Publications by authors named "Hong Bin Kim"

226 Publications

Genetic regulation of nonsense-mediated decay underlies association with risk of severe COVID-19.

medRxiv 2021 Jul 13. Epub 2021 Jul 13.

Genomic regions have been associated with COVID-19 susceptibility and outcomes, including the chr12q24.13 locus encoding antiviral proteins OAS1-3. Here, we report genetic, functional, and clinical insights into genetic associations within this locus. In Europeans, the risk of hospitalized vs. non-hospitalized COVID-19 was associated with a single 19Kb-haplotype comprised of 76 variants included in a 95% credible set within a large genomic fragment introgressed from Neandertals. The risk haplotype was also associated with impaired spontaneous but not treatment-induced SARS-CoV-2 clearance in a clinical trial with pegIFN-λ1. We demonstrate that two exonic variants, rs10774671 and rs1131454, affect splicing and nonsense-mediated decay of . We suggest that genetically-regulated loss of expression contributes to impaired spontaneous clearance of SARS-CoV-2 and elevated risk of hospitalization for COVID-19. Our results provide the rationale for further clinical studies using interferons to compensate for impaired spontaneous SARS-CoV-2 clearance, particularly in carriers of the risk haplotypes.
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http://dx.doi.org/10.1101/2021.07.09.21260221DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8288155PMC
July 2021

Status of antimicrobial stewardship programmes in Korean hospitals including small to medium-sized hospitals and the awareness and demands of physicians: a nationwide survey in 2020.

J Glob Antimicrob Resist 2021 Jun 18;26:180-187. Epub 2021 Jun 18.

Division of Infectious Diseases, Department of Internal Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine, 82 Gumi-ro, 173 beon-gil, Bundang-gu, Seongnam 13620, Gyeonggi-do, South Korea.

Objectives: This study aimed to identify the status of antimicrobial stewardship programmes (ASPs) in small to medium-sized Korean hospitals as well as the awareness and demands about ASPs of physicians.

Methods: A questionnaire was designed based on a questionnaire from a previous nationwide survey in 2018 targeting large hospitals in Korea and modified to reflect the results of in-depth interviews with non-infectious diseases (IDs) physicians at secondary care hospitals. The survey targeted all hospitals with ≥150 beds in South Korea and was performed in May-June 2020. Only one ASP-associated physician per hospital participated in the survey.

Results: The survey response rate was 31.9% (217/680). ID specialists comprised the majority of medical personnel participating in ASPs in tertiary care hospitals. Conversely, in secondary and primary care hospitals there was no predominant medical personnel for ASPs and the median full-time equivalent was 0 for all types of medical personnel. Tertiary care hospitals, more than secondary and primary care hospitals, tended to perform ASP activities more actively. 'Workforce for ASPs', 'Establishment of healthcare fees for ASPs' and 'Development of tools for ASPs' were the most important required support for ASP improvement.

Conclusion: The level of ASP establishment was more limited in primary care hospitals than in secondary and tertiary care hospitals in Korea. To improve ASPs in Korean hospitals, a supporting workforce and the establishment of a healthcare fee for ASPs appear to be necessary.
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http://dx.doi.org/10.1016/j.jgar.2021.06.001DOI Listing
June 2021

Rapid diagnostic testing for antimicrobial stewardship: Utility in Asia Pacific.

Infect Control Hosp Epidemiol 2021 Jul 15;42(7):864-868. Epub 2021 Jun 15.

Clinical Pathology, Faculty of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand.

Rapid diagnostic testing (RDT) can provide prompt, accurate identification of infectious organisms and be a key component of antimicrobial stewardship (AMS) programs. However, their use is less widespread in Asia Pacific than western countries. Cost can be prohibitive, particularly in less resource-replete settings. A selective approach is required, possibly focusing on the initiation of antimicrobials, for differentiating bacterial versus viral infections and identifying locally relevant tropical diseases. Across Asia Pacific, more data are needed on RDT use within AMS, focusing on the impact on antimicrobial usage, patient morbidity and mortality, and cost effectiveness. Moreover, in the absence of formal guidelines, regional consensus statements to guide clinical practice are warranted. These will provide a regionally relevant definition for RDT; greater consensus on its role in managing infections; advice on implementation and overcoming barriers; and guidance on optimizing human resource capacity. By addressing these issues, the outcomes of AMS programs should improve.
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http://dx.doi.org/10.1017/ice.2021.149DOI Listing
July 2021

Impact of immunosuppressive agents on clinical manifestations and outcome of Staphylococcus aureus bloodstream infection - A propensity score matched analysis in two large, prospectively evaluated cohorts.

Clin Infect Dis 2021 Apr 29. Epub 2021 Apr 29.

Division of Infectious Diseases, Department of Medicine II, Medical Centre - University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Background: Staphylococcus aureus bloodstream infection (SAB) is a common, life-threatening infection. The impact of immunosuppressive agents on the outcome of patients with SAB is incompletely understood.

Methods: Data from two large prospective, international, multicenter cohort studies (INSTINCT and ISAC) between 2006 and 2015 were analyzed. Patients receiving immunosuppressive agents were identified and a 1:1 propensity score (PS) matched analysis was performed to adjust for baseline characteristics of patients. Overall survival and time to SAB-related late complications (SAB relapse, infective endocarditis, osteomyelitis, or other deep-seated manifestations) were analyzed by Cox regression and competing risk analyses, respectively. This approach was then repeated for specific immunosuppressive agents (corticosteroids [CSMT] and immunosuppressive agents other than steroids [IMOTS]).

Results: Of 3,188 analyzed patients, 309 were receiving immunosuppressive treatment according to our definitions and were matched to 309 non-immunosuppressed patients. After PS matching, baseline characteristics were well balanced. In the Cox regression analysis, we observed no significant difference in survival between the two groups (death during follow-up: 105/309 (33.9 %) immunosuppressed patients vs. 94/309 (30.4 %) non-immunosuppressed, hazard ratio 1.20 (95% CI 0.84-1.71). Competing risk analysis showed a cause-specific hazard ratio (CSHR) of 1.81 (95% CI 0.85-3.87) for SAB-related late-complications in patients receiving immunosuppressive agents. CSHR was higher in patients taking IMOTS (3.69; 95% CI 1.41-9.68).

Conclusions: Immunosuppressive agents were not associated with an overall higher mortality. The risk for SAB-related late complications in patients receiving specific immunosuppressive agents such as IMOTs warrants further investigations.
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http://dx.doi.org/10.1093/cid/ciab385DOI Listing
April 2021

A standardized glucose-insulin-potassium infusion protocol in surgical patients: Use of real clinical data from a clinical data warehouse.

Diabetes Res Clin Pract 2021 Apr 17;174:108756. Epub 2021 Mar 17.

Department of Internal Medicine, Seoul National University College of Medicine, Seoul, South Korea; Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, South Korea. Electronic address:

Aims: We evaluated the clinical usefulness of a new unified glucose-insulin-potassium (GIK) regimen in a general surgical department.

Methods: Surgical patients treated under the previous diverse GIK regimens (September 2016 to August 2017) and the new unified GIK regimen (September 2017 to August 2018) were identified in records of the Clinical Data Warehouse of Seoul National University Bundang Hospital. Serial and area under the curve (AUC) glucose levels, and percentages of time within the target glucose levels were compared in propensity score matched patients in the diverse GIK regimen and in the unified GIK regimen (n = 227 in each group).

Results: The AUC of glucose at 6 h and 12 h was lower under the unified GIK regimen than the diverse GIK regimen. The percentage of target glucose levels was higher in the unified GIK regimen compared to the diverse GIK regimen (81.5% vs. 75.0%, P = 0.026), but the occurrence of hypoglycaemia did not differ significantly between groups.

Conclusions: The unified GIK regimen was more effective than the diverse GIK regimen for glycaemic control and did not increase the number of patients developing hypoglycaemia. This validated written GIK regimen can be safely used in a general surgical department.
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http://dx.doi.org/10.1016/j.diabres.2021.108756DOI Listing
April 2021

Development of key quality indicators for appropriate antibiotic use in the Republic of Korea: results of a modified Delphi survey.

Antimicrob Resist Infect Control 2021 03 6;10(1):48. Epub 2021 Mar 6.

Division of Infectious Diseases, Department of Internal Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, Republic of Korea.

Background: An effective antibiotic stewardship program relies on the measurement of appropriate antibiotic use, on which there is a lack of consensus. We aimed to develop a set of key quality indicators (QIs) for nationwide point surveillance in the Republic of Korea.

Methods: A systematic literature search of PubMed, EMBASE, and Cochrane Library (publications until 20th November 2019) was conducted. Potential key QIs were retrieved from the search and then evaluated by a multidisciplinary expert panel using a RAND-modified Delphi procedure comprising two online surveys and a face-to-face meeting.

Results: The 23 potential key QIs identified from 21 studies were submitted to 25 multidisciplinary expert panels, and 17 key QIs were retained, with a high level of agreement (13 QIs for inpatients, 7 for outpatients, and 3 for surgical prophylaxis). After adding up the importance score and applicability, six key QIs [6 QIs (Q 1-6) for inpatients and 3 (Q 1, 2, and 5) for outpatients] were selected. (1) Prescribe empirical antibiotic therapy according to guideline, (2) change empirical antibiotics to pathogen-directed therapy, (3) obtain culture samples from suspected infection sites, (4) obtain two blood cultures, (5) adapt antibiotic dosage to renal function, and (6) document antibiotic plan. In surgical prophylaxis, the QIs to prescribe antibiotics according to the guideline and initiate antibiotic therapy 1 h before incision were selected.

Conclusions: We identified key QIs to measure the appropriateness of antibiotic therapy to identify targets for improvement and to evaluate the effects of antibiotic stewardship intervention.
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http://dx.doi.org/10.1186/s13756-021-00913-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7937201PMC
March 2021

Impact of a computerised clinical decision support system on vancomycin loading and the risk of nephrotoxicity.

Int J Med Inform 2021 05 4;149:104403. Epub 2021 Feb 4.

Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, South Korea; Department of Internal Medicine, Seoul National University College of Medicine, Seoul, South Korea.

Background: A vancomycin loading dose is recommended for the treatment of serious methicillin-resistant Staphylococcus aureus (MRSA) infections. However, clinicians often do not adhere to these recommendations, mainly due to nephrotoxicity risk, unfamiliarity with the guideline, or complexity of calculating an individual dose. Therefore, we introduced a computerised clinical decision support system (CDSS) for vancomycin loading (hereafter Vancomycin CDSS) to promote the use of vancomycin loading dose.

Methods: We describe a quasi-experimental study spanning 6 months before and 18 months after the deployment of a Vancomycin CDSS. The Vancomycin CDSS was integrated into the hospital's electronic medical record system in the form of a vancomycin order set. Our primary endpoint was the incidence of nephrotoxicity; the secondary endpoint was mean initial vancomycin trough levels. We also conducted a survey to evaluate the reasons why clinicians opted not to utilise a vancomycin loading dose.

Results: After implementation of Vancomycin CDSS, 363 out of 746 patients (49 %) who were first administered vancomycin received a loading dose. We did not find significant differences in nephrotoxicity between the pre- and post-intervention groups, nor between the loading- and non-loading groups. In the pre-intervention group, the mean initial vancomycin trough level was 7.10 mg/L, which was significantly lower than that in the post-intervention group of 11.11 mg/L. In the vancomycin loading group, the mean initial trough level was 11.95 mg/L, compared to 7.55 mg/L in the non-loading group. The main reason stated for not prescribing a vancomycin loading dose was concern about nephrotoxicity.

Conclusion: Introduction of the Vancomycin CDSS did not increase nephrotoxicity and increased the mean initial dose and trough level of vancomycin.
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http://dx.doi.org/10.1016/j.ijmedinf.2021.104403DOI Listing
May 2021

Whole-Genome Sequencing for Investigating a Health Care-Associated Outbreak of Carbapenem-Resistant .

Diagnostics (Basel) 2021 Jan 29;11(2). Epub 2021 Jan 29.

Department of Laboratory Medicine, Seoul National University Bundang Hospital, Seongnam 13620, Korea.

Carbapenem-resistant (CRAB) outbreaks in hospital settings challenge the treatment of patients and infection control. Understanding the relatedness of clinical isolates is important in distinguishing outbreak isolates from sporadic cases. This study investigated 11 CRAB isolates from a hospital outbreak by whole-genome sequencing (WGS), utilizing various bioinformatics tools for outbreak analysis. The results of multilocus sequence typing (MLST), single nucleotide polymorphism (SNP) analysis, and phylogenetic tree analysis by WGS through web-based tools were compared, and repetitive element polymerase chain reaction (rep-PCR) typing was performed. Through the WGS of 11 isolates, three clonal lineages were identified from the outbreak. The coexistence of and with additional aminoglycoside-inactivating enzymes, predicted to confer multidrug resistance, was identified in all isolates. The MLST Oxford scheme identified three types (ST191, ST369, and ST451), and, through whole-genome MLST and whole-genome SNP analyses, different clones were found to exist within the MLST types. wgSNP showed the highest discriminatory power with the lowest similarities among the isolates. Using the various bioinformatics tools for WGS, CRAB outbreak analysis was applicable and identified three discrete clusters differentiating the separate epidemiologic relationships among the isolates.
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http://dx.doi.org/10.3390/diagnostics11020201DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7910894PMC
January 2021

Stereotypic neutralizing V antibodies against SARS-CoV-2 spike protein receptor binding domain in patients with COVID-19 and healthy individuals.

Sci Transl Med 2021 01 4;13(578). Epub 2021 Jan 4.

Department of Biochemistry and Molecular Biology, Seoul National University College of Medicine, Seoul 03080, Republic of Korea.

Stereotypic antibody clonotypes exist in healthy individuals and may provide protective immunity against viral infections by neutralization. We observed that 13 of 17 patients with COVID-19 had stereotypic variable heavy chain (V) antibody clonotypes directed against the receptor binding domain (RBD) of SARS-CoV-2 spike protein. These antibody clonotypes were composed of immunoglobulin heavy variable 3-53 () or and immunoglobulin heavy joining 6 () genes. These clonotypes included IgM, IgG3, IgG1, IgA1, IgG2, and IgA2 subtypes and had minimal somatic mutations, which suggested swift class switching after SARS-CoV-2 infection. The different IGHV chains were paired with diverse light chains resulting in binding to the RBD of SARS-CoV-2 spike protein. Human antibodies specific for the RBD can neutralize SARS-CoV-2 by inhibiting entry into host cells. We observed that one of these stereotypic neutralizing antibodies could inhibit viral replication in vitro using a clinical isolate of SARS-CoV-2. We also found that these V clonotypes existed in 6 of 10 healthy individuals, with IgM isotypes predominating. These findings suggest that stereotypic clonotypes can develop de novo from naïve B cells and not from memory B cells established from prior exposure to similar viruses. The expeditious and stereotypic expansion of these clonotypes may have occurred in patients infected with SARS-CoV-2 because they were already present.
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http://dx.doi.org/10.1126/scitranslmed.abd6990DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7875332PMC
January 2021

PD-1-Expressing SARS-CoV-2-Specific CD8 T Cells Are Not Exhausted, but Functional in Patients with COVID-19.

Immunity 2021 01 14;54(1):44-52.e3. Epub 2020 Dec 14.

Graduate School of Medical Science and Engineering, Korea Advanced Institute of Science and Technology (KAIST), Daejeon 34141, Republic of Korea; The Center for Epidemic Preparedness, KAIST Institute, Daejeon 34141, Republic of Korea. Electronic address:

Memory T cell responses have been demonstrated in COVID-19 convalescents, but ex vivo phenotypes of SARS-CoV-2-specific T cells have been unclear. We detected SARS-CoV-2-specific CD8 T cells by MHC class I multimer staining and examined their phenotypes and functions in acute and convalescent COVID-19. Multimer cells exhibited early differentiated effector-memory phenotypes in the early convalescent phase. The frequency of stem-like memory cells was increased among multimer cells in the late convalescent phase. Cytokine secretion assays combined with MHC class I multimer staining revealed that the proportion of interferon-γ (IFN-γ)-producing cells was significantly lower among SARS-CoV-2-specific CD8 T cells than those specific to influenza A virus. Importantly, the proportion of IFN-γ-producing cells was higher in PD-1 cells than PD-1 cells among multimer cells, indicating that PD-1-expressing, SARS-CoV-2-specific CD8 T cells are not exhausted, but functional. Our current findings provide information for understanding of SARS-CoV-2-specific CD8 T cells elicited by infection or vaccination.
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http://dx.doi.org/10.1016/j.immuni.2020.12.002DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7834198PMC
January 2021

Psychological Consequences of Survivors of COVID-19 Pneumonia 1 Month after Discharge.

J Korean Med Sci 2020 Dec 7;35(47):e409. Epub 2020 Dec 7.

Department of Internal Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seongnam, Korea.

As the coronavirus disease 2019 (COVID-19) has rapidly spread worldwide, there are growing concerns about patients' mental health. We investigated psychological problems in COVID-19 patients assessed with self-reported questionnaires including the Patient Health Questionnaire-9, Generalized Anxiety Disorder-7 scale, and Impact of Event Scale-Revised Korean version. Ten patients who recovered from COVID-19 pneumonia without complications underwent self-reported questionnaires about 1 month after discharge. Of them, 10% reported depression and posttraumatic stress disorder (PTSD) while 50% had depression during the treatment. Perceived stigma and history of psychiatric treatment affected PTSD symptom severity, consistent with previous emerging infectious diseases. Survivors also reported that they were concerned about infecting others and being discriminated and that they chose to avoid others after discharge. Further support and strategy to minimize their psychosocial difficulties after discharge should be considered.
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http://dx.doi.org/10.3346/jkms.2020.35.e409DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7721563PMC
December 2020

Clonal hematopoiesis is associated with risk of severe Covid-19.

medRxiv 2020 Nov 27. Epub 2020 Nov 27.

Acquired somatic mutations in hematopoietic stem and progenitor cells (clonal hematopoiesis or CH) are associated with advanced age, increased risk of cardiovascular and malignant diseases, and decreased overall survival. These adverse sequelae may be mediated by altered inflammatory profiles observed in patients with CH. A pro-inflammatory immunologic profile is also associated with worse outcomes of certain infections, including SARS-CoV-2 and its associated disease Covid-19. Whether CH predisposes to severe Covid-19 or other infections is unknown. Among 515 individuals with Covid-19 from Memorial Sloan Kettering (MSK) and the Korean Clonal Hematopoiesis (KoCH) consortia, we found that CH was associated with severe Covid-19 outcomes (OR=1.9, 95%=1.2-2.9, p=0.01). We further explored the relationship between CH and risk of other infections in 14,211 solid tumor patients at MSK. CH was significantly associated with risk of (HR=2.0, 95% CI: 1.2-3.3, p=6×10 ) and infections (HR=1.5, 95% CI=1.1-2.1, p=5×10 ). These findings suggest a relationship between CH and risk of severe infections that warrants further investigation.
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http://dx.doi.org/10.1101/2020.11.25.20233163DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7709186PMC
November 2020

Toll-like receptor 2 downregulation and cytokine dysregulation predict mortality in patients with Staphylococcus aureus bacteremia.

BMC Infect Dis 2020 Nov 30;20(1):901. Epub 2020 Nov 30.

Department of Internal Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine, 173 Gumi-ro, Bundang-gu, Seongnam, 463-707, Republic of Korea.

Background: Staphylococcus aureus bacteremia (SAB) presents heterogeneously, owing to the differences in underlying host conditions and immune responses. Although Toll-like receptor 2 (TLR2) is important in recognizing S. aureus, its function during S. aureus infection remains controversial. We aimed to examine the association of TLR2 expression and associated cytokine responses with clinical SAB outcomes.

Methods: Patients from a prospective SAB cohort at two tertiary-care medical centers were enrolled. Blood was sampled at several timepoints (≤5 d, 6-9 d, 10-13 d, 14-19 d, and ≥ 20 d) after SAB onset. TLR2 mRNA levels were determined via real-time PCR and serum tumor necrosis factor [TNF]-α, interleukin [IL]-6, and IL-10 levels were analyzed with multiplex-high-sensitivity electrochemiluminescent ELISA.

Results: TLR2 levels varied among 59 SAB patients. On days 2-5, TLR2 levels were significantly higher in SAB survivors than in healthy controls (p = 0.040) and slightly but not significantly higher than non-survivors (p = 0.120), and SAB patients dying within 7 d had lower TLR2 levels than survivors (P = 0.077) although statistically insignificant. IL-6 and IL-10 levels were significantly higher in non-survivors than in survivors on days 2-5 post-bacteremia (P = 0.010 and P = 0.021, respectively), and those dying within 7 d of SAB (n = 3) displayed significantly higher IL-10/TNF-α ratios than the survivors did (P = 0.007).

Conclusion: TLR2 downregulation and IL-6 and IL-10 concentrations suggestive of immune dysregulation during early bacteremia may be associated with mortality from SAB. TLR2 expression levels and associated cytokine reactions during early-phase SAB may be potential prognostic factors in SAB, although larger studies are warranted.
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http://dx.doi.org/10.1186/s12879-020-05641-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7706030PMC
November 2020

Dysfunctional accessory gene regulator (agr) as a prognostic factor in invasive Staphylococcus aureus infection: a systematic review and meta-analysis.

Sci Rep 2020 11 26;10(1):20697. Epub 2020 Nov 26.

Department of Internal Medicine, Pusan National University School of Medicine and Medical Research Institute, Pusan National University Hospital, 179 Gudeok-ro, Seo-gu, Busan, 49241, Republic of Korea.

The accessory gene regulator (agr) locus of Staphylococcus aureus is a quorum-sensing virulence regulator. Although there are many studies concerning the effect of dysfunctional agr on the outcomes of S. aureus infection, there is no systematic review to date. We systematically searched for clinical studies reporting outcomes of invasive S. aureus infections and the proportion of dysfunctional agr among their causative strains, and we performed a meta-analysis to obtain estimates of the odds of outcomes of invasive S. aureus infection with dysfunctional versus functional agr. Of 289 articles identified by our research strategy, 20 studies were meta-analysed for crude analysis of the impact of dysfunctional agr on outcomes of invasive S. aureus infection. Dysfunctional agr was generally associated with unfavourable outcomes (OR 1.32, 95% CI 1.05-1.66), and the impact of dysfunctional agr on outcome was more prominent in invasive methicillin-resistant S. aureus (MRSA) infections (OR 1.54, CI 1.20-1.97). Nine studies were meta-analysed for the impact of dysfunctional agr on the 30-day mortality of invasive S. aureus infection. Invasive MRSA infection with dysfunctional agr exhibited higher 30-day mortality (OR 1.40, CI 1.03-1.90) than that with functional agr. On the other hand, invasive MSSA infection with dysfunctional agr exhibited lower 30-day mortality (OR 0.51, CI 0.27-0.95). In the post hoc subgroup analysis by the site of MRSA infection, dysfunctional agr was associated with higher 30-day mortality in MRSA pneumonia (OR 2.48, CI 1.17-5.25). The effect of dysfunctional agr on the outcome of invasive S. aureus infection may vary depending on various conditions, such as oxacillin susceptibility and the site of infection. Dysfunctional agr was generally associated with unfavourable clinical outcomes and its effect was prominent in MRSA and pneumonia. Dysfunctional agr may be applicable for outcome prediction in cases of invasive MRSA infection with hardly eradicable foci such as pneumonia.
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http://dx.doi.org/10.1038/s41598-020-77729-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7691521PMC
November 2020

A call for antimicrobial stewardship in patients with COVID-19: a nationwide cohort study in Korea.

Clin Microbiol Infect 2021 Apr 31;27(4):653-655. Epub 2020 Oct 31.

Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Republic of Korea.

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http://dx.doi.org/10.1016/j.cmi.2020.10.024DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7604125PMC
April 2021

Human resources required for antimicrobial stewardship activities for hospitalized patients in Korea.

Infect Control Hosp Epidemiol 2020 12 26;41(12):1429-1435. Epub 2020 Oct 26.

Division of Infectious Diseases, Department of Internal Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Seoul, Korea.

Objectives: We calculated the human resources required for an antimicrobial stewardship program (ASP) in Korean hospitals.

Design: Multicenter retrospective study.

Setting: Eight Korean hospitals ranging in size from 295 to 1,337 beds.

Methods: The time required for performing ASP activities for all hospitalized patients under antibiotic therapy was estimated and converted into hours per week. The actual time spent on patient reviews of each ASP activity was measured with a small number of cases, then the total time was estimated by applying the determined times to a larger number of cases. Full-time equivalents (FTEs) were measured according to labor laws in Korea (52 hours per week).

Results: In total, 225 cases were reviewed to measure time spent on patient reviews. The median time spent per patient review for ASP activities ranged from 10 to 16 minutes. The total time spent on the review for all hospitalized patients was estimated using the observed number of ASP activities for 1,534 patients who underwent antibiotic therapy on surveillance days. The most commonly observed ASP activity was 'review of surgical prophylactic antibiotics' (32.7%), followed by 'appropriate antibiotics recommendations for patients with suspected infection without a proven site of infection but without causative pathogens' (28.6%). The personnel requirement was calculated as 1.20 FTEs (interquartile range [IQR], 1.02-1.38) per 100 beds and 2.28 FTEs (IQR, 1.93-2.62) per 100 patients who underwent antibiotic therapy, respectively.

Conclusion: The estimated time required for human resources performing extensive ASP activities on all hospitalized patients undergoing antibiotic therapy in Korean hospitals was ~1.20 FTEs (IQR, 1.02-1.38) per 100 beds.
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http://dx.doi.org/10.1017/ice.2020.1234DOI Listing
December 2020

Waning Antibody Responses in Asymptomatic and Symptomatic SARS-CoV-2 Infection.

Emerg Infect Dis 2021 01 13;27(1). Epub 2020 Oct 13.

We investigated the kinetics of severe acute respiratory syndrome coronavirus 2 neutralizing antibodies in 7 asymptomatic persons and 11 patients with pneumonia. The geometric mean titer of neutralizing antibodies declined from 219.4 at 2 months to 143.7 at 5 months after infection, indicating a waning antibody response.
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http://dx.doi.org/10.3201/eid2701.203515DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7774548PMC
January 2021

Short course of voriconazole therapy as a risk factor for relapse of invasive pulmonary aspergillosis.

Sci Rep 2020 09 30;10(1):16078. Epub 2020 Sep 30.

Department of Internal Medicine, Seoul National University College of Medicine, Seoul, Republic of Korea.

To investigate associations of the duration of voriconazole treatment and radiological response with relapse of invasive pulmonary aspergillosis (IPA) in immunocompromised patients, we explored the risk factors for IPA relapse after successful initial treatment. All patients with proven or probable IPA who had finished voriconazole treatment between 2005 and 2019 in a tertiary-care hospital were reviewed. IPA relapse was defined as re-diagnosis of proven or probable IPA at the same site within 1 year after treatment termination. Short course of voriconazole treatment was defined as a treatment less than 9 weeks, which is a median of the recommended minimum duration of therapy from the Infectious Disease Society of America. The radiological response was defined as a reduction in IPA burden by more than 50% on chest computed tomography. Of 87 patients who had completed voriconazole treatment, 14 (16.1%) experienced IPA relapse. Multivariable Cox regression identified that short voriconazole treatment duration (adjusted hazard ratio [aHR], 3.7; 95% confidence interval [CI], 1.1-12.3; P = 0.033) and radiological non-response (aHR, 4.6; 95% CI, 1.2-17.5; P = 0.026) were independently associated with relapse of IPA after adjusting for several clinical risk factors. Longer duration of therapy should be considered for those at higher risk of relapse.
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http://dx.doi.org/10.1038/s41598-020-73098-wDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7527978PMC
September 2020

Dynamics of viral load and anti-SARS-CoV-2 antibodies in patients with positive RT-PCR results after recovery from COVID-19.

Korean J Intern Med 2021 01 25;36(1):11-14. Epub 2020 Nov 25.

Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea.

Recently, the number of patients with coronavirus disease 2019 (COVID-19) who have tested positive for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), via the reverse transcription polymerase chain reaction (RT-PCR) test, after recovery has increased; this has caused a dilemma regarding the medical measures and policies. We evaluated the dynamics of viral load and anti-SARS-CoV-2 antibodies in four patients with positive RT-PCR results after recovery. In all patients, the highest levels of immunoglobulin G (IgG) and IgM antibodies were reached after about a month of the onset of the initial symptoms. Then, the IgG titers plateaued, and the IgM titers decreased, regardless of RT-PCR results. The IgG and IgM levels did not increase after the post-negative positive RT-PCR results in any of the patients. Our results reinforced that the post-negative positive RT-PCR results may be due to the detection of RNA particles rather than reinfection in individuals who have recovered from COVID-19.
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http://dx.doi.org/10.3904/kjim.2020.325DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7820639PMC
January 2021

Pneumocystis jirovecii pneumonia in diffuse large B-cell Lymphoma treated with R-CHOP.

Mycoses 2021 Jan 28;64(1):60-65. Epub 2020 Oct 28.

Division of Hematology-Oncology, Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea.

Background: The aim of this study was to estimate the incidence of and risk factors for Pneumocystis pneumonia (PCP) infection in diffuse large B-cell lymphoma (DLBCL) patients treated with rituximab plus cyclophosphamide, doxorubicin, vincristine and prednisone (R-CHOP).

Methods: The medical records of 739 DLBCL patients who received R-CHOP between May 2004 and January 2019 were retrospectively evaluated. Patients were divided into two groups: those who received primary PCP prophylaxis (prophylaxis group) and those who did not (control group). The incidence rate of PCP in each group was calculated, and risk factors for PCP were evaluated in the control group.

Results: Baseline characteristics were significantly different between the two groups. Compared to the 602 patients who did not receive prophylaxis, the prophylaxis group (n = 137) had poor prognostic factors of older age, high lactate dehydrogenase (LDH) levels, advanced Ann Arbour stage, and high International Prognostic Index (IPI) risk scores. None of the patients receiving PCP prophylaxis developed PCP, while the incidence of PCP in the control group was 8.1% (definite cases 5.5% and probable cases 2.7%). Out of the 49 patients who developed PCP, 10 patients (20.4%) were admitted to the intensive care unit, and the PCP-related death rate was 16.3% (8/49).

Conclusion: This study showed that PCP prophylaxis is highly effective against PCP infection and may help guide prevention of PCP during R-CHOP treatment in DLBCL patients.
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http://dx.doi.org/10.1111/myc.13184DOI Listing
January 2021

Impact of national policy on hand hygiene promotion activities in hospitals in Korea.

Antimicrob Resist Infect Control 2020 09 23;9(1):157. Epub 2020 Sep 23.

Department of Internal Medicine, Seoul National University College of Medicine, 103 Daehak-ro, Jongro-gu, Seoul,, 03080, Republic of Korea.

Background: After the Middle East respiratory syndrome coronavirus outbreak in Korea in 2015, the Government established a strategy for infection prevention to encourage infection control activities in hospitals. The new policy was announced in December 2015 and implemented in September 2016. The aim of this study is to evaluate how infection control activities improved within Korean hospitals after the change in government policy.

Methods: Three cross-sectional surveys using the WHO Hand Hygiene Self-Assessment Framework (HHSAF) were conducted in 2013, 2015, and 2017. Using a multivariable linear regression model, we analyzed the change in total HHSAF score according to survey year.

Results: A total of 32 hospitals participated in the survey in 2013, 52 in 2015, and 101 in 2017. The number of inpatient beds per infection control professionals decreased from 324 in 2013 to 303 in 2015 and 179 in 2017. Most hospitals were at intermediate or advanced levels of progress (90.6% in 2013, 86.6% in 2015, and 94.1% in 2017). In the multivariable linear regression model, total HHSAF score was significantly associated with hospital teaching status (β coefficient of major teaching hospital, 52.6; 95% confidence interval [CI], 8.9 to 96.4; P = 0.018), beds size (β coefficient of 100 beds increase, 5.1; 95% CI, 0.3 to 9.8; P = 0.038), and survey time (β coefficient of 2017 survey, 45.1; 95% CI, 19.3 to 70.9; P = 0.001).

Conclusions: After the new national policy was implemented, the number of infection control professionals increased, and hand hygiene promotion activities were strengthened across Korean hospitals.
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http://dx.doi.org/10.1186/s13756-020-00817-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7509816PMC
September 2020

Predictive scoring models for persistent gram-negative bacteremia that reduce the need for follow-up blood cultures: a retrospective observational cohort study.

BMC Infect Dis 2020 Sep 17;20(1):680. Epub 2020 Sep 17.

Department of Internal Medicine, Seoul National University Bundang Hospital, 82, Gumi-ro173 Beon-gil, Bundang-gu, Seongnam-si, Gyeonggi-do, 13620, Republic of Korea.

Background: Although the risk factors for positive follow-up blood cultures (FUBCs) in gram-negative bacteremia (GNB) have not been investigated extensively, FUBC has been routinely carried out in many acute care hospitals. We attempted to identify the risk factors and develop a predictive scoring model for positive FUBC in GNB cases.

Methods: All adults with GNB in a tertiary care hospital were retrospectively identified during a 2-year period, and GNB cases were assigned to eradicable and non-eradicable groups based on whether removal of the source of infection was possible. We performed multivariate logistic analyses to identify risk factors for positive FUBC and built predictive scoring models accordingly.

Results: Out of 1473 GNB cases, FUBCs were carried out in 1268 cases, and the results were positive in 122 cases. In case of eradicable source of infection, we assigned points according to the coefficients from the multivariate logistic regression analysis: Extended spectrum beta-lactamase-producing microorganism (+ 1 point), catheter-related bloodstream infection (+ 1), unfavorable treatment response (+ 1), quick sequential organ failure assessment score of 2 points or more (+ 1), administration of effective antibiotics (- 1), and adequate source control (- 2). In case of non-eradicable source of infection, the assigned points were end-stage renal disease on hemodialysis (+ 1), unfavorable treatment response (+ 1), and the administration of effective antibiotics (- 2). The areas under the curves were 0.861 (95% confidence interval [95CI] 0.806-0.916) and 0.792 (95CI, 0.724-0.861), respectively. When we applied a cut-off of 0, the specificities and negative predictive values (NPVs) in the eradicable and non-eradicable sources of infection groups were 95.6/92.6% and 95.5/95.0%, respectively.

Conclusions: FUBC is commonly carried out in GNB cases, but the rate of positive results is less than 10%. In our simple predictive scoring model, zero scores-which were easily achieved following the administration of effective antibiotics and/or adequate source control in both groups-had high NPVs. We expect that the model reported herein will reduce the necessity for FUBCs in GNB cases.
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http://dx.doi.org/10.1186/s12879-020-05395-8DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7499917PMC
September 2020

Pandemic preparedness of an academic medical centre in the Republic of Korea.

Clin Microbiol Infect 2020 Dec 3;26(12):1595-1599. Epub 2020 Sep 3.

Department of Internal Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine, Gyeonggi-do, Republic of Korea.

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http://dx.doi.org/10.1016/j.cmi.2020.08.032DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7470819PMC
December 2020

Defining persistent Staphylococcus aureus bacteraemia: secondary analysis of a prospective cohort study.

Lancet Infect Dis 2020 12 4;20(12):1409-1417. Epub 2020 Aug 4.

Service of Infectious Diseases, Hospital Clínic of Barcelona, Barcelona, Spain. Electronic address:

Background: Staphylococcus aureus persistent bacteraemia is only vaguely defined and the effect of different durations of bacteraemia on mortality is not well established. Our primary aim was to analyse mortality according to duration of bacteraemia and to derive a clinically relevant definition for persistent bacteraemia.

Methods: We did a secondary analysis of a prospective observational cohort study at 17 European centres (nine in the UK, six in Spain, and two in Germany), with recruitment between Jan 1, 2013, and April 30, 2015. Adult patients who were consecutively hospitalised with monomicrobial S aureus bacteraemia were included. Patients were excluded if no follow-up blood culture was taken, if the first follow-up blood-culture was after 7 days, or if active antibiotic therapy was started more than 3 days after first blood culture. The primary outcome was 90-day mortality. Univariable and time-dependent multivariable Cox regression analysis were used to assess predictors of mortality. Duration of bacteraemia was defined as bacteraemic days under active antibiotic therapy counting the first day as day 1.

Findings: Of 1588 individuals assessed for eligibility, 987 were included (median age 65 years [IQR 51-75]; 625 [63%] male). Death within 90 days occurred in 273 (28%) patients. Patients with more than 1 day of bacteraemia (315 [32%]) had higher Charlson comorbidity index and sequential organ failure assessment scores and a longer interval from first symptom to first blood culture. Crude 90-day mortality increased from 22% (148 of 672) with 1 day of bacteraemia, to 39% (85 of 218) with 2-4 days, 43% (30 of 69) with 5-7 days, and 36% (10 of 28) with more than 7 days of bacteraemia. Metastatic infections developed in 39 (6%) of 672 patients with 1 day of bacteraemia versus 40 (13%) of 315 patients if bacteraemia lasted for at least 2 days. The second day of bacteraemia had the highest HR and earliest cutoff significantly associated with mortality (adjusted hazard ratio 1·93, 95% CI 1·51-2·46; p<0·0001).

Interpretation: We suggest redefining the cutoff duration for persistent bacteraemia as 2 days or more despite active antibiotic therapy. Our results favour follow-up blood cultures after 24 h for early identification of all patients with increased risk of death and metastatic infection.

Funding: None.
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http://dx.doi.org/10.1016/S1473-3099(20)30447-3DOI Listing
December 2020

Recovery of Tenofovir-induced Nephrotoxicity following Switch from Tenofovir Disoproxil Fumarate to Tenofovir Alafenamide in Human Immunodeficiency Virus-Positive Patients.

Infect Chemother 2020 Sep 16;52(3):381-388. Epub 2020 Jul 16.

Department of Internal Medicine, Seoul National University College of Medicine, Seoul, Korea.

Background: Tenofovir disoproxil fumarate (TDF)-induced nephrotoxicity is related to high plasma tenofovir concentrations. Tenofovir alafenamide (TAF) is a tenofovir prodrug with 90% lower plasma tenofovir concentrations. The aim of this study was to evaluate changes in tenofovir-induced nephrotoxicity in Human Immunodeficiency Virus (HIV)-positive patients who switched from TDF to TAF.

Materials And Methods: We identified all HIV-positive patients who switched from elvitegravir/cobicistat/emtricitabine/TDF to elvitegravir/cobicistat/emtricitabine/TAF at a tertiary hospital. We assessed tubulopathy and renal dysfunction before TDF administration, at the time TAF was used following at least 3 months of TDF use, and 3 months after TAF administration. Tubulopathy was defined by the presence of at least three abnormalities in fractional excretion of phosphate, fractional excretion of uric acid, urinary β2-microglobulin, urinary N-acetyl-β-D-glucosaminidase, glucosuria or proteinuria. Renal dysfunction was defined as decreased by more than 25% in the estimated glomerular filtration rate (eGFR) relative to baseline.

Results: In 80 patients, the mean eGFR was 96.8 mL/min/1.73 m² before administration of TDF, 81.2 ( <0.001) at the time of change to TAF, 90.9 ( <0.001) after TAF administration. Renal dysfunction occurred in 19 patients (23.8%) after TDF use for a median 15 months, 11 (57.9%) of these patients recovered from renal dysfunction after TAF administration. Six patients (7.5%) had tubulopathy before TDF administration, 36 (45.0%) after TDF administration ( <0.001), 12 (15.0%) after TAF administration ( = 0.002).

Conclusion: Tenofovir-induced nephrotoxicity in HIV-positive patients receiving TDF was mostly reversible after changing to TAF. Thus, TAF-containing regimens can be administered safely to HIV-positive patients with tenofovir-induced nephrotoxicity.
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http://dx.doi.org/10.3947/ic.2020.52.3.381DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7533205PMC
September 2020

Development of Antibiotic Classification for Measuring Antibiotic Usage in Korean Hospitals Using a Modified Delphi Method.

J Korean Med Sci 2020 Aug 3;35(30):e241. Epub 2020 Aug 3.

Department of Internal Medicine, Yonsei University College of Medicine, Seoul, Korea.

In 2019, a project designed to develop a system for measuring and comparing antibiotic usage in hospitals was launched in Korea. As part of this project, we developed a means to classify antibiotic usage in Korean hospitals using a modified Delphi method. In results, the following categories of antibiotic classification were accepted for use in Korean hospitals: 1) broad-spectrum antibacterial agents predominantly used for hospital-onset infections in adults, 2) broad-spectrum antibacterial agents predominantly used for community-acquired infections in adults, 3) antibacterial agents predominantly used for resistant gram-positive infections in adults, 4) narrow-spectrum beta-lactam agents in adults, 5) antibacterial agents predominantly used for extensive antibiotic resistant gram-negative bacteria in adults, and 6) total antibacterial agents.
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http://dx.doi.org/10.3346/jkms.2020.35.e241DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7402924PMC
August 2020

Lung ultrasound for early diagnosis and severity assessment of pneumonia in patients with coronavirus disease 2019.

Korean J Intern Med 2020 07 1;35(4):771-781. Epub 2020 Jul 1.

Division of Infectious Diseases, Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Korea.

Background/aims: Current evidence supports lung ultrasound as a point-ofcare alternative diagnostic tool for various respiratory diseases. We sought to determine the utility of lung ultrasound for early detection of pneumonia and for assessment of respiratory failure among patients with coronavirus disease 2019 (COVID-19).

Methods: Six patients with confirmed COVID-19 by reverse transcription-polymerase chain reaction were enrolled. All had undergone chest X-ray and chest computed tomography (CT) on the day of admission and underwent multiple point-of-care lung ultrasound scans over the course of their hospitalization.

Results: Lung ultrasound detected early abnormal findings of representative B-lines in a patient with a normal chest X-ray, corresponding to ground-glass opacities on the chest CT scan. The ultrasound findings improved as her clinical condition improved and her viral load decreased. In another minimally symptomatic patient without significant chest X-ray findings, the ultrasound showed B-lines, an early sign of pneumonia before abnormalities were detected on the chest CT scan. In two critically ill patients, ultrasound was performed to assess for evaluation of disease severity. In both patients, the clinicians conducted emergency rapid sequence intubation based on the ultrasound findings without awaiting the laboratory results and radiological reports. In two children, ultrasound was used to assess the improvement in their pneumonia, thus avoiding further imaging tests such as chest CT.

Conclusion: Lung ultrasound is feasible and useful as a rapid, sensitive, and affordable point-of-care screening tool to detect pneumonia and assess the severity of respiratory failure in patients hospitalized with COVID-19.
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http://dx.doi.org/10.3904/kjim.2020.180DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7373970PMC
July 2020

Compliance of Antihypertensive Medication and Risk of Coronavirus Disease 2019: a Cohort Study Using Big Data from the Korean National Health Insurance Service.

J Korean Med Sci 2020 Jun 29;35(25):e232. Epub 2020 Jun 29.

Department of Social and Preventive Medicine, Sungkyunkwan University School of Medicine, Suwon,

Background: There is a controversy whether it is safe to continue renin-angiotensin system blockers in patients with coronavirus disease 2019 (COVID-19). We analyzed big data to investigate whether angiotensin-converting enzyme inhibitors and/or angiotensin II receptor blockers have any significant effect on the risk of COVID-19. Population-based cohort study was conducted based on the prescription data from nationwide health insurance records.

Methods: We investigated the 1,374,381 residents aged ≥ 40 years living in Daegu, the epicenter of the COVID-19 outbreak, between February and March 2020. Prescriptions of antihypertensive medication during the year before the outbreak were extracted from the National Health Insurance Service registry. Medications were categorized by types and stratified by the medication possession ratios (MPRs) of antihypertensive medications after controlling for the potential confounders. The risk of COVID-19 was estimated using a difference in difference analysis.

Results: Females, older individuals, low-income earners, and recently hospitalized patients had a higher risk of infection. Patients with higher MPRs of antihypertensive medications had a consistently lower risk of COVID-19 than those with lower MPRs of antihypertensive medications and non-users. Among patients who showed complete compliance, there was a significantly lower risk of COVID-19 for those prescribed angiotensin II receptor blockers (relative risk [RR], 0.751; 95% confidence interval [CI], 0.587-0.960) or calcium channel blockers (RR, 0.768; 95% CI, 0.601-0.980).

Conclusion: Renin-angiotensin system blockers or other antihypertensive medications do not increase the risk of COVID-19. Patients should not stop antihypertensive medications, including renin-angiotensin system blockers, because of concerns of COVID-19.
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http://dx.doi.org/10.3346/jkms.2020.35.e232DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7324263PMC
June 2020

Antibody Responses to SARS-CoV-2 at 8 Weeks Postinfection in Asymptomatic Patients.

Emerg Infect Dis 2020 10 24;26(10):2484-2487. Epub 2020 Jun 24.

We compared levels of severe acute respiratory syndrome coronavirus 2 neutralizing antibodies in recovery plasma from 7 completely asymptomatic coronavirus disease patients with those in symptomatic patients in South Korea. We found that serologic diagnostic testing was positive for 71% (5/7) of completely asymptomatic patients, but neutralizing antibody response occurred in all 7 patients.
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http://dx.doi.org/10.3201/eid2610.202211DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7510710PMC
October 2020

Microbial Etiology of Pyogenic Vertebral Osteomyelitis According to Patient Characteristics.

Open Forum Infect Dis 2020 Jun 20;7(6):ofaa176. Epub 2020 May 20.

Department of Internal Medicine, Seoul National University College of Medicine, Seoul, Republic of Korea.

Background: It is difficult to select an appropriate empirical antibiotic treatment regimen for patients with culture-negative pyogenic vertebral osteomyelitis (PVO). Having knowledge of the distribution of microorganisms according to patient characteristics can help clinicians make informed choices regarding empirical antibiotics. The aim of this study was to determine the microbial distribution among individuals with PVO according to their demographic and clinical characteristics.

Methods: We reviewed the medical records of patients admitted to our hospital with culture-confirmed PVO between January 2005 and December 2017 and collected data on demographics, underlying diseases, and radiographic and microbiological results. Statistical analysis was performed to identify associations between specific bacteria and specific patient characteristics.

Results: A total of 586 patients were included in the study. The prevalence of infections was higher in young patients than in old patients, while gram-negative bacterial infections and were more prevalent in older patients. Gram-negative bacterial infections were more common in women than in men (32.1% vs 16.4%;  < .05), in patients with cirrhosis than in those without (32.7% vs 21.1%;  < .05), and in patients with a solid tumor than in those without (31.0% vs 20.7%;  < .05). Methicillin-resistant infections were more prevalent in patients with chronic renal disease than in those without (34.4% vs 14.7%;  < .05).

Conclusions: The microbial etiology of PVO varies according to patient characteristics. Patient characteristics should thus be considered when choosing empirical antibiotics in patients with culture-negative PVO.
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http://dx.doi.org/10.1093/ofid/ofaa176DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7270706PMC
June 2020