Journal of Pathology and Translational Medicine

Review

Follicular lymphoma: updates for pathologists: Mahsa Khanlari, Jennifer R. Chapman; J Pathol Transl Med. 2022;56(1):1-15. Published online December 27, 2021; DOI: https://doi.org/10.4132/jptm.2021.09.29

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Follicular lymphoma (FL) is the most common indolent B-cell lymphoma and originates from germinal center B-cells (centrocytes and centroblasts) of the lymphoid follicle. Tumorigenesis is believed to initiate early in precursor B-cells in the bone marrow (BM) that acquire the t(14;18)(q32;q21). These cells later migrate to lymph nodes to continue their maturation through the germinal center reaction, at which time they acquire additional genetic and epigeneticabnormalities that promote lymphomagenesis. FLs are heterogeneous in terms of their clinicopathologic features. Most FLs are indolent and clinically characterized by peripheral lymphadenopathy with involvement of the spleen, BM, and peripheral blood in a substantial subset of patients, sometimes accompanied by constitutional symptoms and laboratory abnormalities. Diagnosis is established by the histopathologic identification of a B-cell proliferation usually distributed in an at least partially follicular pattern, typically, but not always, in a lymph node biopsy. The B-cell proliferation is biologically of germinal center cell origin, thus shows an expression of germinal center-associated antigens as detected by immunophenotyping. Although many cases of FLs are typical and histopathologic features are straightforward, the biologic and histopathologic variability of FL is wide, and an accurate diagnosis of FL over this disease spectrum requires knowledge of morphologic variants that can mimic other lymphomas, and rarely non-hematologic malignancies, clinically unique variants, and pitfalls in the interpretation of ancillary studies. The overall survival for most patients is prolonged, but relapses are frequent. The treatment landscape in FL now includes the application of immunotherapy and targeted therapy in addition to chemotherapy.

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Case Study

Aggressive Supratentorial Ependymoma, RELA Fusion-Positive with Extracranial Metastasis: A Case Report: Seong-Ik Kim, Yoojin Lee, Seung Ki Kim, Hyoung Jin Kang, Sung-Hye Park; J Pathol Transl Med. 2017;51(6):588-593. Published online November 15, 2017; DOI: https://doi.org/10.4132/jptm.2017.08.10

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Abstract PDF

Ependymoma is the third most common pediatric primary brain tumor. Ependymomas are categorized according to their locations and genetic abnormalities, and these two parameters are important prognostic factors for patient outcome. For supratentorial (ST) ependymomas, RELA fusion-positive ependymomas show a more aggressive behavior than YAP1 fusion-positive ependymomas. Extracranial metastases of intra-axial neuroepithelial tumors are extremely rare. In this paper, we report a case of aggressive anaplastic ependymoma arising in the right frontoparietal lobe, which had genetically 1q25 gain, CDKN2A homozygous deletion, and L1CAM overexpression. The patient was a 10-year-old boy who underwent four times of tumor removal and seven times of gamma knife surgery. Metastatic loci were scalp and temporalis muscle overlying primary operation site, lung, liver, buttock, bone, and mediastinal lymph nodes. He had the malignancy for 10 years and died. This tumor is a representative case of RELA fusion-positive ST ependymoma, showing aggressive behavior.

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Magnetic Resonance Imaging Features of Zinc Finger Translocation Associated-RELA Fusion Ependymoma Compared to Its Wild-Type Counterpart
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Original Articles

Reclassification of Mixed Oligoastrocytic Tumors Using a Genetically Integrated Diagnostic Approach: Seong-Ik Kim, Yujin Lee, Jae-Kyung Won, Chul-Kee Park, Seung Hong Choi, Sung-Hye Park; J Pathol Transl Med. 2018;52(1):28-36. Published online September 29, 2017; DOI: https://doi.org/10.4132/jptm.2017.09.25

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Abstract PDF

Background
Mixed gliomas, such as oligoastrocytomas (OA), anaplastic oligoastrocytomas, and glioblastomas (GBMs) with an oligodendroglial component (GBMO) are defined as tumors composed of a mixture of two distinct neoplastic cell types, astrocytic and oligodendroglial. Recently, mutations ATRX and TP53, and codeletion of 1p/19q are shown to be genetic hallmarks of astrocytic and oligodendroglial tumors, respectively. Subsequent molecular analyses of mixed gliomas preferred the reclassification to either oligodendroglioma or astrocytoma. This study was designed to apply genetically integrated diagnostic criteria to mixed gliomas and determine usefulness and prognostic value of new classification in Korean patients.
Methods
Fifty-eight cases of mixed OAs and GBMOs were retrieved from the pathology archives of Seoul National University Hospital from 2004 to 2015. Reclassification was performed according to genetic and immunohistochemical properties. Clinicopathological characteristics of each subgroup were evaluated. Overall survival was assessed and compared between subgroups.
Results
We could reclassify all mixed OAs and GBMOs into either astrocytic or oligodendroglial tumors. Notably, 29 GBMOs could be reclassified into 11 cases of GBM, IDH-mutant, 16 cases of GBM, IDH-wildtype, and two cases of anaplastic oligodendroglioma, IDH mutant. Overall survival was significantly different among these new groups (p<.001). Overall survival and progression-free survival were statistically better in gliomas with IDH mutation, ATRX mutation, no microscopic necrosis, and young patient age (cut off, 45 years old).
Conclusions
Our results strongly suggest that a genetically integrated diagnosis of glioma better reflects prognosis than former morphology-based methods.

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SNUH methylation classifier for CNS tumors
Kwanghoon Lee, Jaemin Jeon, Jin Woo Park, Suwan Yu, Jae-Kyung Won, Kwangsoo Kim, Chul-Kee Park, Sung-Hye Park
Clinical Epigenetics.2025;[Epub] CrossRef
The prognostic significance of p16 expression pattern in diffuse gliomas
Jin Woo Park, Jeongwan Kang, Ka Young Lim, Hyunhee Kim, Seong-Ik Kim, Jae Kyung Won, Chul-Kee Park, Sung-Hye Park
Journal of Pathology and Translational Medicine.2021; 55(2): 102. CrossRef
Dynamic susceptibility contrast and diffusion MR imaging identify oligodendroglioma as defined by the 2016 WHO classification for brain tumors: histogram analysis approach
Anna Latysheva, Kyrre Eeg Emblem, Petter Brandal, Einar Osland Vik-Mo, Jens Pahnke, Kjetil Røysland, John K. Hald, Andrés Server
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Stromal Expression of MicroRNA-21 in Advanced Colorectal Cancer Patients with Distant Metastases: Kyu Sang Lee, Soo Kyung Nam, Jiwon Koh, Duck-Woo Kim, Sung-Bum Kang, Gheeyoung Choe, Woo Ho Kim, Hye Seung Lee; J Pathol Transl Med. 2016;50(4):270-277. Published online May 31, 2016; DOI: https://doi.org/10.4132/jptm.2016.03.19

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Abstract PDF

Background
The aim of this study was to determine the regional heterogeneity and clinicopathological significance of microRNA-21 (miR-21) in advanced colorectal cancer (CRC) patients with distant metastasis.
Methods
miR-21 expression was investigated by using locked nucleic acid– fluorescence in situ hybridization in the center and periphery of the primary cancer and in distant metastasis from 170 patients with advanced CRC. In addition, α-smooth muscle actin and desmin were evaluated to identify cancer-associated fibroblasts (CAFs) by using immunohistochemistry.
Results
The miR-21 signal was observed in the cancer stroma. The expression of miR-21 (a score of 1–4) in the center and periphery of the primary cancer and in distant metastasis was observed in specimens from 133 (78.2%), 105 (61.8%), and 91 (53.5%) patients, respectively. miR-21 expression was heterogeneous in advanced CRC. Discordance between miR-21 expression in the center of the primary cancer and either the periphery of the primary cancer or distant metastasis was 31.7% or 44.7%, respectively. miR-21 stromal expression in the periphery of the primary cancer was significantly associated with a better prognosis (p=.004). miR-21 expression was significantly associated with CAFs in the center of the primary cancer (p=.001) and distant metastases (p=.041).
Conclusions
miR-21 expression is observed in cancer stroma related to the CAF quantity and frequently presents regional heterogeneity in CRC. Our findings indicate that the role of miR-21 in predicting prognosis may be controversial but provide a new perspective of miR-21 level measurement in cancer specimens.

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Review

Molecular Dimensions of Gastric Cancer: Translational and Clinical Perspectives: Yoon Young Choi, Sung Hoon Noh, Jae-Ho Cheong; J Pathol Transl Med. 2016;50(1):1-9. Published online October 26, 2015; DOI: https://doi.org/10.4132/jptm.2015.09.10

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Abstract PDF

Gastric cancer is a global health burden and has the highest incidence in East Asia. This disease is complex in nature because it arises from multiple interactions of genetic, local environmental, and host factors, resulting in biological heterogeneity. This genetic intricacy converges on molecular characteristics reflecting the pathophysiology, tumor biology, and clinical outcome. Therefore, understanding the molecular characteristics at a genomic level is pivotal to improving the clinical care of patients with gastric cancer. A recent landmark study, The Cancer Genome Atlas (TCGA) project, showed the molecular landscape of gastric cancer through a comprehensive molecular evaluation of 295 primary gastric cancers. The proposed molecular classification divided gastric cancer into four subtypes: Epstein-Barr virus–positive, microsatellite unstable, genomic stable, and chromosomal instability. This information will be taken into account in future clinical trials and will be translated into clinical therapeutic decisions. To fully realize the clinical benefit, many challenges must be overcome. Rapid growth of high-throughput biology and functional validation of molecular targets will further deepen our knowledge of molecular dimensions of this cancer, allowing for personalized precision medicine.

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Original Articles

TNF-α and TNF-β Polymorphisms are Associated with Susceptibility to Osteoarthritis in a Korean Population: Lin Han, Joo Hyoun Song, Jung Hwan Yoon, Yong Gyu Park, Suk Woo Lee, Yoo Jin Choi, Suk Woo Nam, Jung Young Lee, Won Sang Park; Korean J Pathol. 2012;46(1):30-37. Published online February 23, 2012; DOI: https://doi.org/10.4132/KoreanJPathol.2012.46.1.30

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Abstract PDF

Background

The tumor necrosis factor (TNF) is believed to play an important role in the pathophysiology of osteoarthritis (OA). Evidence shows that genetic polymorphisms make substantial contributions to the etiology of OA.

Methods

We investigated the genotypes TNF-α and TNF-β in 301 OA patients and 291 healthy subjects as controls. We employed a polymerase chain reaction-restriction fragment length polymorphism and a polymerase chain reaction-single strand conformation polymorphism assay to identify the genotypes TNFA -G308A and TNFB +G252A, respectively.

Results

For TNFA -G308A, the percentages of genotypes GG, AG, and AA were 26.3% (79/301), 62.5% (188/301), and 11.3% (34/301) in OA patients and 88.7% (258/291), 11.3% (33/291), and 0% (0/291) in controls. For TNFB +G252A, the percentages of genotypes GG, AG, and AA were 15.3% (46/301), 41.9% (126/301), and 42.9% (129/301) in OA patients and 12% (35/291), 52.6% (153/291), and 35.4% (103/291) in controls. There were significant differences in genotypes and alleles of TNFA -308 between OA patients and controls (p<0.0001) and in alleles of TNFB +252 (p=0.0325). The risk of OA was significantly higher for carriers of the TNFA -308A allele and the TNFB +252 AA homozygote (p=0.0224).

Conclusions

The results suggest close relationships between TNFA -G308A and TNFB +G252A polymorphisms and individual susceptibility to OA in the Korean population.

Citations

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Expression of Multidrug Resistance Protein 1 in Human Hepatocellular Carcinoma.: Yun Kyung Kang; Korean J Pathol. 2011;45(3):281-289.; DOI: https://doi.org/10.4132/KoreanJPathol.2011.45.3.281

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Abstract PDF

BACKGROUND
Multidrug resistance protein 1 (MDR1) encoded by ATP-binding cassette, sub-family B (Mdr/Tap), member 1 (ABCB1) mediates cross-resistance to antineoplastic drugs, and its expression is related to tumor aggressiveness.
METHODS
MDR1 expression was investigated in 100 hepatocellular carcinomas (HCCs) by immunohistochemical staining. The epigenetic mechanisms underlying ABCB1 transcriptional regulation were investigated in cell lines.
RESULTS
MDR1 was normally localized in the bile canalicular surface of the hepatocytes. Among 100 HCCs, 45 showed canalicular/luminal (CL) staining similar to the normal pattern, another 45 displayed membranous/cytoplasmic (MC) overexpression, and the remaining 10 revealed loss of expression. MC pattern or null staining of HCCs correlated with a higher histological grade and had a poorer prognosis than HCCs with a CL pattern (p<0.05). They also tended to have a poor prognosis by multivariate survival analysis. The ABCB1 promoter was hypomethylated regardless of MDR1 expression or ABCB1 mRNA levels in 10 HCC cell lines. Histone deacetylase inhibitor treatment induced ABCB1 upregulation in 4 cell lines with low or moderate ABCB1 levels.
CONCLUSIONS
Our findings suggest that either an increase or a loss of MDR1 expression may contribute to the poor outcome of HCCs; histone deacetylation may be one of the epigenetic mechanisms directing the ABCB1 expression in HCCs.

Citations

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Preferential expression of prostate specific membrane in CD34 labeled Neo-vasculature of Hepatocellular carcinoma: Prognostic and therapeutic potentials
Safaa MM Abd El Khalek, Mona QR Mohammed, Amira M Al Balakosy
Egyptian Journal of Pathology.2023; 43(1): 66. CrossRef

Intron 1 Polymorphism, Mutation and the Protein Expression of Epidermal Growth Factor Receptor in Relation to the Gefitinib Sensitivity of Korean Lung Cancer Patients.: Mi Jin Kim, Kyeong Cheol Shin, Kwan Ho Lee; Korean J Pathol. 2009;43(6):509-516.; DOI: https://doi.org/10.4132/KoreanJPathol.2009.43.6.509

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Abstract PDF: BACKGROUND
Epidermal growth factor receptor (EGFR) intron 1 polymorphism in non-small cell lung cancer (NSCLC) has been found to have therapeutic implications for the patients treated with EGFR tyrosine kinase inhibitors. However, its clinical significance as related to gefitinib responsiveness is still controversial. We examined CA repeat polymorphism in intron 1 of the EGFR gene and its relation with the EGFR gene mutation in NSCLC patients who were treated with gefitinib. METHODS: Sixty seven patients who were treated with gefitinib were analyzed for intron 1 polymorphism in the EGFR gene, the EGFR mutations and the EGFR protein expression. Two hundred twenty seven samples of NSCLC were analyzed for EGFR mutations. RESULTS: CA repeat was low in 27 patients (40.3%) and high in 40 (59.7%) patients. The response rate for gefitinib therapy was higher in the patient population with a low number of CA repeats in the EGFR gene (p=0.047) and in the patients with the mutated type of EGFR (p=0.048), though these two factors were not related. Thirty four patients (15.0%) harbored EGFR mutations. CONCLUSIONS: This study suggests that the intron 1 CA repeat polymorphism of the EGFR gene may serve as a predictor of the clinical outcome of NSCLC patients treated with gefitinib, and this without regard for EGFR mutation. Our data further supports the importance of EGFR mutations with regard to a distinct clinical profile and the prognostic implications for NSCLC patients.

eNOS Gene Polymorphisms in Perinatal Hypoxic-Ischemic Encephalopathy.: Min Cho, Kwang Sun Hyun, David Chanwook Chung, In Young Choi, Myeung Ju Kim, Young Pyo Chang; Korean J Pathol. 2009;43(4):306-311.; DOI: https://doi.org/10.4132/KoreanJPathol.2009.43.4.306; Retraction in: J Pathol Transl Med 2019;53(5):345

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Clinicopathologic Study of Chromosomal Aberrations in Gastric Lymphomas of Korean Patients.: Wook Youn Kim, Jung Ho Kim, Hyoungsuk Ko, Young A Kim, Yoon Kyung Jeon, Chul Woo Kim; Korean J Pathol. 2009;43(1):5-12.; DOI: https://doi.org/10.4132/KoreanJPathol.2009.43.1.5

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Abstract PDF

BACKGROUND
The incidence and clinical correlation of MALT1 translocation and numerical aberrations in Korean gastric MALT lymphoma patients have been rarely reported. We studied the incidence and clinicopathologic relationship of these chromosomal aberrations in Korean gastric lymphomas.
METHODS
Seventy-six gastric lymphomas, which consisted of 40 low grade MALT lymphoma, 4 high grade MALT lymphoma and 32 diffuse large B-cell lymphoma (DLBCL) cases, were analyzed for the detection of t(11;18) API2-MALT1, t(14;18) IgH-MALT1 and aneuploidies of chromosomes 3 or 18 using fluorescence in situ hybridization.
RESULTS
The t(11;18) was demonstrated in 3 low grade MALT lymphomas (7.5%) and one DLBCL, which was associated with advanced stage, deeper invasion, and disease progression or relapse. The t(14;18) was demonstrated in none of these cases. Trisomy 3 and 18 were detected in 8 (11%) and 11 of 76 cases (12.5%) respectively, and found only in translocation-negative cases. Two of 4 high grade MALT lymphomas showed trisomy 18. All patients survived with successful second treatment after progression or relapse.
CONCLUSIONS
The t(11;18) API2-MALT1 was not quite frequent in Korean low grade gastric MALT lymphomas and was associated with advanced clinical situations. Overall prognosis was good for long-term follow-up regardless of progression or relapse.

Citations

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Clinicopathologic Study of Chromosomal Aberrations in Ocular Adnexal Lymphomas of Korean Patients
Hokyung Choung, Young A Kim, Namju Kim, Min Joung Lee, Sang In Khwarg
Korean Journal of Ophthalmology.2015; 29(5): 285. CrossRef

Histopathology and Mainz Classification of Renal Cell Tumors: A Histogenetic Study and DNA Content Analysis.: Yeong Jin Choi, Tae Kon Hwang, Youn Soo Lee, Byung Kee Kim, Sun Moo Kim, Sang In Shim; Korean J Pathol. 1998;32(7):511-520.

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Abstract: The Mainz classification for renal cell tumors was introduced in 1986 and it's utility has been reported in several histogenetic and genetic studies of renal cell tumors. We present a study of 127 cases of renal cell tumors with clinicopathologic correlation, DNA content analysis, and histogenesis studied by histochemical and immunohistochemical staining. The 127 renal cell tumors classified by the Mainz classification were 87 clear cell, 17 chromophilic, 13 chromophobe and 3 sarcomatoid renal cell carcinomas, 5 oncocytomas and 2 adenomas. These subtypes showed significant correlation not with age, sex, Robson's stage, DNA ploidy or tumor recurrence but with nuclear grade (p=0.001) and tumor size (p=0.001). Hall's colloidal iron (p=0.002) and carbonic anhydrase II (p=0.013) stains, representing the origin of distal nephron especially of collecting duct, were significantly correlated with specific subtypes of renal cell tumors, especially chromophobe cell renal carcinoma. This study demonstrates that the Mainz classification suggests several morphologically different subtypes and variants of renal cell tumors and that some of them may have originated from the distal nephron, particularly from the collecting duct.

Analyses of Genetic Alterations in Breast Cancers by Comparative Genomic Hybridization.: Jin Man Kim, Young Mi Jeon, Young Hyeh Ko, Kyu Sang Song, Howe J Ree, Joo Seob Keum, Jae Hyuk Lee, Sun Hoe Koo; Korean J Pathol. 1999;33(8):603-613.

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Abstract PDF: Transformation and progression of breast cancer are thought to be caused by an accumulation of complex genetic alterations, but little is known about specific changes. In this study, the author has undertaken a genome-wide screening to detect genetic changes in 20 cases of breast cancer among Koreans, including 16 infiltrating ductal carcinomas, 2 medullary carcinomas, 1 invasive lobular carcinoma, and 1 borderline phyllodes tumor. Comparative genomic hybridization (CGH) was used to screen for DNA sequence gains and losses across all human chromosomes. Simultaneous immunohistochemical staining for c-erbB-2 (Her-2/neu), c-myc, cyclin D1, and p53 protein was done to make comparisons with nuclear grade and that with CGH results. Biotin-labeled tumor DNA and digoxigenin-labeled normal DNA were hybridized to normal metaphase cells. The fluorescence signals were captured by fluorescence microscope after detection by avidin-FITC and anti-digoxigenin rhodamine. Then, the ratio of fluorescence was calculated by an image analyzer. The immunohistochemical staining was done in paraffin-embedded tissue with an LSAB kit and avidin-biotin complex (ABC) method. The CGH results showed gains on chromosomes 8q (40%), 1q (30%), 17q (15%), 20q (15%), 18q (15%), 5p (15%), and 13q (15%). Deletions were on chromosomes 17p (45%) and 22q (20%). High-level amplifications (green/red ratio >1.5) were noted on chromosomes 1p31, 1q, 3q25-qter, 5p, 7q31-qter, 8q, 9p22-qter, 10p, 11p, 11q22-qter, 12p, 12q24, 14q21-qter, 15q23-qter, 17q, 18p, 18q12-qter, 20p, and 20q. By comparison with infiltrating ductal carcinoma, the two medullary carcinomas showed high-level amplification on chromosomes 1p31, 1q, 8q, 10p, 11p and 12p. c-erbB-2, c-myc, cyclin D1, and p53 protein expression was immunohistochemically detected in 9 of 20 (45%), 8 of 20 (40%), 10 of 20 (50%), and 13 of 20 (65%), respectively. The results indicate that the amplification on chromosome 8q, 1q and the deletions on chromosomes 17p and 22q are the most frequent genetic alterations in breast cancers among Koreans. The results reveal a different pattern of genetic alteration from previous studies. The CGH results were not correlated with the immunohistochemical profiles. The amplification pattern of medullary carcinomas was quite different from the pattern of infiltrating ductal carcinomas. The CGH was thought to be very useful in the screening of genetic alterations of solid tumors.

mRNA is Synthesized Mainly at the Phase between the Euchromatin and Heterochromatin: Proposal of a Phase Theory.: Mi Sook Kim, Sang Woo Juhng; Korean J Pathol. 2001;35(2):93-97.

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Abstract PDF: BACKGROUND
Malignant cell nuclei, in general, have increased amounts of heterochromatin and decreased electron densities of euchromatin, making the chromatin pattern coarser than that of benign cell nuclei. The chromatin pattern in benign and malignant cells, however, is barely explained in terms of molecular structure. In this study, the chromatin pattern of metaplastic and carcinomatous squamous cells of the uterine cervix was correlated with transcriptional activity by ultrastructural autoradiography. METHODS: Punch-biopsied tissues were cultured with 3H-uridine for 5 minutes and processed for electron microscopy. Thin sections of the tissues on nickel grids were covered with photosensitive emulsion and kept cold in a dark room for 10 to 16 weeks. After development and staining, the tissues were observed by electron microscopy.
RESULTS
The nuclei of the metaplastic squamous cells consisted mostly of euchromatin. A few silver grains were observed, mainly at the periphery of the nuclei. The nuclei of the carcinomatous cells had increased amounts of heterochromatin along the nuclear membrane, and also in the euchromatin area. Silver grains were observed mainly at the boundary between the heterochromatin and euchromatin.
CONCLUSION
These findings suggest that an increased amount of heterochromatin in carcinomatous cells results in an increase of the boundary area between the heterochromatin and euchromatin, an area which may be a transcriptionally active site.

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