Journal of Pathology and Translational Medicine

Original Articles

Upward trend in follicular lymphoma among the Korean population: 10-year experience at a large tertiary institution: Meejeong Kim, Hee Sang Hwang, Hyungwoo Cho, Dok Hyun Yoon, Cheolwon Suh, Chan Sik Park, Heounjeong Go, Jooryung Huh; J Pathol Transl Med. 2021;55(5):330-337. Published online September 2, 2021; DOI: https://doi.org/10.4132/jptm.2021.07.25

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Background
Follicular lymphoma (FL) is the second most common non-Hodgkin lymphoma (NHL) in Western countries. However, it is relatively rare in Asia. This study examined epidemiologic characteristics of FL in South Korea, with an emphasis on recent trends of increase in cases.
Methods
We retrospectively examined 239 cases of newly diagnosed FL at a large tertiary institution in Korea (Asan Medical Center, Seoul, Republic of Korea) between 2008 and 2017. Age-adjusted incidence rates and clinicopathological variables were analyzed, and joinpoint regression analysis was used to identify the changes.
Results
The age-adjusted incidence of FL significantly increased during the study period (p = .034), and the ratio of (relative incidence) patients with FL to patients with NHL increased from 4.28% to 9.35% in the same period. Over the 10-year study assessment duration, the proportion of patients with stage III/IV FL (p = .035) and expression of BCL2 (p = .022) or BCL6 (p = .039) significantly increased. From 2013–2017, the proportion of patients with highrisk Follicular Lymphoma International Prognostic Index (FLIPI) score increased (21.5% to 28.7%), whereas that of low-risk FLIPI decreased (55.4% to 38.6%), although those results were not statistically significant (p = .066).
Conclusions
We found an increasing incidence of FL, with a disproportionate increase in the incidence of high-stage disease and recent changes in the clinicopathologic features of the Korean patient population.

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Incidence Trend of Follicular Lymphoma in Taiwan Compared to Japan and Korea, 2001–2019
Liang-Chun Chiu, Chih-Wen Lin, Hung-Ju Li, Jian-Han Chen, Fu-Cheng Chuang, Sheng-Fung Lin, Yu Chang, Yu-Chieh Su
Journal of Clinical Medicine.2023; 12(4): 1417. CrossRef
A Case Report on the Complete Response of a Patient with Recurrent Follicular Lymphoma Treated with Integrative Medicine
Kyung-dug Park, Jisoo Kim, Yoona Oh, Beom-Jin Jeong, Yu-jin Jung, Sunhwi Bang
The Journal of Internal Korean Medicine.2023; 44(3): 585. CrossRef
Recent Updates on Diagnosis and Treatment of Follicular Lymphoma
Ga-Young Song, Deok-Hwan Yang
The Korean Journal of Medicine.2023; 98(5): 231. CrossRef
Classical Hodgkin lymphoma following follicular lymphoma: a case report
Bomi Kim
Journal of Yeungnam Medical Science.2023; 40(Suppl): S113. CrossRef
Incidence, clinicopathological features and genetics of in‐situ follicular neoplasia: a comprehensive screening study in a Japanese cohort
Naoki Oishi, Takahiro Segawa, Kunio Miyake, Kunio Mochizuki, Tetsuo Kondo
Histopathology.2022; 80(5): 820. CrossRef

Multistaining Optimization for Epstein-Barr Virus–Encoded RNA In Situ Hybridization and Immunohistochemistry of Formalin-Fixed Paraffin-Embedded Tissues Using an Automated Immunostainer: Jae Nam Ko, Jin Kyoung Jung, Yun Ik Park, Hwa Jeong Shin, Jooryung Huh, Sol Back, Yu Jin Kim, Jae Ho Kim, Heounjeong Go; J Pathol Transl Med. 2019;53(5):317-326. Published online August 27, 2019; DOI: https://doi.org/10.4132/jptm.2019.08.06

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Abstract PDF Supplementary Material

Background
Single staining is commonly performed for practical pathologic diagnoses. However, this method is limited in its ability to specify cellular morphology and immunophenotype and often requires consumption of limited tissue. This study aimed to describe an optimized protocol for multiple in situ hybridization (ISH) and immunohistochemistry (IHC).
Methods
The quality of multistaining was evaluated by carefully changing each step of ISH and IHC in an angioimmunoblastic T-cell lymphoma (AITL) case on a Ventana BenchMark XT automated immunostainer. The optimized protocols were also performed using another immunostainer and in 15 cases of five Epstein-Barr virus (EBV)–associated malignancies using formalin-fixed paraffin-embedded tissue.
Results
The quality of various ISHIHC staining protocols was semi-quantitatively evaluated. The best EBV-encoded RNA (EBER)-ISH/double IHC staining quality, equivalent to single staining, was obtained using the following considerations: initial EBER-ISH application, use of protease and antigen retrieval reagent (cell conditioning 1 [CC1] treatment time was minimized due to impact on tissue quality), additional baking/ deparaffinization not needed, and reduced dilution ratio and increased reaction time for primary antibody compared with single immunostaining. Furthermore, shorter second CC1 treatment time yielded better results. Multiple staining was the best quality in another immunostainer and for different types of EBV-associated malignancies when it was performed in the same manner as for the Ventana BenchMark XT as determined for AITL.
Conclusions
EBER-ISH and double IHC could be easily used in clinical practice with currently available automated immunostainers and adjustment of reagent treatment time, dilution ratio, and antibody reaction time.

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Reviews

Epstein-Barr Virus–Associated Lymphoproliferative Disorders: Review and Update on 2016 WHO Classification: Hyun-Jung Kim, Young Hyeh Ko, Ji Eun Kim, Seung-Sook Lee, Hyekyung Lee, Gyeongsin Park, Jin Ho Paik, Hee Jeong Cha, Yoo-Duk Choi, Jae Ho Han, Jooryung Huh; J Pathol Transl Med. 2017;51(4):352-358. Published online June 5, 2017; DOI: https://doi.org/10.4132/jptm.2017.03.15

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Abstract PDF

Epstein-Barr virus (human herpesvirus-4) is very common virus that can be detected in more than 95% of the human population. Most people are asymptomatic and live their entire lives in a chronically infected state (IgG positive). However, in some populations, the Epstein-Barr virus (EBV) has been involved in the occurrence of a wide range of B-cell lymphoproliferative disorders (LPDs), including Burkitt lymphoma, classic Hodgkin’s lymphoma, and immune–deficiency associated LPDs (post-transplant and human immunodeficiency virus–associated LPDs). T-cell LPDs have been reported to be associated with EBV with a subset of peripheral T-cell lymphomas, angioimmunoblastic T-cell lymphomas, extranodal nasal natural killer/T-cell lymphomas, and other rare histotypes. This article reviews the current evidence covering EBV-associated LPDs based on the 2016 classification of the World Health Organization. These LPD entities often pose diagnostic challenges, both clinically and pathologically, so it is important to understand their unique pathophysiology for correct diagnoses and optimal management.

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Molecular Testing of Lymphoproliferative Disorders: Current Status and Perspectives: Yoon Kyung Jeon, Sun Och Yoon, Jin Ho Paik, Young A Kim, Bong Kyung Shin, Hyun-Jung Kim, Hee Jeong Cha, Ji Eun Kim, Jooryung Huh, Young-Hyeh Ko; J Pathol Transl Med. 2017;51(3):224-241. Published online May 10, 2017; DOI: https://doi.org/10.4132/jptm.2017.04.09

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Abstract PDF

Molecular pathologic testing plays an important role for the diagnosis, prognostication and decision of treatment strategy in lymphoproliferative disease. Here, we briefly review the molecular tests currently used for lymphoproliferative disease and those which will be implicated in clinical practice in the near future. Specifically, this guideline addresses the clonality test for B- and T-cell proliferative lesions, molecular cytogenetic tests for malignant lymphoma, determination of cell-of-origin in diffuse large B-cell lymphoma, and molecular genetic alterations incorporated in the 2016 revision of the World Health Organization classification of lymphoid neoplasms. Finally, a new perspective on the next-generation sequencing for diagnostic, prognostic, and therapeutic purpose in malignant lymphoma will be summarized.

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Original Article

GLUT1 as a Prognostic Factor for Classical Hodgkin’s Lymphoma: Correlation with PD-L1 and PD-L2 Expression: Young Wha Koh, Jae-Ho Han, Seong Yong Park, Dok Hyun Yoon, Cheolwon Suh, Jooryung Huh; J Pathol Transl Med. 2017;51(2):152-158. Published online February 21, 2017; DOI: https://doi.org/10.4132/jptm.2016.11.03

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Abstract PDF

Background
Glucose transporter type 1 (GLUT1) expression is linked to glucose metabolism and tissue hypoxia. A recent study reported that GLUT1 was significantly associated with programmed death ligand 1 (PD-L1) as a therapeutic target in relapsed or refractory classical Hodgkin’s lymphoma (cHL). The purpose of this study was to measure the expression of GLUT1 and assess its prognostic significance and potential relationships with PD-L1, programmed death ligand 2 (PD-L2), and programmed death-1 (PD-1) expressions in cHL. Methods: Diagnostic tissues from 125 patients with cHL treated with doxorubicin, bleomycin, vinblastine, and dacarbazine were evaluated retrospectively via immunohistochemical analysis of GLUT1, PD-L1, PD-L2, and PD-1 expression. Results: The median follow-up time was 4.83 years (range, 0.08 to 17.33 years). GLUT1, PD-L1, PD-L2, and PD-1 were expressed in 44.8%, 63.2%, 9.6%, and 13.6% of the specimens, respectively. Positive correlations were found between GLUT1 and PD-L1 expression (p = .004) and between GLUT1 and PD-L2 expression (p = .031). GLUT1 expression in Hodgkin/Reed-Sternberg (HRS) cells was not associated with overall survival or event-free survival (EFS) in the entire cohort (p = .299 and p = .143, respectively). A subgroup analysis according to the Ann Arbor stage illustrated that GLUT1 expression in HRS cells was associated with better EFS in advanced-stage disease (p = .029). A multivariate analysis identified GLUT1 as a marginally significant prognostic factor for EFS (p = .068). Conclusions: This study suggests that GLUT1 expression is associated with better clinical outcomes in advanced-stage cHL and is significantly associated with PD-L1 and PD-L2 expressions.

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Brief Case Reports

Primary Follicular Lymphoma of the Duodenum: A Case Report: Jin Roh, Jooryung Huh, Chan-Sik Park; J Pathol Transl Med. 2016;50(6):479-481. Published online May 9, 2016; DOI: https://doi.org/10.4132/jptm.2016.01.27

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Letter to the editor

TdT+ T-Lymphoblastic Proliferation in Castleman Disease: Chang Gok Woo, Jooryung Huh; J Pathol Transl Med. 2015;49(1):1-4. Published online January 15, 2015; DOI: https://doi.org/10.4132/jptm.2014.11.17

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Brief Case Report

A Case of Type II Enteropathy-Associated T-Cell Lymphoma with Epstein-Barr Virus Positivity: Min Jeong Song, Chan Sik Park, Hee Sang Hwang, Cheol Won Suh, Dok Hyun Yoon, Jooryung Huh; Korean J Pathol. 2014;48(6):426-429. Published online December 31, 2014; DOI: https://doi.org/10.4132/KoreanJPathol.2014.48.6.426

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Original Article

Expression of CD99 in Multiple Myeloma: A Clinicopathologic and Immunohistochemical Study of 170 Cases: Su-Jin Shin, Hyangsin Lee, Geunyoung Jung, Minchan Gil, Hosub Park, Young Soo Park, Dok Hyun Yoon, Cheolwon Suh, Chan-Jeoung Park, Jooryung Huh, Chan-Sik Park; Korean J Pathol. 2014;48(3):209-216. Published online June 26, 2014; DOI: https://doi.org/10.4132/KoreanJPathol.2014.48.3.209

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Abstract PDF

Background

Multiple myeloma (MM) is a heterogeneous and ultimately fatal disease. Risk stratification using prognostic biomarkers is crucial to individualize treatments. We sought to investigate the role of CD99, a transmembrane protein highly expressed in many hematopoietic cells including subpopulations of normal and neoplastic plasma cells, for MM risk stratification.

Methods

CD99 expression was measured in paraffin samples of bone marrow and extramedullary biopsies of 170 patients with MM. Patients were divided into those with high score (moderately and strongly positive) and low score (negative and weakly positive), with all staining being cytoplasmic and/or membranous.

Results

High anti-CD99 immunostaining was observed in 72 of 136 (52.9%) bone marrow biopsies and 24 of 87 (27.6%) extramedullary biopsies in MM. High CD99 expression of extramedullary specimens was associated with significantly longer overall survival (OS; p=.016). High CD99 expression of extramedullary specimens was also associated with better prognosis in the nonautologous stem cell transplantation group of MM patients (p=.044). In multivariate analysis, International Staging System stage was an independent prognostic factor, whereas CD99 expression was no longer statistically significant.

Conclusions

Expression of CD99 in extramedullary specimens was correlated with longer OS, suggesting that CD99 may be a helpful immunohistochemical marker for risk stratification.

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Review

Current Concepts in Primary Effusion Lymphoma and Other Effusion-Based Lymphomas: Yoonjung Kim, Chan Jeong Park, Jin Roh, Jooryung Huh; Korean J Pathol. 2014;48(2):81-90. Published online April 28, 2014; DOI: https://doi.org/10.4132/KoreanJPathol.2014.48.2.81

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Abstract PDF

Primary effusion lymphoma (PEL) is a human herpes virus 8 (HHV8)-positive large B-cell neoplasm that presents as an effusion with no detectable tumor in individuals with human immunodeficiency virus infection or other immune deficiencies. PEL is an aggressive neoplasm with a poor prognosis. PEL cells show diverse morphologies, ranging from immunoblastic or plasmablastic to anaplastic. The immunophenotype of PEL is distinct, but its lineage can be misdiagnosed if not assessed thoroughly. PEL cells usually express CD45, lack B- and T-cell-associated antigens, and characteristically express lymphocyte activation antigens and plasma cell-associated antigens. Diagnosis of PEL often requires the demonstration of a B-cell genotype. HHV8 must be detected in cells to diagnose PEL. In most cases, PEL cells also harbor the Epstein-Barr virus (EBV) genome. Similar conditions associated with HHV8 but not effusion-based are called "extracavitary PELs." PELs should be differentiated from HHV8-negative, EBV-positive, body cavity-based lymphomas in patients with long-standing chronic inflammation; the latter can occur in tuberculous pleuritis, artificial pneumothorax, chronic liver disease and various other conditions. Despite their morphological similarity, these various lymphomas require different therapeutic strategies and have different prognostic implications. Correct diagnosis is essential to manage and predict the outcome of patients with PEL and related disorders.

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Original Article

Prognostic Significance of Absolute Lymphocyte Count/Absolute Monocyte Count Ratio at Diagnosis in Patients with Multiple Myeloma: Su-Jin Shin, Jin Roh, Misung Kim, Min Jung Jung, Young Wha Koh, Chan-Sik Park, Dok Hyun Yoon, Cheolwon Suh, Chan-Jeong Park, Hyun Sook Chi, Jooryung Huh; Korean J Pathol. 2013;47(6):526-533. Published online December 24, 2013; DOI: https://doi.org/10.4132/KoreanJPathol.2013.47.6.526

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Abstract PDF

Background

Absolute lymphocyte count (ALC) in peripheral blood has recently been reported to be an independent prognostic factor in multiple myeloma (MM). Previous studies indicated that the absolute monocyte count (AMC) in peripheral blood reflects the state of the tumor microenvironment in lymphomas. Neither the utility of the AMC nor its relationship with ALC has been studied in MM.

Methods

The prognostic value of ALC, AMC, and the ALC/AMC ratio at the time of diagnosis was retrospectively examined in 189 patients with MM.

Results

On univariate analysis, low ALC (<1,400 cells/µL), high AMC (≥490 cells/µL), and low ALC/AMC ratio (<2.9) were correlated with worse overall survival (OS) (p=.002, p=.038, and p=.001, respectively). On multivariate analysis, the ALC/AMC ratio was an independent prognostic factor (p=.047), whereas ALC and AMC were no longer statistical significant. Low ALC, high AMC, and low ALC/AMC ratio were associated with poor prognostic factors such as high International Staging System stage, plasmablastic morphology, hypoalbuminemia, and high β2-microglobulin.

Conclusions

Univariate analysis demonstrated that changes in ALC, AMC, and the ALC/AMC ratio are associated with patient survival in MM. Multivariate analysis showed that, of these factors, the ALC/AMC ratio was an independent prognostic factor for OS.

Citations

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Real World Experience of Daratumumab: Evaluating Lymphopenia and Adverse Events in Multiple Myeloma Patients
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Normal Absolute Monocyte Count at the Time of Relapse is Associated with Improved Survival After First Salvage Therapy in Adult Patients with Early Relapsed B-Lineage Acute Lymphoblastic Leukemia

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Case Report

Rosai-Dorfman Disease: Report of a Case Associated with IgG4-Related Sclerotic Lesions: Bong-Hee Park, Da Hye Son, Myung-Hwan Kim, Tae Sun Shim, Hee Jin Lee, Jooryung Huh; Korean J Pathol. 2012;46(6):583-586. Published online December 26, 2012; DOI: https://doi.org/10.4132/KoreanJPathol.2012.46.6.583

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Abstract PDF

We describe a rare case of sinus histiocytosis with massive lymphadenopathy (Rosai-Dorfman disease) associated with a six-year history of autoimmune pancreatitis, which was controlled by steroid treatment. The patient presented with multiple, cervical and thoracic lymphadenopathy and abnormal, nodular opacities in the lung. Histologically, Rosai-Dorfman disease with numerous IgG4-positive cells was identified in a subcutaneous lymph node in the patient's left forearm. The patient recovered uneventfully with steroid treatment.

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Original Articles

WHO Classification of Malignant Lymphomas in Korea: Report of the Third Nationwide Study.: Jin Man Kim, Young Hyeh Ko, Seung Sook Lee, Jooryung Huh, Chang Suk Kang, Chul Woo Kim, Yun Kyung Kang, Jai Hyang Go, Min Kyung Kim, Wan Seop Kim, Yoon Jung Kim, Hyun Jung Kim, Hee Kyung Kim, Jong Hee Nam, Hyung Bae Moon, Chan Kum Park, Tae In Park, Young Ha Oh, Dong Wha Lee, Jong Sil Lee, Juhie Lee, Hyekyung Lee, Sung Chul Lim, Kyu Yun Jang, Hee Kyung Chang, Yoon Kyung Jeon, Hye Ra Jung, Min Sun Cho, Hee Jeong Cha, Suk Jin Choi, Jae Ho Han, Sook Hee Hong, Insun Kim; Korean J Pathol. 2011;45(3):254-260.; DOI: https://doi.org/10.4132/KoreanJPathol.2011.45.3.254

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Abstract PDF

BACKGROUND
The aim of study was to determine the relative frequency of malignant lymphoma according to World Health Organization (WHO) classification in Korea.
METHODS
A total of 3,998 cases diagnosed at 31 institutes between 2005 and 2006 were enrolled. Information including age, gender, pathologic diagnosis, site of involvement and immunophenotypes were obtained.
RESULTS
The relative frequency of non-Hodgkin lymphoma (NHL) and Hodgkin lymphoma (HL) was 95.4% and 4.6%, respectively. B-cell lymphomas accounted for 77.6% of all NHL, while T/natural killer (T/NK)-cell lymphomas accounted for 22.4%. The most frequent subtypes of NHL were diffuse large B-cell lymphoma (42.7%), extranodal marginal zone B-cell lymphoma (MZBCL) of mucosa-associated lymphoid tissue (19.0%), NK/T-cell lymphoma (6.3%) and peripheral T-cell lymphoma (PTCL), unspecified (6.3%), in decreasing order. The relative frequency of HL was nodular sclerosis (47.4%), mixed cellularity (30.6%), and nodular lymphocyte predominant (12.1%) subtypes. Compared with a previous study in 1998, increase in gastric MZBCL and nodular sclerosis HL, and slight decrease of follicular lymphoma, PTCL, and NK/T-cell lymphoma were observed.
CONCLUSIONS
Korea had lower rates of HL and follicular lymphoma, and higher rates of extranodal NHL, extranodal MZBCL, and NK/T-cell lymphoma of nasal type compared with Western countries. Changes in the relative frequency of lymphoma subtypes are likely ascribed to refined diagnostic criteria and a change in national health care policy.

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Primary Splenic Vascular Lesions: A Clinicopathologic, Immunophenotypic and Radiopathologic Correlation Study of 40 Cases.: Young Wha Koh, Heejin Lee, Gawon Choi, Gui Young Kwon, Eun Ju Kim, Jooryung Huh; Korean J Pathol. 2010;44(5):502-512.; DOI: https://doi.org/10.4132/KoreanJPathol.2010.44.5.502

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Abstract PDF

BACKGROUND
Primary splenic vascular lesions include the tumor and the inflammatory condition. A primary splenic vascular tumor is rare but is the most common tumor of the benign primary splenic tumors.
METHODS
We describe the clinicopathological, radiological, and immunophenotypical findings of 40 cases of primary vascular lesions identified at our hospital from 1996 to 2009.
RESULTS
The patients included 18 men and 22 women, aged 12 to 74 years, with a mean of 43.3-years and median of 40-years. They comprised 14 hemangiomas (35%), 13 lymphangiomas (32.5%), three hamartomas (7.5%), three littoral cell angiomas (7.5%), three sclerosing angiomatoid nodular transformations (SANT, 7.5%) and four angiosarcomas (10%). The majority of the patients (65%) were asymptomatic. Some of the patients (32.5%) complained of abdominal pain, and 2.5% of the patients presented with fever. Metastases were identified in 75% of the patients with an angiosarcoma at the initial work-up. One angiosarcoma patient died of the disease despite adjuvant chemoradiotherapy. The radiological findings for hamartoma, littoral cell angioma, and SANT were nonspecific. Microscopically, six types of vascular lesions showed classic morphological and immunophenotypical features of their type.
CONCLUSIONS
One should be aware of rare splenic vascular lesions when radiological findings are nonspecific. Histomorphological and immunophenotypical features are helpful for the differential diagnosis.

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A Case of Splenic Hamartoma Diagnosed by Contrast-enhanced Ultrasonography and Magnetic Resonance Imaging
Hyeon Sik Kim, Tae Hyo Kim, Jae Min Lee, Hyun Jin Kim, Woon Tae Jung, Ok Jae Lee, Ji Eun Kim, Kyung Soo Bae
The Korean Journal of Gastroenterology.2014; 64(6): 380. CrossRef

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