David Y Graham

Michael E. DeBakey VA Medical Center, Houston, Texas, United States

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Publications (584)3864.77 Total impact

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    BMC Immunology 12/2015; 16(1). DOI:10.1186/s12865-015-0069-0 · 2.25 Impact Factor
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    ABSTRACT: Both cold-only snare and hot polypectomy snare are used for the removal of small colorectal polyps. To compare the outcome of cold snare polypectomy of small colorectal polyps with a snare exclusively designed as a cold snare versus cold snare polypectomy by using a traditional polypectomy snare. Prospective, randomized, controlled study. Municipal hospital in Japan. Patients with colorectal polyps 10 mm or smaller in diameter were randomized to dedicated cold snare (dedicated cold snare group) or traditional cold snare (traditional cold snare group). The primary outcome measure was complete resection rates by cold snaring based on pathological examination. Secondary outcomes included bleeding within 2 weeks after polypectomy and identification of submucosal arteries and injured arteries in the resected specimens. Seventy-six patients having 210 eligible polyps were randomized: dedicated cold snare group, N = 37 (98 polyps) and traditional cold snare group, N = 39 (112 polyps). Patient demographic characteristics including the number, size, and shape of the polyps removed were similar in the 2 groups. The complete resection rate was significantly greater with the dedicated cold than with the traditional cold snare (91% [89/98] vs 79% [88/112], P = .015), with a marked difference with 8- to 10-mm polyps, both flat and pedunculated. Immediate bleeding and hematochezia rates were similar (19% vs 21%, P = .86; 5.4% vs 7.7%, P = .69). No delayed bleeding occurred. Histology demonstrated a similar prevalence of arteries and injured arteries in the submucosa (33% [32/96] vs 30% [31/104], P = .59; 3.1% [3/96] vs 6.7% [7/104], P = .24). Small sample size, single-center study. Polypectomy by using a dedicated cold snare resulted in complete polyp removal more often than did cold snaring with a traditional snare, especially polyps 8 to 10 mm in diameter, whether flat or pedunculated. (Clinical trial registration number: NCT02036047.). Copyright © 2015 American Society for Gastrointestinal Endoscopy. Published by Elsevier Inc. All rights reserved.
    Gastrointestinal endoscopy 04/2015; DOI:10.1016/j.gie.2015.02.012 · 4.90 Impact Factor
  • Gastroenterology 04/2015; 148(4):S-529. DOI:10.1016/S0016-5085(15)31768-6 · 13.93 Impact Factor
  • Gastroenterology 04/2015; 148(4):S-529. DOI:10.1016/S0016-5085(15)31769-8 · 13.93 Impact Factor
  • Ping-I Hsu, David Y. Graham
    Gastroenterology 04/2015; 148(4):S-420. DOI:10.1016/S0016-5085(15)31417-7 · 13.93 Impact Factor
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    ABSTRACT: Innate immunity plays important roles in the primary defense against pathogens, and epidemiological studies have suggested a role for Toll-like receptor (TLR) 1 in Helicobacter pylori susceptibility. Microarray analysis of gastric biopsy specimens from H. pylori-positive and uninfected subjects showed TLR10 messenger RNA (mRNA) levels were upregulated ∼15-fold in infected subjects and confirmed by the quantitative real-time polymerase chain reaction (qRT-PCR) analysis. Immunohistochemistry showed increased TLR10 expression in the gastric epithelial cells of infected individuals. When H. pylori was co-cultured with NCI-N87 gastric cells, both TLR10 and TLR2 mRNA levels were upregulated. We compared the ability of TLR combinations to mediate nuclear factor-κB (NF-κB) activation. Compared to other TLR2 subfamily heterodimers, the TLR2/TLR10 heterodimer mediated the greatest NF-κB activation following exposure to heat-killed H. pylori or H. pylori lipopolysaccharide. We conclude that TLR10 is a functional receptor involved in the innate immune response to H. pylori infection and that the TLR2/TLR10 heterodimer functions in H. pylori lipopolysaccharide recognition. © The Author 2015. Published by Oxford University Press on behalf of the Infectious Diseases Society of America. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com.
    Gastroenterology 04/2015; 148(4):S-118. DOI:10.1016/S0016-5085(15)30410-8 · 13.93 Impact Factor
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    ABSTRACT: Over the past 50 years, the prevalence of Helicobacter pylori infection has fallen as standards of living improved. The changes in the prevalence of infection and its manifestations (peptic ulcer disease and gastric mucosal lesions) were investigated in a large cohort of Sardinians undergoing upper endoscopy for dyspepsia. A retrospective observational study was conducted involving patients undergoing endoscopy for dyspepsia from 1995 to 2013. H. pylori status was assessed by histology plus the rapid urease test or 13C-UBT. Gastric mucosal lesions were evaluated histologically. Data including non-steroidal anti-inflammatory drugs (NSAIDs) use and the presence of peptic ulcers were collected. The prevalence of H. pylori was calculated for each quartile and for each birth cohort from 1910 to 2000. 11,202 records were retrieved for the analysis (62.9 % women). The overall prevalence of H. pylori infection was 43.8 % (M: 46.6 % vs. F: 42.0 %; P = 0.0001). A dramatic decrease in the prevalence of infection occurred over the 19-year observation period. The birth cohort effect was evident in each category (quartile) reflecting the continuous decline in H. pylori acquisition. Over time, the prevalence of peptic ulcers also declined, resulting in an increase in the proportion of H. pylori negative/NSAID positive and H. pylori negative/NSAID negative peptic ulcers. The prevalence of gastric mucosal changes also declined despite aging. The decline in H. pylori prevalence over time likely reflects the improvement in socioeconomic conditions in Sardinia such that H. pylori infection and its clinical outcomes including peptic ulcer are becoming less frequent even among dyspeptic patients.
    Internal and Emergency Medicine 03/2015; DOI:10.1007/s11739-015-1218-4 · 2.41 Impact Factor
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    David Y Graham
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    ABSTRACT: Most gastric cancers are caused by infection with the common human bacterial pathogen, Helicobacter pylori. It is now accepted that gastric cancer can be prevented and virtually eliminated by H. pylori eradication and this knowledge was responsible for country-wide H. pylori eradication combined with secondary cancer prevention for those with residual risk that was introduced in Japan in 2013. Korea is a high H. pylori prevalence and high gastric cancer incidence country and a good candidate for a gastric cancer elimination program. The presence of an H. pylori infection is now considered as an indication for treatment of the infection. However, antimicrobial drug resistance is common among H. pylori in Korea making effective therapy problematic. Country-wide studies of the local and regional antimicrobial resistance patterns are needed to choose the most appropriate therapies. H. pylori and gastric cancer eradication can be both efficient and cost effective making it possible and practical to make Korea H. pylori and gastric cancer free. There is no reason to delay.
    The Korean Journal of Internal Medicine 03/2015; 30(2):133-139. DOI:10.3904/kjim.2015.30.2.133
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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.
    Clinical Gastroenterology and Hepatology 02/2015; DOI:10.1016/j.cgh.2015.02.005 · 6.53 Impact Factor
  • 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; 148(4). DOI:10.1053/j.gastro.2015.01.040 · 13.93 Impact Factor
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    ABSTRACT: Background. Noroviruses are a leading cause of acute gastroenteritis worldwide. Mucosal and cellular immune responses remain poorly understood in that most studies have focused on serological responses to infection. Methods. We used saliva, feces and peripheral blood mononuclear cells collected from persons administered Norwalk virus (NV) to characterize mucosal (salivary and fecal IgA) and cellular (NV-specific IgA and IgG antibody secreting cells and total and NV-specific IgA and IgG memory B cells) immune responses following infection. Results. Pre-challenge levels of NV-specific salivary IgA and NV-specific memory IgG cells correlated with protection from gastroenteritis whereas pre-challenge NV-specific fecal IgA levels correlated with reduced viral load and a less severe illness. Antibody secreting cell responses were biased towards IgA while memory B-cell responses were biased towards IgG. NV-specific memory B-cells but not antibody secreting cells persisted 180 days post infection. Conclusions. NV-specific salivary IgA and NV-specific memory IgG cells were identified as new correlates of protection against NV gastroenteritis. Understanding the relative importance of mucosal, cellular and humoral immunity is important in developing vaccine strategies for norovirus disease prevention.
    The Journal of Infectious Diseases 01/2015; DOI:10.1093/infdis/jiv053 · 5.78 Impact Factor
  • Takahiro Uotani, David Y Graham
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    ABSTRACT: Helicobacter pylori (H. pylori) is a major human pathogen which causes progressive gastroduodenal damage. Guidelines recommend that, unless there are compelling reasons to delay, treatment is indicated for all patients in whom the infection is diagnosed. The rapid urease test (RUT) is a popular diagnostic test in that it is a rapid, cheap and simple test that detects the presence of urease in or on the gastric mucosa. The sensitivity and specificity are generally high and many versions have been approved for use in humans. Best results are obtained if biopsies are obtained from both the antrum and corpus. The tissue sample embedded in the RUT gel can also be utilized for other tests such as for molecular based tests of microbial susceptibility or for host factors. False-positive results are rare if the RUT contains an antibacterial agent to prevent growth of urease-containing contaminants and the tests are discarded at 24 hours. The use of antimicrobial drugs and proton pump inhibitors as well as the presence of intestinal metaplasia may result in false-negative results. A negative test should not be used as the criteria for cure or in cases where accuracy is important for patient management such as in upper gastrointestinal bleeding. Interpretation of the test should take into account the pretest probability and the prevalence of H. pylori in the population. The test can also be used to provide an informal assessment of the accuracy of the histopathology result and discrepancies should prompt a review of the histopathology and discussions with the pathologist.
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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; 22(2). DOI:10.1128/CVI.00516-14 · 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; 81(4). DOI:10.1016/j.diagmicrobio.2014.12.003 · 2.57 Impact Factor
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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; 20(3). DOI:10.1111/hel.12193 · 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; DOI:10.1038/ajg.2014.351 · 9.21 Impact Factor
  • David Y Graham, Masahiro Asaka
    JNCI Journal of the National Cancer Institute 11/2014; 106(11). DOI:10.1093/jnci/dju352 · 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; 46(1). DOI:10.1016/j.humpath.2014.10.006 · 2.81 Impact Factor
  • Constance Wang, Ann Weber, David Y Graham
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    ABSTRACT: The incidence of gastric cancer varies both within and among populations and can change rapidly without a corresponding decline in Helicobacter pylori prevalence. Here, we describe the changes in gastric cancer mortality in Japan in relation to age-period-cohort effects as well as the decline in H. pylori prevalence. We used data from Japanese for men and women aged 30-94 for birth years 1875-1970 (calendar time 1950-2000) to observe the age, period and cohort effects on gastric cancer mortality rates. Additionally, we used Poisson regression to simultaneously adjust for concurrent age, period and cohort effects as well as for declining H. pylori prevalence in the Japanese population. There was an approximate 60 % decline in gastric cancer mortality between 1965 and 1995. Detailed age, period and cohort analyses and Poisson regression analysis showed these factors interact in complex ways, analyses focused on one or two of these effects, such as birth cohort without considering concurrent age and period would obscure important interactions that affected different age groups at different times to produce this composite effect. The underlying complexity in population-disease dynamics requires population-specific descriptions of trends using multiple methods to provide an in-depth analysis while simultaneously allowing for necessary statistical adjustments as well as identification of interactions. More thorough descriptions of the population-specific general trends in relation to changes in the population structure (age-period-cohort) enable better prevention and health care policy planning, and further, the descriptions enable hypothesis generation regarding causes of population-specific disease patterns.
    Digestive Diseases and Sciences 10/2014; 60(2). DOI:10.1007/s10620-014-3359-0 · 2.55 Impact Factor
  • Cancer Research 10/2014; 74(19 Supplement):4132-4132. DOI:10.1158/1538-7445.AM2014-4132 · 9.28 Impact Factor

Publication Stats

16k Citations
3,864.77 Total Impact Points


  • 2005–2015
    • Michael E. DeBakey VA Medical Center
      Houston, Texas, United States
    • University of Toronto
      Toronto, Ontario, Canada
  • 1980–2015
    • Baylor College of Medicine
      • • Veterans Affairs Medical Center
      • • Department of Medicine
      Houston, Texas, United States
  • 2014
    • United States Department of Veterans Affairs
      Bedford, Massachusetts, United States
  • 2013
    • National Institute of Infectious Diseases, Tokyo
      Edo, Tōkyō, Japan
  • 2007–2013
    • University of Padova
      • Department of Surgery, Oncology and Gastroenterology DISCOG
      Padua, Veneto, Italy
    • Shanghai Jiao Tong University
      Shanghai, Shanghai Shi, China
  • 2011
    • Oita University
      • Faculty of Medicine
      Ōita, Ōita, Japan
  • 2010
    • University of Science Malaysia
      • School of Medical Sciences
      Nibong Tebal, Pulau Pinang, Malaysia
  • 2005–2010
    • The Chinese University of Hong Kong
      • • Institute of Digestive Disease
      • • Department of Medicine and Therapeutics
      Hong Kong, Hong Kong
  • 2009
    • Marshall University
      Huntington, West Virginia, United States
    • Tokoha University
      • School of Medicine
      Hamamatu, Shizuoka, Japan
  • 2008
    • The University of Texas Health Science Center at Houston
      • Medical School
      Houston, TX, United States
  • 1990–2008
    • Spokane VA Medical Center
      Spokane, Washington, United States
  • 2006
    • Wakayama University
      Wakayama, Wakayama, Japan
  • 1998–2005
    • Shinshu University
      • Department of Laboratory Medicine
      Shonai, Nagano, Japan
    • Research Triangle Park Laboratories, Inc.
      Raleigh, North Carolina, United States
  • 2004
    • Showa General Hospital
      Edo, Tōkyō, Japan
  • 2003
    • Kangbuk Samsung Hospital
      Sŏul, Seoul, South Korea
  • 1994–2003
    • Minneapolis Veterans Affairs Hospital
      Minneapolis, Minnesota, United States
  • 2002
    • University of Pittsburgh
      Pittsburgh, Pennsylvania, United States
    • Duke University
      Durham, North Carolina, United States
  • 2001
    • American University Washington D.C.
      Washington, Washington, D.C., United States
  • 2000
    • Università degli Studi di Sassari
      • Dipartimento di Scienze Biomediche
      Sassari, Sardinia, Italy
    • Prince of Wales Hospital, Hong Kong
      Chiu-lung, Kowloon City, Hong Kong
  • 1995–2000
    • Houston Methodist Hospital
      Houston, Texas, United States
  • 1997
    • Université Libre de Bruxelles
      Bruxelles, Brussels Capital Region, Belgium
  • 1983–1994
    • Texas Medical Center
      Houston, Texas, United States
  • 1988–1989
    • Houston Zoo
      Houston, Texas, United States