Am. J. Trop. Med. Hyg., 78(5), 2008, pp. 811–818 Copyright © 2008 by The American Society of Tropical Medicine and Hygiene
Epidemiology of Hospitalizations Associated with Ulcers, Gastric Cancers, and Helicobacter pylori Infection among American Indian and Alaska Native Persons Linda J. Demma,* Robert C. Holman, Jeremy Sobel, Krista L. Yorita, Thomas W. Hennessy, Edna L. Paisano, and James E. Cheek 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
Abstract. 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 ageadjusted 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 ⱖ 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
Alaska Native (AN) persons are known to be at increased risk of H. pylori infection compared with the general US population.14–17 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.
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.1–3 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.4,6–9 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
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%
* Address correspondence to Linda J. Demma, Division of Bacterial and Mycotic Diseases, MS D-63, Atlanta, GA 30333. E-mail:
[email protected]
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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 (ICD9-CM 534). Specific diagnosis selected for gastric cancerassociated 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. pyloriassociated 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. pyloriassociated 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 ulcerassociated hospitalizations was 3 days (quartiles, 2 and 5 days); 4.2% of hospitalizations that included an ulcerassociated discharge diagnosis resulted in a transfer to another facility.
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))
Any ulcer-associated diagnosis* Gastritis and duodenitis (535) Gastric ulcer (531) Peptic ulcer (533) Duodenal ulcer (532) Gastrojejunal ulcer (534) Gastric cancer (151) MALT lymphoma (196.2, 202.9) H. pylori† (041.86)
Number
Rate per 100,000 persons
95% CI
In-hospital fatality rate (%)
46529
232.4
230.1–234.6
0.9
33391 6663 5401 3488
162.5 36.1 28.2 17.8
160.7–164.4 35.2–37.0 27.4–29.0 17.2–18.4
0.6 1.9 1.1 1.4
179 2277
0.9 14.2
0.8–1.1 13.6–14.8
2.7 17.4
1064 2612
6.1 28.2
5.7–6.5 27.1–29.4
6.6 0.2
* 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.
813 14.4 (12.7–16.2) 160.5 (154.7–166.6) 344.0 (331.6–356.8) 527.4 (502.5–553.4) 12.1 (10.8–13.4) 8.5 (7.4–9.5) 29.1 (27.4–30.9) 272 2824 2890 1661 383 290 1162 15.4 (12.8–18.6) 152.0 (143.1–161.5) 294.6 (276.2–314.4) 476.3 (438.3–517.7) 15.4 (13.0–17.7) 4.1 (3.0–5.3) 32.3 (29.3-35.2) * 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.
116 1058 928 563 168 54 516 19.9 (16.0–24.7) 122.3 (112.3–133.2) 325.7 (302.5–350.6) 472.7 (429.9–519.7) 4.2 (2.8–5.6) 5.4 (3.9–6.9) 23.7 (20.5-26.8) 85 538 717 436 35 53 233 10.9 (7.7–15.6) 285.5 (265.4–307.0) 522.2 (482.3–565.3) 596.4 (522.8–680.1) 8.8 (5.9–11.7) 9.6 (6.5–12.6) 34.9 (29.9–39.9) 33 738 618 228 42 45 214 2.7 (0.9–7.5) 67.2 (54.5–82.8) 148.5 (121.9–180.6) 277.3 (217.4–353.0) 2.7 (0.5–5.0) 3.9 (0.9–5.9) 12.4 (8.1–16.7) 13.1 (8.8–19.3) 181.2 (162.0–202.7) 478.9 (434.9–527.4) 1048.0 (938.9–1169.5) 35.0 (28.1–41.8) 37.6 (30.5–44.7) 40.9 (33.9–47.9) 27 313 421 324 114 124 149
