Journal of Pathology and Translational Medicine

Review

Single-cell and spatial sequencing application in pathology: Yoon-Seob Kim, Jinyong Choi, Sug Hyung Lee; J Pathol Transl Med. 2023;57(1):43-51. Published online January 10, 2023; DOI: https://doi.org/10.4132/jptm.2022.12.12

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Traditionally, diagnostic pathology uses histology representing structural alterations in a disease’s cells and tissues. In many cases, however, it is supplemented by other morphology-based methods such as immunohistochemistry and fluorescent in situ hybridization. Single-cell RNA sequencing (scRNA-seq) is one of the strategies that may help tackle the heterogeneous cells in a disease, but it does not usually provide histologic information. Spatial sequencing is designed to assign cell types, subtypes, or states according to the mRNA expression on a histological section by RNA sequencing. It can provide mRNA expressions not only of diseased cells, such as cancer cells but also of stromal cells, such as immune cells, fibroblasts, and vascular cells. In this review, we studied current methods of spatial transcriptome sequencing based on their technical backgrounds, tissue preparation, and analytic procedures. With the pathology examples, useful recommendations for pathologists who are just getting started to use spatial sequencing analysis in research are provided here. In addition, leveraging spatial sequencing by integration with scRNA-seq is reviewed. With the advantages of simultaneous histologic and single-cell information, spatial sequencing may give a molecular basis for pathological diagnosis, improve our understanding of diseases, and have potential clinical applications in prognostics and diagnostic pathology.

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A comparative analysis of single-cell transcriptomic technologies in plants and animals
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Frontiers in Immunology.2023;[Epub] CrossRef

Original Articles

A comparative prognostic performance of definitions of Crohn-like lymphoid reaction in colorectal carcinoma: Younghoon Kim, Jeong Mo Bae, Jung Ho Kim, Nam-Yun Cho, Gyeong Hoon Kang; J Pathol Transl Med. 2021;55(1):53-59. Published online November 27, 2020; DOI: https://doi.org/10.4132/jptm.2020.10.06

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Abstract PDF Supplementary Material: Background
The prognostic potential of Crohn-like lymphoid reaction (CLR) in colorectal carcinoma (CRC) has been investigated through the assessment of different criteria.
Methods
The prognostic impact of CLR was investigated in 636 CRC patients to compare methods from previously published articles. These methods included CLR measured by number of lymphoid aggregates (LAs) (CLR count), LA size greater than or equal to 1 mm (CLR size), CLR density with a cutoff value of 0.38, and subjective criteria as defined by intense CLR.
Results
In univariate survival analysis, CLR-positive CRC as defined by the four aforementioned methods was associated with better overall survival (OS) (hazard ratio [HR], 0.463; 95% confidence interval [CI], 0.305 to 0.702; p <.001; HR, 0.656; 95% CI, 0.411 to 1.046; p=.077; HR, 0.363; 95% CI, 0.197 to 0.669; p=.001; and HR, 0.433; 95% CI, 0.271 to 0.690; p<.001, respectively) and disease-free survival (DFS) (HR, 0.411; 95% CI, 0.304 to 0.639; p<.001; HR, 0.528; 95% CI, 0.340 to 0.821; p=.004; HR, 0.382; 95% CI, 0.226 to 0.645, p=.004; and HR, 0.501; 95% CI, 0.339 to 0.741; p<.001, respectively) than CLR-negative CRC, regardless of criteria with the exception of OS for CLR density. In multivariate analysis, two objective criteria (CLR count and CLR density) and one subjective criterion (intense CLR) for defining CLR were considered independent prognostic factors of OS and DFS in CRC patients.
Conclusions
CLR has similar traits regardless of criteria, but CLR-positivity should be defined by objective criteria for better reproducibility and prognostic value.

Renal Histologic Parameters Influencing Postoperative Renal Function in Renal Cell Carcinoma Patients: Myoung Ju Koh, Beom Jin Lim, Kyu Hun Choi, Yon Hee Kim, Hyeon Joo Jeong; Korean J Pathol. 2013;47(6):557-562. Published online December 24, 2013; DOI: https://doi.org/10.4132/KoreanJPathol.2013.47.6.557

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Abstract PDF

Background

Pre-existing non-neoplastic renal diseases or lesions may influence patient renal function after tumor removal. However, its description is often neglected or omitted in pathologic reports. To determine the incidence and clinical significance of non-neoplastic lesions, we retrospectively examined renal tissues obtained during 85 radical nephrectomies for renal cell carcinoma.

Methods

One paraffin-embedded tissue block from each case containing a sufficient amount of non-tumorous renal parenchyma was cut and processed with hematoxylin and eosin and periodic acid-Schiff methods. Non-neoplastic lesions of each histological compartment were semi-quantitatively and quantitatively evaluated.

Results

Among the various histologic lesions found, tubular atrophy, arterial intimal thickening, and glomerulosclerosis were the most common (94.1%, 91.8%, and 88.2%, respectively). Glomerulosclerosis correlated with estimated glomerular filtration rate at the time of surgery, as well as at 1- and 5-years post-surgery (p=.0071), but tubulointerstitial fibrosis or arterial fibrous intimal thickening did not. Post-hoc analysis revealed that glomerulosclerosis of more than 20% predicted post-operative renal function. However, its significance disappeared when gender and age were considered.

Conclusions

In conclusion, non-neoplastic lesions, especially with regard to glomerulosclerosis percentage, should be described in pathology reports to provide additional information on renal function decline.

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Chronic kidney damage pathology score for systematic assessment of the non-neoplastic kidney tissue and prediction of post-operative renal function outcomes
Yong Jia, Seyed M.M. Poor, Brenden Dufault, Vivian Lu, Jasmir G. Nayak, Deepak K. Pruthi, Ian W. Gibson
Human Pathology.2022; 124: 76. CrossRef
Value of intravoxel incoherent motion for differential diagnosis of renal tumors
Qingqiang Zhu, Wenrong Zhu, Jing Ye, Jingtao Wu, Wenxin Chen, Zhihua Hao
Acta Radiologica.2019; 60(3): 382. CrossRef
Conventional and Papillary Renal Cell Carcinomas and Focal Segmental Glomerulosclerosis in a Nephrectomy
Firas Al-Delfi, Guillermo A. Herrera
Pathology Case Reviews.2015; 20(6): 263. CrossRef

Morphologic Alteration of Metastatic Neuroblastic Tumor in Bone Marrow after Chemotherapy: Go Eun Bae, Yeon-Lim Suh, Ki Woong Sung, Jung-Sun Kim; Korean J Pathol. 2013;47(5):433-442. Published online October 25, 2013; DOI: https://doi.org/10.4132/KoreanJPathol.2013.47.5.433

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Abstract PDF

Background

The aim of this study is to evaluate the histologic features of metastatic neuroblastic tumors (NTs) in bone marrow (BM) before and after chemotherapy in comparison with those of primary NTs.

Methods

A total of 294 biopsies from 48 children diagnosed with NTs with BM metastasis were examined. There were 48 primary neoplasm biopsies, 48 BM biopsies before chemotherapy, 36 primary neoplasm excisional biopsies after chemotherapy, and 162 BM biopsies after chemotherapy.

Results

Metastatic NTs in BM before chemotherapy were composed of undifferentiated and/or differentiating neuroblasts, but had neither ganglion cells nor Schwannian stroma. Metastatic foci of BM after chemotherapy were found to have differentiated into ganglion cells or Schwannian stroma, which became more prominent after further cycles of chemotherapy. Persistence of NTs or tumor cell types in BM after treatment did not show statistically significant correlation to patients' outcome. However, three out of five patients who newly developed poorly differentiated neuroblasts in BM after treatment expired due to disease progression.

Conclusions

Metastatic NTs in BM initially consist of undifferentiated or differentiating neuroblasts regardless of the primary tumor subtype, and become differentiated after chemotherapy. Newly appearing poorly differentiated neuroblasts after treatment might be an indicator for poor prognosis.

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Postchemotherapy gross residual tumor in non‐high‐risk neuroblastoma: Clinical significance and the role of adjuvant therapy
Eun Seop Seo, Hana Lim, Hee Won Cho, Hee Young Ju, Ji Won Lee, Keon Hee Yoo, Sanghoon Lee, Do Hoon Lim, Ki Woong Sung, Hong Hoe Koo
Pediatric Blood & Cancer.2022;[Epub] CrossRef

Histologic Variations and Immunohistochemical Features of Metastatic Clear Cell Renal Cell Carcinoma: Cheol Lee, Jeong-Whan Park, Ja Hee Suh, Kyung Han Nam, Kyung Chul Moon; Korean J Pathol. 2013;47(5):426-432. Published online October 25, 2013; DOI: https://doi.org/10.4132/KoreanJPathol.2013.47.5.426

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Abstract PDF

Background

Due to advancements in treatment of metastatic and advanced renal cell carcinoma (RCC), it has become increasingly important to diagnose metastatic RCC and the specific subtype. In this study, we investigated the diverse histologic features of metastatic clear cell renal cell carcinoma (CCRCC) cases in comparison with corresponding primary lesions.

Methods

We identified 119 metastatic CCRCC cases from 81 corresponding primary lesions diagnosed between 1995 and 2010 and evaluated the diverse histologic and immunohistochemical features of these lesions.

Results

A total of 44 primary lesions (54.3%) had a non-clear cell component in addition to a typical clear cell component. Of the 119 metastatic lesions, 63 lesions (52.9%) contained a non-clear cell component, and 29 metastatic lesions were composed of a non-clear cell component only. Rhabdoid features were the most frequent non-clear cell histology among the metastatic lesions. Metastatic CCRCCs mainly showed positive CD10 and epithelial membrane antigen staining and negative cytokeratin 7 staining.

Conclusions

Metastatic CCRCC commonly showed a variety of histologic features. If there is a difficulty to diagnose metastatic CCRCC due to a variety of histologic features or small biopsy specimen, histologic review of the primary lesion and immunohistochemical analysis can help determine the correct diagnosis.

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Painful, bleeding fingertip papule
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Development and initial clinical testing of a multiplexed circulating tumor cell assay in patients with clear cell renal cell carcinoma
Rory M. Bade, Jennifer L. Schehr, Hamid Emamekhoo, Benjamin K. Gibbs, Tamara S. Rodems, Matthew C. Mannino, Joshua A. Desotelle, Erika Heninger, Charlotte N. Stahlfeld, Jamie M. Sperger, Anupama Singh, Serena K. Wolfe, David J. Niles, Waddah Arafat, John
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Shoujun Chen, Elba A. Turbat-Herrera, Guillermo A. Herrera, Meghna Chadha, Rodney E. Shackelford, Eric X. Wei
Ultrastructural Pathology.2018; 42(4): 369. CrossRef
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Cancer Immunology Research.2018; 6(7): 758. CrossRef
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Cheol Lee, Bohyun Kim, Boram Song, Kyung Chul Moon
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Tsuyoshi Ueno, Motohiro Yamashita, Shigeki Sawada, Ryujiro Sugimoto, Noriko Nishijima, Yoshifumi Sugawara, Iku Ninomiya
General Thoracic and Cardiovascular Surgery.2016; 64(3): 149. CrossRef
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Concordance of Pathologic Features Between Metastatic Sites and the Primary Tumor in Surgically Resected Metastatic Renal Cell Carcinoma
Sarah P. Psutka, John C. Cheville, Brian A. Costello, Suzanne B. Stewart-Merrill, Christine M. Lohse, Bradley C. Leibovich, Stephen A. Boorjian, R. Houston Thompson
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The Correlation of Tissue-Based Biomarkers in Primary and Metastatic Renal Cell Carcinoma Lesions: A Tissue Microarray Study
Sung Han Kim, Weon Seo Park, Eun Young Park, Boram Park, Jungnam Joo, Jae Young Joung, Ho Kyung Seo, Kang Hyun Lee, Jinsoo Chung
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YU ZOU, JINGJING XU, MINMING ZHANG
Oncology Letters.2016; 11(5): 3273. CrossRef
Genetic alterations in renal cell carcinoma with rhabdoid differentiation
Carmen M. Perrino, Vishwanathan Hucthagowder, Michael Evenson, Shashikant Kulkarni, Peter A. Humphrey
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High expression of APRIL correlates with poor prognosis in clear cell renal cell carcinoma
Cheol Lee, Jeong-Whan Park, Ja Hee Suh, Kyung Chul Moon
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Correlation Analysis Between Cervicovaginal Cytologic and Histopathologic Diagnoses in Cervical Squamous Cell Neoplasm.: Kyoung Bun Lee, Woon Sun Park, Jin Hee Sohn, Min Kyung Kim, Dong Hoon Kim, Hee Sung Kim, Seoung Wan Chae, Sung Hee Kang, Young Hye Cho, Hee Dae Pak, Sun Hee Kim; Korean J Pathol. 2009;43(2):157-163.; DOI: https://doi.org/10.4132/KoreanJPathol.2009.43.2.157

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Abstract PDF

BACKGROUND
The aim of this study was to confirm the usefulness of cervicovaginal smears in the screening of squamous cell neoplasms of the uterine cervix by comparative analysis between the cytologic diagnosis of cervicovaginal smears and the histologic diagnosis of tissue specimens.
METHODS
We selected 743 patients who had both cervicovaginal smears and histologic evaluations of the uterine cervix by colposcopic biopsy, conization, or hysterectomy at the Kangbuk Samsung Medical Center between January 2005 and December 2007.
RESULTS
The accuracy rate of cervicovaginal smears and histologic diagnoses was 93.0% (691/743) and showed a high correspondence (kappa value, 0.770, p-value, 0.000). The false-negative and false-positive rates were 0.5% (6/484) and 17.8% (46/259), respectively. The sampling and interpretation errors were identified in four and two cases of six false-negative cases and 29 and 17 cases of 46 false-positive cases, respectively. In screening high grade squamous cell neoplasms, there were no false-negative cases and only one false-positive case which resulted from sampling error. The false-negative rate of cervicovaginal smears and the false-positive rate in high-grade squamous cell neoplsams were very low.
CONCLUSIONS
The cervicovaginal smear is a powerful tool for screening of cervical squamous cell neoplasms.

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Clinical Validation of Anyplex II HPV HR Detection Test for Cervical Cancer Screening in Korea
Sunkyung Jung, Byungdoo Lee, Kap No Lee, Yonggoo Kim, Eun-Jee Oh
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Asian Pacific Journal of Cancer Prevention.2014; 15(14): 5811. CrossRef

Case Reports

Kaposi's Sarcoma: A report of three cases.: Yeon Soo Lee, Yeong Jin Choi, Mi Kyung Jee, Seok Jin Kang, Byoung Kee Kim, Sun Moo Kim; Korean J Pathol. 1995;29(3):385-390.

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Abstract PDF: The classic type of Kaposi's sarcoma, or multifocal hemorrhagic sarcoma histologically characterized by proliferating fibroblastic and microvascular elements was described by Kaposi as a relatively rare neoplasm. During the past nine years, we experienced three cases of sporadic, classic Kaposi's sarcomas. They were presented as multiple papules, macules and nodules on the skin of the hands, lower logs and feet without systemic involvement. Histologically, Kaposi's sarcoma is divided into three stages, early patch, plaque and nodular stages. The nodular lesions(case 1, 2 and 3) showed extensive proliferatiion of spindle shaped, somewhat pleomorphic cells having dark prominent nuclei, proliferation of small vessels with solid aggregates of endothelial cells, and extravasation of erythrocytes. In early patch stage(case 3), widely dilated, anastomosing, thin-walled vascular spaces are noted in the upper half of the dermis. In plaque stage(case I and 3), there are proliferation of spindle shaped cells with extravasated erythrocytes and aggregates of blood vessels lined by prominent endothelial cells.

Granulomatous Mycosis Fungoides: A case report.: Kyung Sin Lee, Young Oak Kim, Kee Suck Suh, Sang Tae Kim, Man Ha Huh; Korean J Pathol. 1995;29(5):694-697.

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Abstract: Granulomatous mycosis fungoides is an extremely rare and unusual histologic variant of mycosis fungoides. This form is clinically characterized by spontaneous resolution of ulcerated nodular lesions into poikiloderma. Histologically, a strong granulomatous component can obscure the underlying cutaneous lymphoma, which is frequently mistaken for non-neoplastic dermatitides or cutaneous sarcoidosis. We report a case of granulomatous mycosis fungoides occurring on the left cheek of 34-year-old man confirmed histologically with an aid of immunohistochemistry and clinical course (immediate response to PROMACE-CYTOBAM chemotherapy), with emphasis on differential diagnosis, along with a review of literature. This is the first documented report in the Korean literature.

Original Article

Analysis of Histological Findings and Estrogen and Progesterone Receptor Status in Luteal Phase Defect Caused by Delayed Ovulation and Clomiphen Treatment.: Kyu Rae Kim, Hee Jeong Ahn, Jai Hyang Go, Dong Hee Choi, Byoung Goo Yoon; Korean J Pathol. 1996;30(12):1106-1115.

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Abstract PDF: Luteal phase defect (LPD) is an ovulatory disorder of considerable clinical importance that leads to delayed endometrial maturation and inadequate endometrium for blastocyst implantation. This disorder is implicated in infertility and recurrent spontaneous abortion. We analyzed the endometrial histological maturation, and the estrogen receptor(ER) and progesterone receptor(PR) status in patients with unexplained delayed ovulation, and in patients with ovulation induction by clomiphen citrate. The purpose of this study was to determine whether the length of the follicular phase influences the endometrial histological maturation and the hormonal receptor status, and to know the effect of clomiphen citrate on the endometrium. In the delayed ovulation group, the endometrium was characterized by an irregular outpouching and dilated lumina of the glands, a decreased secretory activity and predecidualization, and a decreased number of granulocytes in the stroma. In the clomiphen citrate-ovulation induction group, glandular proliferation was markedly diminished with poorly convoluted and narrow glands, secretory activity was decreased, stroma was undecidualized, and there was an absence of granulocytes. ER expression was increased in the glandular epithelium in the delayed ovulation group, and both ER and PR expressions were markedly decreased in the glandular epithelium and stromal cells in the ovulation induction group. Endometrial maturation and differentiation may be diminished by increased estrogenic and relatively deficient progesterone effects in patients with delayed ovulation. The hormonal receptor status might also be influenced by hormonal changes. Clomiphen citrate successfully induced ovulation in patients with delayed ovulation, however, endometrial proliferation and maturation were markedly suppressed. This might be related to the lower pregnancy rate and higher abortion rate in patients with clomiphen citrate induced ovulation.

Case Report

Metanephric Adenoma of the Kidney.: Yoon La Choi, Jung Won Lee, Jai Hyang Go, Cheol Keun Park; Korean J Pathol. 1998;32(1):72-75.

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Abstract PDF: Metanephric adenoma is a rare renal epithelial tumor. Its light microscopic features are very characteristic, and immunohistochemical and electron microscopic studies are not critical to the diagnosis. The literature indicate that, to date, the tumor has behaved in a benign fashion, and predominantly but not exclusively occurred in middle-aged women. It occurs in a wide range up to 11 cm and is usually an incidental finding but may be symptomatic with hematuria or flank pain. Recently, we have experienced a case of renal tumor showing distinctive adenomatous features, which is incidentally found in a 52-year-old female. This tumor is confined to the renal cortex and is well-circumscribed with a characteristic uniform and orderly proliferation of compact well-differentiated small tubules lined by bland oval cells with a very low level of mitotic activity. The term metanephric adenoma is appropriate for this tumor because it accurately describes its bland proliferation of tubules and reflects the embryonic architectural and cytological appearance of this proliferation. The pattern of the tumor, with its occasional papillary glomeruloid- like bodies and foci of elongated tubules, is reminiscent of the fetal metanephric kidney.

Original Articles

Nitric Oxide Synthase Expression in Early Stage of Aging Rat Kidney.: Kye Won Kwon, Hyeon Joo Jeong; Korean J Pathol. 2004;38(2):86-92.

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Abstract PDF: BACKGROUND
Nitric oxide synthase (NOS) has been suggested to have a role in renal injury of aging rats.
METHODS
Renal function and histology were compared between 12 month-and 7-9 week-old rats. Proliferating activity and cell death were evaluated by PCNA index and apoptosis. Three isoforms of NOS (eNOS, iNOS, and nNOS) were stained by immunohistochemistry.
RESULTS
Serum creatinine level was increased in old rats (1.0 mg/dL vs 0.5 mg/dL, p=0.000). 24 h proteinuria and urinary NO were comparable between the two groups. The percentage of global and segmental glomerulosclerosis increased in old rats. PCNA index decreased in the glomeruli (0.1 vs 0.6/glomerulus, p=0.005) and the tubulointerstitium (10.2 vs 19.2/mm2, p=0.019) of old rats compared to that of young rats. However, no difference was observed in the number of TUNEL positive cells. eNOS was not stained in young and old rat kidney, whereas iNOS was stained in the interstitial inflammatory cells of old rats (0.3 vs 0.0 of young rats/mm2, p=0.188). Macula densa nNOS staining significantly decreased in old rats compared to young rats (5.6 vs 9.5/mm2, p=0.009).
CONCLUSIONS
Proliferating activity is more affected than cell death with aging. Decreased nNOS expression without alteration of eNOS and iNOS expressions may implicate nNOS as a marker of renal injury in the early stage of aging.

Papillary Eccrine Adenoma: Histopathological and Immunohistochemical study.: Chan Kum Park; Korean J Pathol. 1993;27(5):518-523.

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Abstract PDF: Papillary eccrine adenoma is a rare benign sweat gland neoplasm. However, it can show locally aggressive clinical course when it is incompletely removed. A case of papillary eccrine adenoma of the thigh of a 46-year-old woman is reported. Immunohistochemical studies showed that this tumor was diffusely positive for cytokeratin(CAM 5.2), and carcinoembryonic antigen, and focally positive for EMA in the luminal cells of the neoplastic ducts. S-100 protein was not stained in the luminal cells and myoepithelial cells of neoplastic ducts. Papillary eccrine adenoma appears to differentiate toward ductal structures of the eccrine sweat apparatus.

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