Influenza is a highly contagious respiratory tract infection caused by the influenza virus.1 Commonly known as the flu, the onset of symptoms is abrupt and can last anywhere from a few days to 2 weeks. Most people recover without incident, but many develop severe, life-threatening complications that often lead to death.1 Although a vaccine-preventable disease,2,3 influenza nevertheless remains a serious threat to public health, resulting in hundreds of thousands of hospitalizations and thousands of deaths in the United States every year.4,5
However, the burden of influenza-related morbidity and mortality is not evenly distributed throughout the United States. In addition to risks common to the general population,1,6,7 American Indians and Alaskan Natives (AI/ANs) are the only racial or ethnic group that is uniquely considered at risk for influenza-related complications.7 While the reasons for this are complex and poorly understood, the impact of influenza among AI/ANs is unmistakable.
Over the last century, there have been 4 major influenza pandemics in the United States: 1918, 1957-1958, 1968, and 2009.8 During each of these outbreaks, AI/ANs suffered significantly higher rates of influenza-related mortality than any other racial or ethnic group.9–11 During the pandemic of 1918 (which resulted in 80-100 million deaths worldwide12), entire AI/AN communities were decimated13–15 whereas in 2009, AI/ANs accounted for nearly 10% of all influenza-related deaths in the country9 despite representing just 3% of the overall population.16
Because of this unique risk, it is necessary to better understand the burden of influenza among AI/ANs. Our intent, therefore, was to examine the frequency and distribution of influenza-related mortality among AI/ANs from 1999 to 2016, especially as compared with non-Hispanic whites (NHWs).
Using publicly available mortality data,17*,18† we analyzed deaths from 1999 to 2016 that were most closely linked to influenza and influenza-like illness (nonspecific respiratory illnesses that cannot be attributed to other causes). We examined data available from 1999 to 2016 due to changes in racial classification for mortality reporting instituted in 1999.
Crude mortality rates for both AI/ANs and NHWs were calculated per 100 000. Population denominators for NHWs were taken from the April 1 census counts for 2000 and 2010 and postcensal estimates for all other years. Bridged-race estimates were used for AI/ANs.
As influenza disproportionately affects younger and older populations,5,6 crude rates were used to capture the impact of influenza-related mortality across all age categories. These rates were analyzed by states to assess the geographic distribution of influenza-related deaths throughout the United States.
Proportional differences between groups were analyzed for statistical significance using χ2 tests of independence or Fisher's exact test for groups of less than 30. Statistical significance was defined at the P < .05 level, while 95% confidence interval (CI) bound odds ratios were further calculated where appropriate to capture the direction and magnitude of statistically significant differences. All analysis was conducted using R 220.127.116.11
The AI/AN mortality rate for all years was 28.5 per 100 000 (95% CI, 26.1-30.9). The lowest rate occurred in Maryland (1.8; 95% CI, 1.6-6.2), whereas the highest rate occurred in South Dakota (56.9; 95% CI, 41.3-77.4). Overall, mortality rates dropped from 35.6 (95% CI, 32.5-38.7) in 1999 to 24.5 (95% CI, 22.5-26.5) in 2016, with an overall low of 23.6 (95% CI, 21.6-25.7) in 2012 and an overall high of 35.7 (95% CI, 32.8-38.6) in 2003. When compared with the NHW population, AI/ANs had a 2.7 times greater risk of dying from influenza-related complications during the same time period.
Significant disparities existed within the AI/AN population when the geographic distribution of mortality was examined (Table); when compared with their overall AI/AN population, a disproportionately higher burden was found in states such as South Dakota, Montana, and North Dakota.
Year-to-year, most states experienced varying mortality rates, although some states did not record any influenza-related deaths for certain years. Furthermore, significant spikes were seen in multiple years (2005, 2011, 2013, and 2015) outside of the Centers for Disease Control and Prevention (CDC)–defined high-severity flu years in 2003, 2009, and 2014.20
Impact on At-Risk Populations
Because AI/ANs are the only racial or ethnic group that is identified as an at-risk population, many of the risk factors that affect the general population could have a compounded effect on the AI/AN population. This seemed particularly true when examining differences between age categories. Younger and older people are at higher risk for developing influenza-related complications, and although AI/AN births make up roughly 1.7% of total births, AI/AN infants younger than 1 year made up approximately 3% of total influenza-related deaths. Still, AI/AN under-5 mortality rates decreased significantly from 30.7 (95% CI, 12.9-61.9) in 1999 to 7.8 (95% CI, 1.7-22.5) in 2016. These decreases were not commensurate, however, with rate decreases experienced by NHWs for the same age groups. From 1999 to 2016, the AI/AN mortality rate for children aged 1 through 4 years was 2.1 times higher than NHWs whereas the rate for infants younger than 1 year was 2.5 times higher than for NHWs. As a result, influenza-related mortality remains a leading cause of death among AI/AN infants and children.21,22
Similar disparities were seen among adults. Mortality rates among AI/ANs climbed steadily beginning at 35 years of age, but similar increases were not seen among NHWs until 75 years of age, resulting in a significantly higher burden of influenza-related mortality among AI/AN adults beginning at earlier ages.
The steady decline in AI/AN influenza-related mortality rates was likely influenced by the increase in the overall AI/AN population, which grew by 53.9% from 1999 to 2016. Because of racial misclassification and underreporting, however, the true burden of AI/AN mortality is likely higher.23,24 It is also concerning that spikes in mortality were observed across multiple years and did not seem to correspond to CDC-identified moderate or severe flu seasons. This could indicate a trend of more common outbreaks among AI/ANs that is not otherwise being captured or reported.
Disparities between AI/ANs and NHWs reflect differences in life expectancies between the two groups. Lower life expectancies among AI/ANs are well-established and are representative of multiple risk factors that disproportionately affect the AI/AN population.25 Many risk factors are shared with an increased influenza-related risk, including chronic disease and various social determinants of health.26 The relationship between these and other health-related indicators was not explored in this analysis but represents an opportunity for additional research.
The disproportionate geographic distribution of influenza-related mortality was also concerning. Of the states listed in the Table, only half were among the 10 states with the highest AI/AN populations. Conversely, states such as Montana, Wisconsin, and North Dakota represent some of the smallest AI/AN populations in the country but had some of the highest mortality rates.
Furthermore, spikes in mortality seemed to follow a disproportionate geographic distribution, with a number of states experiencing higher rates of influenza-related mortality in multiple years than both the general AI/AN and NHW populations. Geography has been suggested as one potential determinant of influenza-related mortality,10,11,27 and the uneven geographic burden of influenza-related mortality seen among certain AI/AN communities during the measurement period could support this hypothesis.
Our study had some limitations. Estimating seasonal influenza-related mortality in the United States can be difficult. States are not required to report individual flu cases or deaths of people older than 18 years, and influenza is often misclassified on death certificates.23,24 This is further hampered by significant degrees of racial misclassification and underreporting of both morbidity and mortality data among the AI/AN population.28,29
Despite under-researched distributions and determinants of influenza-related mortality among AI/AN, influenza-related deaths represent vaccine-preventable mortality.2,3,28 Still, only 42% of AI/ANs were vaccinated in 2016 compared with 48% of the NHW population.29 In addition, vaccination rates vary significantly among AI/AN communities, which could help explain the uneven geographic distribution of influenza-related mortality.
Vaccinations are likely just one of many factors that contribute to the disproportionate number of influenza-related deaths within the AI/AN population. The complexity and relationship between these factors are poorly understood, however, and represent an important area for further research. Tribal Epidemiology Centers in coordination with CDC and the Indian Health Service are uniquely positioned to help better understand these complex relationships. This, along with ongoing regular surveillance and improved reporting of influenza-related morbidity and mortality, would provide a more comprehensive picture of the burden of influenza in the AI/AN population.
Implications for Policy & Practice
- Influenza-related mortality is vaccine-preventable. Health care providers should encourage vaccinations and implement vaccine programs when possible.
- The reason for disproportionate rates of influenza-related mortality in the AI/AN population represents an area of limited research.8 Complex correlations between common risk factors such as vaccination rates, age, chronic disease status, and social determinants of health should be further explored.
- A better understanding of the geographic distribution of influenza-related mortality is needed, especially as it relates to the aforementioned risk factors.
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17. Centers for Disease Control and Prevention, National Center for Health Statistics. Multiple cause of death 1999-2016 on CDC WONDER Online Database, released December, 2017. http://wonder.cdc.gov/mcd-icd10.html
. Accessed October 10, 2018.
18. Centers for Disease Control and Prevention, National Center for Health Statistics. Multiple Cause of Death 1999-2016. Atlanta, GA: Centers for Disease Control and Prevention; 2017.
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. Accessed October 14, 2018.
21. Urban Indian Health Institute, Seattle Indian Health Board. Community Health Profile: National Aggregate of Urban Indian Health Program Service Areas. Seattle, WA: Urban Indian Health Institute; 2016.
22. Wong CA, Gachupin FC, Holman RC, et al American Indian
and Alaska native infant and pediatric mortality
, United States, 1999-2009. Am J Public Health. 2014;104(suppl 3):S320–S328.
23. Jim MA, Arias E, Seneca D, et al Racial misclassification of American Indians and Alaska Natives
by Indian Health Service contract health service delivery area. Am J Public Health. 2014;104(suppl 3):S295–S302.
24. Arias E, Heron M; National Center for Health Statistics, Hakes J; US Census Bureau. The validity of race and Hispanic-origin reporting on death certificates in the United States: an update. Vital Health Stat. 2016;(172):1–21.
25. Arias E, Xu J, Jim MA. Period life tables for the non-Hispanic American Indian
and Alaska Native population, 2007-2009. Am J Public Health. 2014;104(suppl 3):S312–S319.
26. Groom AV, Hennessy TW, Singleton RJ, Butler JC, Holve S, Cheek JE. Pneumonia and influenza mortality
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27. Mamelund S. Geography may explain adult mortality
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28. Centers for Disease Control and Prevention. Estimated Influenza
Illnesses, Medical Visits, Hospitalizations, and Deaths Averted by Vaccination
in the United States. Atlanta, GA: Centers for Disease Control and Prevention, US Department of Health and Human Services; 2016.
29. Centers for Disease Control and Prevention. Behavioral Risk Factor Surveillance System Survey Data. Atlanta, GA: Centers for Disease Control and Prevention, US Department of Health and Human Services; 2016.
* Data are from the Multiple Cause of Death Files, 1999-2016, as compiled from data provided by the 57 vital statistics jurisdictions through the Vital Statistics Cooperative Program.
† Data are compiled from data provided by the 57 vital statistics jurisdictions through the Vital Statistics Cooperative Program.