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      The role of Enterococcus spp. and multidrug-resistant bacteria causing pyogenic liver abscesses

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          Abstract

          Background

          Pyogenic liver abscesses (PLA) remain a significant clinical problem. Unfortunately, little is known about current bacterial susceptibility profiles and the incidence of multidrug resistant organisms (MDROs) causing PLA in Western countries. Yet, this crucial information is pivotal to guide empirical antibiotic therapy. Aim of this study was to provide detailed characteristics of PLA with a special focus on underlying bacterial pathogens and their susceptibility to antibiotics.

          Methods

          A retrospective study of patients diagnosed with PLA from 2009 to 2015 in a large tertiary reference center in Germany was performed in order to characterize PLA and antimicrobial susceptibility profiles of causative bacterial species.

          Results

          Overall, 86 patients were included. The most common causes of PLA were bile duct stenosis/obstruction (31.4%) and leakage of biliary anastomosis (15.1%). Frequent predisposing diseases were malignancies (34.9%), diabetes (24.4%) and the presence of liver cirrhosis (16.3%). Of note, Enterococcus spp. were the most frequently cultured bacterial isolates (28.9%), and in 1/3 of cases vancomycin resistance was observed. In addition, a relevant frequency of gram-negative MDROs was identified. In particular, an alarming 10% and 20% of gram-negative bacteria were resistant to carbapenems and tigecycline, respectively. Of note, MDRO status did not predict ICU stay or survival in multivariate regression analysis. The mortality rate in our series was 16.3%.

          Conclusion

          Our study demonstrates an as yet underreported role of Enterococcus spp., often associated with vancomycin resistance, as well as of gram-negative MDROs causing PLA.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12879-017-2543-1) contains supplementary material, which is available to authorized users.

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          Most cited references22

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          Pyogenic liver abscess: recent trends in etiology and mortality.

          Pyogenic liver abscess, a potentially life-threatening disease, has undergone significant changes in epidemiology, management, and mortality over the past several decades. We reviewed the data for patients admitted to Bellevue Hospital and New York University Downtown Hospital (New York, New York) over a 10-year period. Of 79 cases reviewed, 43% occurred in patients with underlying biliary disease. The most common symptoms were fever, chills, and right upper quadrant pain or tenderness. The most common laboratory abnormalities were an elevated white blood cell count (in 68% of cases), temperature >or=38.1 degrees C (90%), a low albumin level (70.2%), and an elevated alkaline phosphatase level (67%). Seventy percent of the abscesses were in the right lobe, and 77% were solitary. Klebsiella pneumoniae was identified in 41% of cases in which a pathogen was recovered. Eighteen (50%) of 36 Asian patients had K. pneumoniae isolated, in contrast to 6 (27.3%) of 22 non-Asian patients (not statistically significant). Fifty-six percent of cases involved treatment with percutaneous drainage. Although prior reports noted mortality of 11%-31%, we observed only 2 deaths (mortality, 2.5%). The data suggest that K. pneumoniae has become the predominant etiology of pyogenic liver abscess and that mortality from this disease has decreased substantially.
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            Pyogenic Liver Abscess as Endemic Disease, Taiwan

            The epidemiology of pyogenic liver abscess has changed dramatically in recent years ( 1 ). Previously, although incidence was considered rare, the condition was associated with high illness and death rates, usually due to underlying hepatobiliary diseases and polymicrobial infection ( 2 ), with Escherichia coli as the major pathogen ( 3 ). More recently, investigations in Taiwan suggest the role of cryptogenic or primary liver abscess, i.e., abscesses without underlying hepatobiliary diseases, in pyogenic liver abscess ( 4 , 5 ). These reports also indicate that diabetes is the major predisposing factor of liver abscess and that Klebsiella pneumoniae is the primary pathogen. However, these results were obtained from small-scale hospital-based surveys, which could not provide a panoramic view of the disease. To confirm these observation-based results, we conducted a large-scale, unbiased investigation. In addition to epidemiology, the pathogenesis of liver abscess caused by Klebsiella spp. has also been extensively studied, but the mechanism is still not clear. MagA, an outer-membrane protein contributing to capsular polysaccharide formation, coexists with serotype K1 and has been identified as the major virulence factor of K. pneumoniae ( 6 ). MagA-positive (or serotype K1) K. pneumoniae is accordingly recognized as the main pathogen of pyogenic liver abscess ( 7 , 8 ). Nevertheless, how diabetes increases the risk for Klebsiella spp. liver abscess is still not clear. Further research is needed on whether pyogenic liver abscess is affected by immunocompromised conditions, such as malignancy, renal failure, postorgan transplantation, or HIV infection. To clarify the epidemiology and pathogenesis of pyogenic liver abscess, we used information gathered by the Taiwan National Health Insurance (NHI) program, which was initiated in 1995 by the government to cover most Taiwanese citizens. In 2005, 91.25% of healthcare providers were enrolled in the program and 99% of Taiwanese were insured ( 9 ). Consequently, since 1995, the program has obtained comprehensive health data on the population in Taiwan. In this study, we used NHI data to study the incidence and death rates caused by pyogenic liver abscess in Taiwan and to investigate factors modifying the manifestations of this disease. Methods Patients We requested data on patients with pyogenic liver abscess from the Taiwan NHI program. Cases were selected by using the following criteria: patients were hospitalized and reported before 2004, and the discharge diagnoses included abscess of liver per the International Classification of Diseases, 9th revision, Clinical Modication (ICD-9-CM 572.0) but excluded amebic liver abscess (ICD-9-CM 006.3). Though we selected cases documented up to the end of 2004, the database could not provide information from patients who had not yet been discharged. Those admitted before December 31, 2004, but discharged during or after 2005 were therefore not included in our database. This exclusion results in the underestimation of case-patients admitted at the end of 2004. Data on 29,965 case-patients were collected. After excluding patients discharged before 1996 and those without clear records regarding age or sex, we enrolled 29,703 case-patients in our study. Patient data were anonymous. Names of these patients were not included, and patient and healthcare provider identification numbers were encrypted. This primary set of data included the date of admission and discharge, age, sex, diagnoses (up to 5), procedures (up to 5), outcome at discharge (recovered or died), and the fees charged to patients. Laboratory data, including microbiologic data and medication, were not included. Any underlying diseases were determined by the diagnoses listed in the medical records, which were coded by ICD-9-CM. Because K. pneumoniae is the major pathogen of primary pyogenic liver abscess in Taiwan, it is expected to play an important role in the pathogenesis and prognosis of this disease. Unfortunately, the NHI database does not include microbiologic data. To compensate for this, we reviewed the records of patients in National Taiwan University Hospital (NTUH). This hospital is a public medical center in Taipei, functioning both as a primary care hospital and as a tertiary referral center ( 10 ). As the leading hospital in Taiwan ( 10 ) with a 113-year history ( 11 ), NTUH serves patients and accepts referrals evenly distributed from every part of Taiwan. The hospital provides care for ≈2,000 inpatients and 7,000 outpatients a day ( 11 ), which are ≈3.5% and 2%, respectively, of persons included in the NHI database ( 12 ). Therefore, the patients of NTUH are representative of all of the patients in Taiwan, without substantial bias but may be skewed slightly to the severe side. We selected case-patients from this hospital using the same criteria mentioned above, except that the discharge year was between January 1, 2000, and December 31, 2004; complete microbiologic data was preserved in the NTUH laboratory only after 2000. These patients were included in the NHI database anonymously. For case-patients from NTUH, we reviewed actual medical records and obtained microbiologic data from the hospital’s laboratory. Statistical Analysis Numerical data were compared by Student t test or paired t test. Categorical data were processed by χ2 test. Pearson correlation coefficients and χ2 goodness-of-fit test were used to estimate the trend of incidence and death over time. Unfortunately, incidence and death from different years could not be directly compared because the population structure changed slightly over the study period. To correct the bias, we calculated age-standardized incidence and death rates. The correction was based on age-specific population data in 1996. Finally, risk factor analysis was conducted by using the binary logistic regression and curve estimation methods by SPSS version 11.0 for Macintosh (SPSS, Inc. Chicago, IL, USA). Results Demographic Data A total of 29,703 case-patients from the NHI database were enrolled in our analysis (Table 1). Ages of these patients ranged from 85 years of age. Incidence and Risk Factors The gross incidence of pyogenic liver abscess from 1996 through 2004 was 14.87 cases/100,000 population/year (17.94 male cases/100,000 population and 11.65 female cases/100,000 population). The annual increase of incidence was 0.86 cases/100,000 population (r = 0.98, p 5 underlying diseases. For this reason, some minor conditions, such as peptic ulcer, urinary tract infection, and hypertension, paradoxically decreased death rates in our data. Third, in contrast to the comprehensive data of pyogenic liver abscess, detailed health data for each person in the population are not available. We are therefore unable to estimate the interaction among the risk factors of pyogenic liver abscess in the population (Table 3). Nevertheless, this study still provides a clear picture of pyogenic liver abscess in Taiwan. The rapid and steady increase of cases with pyogenic liver abscess in Taiwan should be noted (Table 2). Although the prognosis of liver abscess patients has improved over time (Figure 3), pyogenic liver abscess-related death in the population continues to increase (Table 2). Furthermore, complex interactions between pyogenic liver abscess, diabetes, renal disease, and malignancy are shown to worsen this condition. Further collaboration among clinical medical practitioners, public health workers, and research scientists is mandatory to fight against such a challenge in the future.
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              A population-based study of pyogenic liver abscesses in the United States: incidence, mortality, and temporal trends.

              Few population-based studies have evaluated pyogenic liver abscess (PLA) in North America. We assessed the incidence of PLA and evaluated predictors of mortality. We used the Nationwide Inpatient Sample to identify all patients with discharges for PLA (ICD-9 572.0) between 1994 and 2005. Multivariable logistic regression analysis was performed to determine whether mortality was associated with patient and hospital characteristics including comorbidities, interventions, and bacterial cultures. We determined the annual incidence for PLA in the US population and assessed for temporal changes using generalized linear regression models. We identified 17,787 PLA discharges for an overall incidence of PLA of 3.6 (95% confidence interval (CI): 3.5-3.7) per 100,000 population. From 1994 to 2005, the annual average percent increase in incidence was 4.1% (95% CI: 3.4-4.8; P<0.0001). In-hospital mortality was 5.6% (95% CI: 5.3-6.0). Mortality was associated with older age (65-84 vs. 18-34: odds ratio (OR)=2.28 (1.48-3.51)); Medicaid (OR=1.74 (1.36-2.23)) and Medicare (OR=1.48 (1.18-1.85) vs. private insurance; and comorbidities such as cirrhosis (OR=2.48 (1.85-3.31)), chronic renal failure (OR=1.99 (1.28-3.09)), and cancer (OR=2.32 (1.97-2.73)). Patients who underwent percutaneous liver aspiration (OR=0.45 (0.39-0.52)) had lower mortality, whereas surgical drainage (OR=0.87 (0.68-1.10)) and endoscopic retrograde cholangiopancreatography (OR=0.73 (0.52-1.03)) were not associated with mortality. The most commonly recorded bacterial infections were Streptococcus species (29.5%) and Escherichia coli (18.1%). Patients with bacteremia or septicemia (OR=3.88 (3.36-4.48)) had an increased risk of death. The incidence of PLA is increasing and is associated with significant mortality that is attributable to several modifiable risk factors.
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                Author and article information

                Contributors
                Johanna.Kessel@kgu.de
                Victoria.Muecke@kgu.de
                Katharina.Schwarzkopf@kgu.de
                Michael.Hogardt@kgu.de
                Christoph.Stephan@kgu.de
                Stefan.Zeuzem@kgu.de
                Volkhard.Kempf@kgu.de
                0049-69-6301-87838 , Christian.Lange@kgu.de
                Journal
                BMC Infect Dis
                BMC Infect. Dis
                BMC Infectious Diseases
                BioMed Central (London )
                1471-2334
                26 June 2017
                26 June 2017
                2017
                : 17
                : 450
                Affiliations
                [1 ]ISNI 0000 0004 0578 8220, GRID grid.411088.4, Department of Internal Medicine 1, , University Hospital Frankfurt, ; Frankfurt am Main, Germany
                [2 ]ISNI 0000 0004 0578 8220, GRID grid.411088.4, , University Center for Infectious Diseases, University Hospital Frankfurt, ; Frankfurt am Main, Germany
                [3 ]ISNI 0000 0004 0578 8220, GRID grid.411088.4, Department of Internal Medicine 2, , University Hospital Frankfurt, ; Frankfurt am Main, Germany
                [4 ]ISNI 0000 0004 0578 8220, GRID grid.411088.4, Institute of Medical Microbiology and Infection Control, , University Hospital Frankfurt, ; Frankfurt am Main, Germany
                Author information
                http://orcid.org/0000-0001-8475-8369
                Article
                2543
                10.1186/s12879-017-2543-1
                5485679
                28651522
                b68cc3ac-e918-4842-9eaa-87e22922b0bd
                © The Author(s). 2017

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 11 March 2017
                : 9 June 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: LA 2806/5-1
                Award ID: DFG research unit 2251
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2017

                Infectious disease & Microbiology
                pyogenic liver abscess,bacterial pathogens,susceptibility profiles,multidrug-resistant organisms,vancomycin-resistant enterococci

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