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Subsite distribution of gastric cancer in an area of high prevalence--northwest Iran.
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MedLine Citation:
PMID:  19542688     Owner:  NLM     Status:  MEDLINE    
BACKGROUND: The aim of the present study was to determine subsites of gastric cancer in East Azerbaijan, Iran-a high incidence region for gastric cancer and Helicobacter pylori infection.
METHODS: Data were collected from 2002 through 2007 from patients who sought treatment for gastrointestinal symptoms or signs at a university clinic and subsequently underwent upper gastrointestinal endoscopy.
RESULTS: Cancer was diagnosed and histologically confirmed in 362 patients (352 adenocarcinomas). The mean age of the patients was 64.57 +/- 11.32 (range, 16-94 years) and the male-to-female ratio was 2.8:1. The gastric cardia was involved in 40.3% of patients with gastric adenocarcinoma, while the gastric fundus was involved in 3.7%, the gastric body in 49.1%, and the gastric antrum in 24.1% of patients. Complete evaluation for metastasis was possible in 144 patients; 61 were free of metastasis, and most of these patients underwent surgical therapy. Cardia involvement was not associated with the sex or age of patients.
CONCLUSIONS: Noncardia gastric cancer is still more frequent in East Azerbaijan, which is likely due to the very high prevalence of infection with Helicobacter pylori. The low rate of cancer involving the fundus is a target for further research on the etiology of gastric cancer.
Yousef Bafandeh; Sara Farhang
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Publication Detail:
Type:  Journal Article     Date:  2009-06-20
Journal Detail:
Title:  Journal of epidemiology / Japan Epidemiological Association     Volume:  19     ISSN:  1349-9092     ISO Abbreviation:  J Epidemiol     Publication Date:  2009  
Date Detail:
Created Date:  2009-07-06     Completed Date:  2009-08-14     Revised Date:  2014-05-27    
Medline Journal Info:
Nlm Unique ID:  9607688     Medline TA:  J Epidemiol     Country:  Japan    
Other Details:
Languages:  eng     Pagination:  202-5     Citation Subset:  IM    
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MeSH Terms
Adenocarcinoma / epidemiology*
Aged, 80 and over
Cross-Sectional Studies
Esophagogastric Junction
Gastric Fundus
Helicobacter Infections / epidemiology
Helicobacter pylori
Iran / epidemiology
Linitis Plastica / epidemiology
Middle Aged
Pyloric Antrum
Stomach Neoplasms / epidemiology*
Young Adult

From MEDLINE®/PubMed®, a database of the U.S. National Library of Medicine

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Journal Information
Journal ID (nlm-ta): J Epidemiol
Journal ID (iso-abbrev): J Epidemiol
Journal ID (publisher-id): JE
ISSN: 0917-5040
ISSN: 1349-9092
Publisher: Japan Epidemiological Association
Article Information
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© 2009 Japan Epidemiological Association.
Received Day: 23 Month: 5 Year: 2008
Accepted Day: 25 Month: 3 Year: 2009
Electronic publication date: Day: 5 Month: 7 Year: 2009
epreprint publication date: Day: 20 Month: 6 Year: 2009
collection publication date: Year: 2009
Volume: 19 Issue: 4
First Page: 202 Last Page: 205
PubMed Id: 19542688
ID: 3924110
DOI: 10.2188/jea.JE20080044
Publisher Id: JE20080044

Subsite Distribution of Gastric Cancer in an Area of High Prevalence—Northwest Iran Alternate Title:Subsite Distribution of Gastric Cancer
Yousef Bafandeh1
Sara Farhang2
1Professor of Gastroenterology and Hepatology Liver and Gastrointestinal Diseases Research Center Tabriz University of Medical Sciences, Tabriz, Iran
2General practitioner, Liver and Gastrointestinal Diseases Research Center Tabriz University of Medical Sciences, Tabriz, Iran
Correspondence: Address for correspondence. Dr. Sara Farhang, Liver and Gastrointestinal Diseases Research Center, Imam Reza Hospital Golgasht Ave, Tabriz, East Azerbaijan, Iran (e-mail:


Gastric adenocarcinoma is the second leading cause of cancer-related mortality in the world.1 Although the incidences of adenocarcinomatous and nonadenocarcinomatous noncardia gastric cancer have decreased, the incidence of adenocarcinoma of the gastric cardia has increased in most developed countries.25 Differences in the etiology of stomach cancers at these 2 subsites (cardia vs noncardia) may explain these conflicting trends in incidence. Noncardia gastric cancer is associated with Helicobacter pylori (H pylori)-induced atrophic gastritis,6 while cardia cancer is not associated with colonization of H pylori and the level of acid secretion remains normal.7

Data on trends in gastric adenocarcinoma are lacking in developing countries. The high ratio of distal versus proximal gastric adenocarcinoma did not change in Turkey during the last decade of the 20th century,8 which is due to the fact that H pylori infection is the essential causal factor in noncardia gastric adenocarcinoma.9 This underscores the role of H pylori in the epidemiology of the disease in developing countries.

In Iran, cancer of the stomach is the most common cancer of the gastrointestinal tract and its incidence is high in the region of Azerbaijan, in northwest Iran.10,11 Moreover, the prevalence of infection with H pylori, which is known to be involved in the development of gastric adenocarcinoma,12,13 is more than 85% in the adult population of this region.14 No data are available on the epidemiology of gastric cancer in this population. Such data would reveal the leading causes and ideal interventions for this common and frequently fatal cancer.

We hypothesized that the characteristics of etiologic factors in this population (including dietary habits and the high prevalence of H pylori) result in a subsite distribution of gastric cancer that lies between those observed in Asian and Western countries. We therefore conducted a detailed assessment of gastric cancer tumor subsites in patients from East Azerbaijan.


We studied patients who presented to the referral clinic of Tabriz Medical University and required upper gastrointestinal endoscopy for a chief complaint, or alarming signs or symptoms, related to the gastrointestinal tract. In the period from January 2002 through December 2007, all such patients with endoscopically diagnosed gastric cancer that was subsequently confirmed by histopathology were recruited for the study. The study was approved and supported by the liver and gastrointestinal diseases research center.

Gastroesophageal junction cases were defined as those with cancer originating at the anatomic junction of the esophagus and the stomach. Cardia cases were those with cancer originating within the first 5 cm of gastric mucosa distal to the gastroesophageal junction.15 Cancer diagnoses involving more than 1 site were also included in the analysis.

Statistical comparisons were made by the univariate chi-square test or logistic regression for nominal variables and by the independent samples t-test or ANOVA for difference of means. The P value was set at 0.05 for statistical significance.


During the period of this cross-sectional study, a diagnosis of cancer was confirmed by histopathology of endoscopic biopsies from 362 patients. The participants included 267 men (73.8%) and 95 women (26.2%). Mean age (SD) of patients at initial diagnosis was 64.9 (11.4) in men and 63.5 (10.9) in women (P = 0.319).

Distribution of patients’ complaints were as follows: epigastric pain (58.0%), dysphagia (36.1%), vomiting (26.7%), anorexia (6.3%), upper gastrointestinal tract bleeding (14.9%), weight loss (15.1%), unexplained anemia (2.2%), previous partial gastrectomy for peptic ulcer disease (0.8%), determining origin of a metastasis (0.8%), family history of gastric cancer (0.2%), and hiccups (0.2%).

At the time of initial diagnosis 144 patients were fully evaluated for possible metastasis: 61 (42.3%) had no evidence of metastasis. Surgical resection was possible in 56 (15.5%) patients with gastric cancer, while 11 (3.0%) received chemotherapy and 111 (30.7%) underwent palliative interventions.

Among 362 patients with gastric cancer, 8 had malignant lymphoma, 1 had a gastrointestinal stromal tumor, and 1 had a carcinoid tumor. Age and sex distribution, as well as gastric adenocarcinoma tumor subsite, are shown in the Table. The mean age (SD) of patients at initial diagnosis was 65.1 (11.1) years in men and 63.8 (10.9) years in women (P = 0.358).

Cardia involvement (including cancers involving multiple regions) was observed in 39.2% of patients with gastric cancer, and in 40.3% of patients with gastric adenocarcinoma. No significant difference in the distribution by sex was noted: cardia involvement was observed in 104 of 261 males and in 38 of 91 females (P = 0.749). Patients with and without cardia involvement also did not differ by age (P = 0.808).

Involvement of the fundus was uncommon (4.1% of all gastric cancer patients). It was observed in 0.7% of cases of adenocarcinoma of the cardia and in 5.6% of noncardia cases. There was no association between fundus involvement and either the sex (12/261 males and 1/91 females, P = 0.299) or age (P = 0.554) of the patients.

Metastasis was present in 60.4% of patients with adenocarcinoma of the cardia and in 59.1% of noncardia cases (P = 0.880). The age and sex of patients with metastasis at initial diagnosis (mean [SD], 64.2 [10.7]; 71.6% male) did not differ from those of patients without metastasis (60.9 [11.1], 72.7% male) (P = 0.085 for age, and P = 0.889 for sex). Surgery was performed for 85.7% (48) of patients without metastasis, 2.5% (2) of patients with metastasis, and 14% (6) of patients without known metastasis, but whose evaluation for metastasis was not complete.


In many countries the incidence of esophageal cancer has increased in recent decades, while the incidence of gastric cancer has declined.16 However, an increasing trend in adenocarcinoma of the gastric cardia and esophagus has been reported in many European countries.17 This pattern has not been observed worldwide. Xiaocheng et al found that most upper gastrointestinal tract cancers among American Asian/Pacific Islanders were noncardia adenocarcinomas.18

The incidence of upper gastrointestinal tract cancers in Iran differs from that in Western countries—gastric cancer is the most frequent in Iran.10 We have previously noted a low incidence of Barrett esophagus—a precancerous lesion of the esophagus19—and a low incidence of esophageal adenocarcinoma20 in this region.

The present study reveals that noncardia gastric cancer in East Azerbaijan, Iran is more common than involvement of the cardia, which was seen in 39.2% (41.3% of adenocarcinomatous cancers) of participants. Interestingly, the ratio of gastric cancers originating from the gastric fundus is very low in this population (4.1%). Such a pattern may be due to both luminal factors and the high prevalence of H pylori infection.

The association between the colonization of H pylori in the stomach and gastric adenocarcinoma may depend on the anatomic subsite.21 Although currently there is no consensus,22H pylori colonization is considered by some to be a strong risk factor for noncardia gastric cancer; however, it may be inversely associated with the risk of cancer of the gastric cardia.23 In 1 meta-analysis, the odds ratio for developing gastric noncardia vs cardia adenocarcinoma was 6.0, regardless of histologic subtype.24 The 85% prevalence of H pylori infection in the East Azerbaijan population14 probably explains the higher incidence of noncardia cancer in the present study.

A positive association has been described between intake of total, red, and processed meat and the risk of gastric noncardia cancer.25 This has been explained in part by a dose–response relation between red meat intake and endogenous formation of N-Nitroso compounds.26 There is growing evidence of an association between the Western diet (high intakes of processed meat, red meat, sweets, and high-fat dairy) and an increased risk of gastric cardia adenocarcinoma.27 Further comprehensive studies concerning changes in the eating habits of the Iranian population and gastric cancer patterns are required.

Regardless of the overall incidence of gastric cancer, the fraction of cardia involvement in different populations seems to follow a pattern. Gastric cardia cancer represents a low fraction (2.8%) of gastric cancers in East Asia,28 but an increasing trend has been reported in high-risk areas.29 In contrast, the rate has increased (up to 87%) in Western communities.30 Adenocarcinoma of the gastric cardia accounted for only 11% of gastric cancers in males and 6% in females among American Asian/Pacific islanders.18 In the present study, involvement of the cardia was observed in almost 40% of the patients, which is an intermediate rate. These results support our hypotheses about cardia cancers in East Azerbaijan. The relation of adenocarcinoma of the esophagus and gastroesophageal junction to gastroesophageal reflux disease is well established31; reports suggest an increase in the prevalence of gastroesophageal reflux disease in Iran.32,33

Because no published data on trends in cardia and noncardia gastric cancer among our population are available to clarify whether rates of these cancers are increasing, further investigation is required, as is the case with other high-incidence areas.

A limitation of this study was the use of a sample of patients who visited our university hospital. Although this hospital is the referral center for patients with gastrointestinal tract diseases in our area, we cannot prove that study participants were representative of gastric cancer patients in the general population of the region.

In conclusion, noncardia cancer is still the dominant subsite of gastric cancer in East Azerbaijan, which is most likely due to the very high prevalence of H pylori infection in the region. Additional studies of gastric cancer trends, particularly with respect to cancer subsite, would be most informative. In particular, the low ratio of cancer originating in the fundus is an obvious target for further research on the etiologic factors of gastric cancer.

1. Parkin DM, Mujer CS, Whelan SL. Cancer incidence in five continents. Vol. 6. Lyon: IARC Scientific Publication: 1992.
2. HanssonLE , SparenP , NyrenOIncreasing incidence of carcinoma of the gastric cardia in Sweden from 1970 to 1985 . Br J Surg. Year: 1993;80(3):374–710.1002/bjs.18008003388472157
3. LockeGR , TalleyNJ , CarpenterHA , HarmsenWS , ZinsmeisterAR , MeltonLJChanges in the site- and histology-specific incidence of gastric cancer during a 50 year period . Gastroenterology. Year: 1995;109(6):1750–610.1016/0016-5085(95)90740-87498638
4. PowellJ , McConkeyCC , GillisonEW , SpychalRTContinuing rising trend in oesophageal adenocarcinoma . Int J Cancer. Year: 2002;102(4):422–710.1002/ijc.1072112402314
5. BlaserMJ , SaitoDContinuing rising trend in oesophageal adenocarcinoma . Eur J Gastroenterol Hepatol. Year: 2002;14:107–1310.1097/00042737-200202000-0000311981333
6. UemuraN , OkamotoS , YamamotoS , MatsumuraN , YamaguchiS , YamakidoM , et al. Helicobacter pylori infection and the development of gastric cancer . N Engl J Med. Year: 2001;345:784–910.1056/NEJMoa00199911556297
7. KikuchiSEpidemiology of Helicobacter pylori and gastric cancer . Gastric Cancer. Year: 2002;5:6–1510.1007/s10120020000112021854
8. BorS , VardarR , OrmeciN , MemikF , SuleymanlarI , OguzD , et al. Prevalence patterns of gastric cancers in Turkey: Model of a developing country with high occurrence of Helicobacter pylori . J Gastroenterol Hepatol. Year: 2007;22:2242–510.1111/j.1440-1746.2006.04737.x18031388
9. FockKM , TalleyN , MoayyediP , HuntR , AzumaT , SuganoK , et al. Asia-Pacific consensus guidelines on gastric cancer prevention . J Gastroenterol Hepatol. Year: 2008;23(3):351–6510.1111/j.1440-1746.2008.05314.x18318820
10. SomiMH , FarhangS , MirinezhadSK , NaghashiS , Sief-FarshadM , GolzariMCancer in East Azerbaijan, Iran: Results of a Population-based Cancer Registry . Asian Pac J Cancer Prev. Year: 2008;9:327–3018712985
11. SomiMH , MirinezhadK , FarhangS , JazayeriE , SaniA , Seif-FarshadiM , et al. Gastrointestinal cancer occurrence in East Azerbaijan: a five year study from North Western Iran . Asian Pac J Cancer Prev. Year: 2006;7(2):309–1216839228
12. PisaniP , ParkinDM , MunozN , FerlayJCancer and infection: estimates of the attributable fraction in 1990 . Cancer Epidemiol Biomarkers Prev. Year: 1997;6:387–4009184771
13. WuAH , CrabtreeJE , BernsteinL , HawtinP , CockburnM , TsengCC , et al. Role of Helicobacter pylori CagA+ strains and risk of adenocarcinoma of the stomach and esophagus . Int J Cancer. Year: 2003;103(6):815–2110.1002/ijc.1088712516104
14. MikaeliJ , MalekzadehR , Ziad-AlizadehB , Nasseri-MogaddamS , ValizadehM , KhonchehR , et al. Prevalence of Helicobacter pylori in two Iranian provinces with high and low incidence of gastric carcinoma . Arch Iran Med. Year: 2000;3:6–9
15. SiewertJR , FeithM , SteinHJBiological and clinical variations of adenocarcinoma at the esophago-gastric junction relevance of a topographic subclassification . J Surg Oncol. Year: 2005;90:139–4610.1002/jso.2021815895452
16. Coleman MP, Esteve JP, Damiecki P, Arslan A, Renard H. Trends in cancer incidence and mortality. IARC scientific publications. Lyon: IARC Scientific Publication: 1993.
17. BotterweckAA , SchoutenLJ , VolovicsA , DorantE , van den BrandtPATrends in incidence of adenocarcinoma of the oesophagus and gastric cardia in ten European countries . Int J Epidemiol. Year: 2000;29:645–5410.1093/ije/29.4.64510922340
18. WuX , ChenVW , RuizB , AndrewsO , SuLJ , CorreaPIncidence of esophageal and gastric carcinoma among American Asian/Pacific Islanders, whites and blacks: subsite and histology differences . Cancer. Year: 2006;106(3):683–9210.1002/cncr.2154216388522
19. BafandehY , EsmailiH , AharizadSEndoscopic findigs in Iranian patients with heart burn . Indian J Gastroenterol. Year: 2005;24:236–816424617
20. BafandehY , HashemzadehS , SokoutiM , EsmailiHClinicopathologic characteristics of esophageal cancer patients in Northwest of Iran- very low incidence of Adenocarcinomas . Asian Pac J Cancer Prev. Year: 2006;7:480–217059350
21. Helicobacter and Cancer Collaborative GroupGastric cancer and Helicobacter pylori: a combined analysis of 12 case control studies nested within prospective cohorts . Gut. Year: 2001;49:347–5310.1136/gut.49.3.34711511555
22. LimburgP , QiaoY , MarkSD , WangG , Perez-PerezGI , BlaserM , et al. Helicobacter pylori Seropositivity and Subsite-Specific Gastric Cancer Risks in Linxian, China . J Natl Cancer Inst. Year: 2001;93:226–3310.1093/jnci/93.3.22611158192
23. KamangarF , DawseySM , BlaserMJ , Perez-PerezGI , PietinenP , NewschafferCG , et al. Opposing Risks of Gastric Cardia and Noncardia Gastric Adenocarcinomas Associated With Helicobacter pylori Seropositivity . J Natl Cancer Inst. Year: 2006;98(20):1445–5217047193
24. HuangJQ , SridharS , ChenY , HuntRHMeta-analysis of the relationship between Helicobacter pylori seropositivity and gastric cancer . Gastroenterology. Year: 1998;114:1169–7910.1016/S0016-5085(98)70422-69609753
25. GonzálezCA , JakszynP , PeraG , AgudoA , BinghamS , PalliD , et al. Meat Intake and Risk of Stomach and Esophageal Adenocarcinoma Within the European Prospective Investigation Into Cancer and Nutrition (EPIC) . J Natl Cancer Inst. Year: 2006;98(5):345–5416507831
26. BinghamSA , HughesR , CrossAJEffect of white versus red meat on endogenous N-nitrosation the human colon and further evidence of a dose response . J Nutr. Year: 2002;132:3522S–5S12421881
27. BahmanyarS , YeWDietary patterns and risk of squamous-cell carcinoma and adenocarcinoma of the esophagus and adenocarcinoma of the gastric cardia: a population-based case-control study in Sweden . Nutr Cancer. Year: 2006;54(2):171–810.1207/s15327914nc5402_316898861
28. MaedaH , OkabayashiT , NishimoriI , SugimotoT , NamikawaT , DabanakaK , et al. Clinicopathologic features of adenocarcinoma at the gastric cardia: is it different from distal cancer of the stomach?J Am Coll Surg. Year: 2008;206(2):306–1010.1016/j.jamcollsurg.2007.06.30618222384
29. HeYT , HouJ , ChenZF , QiaoCY , SongGH , MengFS , et al. Trends in incidence of esophageal and gastric cardia cancer in high-risk areas in China . Eur J Cancer Prev. Year: 2008 Apr;17(2):71–610.1097/CEJ.0b013e3282b6fd9718287862
30. WilkinsonNW , HoweJ , GayG , Patel-ParekhL , Scott-ConnerC , DonohueJDifferences in the pattern of presentation and treatment of proximal and distal gastric cancer: results of the 2001 gastric patient care evaluation . Ann Surg Oncol. Year: 2008;15(6):1644–5010.1245/s10434-008-9877-218392661
31. EngelLS , ChowWH , VaughanTL , GammonMD , RischHA , StanfordJL , et al. Population attributable risks of esophageal and gastric cancers . J Natl Cancer Inst. Year: 2003;95:1404–1313130116
32. SomiMH , FarhangS , MirinezhadK , JazayeriE , Nasseri-MoghaddamS , MoayeriS , et al. Prevalence and precipitating factors of gastroesophageal reflux disease in a young population of Tabriz, Northwest of Iran . Saudi Med J. Year: 2006;27(12):1878–8117143368
33. NouraieM , RazjouyanH , AssadyM , MalekzadehR , Nasseri-MoghaddamSEpidemiology of gastroesophageal reflux symptoms in Tehran, Iran: a population-based telephone survey . Arch Iran Med. Year: 2007;10(3):289–9417604463

[TableWrap ID: tbl01] Table.  Characteristics of gastric adenocarcinomas in Iranian patients
Site   No (%) of patients No (%) Female No (%) Male Mean (SD) age
Proximal Gastroesophageal junction and cardia 26 (7.4) 9 (9.9) 17 (6.5) 64.9 (10.5)
  Gastric cardia 67 (19.0) 16 (17.6) 51 (19.5) 64.8 (11.6)
  Gastric fundus 8 (2.3) 1 (1.1) 7 (2.7) 63.5 (9.9)
  Cardia and fundus 1 (0.1) 0 1 (0.4) 65
Middle Gastric body 121 (34.4) 26 (28.6) 95 (36.4) 64.3 (11.3)
Distal Gastric antrum 77 (21.9) 25 (27.5) 52 (19.9) 65.6 (12.1)
Diffuse Cardia and body 44 (12.5) 13 (14.3) 31 (11.9) 66.2 (7.6)
  Body and antrum 4 (1.1) 1 (1.1) 3 (1.1) 62.0 (11.7)
  Linitis plastica (Diffuse) 4 (1.1) 0 4 (1.5) 61.2 (12.2)
  Total 352 (100) 91 (100) 261 (100) 64.86 (10.9)

Article Categories:
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Keywords: Key words: gastric cancer, subsite, gastric cardia, Iran.

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