Gastric Cancer Open Access
Copyright ©The Author(s) 2002. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Dec 15, 2002; 8(6): 1005-1008
Published online Dec 15, 2002. doi: 10.3748/wjg.v8.i6.1005
Mast cell density and the context of clinicopathological parameters and expression of p185, estrogen receptor, and proliferating cell nuclear antigen in gastric carcinoma
Ying-An Jiang, He-Sheng Luo, Department of Gastroenterology, Renming Hospital of Wuhan University, Wuhan 430060, Hubei Province, China
You-Yuan Zhang, Department of Pathology, Central Hospital of Huangshi City, Huangshi 435000, Hubei Province, China
Shou-Fu Xing, Department of Pathology, Medical College of Wuhan University, Wuhan 430071, Hubei Province, China
Author contributions: All authors contributed equally to the work.
Correspondence to: Ying-An Jiang, Central Hospital of Huangshi City, 43 Wuhan Road, Huangshi 435000, Hubei Province, China. hszxyy@public.hs.hb.cn
Telephone: +86-714-6283783 Fax: +86-714-6233931
Received: April 26, 2002
Revised: May 29, 2002
Accepted: June 10, 2002
Published online: December 15, 2002

Abstract

AIM: To investigate the relationship between the mast cell density (MCD) and the context of clinicopathological parameters and expression of p185, estrogen receptor (ER), and proliferating cell nuclear antigen (PCNA) in gastric carcinoma.

METHODS: Mast cell, p185, ER, and PCNA were detected using immunohistochemical S-P labeling method. Mast cell was counted in tissue of gastric carcinoma and regional lymph nodes respectively, and involved lymph nodes (ILN) were examined as usual.

RESULTS: MCD was significantly related to both age and depth of penetration (χ2 = 4.688,P < 0.05 for age and χ2 = 9.350, P < 0.01 for depth of penetration) between MCD > 21/0.03 mm2 and MCD ≤ 21/0.03 mm2 in 100 patients; MCD in 1-6 ILN group patients was significantly higher than that in 7-15 ILN or > 15 ILN group patients (u = 6.881, 8.055, P < 0.01); There were significant differences intergroup in positive expression rate of p185, ER and PCNA between MCD > 21/ 0.03 mm2 and MCD ≤ 21/0.03 mm2 in 100 patients.

CONCLUSION: Mast cell may have effect on inhibiting invasive growth of tumor, especially in the aged patients; The number of mast cells, in certain degree, may predicate the number of involved lymph nodes, which is valuable for assessment of prognosis; MCD was related to the expression of p185, ER, and PCNA in gastric carcinoma. It suggests that mast cell accumulation may inhibit the proliferation and the dissemination of the gastric carcinoma.




INTRODUCTION

Recently, many studies have reported on the association of mast cell with various tumors[1-9]. In several malignancies, mast cell has been found to correlate with growth, penetration and prognosis of tumor[10-13]. Therefore, our study was undertaken to investigate the relationship between the mast cell density (MCD) and the context of clinicopathological parameters and expression of p185, estrogen receptor (ER), and proliferating cell nuclear antigen (PCNA) in gastric carcinoma.

MATERIALS AND METHODS
Materials

The specimens of gastric carcinoma, histologically confirmed, were surgically obtained from 421 patients. The patients had undergone curative tumor resection at our hospital between 1984 and 1998. And only 100 patients were chosen at random in our study. Among 100 patients, 41 patients had lymph node metastases. All resected tissue specimens were fixed in formalin, embedded in paraffin, and cut into 3-4 μm serial sections. 459 lymph nodes were collected from 41 patients (range, 8-26 per patient).

Methods

Mast cell, p185, ER, and PCNA were detected using immuno-histochemical method (agents from Maixin-Bio Corp. Fuzhou, China).The count of mast cells in the tissue of gastric carcinoma was as described by Takanami et al[10]. A grid (0.15 mm by 0.2 mm) which was defined an area of 0.03 mm2 per field was used for to count mast cells. Similarly, that of mast cells in regional lymph nodes was described by Bowers et al[14].A grid which defined an area of mm2 per field was used. ILN was examined using routine pathological method. The results were expressed as the means ± SD. Statistical analyses were performed using the Chi-square and u test. A P value less than or equal to 0.05 was considered significant.

RESULTS

Table 1 showed the clincopathologic parameters for two groups (high MCD group, MCD was more than 21/0.03 mm2, and low MCD group, MCD was equal to 21/0.03 mm2 or less). There were no significant differences between two groups regarding both degree of differentiation and largest dimension of tumor. However, MCD was significantly related to both age and depth of penetration (P < 0.05 for age and P < 0.01 for depth of penetration) (Figure 1).

Table 1 Correlation between MCD and Clinicopathologic find-ing of gastric carcinoma (n = 100).
VariableMCD > 21/0.03 mm2MCD ≤ 21/0.03 mm2P Value
Age (yrs)
< 601625< 0.05
≥ 603623
Degree of differentiation
Well1814> 0.05
Moderately2321
Poorly1113
Largest dimension of tumor ( in mm)
≤ 303036> 0.05
> 302212
Depth of penetration
Involved serosa2134< 0.01
Not involved serosa3114
Figure 1
Figure 1 Mast cells of gastric carcinoma (Tryptase labeling, DAB staining, original magnification, × 100)

Table 2 showed correlation between MCD and cancerous metastases in regional lymph nodes. MCD in 1-6 ILN group patients (n = 21) was 12 ± 3.11, 7-15 ILN (n = 14), 6 ± 2.06, > 15 ILN (n = 6), 5 ± 1.33, respectively. MCD in 1-6 ILN group patients was significantly higher than that in 7-15 ILN or > 15 ILN group patients (P < 0.01), but, MCD in 7-15 ILN group patients was not significantly higher than that in > 15 ILN group patients (P > 0.05) (Figure 2).

Table 2 Correlation between MCD and cancerous metastases in regional lymph nodes (n = 41).
VariablenMCD (mean ± SD, /mm2)
1-6 ILN2112 ± 3.11
7-15 ILN146 ± 2.06
> 15 ILN65 ± 1.33
Figure 2
Figure 2 Mast cells of regional lymph nodes of gastric carci-noma (Tryptase labeling, original magnification, × 100)

There were significant differences intergroup in positive expression rate of p185, ER and PCNA between high MCD group (the MCD was more than 21/0.03 mm2) and low MCD group (the MCD was equal to 21/0.03 mm2 or less) (P < 0.01). As was shown in Table 3 (Figures 3, 4 and 5).

Table 3 Correlation between MCD and the positive expression rate of p185, ER, and PCNA in the gastric carcinoma tissues.
MCDnPositive expression rate (%)
p185ERPCNA
> 21/0.03 mm25222 (42.31)11 (21.15)12 (23.08)
≤ 21/0.03 mm24831 (59.62)28 (53.84)27 (51.92)
P Value< 0.01< 0.001< 0.01
Figure 3
Figure 3 p185 of gastric carcinoma (Original magnification, × 100)
Figure 4
Figure 4 Estrogen receptor of gastric carcinoma (Original magnification, × 100)
Figure 5
Figure 5 PCNA of gastric carcinoma (Original magnification, × 400)
DISCUSSION

Numerous studies have shown that mast cell plays an important role in tumor growth. Dabbou et al[15,16] found that mast cells were accumulated around the periphery of the invasive and metastatic rat mammary adenocarcinoma, and they believed that interactions between mast cell and tumor cell were important for the growth and invasive properties of the tumor. Nakamura et al[17] found the mechanism of mast cell accumulation at sites of tumors was that tumor cells could produce a factor which might not be the already known mast cell growth factors. Wang et al[18] found that the anti-tumor effect of mast cell might be related to releasing of tumor necrosis factor (TNF) and non-TNF cytotoxicity. Our results revealed there were no significant differences intergroup regarding both degree of differentiation and largest dimension of tumor between MCD > 21/0.03 mm2 and MCD ≤ 21/0.03 mm2. MCD was significantly related to both age and depth of penetration (P < 0.05 for age and P < 0.01 for depth of penetration).

The data indicate the lymph node status is associated with the patients’ prognoses in many malignancies, and may be useful in assessing the outcome of this disease[19-28]. The treatment regimen was depended on not only whether involved lymph node was present or not, but also the number of involved lymph node[20,29]. Maurel et al[30] had examined 7.7 ± 0.2 lymph nodes per specimen in 851 patients with resected colorectal carcinoma, the results strongly pointed out that at least eight lymph nodes must be examined and they called the number of eight as a “golden number”. At least eight lymph nodes per specimen were examined in our study as done by Maurel et al[30]. Roder et al[20] followed up 477 patients with gastric carcinoma of lymph node metastasis, and they found that 5-year survival rates were as follows (1) 1-6 involved lymph nodes: 45.5%; (2) 7-15 involved lymph nodes:29.7%; (3) > 15 involved lymph nodes: 10.4%. There was a highly significant difference in survival (P < 0.0001). Our results indicated that MCD in 1-6 ILN group patients was 12 ± 3.11, 7-15 ILN, 6 ± 2.06, > 15 ILN, 5 ± 1.33, respectively. MCD in 1-6 ILN group patients was significantly higher than that in 7-15 ILN or > 15 ILN group patients (P < 0.01), but, MCD in 7-15 ILN group patients was not significantly higher than that in > 15 ILN group patients (P > 0.05). In other words, the higher MCD was in regional lymph nodes, the lower number of ILN of gastric cancerous metastases was. It demonstrates that the number of mast cells, in certain degree, may predicate the number of involved lymph nodes of gastric cancerous metastases. Therefore, MCD is a valuable parameter for assessing the prognosis of patients with gastric carcinoma.

The C-erbB-2 was first identified in ethylnitosourea-induced rat neuroblastoma. It encodes a 185 kilodalton (kDa) glycoprotein. It was reported recently that overexpression and gene amplification of C-erb B-2 were frequently observed in the intestinal type gastric adenocarcinoma, and it was a prognostic indicator in tumor[31-33]. ER is commonly known to be present in the cell of the breast and endometrium, but have also been identified in diverse normal and neoplastic nonreproductive tissues. The expression of ER has been considered to be a favorable prognostic factor in breast carcinoma and endometrial carcinoma but a poor prognostic factor in gastric carcinoma[34]. PCNA is an auxiliary protein of DNA polymerase delta which plays a major role in synthesizing DNA and is expressed in the nuclei, particularly in the late phase of G1 and S. Therefore PCNA is a useful marker for proliferative activity[35-37]. Our results showed there were significant differences intergroup in the positive expression rate of p185, ER and PCNA between MCD > 21/0.03 mm2 and MCD ≤ 21/0.03 mm2. It suggests that mast cell accumulation may inhibit the proliferation and the dissemination of gastric carcinoma. This finding may provide a molecular foundation of the further study on relation between mast cell and gastric carcinoma.

Footnotes

Edited by Liu HX

References
1.  Tomita M, Matsuzaki Y, Edagawa M, Shimizu T, Hara M, Sekiya R, Onitsuka T. Association of mast cells with tumor angiogenesis in esophageal squamous cell carcinoma. Dis Esophagus. 2001;14:135-138.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 25]  [Cited by in F6Publishing: 29]  [Article Influence: 1.3]  [Reference Citation Analysis (0)]
2.  Tomita M, Matsuzaki Y, Onitsuka T. Effect of mast cells on tumor angiogenesis in lung cancer. Ann Thorac Surg. 2000;69:1686-1690.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 75]  [Cited by in F6Publishing: 84]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
3.  Erkiliç S, Erbağci Z. The significance of mast cells associated with basal cell carcinoma. J Dermatol. 2001;28:312-315.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 14]  [Cited by in F6Publishing: 16]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
4.  Terada T, Matsunaga Y. Increased mast cells in hepatocellular carcinoma and intrahepatic cholangiocarcinoma. J Hepatol. 2000;33:961-966.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 52]  [Cited by in F6Publishing: 55]  [Article Influence: 2.3]  [Reference Citation Analysis (0)]
5.  Wilkins BS, Buchan SL, Webster J, Jones DB. Tryptase-positive mast cells accompany lymphocytic as well as lymphoplasmacytic lymphoma infiltrates in bone marrow trephine biopsies. Histopathology. 2001;39:150-155.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 16]  [Cited by in F6Publishing: 17]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
6.  Hart PH, Grimbaldeston MA, Finlay-Jones JJ. Sunlight, immunosuppression and skin cancer: role of histamine and mast cells. Clin Exp Pharmacol Physiol. 2001;28:1-8.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 65]  [Cited by in F6Publishing: 58]  [Article Influence: 2.5]  [Reference Citation Analysis (0)]
7.  Terada T, Matsunaga Y. Increased mast cells in hepatocellular carcinoma and intrahepatic cholangiocarcinoma. J Hepatol. 2000;33:961-966.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 52]  [Cited by in F6Publishing: 55]  [Article Influence: 2.3]  [Reference Citation Analysis (0)]
8.  Sawatsubashi M, Yamada T, Fukushima N, Mizokami H, Tokunaga O, Shin T. Association of vascular endothelial growth factor and mast cells with angiogenesis in laryngeal squamous cell carcinoma. Virchows Arch. 2000;436:243-248.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 90]  [Cited by in F6Publishing: 85]  [Article Influence: 3.5]  [Reference Citation Analysis (0)]
9.  Johansson S, Landström M, Bjermer L, Henriksson R. Effects of tobacco smoke on tumor growth and radiation response of dunning R3327 prostate adenocarcinoma in rats. Prostate. 2000;42:253-259.  [PubMed]  [DOI]  [Cited in This Article: ]
10.  Takanami I, Takeuchi K, Naruke M. Mast cell density is associated with angiogenesis and poor prognosis in pulmonary adenocarcinoma. Cancer. 2000;88:2686-2692.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 3]  [Reference Citation Analysis (0)]
11.  Imada A, Shijubo N, Kojima H, Abe S. Mast cells correlate with angiogenesis and poor outcome in stage I lung adenocarcinoma. Eur Respir J. 2000;15:1087-1093.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 133]  [Cited by in F6Publishing: 145]  [Article Influence: 6.0]  [Reference Citation Analysis (0)]
12.  Tomita M, Matsuzaki Y, Onitsuka T. Correlation between mast cells and survival rates in patients with pulmonary adenocarcinoma. Lung Cancer. 1999;26:103-108.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 39]  [Cited by in F6Publishing: 41]  [Article Influence: 1.6]  [Reference Citation Analysis (0)]
13.  Elpek GO, Gelen T, Aksoy NH, Erdoğan A, Dertsiz L, Demircan A, Keleş N. The prognostic relevance of angiogenesis and mast cells in squamous cell carcinoma of the oesophagus. J Clin Pathol. 2001;54:940-944.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 115]  [Cited by in F6Publishing: 126]  [Article Influence: 5.5]  [Reference Citation Analysis (0)]
14.  Bowers HM, Mahapatro RC, Kennedy JW. Numbers of mast cells in the axillary lymph nodes of breast cancer patients. Cancer. 1979;43:568-573.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 1]  [Reference Citation Analysis (0)]
15.  Dabbous MK, Haney L, Nicolson GL, Eckley D, Woolley DE. Mast cell modulation of tumour cell proliferation in rat mammary adenocarcinoma 13762NF. Br J Cancer. 1991;63:873-878.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 34]  [Cited by in F6Publishing: 36]  [Article Influence: 1.1]  [Reference Citation Analysis (0)]
16.  Hultsch T, Brand P, Lohmann S, Saloga J, Kincaid RL, Knop J. Direct evidence that FK506 inhibition of FcepsilonRI-mediated exocytosis from RBL mast cells involves calcineurin. Arch Dermatol Res. 1998;290:258-263.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 16]  [Cited by in F6Publishing: 18]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
17.  Nakamura K, Tanaka T, Morita E, Kameyoshi Y, Yamamoto S. Enhancement of fibroblast-dependent mast cell growth in mice by a conditioned medium of keratinocyte-derived squamous cell carcinoma cells. Arch Dermatol Res. 1994;287:91-96.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 16]  [Cited by in F6Publishing: 16]  [Article Influence: 0.5]  [Reference Citation Analysis (0)]
18.  Wang X, Ruan Y, Wu Z. [Studies of mast cell-mediated cytotoxicity to hepatoma cells in vitro]. Zhonghua Zhongliu Zazhi. 1996;18:276-278.  [PubMed]  [DOI]  [Cited in This Article: ]
19.  Xu Y, Guo Z. [The number of lymph node with metastases influences survival in patients with cancer of the thoracic esophagus]. Zhonghua Zhongliu Zazhi. 2000;22:244-246.  [PubMed]  [DOI]  [Cited in This Article: ]
20.  Roder JD, Böttcher K, Busch R, Wittekind C, Hermanek P, Siewert JR. Classification of regional lymph node metastasis from gastric carcinoma. German Gastric Cancer Study Group. Cancer. 1998;82:621-631.  [PubMed]  [DOI]  [Cited in This Article: ]
21.  Lanza G, Gafà R, Decarli N. [Pathological factors involved in lymph node status determination in colorectal carcinoma: analysis of 166 cases with long-term follow-up]. Pathologica. 2001;93:631-639.  [PubMed]  [DOI]  [Cited in This Article: ]
22.  Nakajima Y, Nagai K, Miyake S, Ohashi K, Kawano T, Iwai T. Evaluation of an indicator for lymph node metastasis of esophageal squamous cell carcinoma invading the submucosal layer. Jpn J Cancer Res. 2002;93:305-312.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 35]  [Cited by in F6Publishing: 32]  [Article Influence: 1.5]  [Reference Citation Analysis (0)]
23.  Wong JH, Steinemann S, Tom P, Morita S, Tauchi-Nishi P. Volume of lymphatic metastases does not independently influence prognosis in colorectal cancer. J Clin Oncol. 2002;20:1506-1511.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 18]  [Cited by in F6Publishing: 16]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
24.  Rouzier R, Extra JM, Klijanienko J, Falcou MC, Asselain B, Vincent-Salomon A, Vielh P, Bourstyn E. Incidence and prognostic significance of complete axillary downstaging after primary chemotherapy in breast cancer patients with T1 to T3 tumors and cytologically proven axillary metastatic lymph nodes. J Clin Oncol. 2002;20:1304-1310.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 101]  [Cited by in F6Publishing: 100]  [Article Influence: 4.5]  [Reference Citation Analysis (0)]
25.  Katai H, Maruyama K, Sasako M, Sano T. Incidence of nodal metastasis around the superior border of the pancreas based on number of metastatic perigastric nodes. Gastric Cancer. 1998;1:115-117.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 13]  [Cited by in F6Publishing: 13]  [Article Influence: 0.5]  [Reference Citation Analysis (0)]
26.  Ichikura T, Morita D, Uchida T, Okura E, Majima T, Ogawa T, Mochizuki H. Sentinel node concept in gastric carcinoma. World J Surg. 2002;26:318-322.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 88]  [Cited by in F6Publishing: 97]  [Article Influence: 4.4]  [Reference Citation Analysis (0)]
27.  Lau WK, Blute ML, Bostwick DG, Weaver AL, Sebo TJ, Zincke H. Prognostic factors for survival of patients with pathological Gleason score 7 prostate cancer: differences in outcome between primary Gleason grades 3 and 4. J Urol. 2001;166:1692-1697.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 67]  [Cited by in F6Publishing: 67]  [Article Influence: 2.9]  [Reference Citation Analysis (0)]
28.  Sasatomi E, Finkelstein SD, Woods JD, Bakker A, Swalsky PA, Luketich JD, Fernando HC, Yousem SA. Comparison of accumulated allele loss between primary tumor and lymph node metastasis in stage II non-small cell lung carcinoma: implications for the timing of lymph node metastasis and prognostic value. Cancer Res. 2002;62:2681-2689.  [PubMed]  [DOI]  [Cited in This Article: ]
29.  Niemann TH, Yilmaz AG, Marsh WL, Lucas JG. A half a node or a whole node: a comparison of methods for submitting lymph nodes. Am J Clin Pathol. 1998;109:571-576.  [PubMed]  [DOI]  [Cited in This Article: ]
30.  Maurel J, Launoy G, Grosclaude P, Gignoux M, Arveux P, Mathieu-Daudé H, Raverdy N, Faivre J. Lymph node harvest reporting in patients with carcinoma of the large bowel: a French population-based study. Cancer. 1998;82:1482-1486.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in F6Publishing: 2]  [Reference Citation Analysis (0)]
31.  Dursun A, Poyraz A, Celik B, Akyol G. Expression of c-erbB-2 oncoprotein in gastric carcinoma: correlation with histopathologic characteristics and analysis of Ki-67. Pathol Oncol Res. 1999;5:104-106.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 14]  [Cited by in F6Publishing: 15]  [Article Influence: 0.6]  [Reference Citation Analysis (0)]
32.  Aoyagi K, Kohfuji K, Yano S, Murakami N, Miyagi M, Takeda J, Shirouzu K. Evaluation of the epidermal growth factor receptor (EGFR) and c-erbB-2 in superspreading-type and penetrating-type gastric carcinoma. Kurume Med J. 2001;48:197-200.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 17]  [Cited by in F6Publishing: 19]  [Article Influence: 0.9]  [Reference Citation Analysis (0)]
33.  Oshima CT, Lanzoni VP, Iriya K, Forones NM. C-erbB-2 oncoprotein in gastric carcinoma: correlation with clinical stage and prognosis. Int J Biol Markers. 2001;16:250-254.  [PubMed]  [DOI]  [Cited in This Article: ]
34.  Xin Y, Li XL, Wang YP, Zhang SM, Zheng HC, Wu DY, Zhang YC. Relationship between phenotypes of cell-function differentiation and pathobiological behavior of gastric carcinomas. World J Gastroenterol. 2001;7:53-59.  [PubMed]  [DOI]  [Cited in This Article: ]
35.  Noda H, Maehara Y, Irie K, Kakeji Y, Yonemura T, Sugimachi K. Increased proliferative activity caused by loss of p21(WAF1/CIP1) expression and its clinical significance in patients with early-stage gastric carcinoma. Cancer. 2002;94:2107-2112.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 11]  [Cited by in F6Publishing: 16]  [Article Influence: 0.7]  [Reference Citation Analysis (0)]
36.  Tao K, Chen D, Tian Y, Lu X, Yang X. The relationship between apoptosis and the expression of proliferating cell nuclear antigen and the clinical stages in gastric carcinoma. J Tongji Med Univ. 2000;20:222-224.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 3]  [Cited by in F6Publishing: 3]  [Article Influence: 0.1]  [Reference Citation Analysis (0)]
37.  Konno S, Takebayashi Y, Aiba M, Akiyama S, Ogawa K. Clinicopathological and prognostic significance of thymidine phosphorylase and proliferating cell nuclear antigen in gastric carcinoma. Cancer Lett. 2001;166:103-111.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 22]  [Cited by in F6Publishing: 27]  [Article Influence: 1.2]  [Reference Citation Analysis (0)]