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Control of methicillin-resistant Staphylococcus aureus outbreak involving several hospitals
Journal of Hospital Infection (2004) 58, 180–186
www.elsevierhealth.com/journals/jhin
Control of methicillin-resistant Staphylococcus aureus outbreak involving several hospitals S. Pastilaa,*, K.T. Sammalkorpib, J. Vuopio-Varkilac,d, S. Kontiainend, M.A. Ristolab a
¨me Central Hospital, 13530 Ha ¨meenlinna, Finland Kanta-Ha Division of Infectious Diseases, Department of Medicine, Helsinki University Central Hospital, Helsinki, Finland c Department of Microbiology, National Public Health Institute, Helsinki, Finland d HUCH Laboratory Diagnostics, Helsinki University Central Hospital, Helsinki, Finland b
Received 14 March 2004; accepted 24 May 2004
KEYWORDS Epidemiology; Infection control; MRSA; Nosocomial infection; Outbreaks
Summary This population-based, retrospective, cohort study describes a large methicillin-resistant Staphylococcus aureus (MRSA) epidemic caused by one strain (E1) in the greater Helsinki region. The epidemic comprised 210 cases at several hospitals, but was finally controlled. The study period ranged from June 1991 to December 2000. The epidemic peaked in 1993 – 1995 with 143 cases (68% of total cases). From August 1993, all MRSA-positive cases at the eight municipal hospitals were isolated and barrier nursed. Contacts were cohorted and screened for MRSA colonization. Decolonization treatment was administered to some chronic carriers. MRSA cases and contacts were identified in the joint patient register of the municipal hospitals from August 1993. The annual incidence of MRSA E1 in Helsinki City area per 100 000 inhabitants rose from 0.2 in 1991 to 13.6 in 1994. It decreased from 1995, reaching 0.7 per 100 000 in 2000. A jointly agreed policy on MRSA and timely co-operation between all units were essential for control of this epidemic. Q 2004 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved.
Introduction Before the 1990s, strains of methicillin-resistant Staphylococcus aureus (MRSA) were rare and no MRSA epidemics had been reported in Finland. Between 1981 and 1991, the annual number of *Corresponding author. Tel.: þ 358-9-58011; fax: þ 358-95801204. E-mail address: [email protected]
reported sporadic MRSA cases in Finland varied from 95 to 164.1 Since 1992, MRSA strains have been typed systematically, and data on the characteristics and epidemiology of MRSA strains have been collected. Since 1995, MRSA has been notifiable in Finland and the information on MRSA cases is available in the National Infectious Disease Register at the National Public Health Institute. The first published MRSA epidemic in Finland broke out at Turku University Central Hospital in 1991 – 1992.2,3
0195-6701/$ - see front matter Q 2004 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2004.06.024
Control of MRSA outbreak involving several hospitals
The first epidemic MRSA strain in Helsinki began to spread approximately concurrently with the epidemic in Turku. However, the epidemic in Helsinki was only identified in 1993. This article will describe the course of the epidemic and the measures that were undertaken to control the first MRSA epidemic in Helsinki.
Methods Design and setting This was a population-based, retrospective, cohort study, and the study period was from June 1991 to December 2000. All patients at the municipal hospitals (eight secondary care hospitals) and at University Central Hospital (UCH) during the study period were included. The cases were patients who were either infected or colonized with the epidemic MRSA strain E1. The cases were identified by their unique national social security number, which was also used for identification in the joint patient register of the municipal healthcare authority. Each case was only counted once. This paper also describes the MRSA-E1-positive cultures among staff members, but they were not included as cases in this study. In the 1990s, the hospital facilities in Helsinki City consisted of UCH and eight municipal hospitals (Hospitals A – H) that provided secondary care for Helsinki City. Three of the eight municipal hospitals had surgical services and one had extensive facilities for isolation. Hospitals A and G had emergency rooms and wards, and Hospital A had an intermediate care unit (a ward providing intermediate monitoring, between intensive care unit and ward level). The majority of the secondary care hospitals had both acute and long-term care wards. Patients were frequently transported between and within tertiary care, secondary care and long-term wards. UCH provided tertiary care for the greater Helsinki region. Between 1991 and 2000, the population of Helsinki increased from 497 542 to 555 474, and that of the greater Helsinki region increased from 1 248 072 to 1 379 712 (according to official statistics from Statistics Finland). An infectious diseases specialist, who acted as the co-ordinator, collected data on MRSA E1 from 1993 to 1996, as entailed in the Finnish legislation for communicable diseases. A database on the cases admitted to Hospital C from 1993 was set up in 1996. Approval for the database was obtained from the ethics committee of the municipal health
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authority in Helsinki and from the Finnish Ministry of Social Affairs and Health. Data on MRSA cases since 1995 were available in the National Infectious Disease Register at the National Public Health Institute. The information on MRSA cases from 1992 to 1994 was obtained from the Laboratory of Hospital Bacteriology at the National Public Health Institute, which at that time was collecting and typing all suspected MRSA cases in Finland. The three MRSA E1 cases from before August 1992 were detected retrospectively in laboratory files.
Microbiological methods Microbiological samples were processed at two microbiology laboratories with similar analytical procedures. Up to 1994, MRSA strains were detected through standard bacterial culture and resistance testing. From August 1994, enrichment (broth tubes) and selective cultures (mannitol-salt agar plates with oxacillin) were used routinely for detection. These methods were used for all requested MRSA cultures and as a supplement to all ‘pus’ cultures (including wound sampling and clinical puncture or drainage) from hospitals involved in the epidemic. A preliminary positive result for MRSA was defined as growth of typical colonies on selective culture plates and positive Gram stain, catalase and latex agglutination test results. Isolated MRSA strains were verified and typed at the Laboratory of Hospital Bacteriology at the National Public Health Institute. Microbiological methods and the characteristics of MRSA E1 have been described previously.1,4
Organization of the MRSA control team in the municipal hospitals Before August 1993, there was no uniform MRSA policy at the municipal hospitals in Helsinki. As the extent of the epidemic became known, a common strategy for MRSA was developed. A consultant in infectious diseases was appointed by the head of the municipal hospitals as a co-ordinator for the epidemic-related measures in all of the municipal hospitals. Part-time infection control (IC) nurses in the municipal hospitals were the co-ordinator’s primary contacts, and they worked in close cooperation with the physicians of the wards affected by the epidemic. A senior consultant in the microbiological laboratory notified the co-ordinator, the physician in charge of the ward, and the IC nurse by telephone about all new positive MRSA isolations after a preliminary identification. The coordinator had meetings with the IC nurses and
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infectious diseases consultants to guarantee the uniformity of measures in all units.
Clinical infections and decontamination treatment
MRSA sampling procedures
Clinical infections due to MRSA E1 were treated with antimicrobial agents according to resistance testing. Systemic decolonization treatment was only administered to a few selected cases. Nasal MRSA carriage of staff was treated with nasal mupirocin, and absence from work was requested until a negative follow-up sample was obtained.
In August 1993, sampling of MRSA cases and contacts (i.e. roommates of the cases) was started. By the end of 1993, screening samples were only taken from the nares, skin lesions, drains and other sites that were previously positive. During the first three months of the epidemic, more extensive sampling was performed, including throat, groin and armpits. Staff members were sampled once from the nares and potential skin lesions. Hospital staff were only screened on three occasions during the epidemic and no environmental MRSA samples were taken.
Measures to control the epidemic Cohorting, isolation, barrier nursing and screening From August 1993, all MRSA-positive cases identified at the municipal hospitals were cohorted on an isolation ward at Hospital C. The MRSA cases were isolated in separate rooms from other patients, and most of the rooms had an anteroom. The cases were barrier nursed until discharge or until three successive negative MRSA cultures were obtained. From 1993 to 1997, barrier nursing included the use of gloves, a surgical mask and a gown. At the beginning of 1995, the isolation practice in Hospital C was disrupted for two months and the barrier nursing was temporarily reduced to the use of gloves and alcohol hand rub. The use of a mask in barrier nursing was stopped in 1997. Upon subsequent admissions, all cases were isolated and screened for MRSA. This procedure was discontinued if MRSA cultures had been negative for 12 months. Contacts were cohorted, barrier nursed and screened for MRSA colonization twice with a one-week interval. If contacts had been discharged, screening was performed upon subsequent admission. MRSA screening was also performed before any patient was transferred to another hospital from a ward affected by the epidemic. Fortnightly screening of chronic wounds was carried out on the epidemic-affected wards at Hospital B from November to December 1994. At UCH, MRSA cases were isolated and barrier nursed. Nine cases of MRSA E1 were transferred to Hospital C for isolation.
Education of staff and recognition of cases The importance of hand hygiene in patient care was emphasized vigorously in all the municipal hospitals. Lectures was given and practical education on hand hygiene was arranged at all the epidemicaffected hospitals. From 1993, all MRSA-positive cases and their contacts were specifically indicated in the joint patient register of the municipal hospitals, which enabled rapid identification of MRSA carriers and contacts at the municipal hospitals and in primary healthcare facilities.
Results Identification of the epidemic Between August 1992 and June 1993, four MRSA E1 cases were barrier nursed but not isolated on the surgical index ward at Hospital A. No screening of contacts took place. Five additional cases of MRSA that were detected during that period were later typed as E1. All these cases had a recent admission to the surgical index ward at Hospital A. The index ward at Hospital A was closed due to administrative reasons for eight weeks in June 1993, and the patients were transferred to other surgical wards at Hospital A. In August 1993, five cases of MRSA E1 were detected on two of the surgical wards that had received patients from the index ward. At this point, the epidemic was identified and control measures were introduced.
Outbreak at Hospital A The surgical ward at Hospital A, which appeared to have the majority of recent MRSA E1 cases in August 1993, was closed for new admissions for seven days and all patients were screened for MRSA colonization. Screening of all patients was arranged on the other surgical ward with two cases of MRSA E1 in August 1993, but this ward remained open for new admissions. Due to abundant patient traffic
Control of MRSA outbreak involving several hospitals
between the intermediate care unit and surgical wards of Hospital A, all patients in the intermediate care unit were screened for MRSA colonization. The staff of three surgical wards, the intermediate care unit, the operating theatre, the emergency room, and the surgical outpatient clinic of Hospital A were also screened. By the end of 1993, there were eight more cases of MRSA E1 detected with a preceding admission to these two wards. Two cases of MRSA E1 were identified in March 1994 in the intermediate care unit and nine cases were identified between October and December 1994 in the surgical index ward. There were six cases of MRSA E1 related to Hospital A during 1995: five of these had been admitted to one of the two surgical wards which had the majority of cases in August 1993. Since 1995, only two MRSA E1 cases have been detected in Hospital A (Table I and Figure 1).
Outbreak at Hospital B The epidemic spread to Hospital B in March 1994. The first case at Hospital B had a clear connection with Hospital A. In August 1994, two clinical samples from one ward grew MRSA E1. A screening at that ward disclosed nine new cases. On two other wards at Hospital B, four clinical samples were positive for MRSA E1 in September 1994. Screening on all the affected wards during September and October 1994 yielded 19 cases among patients. Screening of chronic wounds was carried out on all wards at Hospital B during November and December 1994; this screening yielded four MRSA E1 cases. In 1997, there was another outbreak of MRSA E1 at Hospital B without any clear connection to the earlier cases. Ten of the 15 cases were due to secondary spread. The outbreak subsided in two months with the same interventions as in 1994 (Table I and Figure 1).
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Figure 1 Annual incidence of new MRSA E1 cases at municipal hospitals in relation to the population of Helsinki from 1991 to 2000. Solid bars, Hospital A; hatched bars, Hospital B; open bars, Hospital D; solid circles, incidence per 100 000 inhabitants.
Cases at other hospitals and in primary care At Hospital C, there was a cluster of five MRSA cases in 1995 that coincided with the two months of discontinuation of the isolation practices and removal of the barrier nursing. At Hospital D, there were 13 sporadic cases of MRSA E1 between 1993 and 1996, without an evident connection to the other hospitals, and eight secondary cases among contacts (Table I and Figure 1). The measures for containment of the epidemic were similar to those at the other municipal hospitals.
Description of cases The median age of the cases was 76 years (range 25 – 102 years). One hundred and sixteen (55%) of the MRSA E1 cases were male. A considerable proportion of MRSA E1 cases throughout the course of the epidemic were only colonized with MRSA. For example, in Hospital B during the autumn of 1994,
Table I MRSA E1—annual number of new cases 1991–2000 Year Hospital A Hospital B Hospital C Hospital D Hospital E Hospital F Hospital G Hospital H MH total PHC UCH Total
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
Total
1 0 0 0 0 0 0 0 1 0 0 1
4 0 0 0 0 0 0 0 4 1 0 5
17 0 0 1 0 0 0 0 18 0 3 21
11 38 1 5 0 7 1 0 63 1 12 76
6 2 5 14 1 4 2 0 34 2 10 46
1 3 0 1 1 0 0 0 6 0 7 13
0 15 0 0 0 0 0 0 15 3 4 22
0 0 0 0 0 0 0 0 0 1 15 16
1 1 0 0 0 0 0 0 2 0 4 6
0 2 0 0 0 0 0 0 2 0 2 4
41 61 6 21 2 11 3 0 145 8 57 210
MH, municipal hospitals; PHC, primary healthcare facilities; UCH, University Central Hospital.
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68% of MRSA-E1-positive cultures were from screening samples. Among the 123 cases that were admitted to the isolation ward at Hospital C between 1993 and 1996, there were 28 (23%) cases with confirmed clinical infection by MRSA E1. Of the 28 cases with clinical MRSA E1 infection, three (11%) had bacteraemia, six (21%) had a surgical-site infection, and 14 (50%) had infection of a chronic pressure wound or another skin lesion. The remaining five cases had MRSA E1 infection of the outer ear, conjunctiva, gastrointestinal tract (two cases) and respiratory tract. Nine additional clinical infections by MRSA E1 were detected at the other municipal hospitals during the study period. The majority (69%) of MRSA E1 cases were detected in secondary care, while 27% were detected at UCH and 4% were detected in primary healthcare facilities (Table I). Of the 57 cases detected at UCH, 32 were residents of Helsinki City. The annual incidence of MRSA E1 between 1992 and 2000 in Helsinki is shown in Figure 1.
MRSA E1 among staff At Hospital A, four staff members were detected as being carriers of MRSA E1. At Hospital B, there were three nasal carriers among the staff, and the screening at Hospital C revealed only one positive culture and it was therefore terminated. In total, there were eight nasal carriers detected among the staff. All had negative nasal swabs after local mupirocin. No follow-up sampling was arranged.
Screening samples By the end of 1995 (i.e. in 29 months), 17 198 screening samples had been taken at the municipal hospitals. Of these, 1010 (5.9%) were positive.
Discussion This population-based, retrospective, cohort study describes a large MRSA epidemic caused by one strain (E1) in the greater Helsinki region. Although the epidemic involved 210 cases at several hospitals, it was finally controlled. According to the Laboratory of Hospital Bacteriology at the National Public Health Institute and the National Infectious Disease Registry, between 1992 and 2000 there were 1522 new MRSA cases in Finland, of which 456 were in Helsinki City. Thus, MRSA E1 constituted 40% of all MRSA cases in Helsinki City during the study period. There were 60
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MRSA E1 cases in other parts of Finland (27% of all MRSA cases) between 1992 and 1996. Identification and typing of suspected MRSA cases in the Laboratory of Hospital Bacteriology at the National Public Health Institute between 1992 and 1994 was non-compulsory, which could have led to the under-reporting of cases. However, the two major clinical microbiological laboratories serving the hospitals included in this study had a close and consistent collaboration with the Laboratory of Hospital Bacteriology, and we believe that there was practically no under-reporting of MRSA in the Helsinki region. We believe that isolation and barrier nursing of cases, and vigorous screening of contacts led to successful control of this MRSA E1 outbreak. Our experience supports the view obtained from smaller MRSA outbreaks that these measures are important to control the spread of MRSA.2,5,6 Data on other major MRSA epidemics7,8 also support the validity of our measures. The ‘wait-and-see’ practice between 1991 and 1993 was followed by an extensive epidemic with 122 new cases and spread to four new hospitals between 1994 and 1995 (Table I). After implementing the control measures in the autumn of 1993, the annual number of new cases increased until the following year and then declined sharply (Figure 1). The closure of wards during staff’s annual holidays and transfer of patients to other wards most likely contributed to the spread of the epidemic in 1993 in a similar manner as described earlier.9 It is also likely that the increase in the workload of nursing staff played a role in the spread of MRSA.10 Natural decline of the epidemic in the mid 1990s is unlikely. The number of new cases at Hospital A in 1993 did not decline until the control measures were implemented, and a smaller outbreak took place in 1994 at Hospital A despite these measures. Additionally, MRSA E1 recurred in 1997 at Hospital B after two years with only sporadic cases. MRSA E1 seemed to spread easily in the hospital setting; all 127 cases detected in the municipal hospitals between August 1992 and December 1996 had a preceding admission to an epidemic-affected unit. As described earlier, 98% of the MRSA E1 cases between 1997 and 1999 also had a preceding hospital contact.4 Only eight of the cases in this study did not have a preceding hospital contact. The MRSA E1 strain has been shown to resemble, by molecular typing, some internationally spread MRSA clones, including the UK EMRSA-3, Paediatric and New York clones (Salmenlinna et al., unpublished). This indicates that MRSA E1 possessed a significant risk for becoming endemic. Between 1992 and 1997, more than 10 cases were reported
Control of MRSA outbreak involving several hospitals
for two other strains of MRSA. One was nontypeable by phage typing and was detected in 36 cases, and the other resembled the most prevalent MRSA strain in the UK, EMRSA-16, and created a minor outbreak at UCH. The index case was transferred from a Turkish hospital in 1995 and the strain spread to 24 patients. EMRSA-16 strain could not, however, generate a major outbreak. It is not possible to give the exact number of clinical infections caused by MRSA E1 during the epidemic. Detailed clinical information is only available for patients admitted to the isolation ward at Hospital C and nine additional clinical infections at other municipal hospitals. One may assume that most cases that were not admitted to the isolation ward did not have a clinical infection caused by MRSA E1. Thus, a minimum estimate of 17% for prevalence of clinical infections in this epidemic can be made. Positive MRSA screening results of staff coincided with circumstances in which there was a high number of MRSA-colonized and -infected cases, i.e. as the epidemic was detected in hospitals A and B. There was a total of eight MRSA E1 carriers detected among the staff. None of the eight staff members developed a clinical infection caused by MRSA E1. The colonization of MRSA seemed to be promptly terminated after treatment with topical mupirocin. However, the staff members were not rescreened for a possible recurrence of MRSA. It is impossible to state the minimum level of action that would have controlled this epidemic. However, the alleviation of both isolation and barrier nursing coincided with a small outbreak of MRSA E1 at Hospital C in 1995. Cohen et al. described control of MRSA in their institution using contact isolation, surveillance cultures and universal precautions.8 They used contact isolation measures recommended by the Centers for Disease Control (CDC) in 1983, which included a private room or cohorting of the cases, and the use of masks, gloves and gowns at all contacts when nursing the cases. During the epidemic described here, the instructions about the use of masks, gloves and gowns were changed in 1997 to be quite similar to the CDC 1983 guidelines. This change in 1997 did not result in an increase of MRSA E1 cases. The measures to control the epidemic included a large number of screening samples and costly isolation of cases and contacts. Cost-effectiveness of these measures has been proven in a neonatal intensive care unit,11 but assessment of the costeffectiveness of containment of a large-scale epidemic remains to be executed. As the municipal hospitals had a joint administration, the interest to limit the epidemic was
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uniform, and the necessary actions could be executed comprehensively and without delay. The organization of the IC team was small enough to work efficiently. It also had the requisite power to act within the whole organization and it received timely information on the new cases. Furthermore, we think that the impact of the co-ordinating activity of the IC nurses was significant in bringing the epidemic under control. The hospitals in Helsinki may have experienced a spread of MRSA similar to that in Europe and North America in recent years 12 – 14 if the administration had refrained from active measures when the epidemic became evident. We also believe that the actions taken prevented MRSA E1 from becoming endemic in the long-term care facilities, which received plenty of patients from epidemic-affected hospitals. This epidemic prompted the creation of national MRSA guidelines. These were instituted in 1995 and are now implemented by hospitals in the Helsinki region. In the Helsinki region, only limited outbreaks of MRSA have occurred and all have been controlled. Since 1997, no outbreaks have been caused by MRSA E1. Outside the Helsinki region, there has been a steady rise in the number of community-acquired MRSA cases and MRSA cases in long-term care facilities4 that constitute a continuous threat of MRSA for hospitals.
Acknowledgements The authors thank Pekka Holmstro ¨m for creating the database of MRSA cases treated in Hospital C, Pa ¨ivi Suomela for collecting the data, and the staff at the epidemic-affected hospitals and the Helsinki region laboratories who took care of the patients. We are also grateful to Saara Salmenlinna, Elina Siren and Ritva Scotford for typing of MRSA strains.
References 1. Salmenlinna S, Lyytikainen O, Kotilainen P, Scotford R, Siren E, Vuopio-Varkila J. Molecular epidemiology of methicillinresistant Staphylococcus aureus in Finland. Eur J Clin Microbiol Infect Dis 2000;19:101—107. 2. Kotilainen P, Routamaa M, Peltonen R, et al. Elimination of epidemic methicillin-resistant Staphylococcus aureus from a university hospital and district institutions, Finland. Emerg Infect Dis 2003;9:169—175. 3. Kotilainen P, Routamaa M, Peltonen R, et al. Eradication of methicillin-resistant Staphylococcus aureus from a health center ward and associated nursing home. Arch Intern Med 2001;161:859—863. 4. Salmenlinna S, Lyytika ¨inen O, Vuopio-Varkila J. Community
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5.
6.
7.
8.
9.
acquired methicillin resistant Staphylococcus aureus, Finland. Emerg Infect Dis 2002;8:602—607. Vandenbroucke-Grauls CM, Frenay HM, van Klingeren B, Savelkoul TF, Verhoef J. Control of epidemic methicillinresistant Staphylococcus aureus in a Dutch university hospital. Eur J Clin Microbiol Infect Dis 1991;10:6—11. Seeberg S, Larsson L, Welinder-Olsson C, et al. How an outbreak of MRSA in Gothenburg was eliminated by strict hygienic routines and massive control-culture program. Lakartidningen 2002;99:3198—3204. [In Swedish]. Coello R, Jimenez J, Garcia M, et al. Prospective study of infection, colonization and carriage of methicillin-resistant Staphylococcus aureus in an outbreak affecting 990 patients. Eur J Clin Microbiol Infect Dis 1994;13:74—81. Cohen SH, Morita MM, Bradford M. A seven-year experience with methicillin-resistant Staphylococcus aureus. Am J Med 1991;91:233S—237S. Deplano A, Witte W, van Leeuwen WJ, Brun Y, Struelens MJ. Clonal dissemination of epidemic methicillin-resistant Staphylococcus aureus in Belgium and neighboring countries. Clin Microbiol Infect 2000;6:239—245.
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10. Vicca AF. Nursing staff workload as a determinant of methicillin-resistant Staphylococcus aureus spread in an adult intensive therapy unit. J Hosp Infect 1999;43: 109—113. 11. Karchmer TB, Durbin LJ, Simonton BM, Farr BM. Costeffectiveness of active surveillance cultures and contact/ droplet precautions for control of methicillin-resistant Staphylococcus aureus. J Hosp Infect 2002;51:126—132. 12. Morgan M, Salmon R, Evans-Williams D, Hosein I, Looker DN. Resistance to methicillin in isolates of Staphylococcus aureus from blood and cerebrospinal fluid in Wales, 1993—1997. J Antimicrob Chemother 1999;44: 541—544. 13. Simor AE, Ofner-Agostini M, Bryce E, et al. Laboratory characterization of methicillin-resistant Staphylococcus aureus in Canadian hospitals: results of 5 years of National Surveillance, 1995—1999. J Infect Dis 2002;186: 652—660. 14. Ayliffe GA. The progressive intercontinental spread of methicillin-resistant Staphylococcus aureus. Clin Infect Dis 1997;24:S74—S79.
www.elsevierhealth.com/journals/jhin
Control of methicillin-resistant Staphylococcus aureus outbreak involving several hospitals S. Pastilaa,*, K.T. Sammalkorpib, J. Vuopio-Varkilac,d, S. Kontiainend, M.A. Ristolab a
¨me Central Hospital, 13530 Ha ¨meenlinna, Finland Kanta-Ha Division of Infectious Diseases, Department of Medicine, Helsinki University Central Hospital, Helsinki, Finland c Department of Microbiology, National Public Health Institute, Helsinki, Finland d HUCH Laboratory Diagnostics, Helsinki University Central Hospital, Helsinki, Finland b
Received 14 March 2004; accepted 24 May 2004
KEYWORDS Epidemiology; Infection control; MRSA; Nosocomial infection; Outbreaks
Summary This population-based, retrospective, cohort study describes a large methicillin-resistant Staphylococcus aureus (MRSA) epidemic caused by one strain (E1) in the greater Helsinki region. The epidemic comprised 210 cases at several hospitals, but was finally controlled. The study period ranged from June 1991 to December 2000. The epidemic peaked in 1993 – 1995 with 143 cases (68% of total cases). From August 1993, all MRSA-positive cases at the eight municipal hospitals were isolated and barrier nursed. Contacts were cohorted and screened for MRSA colonization. Decolonization treatment was administered to some chronic carriers. MRSA cases and contacts were identified in the joint patient register of the municipal hospitals from August 1993. The annual incidence of MRSA E1 in Helsinki City area per 100 000 inhabitants rose from 0.2 in 1991 to 13.6 in 1994. It decreased from 1995, reaching 0.7 per 100 000 in 2000. A jointly agreed policy on MRSA and timely co-operation between all units were essential for control of this epidemic. Q 2004 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved.
Introduction Before the 1990s, strains of methicillin-resistant Staphylococcus aureus (MRSA) were rare and no MRSA epidemics had been reported in Finland. Between 1981 and 1991, the annual number of *Corresponding author. Tel.: þ 358-9-58011; fax: þ 358-95801204. E-mail address: [email protected]
reported sporadic MRSA cases in Finland varied from 95 to 164.1 Since 1992, MRSA strains have been typed systematically, and data on the characteristics and epidemiology of MRSA strains have been collected. Since 1995, MRSA has been notifiable in Finland and the information on MRSA cases is available in the National Infectious Disease Register at the National Public Health Institute. The first published MRSA epidemic in Finland broke out at Turku University Central Hospital in 1991 – 1992.2,3
0195-6701/$ - see front matter Q 2004 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2004.06.024
Control of MRSA outbreak involving several hospitals
The first epidemic MRSA strain in Helsinki began to spread approximately concurrently with the epidemic in Turku. However, the epidemic in Helsinki was only identified in 1993. This article will describe the course of the epidemic and the measures that were undertaken to control the first MRSA epidemic in Helsinki.
Methods Design and setting This was a population-based, retrospective, cohort study, and the study period was from June 1991 to December 2000. All patients at the municipal hospitals (eight secondary care hospitals) and at University Central Hospital (UCH) during the study period were included. The cases were patients who were either infected or colonized with the epidemic MRSA strain E1. The cases were identified by their unique national social security number, which was also used for identification in the joint patient register of the municipal healthcare authority. Each case was only counted once. This paper also describes the MRSA-E1-positive cultures among staff members, but they were not included as cases in this study. In the 1990s, the hospital facilities in Helsinki City consisted of UCH and eight municipal hospitals (Hospitals A – H) that provided secondary care for Helsinki City. Three of the eight municipal hospitals had surgical services and one had extensive facilities for isolation. Hospitals A and G had emergency rooms and wards, and Hospital A had an intermediate care unit (a ward providing intermediate monitoring, between intensive care unit and ward level). The majority of the secondary care hospitals had both acute and long-term care wards. Patients were frequently transported between and within tertiary care, secondary care and long-term wards. UCH provided tertiary care for the greater Helsinki region. Between 1991 and 2000, the population of Helsinki increased from 497 542 to 555 474, and that of the greater Helsinki region increased from 1 248 072 to 1 379 712 (according to official statistics from Statistics Finland). An infectious diseases specialist, who acted as the co-ordinator, collected data on MRSA E1 from 1993 to 1996, as entailed in the Finnish legislation for communicable diseases. A database on the cases admitted to Hospital C from 1993 was set up in 1996. Approval for the database was obtained from the ethics committee of the municipal health
181
authority in Helsinki and from the Finnish Ministry of Social Affairs and Health. Data on MRSA cases since 1995 were available in the National Infectious Disease Register at the National Public Health Institute. The information on MRSA cases from 1992 to 1994 was obtained from the Laboratory of Hospital Bacteriology at the National Public Health Institute, which at that time was collecting and typing all suspected MRSA cases in Finland. The three MRSA E1 cases from before August 1992 were detected retrospectively in laboratory files.
Microbiological methods Microbiological samples were processed at two microbiology laboratories with similar analytical procedures. Up to 1994, MRSA strains were detected through standard bacterial culture and resistance testing. From August 1994, enrichment (broth tubes) and selective cultures (mannitol-salt agar plates with oxacillin) were used routinely for detection. These methods were used for all requested MRSA cultures and as a supplement to all ‘pus’ cultures (including wound sampling and clinical puncture or drainage) from hospitals involved in the epidemic. A preliminary positive result for MRSA was defined as growth of typical colonies on selective culture plates and positive Gram stain, catalase and latex agglutination test results. Isolated MRSA strains were verified and typed at the Laboratory of Hospital Bacteriology at the National Public Health Institute. Microbiological methods and the characteristics of MRSA E1 have been described previously.1,4
Organization of the MRSA control team in the municipal hospitals Before August 1993, there was no uniform MRSA policy at the municipal hospitals in Helsinki. As the extent of the epidemic became known, a common strategy for MRSA was developed. A consultant in infectious diseases was appointed by the head of the municipal hospitals as a co-ordinator for the epidemic-related measures in all of the municipal hospitals. Part-time infection control (IC) nurses in the municipal hospitals were the co-ordinator’s primary contacts, and they worked in close cooperation with the physicians of the wards affected by the epidemic. A senior consultant in the microbiological laboratory notified the co-ordinator, the physician in charge of the ward, and the IC nurse by telephone about all new positive MRSA isolations after a preliminary identification. The coordinator had meetings with the IC nurses and
182
S. Pastila et al.
infectious diseases consultants to guarantee the uniformity of measures in all units.
Clinical infections and decontamination treatment
MRSA sampling procedures
Clinical infections due to MRSA E1 were treated with antimicrobial agents according to resistance testing. Systemic decolonization treatment was only administered to a few selected cases. Nasal MRSA carriage of staff was treated with nasal mupirocin, and absence from work was requested until a negative follow-up sample was obtained.
In August 1993, sampling of MRSA cases and contacts (i.e. roommates of the cases) was started. By the end of 1993, screening samples were only taken from the nares, skin lesions, drains and other sites that were previously positive. During the first three months of the epidemic, more extensive sampling was performed, including throat, groin and armpits. Staff members were sampled once from the nares and potential skin lesions. Hospital staff were only screened on three occasions during the epidemic and no environmental MRSA samples were taken.
Measures to control the epidemic Cohorting, isolation, barrier nursing and screening From August 1993, all MRSA-positive cases identified at the municipal hospitals were cohorted on an isolation ward at Hospital C. The MRSA cases were isolated in separate rooms from other patients, and most of the rooms had an anteroom. The cases were barrier nursed until discharge or until three successive negative MRSA cultures were obtained. From 1993 to 1997, barrier nursing included the use of gloves, a surgical mask and a gown. At the beginning of 1995, the isolation practice in Hospital C was disrupted for two months and the barrier nursing was temporarily reduced to the use of gloves and alcohol hand rub. The use of a mask in barrier nursing was stopped in 1997. Upon subsequent admissions, all cases were isolated and screened for MRSA. This procedure was discontinued if MRSA cultures had been negative for 12 months. Contacts were cohorted, barrier nursed and screened for MRSA colonization twice with a one-week interval. If contacts had been discharged, screening was performed upon subsequent admission. MRSA screening was also performed before any patient was transferred to another hospital from a ward affected by the epidemic. Fortnightly screening of chronic wounds was carried out on the epidemic-affected wards at Hospital B from November to December 1994. At UCH, MRSA cases were isolated and barrier nursed. Nine cases of MRSA E1 were transferred to Hospital C for isolation.
Education of staff and recognition of cases The importance of hand hygiene in patient care was emphasized vigorously in all the municipal hospitals. Lectures was given and practical education on hand hygiene was arranged at all the epidemicaffected hospitals. From 1993, all MRSA-positive cases and their contacts were specifically indicated in the joint patient register of the municipal hospitals, which enabled rapid identification of MRSA carriers and contacts at the municipal hospitals and in primary healthcare facilities.
Results Identification of the epidemic Between August 1992 and June 1993, four MRSA E1 cases were barrier nursed but not isolated on the surgical index ward at Hospital A. No screening of contacts took place. Five additional cases of MRSA that were detected during that period were later typed as E1. All these cases had a recent admission to the surgical index ward at Hospital A. The index ward at Hospital A was closed due to administrative reasons for eight weeks in June 1993, and the patients were transferred to other surgical wards at Hospital A. In August 1993, five cases of MRSA E1 were detected on two of the surgical wards that had received patients from the index ward. At this point, the epidemic was identified and control measures were introduced.
Outbreak at Hospital A The surgical ward at Hospital A, which appeared to have the majority of recent MRSA E1 cases in August 1993, was closed for new admissions for seven days and all patients were screened for MRSA colonization. Screening of all patients was arranged on the other surgical ward with two cases of MRSA E1 in August 1993, but this ward remained open for new admissions. Due to abundant patient traffic
Control of MRSA outbreak involving several hospitals
between the intermediate care unit and surgical wards of Hospital A, all patients in the intermediate care unit were screened for MRSA colonization. The staff of three surgical wards, the intermediate care unit, the operating theatre, the emergency room, and the surgical outpatient clinic of Hospital A were also screened. By the end of 1993, there were eight more cases of MRSA E1 detected with a preceding admission to these two wards. Two cases of MRSA E1 were identified in March 1994 in the intermediate care unit and nine cases were identified between October and December 1994 in the surgical index ward. There were six cases of MRSA E1 related to Hospital A during 1995: five of these had been admitted to one of the two surgical wards which had the majority of cases in August 1993. Since 1995, only two MRSA E1 cases have been detected in Hospital A (Table I and Figure 1).
Outbreak at Hospital B The epidemic spread to Hospital B in March 1994. The first case at Hospital B had a clear connection with Hospital A. In August 1994, two clinical samples from one ward grew MRSA E1. A screening at that ward disclosed nine new cases. On two other wards at Hospital B, four clinical samples were positive for MRSA E1 in September 1994. Screening on all the affected wards during September and October 1994 yielded 19 cases among patients. Screening of chronic wounds was carried out on all wards at Hospital B during November and December 1994; this screening yielded four MRSA E1 cases. In 1997, there was another outbreak of MRSA E1 at Hospital B without any clear connection to the earlier cases. Ten of the 15 cases were due to secondary spread. The outbreak subsided in two months with the same interventions as in 1994 (Table I and Figure 1).
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Figure 1 Annual incidence of new MRSA E1 cases at municipal hospitals in relation to the population of Helsinki from 1991 to 2000. Solid bars, Hospital A; hatched bars, Hospital B; open bars, Hospital D; solid circles, incidence per 100 000 inhabitants.
Cases at other hospitals and in primary care At Hospital C, there was a cluster of five MRSA cases in 1995 that coincided with the two months of discontinuation of the isolation practices and removal of the barrier nursing. At Hospital D, there were 13 sporadic cases of MRSA E1 between 1993 and 1996, without an evident connection to the other hospitals, and eight secondary cases among contacts (Table I and Figure 1). The measures for containment of the epidemic were similar to those at the other municipal hospitals.
Description of cases The median age of the cases was 76 years (range 25 – 102 years). One hundred and sixteen (55%) of the MRSA E1 cases were male. A considerable proportion of MRSA E1 cases throughout the course of the epidemic were only colonized with MRSA. For example, in Hospital B during the autumn of 1994,
Table I MRSA E1—annual number of new cases 1991–2000 Year Hospital A Hospital B Hospital C Hospital D Hospital E Hospital F Hospital G Hospital H MH total PHC UCH Total
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
Total
1 0 0 0 0 0 0 0 1 0 0 1
4 0 0 0 0 0 0 0 4 1 0 5
17 0 0 1 0 0 0 0 18 0 3 21
11 38 1 5 0 7 1 0 63 1 12 76
6 2 5 14 1 4 2 0 34 2 10 46
1 3 0 1 1 0 0 0 6 0 7 13
0 15 0 0 0 0 0 0 15 3 4 22
0 0 0 0 0 0 0 0 0 1 15 16
1 1 0 0 0 0 0 0 2 0 4 6
0 2 0 0 0 0 0 0 2 0 2 4
41 61 6 21 2 11 3 0 145 8 57 210
MH, municipal hospitals; PHC, primary healthcare facilities; UCH, University Central Hospital.
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68% of MRSA-E1-positive cultures were from screening samples. Among the 123 cases that were admitted to the isolation ward at Hospital C between 1993 and 1996, there were 28 (23%) cases with confirmed clinical infection by MRSA E1. Of the 28 cases with clinical MRSA E1 infection, three (11%) had bacteraemia, six (21%) had a surgical-site infection, and 14 (50%) had infection of a chronic pressure wound or another skin lesion. The remaining five cases had MRSA E1 infection of the outer ear, conjunctiva, gastrointestinal tract (two cases) and respiratory tract. Nine additional clinical infections by MRSA E1 were detected at the other municipal hospitals during the study period. The majority (69%) of MRSA E1 cases were detected in secondary care, while 27% were detected at UCH and 4% were detected in primary healthcare facilities (Table I). Of the 57 cases detected at UCH, 32 were residents of Helsinki City. The annual incidence of MRSA E1 between 1992 and 2000 in Helsinki is shown in Figure 1.
MRSA E1 among staff At Hospital A, four staff members were detected as being carriers of MRSA E1. At Hospital B, there were three nasal carriers among the staff, and the screening at Hospital C revealed only one positive culture and it was therefore terminated. In total, there were eight nasal carriers detected among the staff. All had negative nasal swabs after local mupirocin. No follow-up sampling was arranged.
Screening samples By the end of 1995 (i.e. in 29 months), 17 198 screening samples had been taken at the municipal hospitals. Of these, 1010 (5.9%) were positive.
Discussion This population-based, retrospective, cohort study describes a large MRSA epidemic caused by one strain (E1) in the greater Helsinki region. Although the epidemic involved 210 cases at several hospitals, it was finally controlled. According to the Laboratory of Hospital Bacteriology at the National Public Health Institute and the National Infectious Disease Registry, between 1992 and 2000 there were 1522 new MRSA cases in Finland, of which 456 were in Helsinki City. Thus, MRSA E1 constituted 40% of all MRSA cases in Helsinki City during the study period. There were 60
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MRSA E1 cases in other parts of Finland (27% of all MRSA cases) between 1992 and 1996. Identification and typing of suspected MRSA cases in the Laboratory of Hospital Bacteriology at the National Public Health Institute between 1992 and 1994 was non-compulsory, which could have led to the under-reporting of cases. However, the two major clinical microbiological laboratories serving the hospitals included in this study had a close and consistent collaboration with the Laboratory of Hospital Bacteriology, and we believe that there was practically no under-reporting of MRSA in the Helsinki region. We believe that isolation and barrier nursing of cases, and vigorous screening of contacts led to successful control of this MRSA E1 outbreak. Our experience supports the view obtained from smaller MRSA outbreaks that these measures are important to control the spread of MRSA.2,5,6 Data on other major MRSA epidemics7,8 also support the validity of our measures. The ‘wait-and-see’ practice between 1991 and 1993 was followed by an extensive epidemic with 122 new cases and spread to four new hospitals between 1994 and 1995 (Table I). After implementing the control measures in the autumn of 1993, the annual number of new cases increased until the following year and then declined sharply (Figure 1). The closure of wards during staff’s annual holidays and transfer of patients to other wards most likely contributed to the spread of the epidemic in 1993 in a similar manner as described earlier.9 It is also likely that the increase in the workload of nursing staff played a role in the spread of MRSA.10 Natural decline of the epidemic in the mid 1990s is unlikely. The number of new cases at Hospital A in 1993 did not decline until the control measures were implemented, and a smaller outbreak took place in 1994 at Hospital A despite these measures. Additionally, MRSA E1 recurred in 1997 at Hospital B after two years with only sporadic cases. MRSA E1 seemed to spread easily in the hospital setting; all 127 cases detected in the municipal hospitals between August 1992 and December 1996 had a preceding admission to an epidemic-affected unit. As described earlier, 98% of the MRSA E1 cases between 1997 and 1999 also had a preceding hospital contact.4 Only eight of the cases in this study did not have a preceding hospital contact. The MRSA E1 strain has been shown to resemble, by molecular typing, some internationally spread MRSA clones, including the UK EMRSA-3, Paediatric and New York clones (Salmenlinna et al., unpublished). This indicates that MRSA E1 possessed a significant risk for becoming endemic. Between 1992 and 1997, more than 10 cases were reported
Control of MRSA outbreak involving several hospitals
for two other strains of MRSA. One was nontypeable by phage typing and was detected in 36 cases, and the other resembled the most prevalent MRSA strain in the UK, EMRSA-16, and created a minor outbreak at UCH. The index case was transferred from a Turkish hospital in 1995 and the strain spread to 24 patients. EMRSA-16 strain could not, however, generate a major outbreak. It is not possible to give the exact number of clinical infections caused by MRSA E1 during the epidemic. Detailed clinical information is only available for patients admitted to the isolation ward at Hospital C and nine additional clinical infections at other municipal hospitals. One may assume that most cases that were not admitted to the isolation ward did not have a clinical infection caused by MRSA E1. Thus, a minimum estimate of 17% for prevalence of clinical infections in this epidemic can be made. Positive MRSA screening results of staff coincided with circumstances in which there was a high number of MRSA-colonized and -infected cases, i.e. as the epidemic was detected in hospitals A and B. There was a total of eight MRSA E1 carriers detected among the staff. None of the eight staff members developed a clinical infection caused by MRSA E1. The colonization of MRSA seemed to be promptly terminated after treatment with topical mupirocin. However, the staff members were not rescreened for a possible recurrence of MRSA. It is impossible to state the minimum level of action that would have controlled this epidemic. However, the alleviation of both isolation and barrier nursing coincided with a small outbreak of MRSA E1 at Hospital C in 1995. Cohen et al. described control of MRSA in their institution using contact isolation, surveillance cultures and universal precautions.8 They used contact isolation measures recommended by the Centers for Disease Control (CDC) in 1983, which included a private room or cohorting of the cases, and the use of masks, gloves and gowns at all contacts when nursing the cases. During the epidemic described here, the instructions about the use of masks, gloves and gowns were changed in 1997 to be quite similar to the CDC 1983 guidelines. This change in 1997 did not result in an increase of MRSA E1 cases. The measures to control the epidemic included a large number of screening samples and costly isolation of cases and contacts. Cost-effectiveness of these measures has been proven in a neonatal intensive care unit,11 but assessment of the costeffectiveness of containment of a large-scale epidemic remains to be executed. As the municipal hospitals had a joint administration, the interest to limit the epidemic was
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uniform, and the necessary actions could be executed comprehensively and without delay. The organization of the IC team was small enough to work efficiently. It also had the requisite power to act within the whole organization and it received timely information on the new cases. Furthermore, we think that the impact of the co-ordinating activity of the IC nurses was significant in bringing the epidemic under control. The hospitals in Helsinki may have experienced a spread of MRSA similar to that in Europe and North America in recent years 12 – 14 if the administration had refrained from active measures when the epidemic became evident. We also believe that the actions taken prevented MRSA E1 from becoming endemic in the long-term care facilities, which received plenty of patients from epidemic-affected hospitals. This epidemic prompted the creation of national MRSA guidelines. These were instituted in 1995 and are now implemented by hospitals in the Helsinki region. In the Helsinki region, only limited outbreaks of MRSA have occurred and all have been controlled. Since 1997, no outbreaks have been caused by MRSA E1. Outside the Helsinki region, there has been a steady rise in the number of community-acquired MRSA cases and MRSA cases in long-term care facilities4 that constitute a continuous threat of MRSA for hospitals.
Acknowledgements The authors thank Pekka Holmstro ¨m for creating the database of MRSA cases treated in Hospital C, Pa ¨ivi Suomela for collecting the data, and the staff at the epidemic-affected hospitals and the Helsinki region laboratories who took care of the patients. We are also grateful to Saara Salmenlinna, Elina Siren and Ritva Scotford for typing of MRSA strains.
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