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    Percent of hospitalizations with a co-diagnosis of Helicobacter pylori by condition among American Indian and Alaska Native persons, 1996–2005.

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Epidemiology of Hospitalizations Associated with Ulcers, Gastric Cancers, and Helicobacter pylori Infection among American Indian and Alaska Native Persons

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  • 1 Enteric Disease Epidemiology Branch, Division of Foodborne, Bacterial, and Mycotic Diseases, National Center for Zoonotic, Vector Borne, and Enteric Diseases, Centers for Disease Control and Prevention, U.S. Department of Health and Human Services, Atlanta, Georgia; Division of Viral and Rickettsial Diseases, National Center for Zoonotic, Vector Borne, and Enteric Diseases, Centers for Disease Control and Prevention, U.S. Department of Health and Human Services, Atlanta, Georgia; Arctic Investigations Program, National Center for Preparedness, Detection, and Control of Infectious Diseases, Centers for Disease Control and Prevention, U.S. Department of Health and Human Services, Anchorage, Alaska; Division of Program Statistics, Office of Public Health Support, Indian Health Service, U.S. Department of Health and Human Services, Rockville, Maryland; Division of Epidemiology, Office of Public Health Support, Indian Health Service, U.S. Department of Health and Human Services, Albuquerque, New Mexico

To describe the epidemiology of ulcers, gastric cancer, and Helicobacter pylori infection among American Indian (AI) and Alaska Native (AN) persons, we analyzed hospitalization discharge records with physician discharge diagnoses coded as ulcer, gastric cancer, and mucosa-associated lymphoid tissue (MALT) lymphoma during 1980 to 2005, and H. pylori during 1996 to 2005 from the Indian Health Service Inpatient Dataset. The average annual age-adjusted rate of hospitalizations that included an ulcer-associated condition was 232.4 per 100,000 AI/AN persons. The age-adjusted rate for gastric cancer was 14.2 per 100,000 persons. MALT lymphoma was listed as a discharge diagnosis at an age-adjusted rate of 6.1 per 100,000, and the age-adjusted rate of H. pylori discharge diagnoses was 28.2 per 100,000. The AI/AN persons living in the Alaska region and those ≥ 65 years old had the highest rates of hospitalizations that listed ulcer-associated conditions, gastric cancers, MALT lymphoma, and H. pylori as a discharge diagnosis.

INTRODUCTION

Helicobacter pylori is the leading cause of peptic ulcer disease, including gastric and duodenal ulcers, and it is a causative agent of gastric cancer and mucosa-associated lymphoid tissue (MALT) lymphoma.13 Considerable uncertainty remains regarding the precise mode of transmission of H. pylori and the factors that favor persistence of H. pylori infection in some, but not all persons exposed.4 Most H. pylori infections are acquired in early childhood and persist throughout life, except in persons treated with appropriate antimicrobials, and most infected adults develop no clinical consequences from H. pylori colonization.5 Few studies, however, have described the prevalence of H. pylori infection sequelae in a large population.

H. pylori infections occur worldwide, but substantial disparity in infection rates exist between developed and developing countries. In many developing countries, more than 50% of children become colonized before the age of 10 years and the prevalence among middle-aged adults is over 80%.5 In comparison, for developed countries such as the United States, prevalence is < 10% in children and 20–50% in adults.4,69 Recent studies indicate that H. pylori prevalence is declining in developed countries and in countries undergoing rapid socioeconomic improvement.10 However, the prevalence can vary greatly among population groups within the same country. In the United States, prevalence varies by geographic location, ethnic background, socioeconomic status, and age.11 Factors associated with increased risk for H. pylori infection include household crowding, low socioeconomic status, poor personal hygiene, poor quality drinking water sources, lack of indoor plumbing, and lower maternal education.6,12,13

Alaska Native (AN) persons are known to be at increased risk of H. pylori infection compared with the general US population.1417 The seroprevalence of H. pylori among AN adults is as high as 78%, three times that of the general US population.11,16,18 The association of socioeconomic status and living conditions with increased risk for H. pylori infection suggests a need for careful study of the burden and trends of H. pylori among American Indian (AI)/AN persons in the United States to better describe the disparity in incidence between AI/AN persons and the general US population and to more effectively control H. pylori infection. To assess and describe the epidemiology of H. pylori and associated diseases among AI/AN persons in the United States, we examined hospitalization discharge records for AI/AN persons who received medical care through the Indian Health Service (IHS) system.

METHODS

Hospital discharge data for AI/AN persons from the IHS Direct and Contract Health Service Inpatient Dataset for calendar years 1980 through 2005 were analyzed.19 The dataset is maintained by IHS and consists of all patient discharge records from IHS- and tribally-operated hospitals and from hospitals that have contracted with IHS or tribes to provide health care services to federally recognized AI/AN persons within the United States.20 For fiscal year 2001, 49 IHS/tribal hospitals reported hospital discharge data through the IHS system; about 41% of these hospitals were in the Southwest region, 27% in the Northern Plains region, 14% in both the Alaska and Southern Plains regions, and 4% in the East region.21 Approximately 1.3 million of 1.6 million total eligible AI/AN persons for IHS/tribal services used the IHS/tribal health services during fiscal year 2001.21 The IHS California and Portland Administrative Areas were excluded from this study because neither had any IHS or tribally operated hospitals22; these two Areas accounted for approximately 5.0% and 6.8% of the AI/ANs that used the IHS healthcare system, respectively.21 In addition, California Area does not report contract health service inpatient data by diagnosis, and Portland Area has limited contract health service funds for inpatient care.21,23 This study represents AI/AN persons who received direct or contract health care through IHS- or tribally operated inpatient or ambulatory care facilities,20,21 and may not represent all AI/AN persons in the United States.

Hospital discharge records for AI/AN persons with International Classification of Diseases, 9th revision, Clinical Modification (ICD-9-CM) codes24 for diagnosis of ulcers, gastric cancers, or H. pylori illness among the first six (1980–1995) and 15 (1996–2005) listed discharge diagnoses were selected. Specific diagnoses selected for ulcer-associated hospitalizations were duodenal ulcer (ICD-9-CM 532), gastritis/duodenitis (ICD-9-CM 535), gastric ulcer (ICD-9-CM 531), peptic ulcer (ICD-9-CM 533), and gastrojejunal ulcer (ICD-9-CM 534). Specific diagnosis selected for gastric cancer-associated hospitalizations was malignant neoplasm of stomach (ICD-9-CM 151). Two specific diagnosis codes were used for MALT lymphoma, secondary and unspecified malignant neoplasm of intra-abdominal lymph nodes and other/unspecified malignant neoplasms of lymphoid and histiocytic tissue (ICD-9-CM 196.2 and 202.9). Records for H. pylori-associated diagnoses (ICD-9-CM 041.86) from 1996–2005 were selected because the ICD-9-CM code was not available for this condition until October 1, 1995.24 The unit of analysis in this study was a hospitalization.

The IHS regions in this study were defined using the IHS Administrative Areas as follows: East (Nashville), Northern Plains East (Bemidji), Northern Plains West (Aberdeen and Billings), Alaska, Southern Plains (Oklahoma), and Southwest (Albuquerque, Navajo, Phoenix, and Tucson).21 Inhospital fatality rates, month of discharge, and length of stay were also examined. Average annual hospitalization rates with 95% confidence intervals (CIs) were calculated as the number of hospitalizations per 100,000 AI/AN persons. Average annual age-adjusted hospitalization rates with 95% CIs were calculated by standardizing to the year 2000 projected US population using the direct method.25,26 Average annual hospital fatality rates were also calculated and expressed as the number of hospital deaths per 100 hospitalizations. The population denominator for IHS hospitalization rates was estimated for each year and region by using the IHS fiscal year 2006 user population estimates and adjusting the denominator retrospectively for annual changes in the number of AI/AN persons estimated to be eligible for IHS-funded health care, excluding California and Portland areas.20,22 The user population includes all registered AI/AN persons who received IHS-funded healthcare service at least once during the previous 3 years.20 Therefore, the annual population denominators are estimates of the number of AI/AN persons within the IHS healthcare system.

Demographic information for ulcer-, gastric cancer-, MALT lymphoma-, and H. pylori-associated hospitalizations was summarized for the study period, and for 2002–2005 to describe the most recent period. Hospitalization rates were examined by age group, gender, and IHS geographic region. Comparisons of average annual age-specific hospitalization rates and age-adjusted hospitalization rates by demographic characteristic were made.25 To compare epidemiologic changes between time periods, we calculated average annual age-adjusted hospitalization rates for the time periods 1980–1983 and compared them to average annual age-adjusted hospitalization rates for 2002–2005 (1996–1999 and 2002–2005 for H. pylori).

Diagnoses listed concurrently with ulcer- or H. pylori-associated discharge diagnoses were examined. In addition, the proportion of alcoholism-related diagnoses listed with an ulcer-associated or H. pylori-associated or H. pylori diagnoses were examined.24 Alcoholism-related diagnoses was defined as the ICD-9-CM codes 291 (alcohol-induced mental disorders), 303 (alcohol dependence syndrome), 305.0 (alcohol abuse), 357.5 (alcoholic polyneuropathy), 425.5 (alcoholic cardiomyopathy), 535.3 (alcoholic gastritis), 571.0 (alcoholic fatty liver), 571.1 (acute alcoholic hepatitis), 571.2 (alcoholic cirrhosis of liver), and 571.3 (alcoholic liver damage, unspecified).

RESULTS

Ulcer-associated hospitalization rates, 1980–2005.

A total of 46,529 hospitalizations with ulcer-associated discharge diagnoses among AI/ANs were reported to IHS (Table 1). The most frequent ulcer-associated diagnosis was gastritis/duodenitis with an average annual age-adjusted rate of 162.5 hospitalizations per 100,000 persons, accounting for 71.8% of hospitalizations with an ulcer-associated discharge diagnosis. The second most common ulcer-associated discharge diagnosis was gastric ulcer (14.3%), with an age-adjusted rate of 36.1 per 100,000 population, followed by peptic ulcer (11.6%, 28.2 per 100,000 persons), duodenal ulcer (7.5%, 17.8 per 100,000 population), and gastrojejunal ulcer (0.4%, 0.9 per 100,000 persons). In-hospital death occurred most frequently among hospitalizations that included gastrojejunal ulcer as a diagnosis (2.7%). The median length of hospital stay for ulcer-associated hospitalizations was 3 days (quartiles, 2 and 5 days); 4.2% of hospitalizations that included an ulcer-associated discharge diagnosis resulted in a transfer to another facility.

During 2002–2005, the overall rate of hospitalizations that included ulcer-associated conditions differed by gender and by age group (Table 2). Overall and in each region, the highest rate occurred in adults aged ≥ 65 years and decreased with decreasing age group. Adults ≥ 65 years of age had a significantly higher rate of hospitalization than the other age groups in all regions. Overall and in all regions, children ≤ 19 years had the lowest rates of hospitalizations that included these conditions. Males had higher rates than did females, except in the Northern Plains East and Southern Plains regions. Moreover, the Alaska region had a significantly higher rate than each of the other five regions during 2002–2005 (Table 3).

The average annual age-adjusted rates of hospitalizations that included any of the five ulcer-associated diagnoses were compared between the periods 1980–1983 and 2002–2005 (Table 3). The rate decreased significantly between the two time periods, with the greatest percent rate decrease of 61.1% observed for duodenal ulcers. An increase in the rate of hospitalizations that included an ulcer-associated diagnosis occurred in Alaska, while each of the other five regions experienced a rate decrease or did not change significantly over time (Table 3). Significant rate decreases between 1980–1983 and 2002–2005 were observed among both males and females and for all age groups except adults age ≥ 65 years old, for whom the rate increased (Table 3).

The most frequently listed diagnoses concurrent with an ulcer diagnosis were other and unspecified alcohol dependence (303.9; 14.0%), gastritis and gastroduodenitis, unspecified (535.5; 13.4%), alcoholic gastritis (535.3; 12.9%), essential hypertension unspecified (401.9; 11.7%), and peptic ulcer, location unspecified (533.9; 9.3%). An alcohol-related diagnosis was listed with 41.1% of the ulcer-associated hospitalizations and an alcohol-related diagnosis was listed with one-half (49.5%) of the gastritis/duodenitis hospitalizations.

Gastric cancer-associated hospitalization rates, 1980–2005.

A total of 2277 hospitalizations with a discharge diagnosis of gastric cancer were reported, for an annual age-adjusted average rate of 14.2 per 100,000 persons, and an in-hospital fatality rate of 17.4% (Table 1). The median length of hospital stay during 1980–2005 was 7 days (quartiles, 3 and 14 days); 8.6% of hospitalizations with discharge diagnoses that included gastric cancer resulted in a transfer to another facility.

During 2002–2005, the rate of hospitalizations that included gastric cancer was highest in the Alaska region compared with each of the other regions (Table 2). Compared with 1980–1983, the rate for hospitalizations that included gastric cancers showed a 27.1% decline during 2002–2005 (Table 4).

MALT-lymphoma-associated hospitalization rates, 1980–2005.

A total of 1064 hospitalizations (average annual age-adjusted rate of 6.1 per 100,000 persons) listed MALT lymphoma as a discharge diagnosis among AI/AN persons with 70 (6.6%) in-hospital deaths (Table 1). The median length of hospital stay for 1980–2005 was 9 days (quartiles, 6 and 15 days); 3.5% of hospitalizations with a discharge diagnosis that included MALT lymphoma resulted in a transfer to another facility.

During 2002–2005, the Alaska region had a significantly higher rate of hospitalizations that included MALT lymphoma as a discharge diagnosis compared with each of the other regions and the lowest rate was in the Northern Plains East region (Table 2). Compared with 1980–1983, the rate significantly increased from 2.9 per 100,000 during 1980–1983 to 8.5 per 100,000 during 2002–2005 (Table 5). The rate increased significantly among both males and females, in all persons aged ≥ 20 years, and in all regions except the East, Northern Plains East, and Southern Plains regions, in which increases were not significant.

Helicobacter pylori-associated hospitalization rates, 1996–2005.

A total of 2612 hospitalizations (average annual age-adjusted rate of 28.2 per 100,000 population) listed H. pylori as a discharge diagnosis among AI/AN persons with four inhospital deaths (Table 1). The median length of hospital stay for 1996–2005 was 3 days (quartiles, 2 and 5 days). Approximately 2.4% of hospitalizations with a discharge diagnosis that included H. pylori infection resulted in a transfer to another facility.

During 2002–2005, the rate of hospitalizations that included a discharge diagnosis of H. pylori was similar by sex, increased with age and was highest in the Alaska region (Table 6). The highest rate was in persons aged ≥ 65 years and the rate decreased by age group with the lowest rate in the ≤ 19-year-old group. The hospitalization rate among persons aged ≤ 19 years was significantly lower than that for persons aged 20–44 years in all regions. However, Alaska was the only region in which the rate was significantly higher in persons aged ≥ 65 years than that for persons 45–64 years of age, and the only region where the rate was higher in males compared with that for females.

The rate of hospitalizations that included H. pylori as a discharge diagnosis from 1996–1999 and 2002–2005 were similar (27.0 and 29.1 per 100,000, respectively; Table 6). Alaska was the only region in which the rate significantly decreased (51%) from 1996–1999 to 2002–2005, while both the Southern Plains and Southwest regions experienced a significant increase (147% and 36%, respectively). The rate increased significantly among persons aged 20–44 years and among females between the two periods.

The most frequently listed diagnoses with an H. pylori discharge diagnosis were essential hypertension, unspecified (401.9; 17.6%), gastritis and gastroduodenitis, unspecified (535.5; 14.6%), atrophic gastritis without hemorrhage (535.1; 14.0%), type II diabetes mellitus without mention of complication (250.0; 12.1%), acute post-hemorrhagic anemia (285.1; 9.3%); an alcohol-related diagnoses was listed with 21.4% of the H. pylori-associated hospitalizations.

Concurrent diagnosis of H. pylori and ulcer or gastric cancer.

Among hospitalizations associated with ulcers during 1996–2005, 10% were listed with a co-diagnosis of H. pylori (Figure 1). Nineteen percent of duodenal ulcer, 17% of gastric ulcer, and 11% of gastrojejunal ulcer discharge diagnoses listed a co-diagnosis of H. pylori infection. H. pylori infection was a co-diagnosis in 11% of the gastritis/duodenitis discharge diagnoses, and in 4% of the peptic ulcer discharge diagnoses. Only 3% of the gastric cancer and 0.9% of MALT lymphoma discharge diagnoses also had H. pylori infection co-diagnoses.

DISCUSSION

Through examination of hospital discharge records, this study demonstrates that hospitalizations with discharge diagnoses that included ulcer-associated conditions, gastric cancer, MALT lymphoma, and H. pylori are frequent among AI/AN persons in the United States. The rate of hospitalizations with a discharge diagnosis that included ulcer-associated conditions and gastric cancers significantly declined in 2002–2005 compared with 1980–1983. Although hospitalizations that included H. pylori as a discharge diagnosis remained stable, hospitalizations that included MALT lymphoma as a discharge diagnosis significantly increased in 2002–2005 compared with 1980–1983. During 2002–2005, the Alaska region had the highest rates of hospitalizations with discharge diagnoses that included ulcer-associated conditions, gastric cancer, MALT lymphoma, and H. pylori.

Previous studies have shown the rate of infectious disease hospitalizations among AI/AN persons to be higher than the rate for the general US population, demonstrating the health disparities experienced by AI/AN persons.2729 In addition, gastric cancer rates are known to be significantly higher among AI/AN persons compared with the general US population.34 The mortality rate ratio for AI/AN persons was previously shown to be 1.48, indicating a 50% increased risk of death due to gastric cancer for AI/AN persons; in Alaska, the risk was 3-fold higher.30 Alaska Native persons are known to have very high colonization rates of H. pylori and peptic ulcer disease,14,16,17 and the seroprevalence of H. pylori among AN adults is twice that of the general US population, likely contributing to the disparity in gastric cancer mortality.11,16,18

Alaska was the only region in which the rate of hospitalizations that listed H. pylori as a discharge diagnosis has decreased and that for ulcer-associated conditions has increased. Increased efforts to diagnose and treat symptomatic H. pylori infections and related illnesses in this high prevalence area may be contributing to a decline in H. pylori infections. Alternatively, this may be due to decreased testing. In 2000, the Alaska Native Medical Center issued guidelines for diagnosis and treatment of H. pylori infections that discouraged routine screening of patients, and recommended H. pylori treatment only for patients with confirmed gastric or duodenal ulcer, severe gastritis, or MALT lymphoma. H. pylori discharge diagnoses only occurred concurrently in 10% of ulcer-associated diagnoses, a lower than expected proportion in high prevalence areas, suggesting that only certain conditions prompt testing for H. pylori. Our data suggest that H. pylori is likely under-reported especially in the high prevalence region of Alaska. Further study is needed to determine why, among IHS regions, only Alaska has experienced such a significant decrease in H. pylori-associated and concurrent increase in ulcer-associated hospitalizations.

The decreasing rate of hospitalizations with discharge diagnoses that included H. pylori in Alaska may actually reflect a change in other risk factors for peptic ulcer disease and gastric cancer, resulting in larger proportion of cancers due to non-infectious causes such as smoking, alcohol consumption, and dietary practices.31 We found that an alcohol-related diagnosis was listed with approximately 40% of the ulcer-associated hospitalizations and one-half of the gastritis/duodenitis-associated hospitalizations. In contrast, an alcohol-related diagnosis was found in only about 20% of the H. pylori-associated hospitalizations. Although alcohol use is a known risk factor for gastritis and upper gastrointestinal ulcers, our study is consistent with studies that have shown an inverse correlation between H. pylori infection and alcohol consumption,32 and a population-based study in Brazil that showed no relationship between H. pylori infection and alcohol consumption.33

The highest rates of hospitalizations that included ulcer-associated conditions, gastric cancer, MALT lymphoma, and H. pylori discharge diagnoses occurred in persons ≥ 65 years old, similar to findings in other studies in areas of both high and low H. pylori prevalence.34,35 The increased rate of hospitalizations that included a diagnosis of ulcers in persons ≥ 65 years old may be in part due to the use of ulcerogenic treatments such as non-steroidal anti-inflammatory drugs (NSAIDs) in such patients,36 but the relevance of this observation to the AI/AN communities is unknown. Studies of other populations in the United States have also corroborated the observed decline in the rate of ulcer-associated hospitalizations in all age groups shown in this study,37 although it is unclear why the rate of H. pylori discharge diagnoses is declining in older age groups but increasing in persons aged 20–44 years. Of particular interest is the observed increase in the hospitalization rate among females, while the rate for males has remained constant. Published data indicate that H. pylori infection rates are higher in males than females,38 suggesting that recent efforts to reduce H. pylori infections have disproportionately impacted infections among males.

Overall, the most frequent ulcer-associated diagnosis was gastritis/duodenitis, accounting for 71.8% of hospitalizations with an ulcer-associated discharge diagnosis; however, only about 11% of gastritis/duodenitis hospitalizations had co-listed H. pylori as a discharge diagnosis. Hospitalized persons with diagnosis of H. pylori are likely to have an H. pylori-associated illness such as peptic ulcer disease or gastric cancer, so it is likely that overlap exists. In addition, H. pylori infection would not be expected to be a cause of hospitalization. Clinicians may opt to list the clinical illness as the discharge diagnosis rather than the causative organism, so a substantial portion of patients may have tested positive for H. pylori infection without a specific H. pylori diagnosis. Nonetheless, as this study demonstrates, H. pylori- and ulcer-associated illnesses result in a substantial number of hospitalizations within IHS regions of high prevalence.

The association between H. pylori and gastric cancer is well documented39,40 and the recently declining rate of hospitalizations with a discharge diagnosis of H. pylori reported here may correlate with the decrease in gastric cancer hospitalizations. The median length of stay for hospitalizations that included a gastric cancer discharge diagnosis was twice that for those with a discharge diagnosis of H. pylori and ulcer-associated conditions, reinforcing the need to reduce chronic infection with H. pylori to reduce the substantial morbidity associated with gastric cancers.

This study has several limitations. First, this study analyzed data using the hospital discharge diagnoses, and the diagnosis codes reported here may not necessarily reflect hospitalization due to an acute illness. This is an important distinction as some conditions, such as MALT lymphoma and gastric cancer, are much more likely to be the direct cause of a hospitalization than H. pylori or ulcer, which may be chronic or secondary conditions. This study analyzes hospitalizations as opposed to patients, and it is possible that a single patient was hospitalized more than once for the same H. pylori- or ulcer-associated condition. Thus, we are unable to determine the degree to which multiple hospitalizations for the same condition influences the results. Although IHS-funded health care is provided to eligible AI/AN persons, the availability of IHS/tribal services can vary by region and some AI/AN persons eligible for IHS/tribal health care services may have received inpatient care outside of this system, resulting in underestimates of hospitalization rates and hospital fatality rates.22,41 Some AI/AN persons may have private healthcare insurance plans through workplaces, allowing them to obtain healthcare outside of the IHS/tribal system. Furthermore, the in-hospital fatality rate would not reflect any transfers to non-IHS-funded hospitals. The population denominator in this study is an estimate of the number of AI/AN persons annually in the IHS/tribal healthcare system and may not include all eligible AI/AN persons; however, these AI/AN persons most likely receive prepaid health care at an IHS/tribal facility. This study population may not be representative of all AI/AN persons in the United States. Lastly, it is possible that different diagnostic and therapeutic medical practices, including hospitalization practices, may be followed in the care of AI/AN persons regionally.

The current management of H. pylori emphasizes treatment of patients with significant symptoms or disease such as ulcers or gastric cancers. This strategy has been developed over the past 20 years and has likely contributed to the decrease in the ulcer-associated hospitalization rate documented in the present study. Continued focus on early intervention with antimicrobial therapy among AI/AN persons will help substantially reduce the burden of H. pylori colonization, and reduce morbidity associated with this infection. However, because the mode of acquisition of H. pylori is unknown and there are no known prevention strategies, populations with a high prevalence of H. pylori infection are likely to remain so under current practices and conditions. Moreover, the development of antimicrobial resistance among H. pylori threatens to erode the successes of the current treat-only strategy. For example, in Alaska, the high prevalence of resistance among H. pylori to clarithromycin and metronidazole has led to a high frequency of treatment failures and more complicated clinical management.42,43 Several steps could be taken to prevent H. pylori infections and their sequelae in the AI/AN population. First, studies of the risk factors for acquisition are needed to develop appropriate intervention strategies. Studies should focus on young children and include household and environmental conditions to be able to assess person-to-person and environmental sources of infection. Furthermore, large population-based studies of the general US population will help quantify the burden H. pylori infections and their sequelae in the AI/AN population compared with the general population. Second, because antimicrobial treatment of all persons with H. pylori infection is impractical in populations with high prevalence such as Alaska Native adults, studies are needed that focus on identification of risk factors for peptic ulcer and gastric cancers among persons already infected with H. pylori. Such risk factors could be of value for identifying persons at high risk who may be candidates for preventive antimicrobial treatment or screening endoscopy to detect and treat early carcinoma. Finally, the decline in gastric cancer in the United States has correlated with improvements in living conditions (access to improved housing, treated water and wastewater removal) that have presumably led to decreases in H. pylori transmission.44 For much of the AI/AN population, living conditions still include crowded and substandard housing that lack in-home piped water and waste removal. Improvements in these areas for AI/AN persons would have benefits for a variety of infectious diseases and are likely to decrease the burden of H. pylori infections and sequelae that we document in the present study.

Table 1

Hospitalizations and average annual age-adjusted hospitalization rates with discharge diagnoses (ICD-9-CM codes) that included ulcer-associated conditions, gastric cancer, mucosa-associated lymphoid tissue (MALT) lymphoma, and Helicobacter pylori among American Indian and Alaska Native persons, Indian Health Service, 1980–2005

Diagnosis (ICD-9-CM Code(s))NumberRate per 100,000 persons95% CIIn-hospital fatality rate (%)
* Ulcer-associated diagnoses were defined as duodenal ulcer, gastrojejunal ulcer, gastric ulcer, peptic ulcer, gastritis, and duodenitis. Number of individual diagnoses may sum to more than the total due to the potential for multiple diagnoses.
† For 1996–2005; ICD-9-CM codes introduced October 1995.
Any ulcer-associated diagnosis*46529232.4230.1–234.60.9
    Gastritis and duodenitis (535)33391162.5160.7–164.40.6
    Gastric ulcer (531)666336.135.2–37.01.9
    Peptic ulcer (533)540128.227.4–29.01.1
    Duodenal ulcer (532)348817.817.2–18.41.4
    Gastrojejunal ulcer (534)1790.90.8–1.12.7
Gastric cancer (151)227714.213.6–14.817.4
MALT lymphoma (196.2, 202.9)10646.15.7–6.56.6
H. pylori† (041.86)261228.227.1–29.40.2
Table 2

Characteristics of hospitalizations and average annual age-adjusted and age-specific hospitalization rates with discharge diagnoses that included ulcer-associated conditions, gastric cancer, mucosa associated lymphoid tissue (MALT) lymphoma, and Helicobacter pylori by Indian Health Service (IHS) region* among American Indians and Alaska Natives, 2002–2005

Alaska
No.Rate per 100,000 persons (95% CI)Northern Plains EastNorthern Plains WestSouthern PlainsSouthwestOverall IHS
* The Indian Health Service East region was not considered individually due to the region’s small number of hospitalizations. It is included in the overall IHS category.
Sex
    Male605356.5 (325.4–387.7)12486.5 (69.9–103.1)885325.3 (301.4–349.1)800175.7 (162.9–188.6)1483206.0 (194.6–217.4)4039222.5 (215.0–229.9)
    Female480251.7 (228.0–275.4)14595.9 (79.4–112.3)732257.9 (237.8–278.0)976181.6 (169.9–193.3)1182150.6 (141.6–159.7)3614178.7 (172.6–184.8)
Age group (years)
    0–192713.1 (8.8–19.3)< 52.7 (0.9–7.5)3310.9 (7.7–15.6)8519.9 (16.0–24.7)11615.4 (12.8–18.6)27214.4 (12.7–16.2)
    20–44313181.2 (162.0–202.7)9267.2 (54.5–82.8)738285.5 (265.4–307.0)538122.3 (112.3–133.2)1058152.0 (143.1–161.5)2824160.5 (154.7–166.6)
    45–64421478.9 (434.9–527.4)104148.5 (121.9–180.6)618522.2 (482.3–565.3)717325.7 (302.5–350.6)928294.6 (276.2–314.4)2890344.0 (331.6–356.8)
    65+3241048.0 (938.9–1169.5)59277.3 (217.4–353.0)228596.4 (522.8–680.1)436472.7 (429.9–519.7)563476.3 (438.3–517.7)1661527.4 (502.5–553.4)
Gastric cancer11435.0 (28.1–41.8)62.7 (0.5–5.0)428.8 (5.9–11.7)354.2 (2.8–5.6)16815.4 (13.0–17.7)38312.1 (10.8–13.4)
MALT lymphoma12437.6 (30.5–44.7)83.9 (0.9–5.9)459.6 (6.5–12.6)535.4 (3.9–6.9)544.1 (3.0–5.3)2908.5 (7.4–9.5)
H. pylori14940.9 (33.9–47.9)3612.4 (8.1–16.7)21434.9 (29.9–39.9)23323.7 (20.5–26.8)51632.3 (29.3–35.2)116229.1 (27.4–30.9)
Table 3

Comparisons of hospitalizations and average annual age-adjusted and age-specific hospitalization rates with discharge diagnoses that included ulcer-associated conditions among American Indian and Alaska Native persons, Indian Health Service, 1980–1983 and 2002–2005

1980–19832002–2005
NumberRate per 100,000 (95% CI)NumberRate per 100,000 (95% CI)Percent rate change
* 0.01 ≤ P < 0.05.
† 0.001 ≤ P < 0.01.
P < 0.001.
Sex
    Male3630335.7 (324.0–347.4)4033222.5 (215.0–229.9)−33.7‡
    Female2722219.8 (211.2–228.5)3614178.7 (172.6–184.8)−18.7‡
Age group (years)
    0–1935133.7 (30.3–37.4)27214.4 (12.7–16.2)−57.3‡
    20–443187330.8 (319.5–342.5)2824160.5 (154.7–166.6)−51.5‡
    45–641959424.5 (406.0–443.8)2890344.0 (331.6–356.8)−19.0*
    65+855489.7 (457.7–523.8)1661527.4 (502.5–553.4)7.7*
Region
    Alaska661258.6 (237.7–279.5)1085299.9 (280.7–319.0)16.0†
    East133376.1 (308.6–443.6)235183.6 (158.9–208.3)−51.2‡
    Northern Plains East334254.9 (225.7–284.1)26991.9 (80.2–103.7)−63.9‡
    Northern Plains West2553705.9 (675.9–735.9)1617291.4 (275.9–307.0)−58.7‡
    Southern Plains1005177.1 (165.7–188.6)1776179.0 (170.3–187.6)1.0
    Southwest1666173.0 (164.3–181.8)2665177.2 (170.0–184.4)2.4
Ulcer type
    Gastritis and duodenitis4344180.5 (174.9–186.2)5826149.2 (145.2–153.3)−27.8†
    Gastric ulcers80238.8 (35.9–41.3)114931.4 (29.5–33.4)−22.3†
    Peptic ulcers75933.9 (31.3–36.4)75921.3 (19.7–22.9)−53.7†
    Duodenal ulcers60927.2 (25.0–29.6)43511.6 (10.5–12.8)−61.1†
    Gastrojejunal ulcer261.2 (0.7–1.7)220.5 (0.3–0.7)−40.0
Total6352273.6 (266.5–280.8)7647199.5 (194.8–204.3)−27.1†
Table 4

Comparisons of hospitalizations and average annual age-adjusted hospitalization rates with discharge diagnoses that included gastric cancer among American Indian and Alaska Native persons, Indian Health Service, 1980–1983 and 2002–2005

1980–19832002–2005
NumberRate per 100,000 (95% CI)NumberRate per 100,000 (95% CI)Percent rate change*
* 0.01 ≤ P < 0.05.
† 0.001 ≤ P < 0.01.
P < 0.001.
Gastric cancer31416.6 (14.6–18.6)38312.1 (10.8–13.4)−27.2‡
Male17421.0 (17.5–24.5)23316.9 (14.5–19.2)−19.9
Female14013.4 (11.1–15.7)1508.5 (7.1–9.9)−36.6‡
Table 5

Comparisons of hospitalizations and average annual age-adjusted and age-specific hospitalization rates with discharge diagnoses that included mucosa-associated lymphoid tissue (MALT) lymphoma among American Indian and Alaska Native persons, Indian Health Service, 1980–1983 and 2002–2005

1980–19832002–2005
NumberRate per 100,000 (95% CI)No.Rate per 100,000 (95% CI)Percent rate change*
* The 0–19 age group and the East region were not included due to small numbers.
† 0.01 ≤ P < 0.05.
‡ 0.001 ≤ P < 0.01.
§ P < 0.001.
Sex
    Male252.0 (1.2–2.9)1509.9 (8.2–11.7)389.5‡
    Female373.6 (2.4–4.8)1407.4 (6.1–8.7)106.6‡
Age group (years)*
    20–4460.6 (0.3–1.4)502.8 (2.1–3.8)366.7‡
    45–64357.6 (5.4–10.7)12615.0 (12.5–17.9)97.4‡
    65+179.7 (5.9–15.9)11235.6 (29.4–43.0)267.0‡
Region*
Alaska136.0 (2.5–9.6)12437.6 (30.5–44.7)524.6‡
Northern Plains East50.9 (0.0–2.7)83.4 (0.9–5.9)277.9
Northern Plains West92.9 (0.9–5.0)459.6 (6.5–12.6)229.7‡
Southern Plains254.2 (2.5–6.0)535.4 (3.9–6.9)26.6
Southwest131.6 (0.7–2.6)544.1 (3.0–5.3)151.8†
Total622.9 (2.2–3.7)2908.5 (7.4–9.5)187.8‡
Table 6

Comparisons of hospitalizations and average annual age-adjusted and age-specific hospitalization rates with discharge diagnoses that included Helicobacter pylori among American Indian and Alaska Native persons, Indian Health Service, 1996–1999 and 2002–2005

1996–19992002–2005
NumberRate per 100,000 (95% CI)NumberRate per 100,000 (95% CI)Percent Rate Change
* 0.01 ≤ P < 0.05.
† 0.001 ≤ P < 0.01.
P < 0.001.
Sex
    Male50631.5 (28.5–34.4)57531.2 (28.4–33.9)−1.0
    Female41623.0 (20.7–25.3)58727.4 (25.1–29.7)19.3†
Age group (years)
    0–19271.5 (1.1–2.4)432.3 (1.7–3.1)43.8
    20–4431019.9 (17.8–22.3)46226.3 (23.9–28.8)32.2
    45–6439453.1 (48.0–58.6)44352.7 (48.0–57.9)−0.8
    65+19168.5 (59.3–79.1)21467.9 (59.3–77.8)−0.9
Region
    Alaska29283.6 (73.4–93.9)14940.9 (33.9–47.9)−51.1‡
    East1210.8 (4.1–17.5)149.4 (4.4–14.4)−12.8
    Northern Plains East208.9 (4.8–13.0)3612.4 (8.1–16.7)40.1
    Northern Plains West20541.0 (34.9–47.1)21434.9 (29.9–39.9)−15.0
    Southern Plains849.6 (7.5–11.7)23323.7 (20.5–26.8)146.6‡
    Southwest30923.8 (21.0–26.6)51632.3 (29.3–35.2)35.5‡
Total92227.0 (25.1–28.8)116229.1 (27.4–30.9)7.8
Figure 1.
Figure 1.

Percent of hospitalizations with a co-diagnosis of Helicobacter pylori by condition among American Indian and Alaska Native persons, 1996–2005.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 78, 5; 10.4269/ajtmh.2008.78.811

*

Address correspondence to Linda J. Demma, Division of Bacterial and Mycotic Diseases, MS D-63, Atlanta, GA 30333. E-mail: ldemma@emory.edu

Authors’ addresses: Linda J. Demma, Division of Bacterial and Mycotic Diseases, MS D-63, Atlanta, GA 30333, E-mail: ldemma@emory.edu. Robert C. Holman, Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, 1600 Clifton Rd., MS A-39, Atlanta, GA 30333. Jeremy Sobel, Division of Bacterial and Mycotic Diseases, Centers for Disease Control and Prevention, 1600 Clifton Rd., MS A-38, Atlanta, GA 30333, E-mail: jsobel@cdc.gov. Krista L. Yorita, Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, 1600 Clifton Rd., MS A-30, Atlanta, GA 30333. Thomas W. Hennessy, Arctic Investigations Program, Centers for Disease Control and Prevention, 4055 Tudor Centre Rd., Anchorage, Alaska 99508, E-mail: tbh0@cdc.gov. Edna L. Paisano, Division of Program Statistics, Office of Public Health Support, Indian Health Service, Rockville, MD 20852, E-mail: Edna.Paisano@ihs.gov. James E. Cheek, Division of Epidemiology, Office of Public Health Support, Indian Health Service, Albuquerque, NM 87110, E-mail: James.Cheek@ihs.gov.

Acknowledgments: The authors thank Patricia M. Griffin (CDC) for helpful manuscript comments, John Redd, Barbara Strzelczyk (IHS), and Dana Haberling (CDC) for technical assistance, and the staff of all the participating hospitals.

Funding for this report was provided by the United States Department of Health and Human Services, Centers for Disease Control and Prevention.

Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent those of the funding agencies.

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