1887
Systematic Review Open Access
Like 0

Abstract

Background

Antimicrobial resistance (AMR) is of public health concern worldwide.

Aim

We aimed to summarise the German AMR situation for clinicians and microbiologists.

Methods

We conducted a systematic review and meta-analysis of 60 published studies and data from the German (ARS). Primary outcomes were AMR proportions in bacterial isolates from infected patients in Germany (2016–2021) and the case fatality rates (2010–2021). Random and fixed (common) effect models were used to calculate pooled proportions and pooled case fatality odds ratios, respectively.

Results

The pooled proportion of meticillin resistance in infections (MRSA) was 7.9% with a declining trend between 2014 and 2020 (odds ratio (OR) = 0.89; 95% CI: 0.886–0.891; p < 0.0001), while vancomycin resistance in (VRE) bloodstream infections increased (OR = 1.18; (95% CI: 1.16–1.21); p < 0.0001) with a pooled proportion of 34.9%. Case fatality rates for MRSA and VRE were higher than for their susceptible strains (OR = 2.29; 95% CI: 1.91–2.75 and 1.69; 95% CI: 1.22–2.33, respectively). Carbapenem resistance in Gram-negative pathogens (, , spp. and ) was low to moderate (< 9%), but resistance against third-generation cephalosporins and fluoroquinolones was moderate to high (5–25%). exhibited high resistance against carbapenems (17.0%; 95% CI: 11.9–22.8), third-generation cephalosporins (10.1%; 95% CI: 6.6–14.2) and fluoroquinolones (24.9%; 95% CI: 19.3–30.9). Statistical heterogeneity was high (I2 > 70%) across studies reporting resistance proportions.

Conclusion

Continuous efforts in AMR surveillance and infection prevention and control as well as antibiotic stewardship are needed to limit the spread of AMR in Germany.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2023.28.20.2200672
2023-05-18
2024-06-22
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2023.28.20.2200672
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/28/20/eurosurv-28-20-3.html?itemId=/content/10.2807/1560-7917.ES.2023.28.20.2200672&mimeType=html&fmt=ahah

References

  1. Morehead MS, Scarbrough C. Emergence of global antibiotic resistance. Prim Care. 2018;45(3):467-84.  https://doi.org/10.1016/j.pop.2018.05.006  PMID: 30115335 
  2. Murray CJL, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G, Gray A, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629-55.  https://doi.org/10.1016/S0140-6736(21)02724-0  PMID: 35065702 
  3. Cassini A, Högberg LD, Plachouras D, Quattrocchi A, Hoxha A, Simonsen GS, et al. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis. Lancet Infect Dis. 2019;19(1):56-66.  https://doi.org/10.1016/S1473-3099(18)30605-4  PMID: 30409683 
  4. Ayobami O, Brinkwirth S, Eckmanns T, Markwart R. Antibiotic resistance in hospital-acquired ESKAPE-E infections in low- and lower-middle-income countries: a systematic review and meta-analysis. Emerg Microbes Infect. 2022;11(1):443-51.  https://doi.org/10.1080/22221751.2022.2030196  PMID: 35034585 
  5. Ayobami O, Willrich N, Reuss A, Eckmanns T, Markwart R. The ongoing challenge of vancomycin-resistant Enterococcus faecium and Enterococcus faecalis in Europe: an epidemiological analysis of bloodstream infections. Emerg Microbes Infect. 2020;9(1):1180-93.  https://doi.org/10.1080/22221751.2020.1769500  PMID: 32498615 
  6. Bundesministerium für Gesundheit (BMG). DART 2020: Fighting antibiotic resistance for the good of both humans and animals. Bonn: BMG. Accessed: 17 May 2022]. Available from: https://www.bundesgesundheitsministerium.de/fileadmin/Dateien/5_Publikationen/Gesundheit/Berichte/BMG_DART_2020_Bericht_en.pdf
  7. Robert Koch Institute (RKI). ARS - Antibiotika-Resistenz-Surveillance. Berlin: RKI. [Accessed: 25 Jun 2022]. Available from: https://ars.rki.de
  8. Noll I, Schweickert B, Abu Sin M, Feig M, Claus H, Eckmanns T. [Antimicrobial resistance in Germany. Four years of antimicrobial resistance surveillance (ARS)]. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2012;55(11-12):1370-6. German.  https://doi.org/10.1007/s00103-012-1559-3  PMID: 23114435 
  9. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;372(71):n71.  https://doi.org/10.1136/bmj.n71  PMID: 33782057 
  10. Markwart R, Roedenbeck M. The epidemiology and burden of antibiotic resistances in clinical infections in Germany: a systematic review and meta-analysis. PROSPERO 2022 CRD42022306576. Available from: https://www.crd.york.ac.uk/prospero/display_record.php?ID=CRD42022306576
  11. Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M, Monnet DL, et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis. 2018;18(3):318-27.  https://doi.org/10.1016/S1473-3099(17)30753-3  PMID: 29276051 
  12. Barendregt JJ, Doi SA, Lee YY, Norman RE, Vos T. Meta-analysis of prevalence. J Epidemiol Community Health. 2013;67(11):974-8.  https://doi.org/10.1136/jech-2013-203104  PMID: 23963506 
  13. Greenland S, Robins JM. Estimation of a common effect parameter from sparse follow-up data. Biometrics. 1985;41(1):55-68.  https://doi.org/10.2307/2530643  PMID: 4005387 
  14. Hoy D, Brooks P, Woolf A, Blyth F, March L, Bain C, et al. Assessing risk of bias in prevalence studies: modification of an existing tool and evidence of interrater agreement. J Clin Epidemiol. 2012;65(9):934-9.  https://doi.org/10.1016/j.jclinepi.2011.11.014  PMID: 22742910 
  15. Wells GA, Shea B, O’Connell D, Peterson J, Welch V, Losos M, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa: Ottawa Hospital Research Institute. [Accessed: 18 Jan 2022]. Available from: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
  16. R Core Team. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. [Accessed: 18 Mar 2022]. Available from: https://www.r-project.org
  17. Schwarzer G, Carpenter JR, Rücker G. Meta-analysis with R. Springer International Publishing Switzerland; 2015. ISBN: 978-3-319-21416-0.
  18. Schwarzer G. Meta: An R package for meta-analysis. R News. 2007;7:40-5. Available from: https://cran.r-project.org/doc/Rnews/Rnews_2007-3.pdf
  19. Abdrabou AMM, Ul Habib Bajwa Z, Halfmann A, Mellmann A, Nimmesgern A, Margardt L, et al. Molecular epidemiology and antimicrobial resistance of Clostridioides difficile in Germany, 2014-2019. Int J Med Microbiol. 2021;311(4):151507.  https://doi.org/10.1016/j.ijmm.2021.151507  PMID: 33915347 
  20. Banhart S, Selb R, Oehlmann S, Bender J, Buder S, Jansen K, et al. The Mosaic mtr locus as major genetic determinant of azithromycin resistance of Neisseria gonorrhoeae-Germany, 2018. J Infect Dis. 2021;224(8):1398-404.  https://doi.org/10.1093/infdis/jiab091  PMID: 33592101 
  21. Abo Basha J, Kiel M, Görlich D, Schütte-Nütgen K, Witten A, Pavenstädt H, et al. Phenotypic and genotypic characterization of Escherichia coli causing urinary tract infections in kidney-transplanted patients. J Clin Med. 2019;8(7):8.  https://doi.org/10.3390/jcm8070988  PMID: 31284699 
  22. Doenhardt M, Seipolt B, Mense L, Winkler JL, Thürmer A, Rüdiger M, et al. Neonatal and young infant sepsis by Group B Streptococci and Escherichia coli: a single-center retrospective analysis in Germany-GBS screening implementation gaps and reduction in antibiotic resistance. Eur J Pediatr. 2020;179(11):1769-77.  https://doi.org/10.1007/s00431-020-03659-8  PMID: 32447562 
  23. Dörr S, Holland-Letz AK, Weisser G, Chatzitomaris A, Lobmann R. Bacterial diversity, antibiotic resistance, and the risk of lower limb amputation in younger and older individuals with diabetic foot infection. Int J Low Extrem Wounds. 2023;22(1):63-71.  https://doi.org/10.1177/1534734621992290  PMID: 33745353 
  24. Dubler S, Lenz M, Zimmermann S, Richter DC, Weiss KH, Mehrabi A, et al. Does vancomycin resistance increase mortality in Enterococcus faecium bacteraemia after orthotopic liver transplantation? A retrospective study. Antimicrob Resist Infect Control. 2020;9(1):22.  https://doi.org/10.1186/s13756-020-0683-3  PMID: 32005223 
  25. Frickmann H, Hahn A, Berlec S, Ulrich J, Jansson M, Schwarz NG, et al. On the etiological relevance of Escherichia coli and Staphylococcus aureus in superficial and deep infections - a hypothesis-forming, retrospective assessment. Eur J Microbiol Immunol (Bp). 2019;9(4):124-30.  https://doi.org/10.1556/1886.2019.00021  PMID: 31934364 
  26. Friesen J, Neuber R, Fuhrmann J, Kietzmann H, Wenzel T, Schaumburg F, et al. Panton-Valentine leukocidin-positive Staphylococcus aureus in skin and soft tissue infections from primary care patients. Clin Microbiol Infect. 2020;26(10):1416.e1-4.  https://doi.org/10.1016/j.cmi.2020.06.029  PMID: 32619735 
  27. Große K, Ohm D, Würstle S, Brozat JF, Schmid RM, Trautwein C, et al. Clinical characteristics and outcome of patients with enterococcal liver abscess. Sci Rep. 2021;11(1):22265.  https://doi.org/10.1038/s41598-021-01620-9  PMID: 34782684 
  28. Grotelueschen R, Luetgehetmann M, Erbes J, Heidelmann LM, Grupp K, Karstens K, et al. Microbial findings, sensitivity and outcome in patients with postoperative peritonitis a retrospective cohort study. Int J Surg. 2019;70:63-9.  https://doi.org/10.1016/j.ijsu.2019.08.020  PMID: 31437641 
  29. Gudiol C, Albasanz-Puig A, Laporte-Amargós J, Pallarès N, Mussetti A, Ruiz-Camps I, et al. Clinical predictive model of multidrug resistance in neutropenic cancer patients with bloodstream infection due to Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2020;64(4):64.  https://doi.org/10.1128/AAC.02494-19  PMID: 32015035 
  30. Hischebeth GT, Randau TM, Ploeger MM, Friedrich MJ, Kaup E, Jacobs C, et al. Staphylococcus aureus versus Staphylococcus epidermidis in periprosthetic joint infection-Outcome analysis of methicillin-resistant versus methicillin-susceptible strains. Diagn Microbiol Infect Dis. 2019;93(2):125-30.  https://doi.org/10.1016/j.diagmicrobio.2018.08.012  PMID: 30266398 
  31. Hitzenbichler F, Simon M, Holzmann T, Iberer M, Zimmermann M, Salzberger B, et al. Antibiotic resistance in E. coli isolates from patients with urinary tract infections presenting to the emergency department. Infection. 2018;46(3):325-31.  https://doi.org/10.1007/s15010-018-1117-5  PMID: 29368165 
  32. Hoppe PA, Hanitsch LG, Leistner R, Niebank M, Bührer C, von Bernuth H, et al. Periorbital infections and conjunctivitis due to Panton-valentine leukocidin (PVL) positive Staphylococcus aureus in children. BMC Infect Dis. 2018;18(1):371.  https://doi.org/10.1186/s12879-018-3281-8  PMID: 30081842 
  33. Hos NJ, Jazmati N, Stefanik D, Hellmich M, AlSael H, Kern WV, et al. Determining vancomycin Etest MICs in patients with MRSA bloodstream infection does not support switching antimicrobials. J Infect. 2017;74(3):248-59.  https://doi.org/10.1016/j.jinf.2016.12.007  PMID: 28017826 
  34. Jarlier V, Diaz Högberg L, Heuer OE, Campos J, Eckmanns T, Giske CG, et al. Strong correlation between the rates of intrinsically antibiotic-resistant species and the rates of acquired resistance in Gram-negative species causing bacteraemia, EU/EEA, 2016. Euro Surveill. 2019;24(33):1800538.  https://doi.org/10.2807/1560-7917.ES.2019.24.33.1800538  PMID: 31431208 
  35. Klasan A, Schermuksnies A, Gerber F, Bowman M, Fuchs-Winkelmann S, Heyse TJ. Development of antibiotic resistance in periprosthetic joint infection after total knee arthroplasty. Bone Joint J. 2021;103-B(6) Supple A;171-6.  https://doi.org/10.1302/0301-620X.103B6.BJJ-2020-1923.R1  PMID: 34053285 
  36. Klein S, Menz MD, Zanger P, Heeg K, Nurjadi D. Increase in the prevalence of panton-valentine leukocidin and clonal shift in community-onset methicillin-resistant Staphylococcus aureus causing skin and soft-tissue infections in the Rhine-Neckar Region, Germany, 2012-2016. Int J Antimicrob Agents. 2019;53(3):261-7.  https://doi.org/10.1016/j.ijantimicag.2018.10.026  PMID: 30412736 
  37. Klingeberg A, Noll I, Willrich N, Feig M, Emrich D, Zill E, et al. Antibiotic-resistant E. coli in uncomplicated community-acquired urinary tract infection. Dtsch Arztebl Int. 2018;115(29-30):494-500.  https://doi.org/10.3238/arztebl.2018.0494  PMID: 30135009 
  38. Koppe U, von Laer A, Kroll LE, Noll I, Feig M, Schneider M, et al. Carbapenem non-susceptibility of Klebsiella pneumoniae isolates in hospitals from 2011 to 2016, data from the German Antimicrobial Resistance Surveillance (ARS). Antimicrob Resist Infect Control. 2018;7(1):71.  https://doi.org/10.1186/s13756-018-0362-9  PMID: 29992016 
  39. Köstlin-Gille N, Härtel C, Haug C, Göpel W, Zemlin M, Müller A, et al. Epidemiology of early and late onset neonatal sepsis in very low birthweight infants. Pediatr Infect Dis J. 2021;40(3):255-9.  https://doi.org/10.1097/INF.0000000000002976  PMID: 33538544 
  40. Kramer TS, Remschmidt C, Werner S, Behnke M, Schwab F, Werner G, et al. The importance of adjusting for enterococcus species when assessing the burden of vancomycin resistance: a cohort study including over 1000 cases of enterococcal bloodstream infections. Antimicrob Resist Infect Control. 2018;7(1):133.  https://doi.org/10.1186/s13756-018-0419-9  PMID: 30459945 
  41. Kramer TS, Schröder C, Behnke M, Aghdassi SJ, Geffers C, Gastmeier P, et al. Decrease of methicillin resistance in Staphylococcus aureus in nosocomial infections in Germany-a prospective analysis over 10 years. J Infect. 2019;78(3):215-9.  https://doi.org/10.1016/j.jinf.2018.12.005  PMID: 30658080 
  42. Kramer TS, Schwab F, Behnke M, Hansen S, Gastmeier P, Aghdassi SJS. Linezolid use in German acute care hospitals: results from two consecutive national point prevalence surveys. Antimicrob Resist Infect Control. 2019;8(1):159.  https://doi.org/10.1186/s13756-019-0617-0  PMID: 31649816 
  43. Kresken M, Körber-Irrgang B, Korte-Berwanger M, Pfennigwerth N, Gatermann SG, Seifert H, et al. Dissemination of carbapenem-resistant Pseudomonas aeruginosa isolates and their susceptibilities to ceftolozane-tazobactam in Germany. Int J Antimicrob Agents. 2020;55(6):105959.  https://doi.org/10.1016/j.ijantimicag.2020.105959  PMID: 32325200 
  44. Lackermair S, Egermann H, Müller A. Distribution of underlying causative organisms, patient age, and survival in spontaneous spondylodiscitis with special focus on elderly patients. J Neurol Surg A Cent Eur Neurosurg. 2023;84(1):8-13.  https://doi.org/10.1055/s-0040-1721005  PMID: 33583009 
  45. Lâm TT, Nürnberg S, Claus H, Vogel U. Molecular epidemiology of imipenem resistance in invasive Haemophilus influenzae infections in Germany in 2016. J Antimicrob Chemother. 2020;75(8):2076-86. PMID: 32449913 
  46. Leistner R, Gürntke S, Sakellariou C, Denkel LA, Bloch A, Gastmeier P, et al. Bloodstream infection due to extended-spectrum beta-lactamase (ESBL)-positive K. pneumoniae and E. coli: an analysis of the disease burden in a large cohort. Infection. 2014;42(6):991-7.  https://doi.org/10.1007/s15010-014-0670-9  PMID: 25100555 
  47. Markwart R, Willrich N, Haller S, Noll I, Koppe U, Werner G, et al. The rise in vancomycin-resistant Enterococcus faecium in Germany: data from the German Antimicrobial Resistance Surveillance (ARS). Antimicrob Resist Infect Control. 2019;8(1):147.  https://doi.org/10.1186/s13756-019-0594-3  PMID: 31485325 
  48. Meinen A, Reuss A, Willrich N, Feig M, Noll I, Eckmanns T, et al. Antimicrobial resistance and the spectrum of pathogens in dental and oral-maxillofacial infections in hospitals and dental practices in Germany. Front Microbiol. 2021;12:676108.  https://doi.org/10.3389/fmicb.2021.676108  PMID: 34149666 
  49. Meyer E, Schwab F, Gastmeier P. Nosocomial methicillin resistant Staphylococcus aureus pneumonia - epidemiology and trends based on data of a network of 586 German ICUs (2005-2009). Eur J Med Res. 2010;15(12):514-24.  https://doi.org/10.1186/2047-783X-15-12-514  PMID: 21163726 
  50. Michelson K, Löffler B, Höring S. Time to positivity as a prognostic factor in bloodstream infections with Enterococcus spp. Diagn Microbiol Infect Dis. 2021;101(3):115396.  https://doi.org/10.1016/j.diagmicrobio.2021.115396  PMID: 34325178 
  51. Mutters NT, Brooke RJ, Frank U, Heeg K. Low risk of apparent transmission of vancomycin-resistant Enterococci from bacteraemic patients to hospitalized contacts. Am J Infect Control. 2013;41(9):778-81.  https://doi.org/10.1016/j.ajic.2012.11.019  PMID: 23453393 
  52. Neubeiser A, Bonsignore M, Tafelski S, Alefelder C, Schwegmann K, Rüden H, et al. Mortality attributable to hospital acquired infections with multidrug-resistant bacteria in a large group of German hospitals. J Infect Public Health. 2020;13(2):204-10.  https://doi.org/10.1016/j.jiph.2019.07.025  PMID: 31420314 
  53. Nurjadi D, Klein S, Hannesen J, Heeg K, Boutin S, Zanger P. Molecular analysis of an increase in trimethoprim/sulfamethoxazole-resistant MRSA reveals multiple introductions into a tertiary care hospital, Germany 2012-19. J Antimicrob Chemother. 2021;77(1):38-48.  https://doi.org/10.1093/jac/dkab341  PMID: 34529777 
  54. Nürnberg S, Claus H, Krone M, Vogel U, Lâm TT. Cefotaxime resistance in invasive Haemophilus influenzae isolates in Germany 2016-19: prevalence, epidemiology and relevance of PBP3 substitutions. J Antimicrob Chemother. 2021;76(4):920-9.  https://doi.org/10.1093/jac/dkaa557  PMID: 33501993 
  55. Olearo F, Both A, Belmar Campos C, Hilgarth H, Klupp EM, Hansen JL, et al. Emergence of linezolid-resistance in vancomycin-resistant Enterococcus faecium ST117 associated with increased linezolid-consumption. Int J Med Microbiol. 2021;311(2):151477.  https://doi.org/10.1016/j.ijmm.2021.151477  PMID: 33524636 
  56. Perniciaro S, Imöhl M, van der Linden M. Invasive pneumococcal disease in refugee children, Germany. Emerg Infect Dis. 2018;24(10):1934-6.  https://doi.org/10.3201/eid2410.180253  PMID: 30226179 
  57. Pietsch M, Simon S, Meinen A, Trost E, Banerji S, Pfeifer Y, et al. Third generation cephalosporin resistance in clinical non-typhoidal Salmonella enterica in Germany and emergence of blaCTX-M-harbouring pESI plasmids. Microb Genom. 2021;7(10):7.  https://doi.org/10.1099/mgen.0.000698  PMID: 34693903 
  58. Remschmidt C, Schröder C, Behnke M, Gastmeier P, Geffers C, Kramer TS. Continuous increase of vancomycin resistance in enterococci causing nosocomial infections in Germany - 10 years of surveillance. Antimicrob Resist Infect Control. 2018;7(1):54.  https://doi.org/10.1186/s13756-018-0353-x  PMID: 29760912 
  59. Rhim HY, Won SY, Kashefiolasl S, Brawanski N, Hattingen E, Berkefeld J, et al. Multidrug-resistant organisms (MDROs) in patients with subarachnoid hemorrhage (SAH). Sci Rep. 2021;11(1):8309.  https://doi.org/10.1038/s41598-021-87863-y  PMID: 33859304 
  60. Rothe K, Wantia N, Spinner CD, Schneider J, Lahmer T, Waschulzik B, et al. Antimicrobial resistance of bacteraemia in the emergency department of a German university hospital (2013-2018): potential carbapenem-sparing empiric treatment options in light of the new EUCAST recommendations. BMC Infect Dis. 2019;19(1):1091.  https://doi.org/10.1186/s12879-019-4721-9  PMID: 31888581 
  61. Rupp M, Baertl S, Walter N, Hitzenbichler F, Ehrenschwender M, Alt V. Is there a difference in microbiological epidemiology and effective empiric antimicrobial therapy comparing fracture-related infection and periprosthetic joint infection? A retrospective comparative study. Antibiotics (Basel). 2021;10(8):10.  https://doi.org/10.3390/antibiotics10080921  PMID: 34438971 
  62. Said D, Willrich N, Ayobami O, Noll I, Eckmanns T, Markwart R. The epidemiology of carbapenem resistance in Acinetobacter baumannii complex in Germany (2014-2018): an analysis of data from the national Antimicrobial Resistance Surveillance system. Antimicrob Resist Infect Control. 2021;10(1):45.  https://doi.org/10.1186/s13756-021-00909-8  PMID: 33648594 
  63. Sakellariou C, Gürntke S, Steinmetz I, Kohler C, Pfeifer Y, Gastmeier P, et al. Sepsis caused by extended-spectrum beta-lactamase (ESBL)-positive K. pneumoniae and E. coli: comparison of severity of sepsis, delay of anti-infective therapy and ESBL genotype. PLoS One. 2016;11(7):e0158039.  https://doi.org/10.1371/journal.pone.0158039  PMID: 27442425 
  64. Scheich S, Weber S, Reinheimer C, Wichelhaus TA, Hogardt M, Kempf VAJ, et al. Bloodstream infections with gram-negative organisms and the impact of multidrug resistance in patients with hematological malignancies. Ann Hematol. 2018;97(11):2225-34.  https://doi.org/10.1007/s00277-018-3423-5  PMID: 29974230 
  65. Schneider SM, Schaeg M, Gärtner BC, Berger FK, Becker SL. Do written diagnosis-treatment recommendations on microbiological test reports improve the management of Staphylococcus aureus bacteremia? A single-center, retrospective, observational study. Diagn Microbiol Infect Dis. 2020;98(4):115170.  https://doi.org/10.1016/j.diagmicrobio.2020.115170  PMID: 32911296 
  66. Schöneweck F, Schmitz RPH, Rißner F, Scherag A, Löffler B, Pletz MW, et al. The epidemiology of bloodstream infections and antimicrobial susceptibility patterns in Thuringia, Germany: a five-year prospective, state-wide surveillance study (AlertsNet). Antimicrob Resist Infect Control. 2021;10(1):132.  https://doi.org/10.1186/s13756-021-00997-6  PMID: 34493334 
  67. Seitz M, Stief C, Waidelich R. Local epidemiology and resistance profiles in acute uncomplicated cystitis (AUC) in women: a prospective cohort study in an urban urological ambulatory setting. BMC Infect Dis. 2017;17(1):685.  https://doi.org/10.1186/s12879-017-2789-7  PMID: 29037164 
  68. Selb R, Buder S, Dudareva S, Tamminga T, Bremer V, Banhart S, et al. Markedly decreasing azithromycin susceptibility of Neisseria gonorrhoeae, Germany, 2014 to 2021. Euro Surveill. 2021;26(31):26.  https://doi.org/10.2807/1560-7917.ES.2021.26.31.2100616  PMID: 34355690 
  69. Suwono B, Eckmanns T, Kaspar H, Merle R, Zacher B, Kollas C, et al. Cluster analysis of resistance combinations in Escherichia coli from different human and animal populations in Germany 2014-2017. PLoS One. 2021;16(1):e0244413.  https://doi.org/10.1371/journal.pone.0244413  PMID: 33471826 
  70. Tessema B, Lippmann N, Knüpfer M, Sack U, König B. Antibiotic resistance patterns of bacterial isolates from neonatal sepsis patients at university hospital of Leipzig, Germany. Antibiotics (Basel). 2021;10(3):10.  https://doi.org/10.3390/antibiotics10030323  PMID: 33808878 
  71. Theodorou P, Lefering R, Perbix W, Spanholtz TA, Maegele M, Spilker G, et al. Staphylococcus aureus bacteremia after thermal injury: the clinical impact of methicillin resistance. Burns. 2013;39(3):404-12.  https://doi.org/10.1016/j.burns.2012.12.006  PMID: 23313016 
  72. Theodorou P, Thamm OC, Perbix W, Phan VT. Pseudomonas aeruginosa bacteremia after burn injury: the impact of multiple-drug resistance. J Burn Care Res. 2013;34(6):649-58.  https://doi.org/10.1097/BCR.0b013e318280e2c7  PMID: 23817000 
  73. Walker SV, Wolke M, Plum G, Weber RE, Werner G, Hamprecht A. Failure of Vitek2 to reliably detect vanB-mediated vancomycin resistance in Enterococcus faecium. J Antimicrob Chemother. 2021;76(7):1698-702.  https://doi.org/10.1093/jac/dkab101  PMID: 33855441 
  74. Walter J, Haller S, Blank HP, Eckmanns T, Abu Sin M, Hermes J. Incidence of invasive meticillin-resistant Staphylococcus aureus infections in Germany, 2010 to 2014. Euro Surveill. 2015;20(46):30067.  https://doi.org/10.2807/1560-7917.ES.2015.20.46.30067  PMID: 26607355 
  75. Weber S, Hogardt M, Reinheimer C, Wichelhaus TA, Kempf VAJ, Kessel J, et al. Bloodstream infections with vancomycin-resistant enterococci are associated with a decreased survival in patients with hematological diseases. Ann Hematol. 2019;98(3):763-73.  https://doi.org/10.1007/s00277-019-03607-z  PMID: 30666433 
  76. Wilke MH, Becker K, Kloss S, Heimann SM, Goldmann A, Weber B, et al. Treatment of MRSA pneumonia: Clinical and economic comparison of linezolid vs. vancomycin - a retrospective analysis of medical charts and re-imbursement data of real-life patient populations. GMS Infect Dis. 2017;5:Doc02. PMID: 30671324 
  77. Willmann M, Kuebart I, Marschal M, Schröppel K, Vogel W, Flesch I, et al. Effect of metallo-β-lactamase production and multidrug resistance on clinical outcomes in patients with Pseudomonas aeruginosa bloodstream infection: a retrospective cohort study. BMC Infect Dis. 2013;13(1):515.  https://doi.org/10.1186/1471-2334-13-515  PMID: 24176052 
  78. Yayan J, Ghebremedhin B, Rasche K. No outbreak of vancomycin and linezolid resistance in staphylococcal pneumonia over a 10-year period. PLoS One. 2015;10(9):e0138895.  https://doi.org/10.1371/journal.pone.0138895  PMID: 26398276 
  79. Navidinia M. The clinical importance of emerging ESKAPE pathogens in nosocomial infections. Archives of Advances in Biosciences.2016;7(3):43-57.  https://doi.org/10.22037/jps.v7i3.12584 
  80. Puchter L, Chaberny IF, Schwab F, Vonberg RP, Bange FC, Ebadi E. Economic burden of nosocomial infections caused by vancomycin-resistant enterococci. Antimicrob Resist Infect Control. 2018;7(1):1.  https://doi.org/10.1186/s13756-017-0291-z  PMID: 29312658 
  81. Kommission für Krankenhaushygiene und Infektionsprävention (KRINKO) beim Robert Koch-Institut. Hygienemaßnahmen zur Prävention der Infektion durch Enterokokken mit speziellen Antibiotikaresistenzen. [Hygiene measures for the prevention of enterococcal infections with specific antibiotic resistances]. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2018;61(10):1310-61. German.  https://doi.org/10.1007/s00103-018-2811-2 
  82. Markwart R, Willrich N, Eckmanns T, Werner G, Ayobami O. Low proportion of linezolid and daptomycin resistance among bloodborne vancomycin-resistant Enterococcus faecium and methicillin-resistant Staphylococcus aureus infections in Europe. Front Microbiol. 2021;12:664199.  https://doi.org/10.3389/fmicb.2021.664199  PMID: 34135877 
  83. European Centre for Disease Prevention and Control (ECDC). Antimicrobial resistance in the EU/EEA (EARS-Net) - Annual Epidemiological Report for 2020. Stockholm: ECDC; 2022. Available from: https://www.ecdc.europa.eu/en/publications-data/antimicrobial-resistance-eueea-ears-net-annual-epidemiological-report-2020
  84. Lee AS, de Lencastre H, Garau J, Kluytmans J, Malhotra-Kumar S, Peschel A, et al. Methicillin-resistant Staphylococcus aureus. Nat Rev Dis Primers. 2018;4(1):18033.  https://doi.org/10.1038/nrdp.2018.33  PMID: 29849094 
  85. Tübbicke A, Hübner C, Kramer A, Hübner NO, Fleßa S. Transmission rates, screening methods and costs of MRSA--a systematic literature review related to the prevalence in Germany. Eur J Clin Microbiol Infect Dis. 2012;31(10):2497-511.  https://doi.org/10.1007/s10096-012-1632-8  PMID: 22573360 
  86. Kommission für Krankenhaushygiene und Infektionsprävention (KRINKO) beim Robert Koch-Institut. Empfehlungen zur Prävention und Kontrolle von Methicillin resistenten Staphylococcus aureus-Stämmen (MRSA) in medizinischen und pflegerischen Einrichtungen. [Recommendations for the prevention and control of meticillin-resistant Staphylococcus aureus strains (MRSA) in medical and nursing facilities]. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2018;61(10):1310-61. German.  https://doi.org/10.1007/s00103-018-2811-2 
  87. Driscoll JA, Brody SL, Kollef MH. The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs. 2007;67(3):351-68.  https://doi.org/10.2165/00003495-200767030-00003  PMID: 17335295 
  88. Archibald L, Phillips L, Monnet D, McGowan JE Jr, Tenover F, Gaynes R. Antimicrobial resistance in isolates from inpatients and outpatients in the United States: increasing importance of the intensive care unit. Clin Infect Dis. 1997;24(2):211-5.  https://doi.org/10.1093/clinids/24.2.211  PMID: 9114149 
  89. Holstiege J, Schulz M, Akmatov MK, Kern WV, Steffen A, Bätzing J. The decline in outpatient antibiotic use. Dtsch Arztebl Int. 2020;117(41):679-86. PMID: 33357337 
  90. Murray CJL, Ikuta KS, Sharara F, Swetschinski L, Robles Aguilar G, Gray A, et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet. 2022;399(10325):629-55.  https://doi.org/10.1016/S0140-6736(21)02724-0  PMID: 35065702 
  91. Brinkwirth S, Ayobami O, Eckmanns T, Markwart R. Hospital-acquired infections caused by enterococci: a systematic review and meta-analysis, WHO European Region, 1 January 2010 to 4 February 2020. Euro Surveill. 2021;26(45):2001628.  https://doi.org/10.2807/1560-7917.ES.2021.26.45.2001628  PMID: 34763754 
  92. Collignon P, Beggs JJ, Walsh TR, Gandra S, Laxminarayan R. Anthropological and socioeconomic factors contributing to global antimicrobial resistance: a univariate and multivariable analysis. Lancet Planet Health. 2018;2(9):e398-405.  https://doi.org/10.1016/S2542-5196(18)30186-4  PMID: 30177008 
  93. European Committee on Antimicrobial Susceptibility Testing (EUCAST). New definitions of S, I and R from 2019. Växjö: EUCAST. [Accessed: 19 May 2022]. Available from: https://www.eucast.org/newsiandr
  94. Klingeberg A, Noll I, Willrich N, Feig M, Emrich D, Zill E, et al. Antibiotikaresistenz von E. coli bei ambulant erworbener unkomplizierter Harnwegsinfektion. Eine prospektive Kohortenstudie der Jahre 2015/2016 (SARHA-Studie) im Vergleich mit Daten der Antibiotika-Resistenz-Surveillance (ARS). [Antibiotic resistance of E. coli in community-acquired uncomplicated urinary tract infections. A prospective cohort study from 2015/2016 (SARHA study) compared with data from Antibiotic-Resistance-Surveillance (ARS)]. Dtsch Arztebl. 2018;115:494-500. German.
  95. Robert Koch-Institute (RKI). Antibiotika Resistenz Surveillance Datenbank. [Antibiotic-Resistance-Surveillance database]. Berlin: RKI; [Accessed: 7 Apr 2022]. Available from: https://ars.rki.de/Content/Database/Main.aspx
  96. Jafari M, Ansari-Pour N. Why, when and how to adjust your p values? Cell J. 2019;20(4):604-7. PMID: 30124010 
  97. Centers for Disease Control and Prevention (CDC). Antibiotic Resistance & Patient Safety Portal. Atlanta: CDC. [Accessed: 9 May 2023]. Available from: https://arpsp.cdc.gov/profile/antibiotic-resistance?tab=antibiotic-resistance
  98. Kajihara T, Yahara K, Hirabayashi A, Shibayama K, Sugai M. Japan Nosocomial Infections Surveillance (JANIS): current status, international collaboration, and future directions for a comprehensive antimicrobial resistance surveillance system. Jpn J Infect Dis. 2021;74(2):87-96.  https://doi.org/10.7883/yoken.JJID.2020.499  PMID: 32863357 
  99. Hu F, Wang M, Zhu D, Wang F. CHINET efforts to control antimicrobial resistance in China. J Glob Antimicrob Resist. 2020;21:76-7.  https://doi.org/10.1016/j.jgar.2020.03.007  PMID: 32205265 
/content/10.2807/1560-7917.ES.2023.28.20.2200672
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error