Journal of Pathology and Translational Medicine

Original Article

Diagnostic distribution and pitfalls of glandular abnormalities in cervical cytology: a 25-year single-center study: Jung-A Sung, Ilias P. Nikas, Haeryoung Kim, Han Suk Ryu, Cheol Lee; J Pathol Transl Med. 2022;56(6):354-360. Published online November 9, 2022; DOI: https://doi.org/10.4132/jptm.2022.09.05

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Background
Detection of glandular abnormalities in Papanicolaou (Pap) tests is challenging. This study aimed to review our institute’s experience interpreting such abnormalities, assess cytohistologic concordance, and identify cytomorphologic features associated with malignancy in follow-up histology.
Methods
Patients with cytologically-detected glandular lesions identified in our pathology records from 1995 to 2020 were included in this study.
Results
Of the 683,197 Pap tests performed, 985 (0.144%) exhibited glandular abnormalities, 657 of which had tissue follow-up available. One hundred eighty-eight cases were cytologically interpreted as adenocarcinoma and histologically diagnosed as malignant tumors of various origins. There were 213 cases reported as atypical glandular cells (AGC) and nine cases as adenocarcinoma in cytology, yet they were found to be benign in follow-up histology. In addition, 48 cases diagnosed with AGC and six with adenocarcinoma cytology were found to have cervical squamous lesions in follow-up histology, including four squamous cell carcinomas. Among the cytomorphological features examined, nuclear membrane irregularity, three-dimensional clusters, single-cell pattern, and presence of mitoses were associated with malignant histology in follow-up.
Conclusions
This study showed our institute’s experience detecting glandular abnormalities in cervical cytology over a 25-year period, revealing the difficulty of this task. Nonetheless, the present study indicates that several cytological findings such as membrane irregularity, three-dimensional clusters, single-cell pattern, and evidence of proliferation could help distinguishing malignancy from a benign lesion.

Citations

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Analysis of atypical glandular cells in ThinPrep Pap smear and follow-up histopathology
Tengfei Wang, Yinan Hua, Lina Liu, Bing Leng
Baylor University Medical Center Proceedings.2024; 37(3): 403. CrossRef

Review

Clinical management of abnormal Pap tests: differences between US and Korean guidelines: Seyeon Won, Mi Kyoung Kim, Seok Ju Seong; J Pathol Transl Med. 2020;54(3):213-219. Published online April 15, 2020; DOI: https://doi.org/10.4132/jptm.2020.03.11

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Abstract PDF

Cervical cancer has been the most common gynecological cancer in Korea but has become a preventable disease with regular screening and proper vaccination. If regular screening is provided, cervical cancer does not progress to more than carcinoma in situ, due to its comparatively long precancerous duration (years to decades). In 2012, the American Society for Colposcopy and Cervical Pathology published guidelines to aid clinicians in managing women with abnormal Papanicolaou (Pap) tests, and they soon became the standard in the United States. Not long thereafter, the Korean Society of Gynecologic Oncology and the Korean Society for Cytopathology published practical guidelines to reflect the specific situation in Korea. The detailed screening guidelines and management options in the case of abnormal Pap test results are sometimes the same and sometimes different in the United States and Korean guidelines. In this article, we summarize the differences between the United States and Korean guidelines in order to facilitate physicians’ proper management of abnormal Pap test results.

Citations

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Analysis of HR-HPV Infection Concordance Rates in Cervical and Urine Specimens; Proposal of Additional Cervical Screening Process for Women Who Refuse Invasive Cervical Sampling
Dong Hyeok Kim, Hyunwoo Jin, Kyung Eun Lee
Journal of Personalized Medicine.2022; 12(12): 1949. CrossRef
Analysis of HR-HPV Prevalence among Unvaccinated Busan Women
Dong Hyeok Kim, Kyung Eun Lee
Biomedical Science Letters.2022; 28(4): 229. CrossRef

Original Articles

Comparison of papanicolaou smear and human papillomavirus (HPV) test as cervical screening tools: can we rely on HPV test alone as a screening method? An 11-year retrospective experience at a single institution: Myunghee Kang, Seung Yeon Ha, Hyun Yee Cho, Dong Hae Chung, Na Rae Kim, Jungsuk An, Sangho Lee, Jae Yeon Seok, Juhyeon Jeong; J Pathol Transl Med. 2020;54(1):112-118. Published online January 15, 2020; DOI: https://doi.org/10.4132/jptm.2019.11.29

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Abstract PDF

Background
The decrease in incidence of cervical dysplasia and carcinoma has not been as dramatic as expected with the development of improved research tools and test methods. The human papillomavirus (HPV) test alone has been suggested for screening in some countries. The National Cancer Screening Project in Korea has applied Papanicolaou smears (Pap smears) as the screening method for cervical dysplasia and carcinoma. We evaluated the value of Pap smear and HPV testing as diagnostic screening tools in a single institution.
Methods
Patients co-tested with HPV test and Pap smear simultaneously or within one month of each other were included in this study. Patients with only punch biopsy results were excluded because of sampling errors. A total of 999 cases were included, and the collected reports encompassed results of smear cytology, HPV subtypes, and histologic examinations.
Results
Sensitivity and specificity of detecting high-grade squamous intraepithelial lesion (HSIL) and squamous cell carcinoma (SCC) were higher for Pap smears than for HPV tests (sensitivity, 97.14%; specificity, 85.58% for Pap smears; sensitivity, 88.32%; specificity, 54.92% for HPV tests). HPV tests and Pap smears did not differ greatly in detection of low-grade squamous intraepithelial lesion (85.35% for HPV test, 80.31% for Pap smears). When atypical glandular cells were noted on Pap smears, the likelihood for histologic diagnosis of adenocarcinoma following Pap smear was higher than that of high-risk HPV test results (18.8 and 1.53, respectively).
Conclusions
Pap smears were more useful than HPV tests in the diagnosis of HSIL, SCC, and glandular lesions.

Citations

Citations to this article as recorded by

Challenges in the diagmosis of cervical pathologies
D. Y. Chernov, O. A. Tikhonovskaya, S. V. Logvinov, I. A. Petrov, Y. S. Yuriev, A. A. Zhdankina, A. V. Gerasimov, I. V. Zingalyuk, G. A. Mikheenko
Bulletin of Siberian Medicine.2024; 22(4): 201. CrossRef
Selection of endogenous control and identification of significant microRNA deregulations in cervical cancer
T. Stverakova, I. Baranova, P. Mikyskova, B. Gajdosova, H. Vosmikova, J. Laco, V. Palicka, H. Parova
Frontiers in Oncology.2023;[Epub] CrossRef
Attitudes towards prevention of cervical cancer and early diagnosis among female academicians
Nurhan Doğan, Gamze Fışkın
Journal of Obstetrics and Gynaecology Research.2022; 48(6): 1433. CrossRef
Role of Self-Sampling for Cervical Cancer Screening: Diagnostic Test Properties of Three Tests for the Diagnosis of HPV in Rural Communities of Cuenca, Ecuador
Bernardo Vega Crespo, Vivian Alejandra Neira, José Ortíz Segarra, Ruth Maldonado Rengel, Diana López, María Paz Orellana, Andrea Gómez, María José Vicuña, Jorge Mejía, Ina Benoy, Tesifón Parrón Carreño, Veronique Verhoeven
International Journal of Environmental Research and Public Health.2022; 19(8): 4619. CrossRef
Utility of Scoring System for Screening and Early Warning of Cervical Cancer Based on Big Data Analysis
Dan Hou, Binjie Yang, Yangdan Li, Ming Sun
Frontiers in Public Health.2022;[Epub] CrossRef
Evaluation of Urine and Vaginal Self-Sampling versus Clinician-Based Sampling for Cervical Cancer Screening: A Field Comparison of the Acceptability of Three Sampling Tests in a Rural Community of Cuenca, Ecuador
Bernardo Vega Crespo, Vivian Alejandra Neira, José Ortíz S, Ruth Maldonado-Rengel, Diana López, Andrea Gómez, María José Vicuña, Jorge Mejía, Ina Benoy, Tesifón Parrón Carreño, Veronique Verhoeven
Healthcare.2022; 10(9): 1614. CrossRef
Diagnostic distribution and pitfalls of glandular abnormalities in cervical cytology: a 25-year single-center study
Jung-A Sung, Ilias P. Nikas, Haeryoung Kim, Han Suk Ryu, Cheol Lee
Journal of Pathology and Translational Medicine.2022; 56(6): 354. CrossRef
Comparison of Learning Transfer Using Simulation Problem-Based Learning and Demonstration: An Application of Papanicolaou Smear Nursing Education
Jeongim Lee, Hae Kyoung Son
International Journal of Environmental Research and Public Health.2021; 18(4): 1765. CrossRef
Investigating host-virus interaction mechanism and phylogenetic analysis of viral proteins involved in the pathogenesis
Ahmad Abu Turab Naqvi, Farah Anjum, Alaa Shafie, Sufian Badar, Abdelbaset Mohamed Elasbali, Dharmendra Kumar Yadav, Md. Imtaiyaz Hassan, Timir Tripathi
PLOS ONE.2021; 16(12): e0261497. CrossRef
Utility of Human Papillomavirus Testing for Cervical Cancer Screening in Korea
Mee-seon Kim, Eun Hee Lee, Moon-il Park, Jae Seok Lee, Kisu Kim, Mee Sook Roh, Hyoun Wook Lee
International Journal of Environmental Research and Public Health.2020; 17(5): 1726. CrossRef

Expression of CHOP in Squamous Tumor of the Uterine Cervix: Hyun Hee Chu, Jun Sang Bae, Kyoung Min Kim, Ho Sung Park, Dong Hyu Cho, Kyu Yun Jang, Woo Sung Moon, Myoung Jae Kang, Dong Geun Lee, Myoung Ja Chung; Korean J Pathol. 2012;46(5):463-469. Published online October 25, 2012; DOI: https://doi.org/10.4132/KoreanJPathol.2012.46.5.463

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Abstract PDF

Background

High-risk human papillomavirus (HR-HPV) infection and abnormal p53 expression are closely involved in carcinogenesis of squamous cell carcinoma (SqCC) of uterine cervix. Recent studies have suggested that virus-induced endoplasmic reticulum (ER) stress modulates various cell survival and cell death signaling pathways. The C/EBP homologous protein (CHOP) is associated with ER stress-mediated apoptosis and is also involved in carcinogenesis of several human cancers. We hypothesized that CHOP is involved in the carcinogenesis of uterine cervical cancer in association with HR-HPV and/or p53.

Methods

Immunohistochemistry was used to analyze CHOP and p53 protein expression of tissue sections from 191 patients with invasive cancer or preinvasive lesions of the uterine cervix (61 cases of SqCC, 66 cases of cervical intraepithelial neoplasia [CIN] III, and 64 cases of CIN I).

Results

CHOP was expressed in 59.4% of CIN I, 48.5% of CIN III, and 70.5% of SqCC cases. It was also significantly more frequent in invasive SqCC than in preinvasive lesions (p=0.042). Moreover, CHOP expression significantly correlated with HR-HPV infection and p53 expression (p=0.009 and p=0.038, respectively).

Conclusions

Our results suggest that CHOP is involved in the carcinogenesis of the uterine cervix SqCC via association with HR-HPV and p53.

Citations

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Nucleosides, Nucleotides & Nucleic Acids.2023; : 1. CrossRef
Endoplasmic Reticulum Stress and Homeostasis in Reproductive Physiology and Pathology
Elif Guzel, Sefa Arlier, Ozlem Guzeloglu-Kayisli, Mehmet Tabak, Tugba Ekiz, Nihan Semerci, Kellie Larsen, Frederick Schatz, Charles Lockwood, Umit Kayisli
International Journal of Molecular Sciences.2017; 18(4): 792. CrossRef
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Qiao Qiao, Chaonan Sun, Chuyang Han, Ning Han, Miao Zhang, Guang Li
Cancer Science.2017; 108(7): 1421. CrossRef
Curcumin induces ER stress-mediated apoptosis through selective generation of reactive oxygen species in cervical cancer cells
Boyun Kim, Hee Seung Kim, Eun-Ji Jung, Jung Yun Lee, Benjamin K. Tsang, Jeong Mook Lim, Yong Sang Song
Molecular Carcinogenesis.2016; 55(5): 918. CrossRef
Down-regulation of C/EBP homologous protein (CHOP) expression in gastric cardia adenocarcinoma: Their relationship with clinicopathological parameters and prognostic significance
Xiao-Juan Zhu, She-Gan Gao, San-Qiang Li, Zhen-Guo Shi, Zhi-Kun Ma, Shan-Shan Zhu, Xiao-Shan Feng
Clinics and Research in Hepatology and Gastroenterology.2015; 39(3): 391. CrossRef
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Loss of E-cadherin and Acquisition of Vimentin in Epithelial-Mesenchymal Transition are Noble Indicators of Uterine Cervix Cancer Progression: Na-Hye Myong; Korean J Pathol. 2012;46(4):341-348. Published online August 23, 2012; DOI: https://doi.org/10.4132/KoreanJPathol.2012.46.4.341

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Abstract PDF

Background

Epithelial-mesenchymal transition (EMT) has been known to play a key role in the stromal invasion of carcinoma in situ (CIS) lesion. Loss of E-cadherin and acquisition of vimentin are two critical steps in EMT, that are induced by Snail-1 upregulation associated with overexpression of epidermal growth factor receptor (EGFR). However, roles of EMT-related proteins in human cervical tissues have not been fully elucidated. In this study, we investigated the immunoexpressions of EMT-related proteins in CIS, microinvasive squamous cell carcinoma (SCC), and invasive SCC to demonstrate their key roles in tumor progression.

Methods

Eighty one CIS, 17 microinvasive, and 21 invasive SCC cases were immunostained with primary antibodies for Snail-1, EGFR, E-cadherin, and vimentin on paraffin-embedded tissue microarray blocks.

Results

EGFR and Snail-1 proteins were highly expressed but the levels were not significantly different between the three groups. However, loss of E-cadherin and acquisition of vimentin were proven to occur significantly higher in microinvasive and invasive SCC cases than in CIS.

Conclusions

E-cadherin and vimentin were found to be two useful indicators of EMT in evaluating stromal invasion of CIS. However, it was not demonstrated for Snail-1 and EGFR proteins to play any key role in the progression of cervix cancer.

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Case Report

Liquid-Based Cytology of Villoglandular Adenocarcinoma of the Cervix: A Report of 3 Cases: Younghwa Choi, Haeryoung Kim, Haiyoung Choi, Daehyun Hwang, Gheeyoung Choe, Jin-Haeng Chung, So Yeon Park, Hye Seung Lee, Jin Ho Paik, Hyo Jin Park; Korean J Pathol. 2012;46(2):215-220. Published online April 25, 2012; DOI: https://doi.org/10.4132/KoreanJPathol.2012.46.2.215

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Abstract PDF

Villoglandular adenocarcinoma (VGA) is a rare subtype of cervical adenocarcinoma with a more favorable prognosis compared to conventional adenocarcinomas. Although the tumors are usually recognized on colposcopic examination due to the mainly exophytic growth pattern, they may be underdiagnosed as benign lesions by cytology because of their minimal cytologic atypia. We report the liquid-based cytology (LBC) findings of three histologically confirmed VGAs which we have recently identified. They were characterized by hypercellular smears on low-power examination with smooth-bordered three-dimensional papillary fragments. The nuclei were relatively uniform with irregular nuclear membranes. Nucleoli were small but distinct and macronucleoli were also seen. The abnormal architectural patterns such as papillary structures and nuclear overlapping and nuclear hyperchromasia are important clues to the diagnosis of VGA. In addition, nuclear membrane irregularity and prominent nucleoli can be recognized on LBC specimens, further facilitating its diagnosis.

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Villoglandular adenocarcinoma of the uterine cervix: a systematic review and meta-analysis
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Original Articles

Prognostic Significance of Amplification of the c-MYC Gene in Surgically Treated Stage IB-IIB Cervical Cancer.: Tae Jung Kim, Ahwon Lee, Sung Jong Lee, Won Chul Lee, Yeong Jin Choi, Kyo Young Lee, Chang Suk Kang; Korean J Pathol. 2011;45(6):596-603.; DOI: https://doi.org/10.4132/KoreanJPathol.2011.45.6.596

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Abstract PDF

BACKGROUND
Mutations of c-MYC have been described in cervical cancer. However, association between c-MYC gene status and its prognostic significance have not been clarified.
METHODS
Tissue microarray sections from 144 patients with stage IB-IIB cervical cancer treated by radical hysterectomy were analyzed by fluorescence in situ hybridization using a region-specific probe for c-MYC and a centromere-specific probe for chromosome 8.
RESULTS
Seventy five percent (108/144) of c-MYC gain and 6.9% (10/144) of c-MYC gene amplification were observed. c-MYC gene alteration was more frequently observed in squamous cell carcinoma than adenocarcinoma or adenosquamous carcinoma and were associated with low Ki67 labeling index (p=0.013). c-MYC amplification was not associated with clinicopathologic parameters except absence of bcl2 expression (p=0.048). Survival analysis revealed that patients with c-MYC amplification were significantly associated with higher risk of disease recurrence (p=0.007) and cancer related death (p=0.020). However, c-MYC gain was not associated with unfavorable outcome. Multivariate analysis proved c-MYC amplification as independent prognostic factors of shorter disease free survival and cancer-related death (p=0.028 and p=0.025, respectively).
CONCLUSIONS
c-MYC amplification, not gain, is an independent prognostic marker for shorter disease free and cancer specific survival in cervical cancer treated by radical hysterectomy.

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A Rare Case of Cutaneous Plasmacytosis in a Korean Male
Corey Georgesen, Meenal Kheterpal, Melissa Pulitzer
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Human Papillomavirus Prevalence in Gangwon Province Using Reverse Blot Hybridization Assay.: Dongsup Lee, Sunghyun Kim, Sangjung Park, Hyunwoo Jin, Tae Ue Kim, Kwang Hwa Park, Hyeyoung Lee; Korean J Pathol. 2011;45(4):348-353.; DOI: https://doi.org/10.4132/KoreanJPathol.2011.45.4.348

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Abstract PDF

BACKGROUND
Human papillomavirus (HPV) plays an important role in the development of cervical carcinoma. Although there is a general agreement that high levels of HPV are related to cervical cancer, the prevalence and distribution of HPV genotypes seems to vary by geographical region. This study was designed to investigate the prevalence of HPV genotypes in Gangwon Province, Korea.
METHODS
In total, 342 samples were examined by Pap smear and HPV-ID(R) reverse blot hybridization assay (REBA) (M&D, Wonju, Korea).
RESULTS
Overall HPV positivity was 80.9% and 64.4% in women with abnormal and normal cytology by REBA, respectively. The five most common HPV types were: HPV 16, 53, 58, 56, and 33 in samples with abnormal cytology, and HPV 16, 53, 58, 70, and 18 in samples with normal cytology.
CONCLUSIONS
The REBA can provide useful data regarding prevalence of HPV genotypes. Gangwon Province showed high prevalence of HPV infection in women. The most common HPV type in Gangwon Province was HPV16, and HPV 53, 58, 56, 70 were frequently present.

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Geehyuk Kim, Sunghyun Kim, Sunyoung Park, Sangjung Park, Han Lin, Yubo Ren, Li Yingxue, In Soo Lee, Jae Dal Lee, Dongsup Lee
Korean Journal of Clinical Laboratory Science.2015; 47(4): 259. CrossRef
Comparison of Methods for Measuring Histamine by ELISA and HPLC-MS Assay In Vitro
In Hee Lee, Yoo Hyun Kim
Korean Journal of Clinical Laboratory Science.2015; 47(4): 306. CrossRef
Diagnostic Performance of HPV E6/E7 mRNA and HPV DNA Assays for the Detection and Screening of Oncogenic Human Papillomavirus Infection among Woman with Cervical Lesions in China
Hye-young Wang, Dongsup Lee, Sunyoung Park, Geehyuk Kim, Sunghyun Kim, Lin Han, Ren Yubo, Yingxue Li, Kwang Hwa Park, Hyeyoung Lee
Asian Pacific Journal of Cancer Prevention.2015; 16(17): 7633. CrossRef
Uncommon and Rare Human Papillomavirus Genotypes Relating to Cervical Carcinomas
Na Rae Kim, Myunghee Kang, Soon Pyo Lee, Hyunchul Kim, Jungsuk An, Dong Hae Chung, Seung Yeon Ha, Hyun Yee Cho
Korean Journal of Pathology.2014; 48(1): 43. CrossRef

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