Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery

VESCIO, Francesca; AMMERATA, Giorgio; RANIERI, Girolamo; CURCIO, Silvia; AMMENDOLA, Michele; LUPOSELLA, Maria; PATRUNO, Rosa; ZUCCALA, Valeria; LAFACE, Carmelo; MEMEO, Riccardo; NAVARRA, Giuseppe; CURRO, Giuseppe

doi:10.14744/ejmo.2023.53961

Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery

Michele AMMENDOLA, (Department Health of Science, Digestive Surgery Unit, University “Magna Graecia” Medical School, Viale Europa, Germaneto, Catanzaro, Italy)

Francesca VESCIO, (Department Health of Science, Digestive Surgery Unit, University “Magna Graecia” Medical School, Viale Europa, Germaneto, Catanzaro, Italy)

Giorgio AMMERATA, (Department Health of Science, Digestive Surgery Unit, University “Magna Graecia” Medical School, Viale Europa, Germaneto, Catanzaro, Italy)

Maria LUPOSELLA, (Cardiovascular Disease Unit, General Hospital of Soverato, Catanzaro, Itlay)

Rosa PATRUNO, (Chair of Pathology, Veterinary Medical School, University “Aldo Moro” of Bari, Via Casamassima, Bari, Italy)

Carmelo LAFACE, (Interventional Oncology Unit with Integrated Section of Translational Medical Oncology National Cancer Research Centre, Istituto Tumori “Giovanni Paolo II”, viale Orazio Flacco 65, Bari, Italy)

Valeria ZUCCALA, (Pathology Unit, “Pugliese-Ciaccio” Hospital, Viale Pio X°, Catanzaro, Italy)

Silvia CURCIO, (Department Health of Science, Digestive Surgery Unit, University “Magna Graecia” Medical School, Viale Europa, Germaneto, Catanzaro, Italy)

Riccardo MEMEO, (Hepato-Pancreato-Biliary Surgery Unit, Miulli Hospital, Acquaviva delle Fonti, Bari, Italy)

Giuseppe NAVARRA, (Department of Human Pathology of Adult and Evolutive Age, General Surgery Unit, University of Messina, Messina, Italy)

Giuseppe CURRO, (Department Health of Science, General Surgery Unit, University “Magna Graecia” Medical School, Viale Europa, Germaneto, Catanzaro)

Girolamo RANIERI, (Interventional Oncology Unit with Integrated Section of Translational Medical Oncology National Cancer Research Centre, Istituto Tumori “Giovanni Paolo II”, viale Orazio Flacco 65, Bari, Italy)

Diğer Yazarlar

Eurasian Journal of Medicine and Oncology

3 0

Yıl: 2023 Cilt: 7 Sayı: 1 Sayfa Aralığı: 62 - 69 Metin Dili: İngilizce DOI: 10.14744/ejmo.2023.53961 İndeks Tarihi: 05-05-2023

Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery

Öz:

Objectives: Tumor proliferation is guided by neoangiogenesis; microvascular density (MVD) in the tumor micro-environment increases with the action of different immune system stromal cells such as the mast cells (MCs). Methods: We evaluated Ki-67 proliferation rate, MCs positive to tryptase (MCPT), and MVD in a series of 85 gastric cancer (GC) tissue samples from patients undergoing radical surgery. Results: In tumor tissue, a significant correlation between Ki-67 expression, MCPT, and MVD was found through Pearson t-test analysis (p ranged from 0.01 to 0.03). Conclusion: Ki-67 expression and MVD may indicate the survival prognosis of patients and MCPT could repre-sent a biological marker of radical surgery and angiogenesis. Furthermore, MCPT could be consid-ered as a target of novel anti-angiogenic therapies in GC patients.

Anahtar Kelime:

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık

1. Thrift AP, Nguyen TH. Gastric cancer epidemiology. Gastrointest Endosc Clin N Am 2021;31:425–39.
2. Liu X, Qiu H, Liu J, Chen S, Xu D, Li W, et al. Combined preoperative concentrations of CEA, CA 19–9, and 72–4 for predicting outcomes in patients with gastric cancer after curative resection. Oncotarget 2016;7:35446–53.
3. Aponte-López A, Muñoz-Cruz S. Mast cells in the tumor microenvironment. Adv Exp Med Biol 2020;1273:159–73.
4. De Nola R, Menga A, Castegna A, Loizzi V, Ranieri G, Cicinelli E, et al. The crowded crosstalk between cancer cells and stromal microenvironment in gynecological malignancies: biological pathways and therapeutic implication. Int J Mol Sci 2019;20:2401.
5. Patruno R, Passantino G, Laface C, Tinelli A, Zito A, Ruggieri R, et al. Microvascular density, endothelial area, and Ki-67 proliferative index correlate each other in cat post-injection fibrosarcoma. Cells 2020;10:31.
6. Pappa CA, Tsirakis G, Stavroulaki E, Kokonozaki M, Xekalou A, Konsolas I, et al. Mast cells influence the proliferation rate of myeloma plasma cells. Cancer Invest 2015;33:137–41.
7. Vasconcelos RAT, Guimarães Coscarelli P, Vieira TM, Noguera WS, Rapozo DCM, Acioly MA. Prognostic significance of mast cell and microvascular densities in malignant peripheral nerve sheath tumor with and without neurofibromatosis type 1. Cancer Med 2019;8:972–81.
8. Tamma R, Ingravallo G, Annese T, DE Giorgis M, DI Giovanni F, Gaudio F, et al. tumor cell microenvironment and microvessel density analysis in MALT type lymphoma. Anticancer Res 2021;41:1291–7.
9. Ammendola M, Sacco R, Marech I, Sammarco G, Zuccalà V, Luposella M, et al. Microvascular density and endothelial area correlate with Ki-67 proliferative index in surgically-treated pancreatic ductal adenocarcinoma patients. Oncol Lett 2015;10:967–71.
10. Xiong DD, Zeng CM, Jiang L, Luo DZ, Chen G. Ki-67/MKI67 as a predictive biomarker for clinical outcome in gastric cancer patients: an updated meta-analysis and systematic review involving 53 studies and 7078 patients. J Cancer 2019;29;10:5339–54.
11. Bullwinkel J, Baron-Luhr B, Ludemann A, Wohlenberg C, Gerdes J, Scholzen T. Ki-67 protein is associated with ribosomal RNA transcrip¬tion in quiescent and proliferating cells. J Cell Physiol 2006;206:624–35.
12. Schonk DM, Kuijpers HJ, van Drunen E, van Dalen CH, Geurts van Kessel AH, Verheijen R, et al. Assignment of the gene(s) involved in the expression of the proliferation-related Ki-67 antigen to human chromosome 10. Hum Genet 1989;83:297–9.
13. Rahmanzadeh R, Huttmann G, Gerdes J, Scholzen T. Chromophore- assisted light inactivation of pKi-67 leads to inhibition of ribosomal RNA synthesis. Cell Prolif 2007;40:422–30.
14. Bhattacharyya SP, Drucker I, Reshef T, Kirshenbaum AS, Metcalfe DD, Mekori YA. Activated T lymphocytes induce degranulation and cytokine production by human mast cells following cell-to-cell contact. J Leukoc Biol 1998;63:337–41.
15. Marech I, Ammendola M, Sacco R, Sammarco G, Zuccalà V, Zizzo N, et al. Tumour-associated macrophages correlate with microvascular bed extension in colorectal cancer patients. J Cell Mol Med 2016;20:1373–80.
16. Patruno R, Marech I, Zizzo N, Ammendola M, Nardulli P, Gadaleta C, et al. c-Kit expression, angiogenesis, and grading in canine mast cell tumour: a unique model to study c-Kit driven human malignancies. Biomed Res Int 2014;2014:730246.
17. Wasiuk A, de Vries VC, Hartmann K, Roers A, Noelle RJ. Mast cells as regulators of adaptive immunity to tumours. Clin Exp Immunol 2009;155:140–6.
18. Norrby K. Mast cells and angiogenesis. APMIS 2002;110:355– 71.
19. Ribatti D, Ranieri G. Tryptase, a novel angiogenic factor stored in mast cell granules. Exp Cell Res 2015;332:157–62.
20. Liu Y, Mueller BM. Protease-activated receptor-2 regulates vascular endothelial growth factor expression in MDA-MB-231 cells via MAPK pathways. Biochem Biophys Res Commun 2006;344:1263–70.
21. de Souza Junior DA, Santana AC, da Silva EZ, Oliver C, Jamur MC. The role of mast cell specific chymases and tryptases in tumor angiogenesis. Biomed Res Int 2015;2015:142359.
22. Chen X, Song E. Turning foes to friends: targeting cancer-associated fibroblasts. Nat Rev Drug Discov 2019;18:99–115.
23. Wang H, Guo W, Hu Y, Mou T, Zhao L, Chen H, et al. Superiority of the 8th edition of the TNM staging system for predicting overall survival in gastric cancer: Comparative analysis of the 7th and 8th editions in a monoinstitutional cohort. Mol Clin Oncol 2018;9:423–31
24. Liu X, Cai H, Shi Y, Wang Y. Prognostic factors in patients with node-negative gastric cancer: a single center experience from China. J Gastrointest Surg 2012;16:1123–7.
25. Sjo OH, Merok MA, Svindland A, Nesbakken A. Prognostic impact of lymph node harvest and lymph node ratio in patients with colon cancer. Dis Colon Rectum 2012;55:307–15.
26. Tamura S, Takeno A, Miki H. Lymph node dissection in curative gastrectomy for advanced gastric cancer. Int J Surg Oncol 2011;2011:748745
27. Ranieri G, Grammatica L, Patruno R, Zito AF, Valerio P, Iacobellis S, et al. A possible role of thymidine phosphorylase expression and 5-fluorouracil increased sensitivity in oropharyngeal cancer patients. J Cell Mol Med 2007;11:362–8.
28. Matsuda T, Saika K. The 5-year relative survival rate of stomach cancer in the USA, Europe and Japan. Jpn J Clin Oncol 2013;43:1157–8.
29. Tsamandas AC, Kardamakis D, Tsiamalos P, Liava A, Tzelepi V, Vassiliou V, et al. The potential role of Bcl-2 expression, apoptosis and cell proliferation (Ki-67 expression) in cases of gastric carcinoma and correlation with classic prognostic factors and patient outcome. Anticancer Res 2009;29:703–9.
30. Li YZ, Zhao P. Expressions of cyclinB1, FHIT and Ki-67 in 336 gastric carcinoma patients and their clinicopathologic significance. [Article in Chinese]. Zhonghua Yi Xue Za Zhi 2009;89:2337–41.
31. Wen Y, Wang Q, Zhou C, Yan D, Qiu G, Yang C, et al. Decreased expression of RASSF6 is a novel independent prognostic marker of a worse outcome in gastric cancer patients after curative surgery. Ann Surg Oncol 2011;18:3858–67
32. He WL, Li YH, Yang DJ, Song W, Chen XL, Liu FK, et al. Combined evaluation of centromere protein H and Ki-67 as prognostic biomarker for patients with gastric carcinoma. Eur J Surg Oncol 2013;39:141–9.
33. Liu M, Li JS, Tian DP, Huang B, Rosqvist S, Su M. MCM2 expression levels predict diagnosis and prognosis in gastric cardiac cancer. Histol Histopathol 2013;28:481–92.
34. Huang G, Chen S, Wang D, Wang R, Lin L, Chen S, et al. High ki67 expression has prognostic value in surgically-resected T3 gastric adenocarcinoma. Clin Lab 2016;62:141–53.
35. Liu G, Xiong D, Zeng J, Chen B, Huang Z. Clinicopathological and prognostic significance of Ki-67 immunohistochemical expression in gastric cancer: a systematic review and metaanalysis. Onco Targets Ther 2017;10:4321–8.
36. Wang X, Chen X, Fang J, Yang C. Overexpression of both VEGFA and VEGF-C in gastric cancer correlates with prognosis, and silencing of both is effective to inhibit cancer growth. Int J Clin Exp Pathol 2013;6:586–97.
37. Sunderkötter C, Steinbrink K, Goebeler M, Bhardwaj R, Sorg C. Macrophages and angiogenesis. J Leukoc Biol 1994;55:410– 22.
38. Khazaie K, Blatner NR, Khan MW, Gounari F, Gounaris E, Dennis K, et al. The significant role of mast cells in cancer. Cancer Metastasis Rev 2011;30:45–60.
39. Folkman J. The role of angiogenesis in tumor growth. Semin Cancer Biol 1992;3:65–71.
40. Tanaka T, Ishikawa H. Mast cells and inflammation-associated colorectal carcinogenesis. Semin Immunopathol 2013;35:245–54.
41. Ribatti D, Ranieri G, Basile A, Azzariti A, Paradiso A, Vacca A. Tumor endothelial markers as a target in cancer. Expert Opin Ther Targets 2012;16:1215–25.
42. Zhao Y, Wu K, Cai K, Zhai R, Tao K, Wang G, et la. Increased numbers of gastric-infiltrating mast cells and regulatory T cells are associated with tumor stage in gastric adenocarcinoma patients. Oncol Lett 2012;4:755–8.
43. Melillo RM, Guarino V, Avilla E, Galdiero MR, Liotti F, Prevete N, et al. Mast cells have a protumorigenic role in human thyroid cancer. Oncogene 2010;29:6203–15.
44. Huang B, Lei Z, Zhang GM, Li D, Song C, Li B, et al. SCF-mediated mast cell infiltration and activation exacerbate the inflammation and immunosuppression in tumor microenvironment. Blood 2008;112:1269–79
45. Detoraki A, Staiano RI, Granata F, Giannattasio G, Prevete N, de Paulis A, et al. Vascular endothelial growth factors synthesized by human lung mast cells exert angiogenic effects. J Allergy Clin Immunol 2009;123:1142–9.
46. Ammendola M, Sacco R, Sammarco G, Donato G, Zuccalà V, Romano R, et al. Mast cells positive to tryptase and c-kit receptor expressing cells correlates with angiogenesis in gastric cancer patients surgically treated. Gastroenterol Res Pract 2013;2013:703163.
47. Marone G, Varricchi G, Loffredo S, Granata F. Mast cells and basophils in inflammatory and tumor angiogenesis and lymphangiogenesis. Eur J Pharmacol 2016;778:146–51.
48. Zhang X, Wang W, Mize GJ, Takayama TK, True LD, Vessella RL. Protease-activated receptor 2 signaling upregulates angiogenic growth factors in renal cell carcinoma. Exp Mol Pathol 2013;94:91–7.
49. Rasmussen JG, Riis SE, Frøbert O, Yang S, Kastrup J, Zachar V, et al. Activation of protease-activated receptor 2 induces VEGF independently of HIF-1. PLoS One 2012;7:e46087.
50. Chang LH, Pan SL, Lai CY, Tsai AC, Teng CM. Activated PAR-2 regulates pancreatic cancer progression through ILK/HIF-α- induced TGF-α expression and MEK/VEGF-A-mediated angiogenesis. Am J Pathol 2013;183:566–75.
51. Ammendola M, Sacco R, Sammarco G, Piardi T, Zuccalà V, Patruno R, et al. Mast cells positive to tryptase, endothelial cells positive to protease-activated receptor-2, and microvascular density correlate among themselves in hepatocellular carcinoma patients who have undergone surgery. Onco Targets Ther 2016;9:4465–71.
52. Yano H, Kinuta M, Tateishi H, Nakano Y, Matsui S, Monden T, et al. Mast cell infiltration around gastric cancer cells correlates with tumor angiogenesis and metastasis. Gastric Cancer 1999;2:26–32.
53. Ammendola M, Sacco R, Sammarco G, Luposella M, Patruno R, Gadaleta CD, et al. Mast cell-targeted strategies in cancer therapy. Transfus Med Hemother 2016;43:109–13.
54. Marech I, Ammendola M, Sacco R, Capriuolo GS, Patruno R, Rubini R, et al. Serum tryptase, mast cells positive to tryptase and microvascular density evaluation in early breast cancer patients: possible translational significance. BMC Cancer 2014;14:534
55. Marech I, Ammendola M, Gadaleta C, Zizzo N, Oakley C, Gadaleta CD, et al. Possible biological and translational significance of mast cells density in colorectal cancer. World J Gastroenterol 2014;20:8910–20.
56. Ammendola M, Sacco R, Sammarco G, Donato G, Montemurro S, Ruggieri E, et al. Correlation between serum tryptase, mast cells positive to tryptase and microvascular density in colorectal cancer patients: possible biological-clinical significance. PLos One 2014;9:e99512.
57. Ammendola M, Sacco R, Donato G, Zuccalà V, Russo E, Luposella M, et al. Mast cell positivity to tryptase correlates with metastatic lymph nodes in gastrointestinal cancer patients treated surgically. Oncology 2013;85:111–6.
58. Marech I, Leporini C, Ammendola M, Porcelli M, Gadaleta CD, Russo E, et al. Classical and non-classical proangiogenic factors as a target of antiangiogenic therapy in tumor microenvironment. Cancer Lett 2016;380:216–26.
59. Ribatti D, Ranieri G, Nico B, Benagiano V, Crivellato E. Tryptase and chymase are angiogenic in vivo in the chorioallantoic membrane assay. Int J Dev Biol 2011;55:99–102.
60. Blair RJ, Meng H, Marchese MJ, Ren S, Schwartz LB, Tonnesen MG, et al. Human mast cells stimulate vascular tube formation. Tryptase is a novel, potent angiogenic factor. J Clin Invest1997;99:2691–700.
61. Itoh Y, Sendo T, Oishi R. Physiology and pathophysiology of proteinase-activated receptors (PARs): role of tryptase/PAR- 2 in vascular endothelial barrier function. J Pharmacol Sci 2005;97:14–9.
62. Rickard A, Portell C, Kell PJ, Vinson SM, McHowat J. Proteaseactivated receptor stimulation activates a Ca2+-independent phospholipase A2 in bladder microvascular endothelial cells. Am J Physiol Renal Physiol 2005;288:F714–21.
63. Matej R, Mandáková P, Netíková I, Poucková P, Olejár T. Proteinase- activated receptor-2 expression in breast cancer and the role of trypsin on growth and metabolism of breast cancer cell line MDA MB-231. Physiol Res 2007;56:475–84.
64. Morris DR, Ding Y, Ricks TK, Gullapalli A, Wolfe BL, Trejo J. Protease- activated receptor-2 is essential for factor VIIa and Xainduced signaling, migration, and invasion of breast cancer cells. Cancer Res 2006;66:307–14.
65. Ammendola M, Leporini C, Marech I, Gadaleta CD, Scognamillo G, Sacco R, et al. Targeting mast cells tryptase in tumor microenvironment: a potential antiangiogenetic strategy. Biomed Res Int 2014;2014:154702
66. Ammendola M, Sacco R, Sammarco G, Donato G, Zuccalà V, Luposella M, et al. Mast cells density positive to tryptase correlates with angiogenesis in pancreatic ductal adenocarcinoma patients having undergone surgery. Gastroenterol Res Pract 2014;2014:951957.
67. Donato G, Conforti F, Camastra C, Ammendola M, Donato A, Renzulli A. The role of mast cell tryptases in cardiac myxoma: Histogenesis and development of a challenging tumor. Oncol Lett 2014;8:379–83.
68. Ammendola M, Zuccalà V, Patruno R, Russo E, Luposella M, Amorosi A, et al. Tryptase-positive mast cells and angiogenesis in keloids: a new possible post-surgical target for prevention. Updates Surg 2013;65:53–7.
69. Ranieri G, Ammendola M, Patruno R, Celano G, Zito FA, Montemurro S, et al. Tryptase-positive mast cells correlate with angiogenesis in early breast cancer patients. Int J Oncol 2009;35:115–20.
70. Ammendola M, Marech I, Sammarco G, Zuccalà V, Luposella M, Zizzo N, et al. Infiltrating mast cells correlate with angiogenesis in bone metastases from gastric cancer patients. Int J Mol Sci 2015;16:3237–50.
71. Malfettone A, Silvestris N, Saponaro C, Ranieri G, Russo A, Caruso S, et al. High density of tryptase-positive mast cells in human colorectal cancer: a poor prognostic factor related to protease-activated receptor 2 expression. J Cell Mol Med 2013;17:1025–37.
72. Soreide K, Janssen EA, Körner H, Baak JP. Trypsin in colorectal cancer: molecular biological mechanisms of proliferation, invasion, and metastasis. J Pathol 2006;209:147–56.
73. Darmoul D, Marie JC, Devaud H, Gratio V, Laburthe M. Initiation of human colon cancer cell proliferation by trypsin acting at protease-activated receptor-2. Br J Cancer 2001;85:772–9.
74. Uusitalo-Jarvinen H, Kurokawa T, Mueller BM, Andrade-Gordon P, Friedlander M, Ruf W. Role of protease activated receptor 1 and 2 signaling in hypoxia-induced angiogenesis. Arterioscler Thromb Vasc Biol 2007;27:1456–62.
75. Deplanque G, Demarchi M, Hebbar M, Flynn P, Melichar B, Atkins J, et al. A randomized, placebo-controlled phase III trial of masitinib plus gemcitabine in the treatment of advanced pancreatic cancer. Ann Oncol 2015;26:1194–200.
76. Laface C, Laforgia M, Zito AF, Loisi D, Zizzo N, Tamma R, et al. Chymase-positive Mast cells correlate with tumor angiogenesis: first report in pancreatic cancer patients. Eur Rev Med Pharmacol Sci 2021;25:6862–73.

APA	AMMENDOLA M, VESCIO F, AMMERATA G, LUPOSELLA M, PATRUNO R, LAFACE C, ZUCCALA V, CURCIO S, MEMEO R, NAVARRA G, CURRO G, RANIERI G (2023). Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery. , 62 - 69. 10.14744/ejmo.2023.53961
Chicago	AMMENDOLA Michele,VESCIO Francesca,AMMERATA Giorgio,LUPOSELLA Maria,PATRUNO Rosa,LAFACE Carmelo,ZUCCALA Valeria,CURCIO Silvia,MEMEO Riccardo,NAVARRA Giuseppe,CURRO Giuseppe,RANIERI Girolamo Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery. (2023): 62 - 69. 10.14744/ejmo.2023.53961
MLA	AMMENDOLA Michele,VESCIO Francesca,AMMERATA Giorgio,LUPOSELLA Maria,PATRUNO Rosa,LAFACE Carmelo,ZUCCALA Valeria,CURCIO Silvia,MEMEO Riccardo,NAVARRA Giuseppe,CURRO Giuseppe,RANIERI Girolamo Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery. , 2023, ss.62 - 69. 10.14744/ejmo.2023.53961
AMA	AMMENDOLA M,VESCIO F,AMMERATA G,LUPOSELLA M,PATRUNO R,LAFACE C,ZUCCALA V,CURCIO S,MEMEO R,NAVARRA G,CURRO G,RANIERI G Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery. . 2023; 62 - 69. 10.14744/ejmo.2023.53961
Vancouver	AMMENDOLA M,VESCIO F,AMMERATA G,LUPOSELLA M,PATRUNO R,LAFACE C,ZUCCALA V,CURCIO S,MEMEO R,NAVARRA G,CURRO G,RANIERI G Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery. . 2023; 62 - 69. 10.14744/ejmo.2023.53961
IEEE	AMMENDOLA M,VESCIO F,AMMERATA G,LUPOSELLA M,PATRUNO R,LAFACE C,ZUCCALA V,CURCIO S,MEMEO R,NAVARRA G,CURRO G,RANIERI G "Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery." , ss.62 - 69, 2023. 10.14744/ejmo.2023.53961
ISNAD	AMMENDOLA, Michele vd. "Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery". (2023), 62-69. https://doi.org/10.14744/ejmo.2023.53961

APA	AMMENDOLA M, VESCIO F, AMMERATA G, LUPOSELLA M, PATRUNO R, LAFACE C, ZUCCALA V, CURCIO S, MEMEO R, NAVARRA G, CURRO G, RANIERI G (2023). Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery. Eurasian Journal of Medicine and Oncology, 7(1), 62 - 69. 10.14744/ejmo.2023.53961
Chicago	AMMENDOLA Michele,VESCIO Francesca,AMMERATA Giorgio,LUPOSELLA Maria,PATRUNO Rosa,LAFACE Carmelo,ZUCCALA Valeria,CURCIO Silvia,MEMEO Riccardo,NAVARRA Giuseppe,CURRO Giuseppe,RANIERI Girolamo Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery. Eurasian Journal of Medicine and Oncology 7, no.1 (2023): 62 - 69. 10.14744/ejmo.2023.53961
MLA	AMMENDOLA Michele,VESCIO Francesca,AMMERATA Giorgio,LUPOSELLA Maria,PATRUNO Rosa,LAFACE Carmelo,ZUCCALA Valeria,CURCIO Silvia,MEMEO Riccardo,NAVARRA Giuseppe,CURRO Giuseppe,RANIERI Girolamo Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery. Eurasian Journal of Medicine and Oncology, vol.7, no.1, 2023, ss.62 - 69. 10.14744/ejmo.2023.53961
AMA	AMMENDOLA M,VESCIO F,AMMERATA G,LUPOSELLA M,PATRUNO R,LAFACE C,ZUCCALA V,CURCIO S,MEMEO R,NAVARRA G,CURRO G,RANIERI G Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery. Eurasian Journal of Medicine and Oncology. 2023; 7(1): 62 - 69. 10.14744/ejmo.2023.53961
Vancouver	AMMENDOLA M,VESCIO F,AMMERATA G,LUPOSELLA M,PATRUNO R,LAFACE C,ZUCCALA V,CURCIO S,MEMEO R,NAVARRA G,CURRO G,RANIERI G Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery. Eurasian Journal of Medicine and Oncology. 2023; 7(1): 62 - 69. 10.14744/ejmo.2023.53961
IEEE	AMMENDOLA M,VESCIO F,AMMERATA G,LUPOSELLA M,PATRUNO R,LAFACE C,ZUCCALA V,CURCIO S,MEMEO R,NAVARRA G,CURRO G,RANIERI G "Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery." Eurasian Journal of Medicine and Oncology, 7, ss.62 - 69, 2023. 10.14744/ejmo.2023.53961
ISNAD	AMMENDOLA, Michele vd. "Ki-67 Expression, Mast Cells Positive to Tryptase, and Angiogenesis in Gastric Cancer Patients Undergoing Radical Surgery". Eurasian Journal of Medicine and Oncology 7/1 (2023), 62-69. https://doi.org/10.14744/ejmo.2023.53961