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Prolonged delay for controlling KPC-2–producing Klebsiella pneumoniae outbreak: The role of clinical management
American Journal of Infection Control xxx (2015) 1-6
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Major article
Prolonged delay for controlling KPC-2eproducing Klebsiella pneumoniae outbreak: The role of clinical management T. Delory MD, MPH a, E. Seringe MD a, *, G. Antoniotti MD b, I. Novakova RN a, C. Goulenok MD b, I. Paysant RN b, S. Boyer PharmD b, c, A. Carbonne MD d, T. Naas PhD e, f, g, P. Astagneau MD, PhD a, h a
Regional Centre for Nosocomial Infection Control, CClin Nord, Paris, France Groupe Générale de Santé, Paris, France Laboratoire Bactériologie Novescia, Paris, France d Office of Quality and Safety in Care, Direction Générale de l’Offre de Soins-Bureau PF2-Ministère de la Santé, des affaires sociales et du droit des femmes, Paris, France e Department of Bacteriology, APHP, Laboratoire de Bactériologie-Virologie, Hôpital de Bicêtre, Le Kremlin Bicêtre, France f Centre National de Référence de la résistance aux antibiotiques, Le Kremlin Bicêtre, France g EA7361, Faculté de Médecine, Université Paris Sud, France h Department of Epidemiology, Ecole des Hautes Etudes en Santé Publique/Universités Sorbonne Paris Cité, Paris, France b c
Key Words: Carbapenem-producing enterobacteriaceae Infection control Outbreak Root causes analysis
Background: Carbapenemase-producing Enterobacteriaceae (CPE) are becoming of immediate concern for infection control policies. Prompt detection of CPE on health care setting admission is crucial to halt the spread of an outbreak. We report a cluster of 13 Klebsiella pneumoniae carbapenemase (KPC)-2e producing K pneumoniae cases in a tertiary care hospital.The objective of this study was to identify contributing factors originating the outbreak. Methods: An outbreak investigation was conducted using descriptive epidemiology, observation of health care practices, and interviews of management staff. A root cause analysis was performed to identify patent and latent failures of infection control measures using the association of litigation and risk management method. Results: The main patent failure was the delay in identifying KPC-2eproducing K pneumoniae carriers. Contributing factors were work and environmental factors: understaffing, lack of predefined protocols, staff members’ characteristics, and underlying patients’ characteristics. Latent failures were as follows: no promotion of the national guidelines for prevention of CPE transmission, no clear procedure for the management of patients hospitalized abroad, no clear initiative for promoting a culture of quality in the hospital, biologic activity recently outsourced to a private laboratory, and poor communication among hospital members. Conclusion: Clinical management should be better promoted to control hospital outbreaks and should include team work and safety culture. Copyright Ó 2015 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
For the last 5 years, carbapenemase-producing Enterobacteriaceae (CPE) have emerged as an important group of extremely drug-resistant (XDR) health careeassociated pathogens worldwide and are now recognized to be associated with substantial morbidity and mortality.1-5 To date, most of the outbreaks observed in low- and mid-incidence European countries are related to the importation of cases from a foreign country.1,2,6 Delaying the * Address correspondence to Elise Seringe, MD, CClin Nord, 8 rue Maria Helena Vieira da Silva, 75014 Paris, France. E-mail address: [email protected] (E. Seringe). Conflicts of interest: None to report.
detection of patients at risk for CPE carriage and implementation of reinforced infection control measures are factors that facilitate outbreaks.6-8 In addition to the implementation of antimicrobial stewardship programs, the reinforcement of prompt screening and isolation of carriers are the major keys to control CPE spread. In case of a CPE-related outbreak, a heavy reorganization of care, including cohorting of CPE carriers with dedicated health care personnel and identification of contact patients, seems to be effective.3,6,9 In December 2010, the French health authority issued national recommendations for the screening and presumptive isolation of patients transferred from hospitals abroad.10,11 On July 15, 2011, a nonteaching tertiary hospital reported a cluster of Klebsiella
0196-6553/$36.00 - Copyright Ó 2015 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.2015.05.021
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Fig 1. Epidemic curve of the outbreak and implementation of infection control measures. The epidemic curve of 13 patients tested positive for the same clone of Klebsiella pneumoniae carbapenemase-2eproducing K pneumoniae in the ICU and cardiology department. A bundle of interventions was fully implemented on July, 19, 2011. D-1, D-3, D-30, and D-40 are the key points of investigations-intervention start and are figured by arrows on the baseline time frame. The hatching portion bar represents the period without systematic weekly screening for MDR carriage in the ICU. The black points represent the screening of MDR carriage (rectal and throat samples). The light gray box represents ICU cases. The dark gray box represents cardiology cases. The case number 8 was first hospitalized in the ICU and then in cardiology. D-1, day 1; D-3, day 3; D-30, day 30; D-40, day 40; ICU, intensive care unit; MDR, multidrug resistant.
pneumoniae carbapenemase-2 (KPC-2)eproducing K pneumoniae to the regional center for health careeassociated infection control in Paris. The outbreak’s index case was a patient repatriated from a Greek hospital 1 month before. An epidemiologic investigation was then started to estimate the outbreak’s magnitude, identify potential risk factors for a larger spread, and help to implement appropriate control measure. To understand the systemic factors of nonadherence to standard recommendations, which could explain the spread of the outbreak, we conducted a root cause analysis. METHODS The study was carried out in a 320-bed private nonteaching tertiary hospital located in the Paris area of France. From July-August 2011, an expert team from the regional center for infection control conducted a descriptive epidemiologic study of the outbreak. In parallel, they began an observation of health care practices and staff management to conduct a root cause analysis. Patient data were collected, including clinical characteristics, hospitalization and hospital discharge dates, dates of rectal swabs, microbiologic results, and status for CPE colonization or infection. Standard criteria were used to define cases and contact patients. A case was defined as a patient infected or colonized by the same clone of KPC-2eproducing K pneumoniae confirmed by the Antimicrobial Resistance National Reference Center (NRC; Le Kremlin Bicêtre, France). The diagnosis of clinical infection or colonization was made by the physician in charge of the patient. A contact patient was defined as a patient hospitalized in the same ward and cared for by the same personnel as the case during the same period. An exhaustive contact patients screening was performed among 13 French administrative regions. All contact patients were traced by phone recall or mail. Data for auditing practices and root cause analysis were collected through interviews of the health care and management personnel using a standardized report form (Appendix 1). Staff were asked about their workload levels, fatigue, knowledge and training policy, ability or experience, supervision or instruction by the manager, stressful environment conditions, rapid change within an organization, performance of communication, planning and scheduling, and maintenance of equipment and buildings. A systemic analysis was then performed using the association of litigation and risk management method (ALARM) described by Vincent et al.12-14 This method consists of the identification of patent and latent failures. Patent failures12 were considered in case of unsafe acts or omissions, which could have had immediate adverse consequences. Latent failures12 were the conditions in
which errors occur in the clinical wards (contributing factors) and the factors related to organization-management at the institutional level (systemic factors). Screening of cases and contact patients for carbapenemase typing or monoclonal characterization was performed by the NRC, according to standard methods.15-17 Microbiologic techniques consisted of testing antibiotic susceptibility by disk diffusion on Mueller-Hinton agar according to the standards of the Antibiogram Committee of the French Microbiology Society.18 Minimum inhibitory concentrations were determined using Etest strips (BioMérieux, Marcy-l’Étoile, France) and were interpreted as previously described. All carbapenem-resistant strains were sent to the NRC for confirmation. Carbapenemase production was detected using the Hodge test and synergy test between carbapenems and ethylenediaminetetraacetic acid (for class B metallo b-lactamases) or clavulanic acid (for class A b-lactamases).19 The genes encoding carbapenemases were identified by the NRC using polymerase chain reaction and sequencing of the amplified product.20 Genomic relatedness of the KPC-2eproducing K pneumoniae isolates was investigated by semiautomated repetitive polymerase chain reaction typing (DiversiLab; BioMérieux, Marcy-l’Étoile, France) as recommended by the manufacturer.21 RESULTS From July 7-August 30, 2011, in addition to the index case, 12 secondary health careeassociated cases of KPC-2eproducing K pneumoniae in 3 different health care facilities were identified, including 2 clusters of patient-to-patient transmission (Fig 1). None had CPE infection, and 5 deaths not attributable to CPE were observed. Two out of these 13 cases were identified after their transfer to other hospitals. Among the 282 contact patients identified, 149 returned home, 25 died, 32 remained hospitalized, and 76 were transferred to 29 other hospitals. Overall, 210 contact patients were screened (rectal sample) at least once and remained negative. The genetic relatedness is shown in Figure 2. The main patent failure was the delay in case identification. Two main reasons were involved in the delay in CPE carriers’ identification. The first was KPC-2eproducing K pneumoniae carried by the index case was at first characterized as a common Extended-Spectrum Beta-Lactamase (ESBL)-producing Klebiella pneumonia strain (3 days after the patient’s hospitalization). Although the index patient was screened immediately on admission for potentially carbapenemase-producing strains, as recommended by the French guidelines in case of repatriated patients,10 the resistance to
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3
direction, clinical staff members, and quality and safety department. According to the national guidelines,10,11 a bundle of infection control measures was implemented (40 days after index case admission). The bundle included systematic screening of the 25 ICU patients and new suspected cases on admission. Suspected cases and contact patients were cohorted in dedicated wards with dedicated staffs. Staff members received education and training in infection control, and a procedure for the enhancement of environmental and material surfaces’ cleaning was implemented (Table 1). No other secondary transmission occurred after the reinforcement of infection control measures. Since the outbreak was halted, the local infection control team has been provided with a part-time infection control practitioner and a full-time nurse. A local plan for the management of emerging pathogen carriers has been setup. Changes to the hospital teams’ characteristics before and after outbreak are listed in Table 1. DISCUSSION
Fig 2. Genetic relatedness of the KPC-2eproducing K pneumoniae isolates. Semiautomated repetitive polymerase chain reaction typing (DiversiLab; BioMérieux, Marcy-l’Étoile, France) of KPC-2-producingeK pneumoniae isolates is shown. Numbers 1-13 on the dendrogram correspond to the patient numbers, whereas 14 and 15 correspond to 2 nonrelated isolates. Number below the P indicate the number of patterns identified. All the KPC-2eproducing isolates belong to a single pattern. KPC-2, Klebsiella pneumoniae carbapenemase-2.
imipenem was not detected by the hospital laboratory. Second, weekly screening of intensive care unit (ICU) patients using rectal sampling for detection of multidrug-resistant organisms (MDRs) was disrupted during the 4 weeks after index case admission (day 1). The index case CPE carriage was identified by the NRC 30 days after admission to the ICU. At this time (day 30), 2 transmissions had already occurred and were established to be genetically related to the KPC-2eproducing K pneumoniae clone carried by the index case. As shown in Figure 3, factors which were determined as a trigger of patent failures were the following: (1) work and environmental factors (heavy workload in the ICU, summer period, index case hospitalization during a public holiday, delay in K pneumoniae carbapenemase typing method); (2) team factors (understaffed teams, major ICU reorganization before and during the outbreak period); (3) tasks factors (lack of predefined protocols to contain outbreaks); (4) individual characteristics (staff members’ lack of knowledge and misapplication of infection control measures and the national recommendations for CPE spread prevention); and (5) patient characteristics with heavy burden of disease (intensive and invasive cares, high incidence of nosocomial infection, high level of antibiotics consumption). Latent failures at the outbreak onset were related to organizational and management policies: (1) no promotion of the national guidelines for the prevention of XDR bacteria transmission existed in clinical wards; (2) no clear procedure existed for the management of patients hospitalized abroad11; (3) no clear initiative existed for promoting a culture of quality; and in the hospital, (4) biologic activities were recently outsourced to a private laboratory, and (5) there was a poor communication level between hospital
Our study showed that the reasons which explain ineffective control of such outbreaks must be analyzed beyond immediate observation of breaches in hygiene practices, the so-called patent failures. The root cause analysis using the ALARM is an effective, reproducible, and comprehensive approach to identifying deep causes related to institutional, organizational, and management factors.12-14 To our knowledge, the ALARM has not been routinely used in epidemiologic investigations of hospital outbreaks, regardless of the involved pathogens. In comparison with other root cause analysis methods, the ALARM has the advantage of exploring health care team factors, but it needs to collect timedependent items which could be missing because outbreak data are mostly collected retrospectively. In our study, the delay in case identification was the main contributing factor to the outbreak. This was partly because the local microbiology laboratory did not send the strain to the NRC; however, a low susceptibility to imipenem had been identified in a sample from a repatriated patient. However, the secondary cases were mainly because of breaches to infection control measures. They were assumed to be related to a chain of disorders or failures in terms of care organization, including the lack of safety culture promotion and a deficiency in collaborative relationships among hospital direction, clinical staff members, and the quality and safety department. Effective infection control measures for preventing secondary transmission were also delayed. This could be related to institutional factors, including the cost-saving policy with consequences in terms of understaffed teams at every level of both the clinical wards and the local infection control team. This was enhanced by the summer period with difficulties to temporarily replace health care workers on vacation. Before the KPC-2e producing K pneumoniae occurrence, the local infection control team was only composed of a part-time contract nurse. The local infection control practitioner had resigned from his position before the outbreak’s occurrence and had not been replaced at the outbreak’s onset. In addition, laboratory activities were recently outsourced to reduce hospital charges but resulted in a default of MDR-strain screening in the ICU and lack of feedback to ICU staff members when KPC-2eproducing K pneumoniae cases were suspected. We observed that the head of the ICU was absent when the outbreak occurred, which could be considered as a contributing factor to partly explain disorder in organization and management of care and as a risk factor of health careeassociated infections, as shown in a recent review.22 Positive and proactive leadership has
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Fig 3. Latent and patent failures related to the control of a KPC-2eproducing K pneumoniae outbreak using the association of litigation and risk management method. Patent failures were considered in case of unsafe acts or omissions, which could have immediate adverse consequences resulting in immediate observation of breaches in hygiene practices. Latent failures were the conditions in which errors occur in the clinical wards (contributing factors) and the factors related to organization-management at the institution level (systemic factors). CR-KP, Carbapenem-resistant klebsiella pneumonia; KPC-2, Klebsiella pneumoniae carbapenemase-2. Table 1 Characteristics of infection control measures and hospital teams before, during, and after the CR-KP outbreak Measures
Before
Infection control measures Diffusion of the national guidelines for the prevention of CPE transmission Local plan of action for containing XDR-strains outbreak Identification of CPE carriers Mispractices in standard infection control measures Isolation-cohorting wards Staff members’ education Improved protocol for the cleaning of environmental and material surfaces Technical assistance from the regional center to the infection control team Hospital teams ICU department Head of department Local infection control team Infection control practitioner None Nurse Part-time Premises -
During
After
þ
þ
þ
þ -
þ -
þ þ þ
þ þ
þ
None Part-time Part-time Full-time þ þ
CPE, carbapenemase-producing Enterobacteriaceae; CR-KP, Carbapenem-ResistantKlebsiella pneumonia; ICU, intensive care unit; XDR, extremely drug resistant.
already been reported to be associated with a reduced incidence in pneumonia and urinary tract infection.23 This relationship is usually mediated by staff experience and stability.23 In England, a national investigation by the Healthcare Commission had also described that inadequate team work could alter quality of care and
effectiveness to control hospital outbreaks.24 Understaffing nursing teams could also be related to increased rates of health caree associated infections, and several studies22,25,26 have demonstrated that an increasing nurse-patient ratio in the ICU was associated with a reduction in infection risks. Therefore, temporary nursing staff and team instability could be risk factors for health care infections and other adverse events.22 Finally, outbreak control was successfully achieved when a bundle of infection control measures was promptly implemented with the help of an external expert team. Multidisciplinary approaches, especially multifaceted interventions, have been demonstrated to be an effective way to reduce the rate of health careeassociated infection, especially in the ICU for ventilatorassociated pneumonia27 and methicillin-resistant Staphylococcus aureus infections.28 In our study, few infection control measures were assumed to be in place in the ICU before the implementation of the bundle of infection control measures. Indeed, the lack of MDR carriage screening a few weeks before the outbreak and little knowledge and awareness about measures for CPE prevention by the health care staff support this hypothesis. According to French recommendations, all admissions to the ICUs undergo active screening for MDR carriage upon admission29,30 but not weekly. However, most of the French ICUs, including the hospital in this study, have routinely implemented this screening. On the other hand, once the outbreak was identified, the infection control team was very prompt to react and was rapidly involved in the management improvement process. Besides, since this outbreak has occurred, the hospital has developed and used an effective program for the control of XDR-emerging pathogens. The effectiveness of the national guideline recommendations for CPE
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outbreak management10,11 gains to be supported by collaborative initiatives, such as auditing, root cause approach, and experience feedback to health care staff, as described.22,31 Education, training programs, and the promotion of a safety culture toward staff members; the allocation of substantial human resources to infection control teams, especially medical practitioners; and policies for systematic CPE screening in high-risk settings are warranted.
Acknowledgment We thank the Antimicrobial Resistance National Reference Center (France) for the identification of the genetic relatedness among Klebsiella pneumoniae carbapenemaseeproducing strains and the genetic relevance among cases.
References 1. Cantón R, Akóva M, Carmeli Y, Giske CG, Glupczynski Y, Gniadkowski M, et al. Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin Microbiol Infect 2012;18:413-31. 2. Vaux S, Carbonne A, Thiolet JM, Jarlier V, Coignard B, RAISIN and Expert Laboratories Groups. Emergence of carbapenemase-producing Enterobacteriaceae in France, 2004 to 2011. Euro Surveill 2011;16. 3. Munoz-Price LS, Poirel L, Bonomo RA, Schwaber MJ, Daikos GL, Cormican M, et al. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect Dis 2013;13:785-96. 4. Chiu SK, Wu TL, Chuang YC, Lin JC, Fung CP, Lu PL, et al. National surveillance study on carbapenem non-susceptible Klebsiella pneumoniae in Taiwan: the emergence and rapid dissemination of KPC-2 carbapenemase. PLoS One 2013; 8:e69428. 5. Falagas ME, Lourida P, Poulikakos P, Rafailidis PI, Tansarli GS. Antibiotic treatment of infections due to carbapenem-resistant Enterobacteriaceae: systematic evaluation of the available evidence. Antimicrobial Agents Chemother 2014;58:654-63. 6. Fournier S, Monteil C, Lepainteur M, Richard C, Brun-Buisson C, Jarlier V, et al. Long-term control of carbapenemase-producing Enterobacteriaceae at the scale of a large French multihospital institution: a nine-year experience, France, 2004 to 2012. Euro Surveill 2014;19. 7. Kochar S, Sheard T, Sharma R, Hui A, Tolentino E, Allen G, et al. Success of an infection control program to reduce the spread of carbapenemresistant Klebsiella pneumoniae. Infect Control Hosp Epidemiol 2009;30: 447-52. 8. Munoz-Price LS, De La Cuesta C, Adams S, Wyckoff M, Cleary T, McCurdy SP, et al. Successful eradication of a monoclonal strain of Klebsiella pneumoniae during a K. pneumoniae carbapenemase-producing K. pneumoniae outbreak in a surgical intensive care unit in Miami, Florida. Infect Control Hosp Epidemiol 2010;31:1074-7. 9. Guh AY, Limbago BM, Kallen AJ. Epidemiology and prevention of carbapenemresistant Enterobacteriaceae in the United States. Expert Rev Anti Infect Ther 2014;12:565-80. 10. Haut Conseil de la Santé publique. Commission spécialisée Sécurité des patients: infections nosocomiales et autres évènements indésirables liés aux soins et aux pratiques. Recommandations pour le dépistage du portage digestif des bactéries commensales multi-résistantes aux antibiotiques importées en France è l’occasion du rapatriement de patients en provenance de l’étranger et maîtrise de leur diffusion. 2010. Available from: http://www. hcsp.fr/docspdf/avisrapports/hcspr20100518_bmrimportees.pdf. Accessed June 12, 2015.
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11. Lepelletier D, Andremont A, Grandbastien B, National Working Group. Risk of highly resistant bacteria importation from repatriates and travelers hospitalized in foreign countries: about the French recommendations to limit their spread. J Travel Med 2011;18:344-51. 12. Vincent C, Taylor-Adams S, Stanhope N. Framework for analysing risk and safety in clinical medicine. BMJ 1998;316:1154-7. 13. Vincent C, Taylor-Adams S, Chapman EJ, Hewett D, Prior S, Strange P, et al. How to investigate and analyse clinical incidents: clinical risk unit and association of litigation and risk management protocol. BMJ 2000;320: 777-81. 14. Vincent C. Analysis of clinical incidents: a window on the system not a search for root causes. Qual Saf Health Care 2004;13:242-3. 15. Bratu S, Mooty M, Nichani S, Landman D, Gullans C, Pettinato B, et al. Emergence of KPC-possessing Klebsiella pneumoniae in Brooklyn, New York: epidemiology and recommendations for detection. Antimicrobial Agents Chemother 2005;49:3018-20. 16. Bratu S, Landman D, Alam M, Tolentino E, Quale J. Detection of KPC carbapenem-hydrolyzing enzymes in Enterobacter spp. from Brooklyn, New York. Antimicrobial Agents Chemother 2005;49:776-8. 17. Nordmann P, Gniadkowski M, Giske CG, Poirel L, Woodford N, Miriagou V, et al. Identification and screening of carbapenemase-producing Enterobacteriaceae. Clin Microbiol Infect 2012;18:432-8. 18. Société Française de Microbiologie (SFM). Antibiogram committee of the French Society for Microbiology. Recommendations 2011 [French]. Paris, France: SFM; 2011. 19. Picão RC, Andrade SS, Nicoletti AG, Campana EH, Moraes GC, Mendes RE, et al. Metallo-beta-lactamase detection: comparative evaluation of double-disk synergy versus combined disk tests for IMP-, GIM-, SIM-, SPM-, or VIM producing isolates. J Clin Microbiol 2008;46:2028-37. 20. Courvalin P, Leclercq R, Rice LB, editors. Antibiogram. Washington, DC: American Society for Microbiology Press; 2010. 21. Cuzon G, Naas T, Correa A, Quinn JP, Villegas MV, Nordmann P. Dissemination of the KPC-2 carbapenemase in non-Klebsiella pneumoniae enterobacterial isolates from Colombia. Int J Antimicrob Agents 2013;42:59-62. 22. Griffiths P, Renz A, Hughes J, Rafferty AM. Impact of organisation and management factors on infection control in hospitals: a scoping review. J Hosp Infect 2009;73:1-14. 23. Houser J. A model for evaluating the context of nursing care delivery. J Nurs Adm 2003;33:39-47. 24. Healthcare Commission. Learning from investigations. London, England: Commission for Healthcare Audit and Inspection; 2008. 25. Hugonnet S, Harbarth S, Sax H, Duncan RA, Pittet D. Nursing resources: a major determinant of nosocomial infection? Curr Opin Infect Dis 2004;17: 329-33. 26. Hugonnet S, Chevrolet JC, Pittet D. The effect of workload on infection risk in critically ill patients. Crit Care Med 2007;35:76-81. 27. Kaye J, Ashline V, Erickson D, Zeiler K, Gavigan D, Gannon L, et al. Critical care bug team: a multidisciplinary team approach to reducing ventilatorassociated pneumonia. Am J Infect Control 2000;28:197-201. 28. Salaripour M, McKernan P, Devlin R, Infection Prevention and Control Team. A multidisciplinary approach to reducing outbreaks and nosocomial MRSA in a university- affiliated hospital. Healthc Q 2006;9:54-60. 29. Société Française d’Hygiène Hospitalière. Recommandations pour la prévention de la transmission croisée: précautions complémentaires contact. Hygiènes 2009;17:81-137. 30. Haut Conseil de la Santé Publique. Commission spécialisée Sécurité des patients: infections nosocomiales et autres évènements indésirables liés aux soins et aux pratiques. Recommandations relatives aux mesures à mettre en oeuvre pour prévenir l’émergence des entérobactéries BLSE et lutter contre leur dissémination. 2010. Available from http://www.hcsp.fr/Explore.cgi/ Telecharger?NomFichier¼hcspr20100202_enterobactBLSE.pdf. Accessed June 12, 2015. 31. Jamtvedt G, Young JM, Kristoffersen DT, O’Brien MA, Oxman AD. Audit and feedback: effects on professional practice and health care outcomes. Cochrane Database Syst Rev; 2006:CD000259.
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APPENDIX 1. ASSOCIATION OF LITIGATION AND RISK MANAGEMENT APPROACH Investigation process 5. All investigations consist of a series of steps that should be followed, as a matter of routine, when an incident is investigated: 1. Ascertain that a serious clinical incident has occurred and ensure it is formally reported. Alternatively, identify an incident as being fruitful in terms of organizational learning. 2. Trigger the investigation procedure. Notify the senior members of staff who have been trained to carry out investigations. 3. Establish the circumstances as they initially appear and complete an initial summary, decide which part of the process of care requires investigating, prepare an outline chronology of events, and identify any obvious care management problems. 4. Structured interview of staff: Establish chronology of events.
6.
7. 8. 9.
Revisit sequence of events and ask questions about each care management problem identified at the initial stage. Use framework to ask supplementary questions about reasons for each care management problem. If new care management problems have emerged during interviews, add them to the initial list. Interview again if necessary. Collate interviews and assemble composite analysis under each care management problem identified. Identify both specific and, where appropriate, general contributory factors Compile report of events, listing causes of care management problems and recommendations to prevent recurrence. Submit report to senior clinicians and management according to local arrangements. Implement actions arising from report and monitor progress.
Reproduced from [How to investigate and analyse clinical incidents: clinical risk unit and association of litigation and risk management protocol, Vincent C, Taylor-Adams S, Chapman EJ, Hewett D, Prior S, Strange P, Tizzard A, 320, 777-781, 2000] with permission from BMJ Publishing Group Ltd.13
Type of factors
Example
Work and environment Workload Year period Team factors Verbal communication Written communication Supervision and seeking help Structure of team Task factors Standardization of care Task design Structure clarity Individual (staff members) Experience Knowledge Personality Skills Patient characteristics Severe disease Antibiotic consumption Health careeassociated infection Framework for root cause analysis. Reproduced from [Framework for analysing risk and safety in clinical medicine, Vincent C, Taylor-Adams S, Stanhope N, 316, 1154-1157, 1998] with permission from BMJ Publishing Group Ltd.12
Type of failure Management decision Organizational process Institutional context
Example
High workload Holiday No communication between professions Availability of records Responsiveness of senior staff Balance of senior and junior staff Availability of clear and efficient protocols
Junior versus senior staff Knowledge of available protocols
ICU patients High consumption of carbapenems High incidence of ESBL-E carriage
NOTE. Associated factors are conditions proving by latent failures in which unsafe acts occur. ESBL-E, Extended-Spectrum Beta-Lactamase Enterobacteriaceae; ICU, intensive care unit.
Current observation
Reduction in health care staff members Outsourcing of biology acts Cost-saving policy
NOTE. Systemic/latent failures stem from fallible decisions, often taken by people not directly involved in the workplace. In medicine, latent failures would primarily be the responsibility of management and of senior clinicians at those times when they are making decisions on the organization of their unit.
Current observation
Type of failure Action slips Cognitive failures Violation
Example
Current observation
Picking the wrong syringe Memory lapse or mistakes through ignorance Deviation from protocols, standards, procedures
NOTE. Active/patent failures: unsafe acts or omissions committed by those whose actions can have immediate adverse consequences.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
journal homepage: www.ajicjournal.org
Major article
Prolonged delay for controlling KPC-2eproducing Klebsiella pneumoniae outbreak: The role of clinical management T. Delory MD, MPH a, E. Seringe MD a, *, G. Antoniotti MD b, I. Novakova RN a, C. Goulenok MD b, I. Paysant RN b, S. Boyer PharmD b, c, A. Carbonne MD d, T. Naas PhD e, f, g, P. Astagneau MD, PhD a, h a
Regional Centre for Nosocomial Infection Control, CClin Nord, Paris, France Groupe Générale de Santé, Paris, France Laboratoire Bactériologie Novescia, Paris, France d Office of Quality and Safety in Care, Direction Générale de l’Offre de Soins-Bureau PF2-Ministère de la Santé, des affaires sociales et du droit des femmes, Paris, France e Department of Bacteriology, APHP, Laboratoire de Bactériologie-Virologie, Hôpital de Bicêtre, Le Kremlin Bicêtre, France f Centre National de Référence de la résistance aux antibiotiques, Le Kremlin Bicêtre, France g EA7361, Faculté de Médecine, Université Paris Sud, France h Department of Epidemiology, Ecole des Hautes Etudes en Santé Publique/Universités Sorbonne Paris Cité, Paris, France b c
Key Words: Carbapenem-producing enterobacteriaceae Infection control Outbreak Root causes analysis
Background: Carbapenemase-producing Enterobacteriaceae (CPE) are becoming of immediate concern for infection control policies. Prompt detection of CPE on health care setting admission is crucial to halt the spread of an outbreak. We report a cluster of 13 Klebsiella pneumoniae carbapenemase (KPC)-2e producing K pneumoniae cases in a tertiary care hospital.The objective of this study was to identify contributing factors originating the outbreak. Methods: An outbreak investigation was conducted using descriptive epidemiology, observation of health care practices, and interviews of management staff. A root cause analysis was performed to identify patent and latent failures of infection control measures using the association of litigation and risk management method. Results: The main patent failure was the delay in identifying KPC-2eproducing K pneumoniae carriers. Contributing factors were work and environmental factors: understaffing, lack of predefined protocols, staff members’ characteristics, and underlying patients’ characteristics. Latent failures were as follows: no promotion of the national guidelines for prevention of CPE transmission, no clear procedure for the management of patients hospitalized abroad, no clear initiative for promoting a culture of quality in the hospital, biologic activity recently outsourced to a private laboratory, and poor communication among hospital members. Conclusion: Clinical management should be better promoted to control hospital outbreaks and should include team work and safety culture. Copyright Ó 2015 by the Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
For the last 5 years, carbapenemase-producing Enterobacteriaceae (CPE) have emerged as an important group of extremely drug-resistant (XDR) health careeassociated pathogens worldwide and are now recognized to be associated with substantial morbidity and mortality.1-5 To date, most of the outbreaks observed in low- and mid-incidence European countries are related to the importation of cases from a foreign country.1,2,6 Delaying the * Address correspondence to Elise Seringe, MD, CClin Nord, 8 rue Maria Helena Vieira da Silva, 75014 Paris, France. E-mail address: [email protected] (E. Seringe). Conflicts of interest: None to report.
detection of patients at risk for CPE carriage and implementation of reinforced infection control measures are factors that facilitate outbreaks.6-8 In addition to the implementation of antimicrobial stewardship programs, the reinforcement of prompt screening and isolation of carriers are the major keys to control CPE spread. In case of a CPE-related outbreak, a heavy reorganization of care, including cohorting of CPE carriers with dedicated health care personnel and identification of contact patients, seems to be effective.3,6,9 In December 2010, the French health authority issued national recommendations for the screening and presumptive isolation of patients transferred from hospitals abroad.10,11 On July 15, 2011, a nonteaching tertiary hospital reported a cluster of Klebsiella
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Fig 1. Epidemic curve of the outbreak and implementation of infection control measures. The epidemic curve of 13 patients tested positive for the same clone of Klebsiella pneumoniae carbapenemase-2eproducing K pneumoniae in the ICU and cardiology department. A bundle of interventions was fully implemented on July, 19, 2011. D-1, D-3, D-30, and D-40 are the key points of investigations-intervention start and are figured by arrows on the baseline time frame. The hatching portion bar represents the period without systematic weekly screening for MDR carriage in the ICU. The black points represent the screening of MDR carriage (rectal and throat samples). The light gray box represents ICU cases. The dark gray box represents cardiology cases. The case number 8 was first hospitalized in the ICU and then in cardiology. D-1, day 1; D-3, day 3; D-30, day 30; D-40, day 40; ICU, intensive care unit; MDR, multidrug resistant.
pneumoniae carbapenemase-2 (KPC-2)eproducing K pneumoniae to the regional center for health careeassociated infection control in Paris. The outbreak’s index case was a patient repatriated from a Greek hospital 1 month before. An epidemiologic investigation was then started to estimate the outbreak’s magnitude, identify potential risk factors for a larger spread, and help to implement appropriate control measure. To understand the systemic factors of nonadherence to standard recommendations, which could explain the spread of the outbreak, we conducted a root cause analysis. METHODS The study was carried out in a 320-bed private nonteaching tertiary hospital located in the Paris area of France. From July-August 2011, an expert team from the regional center for infection control conducted a descriptive epidemiologic study of the outbreak. In parallel, they began an observation of health care practices and staff management to conduct a root cause analysis. Patient data were collected, including clinical characteristics, hospitalization and hospital discharge dates, dates of rectal swabs, microbiologic results, and status for CPE colonization or infection. Standard criteria were used to define cases and contact patients. A case was defined as a patient infected or colonized by the same clone of KPC-2eproducing K pneumoniae confirmed by the Antimicrobial Resistance National Reference Center (NRC; Le Kremlin Bicêtre, France). The diagnosis of clinical infection or colonization was made by the physician in charge of the patient. A contact patient was defined as a patient hospitalized in the same ward and cared for by the same personnel as the case during the same period. An exhaustive contact patients screening was performed among 13 French administrative regions. All contact patients were traced by phone recall or mail. Data for auditing practices and root cause analysis were collected through interviews of the health care and management personnel using a standardized report form (Appendix 1). Staff were asked about their workload levels, fatigue, knowledge and training policy, ability or experience, supervision or instruction by the manager, stressful environment conditions, rapid change within an organization, performance of communication, planning and scheduling, and maintenance of equipment and buildings. A systemic analysis was then performed using the association of litigation and risk management method (ALARM) described by Vincent et al.12-14 This method consists of the identification of patent and latent failures. Patent failures12 were considered in case of unsafe acts or omissions, which could have had immediate adverse consequences. Latent failures12 were the conditions in
which errors occur in the clinical wards (contributing factors) and the factors related to organization-management at the institutional level (systemic factors). Screening of cases and contact patients for carbapenemase typing or monoclonal characterization was performed by the NRC, according to standard methods.15-17 Microbiologic techniques consisted of testing antibiotic susceptibility by disk diffusion on Mueller-Hinton agar according to the standards of the Antibiogram Committee of the French Microbiology Society.18 Minimum inhibitory concentrations were determined using Etest strips (BioMérieux, Marcy-l’Étoile, France) and were interpreted as previously described. All carbapenem-resistant strains were sent to the NRC for confirmation. Carbapenemase production was detected using the Hodge test and synergy test between carbapenems and ethylenediaminetetraacetic acid (for class B metallo b-lactamases) or clavulanic acid (for class A b-lactamases).19 The genes encoding carbapenemases were identified by the NRC using polymerase chain reaction and sequencing of the amplified product.20 Genomic relatedness of the KPC-2eproducing K pneumoniae isolates was investigated by semiautomated repetitive polymerase chain reaction typing (DiversiLab; BioMérieux, Marcy-l’Étoile, France) as recommended by the manufacturer.21 RESULTS From July 7-August 30, 2011, in addition to the index case, 12 secondary health careeassociated cases of KPC-2eproducing K pneumoniae in 3 different health care facilities were identified, including 2 clusters of patient-to-patient transmission (Fig 1). None had CPE infection, and 5 deaths not attributable to CPE were observed. Two out of these 13 cases were identified after their transfer to other hospitals. Among the 282 contact patients identified, 149 returned home, 25 died, 32 remained hospitalized, and 76 were transferred to 29 other hospitals. Overall, 210 contact patients were screened (rectal sample) at least once and remained negative. The genetic relatedness is shown in Figure 2. The main patent failure was the delay in case identification. Two main reasons were involved in the delay in CPE carriers’ identification. The first was KPC-2eproducing K pneumoniae carried by the index case was at first characterized as a common Extended-Spectrum Beta-Lactamase (ESBL)-producing Klebiella pneumonia strain (3 days after the patient’s hospitalization). Although the index patient was screened immediately on admission for potentially carbapenemase-producing strains, as recommended by the French guidelines in case of repatriated patients,10 the resistance to
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direction, clinical staff members, and quality and safety department. According to the national guidelines,10,11 a bundle of infection control measures was implemented (40 days after index case admission). The bundle included systematic screening of the 25 ICU patients and new suspected cases on admission. Suspected cases and contact patients were cohorted in dedicated wards with dedicated staffs. Staff members received education and training in infection control, and a procedure for the enhancement of environmental and material surfaces’ cleaning was implemented (Table 1). No other secondary transmission occurred after the reinforcement of infection control measures. Since the outbreak was halted, the local infection control team has been provided with a part-time infection control practitioner and a full-time nurse. A local plan for the management of emerging pathogen carriers has been setup. Changes to the hospital teams’ characteristics before and after outbreak are listed in Table 1. DISCUSSION
Fig 2. Genetic relatedness of the KPC-2eproducing K pneumoniae isolates. Semiautomated repetitive polymerase chain reaction typing (DiversiLab; BioMérieux, Marcy-l’Étoile, France) of KPC-2-producingeK pneumoniae isolates is shown. Numbers 1-13 on the dendrogram correspond to the patient numbers, whereas 14 and 15 correspond to 2 nonrelated isolates. Number below the P indicate the number of patterns identified. All the KPC-2eproducing isolates belong to a single pattern. KPC-2, Klebsiella pneumoniae carbapenemase-2.
imipenem was not detected by the hospital laboratory. Second, weekly screening of intensive care unit (ICU) patients using rectal sampling for detection of multidrug-resistant organisms (MDRs) was disrupted during the 4 weeks after index case admission (day 1). The index case CPE carriage was identified by the NRC 30 days after admission to the ICU. At this time (day 30), 2 transmissions had already occurred and were established to be genetically related to the KPC-2eproducing K pneumoniae clone carried by the index case. As shown in Figure 3, factors which were determined as a trigger of patent failures were the following: (1) work and environmental factors (heavy workload in the ICU, summer period, index case hospitalization during a public holiday, delay in K pneumoniae carbapenemase typing method); (2) team factors (understaffed teams, major ICU reorganization before and during the outbreak period); (3) tasks factors (lack of predefined protocols to contain outbreaks); (4) individual characteristics (staff members’ lack of knowledge and misapplication of infection control measures and the national recommendations for CPE spread prevention); and (5) patient characteristics with heavy burden of disease (intensive and invasive cares, high incidence of nosocomial infection, high level of antibiotics consumption). Latent failures at the outbreak onset were related to organizational and management policies: (1) no promotion of the national guidelines for the prevention of XDR bacteria transmission existed in clinical wards; (2) no clear procedure existed for the management of patients hospitalized abroad11; (3) no clear initiative existed for promoting a culture of quality; and in the hospital, (4) biologic activities were recently outsourced to a private laboratory, and (5) there was a poor communication level between hospital
Our study showed that the reasons which explain ineffective control of such outbreaks must be analyzed beyond immediate observation of breaches in hygiene practices, the so-called patent failures. The root cause analysis using the ALARM is an effective, reproducible, and comprehensive approach to identifying deep causes related to institutional, organizational, and management factors.12-14 To our knowledge, the ALARM has not been routinely used in epidemiologic investigations of hospital outbreaks, regardless of the involved pathogens. In comparison with other root cause analysis methods, the ALARM has the advantage of exploring health care team factors, but it needs to collect timedependent items which could be missing because outbreak data are mostly collected retrospectively. In our study, the delay in case identification was the main contributing factor to the outbreak. This was partly because the local microbiology laboratory did not send the strain to the NRC; however, a low susceptibility to imipenem had been identified in a sample from a repatriated patient. However, the secondary cases were mainly because of breaches to infection control measures. They were assumed to be related to a chain of disorders or failures in terms of care organization, including the lack of safety culture promotion and a deficiency in collaborative relationships among hospital direction, clinical staff members, and the quality and safety department. Effective infection control measures for preventing secondary transmission were also delayed. This could be related to institutional factors, including the cost-saving policy with consequences in terms of understaffed teams at every level of both the clinical wards and the local infection control team. This was enhanced by the summer period with difficulties to temporarily replace health care workers on vacation. Before the KPC-2e producing K pneumoniae occurrence, the local infection control team was only composed of a part-time contract nurse. The local infection control practitioner had resigned from his position before the outbreak’s occurrence and had not been replaced at the outbreak’s onset. In addition, laboratory activities were recently outsourced to reduce hospital charges but resulted in a default of MDR-strain screening in the ICU and lack of feedback to ICU staff members when KPC-2eproducing K pneumoniae cases were suspected. We observed that the head of the ICU was absent when the outbreak occurred, which could be considered as a contributing factor to partly explain disorder in organization and management of care and as a risk factor of health careeassociated infections, as shown in a recent review.22 Positive and proactive leadership has
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Fig 3. Latent and patent failures related to the control of a KPC-2eproducing K pneumoniae outbreak using the association of litigation and risk management method. Patent failures were considered in case of unsafe acts or omissions, which could have immediate adverse consequences resulting in immediate observation of breaches in hygiene practices. Latent failures were the conditions in which errors occur in the clinical wards (contributing factors) and the factors related to organization-management at the institution level (systemic factors). CR-KP, Carbapenem-resistant klebsiella pneumonia; KPC-2, Klebsiella pneumoniae carbapenemase-2. Table 1 Characteristics of infection control measures and hospital teams before, during, and after the CR-KP outbreak Measures
Before
Infection control measures Diffusion of the national guidelines for the prevention of CPE transmission Local plan of action for containing XDR-strains outbreak Identification of CPE carriers Mispractices in standard infection control measures Isolation-cohorting wards Staff members’ education Improved protocol for the cleaning of environmental and material surfaces Technical assistance from the regional center to the infection control team Hospital teams ICU department Head of department Local infection control team Infection control practitioner None Nurse Part-time Premises -
During
After
þ
þ
þ
þ -
þ -
þ þ þ
þ þ
þ
None Part-time Part-time Full-time þ þ
CPE, carbapenemase-producing Enterobacteriaceae; CR-KP, Carbapenem-ResistantKlebsiella pneumonia; ICU, intensive care unit; XDR, extremely drug resistant.
already been reported to be associated with a reduced incidence in pneumonia and urinary tract infection.23 This relationship is usually mediated by staff experience and stability.23 In England, a national investigation by the Healthcare Commission had also described that inadequate team work could alter quality of care and
effectiveness to control hospital outbreaks.24 Understaffing nursing teams could also be related to increased rates of health caree associated infections, and several studies22,25,26 have demonstrated that an increasing nurse-patient ratio in the ICU was associated with a reduction in infection risks. Therefore, temporary nursing staff and team instability could be risk factors for health care infections and other adverse events.22 Finally, outbreak control was successfully achieved when a bundle of infection control measures was promptly implemented with the help of an external expert team. Multidisciplinary approaches, especially multifaceted interventions, have been demonstrated to be an effective way to reduce the rate of health careeassociated infection, especially in the ICU for ventilatorassociated pneumonia27 and methicillin-resistant Staphylococcus aureus infections.28 In our study, few infection control measures were assumed to be in place in the ICU before the implementation of the bundle of infection control measures. Indeed, the lack of MDR carriage screening a few weeks before the outbreak and little knowledge and awareness about measures for CPE prevention by the health care staff support this hypothesis. According to French recommendations, all admissions to the ICUs undergo active screening for MDR carriage upon admission29,30 but not weekly. However, most of the French ICUs, including the hospital in this study, have routinely implemented this screening. On the other hand, once the outbreak was identified, the infection control team was very prompt to react and was rapidly involved in the management improvement process. Besides, since this outbreak has occurred, the hospital has developed and used an effective program for the control of XDR-emerging pathogens. The effectiveness of the national guideline recommendations for CPE
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outbreak management10,11 gains to be supported by collaborative initiatives, such as auditing, root cause approach, and experience feedback to health care staff, as described.22,31 Education, training programs, and the promotion of a safety culture toward staff members; the allocation of substantial human resources to infection control teams, especially medical practitioners; and policies for systematic CPE screening in high-risk settings are warranted.
Acknowledgment We thank the Antimicrobial Resistance National Reference Center (France) for the identification of the genetic relatedness among Klebsiella pneumoniae carbapenemaseeproducing strains and the genetic relevance among cases.
References 1. Cantón R, Akóva M, Carmeli Y, Giske CG, Glupczynski Y, Gniadkowski M, et al. Rapid evolution and spread of carbapenemases among Enterobacteriaceae in Europe. Clin Microbiol Infect 2012;18:413-31. 2. Vaux S, Carbonne A, Thiolet JM, Jarlier V, Coignard B, RAISIN and Expert Laboratories Groups. Emergence of carbapenemase-producing Enterobacteriaceae in France, 2004 to 2011. Euro Surveill 2011;16. 3. Munoz-Price LS, Poirel L, Bonomo RA, Schwaber MJ, Daikos GL, Cormican M, et al. Clinical epidemiology of the global expansion of Klebsiella pneumoniae carbapenemases. Lancet Infect Dis 2013;13:785-96. 4. Chiu SK, Wu TL, Chuang YC, Lin JC, Fung CP, Lu PL, et al. National surveillance study on carbapenem non-susceptible Klebsiella pneumoniae in Taiwan: the emergence and rapid dissemination of KPC-2 carbapenemase. PLoS One 2013; 8:e69428. 5. Falagas ME, Lourida P, Poulikakos P, Rafailidis PI, Tansarli GS. Antibiotic treatment of infections due to carbapenem-resistant Enterobacteriaceae: systematic evaluation of the available evidence. Antimicrobial Agents Chemother 2014;58:654-63. 6. Fournier S, Monteil C, Lepainteur M, Richard C, Brun-Buisson C, Jarlier V, et al. Long-term control of carbapenemase-producing Enterobacteriaceae at the scale of a large French multihospital institution: a nine-year experience, France, 2004 to 2012. Euro Surveill 2014;19. 7. Kochar S, Sheard T, Sharma R, Hui A, Tolentino E, Allen G, et al. Success of an infection control program to reduce the spread of carbapenemresistant Klebsiella pneumoniae. Infect Control Hosp Epidemiol 2009;30: 447-52. 8. Munoz-Price LS, De La Cuesta C, Adams S, Wyckoff M, Cleary T, McCurdy SP, et al. Successful eradication of a monoclonal strain of Klebsiella pneumoniae during a K. pneumoniae carbapenemase-producing K. pneumoniae outbreak in a surgical intensive care unit in Miami, Florida. Infect Control Hosp Epidemiol 2010;31:1074-7. 9. Guh AY, Limbago BM, Kallen AJ. Epidemiology and prevention of carbapenemresistant Enterobacteriaceae in the United States. Expert Rev Anti Infect Ther 2014;12:565-80. 10. Haut Conseil de la Santé publique. Commission spécialisée Sécurité des patients: infections nosocomiales et autres évènements indésirables liés aux soins et aux pratiques. Recommandations pour le dépistage du portage digestif des bactéries commensales multi-résistantes aux antibiotiques importées en France è l’occasion du rapatriement de patients en provenance de l’étranger et maîtrise de leur diffusion. 2010. Available from: http://www. hcsp.fr/docspdf/avisrapports/hcspr20100518_bmrimportees.pdf. Accessed June 12, 2015.
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11. Lepelletier D, Andremont A, Grandbastien B, National Working Group. Risk of highly resistant bacteria importation from repatriates and travelers hospitalized in foreign countries: about the French recommendations to limit their spread. J Travel Med 2011;18:344-51. 12. Vincent C, Taylor-Adams S, Stanhope N. Framework for analysing risk and safety in clinical medicine. BMJ 1998;316:1154-7. 13. Vincent C, Taylor-Adams S, Chapman EJ, Hewett D, Prior S, Strange P, et al. How to investigate and analyse clinical incidents: clinical risk unit and association of litigation and risk management protocol. BMJ 2000;320: 777-81. 14. Vincent C. Analysis of clinical incidents: a window on the system not a search for root causes. Qual Saf Health Care 2004;13:242-3. 15. Bratu S, Mooty M, Nichani S, Landman D, Gullans C, Pettinato B, et al. Emergence of KPC-possessing Klebsiella pneumoniae in Brooklyn, New York: epidemiology and recommendations for detection. Antimicrobial Agents Chemother 2005;49:3018-20. 16. Bratu S, Landman D, Alam M, Tolentino E, Quale J. Detection of KPC carbapenem-hydrolyzing enzymes in Enterobacter spp. from Brooklyn, New York. Antimicrobial Agents Chemother 2005;49:776-8. 17. Nordmann P, Gniadkowski M, Giske CG, Poirel L, Woodford N, Miriagou V, et al. Identification and screening of carbapenemase-producing Enterobacteriaceae. Clin Microbiol Infect 2012;18:432-8. 18. Société Française de Microbiologie (SFM). Antibiogram committee of the French Society for Microbiology. Recommendations 2011 [French]. Paris, France: SFM; 2011. 19. Picão RC, Andrade SS, Nicoletti AG, Campana EH, Moraes GC, Mendes RE, et al. Metallo-beta-lactamase detection: comparative evaluation of double-disk synergy versus combined disk tests for IMP-, GIM-, SIM-, SPM-, or VIM producing isolates. J Clin Microbiol 2008;46:2028-37. 20. Courvalin P, Leclercq R, Rice LB, editors. Antibiogram. Washington, DC: American Society for Microbiology Press; 2010. 21. Cuzon G, Naas T, Correa A, Quinn JP, Villegas MV, Nordmann P. Dissemination of the KPC-2 carbapenemase in non-Klebsiella pneumoniae enterobacterial isolates from Colombia. Int J Antimicrob Agents 2013;42:59-62. 22. Griffiths P, Renz A, Hughes J, Rafferty AM. Impact of organisation and management factors on infection control in hospitals: a scoping review. J Hosp Infect 2009;73:1-14. 23. Houser J. A model for evaluating the context of nursing care delivery. J Nurs Adm 2003;33:39-47. 24. Healthcare Commission. Learning from investigations. London, England: Commission for Healthcare Audit and Inspection; 2008. 25. Hugonnet S, Harbarth S, Sax H, Duncan RA, Pittet D. Nursing resources: a major determinant of nosocomial infection? Curr Opin Infect Dis 2004;17: 329-33. 26. Hugonnet S, Chevrolet JC, Pittet D. The effect of workload on infection risk in critically ill patients. Crit Care Med 2007;35:76-81. 27. Kaye J, Ashline V, Erickson D, Zeiler K, Gavigan D, Gannon L, et al. Critical care bug team: a multidisciplinary team approach to reducing ventilatorassociated pneumonia. Am J Infect Control 2000;28:197-201. 28. Salaripour M, McKernan P, Devlin R, Infection Prevention and Control Team. A multidisciplinary approach to reducing outbreaks and nosocomial MRSA in a university- affiliated hospital. Healthc Q 2006;9:54-60. 29. Société Française d’Hygiène Hospitalière. Recommandations pour la prévention de la transmission croisée: précautions complémentaires contact. Hygiènes 2009;17:81-137. 30. Haut Conseil de la Santé Publique. Commission spécialisée Sécurité des patients: infections nosocomiales et autres évènements indésirables liés aux soins et aux pratiques. Recommandations relatives aux mesures à mettre en oeuvre pour prévenir l’émergence des entérobactéries BLSE et lutter contre leur dissémination. 2010. Available from http://www.hcsp.fr/Explore.cgi/ Telecharger?NomFichier¼hcspr20100202_enterobactBLSE.pdf. Accessed June 12, 2015. 31. Jamtvedt G, Young JM, Kristoffersen DT, O’Brien MA, Oxman AD. Audit and feedback: effects on professional practice and health care outcomes. Cochrane Database Syst Rev; 2006:CD000259.
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APPENDIX 1. ASSOCIATION OF LITIGATION AND RISK MANAGEMENT APPROACH Investigation process 5. All investigations consist of a series of steps that should be followed, as a matter of routine, when an incident is investigated: 1. Ascertain that a serious clinical incident has occurred and ensure it is formally reported. Alternatively, identify an incident as being fruitful in terms of organizational learning. 2. Trigger the investigation procedure. Notify the senior members of staff who have been trained to carry out investigations. 3. Establish the circumstances as they initially appear and complete an initial summary, decide which part of the process of care requires investigating, prepare an outline chronology of events, and identify any obvious care management problems. 4. Structured interview of staff: Establish chronology of events.
6.
7. 8. 9.
Revisit sequence of events and ask questions about each care management problem identified at the initial stage. Use framework to ask supplementary questions about reasons for each care management problem. If new care management problems have emerged during interviews, add them to the initial list. Interview again if necessary. Collate interviews and assemble composite analysis under each care management problem identified. Identify both specific and, where appropriate, general contributory factors Compile report of events, listing causes of care management problems and recommendations to prevent recurrence. Submit report to senior clinicians and management according to local arrangements. Implement actions arising from report and monitor progress.
Reproduced from [How to investigate and analyse clinical incidents: clinical risk unit and association of litigation and risk management protocol, Vincent C, Taylor-Adams S, Chapman EJ, Hewett D, Prior S, Strange P, Tizzard A, 320, 777-781, 2000] with permission from BMJ Publishing Group Ltd.13
Type of factors
Example
Work and environment Workload Year period Team factors Verbal communication Written communication Supervision and seeking help Structure of team Task factors Standardization of care Task design Structure clarity Individual (staff members) Experience Knowledge Personality Skills Patient characteristics Severe disease Antibiotic consumption Health careeassociated infection Framework for root cause analysis. Reproduced from [Framework for analysing risk and safety in clinical medicine, Vincent C, Taylor-Adams S, Stanhope N, 316, 1154-1157, 1998] with permission from BMJ Publishing Group Ltd.12
Type of failure Management decision Organizational process Institutional context
Example
High workload Holiday No communication between professions Availability of records Responsiveness of senior staff Balance of senior and junior staff Availability of clear and efficient protocols
Junior versus senior staff Knowledge of available protocols
ICU patients High consumption of carbapenems High incidence of ESBL-E carriage
NOTE. Associated factors are conditions proving by latent failures in which unsafe acts occur. ESBL-E, Extended-Spectrum Beta-Lactamase Enterobacteriaceae; ICU, intensive care unit.
Current observation
Reduction in health care staff members Outsourcing of biology acts Cost-saving policy
NOTE. Systemic/latent failures stem from fallible decisions, often taken by people not directly involved in the workplace. In medicine, latent failures would primarily be the responsibility of management and of senior clinicians at those times when they are making decisions on the organization of their unit.
Current observation
Type of failure Action slips Cognitive failures Violation
Example
Current observation
Picking the wrong syringe Memory lapse or mistakes through ignorance Deviation from protocols, standards, procedures
NOTE. Active/patent failures: unsafe acts or omissions committed by those whose actions can have immediate adverse consequences.