Racial and Ethnic Differences of Influenza-Associated Pediatric Hospitalizations and Deaths,2008

Abstract

Background:

Influenza is one of the most common causes of acute respiratory infections in children; its complications are a leading cause of morbidity and mortality. There is a paucity of pediatric data on influenza disparities among racial/ethnic minorities. Our study assesses if there are racial/ethnic differences in hospitalizations and mortality in children infected with influenza.

Methods:

This was a retrospective cohort study using the National Inpatient Sample (NIS) from January 1, 2008 to December 31, 2017. We included children 18 years and younger hospitalized with a primary or secondary diagnosis of influenza or its subtypes. We generated adjusted odds ratios (aORs) and 95% confidence intervals (CIs) to evaluate the associations between patient characteristics and influenza hospitalizations and influenza-related mortality.

Results:

There were 226,535 (0.04%) influenza-associated hospitalizations. When compared with non-Hispanic (NH) White children, minority children were more likely to be hospitalized with an influenza diagnosis [Hispanics (aOR = 1.25; 95% CI, 1.17 to 1.33), NH-Blacks (aOR = 1.21, 95% CI, 1.17 to 1.33) and NH-Others group (aOR = 1.11; 95% CI, 1.04 to 1.19)]. There was no racial/ethnic difference in mortality.

Conclusions:

Minority children experienced a higher likelihood of influenza-associated hospitalizations but not mortality. Further research is needed to reduce the racial/ethnic disparities of influenza's impact.

Introduction

Influenza is one of the most common causes of acute lower respiratory infections in children younger than 5 years old, and its complications represent a leading cause of morbidity and mortality.^1,2 In the United States, it is estimated that the annual influenza epidemics cause 300,000 hospitalizations and 35,000 deaths.^3,4 As many as 26,000 hospitalizations occur in children younger than 5 years old, and up to 188 deaths occur in the pediatric population.^3–5 In 2009, the H1N1 influenza virus made a devastating surge, and was responsible for as many as 575,400 deaths worldwide, particularly impacting children, with 358 pediatric deaths in the United States alone.^5,6

Previous literature on pediatric influenza-related illnesses provide information on contractility, hospitalization, and mortality rates during various influenza seasons.^5,7,8 However, there is a paucity of information on influenza disparities among racial and ethnic minorities, specifically in the pediatric population. Recent literature has examined influenza's effects on social determinants of health among racial and ethnic minority groups.^9–12 A specific focus on influenza associated hospitalizations and disparities in influenza vaccinations has been studied.^9–13 These studies revealed that African Americans/Blacks and Hispanics as well as those from lower socioeconomic statuses are more likely to be hospitalized from influenza, and less likely to receive flu vaccinations.^9–13

Although there have been improvements in reporting influenza-related racial and ethnic health disparities, there is still a gap in knowledge on influenza-associated racial and ethnic health differences among children. Accordingly, we conducted this study to evaluate if there are racial and ethnic differences in hospitalization and mortality in children infected with influenza.

Materials and Methods

Study design and data collection

This retrospective cohort study on the pediatric population was conducted using the National Inpatient Sample (NIS), the largest all-payer database of hospital admissions in the United States from January 1, 2008 to December 31, 2017. The NIS contains discharge data from ∼35 million hospitalizations annually (when weighted) and constitutes a 20% stratified sample of all US nonfederal, nonrehabilitation, short-term community hospitals. For each hospitalization, up to 30 diagnoses can be captured using International Classification of Diseases, Ninth Edition, Clinical Modification (ICD-9-CM) until September 31, 2015, and International Classification of Diseases, Tenth Edition, Clinical Modification (ICD-10-CM) codes from October 1, 2015 until date. The NIS lacks patient identifiers that allow the linkage of hospitalizations for the same patient over time; the unit of analysis is the hospitalization, or discharge, as opposed to the individual. Because NIS data are publicly available and de-identified, this study was approved as exempt by our institution's Institutional Review Board.

The study sample comprised hospitalizations of patients 18 years and younger. Influenza-related hospitalizations were captured based on the presence of the diagnosis codes indicative of influenza: ICD-9: 487 and ICD-10: J11.1. In addition, based on the diagnosis codes for the following influenza subtypes (1) influenza with pneumonia: ICD-9: 487.0, ICD-10: J11.0x; (2) influenza with respiratory manifestations: ICD-9: 487.0, ICD-10: J11.1x; and (3) influenza with other manifestations: ICD-9: 487.0, ICD-10: J11.2x, J11.81, J11.89. We categorized patients' ages in groups of 0–4, 5–9, 10–14, and 15–18 years old. Ethnicity was initially stratified based on self-report [Hispanic, non-Hispanic (NH)], and the NH group was then subdivided into White, Black, or Other. The primary payer for the hospitalization was grouped into Medicare, Medicaid, private, self-pay, and other (including underinsured/uninsured). As a proxy for socioeconomic status, the Healthcare Cost and Utilization Project provides zip code-level estimates of median household income, grouped into quartiles based on the patient's residence. Hospital factors included census region (Northeast, Midwest, South, West), bed size (small, medium, large), and hospital type (rural, urban nonteaching, urban teaching).

Statistical analysis

We explored temporal trends of hospitalizations related to influenza and its subtypes using joinpoint regression, which is a statistical modeling approach designed to detect changes in the rates of events over time. Using joinpoint regression, we also calculated trends in hospitalization rates and in-hospital mortality rates among those with influenza by race/ethnicity. We used descriptive statistics to capture the frequency distribution of patient and hospital characteristics among influenza-related hospitalizations. In each patient and hospital characteristic subgroup, we also calculated the prevalence of influenza per 10,000 hospitalizations. Next, we calculated the prevalence of influenza and its subtypes across various racial/ethnic groups.

Finally, we used survey logistic regression to generate adjusted odds ratios (aORs) and 95% confidence intervals (CIs) that measured the independent associations between various patient hospitalization characteristics (exposure) and influenza hospitalizations (outcome). We also examined the factors associated with inpatient mortality among influenza patients. We adopted a 5% type I error rate for calculation of CIs and used appropriate survey weighting to generate national prevalence estimates considering the complex sampling design of the NIS. Statistical analyses were performed using R (version 3·6·1) and RStudio (Version 1·2·5001), whereas the trends analyses were run using Joinpoint Regression Program, version 4.7.0.0 (National Cancer Institute).

Results

Over the 10-year study period, there were a total of 57,001,204 pediatric hospitalizations of which 226,535 (0.04%) were associated with influenza (Table 1). Among hospitalized children diagnosed with influenza, those younger than 5 years old comprised 65% of influenza-associated hospitalizations. However, children 5–9 years old had the highest prevalence of influenza-associated hospitalizations (156/10,000 hospitalizations). We also noted differences in sex with a higher prevalence of influenza-related hospitalizations among males (43/10,000 hospitalizations).

Table 1.

Demographic Characteristics of Hospitalized Children With and Without Influenza

	Influenza				Prevalence of influenza per 10,000 hospitalizations
	No (N = 56,774,669), % = 99.6		Yes (N = 226,535), % = 0.04
	n	%	n	%
Patient characteristics
Age, years
0–4	46,937,789	82.7	147,544	65.1	31.34
5–9	2,805,055	4.9	44,476	19.6	156.08
10–14	3,156,830	5.6	22,273	9.8	70.06
15–18	3,874,995	6.8	12,242	5.4	31.49
Sex
Male	28,976,821	51.0	126,237	55.7	43.38
Female	27,692,555	48.8	99,889	44.1	35.94
Missing	105,293	0.2	407	0.2	38.51
Race
NH-White	25,707,325	45.3	89,594	39.5	34.73
NH-Black	7,611,551	13.4	40,574	17.9	53.02
Hispanic	10,682,689	18.8	51,283	22.6	47.78
NH-Other^a	5,862,385	10.3	21,758	9.6	36.98
Missing	6,910,719	12.2	23,325	10.3	33.64
Zip income quartile
Lowest quartile	16,266,480	28.7	83,934	37.1	51.33
Second quartile	14,057,737	24.8	54,350	24.0	38.51
Third quartile	13,480,596	23.7	46,005	20.3	34.01
Highest quartile	11,982,995	21.1	36,973	16.3	30.76
Primary payer
Medicare	153,060	0.3	973	0.4	63.17
Medicaid	26,973,587	47.5	133,187	58.8	49.13
Private insurance	25,469,770	44.9	78,366	34.6	30.67
Self pay	4,078,132	7.2	13,683	6.0	33.44
Discharge status
Routine	53,730,365	94.6	214,879	94.9	39.83
Transfer	1,326,859	2.3	5,328	2.4	39.99
Died	204,272	0.4	722	0.3	35.22
DAMA	40,269	0.1	182	0.1	44.99
Hospital characteristics
Hospital region
Northeast	9,463,603	16.7	37,495	16.6	39.46
Midwest	12,098,858	21.3	41,261	18.2	33.99
South	21,758,889	38.3	103,169	45.5	47.19
West	13,453,319	23.7	44,609	19.7	33.05
Hospital bed size
Small	7,618,276	13.4	31,260	13.8	40.87
Medium	15,516,460	27.3	53,806	23.8	34.56
Large	33,305,292	58.7	139,733	61.7	41.78
Hospital location and teaching status
Rural	5,256,304	9.3	26,291	11.6	49.77
Urban nonteaching	16,477,832	29.0	44,894	19.8	27.17
Urban teaching	34,705,892	61.1	153,614	67.8	44.07
Missing	334,642	0.6	1,734	0.8	51.55

NH-Other group consists of: Asian/Pacific Islander, Native American, and Multiple races group.

NH, non-Hispanic; DAMA, discharged against medical advice.

NH-Whites had the lowest prevalence of influenza-associated hospitalizations at 34 per 10,000 hospitalizations. In contrast, NH-Blacks had the highest prevalence of influenza-related hospitalizations at 53 per 10,000 hospitalizations, followed by Hispanics at 47 per 10,000 hospitalizations, and the NH-Other group (comprising Asian/Pacific Islander, Native American, and Multiple races) at 37 per 10,000 influenza-associated hospitalizations. We noted racial/ethnic differences with NH-Blacks and Hispanics showing higher percentages of influenza-associated hospitalizations than NH-Whites and NH-Other racial group.

We also found differences in socioeconomic statuses with a higher prevalence of influenza-related hospitalizations among children from the lowest income quartile than the highest income quartile (51/10,000 versus 31/10,000 hospitalizations) (Table 1). About 59% of children hospitalized with an influenza infection were on Medicaid; however, children with Medicare had the highest prevalence of influenza-associated hospitalizations (63/10,000 hospitalizations). Ninety-five percent of children were routinely discharged, and the mortality rate was 0.3%.

The highest prevalence of children with influenza-associated hospitalizations were admitted to large hospitals (42/10,000 hospitalizations) compared with small hospitals; in rural areas (50/10,000 hospitalizations) compared with urban teaching centers, located in the Southern region of the country (47/10,000 hospitalizations) compared with the Northeast (Table 1).

The trends in hospitalizations for children with influenza infections remained consistent over the study period with an average annual percentage change (AAPC) of 0.8 (95% CI, −9.7 to 12.6) (Fig. 1). For the influenza subgroups, there were no significant findings in the AAPC for influenza with respiratory symptoms or influenza with pneumonia (Fig. 1). However, there had been a decline in hospitalizations associated with influenza with other manifestations (AAPC: −16, 95% CI, −28.4 to −1.4).

FIG. 1.

Trends in rates of Influenza and Influenza subtypes: 2008–2017 (per 10,000 hospitalization). Influenza with other manifestations consists of influenza with gastrointestinal symptoms, central nervous system symptoms and nonrespiratory symptoms. * represents statistically significant (p-value < 0.05) finding.

There were differences in the prevalence of influenza and influenza subtypes among racial and ethnic groups (Fig. 2). For influenza infections, NH-Blacks had the highest prevalence of admissions at 53 per 10,000 hospitalizations versus NH-Whites with the lowest prevalence at 35 per 10,000 hospitalizations. NH-Black children also had the highest admission rate for influenza with respiratory manifestations at 39 per 10,000 hospitalizations. Hispanic and NH-Black children had similar rates of hospitalizations for influenza with pneumonia at 12.5 and 12.3 per 10,000 hospitalizations, respectively; there was no racial/ethnic difference in the rate of hospitalization for children admitted with influenza and other manifestations. When we assessed the 10-year trends for each racial and ethnic group, there was no difference in the average annual percent change (Supplementary Fig. S1).

FIG. 2.

Prevalence of influenza and influenza subtypes among racial/ethnic groups (per 10,000 hospitalizations). Other group consists of: Asian/Pacific Islander, Native American, and Multiple races group.

Compared with NH-Blacks and Hispanics, we noted increasing trends in mortality rates for NH-Whites and NH-Other racial group; however, there was no statistical difference among each group's AAPC (Supplementary Fig. S2). However, during the year 2010, encompassing the 2009 H1N1 pandemic, all minority children experienced at least five times the rate of inpatient mortality compared with NH-White children (Supplementary Table S1).

After adjustment for covariates, and compared with 15- to 19-year-old adolescents, those <5 years old, and those 5–9 years old were more likely to be hospitalized (aOR = 2.18; 95% CI, 2.06 to 2.30 and aOR = 4.71; 95% CI, 4.43 to 5.02, respectively; Table 2). In addition, males were 17% more likely to be hospitalized for influenza compared with females (aOR: 1.17, 95% CI, 1.15 to 1.19). Patients in the lowest income quartile experienced 19% elevated adjusted odds for influenza-related hospitalization compared with those in the highest income quartile. Insurance status was also predictive of influenza-related hospitalization. Contrary to those with private insurance, patients on Medicaid were 1.37 times as likely to be hospitalized, and among all insurance groups, those on Medicare had the highest adjusted odds of requiring hospitalization associated with influenza infection (aOR = 1.79; 95% CI, 1.05 to 3.06).

Table 2.

Association Between Sociodemographic Characteristics (Exposures) and Influenza and In-Hospital Death by Influenza (Outcomes)

	Influenza	In-hospital death by influenza
	OR (95% CI)	OR (95% CI)
Patient characteristics
Race
NH-White	Reference
NH-Black	1.21 (1.13 to 1.3)	0.54 (0.13 to 2.27)
Hispanic	1.25 (1.17 to 1.33)	0.85 (0.21 to 3.53)
NH-Other^a	1.11 (1.04 to 1.19)	0.71 (0.11 to 4.53)
Sex
Female	Reference
Male	1.17 (1.15 to 1.19)	0.42 (0.13 to 1.31)
Age, years
15–18	Reference
10–14	1.00 (0.94 to 1.05)	—
5–9	4.71 (4.43 to 5.02)	—
0–4	2.18 (2.06 to 2.3)	1.01 (0.73 to 1.39)
Zip income quartile
Highest quartile	Reference
Lowest quartile	1.19 (1.09 to 1.3)	3.71 (0.59 to 23.37)
Second quartile	1.04 (0.98 to 1.11)	1.31 (0.41 to 4.24)
Third quartile	1.01 (0.96 to 1.06)	3.26 (0.27 to 38.96)
Primary payer
Private insurance	Reference
Medicare	1.79 (1.05 to 3.06)	7.02 (6.08 to 8.10)
Medicaid	1.37 (1.33 to 1.41)	0.65 (0.17 to 2.49)
Self pay	0.99 (0.91 to 1.06)	0.38 (0.04 to 4.21)
Hospital characteristics
Hospital location and teaching status
Urban teaching	Reference
Rural	1.23 (1.11 to 1.36)	1.08 (0.05 to 23.02)
Urban nonteaching	0.73 (0.63 to 0.85)	1.29 (0.16 to 10.24)
Hospital bed size
Small	Reference
Medium	0.87 (0.74 to 1.02)	12.12 (0.79 to 185.32)
Large	1.01 (0.87 to 1.17)	33.16 (2.56 to 429.85)
Hospital region
Northeast	Reference
Midwest	0.92 (0.8 to 1.05)	—
South	1.17 (1.02 to 1.34)	—
West	0.9 (0.76 to 1.05)	—

NH-Other group consists of: Asian/Pacific Islander, Native American, and Multiple races group.

CI, confidence interval; OR, odds ratio.

In comparison with the Northeast, children admitted in the South were 17% more likely to be hospitalized with an influenza infection. In addition, those admitted to rural hospitals had increased adjusted odds of hospitalizations (aOR = 1.23; 95% CI, 1.11 to 1.36).

When compared with NH-White children, minority children were more likely to be hospitalized with an influenza diagnosis [Hispanics (aOR = 1.25; 95% CI, 1.17 to 1.33), NH-Blacks (aOR = 1.21; 95% CI, 1.17 to 1.33) and NH-Others group (aOR = 1.11; 95% CI, 1.04 to 1.19)]. There was no racial/ethnic difference in influenza-related mortality. Finally, higher likelihood of influenza-related mortality was noted among children on Medicare (aOR = 7.02; 95% CI, 6.08 to 8.10) and those admitted to large hospitals (aOR = 33.16; 95% CI, 2.56 to 429.85).

Discussion

We conducted a retrospective cohort of 226,535 hospitalizations associated with influenza and evaluated sociodemographic characteristics, specifically racial/ethnic differences. Over the 10 years, we noted invariable trends and several differences in influenza-associated hospitalizations. First, when compared with NH-Whites, NH-Blacks and Hispanics had the highest percentage and prevalence of influenza-associated hospitalizations. In addition, there was no significant change in trends of influenza-related hospitalizations among racial/ethnic groups, thus highlighting persistent disparities. Second, children from the lowest income quartile had the highest prevalence and percentage of influenza-associated hospitalizations and those with Medicaid had the highest percentage of hospitalizations with influenza. Third, there was no racial/ethnic difference in inpatient influenza-associated mortality; however, there was an increase in mortality among children with Medicare.

Our first salient finding was the racial/ethnic differences in influenza-associated hospitalizations. When adjusted for covariates, minority children were more likely to be hospitalized with influenza than NH-White children. Furthermore, NH-Black and Hispanic children had the highest prevalence of hospitalizations. Specifically, NH-Black children had the highest prevalence for most subtypes of influenza infections (influenza, influenza with respiratory manifestations, and influenza with other manifestations); the diagnosis of influenza with pneumonia was highest in Hispanics. These findings are consistent with previous studies that have shown higher rates of hospitalizations for NH-Black children and Hispanic children, specifically during the 2009 H1N1 pandemic.^14,15 One study showed that during 2002–2009 and among three US counties, 8% of Black children were hospitalized from influenza in contrast to 6% of White children.¹⁶ The racial/ethnic differences in influenza-associated hospitalizations could be owing to a number of reasons such as: minority children becoming sicker because of limited access to health care, having more complications from influenza owing to other comorbidities (ie, asthma), or having less access to influenza vaccinations owing to limited resources and/or vaccine hesitancy. There have been reports of lower vaccination rates among minority children.^12,17 Influenza vaccination is the most significant factor for preventing influenza infection and its complications.^5,18 With these disparities in vaccination status, a child from a minority group is vulnerable to influenza-related complications and hospitalizations.⁵

Second, when compared with children with the highest income, children from the lowest income quartile and those with Medicaid had the highest percentage of influenza-associated hospitalizations. A previous study that took place in New Haven, Connecticut is consistent with our finding and revealed that children living in high-poverty and high-crowded areas were at least three times as likely to experience influenza-associated hospitalizations compared with low-poverty and low-crowded areas.⁹ This difference is attributable to children from lower socioeconomic status having a lower probability of being insured, which can lead to a lack of health care resources, a delay in health care resulting in complications from preventable influenza complications.¹⁹ In addition, limited access and availability to influenza vaccinations associated with lower income status influence influenza-associated hospitalizations.^9,19

Third, over our 10-year study period, there was a rising trend in influenza-associated mortality among NH-Other group and NH-White children, but overall, there was no racial/ethnic difference in influenza-associated mortality. One study assessed children older than 6 years and showed that Native Hawaiians/Pacific Islanders, American Indians, and Alaskan children had the highest rates of mortality.⁸ For our study in 2010, when compared with NH-White children, all minority children were five times as likely to experience inpatient mortality. This difference could be reflective of the effects from the 2009 H1N1 pandemic, which took place from October 1, 2008 to August 29, 2009 and August 30, 2009 through September 30, 2010.⁷ Our results differ from previous studies, which revealed that during the 2009 H1N1 pandemic, NH-White children had the highest rate of mortality.^20,21 The divergence in study results could be owing to the timeframe of the pandemic, with our results from 2010 reflecting the second half of the 2009 H1N1 pandemic. Finally, in our study, children with Medicare were more likely to experience inpatient mortality. An explanation could be that these children suffer from debilitating chronic health conditions that place them at a higher risk of mortality. Prior studies also revealed that children with chronic conditions, specifically neurologic, chromosomal, and genetic abnormalities, were more likely to experience death, when also diagnosed with influenza.^7,8

There are several limitations to our study. For one, the NIS database does not include patient identifiers; thus, our analysis was based on hospitalizations instead of individuals. In addition, admission events with influenza were derived from a retrospective review of inpatient influenza admission diagnoses, which implies that some patients might have been misclassified. Second, hospitalizations were associated with an influenza diagnosis, which does not necessarily represent a causal relationship because exposure-outcome sequence (other than mortality) could not be ascertained. In addition, we had no data on influenza testing status; thus, our analysis may also encompass clinical diagnoses of influenza, reflecting a heterogenous population. Finally, differences in molecular testing among hospitals can pose variability and the possibility of misclassification from chronic shedding rather than an active influenza infection.

Conclusion

Our study provides updated information regarding racial/ethnic and socioeconomic differences in influenza-associated pediatric hospitalizations and mortality. Our results showed increase disparities in hospitalizations in minority children, those from lower socioeconomic statuses and elevated mortality in children with Medicare. Our data underscore the need for greater knowledge diffusion and targeted interventions that are crucial in combating the impact of influenza on children, especially those from lower socioeconomic statuses and minority racial groups. Future interventions relative to public health and policy changes focusing on improving access to health care, vaccination, and improving health literacy will be needed to narrow the racial/ethnic gap of influenza's disproportionate adverse impact noted in this study.

Footnotes

Acknowledgments

The authors thank Derek Lockett II, BS, Gabriella Tavera, BS, and Christopher Largaespada, BS for their writing assistance.

Author Disclosure Statement

The authors declare that there is no conflict of interest.

Funding Information

This work was supported by Grant No. 1 D34HP31024-01-00 from the Health Resources and Services Administration (HRSA).

Supplementary Material

References

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Supplementary Material

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Racial and Ethnic Differences of Influenza-Associated Pediatric Hospitalizations and Deaths,2008–2017

Abstract

Background:

Methods:

Results:

Conclusions:

Introduction

Materials and Methods

Study design and data collection

Statistical analysis

Results

Discussion

Conclusion

Footnotes

Acknowledgments

Author Disclosure Statement

Funding Information

Supplementary Material

References

Supplementary Material