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Original Research: Asthma |

Epidemiology of Asthma Hospitalizations Among American Indian and Alaska Native People and the General United States PopulationAsthma Hospitalizations in the United States FREE TO VIEW

Jason M. Mehal, MPH; Robert C. Holman, MS; Claudia A. Steiner, MD, MPH; Michael L. Bartholomew, MD; Rosalyn J. Singleton, MD
Author and Funding Information

From the Division of High-Consequence Pathogens and Pathology (Messrs Mehal and Holman), National Center for Emerging and Zoonotic Infectious Diseases (NCEZID), Centers for Disease Control and Prevention (CDC), Department of Health and Human Services (DHHS), Atlanta, GA; the Healthcare Cost and Utilization Project (Dr Steiner), Center for Delivery, Organizations, and Markets, Agency for Healthcare Research and Quality, DHHS, Rockville, MD; the Indian Health Service (Dr Bartholomew), DHHS, Rockville, MD; the Alaska Native Tribal Health Consortium (Dr Singleton), Anchorage, AK; and the Arctic Investigations Program (Dr Singleton), Division of Preparedness and Emerging Infections, NCEZID, CDC, DHHS, Anchorage, AK.

CORRESPONDENCE TO: Jason M. Mehal, MPH, Centers for Disease Control and Prevention, 1600 Clifton Rd NE, MS A-30, Atlanta, GA 30333; e-mail: jmehal@cdc.gov


FUNDING/SUPPORT: The authors have reported to CHEST that no funding was received for this study.

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.


Chest. 2014;146(3):624-632. doi:10.1378/chest.14-0183
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BACKGROUND:  Asthma, a common chronic disease among adults and children in the United States, results in nearly one-half million hospitalizations annually. There has been no evaluation of asthma hospitalizations for American Indian and Alaska Native (AI/AN) people since a previous study using data for 1988-2002. In this study, we describe the epidemiology and trends for asthma hospitalizations among AI/AN people and the general US population for 2003-2011.

METHODS:  Hospital discharge records with a first-listed diagnosis of asthma for 2003-2011 were examined for AI/AN people, using Indian Health Service (IHS) data, and for the general US population, using the Nationwide Inpatient Sample. Average annual crude and age-adjusted hospitalization rates were calculated.

RESULTS:  The average annual asthma hospitalization rates for AI/AN people and the general US population decreased from 2003-2005 to 2009-2011 (32% and 11% [SE, 3%], respectively). The average annual age-adjusted rate for 2009-2011 was lower for AI/AN people (7.6 per 10,000 population) compared with the general US population (13.2 per 10,000; 95% CI, 12.8-13.6). Age-specific AI/AN rates were highest among infants and children 1 to 4 years of age. IHS regional rates declined in all regions except Alaska.

CONCLUSIONS:  Asthma hospitalization rates are decreasing for AI/AN people and the general US population despite increasing prevalence rates. AI/AN people experienced a substantially lower age-adjusted asthma hospitalization rate compared with the general US population. Although the rates for AI/AN infants and children 1 to 4 years of age have declined substantially, they remain higher compared with other age groups. Improved disease management and awareness should help to further decrease asthma hospitalizations, particularly among young children.

Figures in this Article

Asthma is a common chronic disease among both adults and children in the United States, affecting > 25 million people and resulting in nearly one-half million hospitalizations annually.14 The prevalence of asthma in the United States has increased over the past few decades.1,2 Conversely, asthma hospitalization rates have declined since the late 1980s for both the general US population4,5 and for American Indian and Alaska Native (AI/AN) people.5 Asthma hospitalization rates for AI/AN people increased during the 1980s6,7; reports have shown AI/AN people to have similar or slightly higher prevalence rates1,2,810 and slightly lower hospitalization rates5 compared with the general US population.

Higher asthma prevalence and hospitalization rates have consistently been reported among both young children and female patients; however, boys have higher rates in young childhood and women have higher rates in early to late adulthood.2,4,5,11 Asthma prevalence varies by race, with the highest rates among those of black race.1,2,11 There has been no evaluation of asthma hospitalizations for AI/AN people since a previous study for 1988-2002.5 In this study, we describe the trends of asthma hospitalizations among AI/AN people and the general US population for 2003-2011.

Asthma hospitalizations during 2003-2011 were examined for AI/AN people and the general US population. An asthma hospitalization was defined as a hospital discharge record with the International Classification of Diseases, 9th Revision, Clinical Modification (ICD-9-CM) code for asthma (493) listed as the first diagnosis.12 The unit of analysis was a hospitalization.

Asthma hospitalizations for AI/AN people were analyzed using the Indian Health Service (IHS) direct and contract health service inpatient visit data, which consist of all hospital discharge records from IHS-operated, tribally operated, and community hospitals contracted with IHS to provide health-care services to eligible AI/AN people.13,14 The IHS is composed of administrative areas that are grouped into geographic regions. IHS California and Portland administrative areas were not included in the analysis because neither had IHS- or tribally operated hospitals, California did not report contract health service inpatient data by diagnosis, and Portland had limited contract health services for inpatient care.13 Population denominators were based on the annual IHS user populations for fiscal years 2003-2011; the annual IHS user population consists of all registered AI/AN people who received IHS-funded health care at least once during the previous 3 years.14

For the general US population, asthma hospitalizations were examined using the Nationwide Inpatient Sample (NIS).15,16 The NIS is a nationally representative sample of hospitals conducted by the Healthcare Cost and Utilization Project (HCUP) in collaboration with participating states and includes a 20% sample of participating US community hospitals.15 Participating hospitals are short-term, nonfederal general and specialty hospitals sampled annually from up to 45 states. Estimates of the number of hospitalizations were calculated using the HCUP weighting methodology.17 To account for the NIS sample design, SUDAAN software (RTI International) was used to calculate SEs for hospitalization estimates used to calculate 95% CIs and for percent rate change comparing 2003-2005 to 2009-2011. Population denominators were based on the National Center for Health Statistics bridged race population estimates.18,19

Because use of these datasets specifically prohibits reidentification of patients, data are not individually identifiable per Health and Human Services Office for Human Research Protections guidance. Therefore, the analysis is not considered to involve human subjects and not subject to institutional review board review requirements.

Hospitalization records were analyzed by sex, age group (< 1, 1-4, 5-19, 20-44, 45-64, and ≥ 65 years), region, year, and time period (2003-2005 and 2009-2011). Average annual crude and age-adjusted hospitalization rates were calculated as the number of hospitalizations per 10,000 corresponding population. Age-adjusted rates were calculated using the direct method with the 2000 projected US population as the standard.20 Poisson regression was used to compare unadjusted rates by sex, age group, time period, and region for AI/AN people21; rate ratios with corresponding 95% CIs were used to compare rates among the general US population.22 In-hospital fatality rates were computed as the percent of asthma hospitalizations with a fatal outcome. Month of hospital admission and associated diagnoses, specifically including lower respiratory tract infections (LRTIs) (ICD-9-CM codes: 011, 022.1, 031.0, 033, 095.1, 466, 480-488, 510, 511.1, 513, 517.1, and 770.0), were also examined.

During 2003-2011, there were 10,116 asthma hospitalizations among AI/AN people in the IHS health-care system accounting for 1.5% of all AI/AN hospitalizations. The average annual asthma hospitalization rate for AI/AN people decreased 32% from 2003-2005 to 2009-2011 (P < .0001) (Table 1). For the general US population, an estimated 3,820,242 (SE, 49,382) asthma hospitalizations occurred during 2003-2011, accounting for 1.2% (SE, 0.01%) of all hospitalizations, and the average annual hospitalization rate decreased 11% (SE, 3%) from 2003-2005 to 2009-2011 (Table 2). The average annual age-adjusted rate for 2009-2011 was lower for AI/AN people (7.6 per 10,000) compared with the general US population (13.2 per 10,000; 95% CI, 12.8-13.6).

Table Graphic Jump Location
TABLE 1  ] Number and Average Annual Rate of Asthma Hospitalizations Among American Indian/Alaska Natives, Indian Health Service/Tribal, 2003-2005 and 2009-2011

RR = rate ratio.

a 

Unadjusted rate per 10,000 corresponding population.

b 

Significant change from 2003-2005 to 2009-2011.

Table Graphic Jump Location
TABLE 2  ] Number and Average Annual Rate of Asthma Hospitalizations Among the General US Population, 2003-2005 and 2009-2011

See Table 1 legend for expansion of abbreviation.

a 

Unadjusted rate per 10,000 corresponding population.

b 

Significant change from 2003-2005 to 2009-2011.

The average annual hospitalization rate for female patients was higher than that for male patients among both AI/AN people and the general US population (Tables 1, 2). The rate decreased 35% for male AI/AN patients (P < .0001) and 30% for female AI/AN patients (P < .0001) from 2003-2005 to 2009-2011 (Table 1). Decreases among US male patients (14%; SE, 4%) and female patients (8%; SE, 3%) were significant but of smaller magnitude compared with those for AI/AN people (Table 2). Comparison of age-adjusted rates by sex for 2009-2011 revealed lower rates among male (5.7 per 10,000) and female AI/AN patients (9.0 per 10,000) compared with male patients (10.4 per 10,000; 95% CI, 10.0-10.7) and female patients (15.6 per 10,000; 95% CI, 15.2-16.0) in the general US population.

During 2009-2011, average annual age-specific hospitalization rates varied substantially among age groups for AI/AN people and for the general US population. AI/AN rates were highest among infants (children < 1 year of age) and children 1 to 4 years of age, lower in late childhood and early adulthood, and increased among older adults (Table 1); age-specific rates for the general US population followed a similar pattern to that observed for AI/AN people except the rate among infants was not among the highest age-specific rates (Table 2). Compared with the general US population, age-specific AI/AN rates were lower for all age groups, with the exception of infants (Fig 1). Among both AI/AN people and the general US population, the hospitalization rate was higher for boys in younger age groups (< 5 years of age) and for women in older age groups (≥ 20 years) (Fig 2). The rate decreased for all age groups among AI/AN people, with greater declines seen among infants (63%) and those 1 to 4 years of age (42%) compared with older age groups (range, 24%-29%) (Table 1). For the US population, the rate remained stable for those 45 to 64 and ≥ 65 years of age while declining among all other age groups; the greatest decline was observed among infants (52%; SE, 4%) (Table 2).

Figure Jump LinkFigure 1  Age-specific average annual asthma hospitalization rates among AI/AN people and the general US population, 2009-2011. Error bars represent 95% CIs. AI/AN = American Indian and Alaska Native.Grahic Jump Location
Figure Jump LinkFigure 2  A, Age-specific average annual asthma hospitalization rates by sex among AI/AN people, 2009-2011. B, Age-specific average annual asthma hospitalization rates by sex among the general US population, 2009-2011. Error bars represent 95% CIs. See Figure 1 legend for expansion of abbreviation.Grahic Jump Location

Examination of the AI/AN hospitalization rate by region showed significant decreases in all IHS regions with the exception of Alaska (P = .42) (Table 1). IHS regional rates varied markedly for 2009-2011, with higher rates in the Southwest (10.1 per 10,000) and Alaska (9.0 per 10,000) regions and lower rates in the Northern Plains East (1.8 per 10,000) and Southern Plains (3.1 per 10,000) regions (Table 1). The rate for the general US population declined in all regions except for the Northeast (Table 2). US regional rates varied substantially, with the highest rate in the Northeast (19.7 per 10,000; 95% CI, 17.4-21.9) and the lowest rate in the West region (9.2 per 10,000; 95% CI, 8.5-10.0) (Table 2).

Nearly one-third of AI/AN hospitalizations (32%) occurred during the winter months of January through March, whereas only 18% occurred during the months of June through August (Fig 3). This winter peak was particularly notable for infants (39% of hospitalizations) and those 1 to 4 years of age (38%). A similar winter peak was not evident for the general US population, with consistent numbers of hospitalizations for September through May, although there was a decline in hospitalizations during June through August (17%; SE, 0.1%) (Fig 3). There was, however, a slight winter peak (January through March) for age groups < 1 year (31% [SE, 0.5%] occurring during January through March), 45 to 64 years (30% [SE, 0.1%]), and ≥ 65 years of age (33% [SE, 0.2%]).

Figure Jump LinkFigure 3  Asthma hospitalizations by admission month among AI/AN people and the general US population, 2003-2011. See Figure 1 legend for expansion of abbreviation.Grahic Jump Location

An LRTI was listed for 21% of asthma hospitalizations among AI/AN people; this proportion varied by age group and was highest among infants (30%) and children 1 to 4 years of age (29%). For the general US population, an LRTI was listed for 18% (SE, 0.1%) of asthma hospitalizations; the proportion was highest among infants (26%; SE, 0.5%), those 1 to 4 years of age (21%; SE, 0.3%), and those ≥ 65 years of age (20%; SE, 0.2%). A fatal outcome occurred for 0.1% (n = 7) of AI/AN asthma hospitalizations overall and 0.3% (n = 4) for adults ≥ 65 years of age. Fatal outcomes occurred more often for the general US population, occurring for 0.3% (SE, 0.01%) of asthma hospitalizations overall and 1.0% (SE, 0.03%) for adults ≥ 65 years of age.

Despite increasing prevalence of asthma in the United States,1,2,8,23 asthma hospitalization rates for AI/AN people and the general US population continue to decline.5 Decreasing rates were observed for male and female patients in both populations, all age groups for AI/AN people, and age groups < 45 years of age for the general US population, with more substantial decreases occurring for AI/AN people. Decreasing hospitalization rates may result in part from a more intensive treatment algorithm in outpatient settings, better asthma treatment plans, and/or increased patient education. Improved asthma treatment and education, however, would likely not explain the more rapidly declining rates among AI/AN people compared with the general US population. Another possible reason is increased use of inhaled corticosteroids24,25; however, the largest decreases were observed for both AI/AN and US infants and children 1 to 4 years of age, and physicians are generally more reluctant to prescribe inhaled corticosteroids for young children.24,26 Declining rates among young children may result from more accurate discharge diagnoses. Published guidelines for the diagnosis of asthma27 and bronchiolitis28 may have contributed to fewer misdiagnoses of asthma, thereby reducing the asthma hospitalization rate.

AI/AN people experience a substantially lower age-adjusted asthma hospitalization rate than the general US population, despite having a similar or slightly higher asthma prevalence.9,10,29 Age-specific rates were similar for infants in both populations despite being lower for AI/AN people in all other age groups; this may be due in part to higher rates of bronchiolitis and wheezing with LRTIs among AI/AN infants compared with other US infants.30 The lower rates of asthma hospitalization among AI/AN people may be related to differences in physician diagnosis of asthma or health-care access and use. Poverty and residence in urban areas have been shown to be associated with higher asthma hospitalization rates.31,32 Compared with the general US population, a greater proportion of AI/AN people reside in rural areas,33 which may contribute to lower rates among AI/AN people. Although AI/AN people have lower household income and a higher poverty rate than the general US population,34 they also have potentially greater access to routine health care, which could increase their access to inhaled corticosteroids and other controller medications. Additionally, some AI/AN individuals may receive health care outside the IHS/tribal system, causing AI/AN hospitalization rates to appear lower.

Among AI/AN people and the general US population, asthma hospitalization rates were higher for female patients, and age-specific rates varied, with high rates among young children decreasing into early adulthood and then increasing again among older adults.2,4,5 Diagnostic substitution of asthma for bronchiolitis as well as the role of bronchiolitis and other LRTIs in exacerbating asthma symptoms may contribute to higher asthma hospitalization rates among young AI/AN or US children.31,35 Asthma diagnosis in infants is controversial because of the difficulty in obtaining objective measurements and uncertainty in predicting asthma in wheezing infants.27 The rapid decline in hospitalization rates among young children in both populations, however, has reduced the substantially higher rates among infants and children 1 to 4 years of age to nearly similar levels compared with older adults. Rates were higher among boys in young age groups (< 5 years of age) and women in older age groups (≥ 20 years of age).5 This phenomenon has been widely observed2,4,5,11 and may be due to differences in airway behavior resulting from sociocultural and biologic effects related to sex and gender.36

The IHS Southwest region for AI/AN people and the Northeast region for the general US population continue to have the highest regional rates.5 Regional differences in asthma hospitalization rates may result from differing environmental risk factors, diagnostic practice, asthma presentation, or other comorbid conditions.25,35,37 The Southwest and Alaska IHS regions experience high LRTI hospitalization rates compared with other IHS regions and the general US population,38 which could result in increased asthma hospitalization rates. In the IHS Alaska region, household crowding and a lack of indoor water service may contribute to increased LRTIs.3941 However, LRTI rates are decreasing in Alaska as well as other IHS regions, most likely due to a combination of improved household and environmental conditions and introduction of pneumococcal conjugate vaccine in 2000.30 The winter peak of asthma hospitalizations was more pronounced among AI/AN people, particularly for young children, suggesting the possible influence of LRTIs in asthma exacerbation.5 Other possible explanations include higher upper respiratory tract infection rates among AI/AN people during the winter and increased exposure to indoor air pollutants resulting from more time spent indoors. Use of indoor wood-burning stoves among AI/AN people has been linked to poor indoor air quality42 and higher rates of LRTIs43 and is possibly also related to increased asthma hospitalizations.

Some limitations of the present study should be considered. Hospital diagnoses of asthma may be incomplete or inaccurate because of use of ICD-9-CM coding to identify asthma hospitalizations, and diagnostic coding may vary by practice or geographic region. The first-listed diagnosis was used to identify asthma hospitalizations to limit misclassification of non-asthma hospitalizations; however, this conservative method does not include any true asthma hospitalizations for which asthma is not the first-listed diagnosis. The unit of analysis was a hospitalization; thus, multiple hospitalizations for the same patient and/or hospital transfers were included in the analysis. The denominator for AI/AN people was estimated as the number of AI/AN people who used the IHS/tribal health-care system, whereas the denominator for the general US population was estimated from US census data; this may affect the comparability of rates between the two populations. However, AI/AN people included in the IHS user population would be those people at risk for having an asthma hospitalization included in this study. Additionally, AI/AN individuals may receive health care outside the IHS/tribal system, which would result in an underestimate of AI/AN hospitalizations.

Asthma hospitalization rates continue to decrease for AI/AN people and the general US population despite increasing prevalence rates and have declined more rapidly for AI/AN people. Compared with the general US population, AI/AN people have a substantially lower age-adjusted asthma hospitalization rate, despite having similar or higher prevalence. Although the rates for young AI/AN children have declined substantially, they still remain higher than for older age groups. Improved disease management and awareness should help to further decrease asthma hospitalization rates, particularly among young children. Educational programs and interventions like those provided through the Centers for Disease Control and Prevention’s National Asthma Control Program44 are important in reducing poor outcomes associated with asthma, such as hospitalization and death.

Author contributions: J. M. M. takes responsibility for the content of the manuscript, including the data and analysis. J. M. M. and R. C. H. contributed to the data analysis; J. M. M., R. C. H., C. A. S., M. L. B., and R. J. S. contributed to the study design and writing, critical review, and final approval of the manuscript.

Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Other contributions: We thank Jeanne Moorman, MS (CDC) and Greg Redding, MD (Seattle Children’s Hospital) for critical review of the manuscript. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention (CDC) or the Indian Health Service (IHS).

AI/AN

American Indian and Alaska Native

ICD-9-CM

International Classification of Diseases, 9th Revision, Clinical Modification

IHS

Indian Health Service

HCUP

Healthcare Cost and Utilization Project

LRTI

lower respiratory tract infection

NIS

Nationwide Inpatient Sample

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Figures

Figure Jump LinkFigure 1  Age-specific average annual asthma hospitalization rates among AI/AN people and the general US population, 2009-2011. Error bars represent 95% CIs. AI/AN = American Indian and Alaska Native.Grahic Jump Location
Figure Jump LinkFigure 2  A, Age-specific average annual asthma hospitalization rates by sex among AI/AN people, 2009-2011. B, Age-specific average annual asthma hospitalization rates by sex among the general US population, 2009-2011. Error bars represent 95% CIs. See Figure 1 legend for expansion of abbreviation.Grahic Jump Location
Figure Jump LinkFigure 3  Asthma hospitalizations by admission month among AI/AN people and the general US population, 2003-2011. See Figure 1 legend for expansion of abbreviation.Grahic Jump Location

Tables

Table Graphic Jump Location
TABLE 1  ] Number and Average Annual Rate of Asthma Hospitalizations Among American Indian/Alaska Natives, Indian Health Service/Tribal, 2003-2005 and 2009-2011

RR = rate ratio.

a 

Unadjusted rate per 10,000 corresponding population.

b 

Significant change from 2003-2005 to 2009-2011.

Table Graphic Jump Location
TABLE 2  ] Number and Average Annual Rate of Asthma Hospitalizations Among the General US Population, 2003-2005 and 2009-2011

See Table 1 legend for expansion of abbreviation.

a 

Unadjusted rate per 10,000 corresponding population.

b 

Significant change from 2003-2005 to 2009-2011.

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