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Racial/Ethnic Variation in Use of Ambulatory and Emergency Care for Atopic Dermatitis among US Children

  • Author Footnotes
    5 These authors share co-first authorship.
    Joy Wan
    Footnotes
    5 These authors share co-first authorship.
    Affiliations
    Department of Dermatology, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania
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  • Author Footnotes
    5 These authors share co-first authorship.
    Arman Oganisian
    Footnotes
    5 These authors share co-first authorship.
    Affiliations
    Department of Biostatistics, Epidemiology and Informatics, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA
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  • Andrew J. Spieker
    Affiliations
    Department of Biostatistics, Epidemiology and Informatics, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA

    Department of Biostatistics, Vanderbilt University Medical Center, Nashville, Tennessee, USA
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  • Ole J. Hoffstad
    Affiliations
    Department of Biostatistics, Epidemiology and Informatics, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA
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  • Nandita Mitra
    Affiliations
    Department of Biostatistics, Epidemiology and Informatics, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA
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  • David J. Margolis
    Affiliations
    Department of Dermatology, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania

    Department of Biostatistics, Epidemiology and Informatics, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA

    Center for Clinical Epidemiology and Biostatistics, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA
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  • Junko Takeshita
    Correspondence
    Correspondence: Junko Takeshita, Department of Dermatology, University of Pennsylvania Perelman School of Medicine, 3400 Civic Center Boulevard, PCAM South Tower, 7th Floor, Office 728, Philadelphia, Pennsylvania 19104, USA.
    Affiliations
    Department of Dermatology, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania

    Department of Biostatistics, Epidemiology and Informatics, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA

    Center for Clinical Epidemiology and Biostatistics, University of Pennsylvania Perelman School of Medicine, Philadelphia, Pennsylvania, USA
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  • Author Footnotes
    5 These authors share co-first authorship.
Open ArchivePublished:March 13, 2019DOI:https://doi.org/10.1016/j.jid.2019.02.024
      Previous studies indicate racial/ethnic differences in health care utilization for pediatric atopic dermatitis (AD), but do not account for disease severity impact. We sought to examine the relationship between race/ethnicity and health care utilization, both overall and by specific visit type, while accounting for AD control. A longitudinal cohort study of children with AD in the United States was performed to evaluate the association between race/ethnicity and health care utilization for AD. AD control and health care utilization were assessed biannually. Our study included 7,522 children (34.2% white, 54.2% black, and 11.5% Hispanic) who were followed for a median of 4 years (interquartile range 0.9–8.4 years). After adjusting for sociodemographic and other factors, black and Hispanic children were up to nearly threefold more likely than white children to receive medical care for AD across almost all levels of AD control. Black and Hispanic children had higher odds of primary care and emergency visits compared to whites. Black children with poorly controlled AD were significantly less likely to see a dermatologist than white children with similarly poorly controlled AD (odds ratio = 0.74, 95% confidence interval = 0.64–0.85 for limited control; odds ratio = 0.59, 95% confidence interval = 0.47–0.76 for uncontrolled AD). Together, these findings suggest the presence of racial/ethnic disparities in health care utilization for AD.

      Abbreviations:

      AD (atopic dermatitis), CI (confidence interval), OR (odds ratio), PEER (Pediatric Eczema Elective Registry)

      Introduction

      Atopic dermatitis (AD) is a chronic inflammatory skin disease that affects up to 30% of children (
      • Odhiambo J.A.
      • Williams H.C.
      • Clayton T.O.
      • Robertson C.F.
      • Asher M.I.
      Global variations in prevalence of eczema symptoms in children from ISAAC Phase Three.
      ) and is associated with significant medical, quality of life, and financial burdens (
      • Drucker A.M.
      • Wang A.R.
      • Li W.Q.
      • Sevetson E.
      • Block J.K.
      • Qureshi A.A.
      The burden of atopic dermatitis: summary of a report for the National Eczema Association.
      ,
      • Silverberg J.I.
      • Simpson E.L.
      Association between severe eczema in children and multiple comorbid conditions and increased healthcare utilization.
      ). In the United States, AD is more common among black than white and Hispanic children (
      Centers for Disease Control and Prevention, National Center for Health Statistics
      Table 1. Percentage (and Standard Error) of Children Aged 0–17 with Eczema or Skin Allergy, by Selected Demographics: United States.
      ,
      • Kim Y.
      • Blomberg M.
      • Rifas-Shiman S.L.
      • Camargo Jr., C.A.
      • Gold D.R.
      • Thyssen J.P.
      • et al.
      Racial/ethnic differences in incidence and persistence of childhood atopic dermatitis.
      ,
      • Shaw T.E.
      • Currie G.P.
      • Koudelka C.W.
      • Simpson E.L.
      Eczema prevalence in the United States: data from the 2003 National Survey of Children's Health.
      ). AD may also be more severe and persistent among racial/ethnic minority children (
      • Kim Y.
      • Blomberg M.
      • Rifas-Shiman S.L.
      • Camargo Jr., C.A.
      • Gold D.R.
      • Thyssen J.P.
      • et al.
      Racial/ethnic differences in incidence and persistence of childhood atopic dermatitis.
      ,
      • Silverberg J.I.
      • Simpson E.L.
      Associations of childhood eczema severity: a US population-based study.
      ). Relatively little is known about health care utilization patterns for AD, both overall and by race/ethnicity, and their relation to disease severity. Some data suggest that there may be racial/ethnic disparities in health care for AD whereby black children in the United States are less likely than white children to receive medical care for their skin disease (
      • Fischer A.H.
      • Shin D.B.
      • Margolis D.J.
      • Takeshita J.
      Racial and ethnic differences in health care utilization for childhood eczema: an analysis of the 2001-2013 Medical Expenditure Panel Surveys.
      ). However, among those accessing care, minority children had more ambulatory visits for their AD (
      • Fischer A.H.
      • Shin D.B.
      • Margolis D.J.
      • Takeshita J.
      Racial and ethnic differences in health care utilization for childhood eczema: an analysis of the 2001-2013 Medical Expenditure Panel Surveys.
      ), which has also been suggested in other work (
      • Horii K.A.
      • Simon S.D.
      • Liu D.Y.
      • Sharma V.
      Atopic dermatitis in children in the United States, 1997–2004: visit trends, patient and provider characteristics, and prescribing patterns.
      ,
      • Janumpally S.R.
      • Feldman S.R.
      • Gupta A.K.
      • Fleischer Jr., A.B.
      In the United States, blacks and Asian/Pacific Islanders are more likely than whites to seek medical care for atopic dermatitis.
      ). These latter findings may be an indicator of more severe AD among racial/ethnic minority children, but prior studies have been unable to directly evaluate the effect of AD disease severity on health care utilization. Furthermore, children with AD seek care in a variety of medical settings, including primary care, specialties such as dermatology or allergy, and the emergency department; however, their patterns of health care utilization across different provider or care settings remain uncertain. Given the relative paucity of studies that have evaluated health care utilization for AD, especially across racial/ethnic groups, the purpose of our study was to further elucidate the relationship between race/ethnicity and health care utilization, both overall and by specific visit type, for AD among US children, while accounting for disease control. We hypothesized that racial/ethnic minorities would have different patterns of health care utilization than whites, independent of AD disease control.

      Results

      Our study included 7,522 subjects, of whom 2,576 (34.2%) were white, 4,078 (54.2%) were black, and 868 (11.5%) were Hispanic. The median duration of follow-up across all subjects was 4 years (interquartile range 0.9–8.4 years). Baseline characteristics of the subjects are presented in Table 1. The median age at registry enrollment was approximately 6 years and was similar across all three race/ethnicity groups, though small differences were found to be statistically significantly different. The proportion of males was higher among whites than among blacks and Hispanics (51.3% vs. 43.7% and 45.9%; P < 0.001). Median age of AD onset was similar across all groups; however, AD duration was slightly longer among whites. Annual household income was significantly different across racial/ethnic groups with a greater proportion of black and Hispanic individuals reporting household incomes <$25,000 and a greater proportion of whites being in the highest income category of $100,000 or more (P < 0.001). All geographic regions of the United States were represented in the cohort (Figure 1); however, the South and Midwest were relatively over-represented compared to the Northeast and West. There were greater proportions of whites in the Midwest, blacks in the South, and Hispanics in the West. The median Urban Influence Code value was 1 or 2 in all three groups, indicating large and small metropolitan living environments, respectively. There were also significant differences in baseline AD disease control across the groups with fewer whites reporting uncontrolled disease relative to blacks and Hispanics (7.8% vs. 10.3% and 11.9%; P < 0.001). A greater proportion of whites reported having asthma (51.5% vs. 44.6% and 37.5%; P < 0.001) and seasonal allergies (72.3% vs. 58.1% and 52.1%; P < 0.001) than blacks and Hispanics, respectively.
      Table 1Baseline characteristics of study participants
      Baseline Variable
      Median and interquartile range reported for all continuous variables. Counts and proportions reported for all categorical variables. Counts may not match sample size due to missingness.
      White (n = 2,576)Black (n = 4,078)Hispanic (n = 868)P-value
      P-values were calculated using analysis of variance F tests for continuous variables and χ2 tests for categorical variables.
      Age at enrollment, y6.58 (3.91–10.32)6.68 (4.01–10.58)6.04 (3.87–9.96)0.049
      Male sex1,321 (51.3)1,781 (43.7)398 (45.9)<0.001
      Annual household income<0.001
       $0–$24,999378 (14.7)2,465 (60.5)427 (49.5)
       $25,000–$49,999394 (15.3)490 (12.0)185 (21.4)
       $50,000–$74,999323 (12.5)116 (2.9)67 (7.8)
       $75,000–$99,999228 (8.9)56 (1.4)17 (2.0)
       $100,000 or more295 (11.5)51 (1.3)9 (1.0)
       Prefer not to answer958 (37.2)895 (22.0)158 (18.3)
      Region<0.001
       Northeast261 (10.1)253 (6.2)103 (11.9)
       Midwest665 (25.8)755 (18.5)108 (12.4)
       South1,502 (58.3)2,956 (72.5)540 (62.2)
       West121 (4.7)50 (1.2)113 (13.0)
      Urban Influence Code2 (1–6)2 (1–2.33)1 (1–2)<0.001
      Age at atopic dermatitis onset, y0.75 (0.25–3)0.75 (0.75–3)0.75 (0.25–4)0.12
      Duration of atopic dermatitis, y4.11 (2.3–7.09)4.08 (2.33–7.28)3.55 (2.04–6.23)<0.001
      Atopic dermatitis disease control<0.001
       Complete183 (7.1)135 (3.3)64 (7.4)
       Good1,319 (51.2)1,855 (45.6)373 (43.1)
       Limited871 (33.8)1,662 (40.8)325 (37.6)
       Uncontrolled201 (7.8)419 (10.3)103 (11.9)
       Asthma1,326 (51.5)1,814 (44.6)325 (37.5)<0.001
       Seasonal allergies1,856 (72.3)2,364 (58.1)451 (52.1)<0.001
      1 Median and interquartile range reported for all continuous variables. Counts and proportions reported for all categorical variables. Counts may not match sample size due to missingness.
      2 P-values were calculated using analysis of variance F tests for continuous variables and χ2 tests for categorical variables.
      Figure thumbnail gr1
      Figure 1Geographical distribution of study subjects. Each circle represents an individual ZIP code, and the size of the circle reflects the number of individuals within a ZIP code. Five subjects were missing ZIP code data, and 240 ZIP codes were unable to be matched for mapping.
      Over the course of follow-up, the proportion of subjects reporting at least one health care provider visit in the prior 6 months generally declined over time among all three groups (Figure 2). Compared to whites, a greater proportion of black and Hispanic subjects reported at least one visit to any provider or a primary care provider over time.
      Figure thumbnail gr2
      Figure 2Proportion of subjects with at least one visit.
      In multivariable analyses, we found significant evidence of effect modification by AD disease control; adjusted odds ratios (ORs) measuring the association between race/ethnicity and health care utilization for AD were therefore stratified by level of disease control (Figures 3 and 4). For the primary outcome, both black and Hispanic subjects had significantly higher odds of seeing any health care professional compared to white subjects across all levels of disease control, with the exception of the uncontrolled disease group among Hispanics (Figure 3). The strength of the association between race/ethnicity and health care utilization for AD was attenuated with poorer disease control. Among black subjects, the OR for any health care provider visit was greatest among those with complete disease control (OR = 2.72; 95% CI = 2.28–3.25) and smallest among those with uncontrolled disease (OR = 1.47; 95% CI = 1.06–2.04). A similar pattern was observed among Hispanic subjects, whereby the OR among those with complete disease control was estimated at 2.87 (95% CI = 2.17–3.80) and was lowest among those with uncontrolled disease (OR = 1.30, 95% CI = 0.74–2.26).
      Figure thumbnail gr3
      Figure 3Odds of any health professional visit by race/ethnicity and atopic dermatitis disease control. CI, confidence interval; OR, odds ratio.
      Figure thumbnail gr4
      Figure 4Odds of specific health professional visits by race/ethnicity and atopic dermatitis disease control. CI, confidence interval; OR, odds ratio.
      In adjusted analyses examining specific types of health care visits, both black and Hispanic subjects had higher odds of primary care and emergency department visits compared to whites across all levels of disease control, though not statistically significant in most cases among those with uncontrolled disease (Figure 4). These associations were strongest among those with complete disease control and decreased with poorer disease control, similar to what was observed for the primary outcome. The patterns for dermatology visits were different. Among those with complete disease control, both black and Hispanic subjects were more likely than whites to have seen a dermatologist (OR = 1.77; 95% CI = 1.34–2.34 and OR = 3.15; 95% CI = 2.15–4.62, respectively). Among those with good disease control, only Hispanic subjects remained more likely to have seen a dermatologist than whites (OR = 1.58; 95% CI = 1.29–2.88), whereas black subjects were equally as likely to have seen a dermatologist as whites (OR = 0.90; 95% CI = 0.78–1.04). Of note, among those with either limited control of their AD or uncontrolled AD, black subjects were significantly less likely than whites to have seen a dermatologist (OR = 0.74; 95% CI = 0.64–0.85 and OR = 0.59; 95% CI = 0.47–0.76, respectively) while there were no statistically significant differences in the odds of Hispanic subjects seeing a dermatologist compared to whites (OR = 1.18; 95% CI = 0.96–1.47 and OR = 0.99; 95% CI = 0.69–1.42, respectively). Regarding other medical providers, blacks were less likely to have seen any other types of health professionals than whites across all levels of disease control. Hispanics also had lower odds of having seen other medical providers than whites, but the association was only statistically significant among those with limited disease control.
      The ORs for other covariates from the multivariable regression models are shown in Table 2. Of note, males had lower odds of any health care visit, primary care visit, and dermatology visit. Relative to subjects in the lowest income category, those in the higher income groups were less likely to have visited any health care professional, particularly primary care. Subjects in the higher income groups were also less likely to have had an emergency department visit but increasingly more likely to have seen a dermatologist. Having asthma was associated with greater odds of an emergency department visit and visit with other health care providers. Having seasonal allergies was associated with greater odds of all health care visit types except for emergency department visits. A sensitivity analysis additionally adjusting for geography using region of residence in addition to Urban Influence Code, the latter of which was used in the primary analysis, did not alter the primary findings (data not shown).
      Table 2Adjusted odds ratios for health care utilization outcomes from multivariable model
      Multivariable Model VariablesAny Visit (n = 7,357)Primary Care (n = 7,306)Dermatology (n = 7,148)Emergency (n = 7,101)Other (n = 7,131)
      Male sex0.84 (0.77–0.91)0.89 (0.83–0.96)0.81 (0.73–0.89)0.91 (0.78–1.07)0.97 (0.88–1.08)
      Annual household income (US$)
       $0–$24,999ReferenceReferenceReferenceReferenceReference
       $25,000–$49,9990.77 (0.68–0.88)0.74 (0.65–0.83)1.3 (1.11–1.51)1.03 (0.81–1.31)0.92 (0.78–1.09)
       $50,000–$74,9990.55 (0.47–0.63)0.45 (0.39–0.52)1.42 (1.18–1.7)0.53 (0.39–0.72)0.97 (0.78–1.21)
       $75,000–$99,9990.51 (0.43–0.62)0.39 (0.33–0.48)1.55 (1.24–1.93)0.33 (0.2–0.54)1.01 (0.77–1.31)
       $100,000 or more0.57 (0.48–0.68)0.39 (0.32–0.47)1.94 (1.59–2.35)0.39 (0.25–0.6)1 (0.77–1.3)
       Prefer not to answer0.87 (0.78–0.97)0.85 (0.77–0.94)1.16 (1.01–1.33)1.14 (0.93–1.4)1.27 (1.1–1.45)
      Urban Influence Code0.99 (0.98–1.01)1.02 (1–1.04)0.94 (0.92–0.97)1.00 (0.96–1.04)1.04 (1.02–1.06)
      Age at atopic dermatitis onset (years)0.97 (0.96–0.98)0.97 (0.95–0.98)1.00 (0.98–1.01)0.99 (0.96–1.02)0.98 (0.96–1)
      Duration of atopic dermatitis (years)0.95 (0.95–0.96)0.95 (0.94–0.96)0.99 (0.98–1)0.98 (0.96–0.99)0.97 (0.96–0.98)
      Asthma1.02 (0.93–1.11)1.05 (0.96–1.14)0.96 (0.86–1.06)1.33 (1.13–1.56)1.29 (1.15–1.44)
      Seasonal allergies1.17 (1.07–1.28)1.11 (1.02–1.21)1.17 (1.05–1.31)1.13 (0.95–1.35)1.76 (1.54–2.02)
      Intercept0.36 (0.3–0.43)0.29 (0.24–0.35)0.03 (0.03–0.04)0.005 (0–0.01)0.02 (0.02–0.03)
      Values are odds ratio (95% confidence interval).
      We evaluated the proportion of missing survey responses and found the distribution to be similar across all race/ethnicity groups (Supplementary Figure S1 online), consistent with the idea that missingness is independent of race/ethnicity. Additionally, the baseline characteristics of subjects with ≤50% of their scheduled surveys missing compared to those with >50% missing surveys were similar (Supplementary Table S1 online).

      Discussion

      In this study of a large, diverse longitudinal cohort of children with AD and access to health care, we found important differences in health care utilization patterns for AD by race/ethnicity and disease control. On average, compared to white children, black and Hispanic children were up to nearly three times more likely to have had any medical visits for AD across almost all levels of disease control, with the most striking differences observed among those with better disease control. In particular, black and Hispanic children were more likely than white children to have seen a primary care provider or visited the emergency department for their AD. Black children with complete disease control and Hispanic children with complete and good disease control were also more likely than white children to have seen a dermatologist for their AD. In contrast, among those with poorly controlled AD (i.e., limited control or uncontrolled), black children were less likely than white children to have seen a dermatologist. Importantly, these racial/ethnic differences in health care utilization persisted after controlling for sociodemographic factors, AD history, and atopic comorbidities. Together, our results suggest that previously described racial/ethnic disparities in AD health care utilization are not fully explained by differences in AD severity across racial/ethnic groups; after stratifying by AD disease control, we still observed significant racial/ethnic differences in health care visits for AD.
      To our knowledge, our study is the first to evaluate health care utilization for AD in children while simultaneously accounting for AD control and is, thus, an important addition to the limited existing literature on this topic. To date, only a few studies have assessed racial/ethnic differences in health care utilization for AD. In recent work,
      • Fischer A.H.
      • Shin D.B.
      • Margolis D.J.
      • Takeshita J.
      Racial and ethnic differences in health care utilization for childhood eczema: an analysis of the 2001-2013 Medical Expenditure Panel Surveys.
      found that black children with AD in the United States were less likely than white children to have had at least one outpatient visit for AD. However, among those accessing medical care, black children had greater health care utilization, a pattern also observed in our current study, which was thought to be an indicator of more severe AD. Older studies using data from the National Ambulatory Medical Care Survey and National Hospital Ambulatory Medical Care Survey also found that blacks and Hispanics were more likely than whites to receive care for AD, despite lower health care utilization overall (
      • Horii K.A.
      • Simon S.D.
      • Liu D.Y.
      • Sharma V.
      Atopic dermatitis in children in the United States, 1997–2004: visit trends, patient and provider characteristics, and prescribing patterns.
      ,
      • Janumpally S.R.
      • Feldman S.R.
      • Gupta A.K.
      • Fleischer Jr., A.B.
      In the United States, blacks and Asian/Pacific Islanders are more likely than whites to seek medical care for atopic dermatitis.
      ). However, a major limitation of these previous studies is the lack of information on AD severity and an inability to account for disease severity effects on health care utilization. In our current study, we leveraged Pediatric Eczema Elective Registry (PEER) data to address this limitation and found that for any given level of disease control, black and Hispanic children were still more likely to visit a health care provider for their AD. Furthermore, unlike most previous studies, we examined patterns for specific visit types and found differences in the utilization of primary care providers, dermatologists, and the emergency department that suggest the presence of racial/ethnic disparities in AD care. Consistent with our findings, a recent US survey study also found that black and Hispanic adults with AD were more likely to report emergency or urgent care visits for AD compared to whites (
      • Silverberg J.I.
      • Gelfand J.M.
      • Margolis D.J.
      • Boguniewicz M.
      • Fonacier L.
      • Grayson M.H.
      • et al.
      Atopic dermatitis in US adults: from population to healthcare utilization.
      ); however, the effect of disease severity on emergency or urgent care visits was not evaluated, and examination of other medical visit types by race/ethnicity was not performed.
      As we were unable to determine the precise temporal relationship between AD control and health care visits in our study, the interpretation of our findings is complex. AD severity is likely an important driver of health care utilization, but health care utilization also impacts the level of AD control. For children who had complete or good control of their AD, one interpretation of our data could be that black and Hispanic children are more likely than white children to visit a medical provider because their skin disease is well controlled. As this is an unlikely scenario, we favor an alternative interpretation that black and Hispanic children are more likely than white children to require medical visits for their AD in order to achieve complete or good control of their skin. With regard to specific visit types, our data also suggest that black and Hispanic children are more likely than white children to visit a dermatologist or emergency department in order to maintain complete AD control. Our observations could be related, in part, to possible inherent biological differences in AD activity or therapeutic response across racial/ethnic groups. It has been suggested that AD may be more severe among minority children (
      • Silverberg J.I.
      • Simpson E.L.
      Associations of childhood eczema severity: a US population-based study.
      ), hence they may require more medical care to achieve adequate disease control. It is also possible that differential access to health care providers and treatment across racial/ethnic groups, as has been observed for other diseases (
      • Melfi C.A.
      • Croghan T.W.
      • Hanna M.P.
      • Robinson R.L.
      Racial variation in antidepressant treatment in a Medicaid population.
      ,
      • Melia M.T.
      • Muir A.J.
      • McCone J.
      • Shiffman M.L.
      • King J.W.
      • Herrine S.K.
      • et al.
      Racial differences in hepatitis C treatment eligibility.
      ), may partly drive the different health care utilization patterns observed.
      Among children with limited AD control or uncontrolled AD, black and Hispanic children remained more likely than white children to have had any medical visits, specifically primary care and emergency department visits. However, the relative differences between the racial/ethnic groups were substantially attenuated compared to children with complete or good disease control. Collectively, these data indicate that, at least for primary and emergency care, differences in health care utilization among racial/ethnic groups are smaller when AD is poorly controlled. This was also observed for dermatology visits among Hispanic versus white children. Yet, black children with poor AD control were 25–40% less likely than white children with similarly poorly controlled AD to have seen a dermatologist for their skin disease, suggesting a disparity in specialist care for AD where it would seem most needed.
      The reasons for these observed differences in health care utilization patterns for AD by race/ethnicity are unclear and could be due to various factors, including differential access to primary, emergency, and specialty care, as well as different preferences for specific types of medical care. While we tried to minimize the impact of medical access-related factors on health care utilization by controlling for household income and rurality of residence, additional confounding by insurance status, for example, may still exist. Although preferences for specific types of medical care have not been studied directly in the setting of dermatologic care, one qualitative study of patients of low socioeconomic status identified greater accessibility, lower cost, and perceptions of higher quality care as reasons for such patients to prefer and use acute hospital over primary care (
      • Kangovi S.
      • Barg F.K.
      • Carter T.
      • Long J.A.
      • Shannon R.
      • Grande D.
      Understanding why patients of low socioeconomic status prefer hospitals over ambulatory care.
      ). Further research will be important in exploring reasons for existing racial differences and potential disparities in health care utilization for AD. Nevertheless, our findings emphasize the need to optimize health care utilization for minority children with AD, which should include ensuring access to high-quality and routine primary care, appropriate referral to dermatology, and judicious use of emergency care, the financial burden of which has been estimated to be increasing (
      • Kwa L.
      • Silverberg J.I.
      Financial burden of emergency department visits for atopic dermatitis in the United States.
      ) for this chronic disease. Our findings that minority children are more likely to seek primary and emergency department care for AD also suggest the importance of directing future interventions to reduce disparities in AD care at these points of contact with the health care system.
      There are additional limitations to consider in our study. First, the PEER data are based on self-report, introducing the potential for recall and misclassification biases. While differential reporting of outcomes or disease control by race/ethnicity could also potentially confound our results, the missingness of data did not vary by race/ethnicity, suggesting that this is unlikely. Second, it is possible that unmeasured variables, such as insurance status, may serve as confounders for the estimated associations. Third, the small numbers of subjects in other racial/ethnic groups precluded us from including them in this study. Fourth, as subjects were initially enrolled in PEER through a physician’s office, the population in PEER may not be generalizable to children who are not accessing health care for their AD. Generalizability may also be limited by the requirement for subjects to have used topical pimecrolimus prior to registry enrollment. Topical pimecrolimus is a commonly used treatment for mild-to-moderate AD, and PEER likely represents a population whose AD was severe enough at enrollment to require topical therapy. Our findings may also not be generalizable to non-US or adult populations. Nevertheless, PEER is one of the largest and longest longitudinal cohorts of children with AD in the United States and provides a rich source of data on health care utilization for individual children over time.

      Conclusions

      Compared to whites, black and Hispanic children in the United States are, on average, more likely to have a medical visit for AD, across nearly all levels of AD control and independent of other sociodemographic factors and atopic comorbidities. Our data suggest the presence of racial/ethnic disparities in health care utilization for AD, including greater utilization of the emergency department among black and Hispanic versus white children across almost all levels of disease control and underutilization of dermatologists specifically among black children with poor AD control. Future work will be needed to understand the factors driving these differences in health care utilization and to design interventions to eliminate these suggested disparities in AD care for children.

      Materials and Methods

      Study design and data source

      We conducted a cohort study using data from PEER, an ongoing longitudinal prospective cohort of children with AD. PEER was primarily created for a post-marketing safety evaluation of the risk of malignancy associated with pimecrolimus cream, a common topical calcineurin inhibitor for the treatment of AD (
      • Margolis D.J.
      • Abuabara K.
      • Hoffstad O.J.
      • Wan J.
      • Raimondo D.
      • Bilker W.B.
      Association Between malignancy and topical use of pimecrolimus.
      ). At the time of enrollment, all subjects in PEER were 2–17 years old, had a physician-confirmed diagnosis of AD, and had used pimecrolimus cream for at least 6 weeks. Subjects were not required to continue pimecrolimus treatment to remain in the cohort, and most did not (
      • Kapoor R.
      • Hoffstad O.
      • Bilker W.
      • Margolis D.J.
      The frequency and intensity of topical pimecrolimus treatment in children with physician-confirmed mild to moderate atopic dermatitis.
      ). Subjects completed a baseline questionnaire at enrollment that collected information on basic demographics, including race, ethnicity, and socioeconomic status. At baseline and every 6 months thereafter, subjects were also surveyed about their AD disease control in the preceding 6-month period, measured as complete control, good control, limited control, or uncontrolled. Subjects also reported treatment use and visits to a pediatrician, family physician, dermatologist, emergency department, nurse, or other medical professional specifically for AD in the preceding 6 months. Subjects in the PEER registry are followed for up to 10 years for a total of up to 21 surveys. Informed written consent was obtained from each study participant. The present study was granted exempt status by the University of Pennsylvania Institutional Review Board.

      Study population

      We included subjects who were enrolled between November 2004 and September 2017 and who self-reported race/ethnicity as non-Hispanic white (hereafter referred to as white), non-Hispanic black (hereafter referred to as black), or Hispanic. Other racial groups were excluded due to small numbers.

      Definitions of exposure and covariates

      Race/ethnicity was the primary explanatory variable or exposure, categorized as white (reference), black, and Hispanic. Current age, age of AD onset, gender, duration of AD, annual household income, ZIP code of residence, and the presence of asthma and seasonal allergies were determined at enrollment. ZIP codes were used to assign an Urban Influence Code to each subject’s county of residence. Urban Influence Code is a measure of rurality that has been used in health services research and ranges from 1 (most urban) to 12 (most rural) (
      • Baer L.D.
      • Johnson-Webb K.D.
      • Gesler W.M.
      What is rural? A focus on Urban Influence Code.
      ,
      • Hall S.A.
      • Kaufman J.S.
      • Ricketts T.C.
      Defining urban and rural areas in US epidemiologic studies.
      ). Information on AD disease control was obtained from baseline and biannual surveys. In previous analyses of PEER data, self-reported AD disease control has demonstrated substantial to moderate agreement with the Patient-Oriented Eczema Measure, a core patient-reported outcome measure used in AD research (
      • Chang J.
      • Bilker W.B.
      • Hoffstad O.
      • Margolis D.J.
      Cross-sectional comparisons of patient-reported disease control, disease severity and symptom frequency in children with atopic dermatitis.
      ).

      Definitions of outcomes

      The primary outcome was health care utilization for AD defined by at least one visit to a health care provider (pediatrician, family physician, dermatologist, emergency department, nurse, or other health care provider) in the preceding 6 months specifically for AD. We also examined visits to specific health care providers as follows: primary care (pediatrician, family physician, or nurse), dermatology, emergency department, and other health care provider.

      Statistical analysis

      Comparisons of baseline characteristics between race/ethnicity categories were evaluated using analysis of variance F tests for continuous variables and χ2 test for categorical variables. To assess the association between race/ethnicity and health care utilization for AD, we used binary-outcome (logistic) generalized estimating equations with a working independence correlation structure to estimate covariate-adjusted ORs, while accounting for repeated health care utilization measures for each subject. Separate analyses were performed for the primary outcome and each of the four secondary outcomes. In each analysis, we adjusted for time-stable covariates of gender, age at AD onset, annual household income, Urban Influence Code, and atopic comorbidities (asthma and seasonal allergies); and the time-varying covariates of AD duration and disease control. We also tested for an interaction between race/ethnicity and AD disease control. A sensitivity analysis additionally adjusting for geographic region was also performed. Because the generalized estimating equation method requires the assumption that missingness in the outcome occurs completely at random, we examined missing data patterns to determine if there was any clear evidence that this assumption was violated (Supplementary Table S1, Supplementary Figure S1). Analyses were conducted using R, version 3.4 (R Foundation), SAS, version 9.4 (SAS Institute, Cary, NC), and Stata, version 15.1 (StataCorp, College Station, TX).

      Data availability statement

      The data set related to this article cannot be publicly shared as it is part of an ongoing US Food and Drug Administration–mandated post-marketing study.

      Conflict of Interest

      Junko Takeshita received a research grant from Pfizer (to the Trustees of the University of Pennsylvania) and has received payment for continuing medical education work related to psoriasis that was supported indirectly by Eli Lilly. Joy Wan has received research fellowship funding from Pfizer (to the Trustees of the University of Pennsylvania) and payment for consulting work with Health Union. David J. Margolis has served on advisory committees for Sanofi/Regeneron and Pfizer. The remaining authors state no conflict of interest.

      Acknowledgments

      We thank Anjana Sevagamoorthy for her assistance with the geographic mapping analysis. This study was supported in part by grants from the National Institute of Arthritis and Musculoskeletal and Skin Diseases K23-AR068433 (Takeshita), T32-AR007465 (Wan), R01-AR069062 (Margolis), and R01-AR070873 (Margolis), and a Dermatology Foundation Dermatologist Investigator Research Fellowship (Wan). The data source used in this study is the Pediatric Eczema Elective Registry, which is a study funded by Valeant Pharmaceuticals through a grant to David J. Margolis. No funding sources had a role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; or decision to submit the manuscript for publication.

      Author Contributions

      Conceptualization: JT, JW; Data Curation: OJH, JW; Formal Analysis: NM, AO, AJS, JW; Funding Acquisition: DJM, JT, JW; Investigation: AO, AJS, JT, JW; Methodology: AO, AJS, JT, JW; Project Administration: JT, JW; Resources: DJM; Software: AO, AJS; Supervision: DJM, NM, JT; Validation: NM, AO, AJS; Visualization: AO, JW; Writing - Original Draft Preparation: AO, JT, JW; Writing - Review and Editing: JW, AO, AJS, OJH, NM, DJM, JT

      Supplementary Material

      Figure thumbnail fx1
      Supplementary Figure S1Distribution of missing surveys (outcomes) by race/ethnicity.
      Supplementary Table S1Characteristics of study participants with more than half of surveys missing
      Baseline Variables
      Median and interquartile range reported for all continuous variables. Count and proportions reported for all categorical variables. Counts may not match sample size due to missingness.
      ≤50% Missing (n = 4,415)>50% Missing (n = 3,599)
      Race/ethnicity
       White1,662 (37.6)914 (25.4)
       Black2,121 (48.0)1,957 (54.4)
       Hispanic373 (8.5)495 (13.8)
      Atopic dermatitis disease control
       Complete208 (4.7)198 (5.5)
       Good2,067 (46.9)1,729 (48.1)
       Limited1,726 (39.2)1,310 (36.5)
       Uncontrolled406 (9.2)356 (9.9)
      Age at enrollment, y6.52 (4.01–10.21)6.65 (3.87–10.71)
      Male sex2071 (46.9)1668 (46.4)
      Annual household income (US$)
       $0–$24,9991,665 (37.8)1,722 (47.9)
       $25,000–$49,999661 (15.0)495 (13.8)
       $50,000–$74,999380 (8.6)182 (5.1)
       $75,000–$99,999253 (5.7)74 (2.1)
       $100,000 or more278 (6.3)132 (3.7)
       Prefer not to answer1,173 (26.6)988 (27.5)
      Urban Influence Code2 (1–3)2 (1–2.33)
      Age at atopic dermatitis onset, y0.75 (0.25–3)0.75 (0.75–3)
      Duration of atopic dermatitis, y4.07 (2.32–7.07)4 (2.25–7.21)
      Asthma2,122 (48.1)1,548 (43.1)
      Seasonal allergies2,843 (64.6)2,090 (58.2)
      1 Median and interquartile range reported for all continuous variables. Count and proportions reported for all categorical variables. Counts may not match sample size due to missingness.

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