Stomach cancer was a leading cancer cause of death early in the 20th century in the United States.¹ Both incidence and death rates for the disease declined steadily over the course of the last century in many high-income countries worldwide, including the United States.^2,3 The causes of the decline are not fully understood, but it has been postulated that improved living conditions, the widespread use of refrigerators, the decreased consumption of salt-preserved and smoked food, and the use of antibiotics, which may eradicate Helicobacter pylori from the stomach mucosa, account for part of this decline.⁴ Although incidence rates are now low in the United States, stomach cancer remains an important cause of morbidity and mortality in black, Asian and Pacific Islander, and American Indian/Alaska Native populations, with approximately 23,148 new cases and 11,261 new deaths from the disease expected in the United States in 2013, representing approximately 1.5% of all malignant neoplasms.³

The molecular biology of stomach cancer is complex and varies by site and histology. It is classified into several subsites within the stomach: cardia (roughly the top inch of the stomach), fundus, body, antrum, pylorus, and lesser or greater curvature.⁵ Most gastric tumors may be classified into 2 major histologic types: diffuse and intestinal.⁴ The incidence of gastric cardia cancer has remained stable or increased and is significantly higher among whites than blacks and among males, especially among whites, where the male-to-female ratio was 5:1.^5,6 Cardia carcinomas are most frequent among white males and lowest among females of all racial groups,⁵ and they have a poorer prognosis.^7,8 Non-cardia carcinoma incidence rates among blacks, Asians and Pacific Islanders, and American Indians/Alaska Natives were twice and triple those among whites, respectively,⁵ but the incidence has been dropping.^6,9

Disease stage at diagnosis is an important predictor of prognosis.¹⁰ As for most cancers, stomach cancers diagnosed at an early stage have more favorable survival than disease identified at distant stage.¹¹ However, stomach cancer symptoms are often non-specific, and the vast majority of incident stomach cancers in the United States are diagnosed at distant stage.¹²

Racial and ethnic differences in stomach cancer incidence and mortality rates have been well documented.^5,13,14 Previous research has highlighted racial differences in survival within the United States, with higher survival probabilities reported among whites than among blacks during 1988 through 2006.¹⁵ Differences in gastric cancer survival by country have also been observed.^10,15–17 The CONCORD-2 study established worldwide surveillance of cancer survival using data for over 25 million individuals diagnosed during the 15-year period 1995–2009, supplied by 279 population-based cancer registries in 67 countries.¹⁷ The CONCORD-2 study demonstrated that the 5-year, age-standardized net survival from stomach cancer in the United States was 29% between 2005 through 2009, having increased by 7% since the period 1995–1999.¹⁷ These estimates combined data for patients of all races and diagnosed at all stages. The objective of the current report was to use CONCORD-2 data to characterize differences in stomach cancer survival between whites and blacks in the United States by state and by disease stage at diagnosis. To our knowledge, this is the largest study to date, covering 80% of the US population, thus providing a baseline set of survival estimates just before implementation of the Affordable Care Act from 2010.

We present the results for all patients diagnosed with stomach cancer in the areas covered by the 37 registries in Tables 1, 2 and 3. Results by state are presented in Supporting Tables 1, 2, and 3. In total, 150,700 stomach cancers were diagnosed in the study population between 2001 and 2009: 76.2% were diagnosed in whites, and 15.4% were diagnosed in blacks (Table 1). Overall, for 2004 through 2009, 30.8% of these cancers were diagnosed at a distant stage, 28.8%at regional, 24.9%were localized, and the remaining cancers (15.4%) were of unknown stage. Differences in the proportions of each stage by race between 2004 through 2009 were ≤1%. Case counts by state over the 9-year period as indicated in Supporting Table 1, ranged from a minimum of 227 (Wyoming) to a maximum of 23,247 (California).

Absolute changes in 5-year age-standardized net survival between 2001 through 2003 and 2004 through 2009 by US geographic region and state are illustrated in Figure 1. For all states combined, there was an increase of 2.9% in 5-year age-standardized net survival between these 2 periods. Although age-standardized 5-year net survival increased in 29 of the 37 states, the pooled survival estimate for all 37 states combined was low for both periods (26.1% and 29%, respectively) (Fig. 1).

The 1-year, 3-year, and 5-year survival estimates for patients diagnosed between 2004 through 2009 were 53.1%, 33.8%, and 29%, respectively (Table 2). There were no meaningful differences in survival between blacks and whites when all 37 states were combined. Some states exhibited substantial in-state differences between blacks and whites; however, there were no discernible geographic patterns to the differences (Supporting Table 2). The 5-year age-standardized net survival improvement by race from the first to the second period was 3.1% for whites and 2.2% for blacks, resulting in a slight divergence in survival between blacks and whites over time. The differences in 5-year net survival between whites and blacks indicate that there were no differences in short-term survival but that differences between races could widen over time.

Five-year age-standardized net survival by disease stage (Table 3) for 2004 through 2009 was 64%, 28.2%, and 5.3% for patients with localized, regional, and distant disease, respectively. Improvements in 5-year net survival by stage at diagnosis were observed between the 2 periods for both whites and blacks. At the localized stage, there were no racial differences in survival, and increases of 3% were observed for both races. At the regional stage, survival increased by 3.4% among whites but by only 1.3% among blacks. At the distant stage, the increase between the 2 periods was 0.5% for whites and 1% for blacks. Whereas blacks experienced lower survival than whites when diagnosed at the regional stage, this was not the case at the distant stage, in which whites experienced lower survival than blacks. Five-year age-standardized survival was uniformly low across all states (Supporting Table 3).

Funnel plots were used to illustrate state-specific and race-specific 5-year age-standardized stomach cancer net survival in relation to the precision of the survival estimate. The pooled (US) survival estimates for each calendar period (2001–2003 and 2004–2009, 26.1% and 29%, respectively) are indicated by the solid lines in Figure 2. Five-year, age-standardized net survival was similar for whites (Fig. 2, open circles) and blacks (Fig. 2, closed circles) from 2001 through 2003. For the period from 2004 through 2009, similar patterns were observed, although the aggregates tended to be less clustered, with larger survival differences, especially among white populations in more populous states (Fig. 2, right). The pooled net survival did improve slightly between the 2 periods, as indicated by the solid lines in Figure 2.

Stomach cancer incidence and mortality have been falling in the United States for decades.² However, despite these favorable trends, survival has remained poor.^4,11,29 The current study provides the most comprehensive and current profile of stomach cancer survival patterns in the United States, which may be useful to public health and medical communities focused on stomach cancer research and control efforts. Our findings suggest that there has been only a very modest improvement in stomach cancer survival in recent years. Furthermore, unlike other cancers that were included in the CONCORD-2 study, we did not observe a large difference in survival or disease stage at diagnosis between whites and blacks. Examination of survival by sex, anatomic sub-site and histology was outside the scope of this report, and this may partly explain the lack of survival disparity observed between blacks and whites.

Racial and ethnic differences in the incidence and mortality for stomach cancer exist, with rates greater in males than in females.^14,30 US cancer statistics estimates that incidence rates are 1.7 times higher in blacks than whites, and mortality rates are 2.0 times higher in blacks than in whites.³ SEER data indicate that the stomach cancer burden in the population has been decreasing in the United States.^14,31 The National Center for Health Statistics mortality trend from 1984 to 2008 consistently declined by 30% to 40% in all racial or race-sex groups, and differences in mortality became smaller.³¹ SEER incidence trends from 1974 through 1978 to 2004 through 2008 exhibited a steady decline in all racial or race-sex groups that was consistent with the decline in mortality.³¹ An increased incidence among young white populations in the United States has also been observed in SEER data⁹ but requires further exploration. The reductions in death rates from stomach cancer parallel a reduction in incidence rates.

Previous studies indicated that the decreases in stomach cancer incidence in the United States may be attributed to declines in distal (noncardia) and intestinal tumors.^5,32 The intestinal type at noncardia sites is often identified in males and older adults, and the declining rates could be because of decreases in H. pylori infection during childhood and the use of refrigeration instead of salt to preserve foods.^4,7,9,33 The higher incidence rates of noncardia carcinoma in blacks may reflect higher prevalence of H. pylori infection in this population.³⁰ Cardia stomach cancers, which are more often of the diffuse histologic subtype, occur in all age groups and have been increasing in both males and females.^32,33 The diffuse type was consistently more common among blacks than among whites.⁵ The diffuse type is harder to detect early, which results in a poorer prognosis.³² If cardia and/or diffuse tumors increase as a proportion of the total tumors, then it is possible that overall survival will decrease for gastric cancer.

The distribution of tumors by subsite, for all participating states combined, was 33.8% and 46.2%, for cardia and noncardia sites respectively, for whites, and 11.5% and 62.1%, respectively, for blacks (data not shown). On the basis of these distributions, it is likely that racial differences in survival exist but are being masked because survival has not been examined by anatomic subsite.

Although stomach cancer has a poor prognosis, the increases in overall survival for all stages between the 2 periods are positive, especially because there was an increase in the proportion of the types with the worst prognosis—cardia and diffuse—in the total pool of stomach cancers. The improvement in survival for each stage could be because of better therapy regimens or more access to appropriate treatment.^10,34,35

Some common risk factors for both cardia and noncardia carcinoma of the stomach include alcohol consumption, foods preserved by salting, older age, male gender, tobacco smoking, race, family history, low physical activity, low fiber intake, and radiation.^4,33 Risk factors associated with cardia carcinomas include obesity and gastroesophageal reflux disease.^4,33 During 2011 through 2014, the prevalence of obesity was just over 36% in adults and 17% in younger adults, and it was higher among females than males.³⁶ Between 1999–2000 and 2013–2014, a significant increase in obesity was observed in both adults and youth.³⁶ With obesity on the rise and cardia tumors likely to increase with their worse prognosis, the future burden of stomach cancer may increase.^37,38 Risk factors associated with noncardia carcinomas include infection with H. pylori, low socioeconomic status, consumption of processed meat, high intake of salty and smoked food, and low consumption of fruits and vegetables.^4,33,39–42

Overall, in the current study, we observed a small increase in survival between 2001–2003 and 2004–2009. This may be related to the increase in locally staged cancers; however, most stomach cancers are diagnosed when they are already at a distant stage, and that proportion is increasing (Table 1), at the expense of regional and unknown stages. The increase in locally staged cancer could be related to heightened awareness in the clinical community. More studies are needed to understand why survival is increasing despite the absence of improving stage distribution and the decreasing trend in subcategories with a good prognosis.