Prevalence and risk factors of infections by multiresistant bacteria in cirrhosis: A prospective study
Open accessAbstract
Epidemiology, risk factors, and clinical effect of infections by multiresistant bacteria in cirrhosis are poorly known. This work was a prospective evaluation in two series of cirrhotic patients admitted with infection or developing infection during hospitalization. The first series was studied between 2005 and 2007 (507 bacterial infections in 223 patients) and the second between 2010 and 2011 (162 bacterial infections in 110 patients). In the first series, 32% of infections were community acquired (CA), 32% healthcare associated (HCA), and 36% nosocomial. Multiresistant bacteria (92 infections; 18%) were isolated in 4%, 14%, and 35% of these infections, respectively ( P < 0.001). Extended-spectrum β-lactamase-producing Enterobacteriaceae (ESBL - E ; n = 43) was the main multiresistant organism identified, followed by Pseudomonas aeruginosa (n = 17), methicillin-resistant Staphylococcus aureus (n = 14), and Enterococcus faecium (n = 14). The efficacy of currently recommended empirical antibiotic therapy was very low in nosocomial infections (40%), compared to HCA and CA episodes (73% and 83%, respectively; P < 0.0001), particularly in spontaneous bacterial peritonitis, urinary tract infection, and pneumonia (26%, 29%, and 44%, respectively). Septic shock (26% versus 10%; P < 0.0001) and mortality rate (25% versus 12%; P = 0.001) were significantly higher in infections caused by multiresistant strains. Nosocomial origin of infection (hazard ratio [HR], 4.43), long-term norfloxacin prophylaxis (HR, 2.69), recent infection by multiresistant bacteria (HR, 2.45), and recent use of β-lactams (HR, 2.39) were independently associated with the development of multiresistant infections. Results in the second series were similar to those observed in the first series. Conclusions : Multiresistant bacteria, especially ESBL-producing Enterobacteriaceae , are frequently isolated in nosocomial and, to a lesser extent, HCA infections in cirrhosis, rendering third-generation cephalosporins clinically ineffective. New antibiotic strategies tailored according to the local epidemiological patterns are needed for the empirical treatment of nosocomial infections in cirrhosis. (Hepatology 2012)
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A major problem with norfloxacin is the development of antibiotic resistance.
“A major problem with the use of norfloxacin is the development of antibiotic resistance110–112, suggesting that it might be suitable for treatment lasting weeks to months but not for long-term or life-long application in patients with cirrhosis.”
From The gut microbiome and liver cancer: mechanisms and clinical translation (2017) · cites this paper as [111]
Norfloxacin may be suitable for weeks to months of treatment but not for long-term or life-long use in cirrhosis patients.
“A major problem with the use of norfloxacin is the development of antibiotic resistance110–112, suggesting that it might be suitable for treatment lasting weeks to months but not for long-term or life-long application in patients with cirrhosis.”
From The gut microbiome and liver cancer: mechanisms and clinical translation (2017) · cites this paper as [111]
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Bone, R. C., BALK, R. A., Cerra, F. B., Dellinger, R. P., Fein, A. M., Knaus, W. A., Schein, R. M. H., & Sibbald, W. J. (1992) · CHEST Journal · doi:10.1378/chest.101.6.1644 · Cited by 13,192 · see citing works
American College of Chest Physicians/Society of Critical Care Medicine Consensus Conference
(1992) · Critical Care Medicine · doi:10.1097/00003246-199206000-00025 · Cited by 5,091 · see citing works
(2010) · Journal of Hepatology · doi:10.1016/j.jhep.2010.05.004 · Cited by 1,726 · see citing works
Friedman, N. D., Kaye, K. S., Stout, J. E., McGarry, S. A., Trivette, S. L., Briggs, J. P., Lamm, W., Clark, C., MacFarquhar, J., Walton, A. L., et al. (2002) · Annals of Internal Medicine · doi:10.7326/0003-4819-137-10-200211190-00007 · Cited by 1,664 · see citing works
Arvaniti, V., D’Amico, G., Fede, G., Manousou, P., Tsochatzis, E. A., Pleguezuelo, M., & Burroughs, A. K. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.06.019 · Cited by 1,172 · see citing works
Diagnosis, prevention and treatment of hepatorenal syndrome in cirrhosis
Salerno, F., Gerbes, A. L., Ginès, P., Wong, F. S.-H., & Arroyo, V. (2007) · Postgraduate Medical Journal · doi:10.1136/gut.2006.107789 · Cited by 1,080 · see citing works
Self-citationDiagnosis, treatment and prophylaxis of spontaneous bacterial peritonitis: a consensus document
Rimola, A., García–Tsao, G., Navasa, M., Piddock, L. J. V., Planas, R., Bernard‐Chabert, B., & Inadomi, J. M. (2000) · Journal of Hepatology · doi:10.1016/s0168-8278(00)80201-9 · Cited by 1,058 · see citing works
Management of adult patients with ascites due to cirrhosis
Runyon, B. A. (2009) · Hepatology · doi:10.1002/hep.22853 · Cited by 976 · see citing works
Fernández, J., Navasa, M., Gómez, J., Colmenero, J., Vila, J., Arroyo, V., & Rodés, J. (2002) · Hepatology · doi:10.1053/jhep.2002.30082 · Cited by 954 · see citing works
Self-citationBernard‐Chabert, B., Grangé, J., Khac, E. N., Amiot, X., Opolon, P., & Poynard, T. (1999) · Hepatology · doi:10.1002/hep.510290608 · Cited by 821 · see citing works
Fernández, J., Navasa, M., Planas, R., Montoliu, S., Monfort, D., Soriano, G., Vila, C., Pardo, A., Quintero, E., Vargas, V., et al. (2007) · Gastroenterology · doi:10.1053/j.gastro.2007.06.065 · Cited by 709 · see citing works
Self-citationPaterson, D. L., Ko, W.-C., von Gottberg, A., et al. (2004) · Annals of Internal Medicine · doi:10.7326/0003-4819-140-1-200401060-00008 · Cited by 637 · see citing works
Ginés, P., Rimola, A., Planas, R., Vargas, V., Marco, F., Almela, M., Forne, M., Miranda, M. L., Llach, J., Salmerón, J. M., et al. (1990) · Hepatology · doi:10.1002/hep.1840120416 · Cited by 627 · see citing works
Self-citationBacterial Infections, Sepsis, and Multiorgan Failure in Cirrhosis
Tandon, P., & García–Tsao, G. (2008) · Seminars in Liver Disease · doi:10.1055/s-2008-1040319 · Cited by 549 · see citing works
Changing epidemiology of systemic fungal infections
Richardson, M., & Lass-Flörl, C. (2008) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2008.01978.x · Cited by 524 · see citing works
Ben‐Ami, R., Rodríguez‐Baño, J., Arslan, H., Pitout, J. D. D., Quentin, C., Calbo, E., Azap, Ö. K., Arpin, C., Pascual, Á., Livermore, D. M., et al. (2009) · Clinical Infectious Diseases · doi:10.1086/604713 · Cited by 463 · see citing works
Fernández, J., Arbol, L. R. D., Gómez, C., Durández, R., Serradilla, R., Guarner, C., Planas, R., Arroyo, V., & Navasa, M. (2006) · Gastroenterology · doi:10.1053/j.gastro.2006.07.010 · Cited by 456 · see citing works
Self-citationGustot, T., Durand, F., Lebrec, D., Vincent, J., & Moreau, R. (2009) · Hepatology · doi:10.1002/hep.23264 · Cited by 439 · see citing works
Recurrence of spontaneous bacterial peritonitis in cirrhosis: Frequency and predictive factors
Titó, L., Rimola, A., Ginès, P., Llach, J., Arroyo, V., & Rodés, J. (1988) · Hepatology · doi:10.1002/hep.1840080107 · Cited by 399 · see citing works
Self-citationCardiovascular management of septic shock
Dellinger, R. P. (2003) · Critical Care Medicine · doi:10.1097/01.ccm.0000057403.73299.a6 · Cited by 365 · see citing works
Extended-spectrum β-lactamase-producing organisms
Falagas, M. E., & Karageorgopoulos, D. E. (2009) · Journal of Hospital Infection · doi:10.1016/j.jhin.2009.02.021 · Cited by 348 · see citing works
Rodríguez‐Baño, J., Picón, E., Gijón, P., Hernández, J. R., Ruíz, M., Peña, C., Almela, M., Almirante, B., Grill, F., Colomina, J., et al. (2009) · Clinical Infectious Diseases · doi:10.1086/649537 · Cited by 345 · see citing works
Cirrhotic Patients Are at Risk for Health Care–Associated Bacterial Infections
Merli, M., Lucidi, C., Giannelli, V., Giusto, M., Riggio, O., Falcone, M., Ridola, L., Attili, A. F., & Venditti, M. (2010) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2010.06.024 · Cited by 323 · see citing works
Measurement of pyuria and its relation to bacteriuria
Stamm, W. E. (1983) · The American Journal of Medicine · doi:10.1016/0002-9343(83)90073-6 · Cited by 308 · see citing works
Cefotaxime Is More Effective Than Is Ampicillin–Tobramycin in Cirrhotics With Severe Infections
Felisart, J., Rimola, A., Arroyo, V., et al. (1985) · Hepatology · doi:10.1002/hep.1840050319 · Cited by 306 · see citing works
Self-citationCirrhosis as a Risk Factor for Sepsis and Death
Foreman, M. G., Mannino, D. M., & Moss, M. (2003) · CHEST Journal · doi:10.1378/chest.124.3.1016 · Cited by 301 · see citing works
Azap, Ö. K., Arslan, H., Şerefhanoğlu, K., Çolakoğlu, Ş., Erdoğan, H., Timurkaynak, F., & Senger, S. S. (2009) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2009.02941.x · Cited by 180 · see citing works
Cheong, H. S., Kang, C., Lee, J. A., Moon, S. Y., Joung, M. K., Chung, D. R., Koh, K. C., Lee, N. Y., Song, J., & Peck, K. R. (2009) · Clinical Infectious Diseases · doi:10.1086/597585 · Cited by 178 · see citing works
Rodríguez‐Baño, J., Picón, E., Gijón, P., Hernández, J. R., Cisneros, J. M., Peña, C., Almela, M., Almirante, B., Grill, F., Colomina, J., et al. (2010) · Journal of Clinical Microbiology · doi:10.1128/jcm.02353-09 · Cited by 157 · see citing works
Campillo, B., Dupeyron, C., Richardet, J. P., Mangeney, N., & Leluan, G. (1998) · Clinical Infectious Diseases · doi:10.1086/520273 · Cited by 145 · see citing works
Dupeyron, C., Mangeney, N., Sedrati, L., Campillo, B., Fouet, P., & Leluan, G. (1994) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.38.2.340 · Cited by 128 · see citing works
Blot, S. I. (2007) · Clinical Microbiology and Infection · doi:10.1111/j.1469-0691.2007.01835.x · Cited by 124 · see citing works
Soriano, G., Castellote, J., Álvarez, C., Girbau, A., Gordillo, J., Baliellas, C., Casas, M., Pons, C., Román, E. M., Maisterra, S., et al. (2009) · Journal of Hepatology · doi:10.1016/j.jhep.2009.10.012 · Cited by 122 · see citing works
Umgelter, A., Reindl, W., Miedaner, M., Schmid, R. M., & Huber, W. (2009) · Infection · doi:10.1007/s15010-008-8060-9 · Cited by 121 · see citing works
Depuydt, P. O., Vandijck, D. M., Bekaert, M., Decruyenaere, J. M. A., Blot, S. I., Vogelaers, D., & Benoît, D. (2008) · Critical Care · doi:10.1186/cc7119 · Cited by 115 · see citing works
Angeloni, S., Leboffe, C., Parente, A., Venditti, M., Giordano, A., Merli, M., & Riggio, O. (2008) · World Journal of Gastroenterology · doi:10.3748/wjg.14.2757 · Cited by 104 · see citing works
Song, K., Jeon, J. H., Park, W. B., Park, S., Kim, H. B., Oh, M., Lee, H.-S., Kim, N. J., & Choe, K. W. (2009) · BMC Infectious Diseases · doi:10.1186/1471-2334-9-41 · Cited by 87 · see citing works
Aparicio, J. R., Such, J. M., Pascual, S., Arroyo, A., Plazas, J., Girona, E., Gutiérrez, A., de Vera, F., Palazón, J. M., Carnicer, F., et al. (1999) · Journal of Hepatology · doi:10.1016/s0168-8278(99)80225-6 · Cited by 79 · see citing works
Park, W. B., Lee, K.-D., Lee, C. S., Jang, H., Kim, H. B., Lee, H., Oh, M., & Choe, K. W. (2005) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2004.11.014 · Cited by 74 · see citing works
Bacterial infection in cirrhosis, with and without hepatocellular carcinoma.
Yoshida, H., Hamada, T., Inuzuka, S., et al. (1993) · PubMed · Cited by 72 · see citing works
Park, Y. H., Lee, H. C., Song, H. G., Jung, S., Ryu, S. H., Shin, J. W., Chung, Y., Lee, Y. S., & Suh, D. J. (2003) · Journal of Gastroenterology and Hepatology · doi:10.1046/j.1440-1746.2003.03086.x · Cited by 69 · see citing works
Song, J. Y., Jung, S. J., Park, C. W., Sohn, J. W., Kim, W. J., Kim, M. J., & Cheong, H. J. (2006) · Journal of Korean Medical Science · doi:10.3346/jkms.2006.21.4.666 · Cited by 55 · see citing works
Apisarnthanarak, A., Bailey, T. C., & Fraser, V. J. (2008) · Clinical Infectious Diseases · doi:10.1086/533475 · Cited by 46 · see citing works
Role of host and bacterial virulence factors in Escherichia coli spontaneous bacterial peritonitis
Cereto, F., Herranz, X., Moreno, E., Andreu, A., Vergara, M., Fontanals, D., Roget, M., Simó, M., González, A., Prats, G., et al. (2008) · European Journal of Gastroenterology & Hepatology · doi:10.1097/meg.0b013e3282fc7390 · Cited by 44 · see citing works
Yakar, T., Güçlü, M., Serin, E., & Alışkan, H. E. (2009) · Digestive Diseases and Sciences · doi:10.1007/s10620-009-0825-1 · Cited by 36 · see citing works
Antimicrobial Resistance in the Hospital Setting: Impact, Trends, and Infection Control Measures
Stein, G. E. (2005) · Pharmacotherapy The Journal of Human Pharmacology and Drug Therapy · doi:10.1592/phco.2005.25.10part2.44s · Cited by 29 · see citing works
Kang, C., Kim, S., Park, W. B., et al. (2004) · The Korean Journal of Internal Medicine · doi:10.3904/kjim.2004.19.3.160 · Cited by 26 · see citing works
Yakar, T., Güçlü, M., Serin, E., et al. (2009) · Digestive Diseases and Sciences · doi:10.1007/s10620-009-0868-3 · Cited by 9 · see citing works
Flagged first, then by citations
Research works printed but not linked: 5
- Merli M, Lucidi C, Giannelli V, Giusto M, Riggio O, Falcone M, et al. Cirrhotic patients are at risk for HCA bacterial infections. Clin Gastroenterol Hepatol 2010;8:979-985.
- Mandell GL, Bennet JE, Dolin R, eds. Mandell, Douglas, and Ben- nett's Principles and Practice of Infectious Diseases, 7th ed. Philadel- phia, PA: Churchill Livingstone Elsevier; 2010.
- Valenti WM, Chiarello LA. Overview of hospital infection control and noso- comial infections. In: Resse RE, Douglas RG, Jr., eds. A Practical Approach to Infectious Diseases. Boston, MA: Lippincott; 1986:545-555.
- Guidelines for the management of adults with hospital-acquired, venti- lator-associated, and healthcare-associated pneumonia. American Tho- racic Society; Infectious Diseases Society of America. Am J Respir Crit Care Med 2005;171:388-416.
- Apisarnthanarak A, Bailey TC, Fraser VJ. Duration of stool coloni- zation in patients infected with extended-spectrum beta-lactamase- producing Escherichia coli and Klebsiella pneumoniae. CID 2008;46: 1322-1323.
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Jalan, R., Fernandez, J., Wiest, R., Schnabl, B., Moreau, R., Angeli, P., Stadlbauer, V., Gustot, T., Bernardi, M., Canton, R., et al. (2014) · Journal of Hepatology · doi:10.1016/j.jhep.2014.01.024 · Cited by 906 · see citing works
Self-citationThe gut microbiome and liver cancer: mechanisms and clinical translation
Yu, L.-X., & Schwabe, R. F. (2017) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2017.72 · Cited by 634 · see citing works
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Patidar, K. R., & Bajaj, J. S. (2013) · Metabolic Brain Disease · doi:10.1007/s11011-013-9383-5 · Cited by 110 · see citing works
Lutz, P., Parcina, M., Bekeredjian-Ding, I., Nischalke, H. D., Nattermann, J., Sauerbruch, T., Hoerauf, A., Strassburg, C. P., & Spengler, U. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093909 · Cited by 55 · see citing works
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Agiasotelli, D., Alexopoulou, A., Vasilieva, L., Hadziyannis, E., Goukos, D., Daikos, G. L., & Dourakis, S. P. (2017) · Liver International · doi:10.1111/liv.13264 · Cited by 31 · see citing works
- Authors
- Fernández, J., Acevedo, J., Castro, M., Garcia, O., de Lope, C. R., Roca, D., Pavesi, M., Sola, E., Moreira, L., Silva, A., Seva-Pereira, T., Corradi, F., Mensa, J., Ginès, P., & Arroyo, V.
- Affiliations
- Hospital Clínic de Barcelona (ES)
- Corresponding author
- Fernández, Javier
- ORCID
- Venue
- Hepatology
- Published
- 2012-05
- Volume
- 55
- Issue
- 5
- Pages
- 1551-1561
- ISSN
- 0270-9139 (ISSN-L)
- OpenAlex
- W1989550571
- Cited by
- 620
- References
- 48
- Citations by year
- 2026: 20 · 2025: 25 · 2024: 33 · 2023: 45 · 2022: 52 · 2021: 49 · 2020: 38 · 2019: 58 · 2018: 66 · 2017: 53 · 2016: 42 · 2015: 53 · 2014: 43 · 2013: 29 · 2012: 13
- FWCI
- 17.24
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Hepatology (publishedVersion)
- PubMed (publishedVersion)
- CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
- Funders
- Fundación BBVA
- Instituto de Salud Carlos III (FI09/00510)
- Topics
- Health Sciences › Medicine › Hepatology › Liver Disease and Transplantation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
- Health Sciences › Medicine › Critical Care and Intensive Care Medicine › Nosocomial Infections in ICU
- Keywords
- multidrug-resistant bacteria, liver cirrhosis, bacterial infection, nosocomial infections, community-acquired infections, extended-spectrum beta-lactamase, ESBL-producing Enterobacteriaceae, Pseudomonas aeruginosa, methicillin-resistant Staphylococcus aureus, Enterococcus faecium, empirical antibiotic therapy, septic shock, mortality, risk factors, spontaneous bacterial peritonitis, pneumonia, urinary tract infection
- MeSH terms
- Aged, Bacterial Infections, beta-Lactamases, Cross Infection, Enterobacteriaceae, Female, Gram-Negative Bacteria, Gram-Positive Bacteria, Humans, Liver Cirrhosis, Male, Microbial Sensitivity Tests, Middle Aged, Prognosis, Retrospective Studies, Risk Factors, Spain, Cohort Studies, Prevalence, Multivariate Analysis, Proportional Hazards Models, Survival Analysis, Community-Acquired Infections, Statistics, Nonparametric, Drug Resistance, Multiple, Bacterial, Methicillin-Resistant Staphylococcus aureus
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