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Prognostic value of ABO blood group in patients

with gastric cancer

Ye-Qiong Xu, MD,a,* Ting-Wang Jiang, PhD,b,* Yan-Hong Cui, MD,c

Yi-Lin Zhao, MD,c and Li-Qing Qiu, MDd

a Molecular Laboratory, Changshu Medicine Examination Institute, Suzhou, Jiangsu, Chinab Department of Flow Cytometry, Changshu Medicine Examination Institute, Suzhou, Jiangsu, Chinac Molecular Laboratory, Changshu Medicine Examination Institute, Changshu, Chinad

Laboratory Medicine, Dehua County Hospital, Quanzhou, China

a r t i c l e i n f o

Article history:

Received 8 June 2015

Received in revised form

26 October 2015

Accepted 28 October 2015

Available online 5 November 2015

Keywords:

ABO blood groupsGastric cancer

Prognosis

Survival

a b s t r a c t

Background: Previous studies have shown a link between the ABO blood groups and prog-

noses for several types of malignancies. However, little is known about the relationship

between the ABO blood groups and prognosis in patients with gastric cancer (GC). The aim

of this study was to investigate the prognostic performance of ABO blood groups in

patients with GC.

Methods: A total of 1412 GC patients who had undergone curative intent surgery between

January 2005 and January 2010 participated in the present study. A prognostic nomogram

was constructed to improve the predictive capacity for patients with gastrectomy using R

software, and its predictive accuracy was determined by the concordance index (c-index).Results: The median follow-up period of the 1412 GC patients was 44 mo with 809 alive.

Non-AB blood groups were associated with significantly decreased overall survival in GC

patients (hazard ratio ¼ 2.59; 95% confidence interval ¼ 1.74e3.86, P < 0.001), but patients in

the group AB had a better prognosis than those in the non-AB blood groups. Meanwhile,

group A had the worst prognosis among all the blood groups (hazard ratio ¼ 3.14;

95% confidence interval ¼ 2.09e4.72; P


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to local relapse or metastasis after gastrectomy. Hence, the

survival rate will be obviously improved if GC can be detected

at an early tumor stage [3]. Better understanding of the asso-

ciation of genetic factors and predisposing environmental

factors of GC could improve patients’ prognoses and provide

appropriate therapy strategies.

The ABO blood group system is the first genetic poly-

morphism discovered in humans in 1990 [4]. Blood groupantigens are chemical components on the erythrocyte

membrane, and they are expressed in various epithelial

cells, including lung and gastrointestinal cells, urothelium,

mucosa, saliva, and body fluids [5]. The gene of the ABO blood

groupson chromosome 9q34 encodesglycosyltransferases that

catalyze the transfer of nucleotide donor sugars to H

antigens and form ABO blood group antigens [6]. The antigens

of the ABO blood groups are conveyed on the surface of red

blood cells and other tissues. The correlations of ABO blood

groups with benign or malignant cancers have also been

extensively studied for a long time. Aird et al. [7] reported that

ABO bloodgroups were closely associated with GC, and groupA

was conspicuously more frequent in GC patients than normalindividuals.

Little is known about the connections between ABO blood

groups and clinical prognoses in patients with GC. Over the

past several decades, most studies have shed light on the

relationship between ABO blood groups and the risk of GC

[7e10]. However, the association of ABO blood groups with the

clinical prognosis of patients with gastrectomy remains

unclear. Herein, the aim of this study was to elucidate the

influence of ABO blood groups on the clinical outcomes of

patients with gastrectomy and construct a prognostic nomo-

gram to improve the predictive capacity for overall survival

(OS) in patients with GC based on the ABO blood groups and

clinicopathologic parameters.

2. Materials and methods

2.1. Patients

This study was a retrospective analysis, and all newly diag-

nosed GC patients were obtained from the Changshu Medicine

Examination Institute and Nanjing First Hospital (Jiangsu,

China) between January 2005 and January 2010. The diagnosis

of GC wasbased on histologic evidenceand classified according to the seventh edition of the TNM-UICC/AJCC classification

system (Washington, 2010) [11]. The inclusion criteria were as

follows: (1) patients with gastric adenocarcinoma who had

undergone subtotal or total gastrectomy with full D2

lymphadenectomy; (2) all enrolled patients did not receive

preoperative anticancer therapy, such as radiotherapy or neo-

adjuvant chemotherapy; (3) the postoperation expected life

expectancy was 3 mo; (4) there was no infection or infectious

and hematologic diseases at preoperation; and (5) informed

consent was obtained from the eligible patients. Finally, 1412

patients were enrolled in this study. This study was approved

by the Medical Ethics Committee of Changshu Medicine

Examination Institute and Nanjing First Hospital, Nanjing Medical University.

2.2. Follow-up

Each patient was followed up periodically until death or

January 2015 (every 3 mo for the first 2 y, and every 6 mo up

to the fifth year) after surgery. Endoscopy, physical exami-

nation, and laboratory tests were conducted at each visit.

The follow-up cycles varied from 3e60 mo, with a median

of 44 mo. The OS ranged from the date of surgery to death.The date of the last follow-up was applied to dropout

patients.

2.3. Evaluation of ABO blood groups and covariates

Rh factors (positive or negative) and ABO blood groups (A, B,

AB, or O) were collected for complete medical histories.

Herein, we examined Rh factors and ABO blood groups in the

peripheral sera of enrolled participants. These determinations

were carried out at Changshu Medicine Examination Institute

and Nanjing First Hospital.

Among all the patients with GC, 717 (50.8%) received

adjuvant chemotherapy at postoperation, but 695 (49.2%) didnot receive any chemotherapy due to chemoresistance,

oppressive side effects, and other causes. Radiotherapy was

not administered in the patients routinely.

2.4. Statistical analysis

Chi-square test was used to compare categorical variables.

The survival rates were evaluated by KaplaneMeier survival

analysis, and their significance was calculated by the log-rank

test. The predictors for OS tested by univariate analysis were

calculated by multivariate analysis using the Cox proportional

hazards model. The nomogram for OS was established using

R 3.0.3 software (Institute for Statistics and Mathematics,

Vienna, Austria). The predictive accuracy was calculated

by the Harrell’s concordance index (c-index). All the statistical

analyses were conducted using IBM SPSS 20.0 software (IBM,

Chicago, IL). A P value


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associated with sex (P ¼ 0.013), age (P < 0.001), Helicobacter

pylori infection (P ¼

0.025), grade (P ¼

0.037), chemotherapy(P ¼ 0.007), and CA724 (P ¼ 0.013).

3.2. Association between the clinical prognosis of GC

patients and ABO blood groups

The median follow-up period of the 1412 GC patients was

44 mo with 809 (57.3%) alive and 603 (42.7%) dead from

cancer-related diseases at the final clinical follow-up. The

ABO blood groups were closely associated with OS accord-

ing to the KaplaneMeier analysis. OS was longer in GC

patients with the group AB (median, 58 mo) than in those

with the group O (median, 43 mo), group B (median, 38 mo),

and group A (median, 30 mo; P < 0.001) as shown inFigure 1A. Furthermore, similar results were observed when

stratified by tumor stage (Fig. 1BeD; P < 0.001). In addition,

we evaluated the influence of the patients’ Rh, ABO bloodgroups, sex, age, H pylori status, Lauren classification, grade,

stage, depth of invasion, lymph node, chemotherapy,

CA199, and CA724 on OS by univariate analysis (Table 2).

The OS was significantly associated with the patients’ sex,

age, Lauren classification, grade, tumor stage, depth of in-

vasion, lymph node, chemotherapy, CA199, CA724, and ABO

blood groups (P < 0.05). Meanwhile, the significant param-

eters in univariate analysis were further analyzed in

multivariate analyses. The results showed that the ABO

blood groups were independent predictors for OS (group A:

hazard ratio [HR] ¼ 3.14, 95% confidence interval

[CI] ¼ 2.09e4.72; group B: HR ¼ 2.52, 95% CI ¼ 1.65e3.83;

group O: HR ¼ 2.06, 95% CI ¼ 1.35e3.15; and non-AB bloodgroups: HR ¼ 2.59, 95% CI ¼ 1.74e3.86; P < 0.001; Table 2).

Table 1 e Baseline patient characteristics according to ABO blood group.

Characteristictotal

Number of patients(%) 1412

O (%) 407 A (%) 516 B (%) 346 AB (%) 143 Non-AB (%) 1269 P*

Rh

Positive 1404 (99.4) 405 (99.5) 142 (99.6) 373 (99.1) 142 (99.3) 1262 (99.4) 0.715

Negative 8 (0.6) 2 (0.5) 2 (0.4) 3 (0.9) 1 (0.7) 7 (0.6)

Sex

Male 968 (68.6) 314 (77.1) 333 (64.5) 236 (68.2) 85 (59.4) 883 (69.6) 0.013

Female 444 (31.4) 93 (22.9) 183 (35.5) 110 (31.8) 58 (40.6) 386 (30.4)

Age

64 775 (54.9) 247 (60.7) 280 (54.3) 143 (41.3) 105 (73.4) 670 (52.8) 64 637 (45.1) 202 (39.3) 236 (45.7) 203 (58.7) 38 (26.6) 599 (47.2)

Hp

No 300 (21.2) 88 (21.6) 93 (18.0) 99 (28.6) 20 (18.8) 280 (22.1) 0.025

Yes 1112 (78.8) 319 (78.4) 423 (82.0) 247 (71.4) 123 (81.2) 989 (77.9)

Lauren

Intestinal type 453 (32.1) 131 (32.2) 168 (32.6) 101 (29.2) 53 (37.1) 400 (31.5) 0.379

Mixed type 326 (23.1) 101 (24.8) 102 (19.8) 94 (27.2) 29 (20.3) 297 (23.4)

Diffuse type 633 (44.8) 175 (43.0) 246 (47.7) 151 (43.6) 61 (42.7) 572 (45.1)

Grade

G1 282 (20.0) 83 (20.4) 90 (17.4) 71 (20.5) 38 (26.6) 244 (19.2) 0.037

G2e

G3 1130 (80.0) 324 (79.6) 426 (82.6) 275 (79.5) 105 (73.4) 1025 (80.8)Stagey

Ⅰ 339 (24.0) 97 (23.8) 123 (23.8) 84 (24.3) 35 (24.5) 304 (24.0) 0.849

Ⅱ 404 (28.6) 119 (29.2) 150 (29.1) 97 (28.0) 38 (26.6) 366 (28.8)

Ⅲ 669 (47.4) 191 (46.9) 243 (47.1) 165 (47.7) 70 (49.0) 599 (47.2)

Depth of invasion

T1 216 (15.3) 68 (16.7) 72 (14.0) 53 (15.3) 23 (16.1) 193 (15.2) 0.370

T2 372 (26.3) 107 (26.3) 139 (26.9) 82 (23.7) 44 (30.8) 328 (25.8)

T3eT4 824 (58.4) 232 (57.0) 305 (59.1) 211 (61.0) 76 (53.1) 748 (58.9)

Lymph node

N0 513 (36.3) 152 (37.3) 196 (38.0) 121 (35.0) 44 (30.8) 469 (37.0) 0.145

N1eN3 899 (63.7) 255 (62.7) 320 (62.0) 225 (65.0) 99 (69.2) 800 (63.0)

Chemotherapy

None 695 (49.2) 185 (45.5) 259 (50.2) 196 (56.6) 55 (38.5) 640 (50.4) 0.007

Adjuvant 717 (50.8) 222 (54.5) 257 (49.8) 150 (43.4) 88 (61.5) 629 (49.6)

CA199 (U/mL)37 766 (54.2) 214 (52.6) 281 (54.5) 186 (53.8) 85 (59.4) 681 (53.7) 0.189

>37 646 (45.8) 193 (47.4) 235 (45.5) 160 (46.2) 58 (40.6) 588 (46.3)

CA724 (U/mL)

6 801 (56.7) 233 (57.2) 286 (55.4) 187 (54.0) 95 (66.4) 706 (55.6) 0.013

>6 611 (43.3) 174 (42.8) 230 (44.6) 159 (46.0) 48 (33.6) 563 (44.4)

Hp ¼ Helicobacter pylori.* Differences between the blood group AB and non-AB blood groups were tested by chi-square test.y Tumor stage according to the seventh edition of the American Joint of Committee on Cancer.

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3.3. Prognostic nomogram for OS

A prognostic nomogram was developed to predict the survival

of GC patients after surgical resection using the seven inde-

pendent factors identified in the multivariate analysis

(Table 2). The nomogram was used by summing the points

identified on the top scale for each independent factor. This

total point score was then identified on the total points scale

to determine the probability of 3- and 5-y survival (Fig. 2).

The c-index for this nomogramwas 0.78 based on the fitted

multivariable Coxmodel. The calibration curve (Fig. 3) showed

how the predictions from the nomogram compared withactual outcomes for the 1412 patients. The dashed line

represented the performance of an ideal nomogram, in which

the predicted consequences perfectly matched with the actual

consequences. In addition, traditional AJCC stage groups and

nomogram predictions were compared for their ability to

distinguish among the patients by the c-index. Our con-

structed nomogram was superior to that of traditional AJCC

stage groups (c-index: 0.78 versus 0.69; P < 0.001).

4. Discussion

TheantigensoftheABObloodgroupshavebeeninvestigatedinthe development of malignancy in the past several decades.

Fig. 1 e KaplaneMeier survival curves for OS based on ABO blood type. (A) OS for the entire cohort of patients with gastric

cancer; (B) OS for tumor stage I patients with gastric cancer; (C) OS for tumor stage II patients with gastric cancer; and (D) OS

for tumor stage III patients with gastric cancer. (Color version of the figure is available online.)

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Previous research has found an obvious relationship between

the incidence of malignancies and ABO blood groups [12];

however, many investigations have shown different associa-

tions between ABO blood groups and GC patients [13,14].

However, few studies have explored the prognostic value of

ABOblood groupsin surgicalGC patients. Hence,our studywas

aimed to investigate the impact of ABO blood groups on the

clinical prognosis of 1412 GC patients who had undergone

gastrectomyandfirstattemptedtoestablishapredictivemodel

to improvethe predictive accuracyin patientswith surgicalGC.

A total of 1412 GC patients were enrolled in the retro-spective study. Our results indicated that non-AB blood

groups were associated with significantly decreased OS in GC

patients, but patients with group AB had a better prognosis

than those with non-AB blood groups. Meanwhile, group A

had the worst prognosis among all the blood groups

(HR ¼ 3.14; 95% CI ¼ 2.09e4.72; P 64 1.37 1.17e1.61


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patients typically undergo various heterogeneous treatments.

Herein, patients with stage Ⅳ disease were not evaluated inthe present study. Third, different numbers of samples could

induce a different impact of the ABO blood groups on prog-

nosis of GC patients. However, in the present study, there was

the higher prevalence of younger patients in the AB blood

group than the non-AB blood groups (median age: 61 versus 64

y). To explore the bias, we also investigated the influence of

blood group AB on GC development in 327 patients


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was first reported in 1863, explaining that the “lymphor-

eticular infiltrate” reflected original cancer at the sites of

chronic inflammation [23]. The influence of the inflammatory

microenvironment on malignancy has been supported by

emerging evidence over the past decades. Deeper under-

standing of the relationships between inflammation and

malignancies contributed to the treatment and prevention of

malignancies. These previous results have suggested thatchronic inflammation is closely related to tumor metastasis

and initiation and revealed that ABO blood groups could

impact the clinical prognosis in patients with cancer.

Nomograms have been developed in different cancers and

have been shown to be more accurate than conventional

staging systems for predicting prognosis in various cancers

[24e26]. Furthermore, nomograms have been validated to be

more accurate for predicting the disease-specific survival rate

of GC in Western countries by combining all the independent

prognostic factors and quantified risks [27e30]. A previous

study externally validated the Memorial Sloan Kettering

Cancer Center nomogram in predicting the probability of 5-

and 9-y disease-specific survival after R0 resection for GC. TheMemorial Sloan Kettering Cancer Center nomogram per-

formed well with good discrimination and calibration [31].

Therefore, the present study attempted to establish a predic-

tive nomogram to predict the probability of postoperative

patients who will die of cancer-related causes within 3 and 5 y

based on ABO blood groups and independent factors in

multivariate analyses. The nomogram performed well in

predicting OS, and the prediction was supported by the

c-index (0.78), a finding that was superior to that of the

traditional AJCC stage system (c-index: 0.69). All the results

supported that nomograms may forecast well the clinical

outcome in patients with GC at postoperation.

Some limitations of the retrospective study should be

acknowledged. First, in this study, some patients did not

undergo computed tomography or magnetic resonance

imaging of the chest and/or brain at diagnosis, and it is

possible that many patients had asymptomatic disease at the

time of primary treatment. Second, all the participants of our

study were Chinese, perhaps limiting the generalizability of

this result. Further investigations are urgently needed to

clarify our results, including the evaluation of different races

from other places. Third, there was a selection bias of younger

patients more likely to receive adjuvant chemotherapy than

patients >64 y in the AB versus non-AB groups; however, the

multivariate analysis showed that ABO blood groups wereindependent predictors for OS, particularly independent of

age and receipt of chemotherapy.

5. Conclusions

In conclusion, our data suggested an important link between

surgical GC survival and ABO blood groups. GC patients with

the group AB were more susceptible to show promising

prognostic significance than those with non-AB blood groups

(groups O, A, and B). GC patients with the blood group A had a

worse survival rate than those with the blood groups O, B, and

AB. Our constructed nomogram did well to predict the clinicalprognosis in patients with surgical GC.

Acknowledgment

This study was supported by the Science and Technology

Development Project of Changshu (201218, 201313, 201417).

Authors’ contributions: Y.-Q.X. conceived and designed the

experiments and wrote the article. Y.-Q.X., T.-W.J., and L.-Q.Q.

performed the experiments. Y.-H.C. analyzed the data. Y.-L.Z.contributed to the reagents/materials/analysis tools. Y.-Q.X.

and T.-W.J. designed the software used in analysis.

Disclosure

The authors declare that they have no competing interest.

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