Journal of Pathology and Translational Medicine

Original Articles

Interleukin-31, Interleukin-31RA, and OSMR Expression Levels in Post-burn Hypertrophic Scars: Mi Young Lee, Eun Shin, Hyunchul Kim, In Suk Kwak, Younghee Choi; J Pathol Transl Med. 2018;52(5):307-313. Published online August 16, 2018; DOI: https://doi.org/10.4132/jptm.2018.08.03

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Background
Although several studies have shown the role of interleukin-31 (IL-31) and its receptors in inducing pruritus in certain skin disorders, knowledge of its role in post-burn hypertrophic scars is insufficient. Therefore, the histopathological expression levels of IL-31, IL-31 receptor alpha (IL-31RA), and oncostatin M receptor (OSMR) in post-burn hypertrophic scar tissues were investigated and compared with normal tissue expression levels.
Methods
Samples of hypertrophic scar tissue were obtained from 20 burn patients through punch biopsy. Normal samples were obtained from areas adjacent to the burn injury site of the same patients. Samples were placed in 10% neutral buffered formalin, embedded in paraplast, and processed into serial 5-μm sections. Immunohistochemistry results were semi-quantitatively evaluated for IL-31, IL-31RA, and OSMR. By hematoxylin and eosin staining, epidermal and dermal thickness were assessed with a microscope and digital camera. Intensities were rated on a scale of 1 to 4.
Results
Percentages for IL-31, IL-31RA, and OSMR in the epidermal basal layer cell cytoplasm were significantly greater in the burn scar tissue compared to normal skin, as well as the dermal and epidermal thickness (p < .05). There was a significant difference in IL-31 epidermal basal layer intensity in burn scar tissue compared to normal skin (p < .05). Besides the OSMR basal layer intensity, IL-31 and IL-31RA intensities between the burn scar and normal tissues were not significant. However, correlations were significant, indicating that the greater the infiltration percentage, the higher the intensity (p < .05).
Conclusions
IL-31, IL-31RA, and OSMR expression levels are increased in hypertrophic scars compared with normal tissue.

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Understanding Neural Factors in Burn-related Pruritus and Neuropathic Pain
Dulan A Gunawardena, Edward Stanley, Andrea C Issler-Fisher
Journal of Burn Care & Research.2023; 44(5): 1182. CrossRef
Canine interleukin-31 binds directly to OSMRβ with higher binding affinity than to IL-31RA
Yuxin Zheng, Jing Zhang, Tianling Guo, Jin Cao, Lixian Wang, Jie Zhang, Xuefei Pang, Feng Gao, Hua Sun, Haixia Xiao
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Multimodal roles of transient receptor potential channel activation in inducing pathological tissue scarification
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Role of burn severity and posttraumatic stress symptoms in the co-occurrence of itch and neuropathic pain after burns: A longitudinal study
N. E. E. Van Loey, A. E. E. de Jong, H. W. C. Hofland, A. I. M. van Laarhoven
Frontiers in Medicine.2022;[Epub] CrossRef
Trial of Nemolizumab in Moderate-to-Severe Prurigo Nodularis
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New England Journal of Medicine.2020; 382(8): 706. CrossRef
Post-Burn Pruritus
Bo Young Chung, Han Bi Kim, Min Je Jung, Seok Young Kang, In-Suk Kwak, Chun Wook Park, Hye One Kim
International Journal of Molecular Sciences.2020; 21(11): 3880. CrossRef
Novel Analgesics with Peripheral Targets
Cosmin I. Ciotu, Michael J.M. Fischer
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Post-Burn Pruritus and Its Management—Current and New Avenues for Treatment
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Morphologic Analysis of Cytomegalovirus Infected Cells in Bronchial Washing Cytology: Comparison of Liquid-Based Preparation and Conventional Smear: Jae Yeon Seok, Jungsuk An, Seung Yeon Ha, Dong Hae Chung, Sangho Lee, Hyunchul Kim; J Pathol Transl Med. 2016;50(2):147-154. Published online February 15, 2016; DOI: https://doi.org/10.4132/jptm.2015.12.25

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Abstract PDF

Background
The cytopathic effects of cytomegalovirus (CMV) infection have been well described since the virus was first reported; however, the morphology of CMV infection has not been clearly studied. We examined the difference in detailed cytologic findings in bronchial washing cytology between liquid-based and conventionally prepared smears. Methods: Bronchial washing cytology was processed using either the conventional preparation (CP) or liquid-based preparation (LBP). Sixty-nine cells with typical cytopathic effects of CMV infection were detected on CP slides and 18 cells on LBP slides. Using the image analyzer, area, circumference, major axis, and minor axis of the cytoplasm, nucleus, and intranuclear inclusion were measured in singly scattered CMV-infected cells, and histiocytes were used as a control. Results: The mean cytoplasmic area of CMV-infected cells was 1.47 times larger than that of histiocytes in CP and 2.92 times larger in LBP (p<.05). The mean nuclear area of CMV-infected cells was 2.61 times larger than that of histiocytes in CP and 4.25 times larger in LBP (p<.05). The nucleus to cytoplasm ratio and intranuclear inclusion to cytoplasm ratio of the mean area, circumference, major axis, and minor axis in CP were larger than those in LBP (p<.05). Conclusions: The sizes of cytoplasm, nucleus, and intranuclear inclusion were larger in LBP than in CP, indicating that CMV-infected cells are easily detectable in LBP. However, the nucleus-to-cytoplasm ratio was larger in CP, suggesting that differentiation from malignancy or regenerative atypia requires caution in CP.

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Brief Case Reports

Carney Complex with Multiple Cardiac Myxomas, Pigmented Nodular Adrenocortical Hyperplasia, Epithelioid Blue Nevus, and Multiple Calcified Lesions of the Testis: A Case Report: Hyunchul Kim, Hyun-Yee Cho, Jeong Nam Lee, Kook-Yang Park; J Pathol Transl Med. 2016;50(4):312-314. Published online February 4, 2016; DOI: https://doi.org/10.4132/jptm.2015.11.12

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Mesonephric (Wolffian) Pseudoendometrioid Carcinoma of the Broad Ligament, Arising From a Papillary Cystadenoma
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Bilateral Stafne Bone Cavity in the Anterior Mandible with Heterotopic Salivary Gland Tissue: A Case Report: Hyunchul Kim, Jae Yeon Seok, Sangho Lee, Jungsuk An, Na Rae Kim, Dong Hae Chung, Hyun Yee Cho, Seung Yeon Ha; Korean J Pathol. 2014;48(3):248-249. Published online June 26, 2014; DOI: https://doi.org/10.4132/KoreanJPathol.2014.48.3.248

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Original Articles

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 J Pathol. 2014;48(1):43-49. Published online February 25, 2014; DOI: https://doi.org/10.4132/KoreanJPathol.2014.48.1.43

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Abstract PDF

Background

Human papillomavirus (HPV) is an oncogenic virus in cervical cancer and most invasive carcinomas (ICs) are caused by HPV16 and 18. However, the roles and contributions of other uncommon and rare genotypes remain uncertain.

Methods

HPV genotypes were retrospectively assessed using an HPV DNA chip that can specify up to 32 HPV genotypes. We arbitrarily regarded genotypes accounting for less than 6% of the total as uncommon and rare genotypes.

Results

A total of 3,164 HPV-positive cases were enrolled. In groups 2A, 2B, 3, and unclassified HPV genotypes, 2.4% of cases with uncommon HPV genotypes (68, 26, 34, 53, 66, 69, 70, 73, 40, 42, 43, 44, 54, 55, 61, 62, 6, and 11) showed high grade squamous intraepithelial lesions and ICs. There were no HPV32- and 57-infected cases.

Conclusions

We found that the uncommon and rare HPV genotypes may provide incremental etiologic contributions in cervical carcinogenesis, especially HPV68, 70, and 53. Further studies on these uncommon and rare HPV genotypes will be of importance in establishing the significance of genotypes in different regions, especially in planning a strategy for further vaccine development as well as follow-up on the effectiveness of the currently used vaccines.

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Clinicopathological Analysis of Hepatocellular Adenoma According to New Bordeaux Classification: Report of Eight Korean Cases: Hyunchul Kim, Ja-June Jang, Dong-Sik Kim, Beom Woo Yeom, Nam Hee Won; Korean J Pathol. 2013;47(5):411-417. Published online October 25, 2013; DOI: https://doi.org/10.4132/KoreanJPathol.2013.47.5.411

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Abstract PDF

Background

Hepatocellular adenoma (HCA) is a rare benign tumor of the liver. A subtype classification of HCA (hepatocyte nuclear factor 1α [HNF1α]-mutated, β-catenin-mutated HCA, inflammatory HCA, and unclassified HCA) has recently been established based on a single institutional review of a HCA series by the Bordeaux group.

Methods

We used histologic and immunohistochemical parameters to classify and evaluate eight cases from our institution. We evaluated the new classification method and analyzed correlations between our results and those of other reports.

Results

Seven of our eight cases showed histologic and immunohistochemical results consistent with previous reports. However, one case showed overlapping histologic features, as previously described by the Bordeaux group. Four cases showed glutamine synthetase immunohistochemical staining inconsistent with their classification, indicating that glutamine synthetase staining may not be diagnostic for β-catenin-mutated HCA. HNF1α-mutated HCA may be indicated by the absence of liver fatty acid binding protein expression. Detection of amyloid A may indicate inflammatory HCA. HCA with no mutation in the HNF1α or β-catenin genes and no inflammatory protein expression is categorized as unclassified HCA.

Conclusions

Although the new classification is now generally accepted, validation through follow-up studies is necessary.

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Case Study

Myxoid Liposarcoma with Cartilaginous Differentiation: A Case Study with Cytogenetical Analysis: Hyunchul Kim, Won Hwangbo, Sangjeong Ahn, Suhjin Kim, Insun Kim, Chul Hwan Kim; Korean J Pathol. 2013;47(3):284-288. Published online June 25, 2013; DOI: https://doi.org/10.4132/KoreanJPathol.2013.47.3.284

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Abstract PDF

Myxoid liposarcoma is a subtype of liposarcoma. This specific subtype can be identified based on its characteristic histological and cytogenetical features. The tumor has a fusion transcript of the CHOP and TLS genes, which is caused by t(12;16)(q13;p11). Most of the fusion transcripts that have been identified fall into three categories, specifically type I (exons 7-2), type II (exons 5-2), and type III (exons 8-2). A total of seven myxoid liposarcomas associated with the rare phenomenon of cartilaginous differentiation have been documented in the literature. Currently, only one of these cases has been cytogenetically analyzed, and the analysis indicated that it was a type II TLS-CHOP fusion transcript in both the typical myxoid liposarcoma and cartilaginous areas. This study presents a second report of myxoid liposarcoma with cartilaginous differentiation, and includes a cytogenetical analysis of both the myxoid and cartilaginous areas.

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Original Articles

Naked Cuticle Drosophila 1 Expression in Histologic Subtypes of Small Adenocarcinoma of the Lung: Sangjeong Ahn, Won Hwangbo, Hyunchul Kim, Chul Hwan Kim; Korean J Pathol. 2013;47(3):211-218. Published online June 25, 2013; DOI: https://doi.org/10.4132/KoreanJPathol.2013.47.3.211

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Abstract PDF

Background

Naked cuticle Drosophila 1 (NKD1) has been related to non-small cell lung cancer in that decreased NKD1 levels have been associated with both poor prognosis and increased invasive quality.

Methods

Forty cases of lung adenocarcinoma staged as Tis or T1a were selected. Cases were subclassified into adenocarcinoma in situ (AIS), minimally invasive adenocarcinoma (MIA), and small adenocarcinoma (SAD). Immunohistochemical studies for NKD1 were performed.

Results

Forty samples comprised five cases of AIS (12.5%), eight of MIA (20.0%), and 27 of SAD (67.5%). AIS and MIA showed no lymph node metastasis and 100% disease-free survival, whereas among 27 patients with SAD, 2 (7.4%) had lymph node metastasis, and 3 (11.1%) died from the disease. Among the 40 cases, NKD1-reduced expression was detected in 8 (20%) samples, whereas normal expression was found in 15 (37.5%) and overexpression in 17 (42.5%). Loss of NKD1 expression was significantly associated with lymph node metastasis (p=0.001). All cases with predominant papillary pattern showed overexpression of NKD1 (p=0.026).

Conclusions

Among MIA and SAD, MIA had better outcomes than SAD. Down-regulated NKD1 expression was closely associated with nodal metastasis, and overexpression was associated with papillary predominant adenocarcinoma.

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Jie Li, Sheng Zhang, Qing Hu, Kang Zhang, Jianbin Jin, Xuqing Zheng, Zhenyu Yin, Xiaomin Wang
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The Utility of p16INK4a and Ki-67 as a Conjunctive Tool in Uterine Cervical Lesions: Sangho Lee, Hyunchul Kim, Hyesun Kim, Chulhwan Kim, Insun Kim; Korean J Pathol. 2012;46(3):253-260. Published online June 22, 2012; DOI: https://doi.org/10.4132/KoreanJPathol.2012.46.3.253

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Abstract PDF

Background

Immunohistochemical staining for p16INK4a and Ki-67 has been used to improve the accuracy in making a diagnosis of the uterine cervix cancer on biopsy. This study was conducted to examine the usefulness of these markers in the pathological diagnosis based on cervical biopsy.

Methods

We selected a consecutive series of 111 colposcopically directed cervical punch biopsies. Using these biopsy samples, we performed an immunohistochemical staining for p16INK4a and Ki-67 to establish a diagnosis. The slides were circulated among four pathologists in a sequential order: the hematoxylin and eosin (H&E) slide, H&E slide and p16INK4a-stained slide, and H&E slide, p16INK4a- and Ki-67-stained slides.

Results

The overall rates of the concordance in the first, the second, and the third diagnoses were 77.5%, 82.0%, and 82.0%, respectively. The rate of the concordance in the diagnosis of cervical intraepithelial neoplasm (CIN) 2/3 was increased from 62.2% to 73.0%. But there was a variability in the rate of the revision of the diagnosis between the pathologists. With the application of criteria for interpreting the expressions of p16INK4a and Ki-67, benign and CIN 1 lesions showed a p16INK4a expression score of 0 or 1. But CIN 2 and CIN 3 lesions showed a p16INK4a expression score of 2 and 3, respectively.

Conclusions

The immunostain for p16INK4a and Ki-67 might be useful in reducing an inter-observer variability. But criteria for interpreting both markers should be strictly applied.

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Possible role of negative human papillomavirus E6/E7 mRNA as a predictor of regression of cervical intraepithelial neoplasia 2 lesions in hr-HPV positive women
Maria Teresa Bruno, Nazario Cassaro, Salvatore Giovanni Vitale, Arianna Guaita, Sara Boemi
Virology Journal.2022;[Epub] CrossRef
Evaluation of p16, human papillomavirus capsid protein L1 and Ki-67 in cervical intraepithelial lesions: Potential utility in diagnosis and prognosis
Hanan AlSaeid Alshenawy
Pathology - Research and Practice.2014; 210(12): 916. CrossRef
Distribution of Human Papillomavirus 52 and 58 Genotypes, and Their Expression of p16 and p53 in Cervical Neoplasia
Tae Eun Kim, Hwal Woong Kim, Kyung Eun Lee
Korean Journal of Pathology.2014; 48(1): 24. CrossRef
Detection and pathological value of papillomavirus DNA and p16INK4A and p53 protein expression in cervical intraepithelial neoplasia
JINGBO WU, XIAO-JING LI, WEI ZHU, XIU-PING LIU
Oncology Letters.2014; 7(3): 738. CrossRef
p16INK4a Immunohistochemistry in Cervical Biopsy Specimens
Miriam Reuschenbach, Nicolas Wentzensen, Maaike G. Dijkstra, Magnus von Knebel Doeberitz, Marc Arbyn
American Journal of Clinical Pathology.2014; 142(6): 767. CrossRef

Case Report

Hepatoid Thymic Carcinoma: A Case Report.: Jeong Hyeon Lee, Hyunchul Kim, Yang Seok Chae, Nam Hee Won, Jong Sang Choi, Chul Hwan Kim; Korean J Pathol. 2009;43(6):562-565.; DOI: https://doi.org/10.4132/KoreanJPathol.2009.43.6.562

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Abstract PDF

We report here on a rare case of hepatoid thymic carcinoma in a 34-year-old man. The patient complained of a high fever and headache, and a 6.6cm-sized anterior mediastinal mass was found on chest computed tomography (CT). There was no hepatic mass seen on abdominal CT. The resected mass consisted of epithelioid cells with abundant eosinophilic cytoplasm, pleomorphic vesicular nuclei and prominent nucleoli, and the mass was surrounded by thymic tissue. The tumor cells were immunopositive for cytokeratin 7, alpha-1-antitrypsin, hepatocyte staining, and epithelial membrane antigen, but they were negative for CD5, alpha-fetoprotein (AFP) and placental alkaline phosphatase, and this all led to a diagnosis of hepatoid thymic carcinoma rather than hepatoid yolk sac tumor. This entity should be included in the differential diagnosis of epithelioid thymic tumors.

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Hepatoid thymic carcinoma in a polycythemia vera patient treated with ropeginterferon Alfa-2b: Clinical, histopathological and molecular correlates
Giuseppe G. Loscocco, Margherita Vannucchi, Raffaella Santi, Andrea Amorosi, Stefania Scarpino, Maria Chiara Siciliano, Paola Guglielmelli, Claudio Tripodo, Arianna Di Napoli, Alessandro M. Vannucchi
Pathology - Research and Practice.2024; 263: 155648. CrossRef

Original Article

Detecting Malignant Urothelial Cells by Morphometric Analysis of ThinPrep(R) Liquid-based Urine Cytology Specimens.: Bong Kyung Shin, Young Suk Lee, Hoiseon Jeong, Sang Ho Lee, Hyunchul Kim, Aree Kim, Insun Kim, Han Kyeom Kim; Korean J Cytopathol. 2008;19(2):136-143.; DOI: https://doi.org/10.3338/kjc.2008.19.2.136

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Abstract PDF

Urothelial carcinoma accounts for 90% of all the cases of bladder cancer. Although many cases can be easily managed by local excision, urothelial carcinoma rather frequently recurs, tends to progress to muscle invasion, and requires regular follow-ups. Urine cytology is a main approach for the follow-up of bladder tumors. It is noninvasive, but it has low sensitivity of around 50% with using the conventional cytospin preparation. Liquid-based cytology (LBC) has been developed as a replacement for the conventional technique. We compared the cytomorphometric parameters of ThinPrep(R) and cytospin preparation urine cytology to see whether there are definite differences between the two methods and which technique allows malignant cells to be more effectively discriminated from benign cells. The nuclear-to-cytoplasmic ratio value, as measured by digital image analysis, was efficient for differentiating malignant and benign urothelial cells, and this was irrespective of the preparation method and the tumor grade. Neither the ThinPrep(R) nor the conventional preparation cytology was definitely superior for distinguishing malignant cells from benign cells by cytomorphometric analysis of the adequately preserved cells. However, the ThinPrep(R) preparation showed significant advantages when considering the better preservation and cellularity with a clear background.

Citations

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Utility of Image Morphometry in the Atypical Urothelial Cells and High-Grade Urothelial Carcinoma Categories of the Paris System for Reporting Urinary Cytology
K.C. Sharan, Manish Rohilla, Pranab Dey, Radhika Srinivasan, Nandita Kakkar, Ravimohan S. Mavuduru
Journal of Cytology.2024; 41(3): 137. CrossRef
Comparison of diagnostic accuracy between CellprepPlus® and ThinPrep® liquid‐based preparations in effusion cytology
Yong‐Moon Lee, Ji‐Yong Hwang, Seung‐Myoung Son, Song‐Yi Choi, Ho‐Chang Lee, Eun‐Joong Kim, Hye‐Suk Han, Jin young An, Joung‐Ho Han, Ok‐Jun Lee
Diagnostic Cytopathology.2014; 42(5): 384. CrossRef
A Comparison Between ThinPrep Monolayer and Cytospin Cytology for the Detection of Bladder Cancer
Ji Yong Kim, Hyung Jin Kim
Korean Journal of Urology.2014; 55(6): 390. CrossRef
Cytological and Morphometric Study of Urinary Epithelial Cells with Histopathological Correlation
Asim Kumar Manna, Manisha Sarkar, Ujjal Bandyopadhyay, Srabani Chakrabarti, Swapan Pathak, Diptendra Kumar Sarkar
Indian Journal of Surgery.2014; 76(1): 26. CrossRef
Evaluation of Urine Cytology in Urothelial Carcinoma Patients: A Comparison of CellprepPlus® Liquid-Based Cytology and Conventional Smear
Seung-Myoung Son, Ji Hae Koo, Song-Yi Choi, Ho-Chang Lee, Yong-Moon Lee, Hyung Geun Song, Hae-Kyung Hwang, Hye-Suk Han, Seok-Joong Yun, Wun-Jae Kim, Eun-Joong Kim, Ok-Jun Lee
Korean Journal of Pathology.2012; 46(1): 68. CrossRef

Case Reports

Adenomyoma of Endocervical Type in a First-Trimester Gravid Uterine Corpus: A Brief Report.: Hyunchul Kim, Hoiseon Jeong, Sangho Lee, Young Seok Lee, Bong Kyung Shin, Insun Kim; Korean J Pathol. 2008;42(2):123-124.

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Abstract PDF: Uterine adenomyoma is a neoplasm that is composed of endometrial glands and smooth muscle, and this is found in the uterine corpus; however, the glandular component is occasionally of mucin-secreting endocervical type. We describe here a case of uterine adenomyoma of the endocervical type, and this presented in a 38-year-old pregnant woman.

Sclerosing Mucoepidermoid Carcinoma of the Parotid Gland: A Case Report.: Hyunchul Kim, Ju Han Lee, Eung Seok Lee, Soon Young Kwon, Taik Kun Kim, Young Sik Kim; Korean J Pathol. 2007;41(3):193-197.

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Abstract PDF: Sclerosing mucoepidermoid carcinoma (SMEC) is a very rare tumor of the salivary gland. There have been eight cases of SMEC reported in the medical literature; this is the first reported case in Korea. A 51-year-old woman presented with a right infra-auricular mass that she had for 3 years. We performed superficial parotidectomy. Grossly, the resected parotid gland showed a well-circumscribed firm mass. Histologically, the tumor consisted of central solid or ductal tumor nests within a dense fibrous stroma surrounded by peripheral lymphoid infiltration. The tumor nests were composed of squamous, intermediate and mucin-secreting cells. However, the tumor cells lacked mitosis and nuclear anaplasia. The lymphoid cells were mostly composed of lymphocytes and plasma cells with occasional eosinophils and neutrophils. Immunohistochemically, the tumor cells were positive for high- and low- molecular weight cytokeratins, cytokeratin 7, p16INK4A, Bcl-2 and cyclin D1. The patient also underwent radiation therapy. We report here on a case of SMEC of the parotid gland along with the immunohistochemical characteristics, and we review the relevant literature.

Original Article

The Clinicopathological Characteristics of Gastrointestinal Neuroendocrine Tumors; An Analysis of 65 Cases.: Hyunjoo Lee, Jungwoo Choi, Jung Suk An, Hyunchul Kim, Bong Kyung Shin, Aeree Kim, Hankyeom Kim, Insun Kim; Korean J Pathol. 2007;41(3):149-157.

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Abstract PDF: Background
: This study was designed to investigate gastrointestinal neuroendocrine tumors with an emphasis on their clinicopathological characteristics.
Methods
: Sixty-five cases were reviewed and classified as typical carcinoid (TC), atypical carcinoid (AC), large cell neuroendocrine carcinoma (LCNEC) and small cell carcinoma (SmCC). We performed immunohistochemistry to characterize the expression of the immunoreactivity for synaptophysin, chromogranin, gastrin, somatostatin, thyroid transcription factor-1, p53 and Ki-67.
Results
: Most commonly, the tumors were located in the rectum (54%), followed by the stomach (23%) and colon (9%). Histologically, the tumors were classified as 49 TCs, 4 ACs, 6 LCNECs and 6 SmCCs. Most tumors were stained positive for synaptophysin and/or chromogranin. Four LCNECs and one SmCC were p53-positive. The carcinoids revealed a low level (<5%) of reactivity for Ki-67, while > or =30% of the cells showed reactivity for Ki-67 in the majority of LCNECs and SmCCs. Six patients with metastatic carcinoids were older than those patients without metastasis (64 vs 48 years, respectively, p=0.004). Furthermore, the size of tumors was larger for the patients with metastatic carcinoids than for the patients with nonmetastatic carcinoids (2.3 vs 0.5 cm, respectively, p=0.005).
Conclusion
: Old age, large tumor size and muscle invasion are associated with high grade neuroendocrine tumor and lymph node metastasis for those patients with carcinoids.

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