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Published in: Annals of Surgical Oncology 10/2007

01-10-2007 | Gastrointestinal Oncology

Cytoplasmic CD24 Expression Is a Novel Prognostic Factor in Diffuse-Type Gastric Adenocarcinoma

Authors: Yuh-Yu Chou, MD, Yung-Ming Jeng, MD, Tan-Tsao Lee, MD, Fu-Chang Hu, Hsin-Lien Kao, MS, Wei-Chou Lin, MD, Po-Lin Lai, MS, Rey-Heng Hu, MD, PhD, Ray-Hwang Yuan, MD, PhD

Published in: Annals of Surgical Oncology | Issue 10/2007

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Abstract

Background

CD24, a mucin like cell surface adhesion molecule and a ligand for P-selectin, has been reported as a prognostic factor in a variety of human cancers. However, the role of CD24 in gastric adenocarcinoma remains largely unknown.

Methods

The expression pattern of CD24 in 103 gastric adenocarcinomas (31 diffuse type, 60 intestinal type, and 12 mixed type) was analyzed by immunohistochemistry.

Results

Cytoplasmic CD24 expression occurred in 50% of the gastric adenocarcinoma patients and was associated with high-stage tumor (Stage III–IV, P = .023), serosal invasion (SI, P = .010), lymphovascular invasion (LVI, P = .039), and lower 10-year survival (P = .0238). The CD24 staining pattern was different in intestinal and diffuse-type gastric adenocarcinomas. However, the tumor thrombi in lymphovascular spaces exhibited strong cytoplasmic CD24 expression in both types. Further analysis showed that cytoplasmic CD24 expression was, in fact, correlated with high-stage tumor, SI, LVI, and lower 10-year survival significantly (P = .020, P = .007, P = .018, P = .0285, respectively) in diffuse-type gastric adenocarcinoma. Moreover, multivariate analysis showed that cytoplasmic CD24 expression was an independent risk factor of SI and LVI respectively (P = .0083 and P = .0019), and thus it contributed to high-stage tumor and poor patient survival in diffuse- or mixed-type gastric adenocarcinoma.

Conclusions

Cytoplasmic expression of CD24 was associated with invasiveness and poorer prognosis and can serve as a novel target for prognostic prediction and adjuvant treatment of patients with diffuse-type gastric adenocarcinoma after tumor resection.
Literature
1.
go back to reference Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55:74–108PubMedCrossRef Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55:74–108PubMedCrossRef
2.
go back to reference Mercer DW, Robinson EK. Gastric neoplasia. In: Townsend CM Jr, Beauchamp RD, Evers BM, Mattox KL (eds.) Sabiston Textbook of Surgery: The Biological Basis of Modern Surgical Practice. 17th ed. Philadelphia: Elsevier Saunders, 2004:1265–321 Mercer DW, Robinson EK. Gastric neoplasia. In: Townsend CM Jr, Beauchamp RD, Evers BM, Mattox KL (eds.) Sabiston Textbook of Surgery: The Biological Basis of Modern Surgical Practice. 17th ed. Philadelphia: Elsevier Saunders, 2004:1265–321
3.
go back to reference Japanese Gastric Cancer Association Registration Committee, Maruyama K, Kaminishi M, Hayashi K, et al. Gastric cancer treated in 1991 in Japan: data analysis of nationwide registry. Gastric Cancer 2006; 9:51–66PubMedCrossRef Japanese Gastric Cancer Association Registration Committee, Maruyama K, Kaminishi M, Hayashi K, et al. Gastric cancer treated in 1991 in Japan: data analysis of nationwide registry. Gastric Cancer 2006; 9:51–66PubMedCrossRef
4.
go back to reference Hundahl SA, Menck HR, Mansour EG, Winchester DP. The National Cancer Data Base report on gastric carcinoma. Cancer 1997; 80:2333–41PubMedCrossRef Hundahl SA, Menck HR, Mansour EG, Winchester DP. The National Cancer Data Base report on gastric carcinoma. Cancer 1997; 80:2333–41PubMedCrossRef
5.
go back to reference Serlin O, Keehn RJ, Higgins GA Jr, Harrower HW, Mendeloff GL. Factors related to survival following resection for gastric carcinoma: analysis of 903 cases. Cancer 1977; 40:1318–29PubMedCrossRef Serlin O, Keehn RJ, Higgins GA Jr, Harrower HW, Mendeloff GL. Factors related to survival following resection for gastric carcinoma: analysis of 903 cases. Cancer 1977; 40:1318–29PubMedCrossRef
6.
go back to reference Adachi Y, Yasuda K, Inomata M, Sato K, Shiraishi N, Kitano S. Pathology and prognosis of gastric carcinoma: well versus poorly differentiated type. Cancer 2000; 89:1418–24PubMedCrossRef Adachi Y, Yasuda K, Inomata M, Sato K, Shiraishi N, Kitano S. Pathology and prognosis of gastric carcinoma: well versus poorly differentiated type. Cancer 2000; 89:1418–24PubMedCrossRef
7.
go back to reference Siewert JR, Bottcher K, Stein HJ, Roder JD. Relevant prognostic factors in gastric cancer: ten-year results of the German Gastric Cancer Study. Ann Surg 1998; 228:449–61PubMedCrossRef Siewert JR, Bottcher K, Stein HJ, Roder JD. Relevant prognostic factors in gastric cancer: ten-year results of the German Gastric Cancer Study. Ann Surg 1998; 228:449–61PubMedCrossRef
8.
go back to reference Werner M, Becker KF, Keller G, Hofler H. Gastric adenocarcinoma: pathomorphology and molecular pathology. J Cancer Res Clin Oncol 2001; 127:207–16PubMedCrossRef Werner M, Becker KF, Keller G, Hofler H. Gastric adenocarcinoma: pathomorphology and molecular pathology. J Cancer Res Clin Oncol 2001; 127:207–16PubMedCrossRef
9.
go back to reference Pirruccello SJ, LeBien TW. The human B cell-associated antigen CD24 is a single chain sialoglycoprotein. J Immunol 1986; 136:3779–84PubMed Pirruccello SJ, LeBien TW. The human B cell-associated antigen CD24 is a single chain sialoglycoprotein. J Immunol 1986; 136:3779–84PubMed
10.
go back to reference Fischer GF, Majdic O, Gadd S, Knapp W. Signal transduction in lymphocytic and myeloid cells via CD24, a new member of phosphoinositol-anchored membrane molecules. J Immunol 1990; 144:638–41PubMed Fischer GF, Majdic O, Gadd S, Knapp W. Signal transduction in lymphocytic and myeloid cells via CD24, a new member of phosphoinositol-anchored membrane molecules. J Immunol 1990; 144:638–41PubMed
11.
go back to reference Sammar M, Aigner S, Hubbe M, Schirrmacher V, Schachner M, Vestweber D, Altevogt P. Heat-stable antigen (CD24) as ligand for mouse P-selectin. Int Immunol 1994; 6:1027–36PubMedCrossRef Sammar M, Aigner S, Hubbe M, Schirrmacher V, Schachner M, Vestweber D, Altevogt P. Heat-stable antigen (CD24) as ligand for mouse P-selectin. Int Immunol 1994; 6:1027–36PubMedCrossRef
12.
go back to reference Chen M, Geng JG. P-selectin mediates adhesion of leukocytes, platelets, and cancer cells in inflammation, thrombosis, and cancer growth and metastasis. Arch Immunol Ther Exp (Warsz) 2006; 54:75–84CrossRef Chen M, Geng JG. P-selectin mediates adhesion of leukocytes, platelets, and cancer cells in inflammation, thrombosis, and cancer growth and metastasis. Arch Immunol Ther Exp (Warsz) 2006; 54:75–84CrossRef
13.
go back to reference Elghetany MT, Patel J. Assessment of CD24 expression on bone marrow neutrophilic granulocytes: CD24 is a marker for the myelocytic stage of development. Am J Hematol 2002; 71:348–9PubMedCrossRef Elghetany MT, Patel J. Assessment of CD24 expression on bone marrow neutrophilic granulocytes: CD24 is a marker for the myelocytic stage of development. Am J Hematol 2002; 71:348–9PubMedCrossRef
14.
go back to reference Magnaldo T, Barrandon Y. CD24 (heat stable antigen, nectadrin), a novel keratinocyte differentiation marker, is preferentially expressed in areas of the hair follicle containing the colony-forming cells. J Cell Sci 1996; 109:3035–45PubMed Magnaldo T, Barrandon Y. CD24 (heat stable antigen, nectadrin), a novel keratinocyte differentiation marker, is preferentially expressed in areas of the hair follicle containing the colony-forming cells. J Cell Sci 1996; 109:3035–45PubMed
15.
go back to reference Shirasawa T, Akashi T, Sakamoto K, Takahashi H, Maruyama N, Hirokawa K. Gene expression of CD24 core peptide molecule in developing brain and developing non-neural tissues. Dev Dyn 1993; 198:1–13PubMed Shirasawa T, Akashi T, Sakamoto K, Takahashi H, Maruyama N, Hirokawa K. Gene expression of CD24 core peptide molecule in developing brain and developing non-neural tissues. Dev Dyn 1993; 198:1–13PubMed
16.
go back to reference Suzuki T, Kiyokawa N, Taguchi T, Sekino T, Katagiri YU, Fujimoto J. CD24 induces apoptosis in human B cells via the glycolipid-enriched membrane domains/rafts-mediated signaling system. J Immunol 2001; 166:5567–77PubMed Suzuki T, Kiyokawa N, Taguchi T, Sekino T, Katagiri YU, Fujimoto J. CD24 induces apoptosis in human B cells via the glycolipid-enriched membrane domains/rafts-mediated signaling system. J Immunol 2001; 166:5567–77PubMed
17.
go back to reference Figarella-Branger D, Moreau H, Pellissier JF, Bianco N, Rougon G. CD24, a signal-transducing molecule expressed on human B lymphocytes, is a marker for human regenerating muscle. Acta Neuropathol (Berl) 1993; 86:275–84CrossRef Figarella-Branger D, Moreau H, Pellissier JF, Bianco N, Rougon G. CD24, a signal-transducing molecule expressed on human B lymphocytes, is a marker for human regenerating muscle. Acta Neuropathol (Berl) 1993; 86:275–84CrossRef
18.
go back to reference Kristiansen G, Sammar M, Altevogt P. Tumour biological aspects of CD24, a mucin-like adhesion molecule. J Mol Histol 2004; 35:255–62PubMedCrossRef Kristiansen G, Sammar M, Altevogt P. Tumour biological aspects of CD24, a mucin-like adhesion molecule. J Mol Histol 2004; 35:255–62PubMedCrossRef
19.
go back to reference Su MC, Hsu C, Kao HL, Jeng YM. CD24 expression is a prognostic factor in intrahepatic cholangiocarcinoma. Cancer Lett 2006; 235:34–9PubMedCrossRef Su MC, Hsu C, Kao HL, Jeng YM. CD24 expression is a prognostic factor in intrahepatic cholangiocarcinoma. Cancer Lett 2006; 235:34–9PubMedCrossRef
20.
go back to reference Aigner S, Ramos CL, Hafezi-Moghadam A, Lawrence MB, Friederichs J, Altevogt P, Ley K. CD24 mediates rolling of breast carcinoma cells on P-selectin. FASEB J 1998; 12:1241–51PubMed Aigner S, Ramos CL, Hafezi-Moghadam A, Lawrence MB, Friederichs J, Altevogt P, Ley K. CD24 mediates rolling of breast carcinoma cells on P-selectin. FASEB J 1998; 12:1241–51PubMed
21.
go back to reference Friederichs J, Zeller Y, Hafezi-Moghadam A, Grone HJ, Ley K, Altevogt P. The CD24/P-selectin binding pathway initiates lung arrest of human A125 adenocarcinoma cells. Cancer Res 2000; 60:6714–22PubMed Friederichs J, Zeller Y, Hafezi-Moghadam A, Grone HJ, Ley K, Altevogt P. The CD24/P-selectin binding pathway initiates lung arrest of human A125 adenocarcinoma cells. Cancer Res 2000; 60:6714–22PubMed
22.
go back to reference Jacob J, Bellach J, Grutzmann R, Alldinger I, Pilarsky C, Dietel M, Kristiansen G. Expression of CD24 in adenocarcinomas of the pancreas correlates with higher tumor grades. Pancreatology 2004; 4:454–60PubMedCrossRef Jacob J, Bellach J, Grutzmann R, Alldinger I, Pilarsky C, Dietel M, Kristiansen G. Expression of CD24 in adenocarcinomas of the pancreas correlates with higher tumor grades. Pancreatology 2004; 4:454–60PubMedCrossRef
23.
go back to reference Hosmer DW, Lemeshow S. Applied Logistic Regression, 2nd ed. New York: John Wiley & Sons, 2000 Hosmer DW, Lemeshow S. Applied Logistic Regression, 2nd ed. New York: John Wiley & Sons, 2000
24.
go back to reference Hosmer DW, Lemeshow S. Applied Survival Analysis: Regression Modeling of Time to Event Data. New York: John Wiley & Sons, 1999 Hosmer DW, Lemeshow S. Applied Survival Analysis: Regression Modeling of Time to Event Data. New York: John Wiley & Sons, 1999
25.
go back to reference Lauren P. The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. Acta Path Microbiol Scand 1965; 64:31–49PubMed Lauren P. The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. Acta Path Microbiol Scand 1965; 64:31–49PubMed
26.
go back to reference Lynch HT, Grady W, Suriano G, Huntsman D. Gastric cancer: new genetic developments. J Surg Oncol 2005; 90:114–33PubMedCrossRef Lynch HT, Grady W, Suriano G, Huntsman D. Gastric cancer: new genetic developments. J Surg Oncol 2005; 90:114–33PubMedCrossRef
27.
go back to reference Ming S. Cellular and molecular pathology of gastric carcinoma and precursor lesions: a critical review. Gastric Cancer 1998; 1:31–50PubMedCrossRef Ming S. Cellular and molecular pathology of gastric carcinoma and precursor lesions: a critical review. Gastric Cancer 1998; 1:31–50PubMedCrossRef
28.
go back to reference Roviello F, Marrelli D, Vindigni C, De Stefano A, Spina D, Pinto E. P53 accumulation is a prognostic factor in intestinal-type gastric carcinoma but not in the diffuse type. Ann Surg Oncol 1999; 6:739–45PubMedCrossRef Roviello F, Marrelli D, Vindigni C, De Stefano A, Spina D, Pinto E. P53 accumulation is a prognostic factor in intestinal-type gastric carcinoma but not in the diffuse type. Ann Surg Oncol 1999; 6:739–45PubMedCrossRef
29.
go back to reference Zheng H, Takahashi H, Murai Y, et al. Pathobiological characteristics of intestinal- and diffuse-type gastric carcinoma in Japan: An immunostaining study on the tissue microarray. J Clin Pathol 2007; 60:273–7PubMedCrossRef Zheng H, Takahashi H, Murai Y, et al. Pathobiological characteristics of intestinal- and diffuse-type gastric carcinoma in Japan: An immunostaining study on the tissue microarray. J Clin Pathol 2007; 60:273–7PubMedCrossRef
30.
go back to reference Weichert W, Denkert C, Burkhardt M, et al. Cytoplasmic CD24 expression in colorectal cancer independently correlates with shortened patient survival. Clin Cancer Res 2005; 11:6574–81PubMedCrossRef Weichert W, Denkert C, Burkhardt M, et al. Cytoplasmic CD24 expression in colorectal cancer independently correlates with shortened patient survival. Clin Cancer Res 2005; 11:6574–81PubMedCrossRef
31.
go back to reference Lim SC, Oh SH. The role of CD24 in various human epithelial neoplasias. Pathol Res Pract 2005; 201:479–86PubMedCrossRef Lim SC, Oh SH. The role of CD24 in various human epithelial neoplasias. Pathol Res Pract 2005; 201:479–86PubMedCrossRef
32.
go back to reference Sheen-Chen SM, Chou CW, Chen MC, Chen FC, Chen YS, Chen JJ. Adenocarcinoma in the middle third of the stomach—an evaluation for the prognostic significance of clinicopathological features. Hepatogastroenterology 1997; 44:1488–94PubMed Sheen-Chen SM, Chou CW, Chen MC, Chen FC, Chen YS, Chen JJ. Adenocarcinoma in the middle third of the stomach—an evaluation for the prognostic significance of clinicopathological features. Hepatogastroenterology 1997; 44:1488–94PubMed
33.
go back to reference Ludeman L, Shepherd NA. Serosal involvement in gastrointestinal cancer: its assessment and significance. Histopathology 2005; 47:123–31PubMedCrossRef Ludeman L, Shepherd NA. Serosal involvement in gastrointestinal cancer: its assessment and significance. Histopathology 2005; 47:123–31PubMedCrossRef
34.
go back to reference Miyashiro I, Takachi K, Doki Y, et al. When is curative gastrectomy justified for gastric cancer with positive peritoneal lavage cytology but negative macroscopic peritoneal implant? World J Surg 2005; 29:1131–4PubMedCrossRef Miyashiro I, Takachi K, Doki Y, et al. When is curative gastrectomy justified for gastric cancer with positive peritoneal lavage cytology but negative macroscopic peritoneal implant? World J Surg 2005; 29:1131–4PubMedCrossRef
35.
go back to reference Burke EC, Karpeh MS Jr, Conlon KC, Brennan MF. Peritoneal lavage cytology in gastric cancer: an independent predictor of outcome. Ann Surg Oncol 1998; 5:411–5PubMedCrossRef Burke EC, Karpeh MS Jr, Conlon KC, Brennan MF. Peritoneal lavage cytology in gastric cancer: an independent predictor of outcome. Ann Surg Oncol 1998; 5:411–5PubMedCrossRef
36.
go back to reference Jakl RJ, Miholic J, Koller R, Markis E, Wolner E. Prognostic factors in adenocarcinoma of the cardia. Am J Surg 1995; 169:316–9PubMedCrossRef Jakl RJ, Miholic J, Koller R, Markis E, Wolner E. Prognostic factors in adenocarcinoma of the cardia. Am J Surg 1995; 169:316–9PubMedCrossRef
37.
go back to reference Kristiansen G, Denkert C, Schluns K, Dahl E, Pilarsky C, Hauptmann S. CD24 is expressed in ovarian cancer and is a new independent prognostic marker of patient survival. Am J Pathol 2002; 161:1215–21PubMed Kristiansen G, Denkert C, Schluns K, Dahl E, Pilarsky C, Hauptmann S. CD24 is expressed in ovarian cancer and is a new independent prognostic marker of patient survival. Am J Pathol 2002; 161:1215–21PubMed
38.
go back to reference Kristiansen G, Winzer KJ, Mayordomo E, et al. CD24 expression is a new prognostic marker in breast cancer. Clin Cancer Res 2003; 9:4906–13PubMed Kristiansen G, Winzer KJ, Mayordomo E, et al. CD24 expression is a new prognostic marker in breast cancer. Clin Cancer Res 2003; 9:4906–13PubMed
39.
go back to reference Schindelmann S, Windisch J, Grundmann R, Kreienberg R, Zeillinger R, Deissler H. Expression profiling of mammary carcinoma cell lines: correlation of in vitro invasiveness with expression of CD24. Tumor Biol 2002; 23:139–45CrossRef Schindelmann S, Windisch J, Grundmann R, Kreienberg R, Zeillinger R, Deissler H. Expression profiling of mammary carcinoma cell lines: correlation of in vitro invasiveness with expression of CD24. Tumor Biol 2002; 23:139–45CrossRef
40.
go back to reference Aigner S, Sthoeger ZM, Fogel M, et al. CD24, a mucin-type glycoprotein, is a ligand for P-selectin on human tumor cells. Blood 1997; 89:3385–95PubMed Aigner S, Sthoeger ZM, Fogel M, et al. CD24, a mucin-type glycoprotein, is a ligand for P-selectin on human tumor cells. Blood 1997; 89:3385–95PubMed
41.
go back to reference Kristiansen G, Schluns K, Yongwei Y, Denkert C, Dietel M, Petersen I. CD24 is an independent prognostic marker of survival in nonsmall cell lung cancer patients. Br J Cancer 2003; 88:231–6PubMedCrossRef Kristiansen G, Schluns K, Yongwei Y, Denkert C, Dietel M, Petersen I. CD24 is an independent prognostic marker of survival in nonsmall cell lung cancer patients. Br J Cancer 2003; 88:231–6PubMedCrossRef
42.
go back to reference Smith SC, Oxford G, Wu Z, et al. The metastasis-associated gene CD24 is regulated by Ral GTPase and is a mediator of cell proliferation and survival in human cancer. Cancer Res 2006; 66:1917–22PubMedCrossRef Smith SC, Oxford G, Wu Z, et al. The metastasis-associated gene CD24 is regulated by Ral GTPase and is a mediator of cell proliferation and survival in human cancer. Cancer Res 2006; 66:1917–22PubMedCrossRef
43.
go back to reference Huang LR, Hsu HC. Cloning and expression of CD24 gene in human hepatocellular carcinoma: a potential early tumor marker gene correlates with p53 mutation and tumor differentiation. Cancer Res 1995; 55:4717–21PubMed Huang LR, Hsu HC. Cloning and expression of CD24 gene in human hepatocellular carcinoma: a potential early tumor marker gene correlates with p53 mutation and tumor differentiation. Cancer Res 1995; 55:4717–21PubMed
44.
go back to reference Fogel M, Friederichs J, Zeller Y, et al. CD24 is a marker for human breast carcinoma. Cancer Lett 1999; 143:87–94PubMedCrossRef Fogel M, Friederichs J, Zeller Y, et al. CD24 is a marker for human breast carcinoma. Cancer Lett 1999; 143:87–94PubMedCrossRef
45.
go back to reference Sagiv E, Memeo L, Karin A, et al. CD24 is a new oncogene, early at the multistep process of colorectal cancer carcinogenesis. Gastroenterology 2006; 131:630–9PubMedCrossRef Sagiv E, Memeo L, Karin A, et al. CD24 is a new oncogene, early at the multistep process of colorectal cancer carcinogenesis. Gastroenterology 2006; 131:630–9PubMedCrossRef
46.
go back to reference Baumann P, Cremers N, Kroese F, et al. CD24 expression causes the acquisition of multiple cellular properties associated with tumor growth and metastasis. Cancer Res 2005; 65:10783–93PubMedCrossRef Baumann P, Cremers N, Kroese F, et al. CD24 expression causes the acquisition of multiple cellular properties associated with tumor growth and metastasis. Cancer Res 2005; 65:10783–93PubMedCrossRef
47.
go back to reference Kruger JA, Kaplan CD, Luo Y, Zhou H, Markowitz D, Xiang R, Reisfeld RA. Characterization of stem cell-like cancer cells in immune-competent mice. Blood 2006; 108:3960–12CrossRef Kruger JA, Kaplan CD, Luo Y, Zhou H, Markowitz D, Xiang R, Reisfeld RA. Characterization of stem cell-like cancer cells in immune-competent mice. Blood 2006; 108:3960–12CrossRef
48.
go back to reference Shackleton M, Vaillant F, Simpson KJ, et al. Generation of a functional mammary gland from a single stem cell. Nature 2006; 439:84–8PubMedCrossRef Shackleton M, Vaillant F, Simpson KJ, et al. Generation of a functional mammary gland from a single stem cell. Nature 2006; 439:84–8PubMedCrossRef
49.
go back to reference Li C, Heidt DG, Dalerba P, et al. Identification of pancreatic cancer stem cells. Cancer Res 2007; 67:1030–7PubMedCrossRef Li C, Heidt DG, Dalerba P, et al. Identification of pancreatic cancer stem cells. Cancer Res 2007; 67:1030–7PubMedCrossRef
50.
go back to reference Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: migrating cancer stem cells: an integrated concept of malignant tumor progression. Nat Rev Cancer 2005; 5:744–9PubMedCrossRef Brabletz T, Jung A, Spaderna S, Hlubek F, Kirchner T. Opinion: migrating cancer stem cells: an integrated concept of malignant tumor progression. Nat Rev Cancer 2005; 5:744–9PubMedCrossRef
51.
go back to reference Fischer A, Blanche S, Le Bidois J, et al. Anti-B-cell monoclonal antibodies in the treatment of severe B-cell lymphoproliferative syndrome following bone marrow and organ transplantation. N Engl J Med 1991; 324:1451–6PubMedCrossRef Fischer A, Blanche S, Le Bidois J, et al. Anti-B-cell monoclonal antibodies in the treatment of severe B-cell lymphoproliferative syndrome following bone marrow and organ transplantation. N Engl J Med 1991; 324:1451–6PubMedCrossRef
Metadata
Title
Cytoplasmic CD24 Expression Is a Novel Prognostic Factor in Diffuse-Type Gastric Adenocarcinoma
Authors
Yuh-Yu Chou, MD
Yung-Ming Jeng, MD
Tan-Tsao Lee, MD
Fu-Chang Hu
Hsin-Lien Kao, MS
Wei-Chou Lin, MD
Po-Lin Lai, MS
Rey-Heng Hu, MD, PhD
Ray-Hwang Yuan, MD, PhD
Publication date
01-10-2007
Publisher
Springer-Verlag
Published in
Annals of Surgical Oncology / Issue 10/2007
Print ISSN: 1068-9265
Electronic ISSN: 1534-4681
DOI
https://doi.org/10.1245/s10434-007-9501-x

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