Abstract
Objective
To investigate racial inequities in the use of therapeutic hypothermia (TH) and outcomes in infants with hypoxic ischemic encephalopathy (HIE).
Study design
We queried an administrative birth cohort of mother-baby pairs in California from 2010 through 2019 using ICD codes to evaluate the association between race and ethnicity and the application of TH in infants with HIE. We identified 4,779 infants with HIE. Log-linear regression was used to calculate risk ratios (RR) for TH, adjusting for hospital transfer, rural location, gestational age between 35 and 37 weeks, and HIE severity. Risk of adverse infant outcome was calculated by race and ethnicity and stratified by TH.
Results
From our identified cohort, 1338 (28.0%) neonates underwent TH. White infants were used as the reference sample and 410 (28.4%) received TH. Black infants were significantly less likely to receive TH with 74 (20.0%) with an adjusted risk ratio (aRR) of 0.7 (95% confidence interval 0.5 to 0.9). Black infants with any HIE who did not receive TH were more likely to have a hospital readmission (aRR 1.36, 95% CI 1.10 to 1.68) and a tracheostomy (aRR 3.07, 95% CI 1.19 to 7.97). Black infants with moderate/severe HIE who did not receive TH were more likely to have cerebral palsy (aRR 2.72, 95% CI 1.07 to 6.91).
Conclusions
In this study cohort, Black infants with HIE were significantly less likely to receive TH. Black infants also had significantly increased risk of some adverse outcomes of HIE. Possible reasons for this inequity include systemic barriers to care and systemic bias.
Keywords: Bias, Structural Racism
In the last decade, there has been increased awareness and investigation of inequities in the medical treatment and outcomes of minoritized populations in the United States. While race and ethnicity are a social construct rather than a biological reality, self-identified and perceived race and ethnicity have a significant impact on a patient’s health and care. Previous studies have shown evidence of inequities in the clinical outcomes of Black and Hispanic infants. For example, premature Black and Hispanic infants have higher rates of mortality and severe morbidity such as necrotizing enterocolitis.1,2,3 These previous studies have demonstrated inequities in the outcomes of infants based on race and ethnicity in neonatal intensive care units (NICUs) and demonstrate a trend that may extend to other disease processes, including outcomes of neurological disorders such as neonatal hypoxic ischemic encephalopathy (HIE). Additionally, inequities of outcomes may also extend to inequities in treatment, such as the treatment of HIE with therapeutic hypothermia.
HIE occurs in approximately 1 to 8 per 1000 births in developed countries and is a significant neurological cause of morbidity and mortality in infants.4 Using the same dataset as in this study, Bandoli et al (2022) evaluated maternal factors that may impact an infant receiving a diagnosis of neonatal encephalopathy and showed that “substance-related diagnosis, preexisting diabetes, preeclampsia, and any maternal infection were associated with a two-fold increase in risk”.5 Survivors of HIE can experience lifelong complications including cerebral palsy. HIE is the most common cause of neonatal encephalopathy and occurs due to globally decreased blood flow to the brain during a hypoxic-ischemic perinatal event. Injury occurs initially due to acute hypoxia, and further injury occurs in the subsequent hours and days from reperfusion injury, edema, and secondary energy failure.4 Multiple clinical trials have shown that therapeutic hypothermia decreases morbidity and mortality in infants with HIE in high income countries.6 Currently, the only standard treatment for neonatal HIE is therapeutic hypothermia.6,7,8 At present there is a gap in knowledge concerning inequities in the treatment and outcomes in neonatal HIE.
HIE represents an excellent opportunity to investigate racial/ethnic inequities in neurological disorders in the NICU. HIE is a significant cause of neonatal morbidity and mortality, and therapeutic hypothermia is the only standard treatment. However, the application of therapeutic hypothermia is at risk for inequity given the risk of implicit bias during the categorization of HIE which relies partly on physical exam findings and because therapeutic hypothermia is a limited resource not available in all hospitals. Therefore, the objective of this retrospective cohort study was to investigate whether there were racial or ethnic inequities in the treatment of HIE, measured by the receipt of therapeutic hypothermia, or adverse outcomes of neonates.
Methods
The sample was drawn from the Study of Outcomes in Mothers and Infants (SOMI) which consists of all California live born singleton infants delivered between 2010 and 2019 (n=4,869,099). Birth certificates, maintained by California Vital Statistics, were linked to hospital, emergency department (ED), and ambulatory surgery (AS) discharge records maintained by the California Department of Health Care Access and Information (HCAI). Hospital, ED, and AS discharge records provided ICD 9 and 10 diagnoses and procedure codes based on the International Classification of Diseases, as reported to HCAI by the health care facilities. HCAI records were linked for birthing person (“mothers”) for one year prior to birth to one year after birth and for the infant for up to one year after birth. The study sample was restricted to live born singleton infants with linked HCAI and vital statistics records (n=4,426,626). The sample was further restricted to deliveries at or after 35 weeks of gestation (n = 4,284,138) without major congenital anomalies (n = 4,164,863) with a diagnosis of neonatal HIE (n = 4,779. See supplemental materials for ICD codes). Anomalies were considered “major” if determined by clinical review as causing major morbidity and mortality that would likely be identified in the hospital at birth or lead to hospitalization during the first year of life.
Exposure and Outcomes
The exposure for this study was race and ethnicity of the infant, proxied by self-reported race and ethnicity of the mother who identified as Hispanic or not, and then if not Hispanic further reported as White, Black, Asian, or ‘Other race or ethnicity” (which included American Indian/Alaska Native, Native Hawaiian/Pacific Islander, other race, two or more races, and not stated/unknown). Treatment with therapeutic hypothermia was obtained from hospital discharge/ED/AS diagnostic codes (supplemental materials). Adverse infant outcomes for the study were defined as infant length of stay at birth admission of seven days or more, infant readmission within one year, gastrostomy, tracheostomy, cerebral palsy, newborn feeding problem, and/or infant death. Infant length of stay on birth admission, transfer from birth hospital, number of readmissions, and timing of readmission were gathered and calculated from HCAI patient discharge files. Gastrostomy, tracheostomy, cerebral palsy, and newborn feeding problem were obtained from hospital discharge/ED/AS diagnostic codes. Infant death and age at death were obtained from linked infant death records from California Vital Statistics and/or when infant discharge status indicated ‘died’ on HCAI records.
Covariates
Maternal and infant characteristics obtained from birth certificates included race and ethnicity, maternal age at delivery, maternal education, parity, and Medi-Cal payment for delivery (California’s Medicaid, health insurance for low-income persons). Best obstetric estimate of gestational age at birth was obtained from birth certificate records. County of maternal residence, also obtained from birth certificate records, was coded as rural where the National Center for Health Statistics Urban-Rural Classification Scheme for Counties indicated the county was small metro, micropolitan, or non-core (https://www.cdc.gov/nchs/data/series/sr_02/sr02_166.pdf).
Factors considered to potentially be associated with adverse outcomes of an infant with neonatal HIE included HIE severity, seizures/convulsions in the newborn, and infant sepsis. These factors were obtained from hospital discharge/ED/AS diagnostic codes.
Statistical Analysis
Sample diversity was described by race and ethnicity grouping, maternal age at delivery, maternal education, parity, and payer for delivery. Next, the crude and adjusted risk ratios (RR and aRR) and their 95% confidence intervals (CIs) for receipt of therapeutic hypothermia by maternal race and ethnicity. All RRs calculated were modeled using log-link binary regression with robust standard errors. Comparisons by race and ethnicity used people who identified as White, non-Hispanic as the reference group. White, non-Hispanic infants were used as the reference sample because historically clinical research has predominantly used a homogenous White, non-Hispanic population to produce a “baseline” without including data from racially and ethnically diverse populations. Models were adjusted for gestational age greater than or equal to 35 weeks and less than 37 weeks, transfer from birth hospital, rural county of residence, and severity of neonatal HIE (moderate/severe versus mild).
Crude RRs were calculated by race and ethnicity for factors associated with receipt of therapeutic hypothermia. These included delivery between 35 and 37 weeks gestational age, hospital transfer, rural residence, and severity of neonatal HIE. Crude RRs were also calculated by race and ethnicity for factors which may impact the occurrence of an adverse outcome separate from the diagnosis of HIE. These included severity of neonatal HIE, seizures and sepsis.
Next, risk of adverse outcomes among infants with HIE were examined by race and ethnicity separately among those treated with therapeutic hypothermia and those not treated, using the same methods. Models were adjusted for infant sepsis, neonatal HIE severity, and infant seizure. Adverse outcomes were examined as a composite (any adverse outcome versus none), as well as by length of stay for birth admission 7–14 days, 14 - < 30 days, and 30 or more days (versus < 7 days); any infant hospital readmission during the first year of life, 1 readmission, 2 readmissions, or 3 or more readmissions (versus no readmission); readmission within fewer than 4 days, between 4-<7 days, 7 - < 14 days, 14 - < 30 days, and 30 or more days from birth admission discharge (versus no readmission); newborn feeding problem (yes versus no); gastrostomy (yes versus no); tracheostomy (yes versus no); newborn feeding problem (yes versus no); cerebral palsy (yes versus no); and infant death within 1 year or within 30 days (versus no infant death). Newborn feeding problem and gastrostomy placement were both included to better characterize the spectrum of severity of feeding problems affecting infants with HIE. Adverse outcomes were also separately analyzed for moderate/severe HIE, excluding mild HIE. This separate analysis was done because most infants with moderate/severe HIE should qualify for therapeutic hypothermia.
All analyses were performed using Statistical Analysis Software version 9.4 (Cary, NC). Methods and protocols for the study were approved by the Committee for the Protection of Human Subjects within the Health and Human Services Agency of the State of California, and by the institutional review board at the University of California San Diego.
Results
The sample included 4,779 infants with neonatal HIE and was predominately White, non-Hispanic or Hispanic (71.5%), with maternal age between 18–34 years at delivery (75.0%), and more than 12 years maternal education (56.0%). Over 40% of the sample participated in Medi-Cal for payment for delivery (Table I).
Table 1.
Sample characteristics of infants with HIE
| n (%) | |
|---|---|
| Sample | 4,779 |
| Race and ethnicity | |
| White, non-Hispanic | 1,446 (30.3) |
| Hispanic | 1,968 (41.2) |
| Black | 370 (7.7) |
| Asian | 641 (13.4) |
| Other race and ethnicity | 349 (7.3) |
| Maternal age at delivery | |
| < 18 years | 75 (1.6) |
| 8 – 34 years | 3,585 (75.0) |
| >34 years | 1,119 (23.4) |
| Education | |
| < 12 years | 691 (14.5) |
| 12 years | 1,129 (23.6) |
| > 12 years | 2,677 (56.0) |
| Nulliparous | 2,458 (51.4) |
| Medi-Cal payer for delivery | 2,080 (43.5) |
With respect to the primary outcome, the rate of treatment did differ depending on race and ethnicity. While 28.4% of White, non-Hispanic infants received therapeutic hypothermia treatment, only 20.0% of Black infants (aRR 0.69, 95% CI 0.54 to 0.89) received therapeutic hypothermia. Of the 354 ‘other race and ethnicity’ infants, 37.0% received therapeutic hypothermia treatment (aRR 1.31, 95% CI 1.08 to 1.60). Likelihood of therapeutic hypothermia treatment did not significantly differ between Hispanic or Asian infants versus White, non-Hispanic infants (Table II).
Table 2.
Therapeutic hypothermia treatment by race and ethnicity
| Therapeutic hypothermia treatment | ||||
|---|---|---|---|---|
| Yes | No | |||
| n (row %) | n (row %) | cRR (95% CI) | aRR (95% CI) | |
| Sample (n = 4,779) | 1,338 (28.0) | 3,441 (72.0) | ||
| White, non-Hispanic (n = 1,446) | 410 (28.4) | 1,036 (71.7) | Reference | Reference |
| Hispanic (n = 1,968) | 524 (26.6) | 1,444 (73.4) | 0.94 (0.83, 1.07) | 0.93 (0.82, 1.06) |
| Black (n = 370) | 74 (20.0) | 296 (80.0) | 0.71 (0.55, 0.90) | 0.69 (0.54, 0.89) |
| Asian (n = 641) | 199 (31.1) | 442 (69.0) | 1.09 (0.92, 1.30) | 1.08 (0.91, 1.29) |
| Other race/ethnicity (n = 349) | 130 (37.3) | 219 (62.8) | 1.31 (1.08, 1.60) | 1.32 (1.09, 1.62) |
aRR adjusted for late preterm, transferred, rural, HIE severity
RR – crude risk ratio
aRR – adjusted risk ratio
When examining factors that may influence the decision to treat with therapeutic hypothermia, there were some differences by race and ethnicity. Asian infants were less likely to be born between 35 and 37 weeks gestational age than White, non-Hispanic infants (RR 0.71, 95% CI 0.51 to 0.99). Hispanic, Black, and Asian infants were less likely to live in a rural county compared with White, non-Hispanic infants (RRs 0.16 to 0.56). There was no significant difference by race and ethnicity in rate of transfer from birth hospital or severity of neonatal HIE (Supplemental table 1). There were no significant differences in diagnosis of seizure/convulsions of the newborn by race and ethnicity, although Hispanic and ‘other race and ethnicity’ infants were at higher risk of sepsis (RRs 1.24 – 1.32) (Supplemental table 2).
In risk adjusted models, there was no significant difference in adverse outcomes (hospital stay longer than 1 week, readmission, gastrostomy, tracheostomy, newborn feeding problem, cerebral palsy, death) in aggregate among infants who did not receive therapeutic hypothermia by race and ethnicity; however there were significant differences between groups when outcomes were evaluated individually (Table III). Hispanic infants were more likely to have a birth hospital stay of more than 30 days (aRR 1.75, 95% CI 1.26 to 2.43), a hospital readmission (aRR 1.28, 95% CI 1.12 to 1.48), and a tracheostomy (aRR 2.20, 95% CI 1.03 to 4.68) compared with White, non-Hispanic infants. Black infants were more likely to have a hospital readmission (aRR 1.36, 95% CI 1.10 to 1.68) and a tracheostomy (aRR 3.07, 95% CI 1.19 to 7.97). Asian and ‘other race and ethnicity’ infants did not statistically differ from White, non-Hispanic infants on any of the individual adverse outcomes measured. (Table III). When the analysis was restricted to infants with moderate/severe HIE who did not receive therapeutic hypothermia, Hispanic and Black infants were more likely to have three or more admissions in the first year of life (aRRs 3.90 and 4.06, respectively). Hispanic infants were more likely to receive a gastrostomy tube (aRR 2.02, 95% CI 1.11 to 3.66). Black infants with moderate/severe HIE who did not receive therapeutic hypothermia were more likely receive a tracheostomy (aRR 4.15, 95% CI 1.26 to 13.61) and, notably, were more likely to be diagnosed with cerebral palsy (aRR 2.72, 95% CI 1.07 to 6.91) (Supplemental Table 3).
Table 3.
Risk of adverse outcome for infants who were not cooled by race and ethnicity
| Non-Hispanic White | Hispanic | Black | Asian | Other | |
|---|---|---|---|---|---|
| n (%) | n (%) | n (%) | n (%) | n (%) | |
| cRR (95% CI) | cRR (95% CI) | cRR (95% CI) | cRR (95% CI) | ||
| aRR (95% CI) | aRR (95% CI) | aRR (95% CI) | aRR (95% CI) | ||
| Sample | 1,036 | 1,444 | 296 | 442 | 219 |
| Any adverse outcome * | |||||
| No | 183 (17.7 ) | 194 (13.4) | 43 (14.5) | 80 (18.1) | 40 (18.3) |
| Reference | |||||
| Reference | |||||
| Yes | 853 (82.3) | 1,250 (86.6) | 253 (85.5) | 362 (81.9) | 179 (81.7) |
| 1.05 (0.96, 1.15) | 1.04 (0.90, 1.19) | 0.99 (0.89, 1.12) | 0.99 (0.85, 1.17) | ||
| 1.05 (0.97, 1.15) | 1.04 (0.90, 1.19) | 1.00 (0.88, 1.13) | 0.99 (0.84, 1.17) | ||
| Length of stay for birth admission (including time at hospital of transfer) | |||||
| < 7 days | 401 (38.7) | 574 (39.8) | 133 (44.9) | 168 (38.0) | 81 (37.0) |
| Reference | |||||
| Reference | |||||
| Any stay of 7 days or more | 283 (47.2) | 682 (47.2) | 122 (41.2) | 218 (49.30 | 100 (45.7) |
| 0.99 (0.98, 1.12) | 0.88 (0.72, 1.07) | 1.03 (0.88, 1.21) | 1.01 (0.82, 1.26) | ||
| 1.00 (0.89, 1.13) | 0.88 (0.72, 1.07) | 1.03 (0.89, 1.22) | 1.02 (0.82, 1.27) | ||
| 7 - < 14 days | 312 (30.1) | 377 (26.1) | 71 (24.0) | 129 (29.2) | 69 (31.5) |
| 0.91 (0.78, 1.05) | 0.79 (0.61, 1.03) | 0.99 (0.81, 1.22) | 1.05 (0.81, 1.37) | ||
| 0.91 (0.79, 1.06) | 0.79 (0.62, 1.03) | 1.00 (0.81, 1.22) | 1.06 (0.81, 1.37) | ||
| 14 - < 30 days | 179 (17.3) | 256 (17.7) | 46 (15.5) | 89 (20.1) | 33 (15.1) |
| 1.00 (0.83, 1.21) | 0.84 (0.61, 1.16) | 1.14 (0.88, 1.47) | 0.94 (0.65, 1.36) | ||
| 1.03 (0.85, 1.25) | 0.86 (0.63, 1.20) | 1.18 (0.92, 1.53) | 0.98 (0.67, 1.42) | ||
| 30+ days | 50 (4.8) | 132 (9.1) | 21 (7.1) | 24 (5.4) | 9 (4.1) |
| 1.69 (1.22, 2.34) | 1.23 (0.74, 2.05) | 1.13 (0.69, 1.83) | 0.90 (0.44, 1.83) | ||
| 1.75 (1.26, 2.43) | 1.17 (0.70, 1.96) | 1.26 (0.77, 2.05) | 0.98 (0.48, 2.00) | ||
| Number of readmissions in first year of life | |||||
| None | 732 (70.7) | 897 (39.2) | 177 (59.8) | 321 (72.6) | 161 (73.5) |
| Reference | |||||
| Reference | |||||
| Any Readmission | 304 (29.3) | 547 (37.9) | 119 (40.2) | 121 (27.4) | 58 (26.5) |
| 1.29 (1.12, 1.49) | 1.37 (1.11, 1.69) | 0.93 (0.76, 1.15) | 0.90 (0.68, 1.20) | ||
| 1.28 (1.12, 1.48) | 1.36 (1.10, 1.68) | 0.94 (0.76, 1.16) | 0.89 (0.67, 1.18) | ||
| 1 | 221 (21.3) | 376 (26.0) | 77 (26.0) | 85 (19.2) | 35 (16.0) |
| 1.27 (1.08, 1.50) | 1.31 (1.01, 1.69) | 0.90 (0.70, 1.16) | 0.77 (0.54, 1.10) | ||
| 1.23 (1.05, 1.46) | 1.30 (1.01, 1.69) | 0.92 (0.71, 1.18) | 0.78 (0.54, 1.11) | ||
| 2 | 50 (4.8) | 86 (6.0) | 26 (8.8) | 23 (5.2) | 11 (5.0) |
| 1.37 (0.97, 1.94) | 2.00 (1.25, 3.22) | 1.05 (0.64, 1.71) | 1.00 (0.52, 1.92) | ||
| 1.26 (0.89, 1.79) | 1.74 (1.07, 2.83) | 1.04 (0.63, 1.71) | 0.98 (0.51, 1.90) | ||
| 3+ | 33 (3.2) | 85 (5.9) | 16 (5.4) | 13 (2.9) | 12 (5.5) |
| 2.01 (1.34, 3.00) | 1.92 (1.06, 3.49) | 0.90 (0.47, 1.71) | 1.61 (0.83, 3.11) | ||
| 1.56 (1.03, 2.35) | 1.68 (0.89, 3.16) | 0.82 (0.43, 1.57) | 1.46 (0.75, 2.85) | ||
| Time to first readmission after discharge from birth admission | |||||
| No readmissions | 732 (70.7) | 897 (39.2) | 177 (59.8) | 321 (72.6) | 161 (73.5) |
| Reference | |||||
| Reference | |||||
| < 4 days | 184 (17.8) | 311 (21.5) | 65 (22.0) | 77 (17.4) | 42 (19.2) |
| 1.28 (1.07, 1.54) | 1.34 (1.01, 1.77) | 0.96 (0.74, 1.26) | 1.03 (0.74, 1.44) | ||
| 1.22 (1.01, 1.46) | 1.32 (0.99, 1.75) | 0.97 (0.75, 1.27) | 1.02 (0.73, 1.42) | ||
| 4 - < 7 days | 13 (1.3) | 14 (1.0) | • | • | • |
| 0.88 (0.41, 1.87) | n/c | n/c | n/c | ||
| 0.86 (0.40, 1.83) | n/c | n/c | n/c | ||
| 7 - < 14 days | 24 (2.3) | 29 (2.0) | • | • | • |
| 0.99 (0.57, 1.69) | n/c | n/c | n/c | ||
| Didn’t converge | n/c | n/c | n/c | ||
| 14 - < 30 days | 17 (1.6) | 56 (3.2) | 11 (3.7) | 5 (1.1) | • |
| 2.15 (1.23, 3.75) | 2.58 (1.21, 5.50) | 0.68 (0.25, 1.83) | n/c | ||
| 2.04 (1.17, 3.57) | 22.59 (1.21, 5.54) | 0.72 (0.27, 1.98) | n/c | ||
| 30+ days | 66 (6.4) | 147 (10.2) | 37 (12.5) | 31 (7.0) | 10 (4.6) |
| 1.70 (1.27, 2.28) | 2.09 (1.40, 3.13) | 1.06 (0.69, 1.63) | 0.71 (0.36, 1.38) | ||
| 1.51 (1.12, 2.03) | 1.79 (1.18, 2.72) | 1.07 (0.70, 1.65) | 0.76 (0.39, 1.48) | ||
| Gastrostomy | |||||
| No | 1,005 (97.0) | 1,352 (93.6) | 281 (94.9) | 425 (96.2) | 213 (97.3) |
| Reference | |||||
| Reference | |||||
| Yes | 31 (3.0) | 92 (6.4) | 15 (5.1) | 17 (3.9) | 6 (2.7) |
| 2.13 (1.42, 3.20) | 1.69 (0.91, 3.14) | 1.29 (0.71, 2.32) | 0.92 (0.38, 2.19) | ||
| 2.17 (1.44, 3.26) | 1.71 (0.92, 3.17) | 1.26 (0.70, 2.28) | 0.98 (0.41, 2.36) | ||
| Tracheostomy | |||||
| No | 1,027 (99.1) | 1,417 (98.1) | 288 (97.3) | 441 (99.8) | 217 (99.1) |
| Reference | |||||
| Reference | |||||
| Yes | 9 (0.9) | 27 (1.9) | 8 (2.7) | • | • |
| 2.15 (1.01, 4.58) | 3.11 (1.20, 8.06) | n/c | n/c | ||
| 2.20 (1.03, 4.68) | 3.07 (1.19, 7.97) | n/c | |||
| Newborn feeding problem | |||||
| No | 765 (73.8) | 1,041 (72.1) | 223 (75.3) | 320 (72.4) | 163 (74.4) |
| Reference | |||||
| Reference | |||||
| Yes | 271 (26.2) | 403 (27.9) | 73 (24.7) | 122 (27.6) | 56 (25.6) |
| 1.07 (0.91, 1.24) | 0.94 (0.73, 1.22) | 1.06 (0.85, 1.31) | 0.98 (0.73, 1.30) | ||
| 1.06 (0.91, 1.24) | 0.93 (0.72, 1.20) | 1.07 (0.86, 1.32) | 0.94 (0.71, 1.26) | ||
| CP | |||||
| No | 1,011 (97.6) | 1,388 (96.1) | 287 (97.0) | 436 (98.6) | 213 (97.3) |
| Reference | |||||
| Reference | |||||
| Yes | 25 (2.4) | 56 (3.9) | 9 (3.0) | 6 (1.4) | 6 (2.7) |
| 1.61 (1.003, 2.58) | 1.26 (0.69, 2.70) | 0.56 (0.23, 1.37) | 1.14 (0.47, 2.77) | ||
| 1.18 (0.73, 1.92) | 0.81 (0.36, 1.86) | 0.52 (0.21, 1.30) | 1.05 (0.43, 2.58) | ||
| Mortality | |||||
| No | 920 (88.8) | 1,260 (87.3) | 262 (88.5) | 391 (88.5) | 190 (86.8) |
| Reference | |||||
| Reference | |||||
| Yes | 116 (11.2) | 184 (12.7) | 34 (11.5) | 51 (11.5) | 29 (13.2) |
| 1.14 (0.90, 1.44) | 1.03 (0.70, 1.50) | 1.03 (0.74, 1.43) | 1.18 (0.79, 1.78) | ||
| 1.21 (0.96, 1.53) | 1.03 (0.70, 1.51) | 1.07 (0.77, 1.49) | 1.19 (0.79, 1.79) | ||
| < 30 days | 92 (8.9) | 138 (9.6) | 23 (7.8) | 39 (8.8) | 24 (11.0) |
| 1.09 (0.83, 1.41) | 0.89 (0.56, 1.40) | 1.00 (0.69, 1.45) | 1.23 (0.79, 1.93) | ||
| 1.18 (0.90, 1.54) | 0.92 (0.58, 1.46) | 1.03 (0.71, 1.50) | 1.23 (0.78, 1.93) |
adverse outcome = LOS longer than 1 week, readmission, gastrostomy, tracheostomy, newborn feeding problem, CP, death
aRR adjusted for sepsis, NHIE severity, and seizure
n < 5
n/c – not calculated
RR – crude risk ratio
aRR – adjusted risk ratio
CI – confidence interval
When looking at outcomes among infants who received therapeutic hypothermia, Hispanic and Black infants were more likely to have a birth hospital stay of more than 30 days (aRRs 2.51 and 2.79, respectively) compared with White, non-Hispanic infants. Hispanic infants were also more likely to have a gastrostomy (aRR 2.87, 95% CI 1.31 to 6.28) and a newborn feeding problem (aRR 1.27, 95% CI 1.02 to 1.59). ‘Other race and ethnicity’ infants were more likely to die within 30 days of birth compared with White, non-Hispanic infants (10.7% versus 6.1%, aRR 1.97, 95% CI 1.01, 3.86). (Table IV). When analysis was restricted to infants with moderate/severe HIE who received therapeutic hypothermia, Hispanic infants were more likely to have newborn feeding problems (aRR 1.49, 95% CI 1.10 to 2.03). There were no other significant differences between infants with moderate/severe HIE who received therapeutic hypothermia (Supplemental Table IV).
Table 4.
Risk of adverse outcome for infants who were cooled by race and ethnicity
| Non-Hispanic White | Hispanic | Black | Asian | Other | |
|---|---|---|---|---|---|
| n (%) | n (%) | n (%) | n (%) | n (%) | |
| cRR (95% CI) | cRR (95% CI) | cRR (95% CI) | cRR (95% CI) | ||
| aRR (95% CI) | aRR (95% CI) | aRR (95% CI) | aRR (95% CI) | ||
| Sample | 410 | 524 | 74 | 199 | 130 |
| Any adverse outcome * | |||||
| No | 54 (13.2) | 45 (8.6) | 8 (10.8) | 25 (12.6) | 15 (11.5) |
| Reference | |||||
| Reference | |||||
| Yes | 356 (86.8) | 479 (91.4) | 66 (89.2) | 174 (87.4) | 115 (88.5) |
| 1.05 (0.92, 1.21) | 1.03 (0.79, 1.34) | 1.01 (0.84, 1.21) | 1.02 (0.83, 1.26) | ||
| 1.05 (0.91, 1.20) | 1.03 (0.79, 1.34) | 1.00 (0.83, 1.20) | 1.02 (0.82, 1.25) | ||
| Length of stay for birth admission (including time at hospital of transfer) | |||||
| < 7 days | 137 (33.4) | 143 (27.3) | 24 (32.4) | 66 (33.2) | 37 (28.50 |
| Reference | |||||
| Reference | |||||
| Any stay of 7 days or more | 229 (55.9) | 336 (64.1) | 42 (56.8) | 109 (54.8) | 75 (57.7) |
| 1.12 (0.95, 1.33) | 1.02 (0.73, 1.41) | 1.00 (0.79, 1.25) | 1.07 (0.82, 1.39) | ||
| 1.12 (0.95, 1.33) | 1.02 (0.73, 1.42) | 0.99 (0.79, 1.25) | 1.06 (0.82, 1.38) | ||
| 7 - < 14 days | 163 (39.8) | 218 (41.6) | 21 (28.4) | 72 (36.2) | 44 (33.9) |
| 1.11 (0.90, 1.36) | 0.87 (0.56, 1.38) | 0.96 (00.73, 1.27) | 1.00 (0.72, 1.39) | ||
| 1.11 (0.91, 1.37) | 0.89 (0.56, 1.40) | 0.97 (0.73, 1.28) | 1.00 (0.71, 1.39) | ||
| 14 - < 30 days | 75 (18.3) | 113 (21.6) | 19 (25.7) | 40 (20.1) | 32 (24.6) |
| 1.26 (0.94, 1.69) | 1.20 (0.73, 1.99) | 1.07 (0.73, 1.57) | 1.29 (0.85, 1.95) | ||
| 1.20 (0.90, 1.61) | 1.22 (0.74, 2.03) | 1.01 (0.68, 1.49) | 1.22 (0.81, 1.86) | ||
| 30+ days | 15 (3.7) | 51 (9.7) | 9 (12.2) | 10 (5.0) | 8 (6.2) |
| 2.66 (1.50, 4.74) | 2.76 (1.21, 6.32) | 1.33 (0.60, 2.97) | 1.80 (0.76, 4.24) | ||
| 2.51 (1.40, 4.48) | 2.79 (1.18, 6.61) | 1.29 (0.57, 2.88) | 1.80 (0.76, 4.25) | ||
| Number of readmissions in first year of life | |||||
| None | 302 (73.7) | 356 (67.9) | 51 (68.9) | 148 (74.4) | 97 (74.6) |
| Reference | |||||
| Reference | |||||
| Any Readmission | 108 (26.3) | 168 (32.1) | 23 (31.1) | 51 (25.6) | 33 (25.4) |
| 1.22 (0.96, 1.55) | 1.18 (0.75, 1.85) | 0.97 (0.70, 1.36) | 0.96 (0.65, 1.42) | ||
| 1.17 (0.92, 1.49) | 1.16 (0.74, 1.82) | 0.94 (0.68, 1.32) | 0.95 (0.65, 1.41) | ||
| 1 | 78 (19.0) | 116 (22.1) | 21 (28.4) | 36 (18.1) | 30 (23.1) |
| 1.20 (0.90, 1.60) | 1.42 (0.88, 2.30) | 0.95 (0.64, 1.41) | 1.15 (0.76, 1.75) | ||
| 1.09 (0.81, 1.46) | 1.39 (0.86, 2.27) | 0.91 (0.61, 1.35) | 1.13 (0.74, 1.72) | ||
| 2 | 21 (5.1) | 27 (5.2) | • | 11 (5.5) | • |
| 1.08 (0.61, 1.92) | n/c | 1.06 (0.51, 2.21) | n/c | ||
| 0.90 (0.50, 1.61) | n/c | 0.97 (0.46, 2.05) | n/c | ||
| 3+ | 9 (2.2) | 25 (4.8) | • | • | • |
| 2.27 (1.06, 4.86) | n/c | n/c | n/c | ||
| 1.85 (0.85, 4.02) | n/c | n/c | n/c | ||
| Time to first readmission after discharge from birth admission | |||||
| No readmissions | 302 (73.7) | 356 (67.9) | 51 (68.9) | 148 (74.4) | 97 (74.6) |
| Reference | |||||
| Reference | |||||
| < 4 days | 85 (20.7) | 124 (23.7) | 17 (23.0) | 39 (19.6) | 24 (18.5) |
| 1.18 (0.90, 1.55) | 1.14 (0.68, 1.92) | 0.95 (0.65, 1.39) | 0.90 (0.57, 1.42) | ||
| 1.07 (0.81, 1.42) | 1.09 (0.64, 1.84) | 0.86 (0.58, 1.26) | 0.88 (0.56, 1.38) | ||
| 4 - < 7 days | • | 6 (1.2) | • | • | • |
| n/c | n/c | n/c | n/c | ||
| n/c | n/c | n/c | n/c | ||
| 7 - < 14 days | 7 (1.7) | 11 (2.1) | • | • | • |
| 1.32 (0.51, 3.41) | n/c | n/c | n/c | ||
| Didn’t converge | n/c | n/c | n/c | ||
| 14 - < 30 days | • | 12 (2.3) | • | • | • |
| n/c | n/c | n/c | n/c | ||
| n/c | n/c | n/c | n/c | ||
| 30+ days | 8 (2.0) | 15 (2.9) | • | • | 7 (5.4) |
| 1.57 (0.66, 3.70) | n/c | n/c | 2.61 (0.95, 7.19) | ||
| 1.11 (0.46, 2.71) | n/c | n/c | 2.61 (0.94, 7.26) | ||
| Gastrostomy | |||||
| No | 402 (98.1) | 495 (94.5) | 72 (97.3) | 193 (97.0) | 128 (98.5) |
| Reference | |||||
| Reference | |||||
| Yes | 8 (2.0) | 29 (5.5) | • | 6 (3.0) | • |
| 2.84 (1.30, 6.20) | n/c | 1.55 (0.54, 4.45) | n/c | ||
| 2.87 (1.31, 6.28) | n/c | 1.61 (0.56, 4.66) | n/c | ||
| Tracheostomy | |||||
| No | 410 (100.0) | 523 (99.8) | 74 (100.0) | 198 (99.5) | 130 (100.0) |
| Reference | |||||
| Reference | |||||
| Yes | • | • | • | • | • |
| n/c | n/c | n/c | n/c | ||
| n/c | n/c | n/c | n/c | ||
| Newborn feeding problem | |||||
| No | 283 (69.0) | 310 (59.2) | 50 (67.6) | 123 (61.8) | 88 (67.7) |
| Reference | |||||
| Reference | |||||
| Yes | 127 (31.0) | 314 (40.8) | 24 (32.4) | 76 (38.2) | 42 (32.3) |
| 1.32 (1.06, 1.64) | 1.05 (0.68, 1.62) | 1.23 (0.93, 1.64) | 1.04 (0.74, 1.48) | ||
| 1.27 (1.02, 1.59) | 1.02 (0.66, 1.58) | 1.21 (0.91, 1.61) | 1.03 (0.73, 1.46) | ||
| CP | |||||
| No | 409 (99.8) | 512 (97.7) | 73 (98.7) | 197 (99.0) | 130 (100.0) |
| Reference | |||||
| Reference | |||||
| Yes | • | 12 (2.3) | • | • | • |
| n/c | n/c | n/c | n/c | ||
| n/c | n/c | n/c | n/c | ||
| Mortality | |||||
| No | 381 (92.9) | 487 (92.9) | 69 (93.2) | 189 (95.0) | 116 (89.2) |
| Reference | |||||
| Reference | |||||
| Yes | 29 (7.1) | 37 (7.1) | 5 (6.8) | 10 (5.0) | 14 (10.8) |
| 1.00 (0.61, 1.62) | 0.96 (0.37, 2.47) | 0.71 (0.35, 1.46) | 1.52 (0.80, 2.88) | ||
| 1.05 (0.64, 1.72) | 1.03 (0.40, 2.66) | 0.70 (0.34, 1.43) | 1.52 (0.80, 2.89) | ||
| < 30 days | 22 (5.4) | 32 (6.1) | 5 (6.8) | 10 (5.0) | 14 (10.8) |
| 1.13 (0.66, 1.94) | 1.24 (0.47, 3.27) | 0.92 (0.44, 1.94) | 1.97 (1.01, 3.86) | ||
| Didn’t converge | 1.36 (0.52, 3.61) | Didn’t converge | 1.95 (0.999, 3.82) |
adverse outcome = LOS longer than 1 week, readmission, gastrostomy, tracheostomy, newborn feeding problem, CP, death
aRR adjusted for sepsis, NHIE severity, and seizure
n < 5
n/c – not calculated
RR – crude risk ratio
aRR – adjusted risk ratio
CI – confidence interval
Discussion
Therapeutic hypothermia is currently the only standard treatment shown to improve outcomes for neonatal HIE. The sample of infants with neonatal HIE in this cohort is proportional in overall percentage to the racial and ethnic demographics of California based on the 2020 census data.9 In this research cohort, infants with HIE born to Black mothers were significantly less likely to receive therapeutic hypothermia treatment despite adjusting for factors that may impact the decision to offer therapeutic hypothermia such as severity of neonatal HIE, hospital transport, or rural hospital location. Infants of Black and Hispanic mothers who did not receive therapeutic hypothermia had an increased risk of certain adverse outcomes of HIE. Black infants were more likely to receive a tracheostomy, Hispanic infants were more likely to have a prolonged (>30 day) initial hospital stay, and both Black and Hispanic infants were more likely to require a tracheostomy and readmission compared with non-Hispanic White infants with HIE. When the analysis was restricted to only infants diagnosed with moderate/severe neonatal HIE, Hispanic and Black infants continued to be more likely to receive a gastrostomy and tracheostomy, respectively. Additionally, Black infants in this analysis were also more likely to be diagnosed with cerebral palsy.
However, even infants of Black and Hispanic mothers who received therapeutic hypothermia were at increased risk of some adverse outcomes of neonatal HIE compared with infants of non-Hispanic White mothers. Black and Hispanic infants who received therapeutic hypothermia were more likely to have a prolonged initial hospital stay, and Hispanic infants were also at increased risk to have newborn feeding problems and receive a gastrostomy tube. This suggests not all differences in adverse outcomes seen in Black and Hispanic infants with HIE is due to not receiving therapeutic hypothermia. Notably, most of these differences resolve when restricting the analysis to infants diagnosed with moderate/severe neonatal HIE. Further investigation into the inequities in the adverse outcomes seen by infants with HIE that received therapeutic hypothermia should be performed.
While this study is not able to determine the cause of the significant racial inequities in the treatment and outcomes of neonatal HIE, previous studies have found that Black and Hispanic mothers are more likely to give birth at low resource hospitals and that infants of Black and Hispanic mothers are more likely to be admitted to low resource NICUs.3,10 We can speculate that the differences seen in the rates of therapeutic hypothermia for infants of Black and Hispanic mothers are related to being more likely to be born at lower resource hospitals.
Studies such as Profit et al (2017) and Howell et al (2018) demonstrate that infants of Black and Hispanic mothers are more likely to be born at lower resource NICUs, which suggests that the difference in the resources available to infants of Black and Hispanic mothers and those of White mothers may be secondary to systemic and structural racism which impacts the location mothers give birth and leads to the racial segregation of where their infants receive care.10,11 Additionally, qualitative studies focusing on the families of premature infants in the NICU have demonstrated that Black and Hispanic mothers report experiencing unique stresses on an individual, institutional, and community level.12,13 These studies allow mothers to give voice to how the quality of care at a hospital level impacted both their infants’ and their own treatment in the NICU. Black mothers of neonates in the NICU report experiencing the results of both individual and structural racism while their infants are being cared for in the NICU. They recall individual health care staff making race related comments and referring to racial stereotypes which caused the mothers to be fearful that their babies were being neglected compared with other patients. For example, in one qualitative study asking Black mothers to share their experiences in the NICU, one mother “talked about “wimpy White boy syndrome” and her concerns that this may cause health care providers to be less attentive to her infant, and a second mother confirmed that she had heard about this concept from a health care provider.”13 Additionally, the Black mothers surveyed felt their infants were receiving inadequate treatment due to being in a low resource location and that less money was allocated to caring for their babies.13 Further qualitative studies specifically investigating the experiences of Black and Hispanic parents of infants with HIE would elucidate how families are counseled by healthcare providers regarding the management of HIE and if they were offered therapeutic hypothermia.
This study had several limitations. It was a retrospective cohort study and was limited by the available records, documentation, and the use of ICD-9 and 10 codes. The administrative database does not contain data on how many infants met the cooling criteria, and we cannot ascertain how many infants who should have undergone therapeutic hypothermia were indeed not cooled. Incomplete or inaccurate medical provider documentation of diagnoses or procedures could influence the accuracy of this study. The ICD-9 and 10 codes for HIE were used in this study. Patients diagnosed exclusively with neonatal encephalopathy who did not also receive a code for HIE were excluded from the study due to the lack of specificity of diagnosis. The study was also limited by a one-year follow-up period. Some adverse outcomes of HIE such as cerebral palsy may not be diagnosed and detected by one year of life. A longer follow-up period may demonstrate additional increased risk in this sample. This study was also limited by covering a large number of hospitals over multiple years and did not determine the therapeutic hypothermia capabilities and protocols at each hospital at the time of each infant’s birth or if infants qualified for therapeutic hypothermia at the time of birth based on their birth hospital protocol and capabilities. However, infants with moderate/severe HIE were separately evaluated as most should be expected to qualify for therapeutic hypothermia. Finally, this study grouped infants based on the self-reported race and ethnicity of their mother. The race and ethnicity of the father of the infant was not included in the analysis. Self-reported discrete racial and ethnic data may not fully capture the cultural complexities of race and ethnicity such as multi-racial infants and cross-cultural adoption. This is evidenced by 7.3% of the cohort sample being reported as unknown/other.
Despite these limitations, this study is important for demonstrating unequal treatment and outcomes in neonatal HIE. This indicates that more can be done to educate medical providers about implicit bias and culturally competent care to ensure that all infants receive appropriate treatment. Additionally, it demonstrates that further support is needed for families of the impacted infants to ensure that they receive appropriate counseling on the available treatment options for their children.
This study has important public health implications including regarding the way in which HIE is classified and in the access to therapeutic hypothermia. Currently, the diagnosis and severity of HIE is based on both laboratory findings and physical exam (Modified SARNAT exam).6 Previous studies have shown that many aspects of physical exams are subjective and may be at risk for implicit bias.14 In addition, Black infant mortality has shown to be reduced if their medical provider is also Black.15 One explanation for this finding is the impact of implicit bias on neonatal care. While implicit bias was not directly explored in this study, the results indicate implicit bias education for neonatal providers may be beneficial. Physical exams will always be a foundational part of the practice of medicine, but further research should also be performed in finding additional objective and unbiased ways to classify HIE to help combat implicit bias and racial and ethnic inequities.
This study also highlights that many hospitals and NICUs are not equipped to perform therapeutic hypothermia. Structural racism affects healthcare accessibility and is a major public health concern.10,11 The expansion of therapeutic hypothermia capabilities and ambulances that are equipped to provide therapeutic hypothermia to neonates during transport would likely begin to address the racial and ethnic inequities shown in this study.
Future directions include comparing rates of therapeutic hypothermia by race and ethnicity in private versus public hospital systems and in different regions of the state to see if these inequities persist. Additionally, other states should evaluate if these inequities are present nationally or are limited to California. California is one of the most racially and ethnically diverse states in the country and in recent years has implemented progressive state-wide policies to address racial and ethnic inequities. The 2020 national census reports that 39% of Californians identify as Hispanic/Latino, 35% as non-Hispanic White, 15% as Asian/Pacific Islander, 5% as Black, 4 % as mixed ethnicity, and <1% as Indigenous/Native American.9 Racial and ethnic inequities may be different in states or counties with different demographics and political policies. Additionally, future studies could use geographic and temporal models to determine which hospitals were capable of therapeutic hypothermia at the time of each infant’s birth and how this impacted the receipt of therapeutic hypothermia by race and ethnicity. Finally, future studies should also investigate inequities in maternal health and if there is correlation with the inequities of treatment of infants with HIE.
In conclusion, HIE is a major cause of morbidity and mortality in term infants. This study demonstrates that inequities present in the treatment and outcomes of Black and Hispanic infants diagnosed with neonatal HIE. We believe that this is an important finding that fills a gap in the current research on racial and ethnic inequities in the management and outcomes of infants in the NICU. Further qualitative and quantitative research should be performed to better understand the reasons for these findings and if they are reproducible outside of California.
Supplementary Material
Acknowledgements:
We would like to thank the Study of Mothers and Infants Research Group for their assistance. This study was supported by the San Diego Study of Mothers and Infants at the University of California San Diego. Gretchen Bandoli is funded by a NIH award (K01 AA027811). Carolyn Fall formulated the research question, designed the study, and drafted the manuscript. Rebecca J. Baer performed the statistical analysis for this study. Gretchen Bandoli provided mentorship expertise on study design and manuscript editing. Laura Jelliffe-Pawlowski, Nana Matoba, Henry C. Lee, and Christina D. Chambers provided expertise in inequity research, hypoxic ischemic encephalopathy, and manuscript editing.
Abbreviations/Acronyms:
- aRR
Adjusted risk ratio
- AS
Ambulatory surgery
- CI
Confidence interval
- ED
Emergency Department
- HCAI
California Department of Health Care Access and Information
- HIE
Hypoxic ischemic encephalopathy
- NICU
Neonatal intensive care unit
- RR
Crude/unadjusted risk ratio
- SOMI
Study of mothers and infants
- TH
Therapeutic hypothermia
Footnotes
The authors have no financial disclosures or conflicts of interests.
Conflict of Interest: The authors have no conflicts of interest.
Prior Presentations: The data in this manuscript has been previously presented at:
Western Society for Pediatric Research Conference, January 2023, Podium presentation
Cool Topics in Neonatology Conference, March 2023, Poster presentation
Western Perinatal and Developmental Medicine Symposium, June 2023, Podium presentation
Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Contributor Information
Carolyn Fall, University of California, San Diego, Rady Children’s Hospital of San Diego.
Rebecca J. Baer, University of California San Diego, University of California San Francisco.
Laura Jelliffe-Pawlowski, University of California San Francisco.
Nana Matoba, University of California, San Diego, Rady Children’s Hospital of San Diego.
Henry C. Lee, University of California, San Diego, Rady Children’s Hospital of San Diego.
Christina D. Chambers, University of California, San Diego, Rady Children’s Hospital of San Diego.
Gretchen Bandoli, University of California, San Diego, Rady Children’s Hospital of San Diego.
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