Robert A Bonomo

Cleveland Clinic, Cleveland, Ohio, United States

Are you Robert A Bonomo?

Claim your profile

Publications (336)1391.16 Total impact

  • [Show abstract] [Hide abstract]
    ABSTRACT: Broad-range 16S ribosomal RNA gene PCR coupled with Sanger sequencing was originally employed by soil scientists and was subsequently adapted for clinical applications. PCR coupled with electrospray ionization mass spectrometry has also progressed from initial applications in the detection of organisms from environmental samples into the clinical realm and has demonstrated promise in detection of pathogens in clinical specimens obtained from patients with suspected infection but negative cultures. We review studies of multiplex PCR, 16S ribosomal RNA gene PCR and sequencing and PCR coupled with electrospray ionization mass spectrometry for detection of bacteria in specimens that were obtained from patients during or after administration of antibiotic treatment, and examine the role of each for assisting in antimicrobial treatment and stewardship efforts. Following an exploration of the available data in this field, we discuss the opportunities that the preliminary investigations reveal, as well as the challenges faced with the implementation of these strategies in clinical practice.
    Expert Review of Molecular Diagnostics 12/2014; · 4.09 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Carbapenem-resistant Klebsiella pneumoniae (CRKP) is an important healthcare-associated pathogen. We evaluated the impact of CRKP strain type and treatment on outcomes of patients with CRKP bacteriuria. Physician-diagnosed CRKP urinary tract infection (UTI)-defined as those patients who received directed treatment for CRKP bacteriuria-was studied in the multicentre, prospective Consortium on Resistance against Carbapenems in Klebsiella pneumoniae (CRaCKle) cohort. Strain typing by repetitive extragenic palindromic PCR (rep-PCR) was performed. Outcomes were classified as failure, indeterminate or success. Univariate and multivariate ordinal analyses to evaluate the associations between outcome, treatment and strain type were followed by binomial analyses. One-hundred-and-fifty-seven patients with physician-diagnosed CRKP UTI were included. After adjustment for CDC/National Healthcare Safety Network (NHSN)-defined UTI, critical illness and receipt of more than one active antibiotic, patients treated with aminoglycosides were less likely to fail therapy [adjusted OR (aOR) for failure 0.34, 95% CI 0.15-0.73, P = 0.0049]. In contrast, patients treated with tigecycline were more likely to fail therapy (aOR for failure 2.29, 95% CI 1.03-5.13, P = 0.0425). Strain type data were analysed for 55 patients. The predominant clades were ST258A (n = 18, 33%) and ST258B (n = 26, 47%). After adjustment for CDC/NHSN-defined UTI and use of tigecycline and aminoglycosides, infection with strain type ST258A was associated with clinical outcome in ordinal analysis (P = 0.0343). In multivariate binomial models, strain type ST258A was associated with clinical failure (aOR for failure 5.82, 95% CI 1.47-28.50, P = 0.0113). In this nested cohort study of physician-diagnosed CRKP UTI, both choice of treatment and CRKP strain type appeared to impact on clinical outcomes. © The Author 2014. Published by Oxford University Press on behalf of the British Society for Antimicrobial Chemotherapy. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com.
    Journal of Antimicrobial Chemotherapy 12/2014; · 5.34 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Pseudomonas aeruginosa is a notoriously difficult-to-treat pathogen that is a common cause of severe nosocomial infections. By investigating a collection of β-lactam resistant P. aeruginosa clinical isolates from a decade ago, we uncovered resistance to ceftazidime-avibactam, a novel β-lactam-β-lactamase inhibitor combination. The isolates were systematically analyzed through a variety of genetic, biochemical, genomic, and microbiological methods to understand how resistance manifests to a unique drug combination that is not yet clinically released. We discovered that avibactam was able to inactivate different AmpC β-lactamase enzymes and that blaPDC regulatory elements and penicillin-binding protein differences did not contribute in a major way to resistance. By using carefully selected combinations of antimicrobial agents, we deduced that the greatest barrier to ceftazidime-avibactam is membrane permeability and drug efflux. To overcome the constellation of resistance determinants, we show that a triple combination of antimicrobial agents targeting multiple cell wall synthetic pathways can restore susceptibility. In P. aeruginosa, efflux, as a general mechanism of resistance, may pose the greatest challenge to future antibiotic development. Our unexpected findings create concern that even the developing of antimicrobial agents targeted for the treatment of multidrug-resistant bacteria may encounter clinically important resistance. The development of antibiotic therapy in the future must consider these factors. Copyright © 2014, American Society for Microbiology. All Rights Reserved.
    Antimicrobial Agents and Chemotherapy 12/2014; · 4.57 Impact Factor
  • Federico Perez, Javier Adachi, Robert A Bonomo
    [Show abstract] [Hide abstract]
    ABSTRACT: Patients with cancer are at high risk for infections caused by antibiotic resistant gram-negative bacteria. In this review, we summarize trends among the major pathogens and clinical syndromes associated with antibiotic resistant gram-negative bacterial infection in patients with malignancy, with special attention to carbapenem and expanded-spectrum β-lactam resistance in Escherichia coli, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Stenotrophomonas maltophilia-all major threats to our cancer patients. Optimal therapy for these antibiotic-resistant pathogens still remains to be determined.
    Clinical infectious diseases : an official publication of the Infectious Diseases Society of America. 11/2014; 59 Suppl 5:S335-9.
  • [Show abstract] [Hide abstract]
    ABSTRACT: The emergence of multidrug-resistant (MDR) Klebsiella pneumoniae (Kp) has resulted in a more frequent reliance on treatment using colistin. However, resistance to colistin (ColR) is increasingly reported from clinical settings. The genetic mechanisms that lead to colR are not fully characterized in K. pneumoniae. Using a combination of genome sequencing and transcriptional profiling by RNA-seq analysis, distinct genetic mechanisms were found among nine ColR clinical isolates. ColR was related to mutations in three different genes in Kp strains, with distinct impacts on gene expression. Up-regulation of the pmrH operon encoding 4-amino-4-deoxy-L-arabinose (Ara4N) modification of lipid A was found in all ColR strains. Alteration of the mgrB gene was observed in six strains. One strain had a mutation in phoQ. Common among these seven strains was elevated expression of phoPQ and unaltered expression of pmrCAB which is involved in phosphoethanolamine addition to LPS. In two strains, separate mutations were found in a previously uncharacterized histidine kinase gene that is part of a two-component regulatory system (TCRS) now designated crrAB. In these strains, expression of pmrCAB, crrAB, and an adjacent glycosyltransferase gene were elevated, but not phoPQ. The crrAB genes are present in most Kp genomes, but not in Escherichia coli. Complementation with the wild-type allele restored colistin susceptibility in both strains. Additional up-regulated genes in all strains include those involved in cation transport and maintenance of membrane integrity. Because the crrAB genes are only present in some strains, ColR mechanisms may be dependent on the genetic background.
    Antimicrobial Agents and Chemotherapy 11/2014; · 4.57 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: β-lactam resistance in Acinetobacter baumannii presents one of the greatest challenges to contemporary antimicrobial chemotherapy. Much of this resistance to cephalosporins derives from the expression of the class C β-lactamase enzymes, known as Acinetobacter-derived cephalosporinases (ADCs). Currently, β-lactamase inhibitors are structurally similar to β-lactam substrates and are not effective inactivators of this class C cephalosporinase. Herein, two boronic acid transition state inhibitors (BATSIs S02030 and SM23) that are chemically distinct from β-lactams were designed and tested for inhibition of ADC enzymes. BATSIs SM23 and S02030 bind with high affinity to ADC-7, a chromosomal cephalosporinase from Acinetobacter baumannii (Ki = 21.1 ± 1.9 nM and 44.5 ± 2.2 nM, respectively). The X-ray crystal structures of ADC-7 were determined in both the apo form (1.73 Å resolution) and in complex with S02030 (2.0 Å resolution). In the complex, S02030 makes several canonical interactions: the O1 oxygen of S02030 is bound in the oxyanion hole, and the R1 amide group makes key interactions with conserved residues Asn152 and Gln120. In addition, the carboxylate group of the inhibitor is meant to mimic the C3/C4 carboxylate found in β-lactams. The C3/C4 carboxylate recognition site in class C enzymes is comprised of Asn346 and Arg349 (AmpC numbering), and these residues are conserved in ADC-7. Interestingly, in the ADC-7/S02030 complex, the inhibitor carboxylate group is observed to interact with Arg340, a residue that distinguishes ADC-7 from the related class C enzyme AmpC. A thermodynamic analysis suggests that ΔH driven compounds may be optimized to generate new lead agents. The ADC-7/BATSI complex provides insight into recognition of non-β-lactam inhibitors by ADC enzymes and offers a starting point for the structure-based optimization of this class of novel β-lactamase inhibitors against a key resistance target.
    Biochemistry 11/2014; · 3.38 Impact Factor
  • The Journal of infectious diseases. 11/2014;
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: This study examines metal binding to metallo-β-lactamase VIM-2, demonstrating the first successful preparation of a Co(II)-substituted VIM-2 analog. Spectroscopic studies of the half- and fully-metal loaded enzymes show that both Zn(II) and Co(II) bind cooperatively, where the major species present, regardless of stoichiometry, are apo- and di-Zn (or di-Co) enzymes. We determined the di-Zn VIM-2 structure to a resolution of 1.55 Å, and this structure supports results from spectroscopic studies. Kinetics, both steady-state and pre-steady-state, show that VIM-2 utilizes a mechanism that proceeds through a very short-lived anionic intermediate when chromacef is used as the substrate. Comparison with other B1 enzymes shows that those that bind Zn(II) cooperatively are better poised to protonate the intermediate on its formation, compared to those that bind Zn(II) non-cooperatively, which uniformly build up substantial amounts of the intermediate.
    Biochemistry 10/2014; · 3.38 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Background: Carbapenem Resistant Klebsiella Pneumoniae (CRKP) is an emerging threat, and hospital readmissions of patients with persistent or recurrent CRKP may contribute to the spread of CRKP. We evaluated CRKP readmissions in the Consortium on Resistance against Carbapenems in K. pneumoniae (CRaCKle). Methods: CRaCKle is a prospective multicenter consortium which includes 21 hospitals in the Great Lakes region. All hospitalized patients who were discharged alive were included, if their hospitalization during which CRKP was isolated began and ended between 12/24/2011 and 7/1/2013. Each patient was included once at the time of the first CRKP positive culture. Standard criteria were used to define infection. All readmissions during which CRKP was again found (CRKP readmission) were documented. Risk factors for CRKP readmission were evaluated in multivariable logistic models. Kaplan-Meier curve was used to compare time to readmission. Results: 287 unique patients were included; 109 (38%) with CRKP infection. Most CRKP was recovered from urine (192, 67%). 56 (20%) patients had a CRKP readmission within 90 days. Risk factors for CRKP readmission included history of cancer (OR 2.74 95%CI 1.22-5.96, p=0.01), and renal insufficiency (OR 2.06, 95%CI 1.05-3.96, p=0.03). 160/287 (56%) of patients received anti-CRKP antibiotic treatment during their index hospitalization. In these 160 patients, 65/160 (41%) received aminoglycoside-based regimens, 49/160 (31%) tigecycline-based regimens, 27/160 (17%) colistin-based regimens, and 19/160 (12%) other regimens. Receiving a tigecycline-based regimen was associated with an increased risk for CRKP readmission; 14/49 (28%) of patients who received tigecycline were readmitted within 90 days, as compared to 16/111 (14%) of all other treatment regimens. The OR for tigecycline for 90-day CRKP readmission was 2.71 (95%CI 1.14-6.48, p=0.02) after adjusting for infection status, source, renal failure, and cancer history. Conclusion: Hospitalized patients with CRKP are at high risk of readmission with recurrent CRKP which may contribute to the spread of CRKP in health care systems. Treatment during index hospitalization with a tigecycline-based regimen may increase that risk.
    IDWeek 2014 Meeting of the Infectious Diseases Society of America; 10/2014
  • [Show abstract] [Hide abstract]
    ABSTRACT: Background: A. baumannii is commonly recognized as an emerging multi-drug resistant (MDR) organism frequently impervious to majority of the commonly prescribed antibiotics. Colistin is one of the few therapeutic agents which possess activity against this pathogen, and its use has dramatically increased. As a result, colistin resistance is increasingly reported among A. baumannii and presents a unique challenge. Methods: A cluster of colistin-resistant A. baumannii cases at Detroit Receiving Hospital were identified from May 1st, 2013 to October 31st, 2013. Colistin resistance was defined as an MIC of >2 μg/ml (E-test). Epidemiologic data for these cases were collected and isolates assayed for clonality with Diversilab rep-PCR and multi-locus sequence typing (ST). Results: 11 cases were identified. The mean age of the patients was 48.8 years (range 17-76) and 10 (91%) resided in one of two intensive care units. All patients were treated with broad spectrum antimicrobials (but not colistin) prior to isolation of the colistin-resistant isolate. 9 (82%) patients were mechanically ventilated and the pathogen was detected from sputum specimen in 8 (73%) of patients. Other features frequently identified in these cases were the use of glucometer (73%) and tube feeds (82%). Colistin MIC ranged from 3-32. Environmental surveillance cultures were performed, but only one specimen was positive for the same organism. Genotyping was performed on 5 patient isolates which revealed 95% similarity between strains (Figure 1) and all isolates were ST281. In order to contain the outbreak, optimal infection prevention practices were reinforced, active surveillance screening of high risk patients implemented, with presumptive contact isolation. Conclusion: To our knowledge this is the first reported outbreak of colistin-resistant A. baumannii in United States. The hands of healthcare workers and environmental reservoirs are hypothesized to be the source of the outbreak. We observed a wide range of colistin MICs among outbreak strains, possibly due to 1) the emergence of heteroresistance or 2) differences in the population structure. A case-control study will help to further help delineate the cause of the outbreak. Genotype results (Figure 1):
    IDWeek 2014 Meeting of the Infectious Diseases Society of America; 10/2014
  • [Show abstract] [Hide abstract]
    ABSTRACT: Klebsiella pneumoniae carbapenemases (KPCs) were first identified in 1996 in the USA. Since then, regional outbreaks of KPC-producing K. pneumoniae (KPC-Kp) have occurred in the USA, and have spread internationally. Dissemination of blaKPC involves both horizontal transfer of blaKPC genes and plasmids, and clonal spread. Of epidemiological significance, the international spread of KPC-producing K. pneumoniae is primarily associated with a single multilocus sequence type (ST), ST258, and its related variants. However, the molecular factors contributing to the success of ST258 largely remain unclear. In this review, we discuss the recent progresses in understanding KPC-producing K. pneumoniae that are contributing to our knowledge of plasmid and genome composition and structure among the KPC epidemic clone, and we identify possible factors that influence its epidemiological success.
    Ttrends in microbiology. 10/2014;
  • Source
    Antimicrobial Agents and Chemotherapy 10/2014; 58(10):6343. · 4.57 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: We describe the first reported case of acute respiratory distress syndrome (ARDS) attributed to Neosartorya udagawae infection which grew rapidly in cultures of multiple respiratory specimens from a previously healthy 43-year-old women. Neosartorya spp. are a recently recognized cause of invasive disease in immunocompromised patients that can be mistaken for their sexual teleomorph, Aspergillus fumigatus. Because the cultures were sterile, phenotypic identification was not possible. DNA sequencing of ITS, calmodulin and β-tubulin genes supported identification of Neosartorya udagawae. Our case is the first report of ARDS associated with Neosartorya sp. infection and defines a new clinical entity.
    Medical Mycology Case Reports. 10/2014;
  • Emerging infectious diseases. 09/2014; 20(9):1583-1585.
  • [Show abstract] [Hide abstract]
    ABSTRACT: Currently, Acinetobacter baumannii is recognized as one of the major pathogens seriously threatening our health care delivery system. Aspects of the innate immune response to A. baumannii infection are not yet well understood. Human β-defensins (hBDs) are epithelial-derived cationic antimicrobial peptides (AMPs) that also function to bridge the innate and adaptive immune system. We tested induction of hBD-2 and -3 by A. baumannii on primary oral and skin epithelial cells and found that A. baumannii induces hBD-3 transcripts to a greater extent than hBD-2 on both types of cells. In addition, we found that A. baumannii are susceptible to hBD-2 and -3 killing at sub-μM concentrations. Moreover, hBD-3 induction by A. baumannii was found to be dependent on epidermal growth factor receptor (EGFR) signaling. Inhibition of MAP kinase resulted in reduced expression of both hBD-2 and -3. Lastly, a disintegrin and metalloprotease 17 (ADAM17, also known as TACE) was found to be critical for hBD-3 induction, while ADAM10 and dual oxidase 1 (Duox1) were not required for hBD-3 induction. Induction of AMPs is an important component of innate sensing of pathogens and may play an important role in triggering systemic immune responses to A. baumannii infection. Further studies on the interactions between epithelial cells and A. baumannii will help us understand early stages of infection and may shed light on why some individuals are more vulnerable to A. baumannii infection.
    Infection and immunity. 08/2014;
  • [Show abstract] [Hide abstract]
    ABSTRACT: In Gram-negative bacteria, resistance to β-lactam antibacterials is largely due to β-lactamases and is a growing public health threat.One of the most concerning β-lactamases to evolve in bacteria are the class B enzymes, the metallo-β-lactamases (MBLs). To date, penams and cephems resistant to hydrolysis by MBLs have not yet been found. As a result of this broad substrate specificity, a better understanding of the role of catalytically important amino acids in MBLs is necessary to design novel β-lactams and inhibitors. Two MBLs, the wild type IMP-1 with serine at position 262, and an engineered variant with valine at the same position (IMP-1-S262V), were previously found to exhibit very different substrate spectra.These findings compelled us to investigate the impact of a threonine at position 262 (IMP-1-S262T) on the substrate spectrum. Here, we explore MBL sequence-structure-activity relationships by predicting and experimentally validating the effect of the S262T substitution in IMP-1. Using site-directed mutagenesis,threonine was introduced at position 262, and the IMP-1-S262T enzyme, as well as the other two enzymes IMP-1 and IMP-1-S262V, were purified and kinetic constants were determined against a range of β-lactam antibacterials. Catalytic efficiencies (kcat/Km) obtained with IMP-1-S262T and minimum inhibitory concentrations (MICs)observed with bacterial cells expressing the protein were intermediate or comparable to the corresponding values with IMP-1 and IMP-1-S262V, validating the role of this residue in catalysis.Our results reveal the important role of IMP S262 in β-lactam turnover and support this approach to predict activities of certain novel MBL variants.
    Protein Science 08/2014; · 2.74 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Carbapenems are a mainstay of treatment for infections caused by Pseudomonas aeruginosa. Carbapenem-resistance mediated by metallo-β-lactamases (MBLs) remains uncommon in the United States, despite the worldwide emergence of this group of enzymes. Between March 2012 and May 2013, we detected MBL-producing P. aeruginosa in a university-affiliated healthcare system in Northeast Ohio. We examined the clinical characteristics and outcomes of patients, defined the resistance determinants and structure of the genetic element harboring the blaMBL gene through genome sequencing, and typed MBL-producing P. aeruginosa using pulsed-field gel electrophoresis (PFGE), repetitive sequence-based PCR (rep-PCR), and multilocus sequence typing (MLST). Seven patients were affected, hospitalized at three community hospitals, a long term care facility, and a tertiary care center; one of the patients died as a result of infection. Isolates belonged to sequence type ST233, and were extensively drug resistant (XDR), including resistance to all fluoroquinolones, aminoglycosides and β-lactams; two isolates were non-susceptible to colistin. The blaMBL gene was identified as blaVIM-2 contained within a class 1 integron (In559), similar to the cassette array previously detected in isolates from Norway, Russia, Taiwan, and Chicago. Genomic sequencing and assembly revealed that In559 was part of a novel 35 Kb region that also included a Tn501-like transposon and Salmonella Genomic Island 2 (SGI2) homologous sequences. This analysis of XDR strains producing VIM-2 from Northeast Ohio revealed a novel recombination event between Salmonella and P. aeruginosa, heralding a new antibiotic resistance threat in this region's health care system.
    Antimicrobial Agents and Chemotherapy 07/2014; · 4.57 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: By reacting fluorescein isothiocyanate with meropenem, we have prepared a carbapenem-based fluorescent β-lactam. Fluorescein-meropenem binds both penicillin binding proteins and β-lactam sensors, and undergoes a typical acylation reaction in the active site of these proteins. The probe binds the class D carbapenemase OXA-24/40 with close to the same affinity as meropenem, and undergoes a complete catalytic hydrolysis reaction. The visible light excitation and strong emission of fluorescein render this molecule a useful structure-function probe through its application in SDS-polyacrylamide gel electrophoresis assays, as well as solution-based kinetic anisotropy assays. Its classification as a carbapenem β-lactam and the position of its fluorescent modification render it a useful complement to other fluorescent β-lactams, most notably Bocillin FL. In this study we show the utility of fluorescein-meropenem by using it to detect mutants of OXA-24/40 that arrest at the acyl-intermediate state with carbapenem substrates, but maintain catalytic competency with penicillin substrates.
    Analytical Biochemistry 07/2014; · 2.58 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Anaerobic bacteria are often difficult to detect, especially after the initiation of antibiotics. We describe the application of PCR electrospray ionization mass spectrometry (PCR/ESI-MS) using a sample of cerebrospinal fluid to identify an anaerobic gram negative bacillus, Fusobacterium nucleatum, in a patient with "culture negative" meningitis and cerebral abscesses.
    Journal of clinical microbiology. 06/2014;
  • [Show abstract] [Hide abstract]
    ABSTRACT: Carbapenem-resistant Klebsiella pneumoniae (CRKP) is an increasing global threat. Here, we describe the prevalence and impact of tigecycline use in a cohort of patients with CRKP bacteriuria nested within a multicenter, prospective study. In the 21 month study period, 260 unique patients were included. Tigecycline was given to 80 (31%) patients. The use of tigecycline during the index hospitalization was significantly associated with the subsequent development of tigecycline resistance in the same patient (OR 6.13, 95%CI 1.15-48.65, p=0.03). In conclusion, the use of tigecycline with CRKP bacteriuria is common, and is associated with the subsequent development of tigecycline resistance. This article is protected by copyright. All rights reserved.
    Clinical Microbiology and Infection 06/2014; · 4.58 Impact Factor

Publication Stats

7k Citations
1,391.16 Total Impact Points

Institutions

  • 2014
    • Cleveland Clinic
      Cleveland, Ohio, United States
  • 2012–2014
    • United States Department of Veterans Affairs
      Bedford, Massachusetts, United States
    • Los Angeles Biomedical Research Institute at Harbor-UCLA Medical Center
      Torrance, California, United States
    • University of Minnesota Duluth
      Duluth, Minnesota, United States
    • Albert Einstein College of Medicine
      • Department of Medicine
      New York City, NY, United States
    • OSF Saint Francis Medical Center
      Peoria, Illinois, United States
    • St. John's Medical Center
      Jackson, Wyoming, United States
  • 2002–2014
    • Case Western Reserve University School of Medicine
      • • Department of Medicine
      • • Department of Pathology
      • • Division of Infectious Diseases and HIV Medicine
      • • Department of Pharmacology
      Cleveland, Ohio, United States
  • 1996–2014
    • Louis Stokes Cleveland VA Medical Center
      Cleveland, Ohio, United States
  • 1992–2014
    • Case Western Reserve University
      • • Department of Molecular Biology and Microbiology
      • • Department of Biochemistry
      • • School of Medicine
      • • Department of Oral Pathology
      • • Department of Medicine (University Hospitals Case Medical Center)
      • • Department of Chemistry
      • • Division of Infectious Diseases and HIV Medicine
      Cleveland, Ohio, United States
  • 2013
    • Rutgers, The State University of New Jersey
      New Brunswick, New Jersey, United States
    • Southern Illinois University School of Medicine
      Springfield, Illinois, United States
    • Universität Bern
      • Institute of Veterinary Bacteriology
      Bern, BE, Switzerland
    • Northeast Ohio Medical University
      Ravenna, Ohio, United States
  • 2011–2013
    • Rutgers New Jersey Medical School
      • Public Health Research Institute
      Newark, NJ, United States
    • Mount Sinai School of Medicine
      • Department of Medicine
      Manhattan, NY, United States
    • University at Buffalo, The State University of New York
      Buffalo, New York, United States
    • Wayne State University
      Detroit, Michigan, United States
    • Jersey Shore University Medical Center
      Neptune City, New Jersey, United States
    • Catholic University of Louvain
      Walloon Region, Belgium
    • Centre Hospitalier Universitaire de Clermont-Ferrand
      Clermont, Auvergne, France
  • 2008–2013
    • Grand Valley State University
      • Department of Chemistry
      Grand Rapids, MI, United States
    • University of Queensland
      Brisbane, Queensland, Australia
    • Josai International University
      Tiba, Chiba, Japan
  • 2011–2012
    • Detroit Medical Center
      Detroit, Michigan, United States
  • 2007–2012
    • Emory University
      • Department of Microbiology and Immunology
      Atlanta, GA, United States
  • 1997–2012
    • Cleveland State University
      • Department of Chemistry
      Cleveland, Ohio, United States
  • 2010–2011
    • Southern Methodist University
      • Department of Chemistry
      Dallas, TX, United States
    • Instituto de Investigación Biomédica de A Coruña
      La Corogne, Galicia, Spain
  • 2008–2010
    • University of California, Berkeley
      • Biophysics Graduate Group
      Berkeley, MO, United States
  • 2000–2010
    • U.S. Department of Veterans Affairs
      Washington, Washington, D.C., United States
  • 2001–2009
    • University of Pittsburgh
      • Division of Infectious Diseases
      Pittsburgh, PA, United States
  • 2006
    • University of California, San Diego
      • Skaggs School of Pharmacy and Pharmaceutical Sciences
      San Diego, CA, United States
  • 2005
    • Semmelweis University
      • Department of Medical Microbiology
      Budapest, Budapest fovaros, Hungary
  • 2003–2004
    • University of Connecticut
      • Department of Molecular and Cell Biology
      Storrs, CT, United States
  • 1999
    • National and Kapodistrian University of Athens
      • Faculty of Medicine
      Athens, Attiki, Greece