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Infection prevention and control in patients with cystic fibrosis (CF): Results from a survey in 35 German CF treatment centers Sonja Meyer a, Thomas Nüßlein b, Lutz Nährlich c, Jutta Bend d, Barbara Gärtner e, Sören L. Becker e, Arne Simon a,∗ a
Department of Pediatric Hematology and Oncology, Children’s Hospital Medical Center, University Hospital of Saarland, Kirrberger Str. Building 9, 66421 Homburg/Saar, Germany Gemeinschaftsklinikum Mittelrhein -Klinik für Kinder- und Jugendmedizin, Koblenzer Str. 115-155, 56073 Koblenz, Germany c Department of Pediatrics, Justus-Liebig-University Giessen, Feulgenstr. 12, 35385 Giessen, Germany d Mukoviszidose e.V. & Mukoviszidose Institut gGmbH In den Dauen 6, 53117 Bonn, Germany e Institute of Medical Microbiology and Hygiene, Saarland University, Kirrberger Str., Building 43, 66421 Homburg/Saar, Germany b
a r t i c l e
i n f o
Article history: Received 8 May 2019 Revised 6 October 2019 Accepted 9 October 2019 Available online xxx Keywords: Cystic fibrosis Infection prevention and control Commission for hygiene and infection control Pseudomonas aeruginosa Survey Segregation
a b s t r a c t This survey evaluates whether the Cystic Fibrosis (CF)-specific infection prevention and control (IPC) recommendations released by the Commission for Hospital Hygiene and Infection Prevention (KRINKO) in 2012 have been implemented in specialized German CF facilities. Of 35 participating centers (response rate 32.7%), 37% care for more than 100 patients and 44% treat mainly adults. Clinics for adult CF patients report a shortage of qualified personnel for intensified environmental cleaning. Some hospitals struggle to provide single patient rooms with an adjacent sanitary area to segregate CF patients strictly. Most centers offer at least one decolonization cycle (including systemic and inhalative antibiotics) to patients colonized with MRSA. In CF centers in Germany, the KRINKO IPC recommendations are considered helpful by the attending physicians and thoroughly implemented. There is room for improvement concerning strict segregation of inpatients with CF in single patient rooms, in particular in large CF centers mainly caring for adults. © 2019 European Cystic Fibrosis Society. Published by Elsevier B.V. All rights reserved.
1. Introduction
2. Methods
The prevention of cross-infection continues to be an issue of considerable concern for the CF community, since progressive respiratory infection still accounts for the majority of CF-related morbidity and mortality [1,2]. In view of this complex background (more information in the online supplementary material), a working group of the German Commission for Hospital Hygiene and Infection Prevention (KRINKO) issued Infection Prevention and Control (IPC) recommendations for the medical treatment of CF patients in inpatient facilities and outpatient departments in 2012 [3]. The present survey aims to evaluate the implementation of these IPC recommendations in German medical centers specialized in the treatment of patients with CF.
Based on the recommendations released by the KRINKO in 2012 [3], the authors developed an internet-based survey (Survey MonkeyTM ; San Mateo, USA). The online supplementary material (available on the journal website) comprises the survey in detail and the specific KRINKO recommendations, and KRINKO definitions for multidrug-resistant Gram-negative pathogens (3MRGN and 4 MRGN).1 Collection of data and analysis of anonymized results took place according to German data protection laws.
∗ Corresponding author at: Children’s Hospital Medical Center, University Hospital Homburg, Kirrberger Str. Building 09, 66421 Homburg, Germany. E-mail addresses:
[email protected] (S. Meyer),
[email protected] (T. Nüßlein),
[email protected] (L. Nährlich),
[email protected] (J. Bend),
[email protected] (B. Gärtner),
[email protected] (S.L. Becker),
[email protected] (A. Simon).
1 With regard to Enterobacterales, 3MRGN refers to Gram-negative bacteria that are resistant to piperacillin, ceftazidime, cefotaxime and ciprofloxacin, whereas 4MRGN describes isolates that are additionally resistant to imipenem and/or meropenem. Of note, carbapenemase-producing strains are categorized as 4MGRN regardless of their susceptibility pattern towards other beta-lactams and fluoroquinolones. For P. aeruginosa, 3MRGN is defined as any isolate with susceptibility to only one of the aforementioned classes of antibiotics, whereas 4MRGN strains are resistant to all four classes.
https://doi.org/10.1016/j.jcf.2019.10.012 1569-1993/© 2019 European Cystic Fibrosis Society. Published by Elsevier B.V. All rights reserved.
Please cite this article as: S. Meyer, T. Nüßlein and L. Nährlich et al., Infection prevention and control in patients with cystic fibrosis (CF): Results from a survey in 35 German CF treatment centers, Journal of Cystic Fibrosis, https://doi.org/10.1016/j.jcf.2019.10.012
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Cleaning Staff
Cardiology (EKG, Echo, Outpaent Clinic)
Radiology
43%
29%
37%
Members of the psycho-social team (Psychologists, Social Workers)
63%
Nutrionists
57%
Physical therapists
77%
Doctors
97%
Nursing staff
97%
Fig. 1. Proportion of professions, to whom educational sessions concerning infection prevention and control topics in CF patients are offered.
3. Results
3.5. Hand hygiene
3.1. Response rate, center characteristics
The KRINKO recommendation “Hand Hygiene” [5] is readily available in 80% (n = 28) of all centers, and 92% participate in the German “Clean Hands Campaign” [6]. 97% (n = 34) of all centers recommend to disinfect hands on arrival and when leaving the inpatient ward or the CF outpatient clinic. In addition, 92% promote a strict “No handshake” policy.
In total, we invited 107 German CF centers by e-mail to participate. One physician each from 35 centers sufficiently completed the survey (response rate 32.7%). Referring to data from the German CF Registry [4] the centers participating in this survey are responsible for the treatment of 55% of all registered CF patients in Germany (n = 6.106). The median number of CF patients per center was 90 (interquartile range, IQR, 50–160; max. 400 patients). The centers were classified into the category “small” (up to 100 patients; 63%; n = 22) or “large” (more than 100 patients; 37%, n = 13). The median proportion of adult patients (>18 years) was 50% (IQR, 25%–60%).
3.6. Intensified environmental cleaning Fig. 2 depicts the regular availability of qualified personnel to perform intensified environmental cleaning / disinfection. A shortage of qualified personnel is statistically more often indicated by CF inpatient units primarily treating adult patients (80% vs. 20% in age balanced units and 0% in primary pediatric units; p = 0,044).
3.2. Awareness of the KRINKO recommendations 97% stated to be aware of the KRINKO recommendation; 54% confirmed having translated its main topics into IPC written instructions. Twenty percent stated that they have only implemented certain topics out of the recommendation and 26% negated this question.
3.3. Education concerning IPC issues 86% of all centers offer interdisciplinary educational sessions to inform about CF specific IPC issues. Fig. 1 shows the different professional groups to whom such training is offered. 89% (n = 31) educate patients / families; 51% (n = 18) use age adjusted written materials. Only 6% (n = 2) actively involve patients into the conception and design of these materials.
3.7. Single rooms and other isolation precautions Inpatients with CF are allocated to single rooms with an adjacent sanitary area (toilet and bath) in 81% (n = 33) of all participating centers, in 7% (n = 3) to single rooms without adjacent sanitary area. 12% (n = 5) do not regularly allocate CF patients to single rooms. The latter group included only centers which primarily treat adult CF patients (p = 0.033), and large centers (concerning single patient rooms with adjacent sanitary area; 23% vs. 0% in small centers; p = 0.044). Fig. 3 shows additional measures implemented by the CF center in case of the detection of a resistant pathogen. Small centers more often implement contact and droplet isolation in CF patients colonized/infected with 3 MRGN P. aeruginosa (100% vs. 62%; p = 0.004) or admitted to the intensive care unit (95% vs. 62%; p = 0.015).
Please cite this article as: S. Meyer, T. Nüßlein and L. Nährlich et al., Infection prevention and control in patients with cystic fibrosis (CF): Results from a survey in 35 German CF treatment centers, Journal of Cystic Fibrosis, https://doi.org/10.1016/j.jcf.2019.10.012
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3
100%
78%
80%
66% 60%
40%
20%
20%
14%
14% 9%
0%
Yes
No
Don't know
Yes
On the ward
No
Don't know
In the CF outpaent clinic
Fig. 2. Regular availability of personnel for environmental cleaning and disinfection in different areas.
MRSA
4MRGN P. aeruginosa
3MRGN P. aeruginosa
B. cepacia complex
Non-tuberculous mycobacteria
Don't know
Single room
Disposable gown
Face mask
0.0%
10.0%
20.0%
30.0%
40.0%
50.0%
60.0%
70.0%
80.0%
90.0%
100.0%
Fig. 3. Inpatient ICP management in case of colonization or infection with certain bacterial pathogens.
3.8. MRSA management 97% of all participating centers offer at least one course of decolonization treatment to patients having a recent MRSA finding; 86% administer systemic antibiotics, and 57% use vancomycin inhalation in addition to mupirocin nasal ointment and chlorhexidine (or octenidine) bathing or showering.
3.9. Inhalation treatment 15% (n = 9) of all participating centers only use single-use inhalation equipment, 38% (n = 23) use medical devices with reprocessing (disinfection or sterilization) between patients; 48%
(n = 29; multiple answers allowed) request patients to bring their own inhalation equipment into the hospital.
3.10. IPC efforts in outpatient CF clinics All participants (herein 100% refers to n = 34). segregate P. aeruginosa colonized patients, and 97% have implemented the same segregation strategy for patients colonized/infected with non-tuberculosis mycobacteria. 97% inform patients and parents/caregivers about the potential risk of transmission of CF relevant pathogens during recreational activities shared by different CF patients. 60% supply (and 12% do not supply) their CF patients with a (surgical) facemask at the entrance to the outpatient clinic.
Please cite this article as: S. Meyer, T. Nüßlein and L. Nährlich et al., Infection prevention and control in patients with cystic fibrosis (CF): Results from a survey in 35 German CF treatment centers, Journal of Cystic Fibrosis, https://doi.org/10.1016/j.jcf.2019.10.012
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29% hand out facemasks to their patients for using it during subsequent appointments. Patients are advised to reprocess their nebulizer equipment at home (multiple answers allowed) by vaporization in a device (97%), by boiling (47%) or in a dishwasher (12%; multiple answers allowed). 4. Discussion This survey provides the first comprehensive dataset about the practical implementation of IPC strategies in German CF centers. The participating centers provide treatment to 55% of all registered CF patients in Germany. All participants considered evidence-based recommendations from IPC authorities as necessary and helpful. Many of the recommendations have readily been translated into clinical practice [7–9]. Although aware of the KRINKO recommendations, 26% of the centers do not refer to them, perhaps they had enacted some (or many) of these IPC practices prior to their release. If CF centers request their patients to bring their nebulizer equipment into the hospital, the question has to be addressed who is responsible for the reprocessing of these contaminated private medical devices [10]. According to the 2016 CF Registry annual report [4], the proportion of CF patients in Germany with first detection of MRSA in respiratory cultures was 4,0% in patients <18 years, and 6,3% in patients ≥18 years. Although the long-term consequences of MRSA colonization in patients with CF are still debated [11], nearly all (97%) participating centers offer at least one course of decolonization treatment, and most centers (86%) use systemic antibiotics and/or inhaled vancomycin The survey results presented here reflect the changing CF landscape in terms of a growing population of adult patients [4]. Our results point out a shortage of qualified cleaning and disinfection personnel in some adult inpatient facilities [12,13]. Pediatric CF inpatients in Germany are nearly always accompanied by a parent and stay in a single patient room. Centers (12%) that did not allocate single rooms to CF patients were exclusively centers that primarily treat adult patients or large centers. The increasing number of adult patients as well as the continuing inadequacy of funding for adult CF inpatient care may still represent relevant barriers to adhere to CF infection control guidelines [14,15]. Declaration of Competing Interest None. Acknowledgment We thankfully acknowledge the time and effort spent by the participating physicians. The German Society for Pediatric Infectious Diseases (https://dgpi.de/) and the German patient organization Mukoviszidose e.V. (https://www.muko.info/) supported this project.
Supplementary materials Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.jcf.2019.10.012. References [1] Saiman L, Siegel J. Infection control recommendations for patients with cystic fibrosis: microbiology, important pathogens, and infection control practices to prevent patient-to-patient transmission. Infect Control Hosp Epidemiol 2003;24:S6–52. [2] Saiman L, Siegel JD, LiPuma JJ, Brown RF, Bryson EA, Chambers MJ, et al. Infection prevention and control guideline for cystic fibrosis: 2013 update. Infect Control Hosp Epidemiol 2014;35(Suppl 1):S1–S67. [3] Simon A, Schmitt-Grohe S, Erdmann U, Vonberg RP, Herr C, Bend J. Anforderungen an die Hygiene bei der medizinischen Versorgung von Patienten mit Cystischer Fibrose (Mukoviszidose) - unter Beteiligung der Deutschen Gesellschaft für Pädiatrische Infektiologie (Frau Prof. Dr. med. Roswitha Bruns und Herr Prof. Dr. med. Markus A. Rose), der Arbeitsgemeinschaft Mukoviszidose der Gesellschaft für Pädiatrische Pneumologie (Herr Prof. Dr. med. FrankMichael Müller) sowie der Deutschen Gesellschaft für Kinderheilkunde und Jugendmedizin (Herr Dr. med. Ernst Rietschel). mhp Verlag, Wiesbaden. 2012;1. Auflage, 2012. [4] Naehrlich L, Burkhart M, Wosniok L. German Cystic Fibrosisregistry Annual Report 2017 Release Date: November 4th Ed 2017. 2017;file:///D:/Dissertationen/Sonja%20Meyer/Meyer_Manuscript/R2%20Version %20JCF/CF%20Registry%20Germany%20annual_report_2017.pdf. [5] Kommission für Krankenhaushygiene und Infektionsprävention beim Robert Koch Institut. Händehygiene in Einrichtungen des Gesundheitswesens Empfehlung der Kommission für Krankenhaushygiene und Infektionsprävention (KRINKO) beim Robert Koch-Institut (RKI). Bundesgesundheitsblatt Gesundheitsforschung - Gesundheitsschutz 2016;59:1189–220. [6] Reichardt C, Koniger D, Bunte-Schonberger K, van der Linden P, Monch N, Schwab F, et al. Three years of national hand hygiene campaign in Germany: what are the key conclusions for clinical practice? J Hosp Infect 2013;83(Suppl 1):S11–16. [7] Savant AP, O’Malley C, Bichl S, McColley SA. Improved patient safety through reduced airway infection rates in a paediatric cystic fibrosis programme after a quality improvement effort to enhance infection prevention and control measures. BMJ Qual Saf 2014;23(Suppl 1):i73–80. [8] Wiehlmann L, Cramer N, Ulrich J, Hedtfeld S, Weissbrodt H, Tummler B. Effective prevention of Pseudomonas aeruginosa cross-infection at a cystic fibrosis centre - results of a 10-year prospective study. Int J Med Microbiol 2012;302:69–77. [9] Elborn JS, Hodson M, Bertram C. Implementation of European standards of care for cystic fibrosis–control and treatment of infection. J Cyst Fibros 2009;8:211–17. [10] O’Malley CA, VandenBranden SL, Zheng XT, Polito AM, McColley SA. A day in the life of a nebulizer: surveillance for bacterial growth in nebulizer equipment of children with cystic fibrosis in the hospital setting. Respir Care 2007;52:258–62. [11] Akil N, Muhlebach MS. Biology and management of methicillin resistant Staphylococcus aureus in cystic fibrosis. Pediatr Pulmonol 2018;53:S64–74. [12] Leas BF, Sullivan N, Han JH, Pegues DA, Kaczmarek JL, Umscheid CA.Environmental cleaning for the prevention of healthcare-associated infections. Rockville MD 2015. [13] Havill NL. Best practices in disinfection of noncritical surfaces in the health care setting: creating a bundle for success. Am J Infect Control 2013;41:S26–30. [14] Garber E, Desai M, Zhou J, Alba L, Angst D, Cabana M, et al. Barriers to adherence to cystic fibrosis infection control guidelines. Pediatr Pulmonol 20 08;43:90 0–7. [15] Zhou J, Garber E, Saiman L. Survey of infection control policies for patients with cystic fibrosis in the United States. Am J Infect Control 2008;36:220–2.
Please cite this article as: S. Meyer, T. Nüßlein and L. Nährlich et al., Infection prevention and control in patients with cystic fibrosis (CF): Results from a survey in 35 German CF treatment centers, Journal of Cystic Fibrosis, https://doi.org/10.1016/j.jcf.2019.10.012