David Y Graham

Baylor College of Medicine, Houston, Texas, United States

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Publications (558)3509.42 Total impact

  • Source
    BMC Immunology 12/2015; 16(1). · 2.25 Impact Factor
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    ABSTRACT: The most recent information published on resistance of Helicobacter pylori to antibiotics in a large population in the United States is more than 10 y old. We assessed the susceptibility of H pylori to antibiotics among patients in a large metropolitan hospital, as well as demographic, clinical, and life-style factors associated with antimicrobial resistance. We performed a cross-sectional study at the Houston Veterans Affairs Medical Center of a random sample of 656 patients (90.2% men) from a cohort of 1559 undergoing esophagastroduodenoscopy with collection of gastric biopsies from 2009 through 2013. We performed culture analyses of gastric tissues to detect H pylori. The minimum inhibitory concentrations of amoxicillin, clarithromycin, metronidazole, levofloxacin, and tetracycline were determined by the Epsilometer test. Logistic regression analysis was performed to estimate the association between risk factors and antimicrobial resistance. Biopsies from 135 subjects (20.6%) tested positive for H pylori; 128 of these were from men (94.8%). Only 65 strains were susceptible to all 5 antibiotics. The prevalence of resistance to levofloxacin was 31.3% (95% confidence interval [CI], 23.1-39.4), to metronidazole was 20.3% (95% CI, 13.2-27.4), to clarithromycin was 16.4% (95% CI, 9.9-22.9), and to tetracycline was 0.8% (95% CI, 0.0-2.3). No isolate was resistant to amoxicillin. Clarithromycin resistance increased from 9.1% in 2009-2010 to 24.2% in 2011-2013. In multivariate analysis, prior treatment of H pylori infection and use of fluoroquinolones were significantly associated with clarithromycin and levofloxacin resistance, respectively. H pylori resistance to clarithromycin increased between 2009 and 2013; resistance to metronidazole remains high in infected men in the US. The high frequency of resistance to levofloxacin is a new and concerning finding. Copyright © 2015 AGA Institute. Published by Elsevier Inc. All rights reserved.
    02/2015;
  • David Y. Graham
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    ABSTRACT: Helicobacter pylori infection contributes to development of diverse gastric and extra-gastric diseases. The infection is necessary but not sufficient for development of gastric adenocarcinoma. Its eradication would eliminate a major worldwide cause of cancer death, so there is much interest in identifying how, if, and when this can be accomplished. There are several mechanisms by which H pylori contributes to development of gastric cancer. Gastric adenocarcinoma is one of many cancers associated with inflammation, which is induced by H pylori infection, yet the bacteria also cause genetic and epigenetic changes that lead to genetic instability in gastric epithelial cells. H pylori eradication reduces both. However, many factors must be considered in determining whether treating this bacterial infection will prevent cancer or only reduce its risk—these must be considered in designing reliable and effective eradication therapies. Furthermore, H pylori infection has been proposed to provide some benefits, such as reducing the risks of obesity or childhood asthma, although there are no convincing data to support the benefits of H pylori infections.
    Gastroenterology 02/2015; · 12.82 Impact Factor
  • The Journal of infectious diseases. 01/2015;
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    ABSTRACT: The human noroviruses (NoVs) are genetically diverse, rapidly evolving RNA viruses and are the major cause of epidemic gastroenteritis of humans. Serum antibodies that block the interaction of NoVs and NoV virus-like particles (VLPs) with host attachment factors are considered surrogate neutralizing antibodies in the absence of cell culture and small animal replication models for the human NoVs. A serological assay for NoV blocking antibodies was used to assess the breadth of the heterotypic antibody response in the context of an experimental challenge study with a human NoV. Heterotypic HBGA-blocking activity against GI.4, GI.7, and GII.4 NoVs increased significantly in the serum of individuals (n=18) infected with Norwalk virus (GI.1). Although the fold increases and peak titers of heterotypic antibody were more modest than titers of antibody reactive with the challenge antigen, Norwalk virus infection elicited a serological rise even against the novel Sydney variant of GII.4 NoVs. These observations indicate that the development of a broadly cross-protective NoV vaccine containing a limited number of genotypes may be possible. Copyright © 2014, American Society for Microbiology. All Rights Reserved.
    Clinical and vaccine Immunology: CVI 12/2014; · 2.37 Impact Factor
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    ABSTRACT: Molecular testing can rapidly detect H. pylori susceptibility using gastric biopsies. ASP-PCR was used to identify H. pylori 23S rRNA and gyrA mutation using gastric biopsies from Colombian patients and confirmed by PCR and sequencing of the 23S rRNA and gyrA genes. The sensitivity and specificity of ASP-PCR were compared with susceptibilities measured by agar dilution. Samples included gastric biopsies from 107 biopsies with H. pylori infections and 20 H. pylori negative. The sensitivity and specificity of ASP-PCR for the 23S rRNA gene were both 100%. The sensitivity and specificity of ASP-PCR for the gyrA gene, published in 2007 by Nishizawa et al., were 52% and 92.7% respectively; the lower sensitivity was due to the presence of mutations N87I in our samples which were not detected by the test. In this study we designed new primers to detect the mutation N87I in GyrA. The ASP-PCR was performed with the original primers plus the new primers. The molecular test with the new primers improved the sensitivity to 100%. In conclusion, ASP-PCR provides a specific and rapid means of predicting resistance to clarithromycin and levofloxacin in gastric biopsies.
    Diagnostic Microbiology and Infectious Disease. 12/2014;
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    ABSTRACT: Background Helicobacter pylori infection produces progressive mucosal damage that may eventually result in gastric cancer. We studied the changes that occurred in the presence and severity of atrophic gastritis and the prevalence of H. pylori infection that occurred coincident with improvements in economic and hygienic conditions in Japan since World War II.Materials and Methods The prevalence of H. pylori infection and histologic grades of gastric damage were retrospectively evaluated using gastric biopsy specimens obtained over a 40-year period. Gastric atrophy and intestinal metaplasia were scored using the updated Sydney classification system.ResultsThe prevalence of H. pylori and severity of atrophy were examined in 1381 patients including 289 patients examined in the 1970s (158 men; mean age, 44.9 years), 787 in the 1990s (430 men; 44.2 years), and 305 in the 2010s (163 men; 53.2 years). Overall, the prevalence of H. pylori infection decreased significantly from 74.7% (1970s) to 53% (1990s) and 35.1% (2010s) (p < .01). The prevalence of atrophy in the antrum and corpus was significantly lower in the 2010s (33, 19%, respectively) compared to those evaluated in either the 1970s (98, 82%) (p < .001) or 1990s (80, 67%) (p < .001). The severity of atrophy and intestinal metaplasia also declined remarkably among those with H. pylori infection.Conclusions There has been a progressive and rapid decline in the prevalence of H. pylori infection as well a fall in the rate of progression of gastric atrophy among H. pylori-infected Japanese coincident with the westernization and improvements in economic and hygienic conditions in Japan since World War II.
    Helicobacter 12/2014; · 2.99 Impact Factor
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    ABSTRACT: OBJECTIVES:Esophageal adenocarcinoma is more common among non-Hispanic Whites (NHWs) than African Americans (AAs). It is unclear whether its precursor, Barrett's esophagus (BE), is also less common among AAs, and whether differences in risk factor profiles explain the racial disparity.METHODS:Data were from a case-control study among eligible Veterans Affairs patients scheduled for an upper endoscopy, and a sample identified from primary care clinics. Participants completed a questionnaire on sociodemographic and clinical factors and underwent a study esophagogastroduodenoscopy. We calculated race-specific BE prevalence rates and used logistic regression to estimate odds ratios (ORs) and 95% confidence intervals (95% CIs) for BE.RESULTS:There were 301 BE cases and 1,651 controls. BE prevalence was significantly higher among NHWs than AAs (21.3 vs. 5.0%; P<0.001). NHWs were more likely than AAs to be male, have a high waist-to-hip ratio (WHR), hiatal hernia, and use proton-pump inhibitors (PPIs), but less likely to have Helicobacter pylori (P<0.001). Among cases, NHWs were more likely to have long-segment BE and dysplasia than AAs. Independent BE risk factors for AAs included a hiatus hernia ≥3 cm (OR 4.12; 95% CI, 1.57-10.81) and a history of gastroesophageal reflux disease or PPI use (OR, 3.70; 95% CI, 1.40-9.78), whereas high WHR (OR, 2.82; 95% CI, 1.41-5.63), hiatus hernia ≥3 cm (OR, 4.95; 95% CI, 3.05-8.03), PPI use (OR, 1.88; 95% CI, 1.33-2.66), and H. pylori (OR, 0.64; 95% CI, 0.41-0.99) were statistically significantly associated with BE risk for NHWs. Among all cases and controls, race was a risk factor for BE, independent of other BE risk factors (OR for AAs, 0.26; 95% CI, 0.17-0.38).CONCLUSIONS:Among veterans, the prevalence of BE was lower in AAs compared with NHWs. This disparity was not accounted for by differences in risk estimates or prevalence of risk factors between NHWs and AAs.Am J Gastroenterol advance online publication, 25 November 2014; doi:10.1038/ajg.2014.351.
    The American Journal of Gastroenterology 11/2014; · 9.21 Impact Factor
  • David Y Graham, Masahiro Asaka
    JNCI Journal of the National Cancer Institute 11/2014; 106(11). · 15.16 Impact Factor
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    ABSTRACT: The outcomes of Helicobacter pylori infection vary geographically. H. pylori strains, disease presentation, and environments differ markedly in Bhutan and Dominican Republic. The aims were to compare the strains, histology and expression of interleukin (IL)-8 and IL-10 from gastric mucosa from the two countries. H. pylori status was assessed by the combination of rapid urease test, culture and histology. Histology was evaluated using the updated Sydney System and cytokines in gastric biopsies were measured using real-time PCR. There were 138 subjects from Bhutan and 155 from Dominican Republic. The prevalence of H. pylori infection was 65% and 59%, respectively. The genotype of cagA was predominantly East-Asian type in Bhutan vs. Western type in Dominican Republic. Gastritis severity was significantly higher in H. pylori-infected subjects from Bhutan than those from Dominican Republic. IL-8 expression by H. pylori-infection was 5.5-fold increase in Bhutan vs. 3-fold in Dominican Republic (p <0.001); IL-10 expression was similar. IL-8 expression levels among H. pylori-infected cases tended to be positively correlated with polymorphonuclear leucocyte (PMN) and monocyte infiltration (MNC) scores in both countries. IL-8 expression among those with grade 2 and 3 PMN and MNC was significantly higher in Bhutan than in Dominican Republic. The difference in IL-8 expression in two countries is reflected in the different disease pattern between them. Whether the dominant factor is differences in H. pylori virulence, in host-H. pylori-environmental interactions, genetic factors or all remains unclear. However, severity of inflammation appears to be a critical factor in disease pathogenesis. We compared IL-8 mRNA levels between high gastric cancer risk country; Bhutan (mainly East Asian type H. pylori) and lower gastric cancer risk country; Dominican Republic (mainly Western type H. pylori).
    Human pathology 10/2014; · 2.81 Impact Factor
  • Source
    The Journal of Infectious Diseases 09/2014; · 5.78 Impact Factor
  • Akiko Shiotani, Ken Haruma, David Y Graham
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    ABSTRACT: The high incidence of gastric cancer in Japan initially resulted in establishment of a country-wide gastric cancer screening program to detect early and treatable cancers. In 2013 countrywide Helicobacter pylori (H. pylori) eradication was approved coupled with endoscopy to assess for the presence of chronic gastritis. Current data support the notion that cure of the infection in those with non-atrophic gastritis will prevent development of gastric cancer. However, while progression to more severe damage is halted in those who have already developed, atrophic gastritis/gastric atrophy remain at risk for subsequent development of gastric cancer. That risk is directly related to the extent and severity of atrophic gastritis. Methods to stratify cancer risk include those based on endoscopic assessment of the atrophic border, histologic grading, and non-invasive methods based on serologic testing of pepsinogen levels. Continued surveillance is required because those with atrophic gastritis/gastric atrophy retain considerable gastric cancer risk even after H. pylori eradication. Those who have already experienced a resectable early gastric cancer are among those at highest risk as metachronous lesions are frequent even after H. pylori eradication. We review the role of H. pylori and effect of H. pylori eradication indicating the incidence and the predictive factors on development of metachronous cancer after endoscopic therapy of early gastric cancer. Studies to refine risk markers to stratify for risk, surveillance methods, intervals, and duration after successful H. pylori eradication, and whether adjuvant therapy would change risk are needed.
    World Journal of Gastroenterology 09/2014; 20(33):11552-11559. · 2.43 Impact Factor
  • Tony Trang, Johanna Chan, David Y Graham
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    ABSTRACT: Restitution of normal fat absorption in exocrine pancreatic insufficiency remains an elusive goal. Although many patients achieve satisfactory clinical results with enzyme therapy, few experience normalization of fat absorption, and many, if not most, will require individualized therapy. Increasing the quantity of lipase administered rarely eliminates steatorrhea but increases the cost of therapy. Enteric coated enzyme microbead formulations tend to separate from nutrients in the stomach precluding coordinated emptying of enzymes and nutrients. Unprotected enzymes mix well and empty with nutrients but are inactivated at pH 4 or below. We describe approaches for improving the results of enzyme therapy including changing to, or adding, a different product, adding non-enteric coated enzymes, (e.g., giving unprotected enzymes at the start of the meal and acid-protected formulations later), use of antisecretory drugs and/or antacids, and changing the timing of enzyme administration. Because considerable lipid is emptied in the first postprandial hour, it is prudent to start therapy with enteric coated microbead prior to the meal so that some enzymes are available during that first hour. Patients with hyperacidity may benefit from adjuvant antisecretory therapy to reduce the duodenal acid load and possibly also sodium bicarbonate to prevent duodenal acidity. Comparative studies of clinical effectiveness of different formulations as well as the characteristics of dispersion, emptying, and dissolution of enteric-coated microspheres of different diameter and density are needed; many such studies have been completed but not yet made public. We discuss the history of pancreatic enzyme therapy and describe current use of modern preparations, approaches to overcoming unsatisfactory clinical responses, as well as studies needed to be able to provide reliably effective therapy.
    World Journal of Gastroenterology 09/2014; 20(33):11467-85. · 2.43 Impact Factor
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    ABSTRACT: Helicobacter pylori are Gram-negative, spiral-shaped microaerophilic bacteria etiologically related to gastric cancer. Lactate utilization has been implicated although no corresponding genes have been identified in the H. pylori genome. Here, we report that gene products of hp0137-0139 (lldEFG), hp0140-0141 (lctP), and hp1222 (dld) contribute to D- and L-lactate utilization in H. pylori. The three-gene unit hp0137-0139 in H. pylori 26695 encodes L-lactate dehydrogenase (LDH) that catalyzes the conversion of lactate to pyruvate in an NAD-dependent manner. Isogenic mutants of these genes were unable to grow on L-lactate-dependent medium. The hp1222 gene product functions as an NAD-independent D-LDH and also contributes to the oxidation of L-lactate; the isogenic mutant of this gene failed to grow on D-lactate-dependent medium. The parallel genes hp0140-0141 encode two nearly identical lactate permeases (LctP) that promote uptake of both D- and L-lactate. Interestingly an alternate route must also exist for lactate transport as the knockout of genes did not completely prevent growth on D- or L-lactate. Gene expression levels of hp0137-0139 and hp1222 were not enhanced by lactate as the carbon source. Expression of hp0140-0141 was slightly suppressed in the presence of L-lactate but not D-lactate. This study identified the genes contributing to the lactate utilization and demonstrated the ability of H. pylori to utilize both D- and L-lactate.
    PLoS ONE 07/2014; 9(7):e103506. · 3.53 Impact Factor
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    ABSTRACT: Gastric cancer is an inflammation-related malignancies related to long standing acute and chronic inflammation caused by infection with the human bacterial pathogen, Helicobacter pylori. Inflammation can result in genomic instability. However, there are considerable data that H. pylori itself can also produce genomic instability both directly and through epigenetic pathways. Overall, the mechanisms of H. pylori-induced host genomic instabilities remains poorly understood. We used microarray screening of H. pylori-infected human gastric biopsies to identify candidate genes involved in H. pylori-induced host genomic instabilities. We found upregulation of ATM expression in vivo in gastric mucosal cells infected with H. pylori. Using gastric cancer cell lines, we confirmed that the H. pylori-related ATM activation was due to the accumulation of DNA double-stranded breaks (DSBs). DSBs were observed following infection with both cag pathogenicity island (PAI)-positive and -negative strains, but the effect was more robust with cag PAI-positive strains. These results are consistent with the fact that both cag PAI-positive and -negative infections are associated with gastric carcinogenesis but the risk is higher in individuals infected with cag PAI-positive strains.
    Infection and Immunity 07/2014; · 4.16 Impact Factor
  • The Journal of infectious diseases. 07/2014;
  • Source
    Akira Horiuchi, David Y Graham
    Gastrointestinal Endoscopy 06/2014; · 4.90 Impact Factor
  • Yoshio Yamaoka, David Y Graham
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    ABSTRACT: Helicobacter pylori is human gastric pathogen that causes chronic and progressive gastric mucosal inflammation and is responsible for the gastric inflammation-associated diseases, gastric cancer and peptic ulcer disease. Specific outcomes reflect the interplay between host-, environmental- and bacterial-specific factors. Progress in understanding putative virulence factors in disease pathogenesis has been limited and many false leads have consumed scarce resources. Few in vitro-in vivo correlations or translational applications have proved clinically relevant. Reported virulence factor-related outcomes reflect differences in relative risk of disease rather than specificity for any specific outcome. Studies of individual virulence factor associations have provided conflicting results. Since virulence factors are linked, studies of groups of putative virulence factors are needed to provide clinically useful information. Here, the authors discuss the progress made in understanding the role of H. pylori virulence factors CagA, vacuolating cytotoxin, OipA and DupA in disease pathogenesis and provide suggestions for future studies.
    Future Oncology 06/2014; 10(8):1487-500. · 2.61 Impact Factor
  • David Y Graham
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    ABSTRACT: Helicobacter pylori (H. pylori) infection underlies gastric ulcer disease, gastric cancer and duodenal ulcer disease. The disease expression reflects the pattern and extent of gastritis/gastric atrophy (i.e., duodenal ulcer with non-atrophic and gastric ulcer and gastric cancer with atrophic gastritis). Gastric and duodenal ulcers and gastric cancer have been known for thousands of years. Ulcers are generally non-fatal and until the 20(th) century were difficult to diagnose. However, the presence and pattern of gastritis in past civilizations can be deduced based on the diseases present. It has been suggested that gastric ulcer and duodenal ulcer both arose or became more frequent in Europe in the 19(th) century. Here, we show that gastric cancer and gastric ulcer were present throughout the 17(th) to 19(th) centuries consistent with atrophic gastritis being the predominant pattern, as it proved to be when it could be examined directly in the late 19(th) century. The environment before the 20(th) century favored acquisition of H. pylori infection and atrophic gastritis (e.g., poor sanitation and standards of living, seasonal diets poor in fresh fruits and vegetables, especially in winter, vitamin deficiencies, and frequent febrile infections in childhood). The latter part of the 19(th) century saw improvements in standards of living, sanitation, and diets with a corresponding decrease in rate of development of atrophic gastritis allowing duodenal ulcers to become more prominent. In the early 20(th) century physician's believed they could diagnose ulcers clinically and that the diagnosis required hospitalization for "surgical disease" or for "Sippy" diets. We show that while H. pylori remained common and virulent in Europe and the United States, environmental changes resulted in changes of the pattern of gastritis producing a change in the manifestations of H. pylori infections and subsequently to a rapid decline in transmission and a rapid decline in all H. pylori-related diseases.
    World Journal of Gastroenterology 05/2014; 20(18):5191-5204. · 2.43 Impact Factor
  • Katsuhiro Hanada, David Y Graham
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    ABSTRACT: Gastric carcinoma is an inflammation-related cancer caused by long-term infection with the human bacterial pathogen, Helicobacter pylori. The pattern of acute-on-chronic inflammation causes progressive mucosal damage which may result in atrophy with metaplastic epithelia and eventually gastric cancer. Recently, it has been recognized that H. pylori can also cause genetic instability such as double-stranded DNA breaks and can produce gene activation and silencing via epigenetic pathways. As genetic instability is the hallmark of cancer, we highlight recent progress in understanding the gastric carcinogenesis in relation to H. pylori-related inflammation, H. pylori-induced double-stranded DNA breakage and aberrant gene expression as well as the mechanisms and role of H. pylori-associated epigenetic change in gene expression.
    Expert Review of Anti-infective Therapy 05/2014; · 3.06 Impact Factor

Publication Stats

14k Citations
3,509.42 Total Impact Points

Institutions

  • 1980–2015
    • Baylor College of Medicine
      • • Department of Medicine
      • • Veterans Affairs Medical Center
      Houston, Texas, United States
  • 2014
    • Oxford University Hospitals NHS Trust
      • Department of Gastroenterology
      Oxford, England, United Kingdom
    • United States Department of Veterans Affairs
      Bedford, Massachusetts, United States
  • 2005–2014
    • Michael E. DeBakey VA Medical Center
      Houston, Texas, United States
    • Shinshu University
      Shonai, Nagano, Japan
    • Wakayama University
      Wakayama, Wakayama, Japan
    • Chulalongkorn University
      • Department of Medicine
      Bangkok, Bangkok, Thailand
  • 2013
    • Xin Hua Hospital Affiliated to Shanghai Jiao Tong University School of Medicine
      Shanghai, Shanghai Shi, China
    • Shanghai Jiao Tong University
      Shanghai, Shanghai Shi, China
    • Pontificia Universidad Javeriana
      Μπογκοτά, Bogota D.C., Colombia
    • National Institute of Infectious Diseases, Tokyo
      Edo, Tōkyō, Japan
  • 2010–2013
    • University of Science Malaysia
      • • Department of Medicine(Med.)
      • • School of Medical Sciences
      George Town, Pulau Pinang, Malaysia
    • Hong Kong Hospital Authority
      Hong Kong, Hong Kong
    • The Chinese University of Hong Kong
      • Institute of Digestive Disease
      Hong Kong, Hong Kong
    • Hokkaido University
      • Department of Gastroenterology and Hepatology
      Sapporo-shi, Hokkaido, Japan
  • 2004–2013
    • Showa General Hospital
      Edo, Tōkyō, Japan
  • 2012
    • Washington University in St. Louis
      San Luis, Missouri, United States
  • 2006–2012
    • University of Texas at El Paso
      • Department of Biological Sciences
      El Paso, Texas, United States
  • 2000–2012
    • University of Padova
      • • Department of Medicine DIMED
      • • Department of Surgery, Oncology and Gastroenterology DISCOG
      Padua, Veneto, Italy
  • 1999–2012
    • Università degli Studi di Sassari
      • Dipartimento di Scienze Biomediche
      Sassari, Sardinia, Italy
  • 2011
    • National Yang Ming University
      • Department of Internal Medicine
      T’ai-pei, Taipei, Taiwan
    • Oita University
      • Faculty of Medicine
      Ōita, Ōita, Japan
  • 2009–2010
    • Hamamatsu University School of Medicine
      • • Center for Clinical Research
      • • School of Medicine
      Hamamatu, Shizuoka, Japan
    • Marshall University
      Huntington, West Virginia, United States
    • Kawasaki Medical University
      • Department of General Internal Medicine 2
      Kurasiki, Okayama, Japan
    • Kaohsiung Medical University
      Kao-hsiung-shih, Kaohsiung, Taiwan
  • 2008–2010
    • University of Texas Health Science Center at Houston
      • • School of Public Health
      • • Medical School
      Houston, TX, United States
  • 2003–2009
    • Thammasat University
      Krung Thep, Bangkok, Thailand
    • Treatment Research Institute, Philadelphia PA
      Philadelphia, Pennsylvania, United States
    • Kangbuk Samsung Hospital
      Sŏul, Seoul, South Korea
  • 1989–2008
    • Spokane VA Medical Center
      Spokane, Washington, United States
  • 2007
    • Helsinki University Central Hospital
      • Department of Pathology
      Helsinki, Province of Southern Finland, Finland
  • 1991–2003
    • Minneapolis Veterans Affairs Hospital
      Minneapolis, Minnesota, United States
  • 2002
    • Hokkaido University Hospital
      • Division of Internal Medicine II
      Sapporo-shi, Hokkaido, Japan
    • Sungkyunkwan University
      • School of Medicine
      Seoul, Seoul, South Korea
    • University of Pittsburgh
      • Department of Pathology
      Pittsburgh, PA, United States
  • 2001
    • American University Washington D.C.
      Washington, Washington, D.C., United States
    • University of Bologna
      Bolonia, Emilia-Romagna, Italy
  • 1998
    • Hallym University
      • College of Medicine
      Seoul, Seoul, South Korea
  • 1997
    • Université Libre de Bruxelles
      Bruxelles, Brussels Capital Region, Belgium
  • 1995
    • Houston Methodist Hospital
      Houston, Texas, United States
  • 1994
    • Texas Medical Center
      Houston, Texas, United States
  • 1988–1989
    • Houston Zoo
      Houston, Texas, United States