ruled in favor of the patients. Limitations The respective outbreak occurred 10 years ago, but the investigations (both sanitary-epidemiologic and judicial) lasted for several consecutive years. Analysis of the HCV outbreak did not take into account the virus’s genotype because at this time it was not performed routinely. The investigation did not include all patients hospitalized at the time. Therefore, the scale of the epidemic might be underestimated. CONCLUSION Outbreaks of HCV hepatitis may result from ineffective infection control systems and remains a significant public health problem. Asymptomatic HCV nosocomial infections might go unnoticed or concealed and underreported. Auditing medical centers and health care workers for compliance with sanitary and epidemiologic requirements is an essential need. New procedures, including protection for employees against their own failings, have to be implemented to limit the risk of nosocomial infections. References 1. Silini E, Locasciulli A, Santoleri L, Gargantini L, Pinzello G, Montillo M, et al. Hepatitis C virus infection in a hematology ward: evidence for nosocomial transmission and impact on hematologic disease outcome. Haematologica 2002;87:1200-8. 2. Katsoulidou A, Paraskevis D, Kalapothaki V, Arvanitis D, Karayiannis P, Hadjiconstantiou V, et al. Molecular epidemiology of a hepatitis C virus outbreak in a haemodialysis unit. Multicentre Haemodialysis Cohort Study on Viral Hepatitis. Nephrol Dial Transplant 1999;14:1188-94. 3. Ross RS, Viazov S, Khudyakov YE, Xia GL, Lin Y, Holzmann H, et al. Transmission of hepatitis C virus in an orthopedic hospital ward. J Med Virol 2009;81:249-57. 4. Dawar M, Stuart TL, Sweet LE, Neatby AM, Abbott LP, Andonov AP, et al. Canadian hepatitis C look-back investigation to detect transmission from an infected general surgeon. Can J Infect Dis Med Microbiol 2010;21:e6-11. 5. Palka J, Truszkiewicz W. Nosocomial infections as a cause of liability claims. Arch Med Sad Krym 2007;57:81-4. 6. Danzmann L, Gastmeier P, Schwab F, Vonberg RP. Healthcare workers causing large nosocomial outbreaks: a systematic review. BMC Infect Dis 2013;13:98. 7. Vonberg RP, Weitzel-Kage D, Behnke M, Gastmeier P. Worldwide out break database: the largest collection of nosocomial outbreaks. Infection 2011; 39:29-34. 8. Su Y, Norris JL, Zang C, Peng Z, Wang N. Incidence of hepatitis C virus infection in patients on hemodialysis: a systematic review and meta-analysis. Hemodial Int; 2012. 9. Fabrizi F, Lunghi G, Ganeshan SV, Martin P, Messa P. Hepatitis C virus infection and the dialysis patient. Semin Dial 2007;20:416-22.
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10. de Lédinghen V, Trimoulet P, Mannant PR, Dumas F, Champbenoît P, Baldit C, et al. Outbreak of hepatitis C virus infection during sclerotherapy of varicose veins: long-term follow-up of 196 patients (4535 patient-years). J Hepatol 2007;46:19-25. 11. Lagging LM, Aneman C, Nenonen N, Brandberg A, Grip L, Norkrans G, 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;34:580-2. 12. Kidd-Ljunggren K, Broman E, Ekvall H, Gustavsson O. Nosocomial transmission of hepatitis B virus infection through multiple-dose vials. J Hosp Infect 1999; 43:57-62. 13. Germain J-M, Carbonne A, Thiers V, Gros H, Chastan S, Bouvet E, et al. Patientto-patient transmission of hepatitis C virus through the use of multidose vials during general anaesthesia. Infect Control Hosp Epidemiol 2005;26:789-92. 14. Ross RS, Viazov S, Thormählen M, Bartz L, Tamm J, Rautenberg P, et al. Risk of hepatitis C virus transmission from an infected gynecologist to patients: results of a 7-year retrospective investigation. Arch Intern Med 2002;162:805-10. 15. Wiese M, Grüngreiff K, Güthoff W, Lafrenz M, Oesen U, Porst H. East German Hepatitis C Study Group. Outcome in a hepatitis C (genotype 1b) single source outbreak in Germany: a 25-year multicenter study. J Hepatol 2005;43:590-8. 16. Lawlor E, Power J, Garson J, Yap P, Davidson F, Columb G, et al. Transmission rates of hepatitis C virus by different batches of a contaminated anti-D immunoglobulin preparation. Vox Sang 1999;76:138-43. 17. Smith DB, Lawlor E, Power J, O’Riordan J, McAllister J, Lycett C, et al. A second outbreak of hepatitis C virus infection from anti-D immunoglobulin in Ireland. Vox Sang 1999;76:175-80.
18. Massari M, Petrosillo N, Ippolito G, Solforosi L, Bonazzi L, Clementi M, et al. Transmission of hepatitis C virus in a gynaecological surgery setting. J Clin Microbiol 2001;39:2860-3. 19. Lesourd F, Izopet J, Mervan C, Payen JL, Sandres K, Monrozies X, et al. Transmissions of hepatitis C virus during the ancillary procedures for assisted conception. Hum Reprod 2000;15:1083-5. 20. Kretzschmar E, Chudy M, Nübling CM, Ross RS, Kruse F, Trobisch H. First case of hepatitis C virus transmission by a red blood cell concentrate after introduction of nucleic acid amplification technique screening in Germany: a comparative study with various assays. Vox Sang 2007;92:297-301. 21. Tallis GF, Ryan GM, Lambert SB, Bowden DS, McCaw R, Birch CJ, et al. Evidence of patient-to-patient transmission of hepatitis C virus through contaminated intravenous anaesthetic ampoules. J Viral Hepat 2003;10:234-9. 22. Bronowicki JP, Venard V, Botte C, Monhoven N, Gastin I, Chone L, et al. Patientto-patient transmission of hepatitis C virus during colonoscopy. N Engl J Med 1997;337:237-40. 23. González-Candelas F, Guiral S, Carbó R, Valero A, Vanaclocha H, González F, et al. Patient-to-patient transmission of hepatitis C virus (HCV) during colonoscopy diagnosis. Virol J 2010;7:217. 24. 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. 25. Siegel JD, Rhinehart E, Jackson M, Chiarello L. Health Care Infection Control Practices Advisory Committee: 2007 Guideline for isolation precautions: preventing transmission of infectious agents in health care settings. Am J Infect Control 2007;35:65-164.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Major article
Outbreak of hepatitis C among patients admitted to the Department of Gynecology, Obstetrics, and Oncology Marta Rorat MD *, Tomasz Jurek PhD, Lukasz Szleszkowski PhD, Andrzej Gladysz PhD Department of Forensic Medicine, Wroclaw Medical University, Wroclaw, Poland
Key Words: Safety Infection control Equipment contamination Adverse event
Background: In Poland, nosocomial infections account for 32% of all patients’ claims against public hospitals, with hepatitis B virus and hepatitis C virus (HCV) being the most common causes. We present a major nosocomial outbreak of the HCV infection in the Department of Gynecology, Obstetrics, and Oncology and the results of detailed sanitary and epidemiologic research. Methods: A retrospective analysis of medicolegal opinions issued at the request of the civil court regarding the suspicion of HCV nosocomial infections was conducted. Results: The detailed medical data analysis proved 26 patients aged 19 to 72 years with recent HCV hepatitis hospitalized on the same gynecology ward. Twenty women were operated on for neoplasm. The State Sanitary Inspection’s investigation revealed a number of malpractices: incorrect sterilization procedures, insufficient hygiene habits of health care workers, poor condition of premises, and equipment being in poor condition. Numerous cases of staff breaking basic sanitary rules and hygiene standards and a lack of crucial procedures were discovered. The high number of women infected and the multiple errors recognized led to closure of the ward. Conclusion: Outbreaks of HCV hepatitis may be the result of ineffective infection control systems and remains a significant public health problem. Asymptomatic HCV nosocomial infections might go unnoticed or concealed and underreported. Auditing medical centers and health care workers for compliance with sanitary and epidemiologic requirements is an essential need. Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Despite the introduction of multiple procedures minimizing the risk of the nosocomial hepatitis C virus (HCV) infection (blood donor screening in particular), local outbreaks are still being observed. The risk of acquiring HCV hepatitis is highest among hemodialysis patients or those treated for hematologic malignancies.1,2 Because HCV is most commonly transmitted via the parenteral route, blood transfusions, fluid infusions, injections, and invasive medical and surgical interventions using contaminated specimens and equipment is a major source of hospital infections. Some studies show the correlation between the risk of HCV infection and the duration of previous hospital admissions as well as the type and number of invasive medical procedures the patient has undergone.3 HCV transmission has also been documented to result from contact with infected health care workers, eg, during surgery. In these cases, the risk of infection depends on the viral status of the
* Address correspondence to Marta Rorat, MD, Mikulicza-Radeckiego 4, 50-345 Wroclaw, Poland. E-mail address: [email protected] (M. Rorat). Conflicts of interest: None to report.
source person and the type and duration of exposure-prone procedures.4 The nosocomial spread of the HCV infection is usually difficult to prove because the majority of patients do not present any symptoms of acute hepatitis. The detection of the disease is accidental and predominantly delayed for many years. In addition, other sources of infectiondintravenous drug use and perinatal or sexual transmissiondcannot be ruled out definitively. Nosocomial HCV infections do not just have significant medical implications but legal ones as well. In Poland, nosocomial infections account for 32% of all patients’ claims against public hospitals, with hepatitis B virus and HCV being the most common cause, especially on gynecology and obstetrics wards.5 In the following study, we present a major nosocomial outbreak of HCV infection in the Department of Gynecology, Obstetrics, and Oncology, discovered as a result of thorough research. MATERIALS AND METHODS A retrospective analysis of 26 medicolegal opinions issued at the request of the civil court regarding the suspicion of hepatitis C
0196-6553/$36.00 - Copyright Ó 2014 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2013.07.016
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M. Rorat et al. / American Journal of Infection Control 42 (2014) e7-e10
nosocomial infections was conducted. An epidemiologic investigation was performed to identify the cases, the source of infection/ contamination, and the route of the spreading of the virus. All the patients in question were diagnosed with a HCV infection between May and November 2003. All cases of infection were confirmed using polymerase chain reaction. The study protocol comprised the following: age, data included in medical records (diagnosis, all procedures performed, medical history), and results of the epidemiologic investigation conducted by the sanitary-epidemiologic services as well as testimonies provided by patients during court proceedings on the alleged malpractice. In our study, we have focused on the clinical course and evidence of HCV infection: signs, symptoms, laboratory selected, serology, and molecular tests results. The second point of interest was the condition of the ward where all the patients were hospitalized, particularly in terms of its sanitary and epidemiologic aspects. Proximate cause between infection and hospitalization was established on the basis of the highest risk and probability in accordance with the principles of opinions issued in civil cases. RESULTS In 2003, several women were hospitalized because of acute hepatitis in one of the infectious disease departments in Poland. Medical interviews revealed that all infected patients were previously admitted to the Department of Gynecology, Obstetrics, and Oncology. The detailed investigation and medical data analysis (clinical course, evolution of liver enzymes, and serologic and molecular HCV test results) proved 26 patients aged 19 to 72 years with recent HCV hepatitis hospitalized on the same gynecology ward during the infection’s incubation period (6 weeks to 6 months). In few patients, the disease was detected through the symptoms, eg, jaundice, weakness, fatigue, dyspepsia. Some women with chronic diseases were admitted to this ward several times. In these cases, aminotranspherase activity was determined each time so the dynamic of changes could be observed. The diagnostic criteria of acute hepatitis included the following: clinical course (symptoms, time of their appearance), high aminotranspherase activity or its increase, seroconversion (in a few cases, the primary serologic status was known), and HCV RNA detection. Twenty women were operated on for neoplasms: 15 had a laparotomy (genital removal); 5 had a mastectomy. In 2 cases, curettage was performed because of fetal death and diagnosis of an endometrial pathology; in 1 case, a hysteroscopy was carried out. In 3 patients, no invasive procedures were ordered during the period of hospitalization. Other procedures performed included the following: routine gynecologic examination, cytology, colposcopy, transvaginal ultrasound, blood sample collections, injections, fluid infusions, chemotherapy, and blood transfusions. The State Sanitary Inspection’s investigation revealed a number of malpractices, which finally led to the closure of the ward. The list of failures included incorrect sterilization procedures (Table 1), insufficient hygiene habits of health care workers (Table 2), poor condition of premises, and equipment being in poor condition (Table 3). The investigation revealed numerous cases of basic sanitary rules and hygienic standards being flouted as well as a lack of crucial procedures. The most significant sterilization errors related to the use of old, damaged, or prohibited sterilization packaging systems without adequate control, particularly biologic indicators. In addition, the sterilization unit, transport of contaminated and decontaminated tools, and procedures to prepare equipment for sterilization did not comply with recognized standards. Poor hygiene habits of health care workers such as washing hands, neonates, and instruments in the same washbasin or pouring bodily fluids down the toilet were
Table 1 Failings in sterilization procedures Incorrect transportation of contaminated equipment and sterile supplies Incorrect packaging material for the sterilization Using decommissioned sterilization equipment (eg, Schimmelbusch container: to multiple sterilizations) Using a dry air sterilizer Medical instrument sterilization without tray No control of packaging seals Using expired biologic tests No procedures for dealing with air becoming contaminated with contagious agents Paper packaging wet, too small, and broken Using the wrong sterilization indicator tapes
Table 2 Poor hygiene habits of health care workers Lack of compliance with proper hand hygiene (eg, washing hands, instruments, and newborns in the same washbasin: no separate handwashing sink) Medical equipment dried with hand towels Inappropriate management of sharps waste Using nonsterile materials (swabs), instruments, and equipment Lack of compliance with sanitary regulations when handling sterilized packages Lack of differentiation between behavior in sterile and nonsterile areas Incorrect disposal of biologic material (eg, pouring bodily fluids down the toilet) Using inappropriate disinfectant liquids Inappropriate frequency of thorough cleaning of operating theaters Using wicker baskets for dirty clothes and linen Lack of regular bed linen changes
noticed. A lack of proper cleaning (including insufficient cleaning equipment) and disinfection was reported. The condition of the premises was also very poor: the equipment obsolete and requiring replacement. DISCUSSION Health care-associated infections caused by medical interventions are quite rare. Epidemics called “nosocomial outbreaks” can occur in any medical department.6,7 HCV infections are predominantly reported in hemodialysis units.8 It is well-known that HCV has a significant impact on the morbidity of patients undergoing dialysis. Despite anti-HCV screening of blood products, HCV infections still occur in this group of patients because of nosocomial spread, although this is less common.9 HCV transmission may occur because of the reuse of dialysis filters, internal contamination of hemodialysis machines, and contamination of the environment but also because of a lack of standard precautions. Molecular and epidemiologic analysis shows that patient-to-patient transmission is the most common way of HCV being transmitted in this group of patients.8 Multiple intravenous procedures other than hemodialysis also carry a risk of HCV nosocomial spread. De Lédinghen et al described a large outbreak of HCV in 43 patients with a medical history of sclerotherapy of varicose veins performed by the same physician. The HCV transmission was connected with use of multidose vials.10 This method of transmitting bloodborne viruses (hepatitis B virus, HCV), which is also attributed to unsafe injection practices in nosocomial outbreaks, has been previously identified by many researchers.11-14 Nosocomial infections on gynecology wards are not particularly common. Bacterial infections are observed far more frequently than viral infections.7 Only a few HCV epidemics, including 3 because of anti-D immunoglobulin, 1 because of propofol administration, and 1 during ancillary procedures for assisted conception were described in the publications available.15-19 The 3 main ways of transmitting HCVdprimary medication contamination, patient to
M. Rorat et al. / American Journal of Infection Control 42 (2014) e7-e10 Table 3 Premises and equipment Poor condition of premises: dirty walls, damaged leather on gynecologic chairs No separation of sterile and nonsterile areas Cleaning irregularities (eg, insufficient number of mops dedicated to operating theaters; no single contact mops policy, lack of chemical reagents) Lack of washing stations for medical tools and equipment Lack of protective clothing Inappropriate “birth tract” cleansing techniques No dedicated wheelchair to carry patients to operating theaters Lack of appropriate taps meeting sanitary requirements
patient, and health care worker to patientdhave been discussed in the literature.14-19 Fortunately, the risk of hepatitis C being transmitted from an infected gynecologist to patients during medical care is marginal. Ross et al estimated this at 0.04%.14 In addition, blood transfusion became a practically safe procedure as a result of pooled nucleic acid amplification techniques and anti-HCV screening of blood donors. Cases of transfusion-acquired HCV infection only occur occasionally.20 To recognize a nosocomial outbreak, improve health safety, and prevent further incidents, a detailed investigation needs to be carried out. A sanitary and epidemiologic inspection was carried out as part of our study. The control protocol comprises multiple allegations concerning hygiene, sanitation procedures, and technical condition of equipment and facilities. Such significant negligence should not occur in any medical institution, especially one caring for oncologic patients. The key issue was lack of knowledge or ignorance of the risk of hospital-acquired infections among health care workersda typical human factor. They did not know or were not familiar with the protection procedures and were not aware of the need to obey them. The most significant malpractices concerned sterilization procedures in various stages: preparation, sterilization, packaging, segregation, and storage. No putative source of HCV infection was discovered in this epidemic, although analysis showed that 77% of patients were operated on for a gynecologic disorder. This suggests that the nosocomial spread might have been related to surgical or anesthetic procedures connected with the contamination of equipment or medication vials. Outbreaks with a similar route of transmission have been described, eg, Massari et al18 or Tallis et al.21 The medical history analysis also revealed that endoscopy procedures (colposcopy, hysteroscopy) were performed numerous times. According to the literature, some researchers conclude that these procedures are a potential source of nosocomial infections.22,23 Others prove that strict adherence to standard safety procedures eliminates the HCV transmission risk.24 Of course, in such cases, it is often difficult to determine whether the transmission resulted from contamination of medication vials or inadequate disinfection of endoscopes, especially when the investigation is conducted a long time after the outbreak.24 The investigation carried out revealed a lack of suitable sterilization standards in the gynecology department, which has been identified as one of the most important risk factors of HCV transmission. Sterilization procedures change constantly. New technologies, equipment, and control systems are always being introduced. The goal is the prevention of patient-to-patient infections. However, such actions will not prevent pathogens spreading if standard precautions such as hand hygiene, use of gloves and disposable equipment, or safe injection practices are not implemented.25 In the outbreak presented, the high number of infected women and multiple recognized errors eventually led to ward closure. Major refurbishment of the ward was then carried out, and all required procedures were implemented to improve patients’ safety. This
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epidemic highlighted the underreported and neglected problem of nosocomial infections in Polish hospitals. This was an incentive to increase awareness among health care workers, create appropriate procedures, and better control systems to protect against pathogens spreading. In all cases, the patients analyzed filed complaints against the hospital with the civil court. The subject of the claim was compensation for damage to health, psychologic trauma, medical expenses, inability to work, and poor prognosis for the future. The medicolegal opinions commissioned by the court and analyzed in our study focused on determining the existence of the HCV infection, the time the infection occurred, and the causal relationship with hospitalization. In accordance with the existing principles of judicial opinion delivery, both the time of development and the source of the infection were determined. We analyzed not only the defendant hospital’s malpractices but also other possible sources of infection. We used the theory of adequate causal link, which allows for determining the most likely source of infection. In all cases analyzed, both the temporal relationship with the development of the disease and the scale of the sanitary irregularities pointed to the defendant hospital. The courts ruled in favor of the patients. Limitations The respective outbreak occurred 10 years ago, but the investigations (both sanitary-epidemiologic and judicial) lasted for several consecutive years. Analysis of the HCV outbreak did not take into account the virus’s genotype because at this time it was not performed routinely. The investigation did not include all patients hospitalized at the time. Therefore, the scale of the epidemic might be underestimated. CONCLUSION Outbreaks of HCV hepatitis may result from ineffective infection control systems and remains a significant public health problem. Asymptomatic HCV nosocomial infections might go unnoticed or concealed and underreported. Auditing medical centers and health care workers for compliance with sanitary and epidemiologic requirements is an essential need. New procedures, including protection for employees against their own failings, have to be implemented to limit the risk of nosocomial infections. References 1. Silini E, Locasciulli A, Santoleri L, Gargantini L, Pinzello G, Montillo M, et al. Hepatitis C virus infection in a hematology ward: evidence for nosocomial transmission and impact on hematologic disease outcome. Haematologica 2002;87:1200-8. 2. Katsoulidou A, Paraskevis D, Kalapothaki V, Arvanitis D, Karayiannis P, Hadjiconstantiou V, et al. Molecular epidemiology of a hepatitis C virus outbreak in a haemodialysis unit. Multicentre Haemodialysis Cohort Study on Viral Hepatitis. Nephrol Dial Transplant 1999;14:1188-94. 3. Ross RS, Viazov S, Khudyakov YE, Xia GL, Lin Y, Holzmann H, et al. Transmission of hepatitis C virus in an orthopedic hospital ward. J Med Virol 2009;81:249-57. 4. Dawar M, Stuart TL, Sweet LE, Neatby AM, Abbott LP, Andonov AP, et al. Canadian hepatitis C look-back investigation to detect transmission from an infected general surgeon. Can J Infect Dis Med Microbiol 2010;21:e6-11. 5. Palka J, Truszkiewicz W. Nosocomial infections as a cause of liability claims. Arch Med Sad Krym 2007;57:81-4. 6. Danzmann L, Gastmeier P, Schwab F, Vonberg RP. Healthcare workers causing large nosocomial outbreaks: a systematic review. BMC Infect Dis 2013;13:98. 7. Vonberg RP, Weitzel-Kage D, Behnke M, Gastmeier P. Worldwide out break database: the largest collection of nosocomial outbreaks. Infection 2011; 39:29-34. 8. Su Y, Norris JL, Zang C, Peng Z, Wang N. Incidence of hepatitis C virus infection in patients on hemodialysis: a systematic review and meta-analysis. Hemodial Int; 2012. 9. Fabrizi F, Lunghi G, Ganeshan SV, Martin P, Messa P. Hepatitis C virus infection and the dialysis patient. Semin Dial 2007;20:416-22.
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10. de Lédinghen V, Trimoulet P, Mannant PR, Dumas F, Champbenoît P, Baldit C, et al. Outbreak of hepatitis C virus infection during sclerotherapy of varicose veins: long-term follow-up of 196 patients (4535 patient-years). J Hepatol 2007;46:19-25. 11. Lagging LM, Aneman C, Nenonen N, Brandberg A, Grip L, Norkrans G, 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;34:580-2. 12. Kidd-Ljunggren K, Broman E, Ekvall H, Gustavsson O. Nosocomial transmission of hepatitis B virus infection through multiple-dose vials. J Hosp Infect 1999; 43:57-62. 13. Germain J-M, Carbonne A, Thiers V, Gros H, Chastan S, Bouvet E, et al. Patientto-patient transmission of hepatitis C virus through the use of multidose vials during general anaesthesia. Infect Control Hosp Epidemiol 2005;26:789-92. 14. Ross RS, Viazov S, Thormählen M, Bartz L, Tamm J, Rautenberg P, et al. Risk of hepatitis C virus transmission from an infected gynecologist to patients: results of a 7-year retrospective investigation. Arch Intern Med 2002;162:805-10. 15. Wiese M, Grüngreiff K, Güthoff W, Lafrenz M, Oesen U, Porst H. East German Hepatitis C Study Group. Outcome in a hepatitis C (genotype 1b) single source outbreak in Germany: a 25-year multicenter study. J Hepatol 2005;43:590-8. 16. Lawlor E, Power J, Garson J, Yap P, Davidson F, Columb G, et al. Transmission rates of hepatitis C virus by different batches of a contaminated anti-D immunoglobulin preparation. Vox Sang 1999;76:138-43. 17. Smith DB, Lawlor E, Power J, O’Riordan J, McAllister J, Lycett C, et al. A second outbreak of hepatitis C virus infection from anti-D immunoglobulin in Ireland. Vox Sang 1999;76:175-80.
18. Massari M, Petrosillo N, Ippolito G, Solforosi L, Bonazzi L, Clementi M, et al. Transmission of hepatitis C virus in a gynaecological surgery setting. J Clin Microbiol 2001;39:2860-3. 19. Lesourd F, Izopet J, Mervan C, Payen JL, Sandres K, Monrozies X, et al. Transmissions of hepatitis C virus during the ancillary procedures for assisted conception. Hum Reprod 2000;15:1083-5. 20. Kretzschmar E, Chudy M, Nübling CM, Ross RS, Kruse F, Trobisch H. First case of hepatitis C virus transmission by a red blood cell concentrate after introduction of nucleic acid amplification technique screening in Germany: a comparative study with various assays. Vox Sang 2007;92:297-301. 21. Tallis GF, Ryan GM, Lambert SB, Bowden DS, McCaw R, Birch CJ, et al. Evidence of patient-to-patient transmission of hepatitis C virus through contaminated intravenous anaesthetic ampoules. J Viral Hepat 2003;10:234-9. 22. Bronowicki JP, Venard V, Botte C, Monhoven N, Gastin I, Chone L, et al. Patientto-patient transmission of hepatitis C virus during colonoscopy. N Engl J Med 1997;337:237-40. 23. González-Candelas F, Guiral S, Carbó R, Valero A, Vanaclocha H, González F, et al. Patient-to-patient transmission of hepatitis C virus (HCV) during colonoscopy diagnosis. Virol J 2010;7:217. 24. 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. 25. Siegel JD, Rhinehart E, Jackson M, Chiarello L. Health Care Infection Control Practices Advisory Committee: 2007 Guideline for isolation precautions: preventing transmission of infectious agents in health care settings. Am J Infect Control 2007;35:65-164.
