Cross-Sectional Analysis on Racial and Economic Disparities Affecting Mortality in Preterm Infants with Posthemorrhagic Hydrocephalus

Cross-Sectional Analysis on Racial and Economic Disparities Affecting Mortality in Preterm Infants with Posthemorrhagic Hydrocephalus

Original Article Cross-Sectional Analysis on Racial and Economic Disparities Affecting Mortality in Preterm Infants with Posthemorrhagic Hydrocephalu...

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Original Article

Cross-Sectional Analysis on Racial and Economic Disparities Affecting Mortality in Preterm Infants with Posthemorrhagic Hydrocephalus Diana L. Jin1, Eisha A. Christian1, Frank Attenello1, Edward Melamed2, Steven Cen1, Mark D. Krieger1,2, J. Gordon McComb1,2, William J. Mack1

BACKGROUND: Despite major advances in medicine, racial and socioeconomic disparities continue to affect health care outcomes. Higher overall infant mortality has been reported for black neonates compared with their Hispanic and white counterparts. The underlying basis for these differences remains unclear. A potential influencing factor is the management of premature neurologic complications in this disadvantaged group. This study examines racial and socioeconomic disparities on mortality in preterm infants with posthemorrhagic hydrocephalus (PHH).

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METHODS: Data from the Nationwide Inpatient Sample and Kids Inpatient Database were combined from 2000 to 2010. Discharges with International Classification of Diseases, Ninth Revision, Clinical Modification codes for preterm births with intraventricular hemorrhage and PHH were included. Relative risk (RR) ratios for mortality, complications, length of stay, and hospital costs were obtained with multivariate analysis after controlling for patient-level, hospital-level, and admission-level factors.

mortality compared with those with private insurance (RR [ 1.2; P [ 0.04) after adjusting for patient and hospital factors. CONCLUSIONS: Among preterm infants with intraventricular hemorrhage and resultant PHH, black infants and those insured by Medicaid have significantly increased mortality but these 2 effects are independent. Further studies are needed to fully understand the factors affecting these racial and socioeconomic disparities.

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RESULTS: When controlling for patient and hospital factors, black neonates had increased mortality compared with whites and Hispanics (RR [ 1.47; P < 0.01). This association existed despite lower rates of congenital cardiac defects (RR [ 0.84; P < 0.01), gastrointestinal complications (RR [ 0.84; P < 0.01), and general complications of prematurity (RR [ 0.95; P [ 0.04) in the black cohort. Preterm infants insured by Medicaid had increased

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Key words Hydrocephalus - Intraventricular hemorrhage - Kids Inpatient Database - Nationwide Inpatient Sample - Preterm neonate - Preterm infant - Posthemorrhagic hydrocephalus -

Abbreviations and Acronyms IMR: Infant mortality rate IVH: Intraventricular hemorrhage KID: Kids Inpatient Database NIS: Nationwide Inpatient Sample

WORLD NEUROSURGERY 88: 399-410, APRIL 2016

INTRODUCTION

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nfant mortality has long been considered a sensitive indicator of the impact of disparities on the health of populations. The infant mortality rate (IMR, defined as the death of an infant per 1000 live births) in the United States has declined since 19601; however, the United States ranks 31st among the Organization for Economic Cooperation and Development countries, with an IMR of 6.2 (mean for the index is 4.2). Although the United States and Turkey have the highest preterm birth rates (12%), this characteristic alone does not sufficiently explain the relatively high IMR in the United States (e.g., Austria has a preterm birth rate of 11% but an IMR of 3.8).1 Racial and socioeconomic disparities have a profound impact on infant mortality in the United States. For example, the IMR ratio for black to white infants from 1960 to 2011 has remained unchanged, and the IMR of black infants is still double that of

PHH: Posthemorrhagic hydrocephalus RR: Relative risk From the 1Department of Neurosurgery, Keck School of Medicine of USC; and 2Division of Neurosurgery, Children’s Hospital Los Angeles, Los Angeles, California, USA To whom correspondence should be addressed: Diana L. Jin, B.A. [E-mail: [email protected]] Citation: World Neurosurg. (2016) 88:399-410. http://dx.doi.org/10.1016/j.wneu.2015.12.046 Journal homepage: www.WORLDNEUROSURGERY.org Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2016 Elsevier Inc. All rights reserved.

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ORIGINAL ARTICLE DIANA L. JIN ET AL.

FACTORS AFFECTING DEATH IN NEONATES WITH PHH

Table 1. Continued

Table 1. Cohort Demographics: Patient Factors Variable

Category

Frequency

Percentage

13,736

100

Male

8028

58

Female

5706

Total patients Gender

Missing Race

*

42

3

4890

36

01

4

5651

41

Unspecified

1518

11

Hispanic

2070

15

240

2

86

1

821

6

3346

24 01

Medicare

12

Medicaid

7449

54

Private including HMO

5477

40

No charge Other

Gestational age

8

19

Self-pay

Birth weight

1127

2610

Missing Payer status

2

Black

Other

248

2 01

* 504

4

Missing

43

1

<500 g

197

1

500e749 g

3299

24

750e999 g

3699

27

1000e1249 g

2336

17

1250e1499 g

1526

11

1500e1749 g

789

6

1750e1999 g

583

5

2000e2499 g

614

5

>2500 g

271

2

Missing

305

2

<24 weeks

670

5

24 weeks

1095

8

25e26 weeks

2514

18

27e28 weeks

2111

15

29e30 weeks

1165

9

31e32 weeks

819

6

33e34 weeks

448

3

35e36 weeks Missing Unspecified

269

2

4620

34

26

01 Continues

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Percentage 4

33

Native American

Frequency 549

4563

Intraventricular hemorrhage grade

Category 1

White

Asian/Pacific

Variable

HMO, Health Maintenance Organization. *Frequency 10.

white infants.1 The impact of insurance status, often used as a proxy for socioeconomic status, on IMRs has also been described: in 2011, the state of Washington reported that infants insured by Medicaid had an IMR of 6.5 versus 3.9 in neonates who did not receive Medicaid.2 Moss and Carver,3 in 1998, also noted that infants covered by Medicaid had higher odds of infant mortality. Disorders related to short gestational periods and low birth weight are among the leading causes of infant mortality in the United States. The management of neurologic complications secondary to premature birth can have a substantial impact on patient outcomes and survival. This study examines outcome disparities in the setting of intraventricular hemorrhage (IVH) and posthemorrhagic hydrocephalus (PHH) in preterm infants after controlling for both patient and hospital factors. METHODS Data Source This study uses 2 of the largest public all-payer inpatient care datasets in the United States4,5 from the Healthcare Cost and Utilization Project. The Nationwide Inpatient Sample (NIS) and Kids Inpatient Database (KID) have longitudinal hospital inpatient discharge data from more than 1000 hospitals, with the NIS representing 20% of all hospital discharges and KID representing 80% of pediatric discharges in the United States. Data from the KID were available for 2000, 2003, 2006, and 2009. For the years that the KID dataset did not cover, pediatric data were extracted from the 2000e2010 NIS database. NIS also has a built-in method for obtaining national estimates of prevalence as described in the Healthcare Cost and Utilization ProjecteNIS Calculating NIS Variances Guide.6 Study Cohort The study population was limited to preterm infants with IVH and hydrocephalus. Admission data were extracted using the International Classification of Diseases, Ninth Revision, Clinical Modification codes for patients with a preterm birth weight (765.00e765.29), IVH grade (772.10e772.14), and hydrocephalus (742.3, 331.3, 331.4). To prevent double-counting, admissions that resulted in a discharge to another short-term, acute-care facility

WORLD NEUROSURGERY, http://dx.doi.org/10.1016/j.wneu.2015.12.046

ORIGINAL ARTICLE DIANA L. JIN ET AL.

FACTORS AFFECTING DEATH IN NEONATES WITH PHH

Table 2. Patient Demographics: Hospital Factors Variable

Category

Table 3. Complications and Comorbidities

Frequency Percentage Event

Hospital region

Teaching status

Northeast

1704

13

Midwest

3076

22

South

5759

42

West

3197

23

Nonteaching Teaching Missing

Hospital bed size Small

Hospital location

Admission type

11,155

81

366

3 11

Medium

3175

23

Large

8723

64

Missing

366

2

Rural

122

1

Missing

Discharge

16

1472

Urban

Hospital type

2215

Not children’s hospital

13,248

96

366

3

2068

15

Children’s general or specialty

1199

9

Children’s unit

1307

9

Missing

9161

67

Nonroutine

7140

52

Routine

6594

48

Emergency

1938

14

Urgent

3538

26

Elective

993

7

Newborn

5314

39

Trauma center Other Missing

28

01 01

* 1911

14

Admission source Emergency room

96

1

another hospital

4445

32

Other facility

309

2

Routine

4944

36

Missing

3942

29

*Frequency 10.

(pretransfer hospitalizations) were excluded from the study.7 In addition, age of admission was limited to less than 3 months. Both NIS and KID include patient and hospital factors as categorical demographic variables. Discrete patient factors, including race (white, black, Hispanic, Asian, or Pacific Islander, Native American, other), payer status (Medicare, Medicaid, private insurance, self-pay, no charge), gender, length of stay, cost of hospitalization, weight, gestational age, and IVH grade, were

WORLD NEUROSURGERY 88: 399-410, APRIL 2016

Frequency Percent

95% Confidence Interval

Shunt replacement

718

5

4.2e6.2

Mechanical implant complication

437

3

2.5e3.9

Shunt removal

857

6

5.2e7.3

Shunt infection

339

2.5

1.8e3.1

67

0.5

0.3e0.7

Other implant complication Neurologic complications Meningitis

42 839

Wound breakdown

56

Wound infection

0.3

0.1e0.5

6

5.2e7

0.4

0.2e0.6

118

0.9

0.5e1.2

Seizures

1997

14.5

12.9e16.2

Necrotizing enterocolitis

1368

10

Intestinal perforation

621

Pulmonary complication

11,437

Gastrointestinal complication Hematologic complication

621 7011

4.5 83 4.5 51

8.9e11.1 3.8e5.3 81.8e84.8 3.8e5.3 48.2e53.9

Sepsis

6547

48

45e50.3

Endocrinologic complication

4960

36

33.8e38.4

Cardiac complications

76

Congenital heart defects

5606

0.6 41

0.2e0.9 38.4e43.3

encoded as categorical variables in NIS and KID. Hospital-level variables such as hospital bed size (small, <200 beds; medium: 201e400 beds; large, >400 beds), region (Northeast, Midwest, South, West), location (urban and rural), type (children’s general/ specialty hospital, children’s unit in a general hospital, general hospital), and teaching status (teaching, nonteaching) were included as categorical variables. Admission status such as admission type (emergency, elective, urgent, trauma center, newborn) and admission source (emergency department, routine, another facility, another hospital) was also included. Because the NIS dataset did not classify hospitals based on the National Association of Children’s Hospitals and Related Institutions as did the KID database, hospitals in the NIS database were identified with their hospital identification ID number and were assigned a classification based on what their KID designation was for the previous available KID year dataset. The primary outcome of interest was mortality. Secondary outcomes of interest included general complications and shunt complications. Shunt complications of interest included replacement of a shunt (2.42), mechanical implant complication (996.2), implant infection (996.63), and other implant complication (996.75). General complications and comorbidities of interest included seizures (779.0), gastrointestinal complications (necrotizing enterocolitis, 777.5e777.53; intestinal perforation, 777.6), pulmonary complications (mechanical ventilation, 96.71, 96.72; respiratory support, 93.90e96.72; respiratory distress, 769,

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Table 4. Continued

Table 4. Multivariate Analysis of Mortality Rate Ratio

95% Confidence Interval

Gender Female

1.18

Male

1.01e1.39

0.04

Reference

Private

1.20

1.01e1.44

0.04

Reference

Medium

0.87

0.61e1.24

0.43

Large

1.09

0.77e1.55

0.62

Midwest

0.85

0.61e1.17

0.32

South

0.87

0.66e1.15

0.33

West

0.98

0.68e1.40

0.90

0.42

0.34e0.52

< 0.01

P Value

Northeast

Race Asian/Pacific

1.62

0.92e2.83

0.09

Black

1.47

1.18e1.83

< 0.01

Hispanic

0.81

0.61e1.08

0.14

Native American

0.86

0.37e2.01

0.73

White

Reference

Weight <500 g

4.47

2.33e8.56

< 0.01

500e749 g

2.55

1.55e4.21

< 0.01

750e999 g

1.66

0.97e2.65

0.06

1000e1249 g

1.10

0.64e1.92

0.73

1250e1499 g

Reference

1500e1749 g

0.73

0.31e1.75

0.48

1750e1999 g

0.44

0.13e1.51

0.19

2000e2499 g

0.75

0.29e1.95

0.56

>2500 g

1.42

0.57e3.54

0.45

Gestational age <24 weeks

3.36

1.65e6.85

0.01

24 weeks

2.06

1.02e4.14

0.04

25e26 weeks

3.49

1.78e6.83

0.01

27e28 weeks

1.29

0.63e2.65

0.49

29e30 weeks

Reference

31e32 weeks

0.80

0.30e2.12

0.65

33e34 weeks

1.17

0.38e3.58

0.78

35e36 weeks

2.3

0.86e6.16

0.10

0.88

0.44e1.76

0.73

2

1.21

0.80e1.84

0.40

3

Reference

4

2.83

2.26e3.55

< 0.01

Intraventricular hemorrhage grade 1

Hospital bed size Small Continues

402

95% Confidence Interval

Hospital region

Payer Medicaid

Rate Ratio

P Value

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Teaching status Teaching Nonteaching Hospital type Children’s unit

0.73

0.50e1.09

0.12

Not children’s hospital

0.81

0.58e1.15

0.25

Children’s hospital

Reference

Bold indicates statistically significant with P < 0.05.

770.6e770.8, 770.89), cardiac complications (cardiac arrest, 779.85; hypotension, 458.9; hypovolemia, 785.59), hematologic complications (disseminated intravascular coagulation, 776.2; jaundice, 774.2, 774.6; hematologic disorder, 776.0e776.9), sepsis (V29.0, 771.8, 771.81, 771.83, 771.89), endocrine complications (775.1e775.9), and congenital heart defects (745.0e747.9). Length of stay was also included as a dichotomized outcome: high length of stay was defined as greater than 120 days (90th percentile). Daily cost was dichotomized into high and low, with high daily cost being more than $12,654 (90th percentile). High total cost was defined as greater than $807,627 (90th percentile). For categorical variables, missing code was generated to represent missing data when fitting the model. Statistical Analysis The primary goal was to assess socioeconomic, demographic, and hospital factors associated with mortality. Outcomes of interest were 1) mortality; 2) general and specific complications as listed above; and 3) length and cost of stay. The predicting factors included patient-level factors, hospital-level factors, and admission statuselevel factors. Hospital location (urban vs. rural) was excluded as a predicting factor because nearly all patients went to urban hospitals. A univariate model (unadjusted model) was initially generated for all patient and hospital factors for the sample, after which a multivariate logistic regression model was created that adjusted for patient-level factors (race, payment type, comorbidity, sex, gestational age, birth weight, and IVH grade), hospital-level factors (region, teaching status, bed size, children’s hospital type), admission type (emergency, elective, urgent, trauma center,

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ORIGINAL ARTICLE DIANA L. JIN ET AL.

FACTORS AFFECTING DEATH IN NEONATES WITH PHH

Table 5. Continued

Table 5. Multivariate Analysis of General Complications Rate Ratio

95% Confidence Interval

Gender Female Male

1.00

0.97e1.04

0.80

Private

95% Confidence Interval

Medium

1.19

0.71e2.01

0.51

Large

1.48

0.87e2.52

0.15

1.28e4.41

< 0.01

Reference

Hospital region Midwest

2.38

1.03

Northeast

Reference

Payer Medicaid

Rate Ratio

P Value

0.99e1.07

0.15

Reference

Race

South

1.61

0.90e2.87

0.11

West

1.28

0.59e2.78

0.53

2.57

1.44e4.58

< 0.01

Asian/Pacific

0.99

0.87e1.12

0.84

Teaching status

Black

0.95

0.90e1.00

0.04

Teaching Nonteaching

Hispanic

0.97

0.91e1.02

0.23

Native American

0.94

0.74e1.20

0.63

White Weight <500 g

1.07

0.91e1.27

0.40

500e749 g

1.10

1.02e1.19

< 0.01

750e999 g

1.11

1.03e1.19

< 0.01

1000e1249 g

1.06

0.99e1.14

0.10

1250e1499 g

Reference

1500e1749 g

0.98

0.89e1.07

0.65

1750e1999 g

0.85

0.76e0.96

< 0.01

2000e2499 g

0.93

0.83e1.05

0.25

>2500 g

0.87

0.74e1.02

0.10

Gestational age <24 weeks

1.06

0.95e1.18

0.32

24 weeks

1.08

0.98e1.19

0.13

25e26 weeks

1.10

1.01e1.19

0.03

27e28 weeks

1.05

0.96e1.13

0.28

29e30 weeks

Reference

31e32 weeks

0.90

0.81e1.00

0.05

33e34 weeks

0.89

0.78e1.02

0.09

35e36 weeks

0.89

0.74e1.05

0.17

0.98

0.90e1.08

0.73

2

1.04

0.97e1.11

0.25

3

Reference

4

0.98

0.94e1.02

0.36

Intraventricular hemorrhage grade 1

Reference

Hospital type Children’s hospital

Reference

Hospital bed size Small Continues

WORLD NEUROSURGERY 88: 399-410, APRIL 2016

P Value

Reference

Children’s unit

0.99

0.56e1.75

0.97

Not children’s hospital

0.82

0.47e1.42

0.48

Bold indicates statistically significant with P < 0.05.

newborn), and admission source (emergency department, routine, another facility, another hospital). The association between predicting factors and outcome was assessed by the relative risk (RR) ratio, and statistical significance was predetermined as P < 0.05. All descriptive, univariate, and multivariate analyses were performed using SAS 9.4 (SAS Institute Inc., Cary, North Carolina, USA). RESULTS Patient Demographics A total of 13,736 patients had IVH and PHH. Patient and hospital demographics are presented in Tables 1 and 2. Most patients were white (33%), covered by Medicaid (54%), had a birth weight between 750 and 999 g (27%), had a gestational age of 25e26 weeks (18%), and presented with grade 4 IVH (41%). Most patients were admitted to urban, nonchildren’s teaching hospitals with a large bed size. Average length of stay for the entire cohort was 62 days, and average hospital cost $359,158 per admission. Mortality was 10.6%. Complications and comorbidities are presented in Table 3. The most common complications were pulmonary (83%) and hematologic (51%). Variables Affecting Inpatient Mortality Multivariable analyses examining associations between patient demographics/hospital-level factors and inpatient mortality are presented in Table 4. Black patients had a 47% increased risk of inpatient death compared with white patients (RR ¼ 1.47; P < 0.01). Medicaid patients had a 20% increased rate of

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FACTORS AFFECTING DEATH IN NEONATES WITH PHH

Table 6. Multivariate Analysis of Congenital Heart Anomalies Rate Ratio

95% Confidence Interval

Table 6. Continued

P Value

Rate Ratio

95% Confidence Interval

P Value

Hospital bed size

Gender Female

1.11

Male

1.02e1.22

0.02

Private

Reference

0.93

0.78e1.11

0.43

Large

1.01

0.85e1.21

0.90

1.03

Hospital region Midwest

1.02

0.86e1.22

0.78

South

1.02

0.88e1.19

0.81

West

0.96

0.79e1.18

0.71

1.01e1.32

0.04

0.94e1.14

0.50

Reference

Race Asian/Pacific

1.00

0.73e1.38

1.00

Black

0.84

0.73e0.95

< 0.01

Northeast

Hispanic

0.91

0.79e1.05

0.22

Teaching status

Native American

1.02

0.57e1.82

0.95

Teaching

White

Reference

Medium

Payer Medicaid

Small

Nonteaching

Reference

Reference

1.15 Reference

Hospital type

Weight <500 g

1.31

0.88e1.96

0.18

Children’s unit

0.92

0.76e1.12

0.43

0.95

0.8e1.14

0.57

500e749 g

1.20

0.98e1.48

0.08

Not children’s hospital

750e999 g

1.20

0.99e1.45

0.07

Children’s hospital

1000e1249 g

1.19

0.98e1.45

0.07

1250e1499 g

Reference

1500e1749 g

1.07

0.83e1.38

0.58

1750e1999 g

0.87

0.62e1.20

0.39

2000e2499 g

0.96

0.69e1.34

0.82

>2500 g

1.07

0.70e1.63

0.76

<24 weeks

1.5

1.13e1.98

< 0.01

24 weeks

1.42

1.11e1.82

< 0.01

25e26 weeks

1.43

1.15e1.78

< 0.01

27e28 weeks

1.23

1.00e1.52

0.05

29e30 weeks

Reference

Reference

Bold indicates statistically significant with P < 0.05.

inpatient mortality compared with those with private insurance (RR ¼ 1.20; P ¼ 0.04). Female gender, weight <750 g, gestational age <27 weeks, and patients with grade 4 IVH had increased inpatient mortality. Teaching hospitals had lower mortality compared with nonteaching hospitals.

Gestational age

31e32 weeks

0.88

0.67e1.17

0.38

33e34 weeks

0.86

0.59e1.26

0.44

35e36 weeks

1.09

0.7e1.69

0.70

1.04

0.81e1.33

0.75

2

1.17

0.99e1.38

0.07

3

Reference

4

1.04

0.94e1.15

0.46

Intraventricular hemorrhage grade 1

Continues

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Variables Affecting Perinatal Complications Multivariable analyses examining associations between patient demographics/hospital-level factors and perinatal complications are presented in Tables 5e8. Compared with their white counterparts, black infants had a lower rate of general complications (RR ¼ 0.95; P ¼ 0.04, Table 4), fewer cardiac anomalies (RR ¼ 0.84; P < 0.01), and fewer gastrointestinal complications (RR ¼ 0.59; P ¼ 0.01). Medicaid patients had a higher likelihood of overall shunt complications (RR ¼ 1.16; P ¼ 0.02). Gestational age less than 26 weeks was associated with an increased rate of cardiac defects, and birth weight less than 1000 g was associated with an increased risk of gastrointestinal complications, including necrotizing enterocolitis and intestinal perforation. Length of Stay Multivariable analyses examining associations between patient demographics/hospital-level factors and length of stay are presented in Table 9. Blacks and Asians had increased length of stay compared with their white counterparts (RR ¼ 1.37; P ¼ 0.02 and

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ORIGINAL ARTICLE DIANA L. JIN ET AL.

FACTORS AFFECTING DEATH IN NEONATES WITH PHH

Table 7. Multivariate Analysis of Gastrointestinal Complications Rate Ratio

95% Confidence Interval

Male

0.63

0.47e0.84

< 0.01

Reference

Private

1.06

95% Confidence Interval

Medium

1.19

0.71e2.01

0.51

Large

1.48

0.87e2.52

0.15

Midwest

2.38

1.28e4.41

< 0.01

South

1.61

0.90e2.87

0.11

West

1.28

0.59e2.78

0.53

1.44e4.58

< 0.01

0.79e1.42

0.68

Reference

Northeast

Race Asian/Pacific

0.91

0.33e2.53

0.85

Teaching status

Black

0.59

0.39e0.90

0.01

Teaching

Hispanic

0.86

0.55e1.35

0.52

Native American White

0.73

P Value

Hospital region

Payer Medicaid

Rate Ratio

P Value

Gender Female

Table 7. Continued

0.10e5.36

0.75

Reference

Weight <500 g

5.23

1.42e19.33

0.01

500e749 g

4.93

2.04e11.89

< 0.01

750e999 g

3.82

1.60e9.15

< 0.01

1000e1249 g

2.47

1.00e6.12

0.05

1250e1499 g

Reference

1500e1749 g

0.28

0.03e2.35

0.24

1750e1999 g

0.45

0.05e3.86

0.46

2000e2499 g

N/A

N/A

N/A

>2500 g

N/A

N/A

N/A

<24 weeks

1.92

0.59e6.28

0.28

24 weeks

2.03

0.66e6.23

0.21

25e26 weeks

1.67

0.57e4.94

0.35

27e28 weeks

1.02

0.33e3.16

0.97

29e30 weeks

Reference

Reference

2.57

Nonteaching

Reference

Hospital type Children’s unit

0.99

0.56e1.75

0.97

Not children’s hospital

0.82

0.47e1.42

0.48

Children’s hospital

Reference

Bold indicates statistically significant with P < 0.05.

RR ¼ 2.21; P < 0.01, respectively). Furthermore, Medicaid patients had increased length of stay compared with private insurance patients (RR ¼ 1.38; P < 0.01). Patients with grade 4 IVH had longer lengths of stay and patients at teaching hospitals had longer lengths of stay compared with patients at nonteaching hospitals.

Gestational age

31e32 weeks

1.30

0.23e7.31

0.76

33e34 weeks

1.89

0.20e17.50

0.57

35e36 weeks

N/A

N/A

N/A

Intraventricular hemorrhage grade 1

0.56

0.17e1.78

0.32

2

0.60

0.30e1.21

0.16

3

Reference

4

1.02

0.74e1.39

0.92

Hospital bed size Small

Reference Continues

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Hospital Cost Multivariable analyses examining associations between patient demographics/hospital-level factors and high daily and total hospital costs were also conducted, presented in Tables 10 and 11. Fewer black patients had high daily costs compared with their white counterparts (RR ¼ 0.69; P ¼ 0.02). Yet, more Hispanic patients had higher daily costs than did white patients (RR ¼ 1.33; P ¼ 0.03). Fewer female patients (RR ¼ 0.76; P < 0.01) and medium bed size hospitals (RR ¼ 0.51; P < 0.01) had higher costs than did male patients and small bed size hospitals, respectively. Patients in the Midwest (RR ¼ 0.39; P < 0.01) and South (RR ¼ 0.51; P < 0.01), and teaching hospitals (RR ¼ 0.65; P < 0.01) had less high daily costs than did patients in the Northeast and nonteaching hospitals, respectively. DISCUSSION Racial and socioeconomic factors affect health care delivery in the United States despite widespread efforts to reduce disparities. Minorities and economically disadvantaged groups continue to experience inferior outcomes across an array of diseases and diagnoses, including cancer,8 heart disease,9 stroke,9 and

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FACTORS AFFECTING DEATH IN NEONATES WITH PHH

Table 8. Multivariate Analysis of Overall Shunt Complications Rate Ratio

95% Confidence Interval

Table 8. Continued

P Value

Rate Ratio

Female

1.05

Male

0.93e1.18

0.41

Medicaid Private

Small

Reference

0.63

0.51e0.78

< 0.01

Large

0.94

0.77e1.16

0.59

1.16

Hospital region Midwest

1.07

0.86e1.33

0.56

South

0.92

0.75e1.12

0.39

West

1.49

1.16e1.92

< 0.01

1.59e2.49

< 0.01

0.75

0.59e0.94

0.01

0.48

0.38e0.60

< 0.01

1.03e1.32

0.02

Reference

Race Asian/Pacific

0.74

0.46e1.20

0.23

Black

0.99

0.84e1.17

0.91

Northeast

Hispanic

0.96

0.79e1.16

0.67

Teaching status

Native American

0.76

0.31e1.86

0.55

Teaching

White

Reference

Medium

Payer

Nonteaching

Reference

Reference

1.99 Reference

Hospital type

Weight <500 g

0.74

0.35e1.54

0.42

500e749 g

1.41

1.08e1.83

0.01

750e999 g

1.49

1.16e1.91

< 0.01

1000e1249 g

1.23

0.95e1.59

0.12

1250e1499 g

Reference

1500e1749 g

1.52

1.12e2.07

< 0.01

1750e1999 g

0.95

0.61e1.46

0.80

2000e2499 g

0.89

0.55e1.41

0.61

>2500 g

1.21

0.70e2.09

0.49

Gestational age <24 weeks

0.98

0.68e1.42

0.93

24 weeks

0.76

0.55e1.05

0.10

25e26 weeks

1.01

0.77e1.32

0.97

27e28 weeks

0.81

0.62e1.06

0.13

29e30 weeks

Reference

31e32 weeks

0.61

0.42e0.90

0.01

33e34 weeks

0.80

0.49e1.31

0.38

35e36 weeks

0.57

0.29e1.12

0.10

0.65

0.43e0.99

0.05

2

0.57

0.43e0.77

< 0.01

3

Reference

4

1.31

1.15e1.49

< 0.01

Intraventricular hemorrhage grade

Continues

406

P Value

Hospital bed size

Gender

1

95% Confidence Interval

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Children’s unit Not children’s hospital Children’s hospital

Reference

Bold indicates statistically significant with P < 0.05.

diabetes.10 Epidemiologic studies have noted that African American women exhibit a 6% lower incidence of cancer than white women, but a 16% higher mortality as a result of the disease.8 Researchers have suggested multiple factors that may affect these outcomes, including availability of proper nutrition, health insurance coverage, income, education level, access to disease screening, and physicianepatient interactions.1,11 Elimination of these disparities has been designated a major goal in Healthy People 2010.12 Most studies of health care disparities focus on the adult population, but these inequalities have also extended into the pediatric realm. African American children have decreased access to care, substantially lower adherence to preventive health measures, and decreased quality in delivery of health care.13 Black children are less likely than white children to be selected from the kidney transplant waiting list and are more likely to receive inadequate hemodialysis.13 These disparities have also been documented in the perinatal literature. El-Sayed et al.14 recently published a study examining all births in Michigan between 1989 and 2005. These investigators found that socioeconomic factors and maternal demographic, behavioral, and health access differences explained approximately 30% of disparities in infant mortality in disorders relating to preterm birth. Willis et al.1 reported an IMR of 11.4 per 1000 live births for black infants and an IMR of

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ORIGINAL ARTICLE DIANA L. JIN ET AL.

FACTORS AFFECTING DEATH IN NEONATES WITH PHH

Table 9. Continued

Table 9. Multivariate Analysis of High Length of Stay Rate Ratio

95% Confidence Interval

Gender Female Male

0.93

0.77e1.11

0.43

Reference

Private

1.38

95% Confidence Interval

Medium

0.84

0.60e1.17

0.29

Large

1.11

0.79e1.55

0.55

1.13e1.69

< 0.01

Reference

Midwest

1.48

1.04e2.1

0.03

South

1.20

0.87e1.65

0.27

West

1.17

0.75e1.83

0.50

1.15e2.25

< 0.01

Northeast

Race 2.21

1.27e3.86

< 0.01

Black

1.37

1.06e1.76

0.02

Teaching Nonteaching

Hispanic

1.25

0.91e1.71

0.17

Native American

1.02

0.32e3.24

0.98

Reference

Weight <500 g

12.85

3.93e42.07

< 0.01

500e749 g

14.92

5.41e41.13

< 0.01

750e999 g

10.63

3.86e29.27

< 0.01

5.35

1.89e15.17

< 0.01

1000e1249 g 1250e1499 g

Reference

1500e1749 g

1.78

0.44e7.14

0.42

1750e1999 g

0.71

0.08e6.46

0.76

2000e2499 g

2.05

0.43e9.74

0.37

>2500 g

1.15

0.12e11.09

0.90

<24 weeks

1.83

0.85e3.93

0.12

24 weeks

2.23

1.07e4.64

0.03

25e26 weeks

1.15

0.55e2.37

0.71

0.62

0.28e1.37

0.24

Gestational age

27e28 weeks 29e30 weeks

Reference

31e32 weeks

0.67

0.18e2.52

0.55

33e34 weeks

0.42

0.05e3.47

0.42

35e36 weeks

1.40

0.27e7.33

0.69

1.20

0.66e2.18

0.56

1.15

0.79e1.67

0.48

1.02e1.58

0.03

Intraventricular hemorrhage grade 1 2 3 4

Reference 1.27

Hospital bed size Small

Reference Continues

WORLD NEUROSURGERY 88: 399-410, APRIL 2016

Reference

Teaching status

Asian/Pacific

White

P Value

Hospital region

Payer Medicaid

Rate Ratio

P Value

1.61 Reference

Hospital type Children’s unit

0.67

0.46e0.96

0.03

Not children’s hospital

0.46

0.32e0.65

< 0.01

Children’s hospital

Reference

Bold indicates statistically significant with P < 0.05.

5.1 per 1000 live white births in 2011. Furthermore, multiple studies examining U.S.- and African-born infants have demonstrated that genetic differences alone fail to explain the disparity.15-17 When accounting for traditional confounders such as payer status, gestational age, birth weight, and IVH grade, our model demonstrates that black preterm infants with PHH have a higher mortality and increased length of hospital stay compared with their white counterparts. Paradoxically, we demonstrate that black infants with PHH have a lower rate of overall general comorbidities and complications related to prematurity such as congenital cardiac anomalies and gastrointestinal complications, including necrotizing enterocolitis and intestinal perforation. Despite these lower overall comorbidities and complication rates, black PHH infants had a 47% higher rate of mortality than had their white counterparts. By contrast, our Hispanic cohort did not demonstrate an increased risk of mortality. Our findings comport with an existing perinatal literature that describes the Hispanic Paradox.18 Gould et al.19 reported that despite a highrisk profile for Hispanic mothers (because of lack of access to prenatal care), the population did not have an increased rate of low-birth-weight infants and neonatal mortality. In this report, both black and Hispanic mothers had decreased access to prenatal healthcare and less maternal education, yet black neonates had worse outcomes than had Hispanic neonates. One potential explanation for this paradox is that Hispanic mothers are subject to lower incidences of both preterm and low-birth-weight infants. Our study cohort, for this reason, is specifically limited to low-birth-weight, preterm infants who develop IVH and PHH.

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FACTORS AFFECTING DEATH IN NEONATES WITH PHH

Table 10. Continued

Table 10. Multivariate Analysis of High Daily Cost Rate Ratio

95% Confidence Interval

Rate Ratio

95% Confidence Interval

P Value

Midwest

0.39

0.25e0.59

< 0.01

South

0.51

0.36e0.72

< 0.01

0.75

0.49e1.15

0.19

0.5e0.83

< 0.01

P Value Hospital region

Gender Female

1.00

Male

0.82e1.21

0.97

Reference

West

Payer Medicaid Private

0.87

0.7e1.07

0.18

Northeast

Reference

Teaching status

Reference

Teaching

Race

0.65

Nonteaching

Reference

Asian/Pacific

1.11

0.64e1.93

0.70

Black

0.69

0.50e0.94

0.02

Hispanic

1.33

1.03e1.72

0.03

Children’s unit

1.44

0.97e2.15

0.07

Native American

0.89

0.22e3.66

0.87

Not children’s hospital

0.87

0.61e1.24

0.44

White

Hospital type

Children’s hospital

Reference

Reference

Bold indicates statistically significant with P < 0.05.

Weight <500 g

2.81

1.31e6.03

< 0.01

500e749 g

2.11

1.30e3.43

< 0.01

750e999 g

1.45

0.91e2.31

0.12

1000e1249 g

1.31

0.82e2.11

0.26

1250e1499 g

Reference

1500e1749 g

1.18

0.65e2.16

0.58

1750e1999 g

1.00

0.47e2.14

1.00

2000e2499 g

0.57

0.23e1.40

0.22

>2500 g

0.93

0.37e2.34

0.89

Gestational age <24 weeks

1.62

0.88e2.97

0.12

24 weeks

1.64

0.94e2.86

0.08

25e26 weeks

1.64

0.98e2.75

0.06

27e28 weeks

1.18

0.71e1.96

0.53

29e30 weeks

Reference

31e32 weeks

0.86

0.43e1.73

0.68

33e34 weeks

1.21

0.52e2.82

0.65

35e36 weeks

3.40

1.51e7.66

< 0.01

0.80

0.45e1.41

0.44

2

0.64

0.42e0.98

0.04

3

Reference

4

1.24

1.00e1.53

0.05

Even within this selected subgroup, black infants demonstrate higher mortality. We also demonstrate that patients covered by Medicaid have an increased mortality and length of stay compared with those with private insurance after controlling for relevant confounders. This finding is consistent with results in previous socioeconomic studies in the pediatric neurosurgical population. Attenello et al.20 demonstrated that pediatric patients insured by Medicaid were 12% less likely to have routine discharges after cerebrospinal fluid shunting procedures compared with patients with private insurance. Additional studies have demonstrated that pediatric patients of lower socioeconomic status have longer hospital lengths of stay and higher infection rates.21,22 The principal limitations to this study result from the use of a large population-based administrative database. International Classification of Diseases, Ninth Revision, Clinical Modification codes are entered by hospital staff with varied training and

Intraventricular hemorrhage grade 1

Hospital bed size Small

Reference

Medium

0.94

0.64e1.38

0.77

Large

0.87

0.59e1.28

0.49 Continues

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Figure 1. Admission frequency.

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ORIGINAL ARTICLE DIANA L. JIN ET AL.

FACTORS AFFECTING DEATH IN NEONATES WITH PHH

Table 11. Continued

Table 11. Multivariate Analysis of High Total Cost Rate Ratio

95% Confidence Interval

P Value

Male

0.76

0.63e0.93

< 0.01

Private

Small

0.51

0.36e0.73

< 0.01

Large

0.74

0.52e1.05

0.09

0.95

Hospital region Midwest

1.07

0.74e1.53

0.73

South

0.89

0.64e1.24

0.50

West

1.51

1.00e2.28

0.05

0.95e1.75

0.10

0.82

0.55e1.22

0.32

0.54

0.37e0.78

< 0.01

0.77e1.16

0.59

Reference

Asian/Pacific

0.89

0.46e1.71

0.73

Black

1.06

0.81e1.37

0.68

Northeast

Hispanic

1.34

1.00e1.78

0.05

Teaching status

Native American

1.54

0.62e3.86

0.35

Teaching

Reference

1.29

Nonteaching

Reference

Reference

Hospital type

Weight <500 g

2.08

0.78e5.51

500e749 g

3.35

1.90e5.9

0.14

Children’s unit

< 0.01

Not children’s hospital Children’s hospital

750e999 g

2.75

1.57e4.81

< 0.01

1000e1249 g

1.52

0.84e2.74

0.17

1250e1499 g

Reference

1500e1749 g

0.44

0.15e1.33

0.14

1750e1999 g

0.59

0.17e2.07

0.41

2000e2499 g

0.42

0.11e1.62

0.21

>2500 g

0.58

0.14e2.40

0.45

Gestational age <24 weeks

1.48

0.77e2.84

0.24

24 weeks

1.53

0.83e2.82

0.17

25e26 weeks

1.25

0.70e2.25

0.46

27e28 weeks

0.74

0.40e1.37

0.33

29e30 weeks

Reference

31e32 weeks

0.24

0.05e1.06

0.06

33e34 weeks

0.90

0.24e3.31

0.87

35e36 weeks

2.45

0.80e7.54

0.12

0.83

0.43e1.59

0.58

2

1.22

0.85e1.77

0.28

3

Reference

4

1.24

1.00e1.54

0.05

Reference

Bold indicates statistically significant with P < 0.05.

oversight. The potential for recording bias results in estimates of coding accuracy of approximately 80%.23 This bias can affect not only coding of diagnoses but also covariates and complications. In addition, these data sets capture only a single admission, and therefore patients who develop delayed hydrocephalus are not included. Although we used previously published methods of preventing double-counting,7 this phenomenon cannot be completely eliminated because of the lack of individual identifiers. CONCLUSIONS

Intraventricular hemorrhage grade 1

Reference

Reference

Race

White

P Value

Medium

Payer Medicaid

95% Confidence Interval

Hospital bed size

Gender Female

Rate Ratio

Continues

WORLD NEUROSURGERY 88: 399-410, APRIL 2016

The United States continues to have a high IMR compared with other Organization for Economic Cooperation and Development countries. The presence of socioeconomic disparities in health care delivery may contribute to this increased mortality. Our data, after multivariable analyses accounting for both patient and hospital factors, suggest that black preterm neonates with PHH have increased mortality despite lower overall complications of prematurity. Increased mortality is also seen in preterm neonates with PHH who have Medicaid insurance coverage independent of their racial status. Further studies are needed to understand the extent of these differences and potential causative factors.

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10. Hedderson M, Ehrlich S, Sridhar S, Darbinian J, Moore S, Ferrara A. Racial/ethnic disparities in the prevalence of gestational diabetes mellitus by BMI. Diabetes Care. 2012;35:1492-1498.

19. Gould JB, Madan A, Qin C, Chavez G. Perinatal outcomes in two dissimilar immigrant populations in the United States: a dual epidemiologic paradox. Pediatrics. 2003;111:e676-682.

2. Wasserman C, Taylor P. Infant Mortality. Washington, DC: Washington State Department of Health; 2013.

11. Smedley BD, Stith AY, Nelson AR, eds. Unequal Treatment: Confonting Racial and Ethnic Disparities in Healthcare. Washington, DC: The National Academies Press; 2003.

20. Attenello FJ, Ng A, Wen T, Cen SY, Sanossian N, Amar AP, et al. Racial and socioeconomic disparities in outcomes following pediatric cerebrospinal fluid shunt procedures. J Neurosurg Pediatr. 2015;15:560-566.

3. Moss N, Carver K. The effect of WIC and Medicaid on infant mortality in the United States. Am J Public Health. 1998;88:1354-1361.

12. National Center for Health Statistics. Healthy People 2010 Final Review. Hyattsville: US Government Printing Office, MD. 2012.

4. Nationwide Inpatient Sample. Agency for Healthcare Research and Quality; 2007. Available at: www. hcup-us.ahrq.gov/databases.jsp. Accessed June 20, 2014.

13. Flores G, Committee On Pediatric Research. Technical reporteracial and ethnic disparities in the health and health care of children. Pediatrics. 2010;125:e979-e1020.

5. Introduction to the KID. Healthcare Cost and Utilization Project (HCUP). 2015. Available at: www.hcup-us.ahrq.gov/db/nation/kid/kid_2012_ introduction.jsp. Accessed February 20, 2015.

14. El-Sayed AM, Finkton DW Jr, Paczkowski M, Keyes KM, Galea S. Socioeconomic position, health behaviors, and racial disparities in causespecific infant mortality in Michigan, USA. Prev Med. 2015;76:8-13.

6. Final Report on Calculating Nationwide Inpatient Sample (NIS) Variances, 2001. U.S. Agency for Healthcare Research and Quality; 2005. Available at: http://www.hcup-us.ahrq.gov/reports/ methods/CalculatingNISVariances200106092005.pdf. Accessed December 10, 2014.

15. David RJ, Collins JW Jr. Differing birth weight among infants of U.S.-born blacks, African-born blacks, and U.S.-born whites. N Engl J Med. 1997; 337:1209-1214.

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16. Collins JW Jr, Wu SY, David RJ. Differing intergenerational birth weights among the descendants of US-born and foreign-born Whites and African Americans in Illinois. Am J Epidemiol. 2002;155:210-216.

21. Walker CT, Stone JJ, Jain M, Jacobson M, Phillips V, Silberstein HJ. The effects of socioeconomic status and race on pediatric neurosurgical shunting. Childs Nerv Syst. 2014;30:117-122. 22. Simon TD, Hall M, Riva-Cambrin J, Albert JE, Jeffries HE, Lafleur B, et al. Infection rates following initial cerebrospinal fluid shunt placement across pediatric hospitals in the United States. J Neurosurg Pediatr. 2009;4:156-165. 23. Burns EM, Rigby E, Mamidanna R, Bottle A, Aylin P, Ziprin P, et al. Systematic review of discharge coding accuracy. J Public Health (Oxf). 2012;34:138-148.

Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

17. David R, Collins J Jr. Disparities in infant mortality: what’s genetics got to do with it? Am J Public Health. 2007;97:1191-1197.

Received 16 November 2015; accepted 12 December 2015

8. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63:11-30. 9. Lloyd-Jones D, Adams RJ, Brown TM, Carnethon M, Dai S, De Simone G, et al. Executive summary: heart disease and stroke statisticse 2010 update: a report from the American Heart Association. Circulation. 2010;121:948-954.

18. Brown HL, Chireau MV, Jallah Y, Howard D. The “Hispanic paradox”: an investigation of racial disparity in pregnancy outcomes at a tertiary care medical center. Am J Obstet Gynecol. 2007;197: 197.e1-197.e7 [discussion: 197.e7-197.e9].

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Citation: World Neurosurg. (2016) 88:399-410. http://dx.doi.org/10.1016/j.wneu.2015.12.046

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