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Mucin expression in gastric cancer: reappraisal of its clinicopathologic and prognostic significance.

Gastric cancer, which is one of the most prevalent malignancies worldwide, is usually divided into 2 groups based on the tendency of gland formation: intestinal (or differentiated) and diffuse (or undifferentiated). (1,2) The morphologic classification of gastric cancers--intestinal (or differentiated) and diffuse (or undifferentiated)--is confusing, with expression of a gastric phenotype in intestinal"-type cancers and intestinal phenotypic mucin expression associated with diffuse" adenocarcinomas. (3) Mucins, which are a group of complex and diverse highly glycosylated extracellular proteins, are the major component of the mucus gel covering stomach mucosa. (4) Recently, immunohistochemistry specific to various mucins (MUC1, MUC2, MUC3, MUC4, MUC5AC, MUC5B, MUC6, MUC7, and MUC8) has been used to evaluate the mucin phenotypes of gastric cancer. (5-13) Of these mucin markers, MUC5AC, MUC2, MUC6, and CD10 are generally used to classify gastric cancers. CD10 is used to detect the brush border of intestinal-typed cells. MUC5AC and MUC6 are markers of gastric foveolar cells and antral/cardiac mucous glandular cells, respectively, and they reflect gastric phenotypes. MUC2 and CD10 exhibit the typical intestinal epithelial cell phenotype, decorating goblet cells and the brush border of intestinal absorptive epithelial cells, respectively. Interestingly, the correspondence between the morphology and mucin expression is controversial. Furthermore, the clinical validity of mucin expression in gastric cancer remains debated despite many attempts to investigate the clinicopathologic and prognostic significance of the mucin immunophenotype of gastric cancer. (5-13) Although there are several reports demonstrating a correlation between mucin expression and prognosis in gastric cancers, controversies or conflicting results have been published. For example, several investigators report that a gastric mucin phenotype is a poor prognostic indicator, whereas other reports indicate the intestinal mucin phenotype to be associated with a worse outcome or to have no correlation with survival. (5-13) With this information in hand, we tried to elucidate the precise clinicopathologic and prognostic importance of mucin expression in 412 gastric cancer patients.


Tumor Samples and Patient Population

We studied a cohort of 412 gastric cancer patients who underwent gastrectomy with lymph node dissection at Pusan National University Hospital between 2005 and 2007. The group comprised 286 men and 126 women with a mean age of 58.5 years (range, 42-75 years). Standard formalin-fixed, paraffin-embedded sections were obtained from the Department of Pathology, Pusan National University Hospital, and the National Biobank of Korea, Pusan National University Hospital. The study was approved by the institutional review board. None of the patients received preoperative radiotherapy and/or chemotherapy. We assessed the several clinicopathologic factors (tumor site, gross appearance and size, histologic classification [ie, intestinal or diffuse], and lymphovascular invasion) according to the Korean standardized pathology report for gastric cancer (14) and the Japanese classification of gastric carcinoma, 3rd English edition, (15) and made staging (depth of invasion, lymph node status) based on the American Joint Committee on Cancer Staging Manual, 7th edition. (16) The clinical outcome of each patient was followed from the date of surgery to the date of death or March 1, 2011. The follow-up period ranged from approximately 1 to 74 months (average, 46.0 months). Cases lost to follow-up or with death from any cause other than gastric cancer were censored for the analysis of survival rates.

Immunohistochemical Staining for Mucin Phenotypes

Sections were dewaxed and rehydrated according to the standard procedure and washed with phosphate-buffered saline. For immunohistochemical staining, sections were heated in a 600-W microwave oven twice for 5 minutes in 0.01 M citrate buffer (pH 6.0). Sections were immersed in 3% [H.sub.2][O.sub.2] to quench endogenous peroxidase activity, and unspecified binding was blocked in 5% normal goat serum (0.1% bovine serum albumin in phosphate-buffered saline). Immunohistochemical staining was performed using the avidin-biotin peroxidase complex method with amino-ethylcarbazole as a chromogen, using the Vectastain ABC elite kit (Vector Laboratories, Burlingame, California) according to the manufacturer's instructions. Sections were counterstained with Mayer hematoxylin solution. Immunohistochemical staining was carried out with monoclonal antibodies against the mucin antigen (Table 1).

MUC5AC and MUC6 are markers of gastric foveolar cells and antral/cardiac mucous glandular cells, respectively, and they reflect gastric phenotypes (Figure 1, A and B). MUC2 and CD10 exhibit the typical intestinal epithelial cell phenotype, decorating goblet cells and the brush border of intestinal absorptive epithelial cells, respectively (Figure 1, C and D). Adenocarcinomas with at least 10% reactivity for each mucin gene antibody were identified as positive as previously reported. (7,8,13) Mucin phenotypes were further subdivided into gastric (only gastric mucin positive) and gastric-predominant gastrointestinal phenotypes and intestinal (only intestinal mucin positive) and intestinal-predominant gastrointestinal phenotypes and null type based on the combination of predominant patterns of MUC5AC, MUC2, MUC6, and CD10 staining according to Tsukashita et al. (17) We defined gastric cancer with gastric mucin predominant type (GC-GP) as gastric type plus gastric-predominant gastrointestinal phenotypes (gastric type + gastric-predominant gastrointestinal type) and gastric cancer with intestinal mucin predominant type (GC-IP) as intestinal type plus intestinal-predominant gastrointestinal phenotypes (intestinal type + intestinal-predominant gastrointestinal type) for comparison based on the predominant mucin expression.

Statistical Analysis

Clinicopathologic features were analyzed by Student t test, the [chi square] test, or Fisher exact test to test for differences among the mucin phenotypes. Cumulative survival plots were obtained using the Kaplan-Meier method, and significance was compared using the log-rank test. Prognostic factors were identified using the Cox regression stepwise method (proportional hazard model) adjusted for the patients' age, gender, tumor site, and morphologic type (intestinal versus diffuse). Statistical significance was set at P < .05. Statistical calculations were performed with SPSS version 10.0 for Windows software (SPSS Inc., Chicago, Illinois).


Clinicopathologic Significance of Mucin Expression in Gastric Cancer

Of the 412 specimens, 67.5% (278 of 412), 44.9% (185 of 412), 35.4% (146 of 412), and 20.6% (85 of 412) were positive for MUC5AC, MUC6, MUC2, and CD10, respectively (Figure 2, A through D). As shown in Table 2, 63.8% (262 of 412), 24.5% (102 of 412), and 11.7% (48 of 412) of gastric cancers were classified as having GC-GP, GC-IP, and null phenotypes, respectively, on the basis of the predominant pattern of mucin expression.

Mucin phenotype was significantly correlated with sex, size, depth of invasion, gross type, histologic type, and lymphovascular invasion. The men had more null phenotype than GC-GPs and GC-IPs (P = .004). The tumor size of GC-GPs was smaller (P = .04) than that of GC-IP and null phenotypes. Early gastric cancer (EGC; limited to the mucosa and submucosa) showed more GC-GPs than advanced gastric cancer (invasion into muscularis propria and beyond) (P = .01). Diffuse histologic type was more strongly associated with GC-GP than with GC-IP or null phenotypes (P = .02). In addition, the presence of lymphovascular emboli was more related to GC-IP and null phenotypes than to GC-GP phenotype (P = .001). Also, there was a tendency of more lymph node metastasis in the GC-IP and null phenotypes than the GC-GP phenotype (P = .09) (Table 2).

Survival of Gastric Cancer With Respect to Mucin Expression

In overall and advanced gastric cancers, the depth of invasion and nodal status were significantly associated with cumulative survival (P < .001) (Figures 3, A through C, and 4, A through C). Alternatively, there was no association between mucin phenotype and survival in the cases of overall gastric cancer (P= .41) or advanced cancers (P= .29).

In contrast, there was a significant correlation between mucin phenotype and survival in EGC (P= .02) (Figure 5, A through C). The GC-GPs showed longer survival rate than GC-IP (P = .01) and null phenotypes (P = .01) in EGC. Furthermore, MUC5AC-positive EGCs had a longer survival rate than MUC5AC-negative EGCs (P = .009) (Figure 6, A through C). The expression of MUC5AC was identified as an independent prognostic factor in EGC adjusted for age, sex, histologic classification, tumor location, depth of invasion, and lymph node metastasis in the Cox regression proportional hazard model (P = .045) (Table 3). Notably, there was no significant association between survival rate and the expression of other mucins (ie, MUC2, MUC6, CD10) or mucin phenotypes (data not shown).


The present study demonstrates that the expression of a gastric mucin phenotype (especially MUC5AC expression) is significantly associated with favorable outcome, and should be considered as a possible prognostic predictor in the gastric cancer, especially in the EGCs.

From the perspective of carcinogenesis, the mucin plays an important role in the development of neoplasm. Alterations in mucin expression or glycosylation of tumor cells control the local microenvironment, playing a role in invasion and metastasis of tumor cells. (4) In addition, mucins regulate the differentiation, proliferation, and tumor suppression of tumor cells. (4)

It has been reported that EGC exhibits a gastric mucin phenotype independently regarding the histologic type, whereas advanced gastric cancers have a higher tendency to express an intestinal phenotype. (18-20) In the present study, the gastric mucin phenotype was more commonly expressed in EGC whereas the intestinal phenotype was more common in advanced gastric cancer, which is concordant with previous reports. (18-20) In addition, Saito et al (21) revealed that small intestinal-type EGCs (<1 cm) commonly express gastric mucin but transform into more undifferentiated and intestinal phenotypes with progression. Taking into account previous reports and our study, we confirm that during the progression of gastric cancer, there is a frequent phenotypic switch, with a mucin intestinal phenotype being acquired in most gastric cancers.

The clinical and, particularly, the prognostic significance of the mucin immunophenotype of gastric cancers are debated (Table 4). Lee et al (6) reported that the mucin intestinal phenotype was associated with a significantly better prognosis. In contrast, Wakatsuki et al (7) found that the same immunophenotype was associated with a significantly worse prognosis and a higher rate of postoperative liver metastasis. Notably, many different antibodies have been used to evaluate mucin expression, as well as different cutoff values for the definition of mucin positivity, leading us to speculate that these differences are responsible for the inconsistent results.

Compared with previous findings, (5-13) no relationship was found in our study between survival and mucin phenotypes in overall gastric cancer or in the advanced cancer subgroup. Instead, there was a significant relationship solely in EGC; expression of a mucin gastric phenotype was associated with a longer survival rate in EGC. Furthermore, foveolar gastric mucin expression, for example MUC5AC, was also associated with longer survival. Concordant with other reports, depth of invasion and lymph node metastasis were noted as prognostic markers in our entire cohort and the advanced tumor subgroup. (16) However, in the EGCs of the present study, lymph node metastasis and depth of invasion (mucosa versus submucosa) were determined to be not predictive of outcome in EGC. Alternatively, retained MUC5AC expression was associated with extended survival in EGC, and this independently of the depth of invasion. It is noteworthy that in contrast to our results, Koseki et al (22) reported that in their experience, the expression of a gastric phenotype was associated with increased risk of lymph node metastasis among intestinal-type EGC. Yet, in contrast to these 2 reports and in agreement with our data, Wang et al (10) noted that in a series of 76 gastric cancers, MUC5AC expression was associated with a favorable prognosis. In addition, others have detected an increased number of genetic alterations in adenocarcinomas with an intestinal mucin phenotype compared with those with a gastric mucin phenotype. (23-24) For example, EGCs with an intestinal mucin phenotype have been shown to display more p53 and nuclear [beta]-catenin expression and undergo more frequent chromosomal alteration compared with those with a gastric mucin phenotype, suggesting a more aggressive behavior. And our findings suggest that MUC5AC expression can be used to predict outcomes in EGC. However, out study is not sufficient for ending conflicts about the relationship between the mucin phenotype and the gastric cancer prognosis. Because the reasons underlying these discrepancies are still undetermined, additional molecular and clinical studies are needed to sort out these results.

This study was supported by grant 0920050 from the National R&D Program for Cancer Control, Ministry for Health, Welfare and Family Affairs, Republic of Korea, and a clinical research grant from Pusan National University Hospital 2011.

Caption: Figure 1. Mucin expression in gastric mucosa. MUC5AC expression in gastric foveolar epithelial cells (A). MUC6 expression in antral mucous glands (B). MUC2 reactivity in goblet cells of intestinal metaplastic cells (C). CD10 positivity on the brush border of intestinal metaplastic cells (D) (original magnifications X200).

Caption: Figure 2. Mucin expression in gastric adenocarcinoma. MUC5AC-positive (A), MUC6-positive (B), MUC2-positive (C), and CD10-positive (D) gastric adenocarcinoma (original magnifications X200).

Caption: Figure 3. Overall survival rates for gastric cancer according to the depth of invasion in overall gastric cancer (A), early gastric cancer (B), and advanced gastric cancer (C). The survival rate was higher in early-stage gastric cancer. Abbreviations: M, mucosa; MP, muscularis propria; SE, serosa exposed; SM, submucosa; SS, subserosa.

Caption: Figure 4. Overall survival rates according to lymph node metastasis status for all gastric cancers (A), early gastric cancers (B), and advanced gastric cancers (C).

Caption: Figure 5. Overall survival rates for gastric cancer according to mucin phenotypes for all cancers (A), early gastric cancers (B), and advanced gastric cancers (C). The GC-GP phenotype showed longer survival rates compared with the GC-IP (P =.01) and null phenotypes (P = .01). Abbreviations: GC-IP, gastric cancer with intestinal mucin predominant; GC-GP, gastric cancer with gastric mucin predominant.

Caption: Figure 6. Overall survival rates for gastric cancer according to MUC5AC expression for all cancer (A), early gastric cancers (B), and advanced gastric cancers (C). MUC5AC(+) early gastric cancer demonstrated a longer survival rate than MUC5AC(-) lesions (P = .009).


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Dae Hwan Kim, MD, PhD; Nari Shin, MD; Gwang Ha Kim, MD, PhD; Geum Am Song, MD, PhD; Tae-Yong Jeon, MD, PhD; Dong-Heon Kim, MD, PhD; Gregory Y. Lauwers, MD; Do Youn Park, MD, PhD

Accepted for publication August 30, 2012.

From the Departments of Surgery (Drs D. H. Kim, Jeon, and D.-H. Kim), Pathology (Drs Shin and Park), and Internal Medicine (Drs G. H. Kim and Song), Pusan National University Hospital and Pusan National University School of Medicine and BioMedical Research Institute, Pusan National University Hospital, Busan, Korea; and the Department of Pathology, Massachusetts General Hospital and Harvard Medical School, Boston (Dr Lauwers).

The authors have no relevant financial interest in the products or companies described in this article.

Reprints: Do Youn Park, MD, PhD, Department of Pathology, Pusan National University Hospital and Pusan National University School of Medicine, 1-10 Ami-Dong, Seo-Gu, Busan 602-739, Korea (e-mail:

Table 1. Primary Antibodies Used in This Study (a)

Primary Antibody (Clone)    Dilution

MUC2 (CLH2)                   1:500
MUC5AC (CLH5)                 1:500
MUC6 (Ccp58)                  1:500
CD10 (56C6)                   1:100

(a) All antibodies are from Novocastra Laboratories, Newcastle, United

Table 2. Relationship Between Mucin Phenotypes With Clinicopathologic
Characteristics in Gastric Cancers

                                         Mucin Phenotypes
                      No. of
                      Cases          GC-GP                GC-IP

Age y                          58.5 [+ or -] 11.3   59.4 [+ or -] 10.4
  Male                 286            171                   72
  Female               126             91                   30
Tumor size, cm                 3.55 [+ or -] 0.15   4.21 [+ or -] 0.28
  Upper/middle         219            143                   55
  Lower                193            120                   46
Invasion depth
  M, SM                223            157                   44
  MP, SS, SE           189            106                   57
Gross type
  Elevated/flat/       283            189                   65
  Excavated            129             74                   36
Histologic type
  Intestinal +         251            147                   71
  Diffuse              161            116                   30
Perineural invasion
  Negative             278            182                   65
  Positive             134             81                   36
  Negative             259            183                   53
 Positive              153             80                   49
Lymph node
  metastasis (a)
  Negative             244            164                   57
  Positive             168             99                   44

                       Mucin Phenotypes

                             Null            P

Age y                 60.5 [+ or -] 13.3    .49
  Male                        43            .004
  Female                      5
Tumor size, cm        4.32 [+ or -] 0.43    .04
  Upper/middle                21            .38
  Lower                       27
Invasion depth
  M, SM                       22            .01
  MP, SS, SE                  26
Gross type
  Elevated/flat/              29            .16
  Excavated                   19
Histologic type
  Intestinal +                33            .02
  Diffuse                     15
Perineural invasion
  Negative                    31            .61
  Positive                    17
  Negative                    24            .001
 Positive                     24
Lymph node
  metastasis (a)
  Negative                    23            .09
  Positive                    25

Abbreviations: GC-GP, gastric cancer with gastric mucin predominant
type; GC-IP, intestinal type early gastric cancer with intestinal
mucin predominant type; M, mucosa; MP, muscularis propria;
SE, serosa; SM, submucosa; SS, subserosa.

(a) Compared between GC-GP versus GC-IP + null type.

Table 3. Multivariate Survival Analysis With Cox Regression Model in
Early Gastric Cancers

Variable                                B        SE

Age ([less than or equal to] 59       -1.401    0.798
  versus >59)
Sex (male versus female)               0.652    0.788
Site (upper and middle versus          0.378    0.622
Histologic type (intestinal versus     0.319    0.809
Depth of invasion (mucosa versus      -0.134    0.617
Lymph node metastasis (positive       -0.448    0.714
  versus negative)
MUC5AC (positive versus negative)      1.253    0.626

Variable                                  HR (95% CI)         P

Age ([less than or equal to] 59       0.246 (0.052-1.177)    .08
  versus >59)
Sex (male versus female)              1.920 (0.410-8.999)    .41
Site (upper and middle versus         1.460 (0.431-4.945)    .54
Histologic type (intestinal versus    1.376 (0.282-6.713)    .69
Depth of invasion (mucosa versus      0.875 (0.261-2.929)    .83
Lymph node metastasis (positive       0.639 (0.158-2.590)    .53
  versus negative)
MUC5AC (positive versus negative)     3.500 (0.026-11.937)   .045

Abbreviations: CI, confidence interval; HR, hazard ratio.

Table 4. Reported Datasets About Relationship Between Mucin
Expression and Survival in Gastric Cancer

Source, y              No.   Antibodies            Positivity, %

Present study          412   MUC5AC, MUC6,              10
                               MUC2, CD10
Toki et al, (5) 2010   95    MUC5AC, HGM, MUC6,          5
                               M-GGMC-1, MUC2,
Lee et al, (6) 2009    106   HGM, Con A, MUC2,           5
Wakatsuki et           97    MUC5AC, MUC6,              10
  al, (7) 2008                 MUC2, CD10
Lee et al, (8) 2007    150   MUC1, MUC5AC, MUC6,        10
                               MUC2, CD10
Wang et al,            76    MUC1, MUC5AC                5
  (10) 2003
Pinto-de-Sousa et      94    MUC5AC, MUC6,               5
  al, (12) 2002                MUC2, MUC1
Tajima et              136   HGM, MUC2,                 10
  al, (13) 2001                MUC6, CD10
Lee et al, (11) 2001   300   MUC5AC, MUC6,              20
                               MUC2, MUC1

Source, y              Phenotypes           Survival

Present study          GC-GP, GC-IP, null   GC-GP and MUC5AC(+) has
                                              good survival in EGC
Toki et al, (5) 2010   G, GI, I, U          No correlation
Lee et al, (6) 2009    G, GI, I, U          I phenotype has good
Wakatsuki et           G, GI, I, U          I phenotype has poor
  al, (7) 2008                                survival
Lee et al, (8) 2007    G, GI, I, U          G, GI phenotype have
                                              poor survival
Wang et al,            N/A                  Muc1(+)/Muc5AC(-) has
  (10) 2003                                   poor survival
Pinto-de-Sousa et      N/A                  No correlation
  al, (12) 2002
Tajima et              G, GI, I, U          G phenotype has poor
  al, (13) 2001                               survival
Lee et al, (11) 2001   N/A                  Muc1(+) has poor

Abbreviations: EGC, early gastric cancer; G, gastric mucin
phenotype; GC-GP, gastric cancer with gastric mucin predominant
type; GC-IP, intestinal type early gastric cancer with intestinal
mucin predominant type; GI, gastric-intestinal mucin phenotype;
HGM, human gastric mucin; I, intestinal mucin phenotype;
N/A, not assessed; U, unclassified mucin phenotype.


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Author:Kim, Dae Hwan; Shin, Nari; Kim, Gwang Ha; Song, Geum Am; Jeon, Tae-Yong; Kim, Dong-Heon; Lauwers, Gr
Publication:Archives of Pathology & Laboratory Medicine
Article Type:Report
Geographic Code:9SOUT
Date:Aug 1, 2013
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