Skip to main content
Top
Published in: BMC Nephrology 1/2019

Open Access 01-12-2019 | Septicemia | Research article

Staphylococcus aureus colonization in hemodialysis patients: a prospective 25 months observational study

Authors: Matthias Scheuch, Sabrina Freiin von Rheinbaben, Antje Kabisch, Jonas Engeßer, Susanne Ahrendt, Thomas Dabers, Christian Kohler, Silva Holtfreter, Barbara M. Bröker, Sylvia Stracke

Published in: BMC Nephrology | Issue 1/2019

Login to get access

Abstract

Background

Dialysis patients are frequently exposed to Staphylococcus aureus due to stays in dialysis centers, hospitals or rest homes. The hemodialysis vascular access is a potential entry site for S. aureus, in particular when using a central venous catheter (CVC) which increases the risk of sepsis compared to arteriovenous (AV) fistula. We prospectively followed a cohort of 86 hemodialysis patients from an outpatient dialysis center over 25 months analyzing S. aureus carrier status, S. aureus infection rates and mortality.

Methods

Demographic data and patients´ medical histories were collected and followed from all hemodialysis patients. Blood samples, nasal swabs and swabs from the hemodialysis vascular access site were taken every six months for a period of 25 months and tested for S. aureus. Strains were cultured and further characterized by spa PCR and microarray-based genotyping. Resulting data were compared with those from the general population.

Results

In cross-sectional analyses, an average of 40% of hemodialysis patients were S. aureus carriers compared to 27% in the general population. Longitudinally, a total of 65% were S. aureus carriers: 16% were persistent carriers, 43% were intermittently colonized. The most common S. aureus lineage in the dialysis patient cohort was the clonal complex (CC) 8 and the spa type t008, while in the general population, the clonal complex CC30 dominates. During the study period, we observed six S. aureus-associated blood stream infections with one S. aureus attributable death. S. aureus carriers with an AV fistula were more densely colonized in the nasal mucosa compared to patients with a CVC. Overall mortality was lower for hemodialysis patients with a positive S. aureus carrier status compared to non-carriers (hazard ratio of 0.19).

Conclusions

Compared to the general population, hemodialysis patients were more frequently colonized with S. aureus and displayed both different S. aureus colonization densities as well as lineages, possibly explained by more frequent exposure to health care environments. The lower overall mortality in carriers compared to non-carriers is intriguing and will be investigated in detail in the future.

Trial registration

ISRCTN 14385893, 2. October 2018, retrospectively registered.
Appendix
Available only for authorised users
Literature
1.
go back to reference Mulcahy ME, McLoughlin RM. Host–bacterial crosstalk determines Staphylococcus aureus nasal colonization. Trends Microbiol. 2016;24(11):872–86.CrossRef Mulcahy ME, McLoughlin RM. Host–bacterial crosstalk determines Staphylococcus aureus nasal colonization. Trends Microbiol. 2016;24(11):872–86.CrossRef
2.
go back to reference den Heijer CDJ, van Bijnen EME, Paget WJ, Pringle M, Goossens H, Bruggeman CA, Schellevis FG, Stobberingh EE. Prevalence and resistance of commensal Staphylococcus aureus, including meticillin-resistant S aureus, in nine European countries: a cross-sectional study. Lancet Infect Dis. 2013;13(5):409–15.CrossRef den Heijer CDJ, van Bijnen EME, Paget WJ, Pringle M, Goossens H, Bruggeman CA, Schellevis FG, Stobberingh EE. Prevalence and resistance of commensal Staphylococcus aureus, including meticillin-resistant S aureus, in nine European countries: a cross-sectional study. Lancet Infect Dis. 2013;13(5):409–15.CrossRef
3.
go back to reference Holtfreter S, Grumann D, Balau V, Barwich A, Kolata J, Goehler A, Weiss S, Holtfreter B, Bauerfeind SS, Döring P, Friebe E, Haasler N, Henselin K, Kühn K, Nowotny S, Radke D, Schulz K, Schulz SR, Trübe P, Vu CH, Walther B, Westphal S, Cuny C, Witte W, Völzke H, Grabe HJ, Kocher T, Steinmetz I, Bröker BM. Molecular epidemiology of Staphylococcus aureus in the general population in Northeast Germany: results of the study of health in Pomerania (SHIP-TREND-0). J Clin Microbiol. 2016;54(11):2774–85.CrossRef Holtfreter S, Grumann D, Balau V, Barwich A, Kolata J, Goehler A, Weiss S, Holtfreter B, Bauerfeind SS, Döring P, Friebe E, Haasler N, Henselin K, Kühn K, Nowotny S, Radke D, Schulz K, Schulz SR, Trübe P, Vu CH, Walther B, Westphal S, Cuny C, Witte W, Völzke H, Grabe HJ, Kocher T, Steinmetz I, Bröker BM. Molecular epidemiology of Staphylococcus aureus in the general population in Northeast Germany: results of the study of health in Pomerania (SHIP-TREND-0). J Clin Microbiol. 2016;54(11):2774–85.CrossRef
4.
go back to reference Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5(12):751–62.CrossRef Wertheim HF, Melles DC, Vos MC, van Leeuwen W, van Belkum A, Verbrugh HA, Nouwen JL. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infect Dis. 2005;5(12):751–62.CrossRef
5.
go back to reference Fowler VG Jr, Olsen MK, Corey GR, Woods CW, Cabell CH, Reller LB, Cheng AC, Dudley T, Oddone EZ. Clinical identifiers of complicated Staphylococcus aureus bacteremia. Arch Intern Med. 2003;163(17):2066–72.CrossRef Fowler VG Jr, Olsen MK, Corey GR, Woods CW, Cabell CH, Reller LB, Cheng AC, Dudley T, Oddone EZ. Clinical identifiers of complicated Staphylococcus aureus bacteremia. Arch Intern Med. 2003;163(17):2066–72.CrossRef
6.
go back to reference Chang FY, MacDonald BB, Peacock JE Jr, Musher DM, Triplett P, Mylotte JM, O'Donnell A, Wagener MM, Yu VL. A prospective multicenter study of Staphylococcus aureus bacteremia: incidence of endocarditis, risk factors for mortality, and clinical impact of methicillin resistance. Medicine (Baltimore). 2003;82(5):322–32.CrossRef Chang FY, MacDonald BB, Peacock JE Jr, Musher DM, Triplett P, Mylotte JM, O'Donnell A, Wagener MM, Yu VL. A prospective multicenter study of Staphylococcus aureus bacteremia: incidence of endocarditis, risk factors for mortality, and clinical impact of methicillin resistance. Medicine (Baltimore). 2003;82(5):322–32.CrossRef
7.
go back to reference von Eiff C, Becker K, Machka K, Stammer H, Peters G. Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med. 2001;344(1):11–6.CrossRef von Eiff C, Becker K, Machka K, Stammer H, Peters G. Nasal carriage as a source of Staphylococcus aureus bacteremia. Study Group. N Engl J Med. 2001;344(1):11–6.CrossRef
8.
go back to reference Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev. 1997;10(3):505–20.CrossRef Kluytmans J, van Belkum A, Verbrugh H. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin Microbiol Rev. 1997;10(3):505–20.CrossRef
9.
go back to reference Astor BC, Eustace JA, Powe NR, Klag MJ, Fink NE, Coresh J. Type of vascular access and survival among incident hemodialysis patients: the choices for healthy outcomes in caring for ESRD (CHOICE) study. J Am Soc Nephrol. 2005;16(5):1449–55.CrossRef Astor BC, Eustace JA, Powe NR, Klag MJ, Fink NE, Coresh J. Type of vascular access and survival among incident hemodialysis patients: the choices for healthy outcomes in caring for ESRD (CHOICE) study. J Am Soc Nephrol. 2005;16(5):1449–55.CrossRef
10.
go back to reference Lafrance JP, Rahme E, Lelorier J, Iqbal S. Vascular access-related infections: definitions, incidence rates, and risk factors. Am J Kidney Dis. 2008;52(5):982–93.CrossRef Lafrance JP, Rahme E, Lelorier J, Iqbal S. Vascular access-related infections: definitions, incidence rates, and risk factors. Am J Kidney Dis. 2008;52(5):982–93.CrossRef
11.
go back to reference Sarnak MJ, Jaber BL. Mortality caused by sepsis in patients with end-stage renal disease compared with the general population. Kidney Int. 2000;58(4):1758–64.CrossRef Sarnak MJ, Jaber BL. Mortality caused by sepsis in patients with end-stage renal disease compared with the general population. Kidney Int. 2000;58(4):1758–64.CrossRef
12.
go back to reference Layer F, Strommenger B, Cuny C, Werner G. Eigenschaften, Häufigkeit und Verbreitung von MRSA in Deutschland. Epid Bull. 2018;5:57–62. Layer F, Strommenger B, Cuny C, Werner G. Eigenschaften, Häufigkeit und Verbreitung von MRSA in Deutschland. Epid Bull. 2018;5:57–62.
13.
go back to reference Aghdassi S, Behnke M, Gastmeier P, Gropmann A, Hansen S, Diaz LA, Piening B, Rosenbusch M, Schröder C, Schwab F. Deutsche nationale Punkt-Prävalenzerhebung zu nosokomialen Infektionen und Antibiotika-Anwendung 2016: Abschlussbericht. Nationales Referenzzentrum für Surveillance von nosokomialen Infektionen; 2016. Aghdassi S, Behnke M, Gastmeier P, Gropmann A, Hansen S, Diaz LA, Piening B, Rosenbusch M, Schröder C, Schwab F. Deutsche nationale Punkt-Prävalenzerhebung zu nosokomialen Infektionen und Antibiotika-Anwendung 2016: Abschlussbericht. Nationales Referenzzentrum für Surveillance von nosokomialen Infektionen; 2016.
14.
go back to reference Köck R, Mellmann A, Schaumburg F, Friedrich AW, Kipp F, Becker K. Methicillin-resistenter Staphylococcus aureus in Deutschland. Dtsch Arztebl Int. 2011;108(45):761–7.PubMedPubMedCentral Köck R, Mellmann A, Schaumburg F, Friedrich AW, Kipp F, Becker K. Methicillin-resistenter Staphylococcus aureus in Deutschland. Dtsch Arztebl Int. 2011;108(45):761–7.PubMedPubMedCentral
15.
go back to reference Shopsin B, Gomez M, Montgomery SO, Smith DH, Waddington M, Dodge DE, Bost DA, Riehman M, Naidich S, Kreiswirth BN. Evaluation of protein a gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol. 1999;37(11):3556–63.PubMedPubMedCentral Shopsin B, Gomez M, Montgomery SO, Smith DH, Waddington M, Dodge DE, Bost DA, Riehman M, Naidich S, Kreiswirth BN. Evaluation of protein a gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains. J Clin Microbiol. 1999;37(11):3556–63.PubMedPubMedCentral
16.
go back to reference Monecke S, Slickers P, Ehricht R. Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol Med Microbiol. 2008;53(2):237–51.CrossRef Monecke S, Slickers P, Ehricht R. Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol Med Microbiol. 2008;53(2):237–51.CrossRef
17.
go back to reference Price A, Sarween N, Gupta I, Baharani J. Meticillin-resistant Staphylococcus aureus and meticillin-susceptible Staphylococcus aureus screening in a cohort of haemodialysis patients: carriage, demographics and outcomes. J Hosp Infect. 2015;90(1):22–7.CrossRef Price A, Sarween N, Gupta I, Baharani J. Meticillin-resistant Staphylococcus aureus and meticillin-susceptible Staphylococcus aureus screening in a cohort of haemodialysis patients: carriage, demographics and outcomes. J Hosp Infect. 2015;90(1):22–7.CrossRef
18.
go back to reference Zacharioudakis IM, Zervou FN, Ziakas PD, Mylonakis E. Meta-analysis of methicillin-resistant Staphylococcus aureus colonization and risk of infection in Dialysis patients. J Am Soc Nephrol. 2014;25:2131–41.CrossRef Zacharioudakis IM, Zervou FN, Ziakas PD, Mylonakis E. Meta-analysis of methicillin-resistant Staphylococcus aureus colonization and risk of infection in Dialysis patients. J Am Soc Nephrol. 2014;25:2131–41.CrossRef
19.
go back to reference Hübner NO, Dittmann K, Begunk R, Kramer A. Infection control measures and prevalence of multidrug-resistant organisms in non-hospital care settings in northeastern Germany: results from a one-day point prevalence study. J Hosp Infect. 2017;97(3):234–40.CrossRef Hübner NO, Dittmann K, Begunk R, Kramer A. Infection control measures and prevalence of multidrug-resistant organisms in non-hospital care settings in northeastern Germany: results from a one-day point prevalence study. J Hosp Infect. 2017;97(3):234–40.CrossRef
20.
go back to reference Neuhaus B, Bocter N, Braulke C, Heuck D, Witte W. Methicillin-resistente Staphylokokken: In Altenheimen ebenso häufig vertreten wie in Krankenhäusern. Dtsch Arztebl. 2003;100(45). Neuhaus B, Bocter N, Braulke C, Heuck D, Witte W. Methicillin-resistente Staphylokokken: In Altenheimen ebenso häufig vertreten wie in Krankenhäusern. Dtsch Arztebl. 2003;100(45).
21.
go back to reference Peacock SJ, de Silva GDI, Justice A, Cowland A, Moore CE, Winearls CG, Day NPJ. Comparison of multilocus sequence typing and pulsed-field gel electrophoresis as tools for typing Staphylococcus aureus isolates in a microepidemiological setting. J Clin Microbiol. 2002;40(10):3764–70.CrossRef Peacock SJ, de Silva GDI, Justice A, Cowland A, Moore CE, Winearls CG, Day NPJ. Comparison of multilocus sequence typing and pulsed-field gel electrophoresis as tools for typing Staphylococcus aureus isolates in a microepidemiological setting. J Clin Microbiol. 2002;40(10):3764–70.CrossRef
22.
go back to reference Herman-Bausier P, El-Kirat-Chatel S, Foster TJ, Geoghegan JA, Dufrêne YF. Staphylococcus aureus fibronectin-binding protein a mediates cell-cell adhesion through low-affinity Homophilic bonds. MBio. 2015;6(3):e00413–5.CrossRef Herman-Bausier P, El-Kirat-Chatel S, Foster TJ, Geoghegan JA, Dufrêne YF. Staphylococcus aureus fibronectin-binding protein a mediates cell-cell adhesion through low-affinity Homophilic bonds. MBio. 2015;6(3):e00413–5.CrossRef
23.
go back to reference Switalski LM, Patti JM, Butcher W, Gristina AG, Speziale P, Hook M. A collagen receptor on Staphylococcus aureus strains isolated from patients with septic arthritis mediates adhesion to cartilage. Mol Microbiol. 1993;7(1):99–107.CrossRef Switalski LM, Patti JM, Butcher W, Gristina AG, Speziale P, Hook M. A collagen receptor on Staphylococcus aureus strains isolated from patients with septic arthritis mediates adhesion to cartilage. Mol Microbiol. 1993;7(1):99–107.CrossRef
24.
go back to reference Lin Y, Wu P, Kuo M, Lin M, Lee T, Chiu Y, Hwang S, Chen HC. High cost and low survival rate in high comorbidity incident elderly hemodialysis patients. PLoS One. 2013;8(9):e75318.CrossRef Lin Y, Wu P, Kuo M, Lin M, Lee T, Chiu Y, Hwang S, Chen HC. High cost and low survival rate in high comorbidity incident elderly hemodialysis patients. PLoS One. 2013;8(9):e75318.CrossRef
25.
go back to reference Foster BJ, Mitsnefes MM, Dahhou M, Zhang X, Laskin BL. Changes in excess mortality from end stage renal disease in the United States from 1995 to 2013. Clin J Am Soc Nephrol. 2018;13(1):91–9.CrossRef Foster BJ, Mitsnefes MM, Dahhou M, Zhang X, Laskin BL. Changes in excess mortality from end stage renal disease in the United States from 1995 to 2013. Clin J Am Soc Nephrol. 2018;13(1):91–9.CrossRef
26.
go back to reference Bröker BM, Holtfreter S, Bekeredjian-Ding I. Immune control of Staphylococcus aureus - regulation and counter-regulation of the adaptive immune response. Int J Med Microbiol. 2014;304:204–14.CrossRef Bröker BM, Holtfreter S, Bekeredjian-Ding I. Immune control of Staphylococcus aureus - regulation and counter-regulation of the adaptive immune response. Int J Med Microbiol. 2014;304:204–14.CrossRef
27.
go back to reference van den Berg S, de Vogel CP, van Belkum A, Bakker-Woudenberg IAJM. Mild Staphylococcus aureus skin infection improves the course of subsequent Endogenous S. aureus bacteremia in mice. PLoS One. 2015;10(6):e0129150.CrossRef van den Berg S, de Vogel CP, van Belkum A, Bakker-Woudenberg IAJM. Mild Staphylococcus aureus skin infection improves the course of subsequent Endogenous S. aureus bacteremia in mice. PLoS One. 2015;10(6):e0129150.CrossRef
28.
go back to reference Stentzel S, Sundaramoorthy N, Michalik S, Nordengrün M, Schulz S, Kolata J, Kloppot P, Engelmann S, Steil L, Hecker M, Schmidt F, Völker U, Roghmann M-C, Bröker BM. Specific serum IgG at diagnosis of Staphylococcus aureus bloodstream invasion is correlated with disease progression. J Proteome. 2015;128:1–7.CrossRef Stentzel S, Sundaramoorthy N, Michalik S, Nordengrün M, Schulz S, Kolata J, Kloppot P, Engelmann S, Steil L, Hecker M, Schmidt F, Völker U, Roghmann M-C, Bröker BM. Specific serum IgG at diagnosis of Staphylococcus aureus bloodstream invasion is correlated with disease progression. J Proteome. 2015;128:1–7.CrossRef
29.
go back to reference Zamiah SS, Draman CR, Seman MR, Safhan AF, Rozalina R, Nik Ruzni NI. The cardiovascular risk factor profiles among end-stage renal failure patients treated with continuous ambulatory peritoneal dialysis and intermittent hemodialysis. Saudi J Kidney Dis Transpl. 2018;29:114–9.CrossRef Zamiah SS, Draman CR, Seman MR, Safhan AF, Rozalina R, Nik Ruzni NI. The cardiovascular risk factor profiles among end-stage renal failure patients treated with continuous ambulatory peritoneal dialysis and intermittent hemodialysis. Saudi J Kidney Dis Transpl. 2018;29:114–9.CrossRef
30.
go back to reference Wetmore JB, Molony JT, Liu J, Peng Y, Herzog CA, Collins AJ, Gilbertson DT. Readmissions following a hospitalization for cardiovascular events in Dialysis patients: a retrospective cohort study. J Am Heart Assoc. 2018;7(4):e007231.CrossRef Wetmore JB, Molony JT, Liu J, Peng Y, Herzog CA, Collins AJ, Gilbertson DT. Readmissions following a hospitalization for cardiovascular events in Dialysis patients: a retrospective cohort study. J Am Heart Assoc. 2018;7(4):e007231.CrossRef
31.
go back to reference Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective Nationwide surveillance study. Clin Infect Dis. 2004;39(3):309–17.CrossRef Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective Nationwide surveillance study. Clin Infect Dis. 2004;39(3):309–17.CrossRef
Metadata
Title
Staphylococcus aureus colonization in hemodialysis patients: a prospective 25 months observational study
Authors
Matthias Scheuch
Sabrina Freiin von Rheinbaben
Antje Kabisch
Jonas Engeßer
Susanne Ahrendt
Thomas Dabers
Christian Kohler
Silva Holtfreter
Barbara M. Bröker
Sylvia Stracke
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Nephrology / Issue 1/2019
Electronic ISSN: 1471-2369
DOI
https://doi.org/10.1186/s12882-019-1332-z

Other articles of this Issue 1/2019

BMC Nephrology 1/2019 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.