Disparities in Pediatric Rheumatic Diseases

Introduction

Major health disparities have been identified among youth with rheumatic diseases. In particular, recent studies in pediatric rheumatology have found that youth from disadvantaged socioeconomic backgrounds report worse quality of life and experience worse disease outcomes, delays in care, and even sub-optimal treatment. This aligns with the greater body of health disparity literature that documents the significant impact of social determinants of health on a wide spectrum of health outcomes among children and adolescents¹. In this review we discuss the current literature on health and healthcare disparities affecting youth with rheumatic diseases, intervention studies that have aimed to mitigate disparities, and strategies to achieve healthcare equity that urgently require investigation within pediatric rheumatology.

Healthy People 2020 defines health disparity as “a health difference that is closely linked with social, economic, and/or environmental disadvantage”² . Furthermore, healthcare disparities can be attributed to disparities in financial resources available for health spending, as well as structural and institutional barriers that prevent equitable delivery of health services². While health differences exist across the spectrum of health outcomes, health disparities are those that are systematic, avoidable, unfair, and unjust³. Social-ecological models, adapted from Bronfenbrenner’s ecological model of human development⁴, can be used to help define the nested factors related to familial, individual care, health systems, and broader societal environments that contribute to health and healthcare disparities in pediatric rheumatology (Fig. 1)⁵.

Figure 1. Modified Social-Ecological Model of Contributors to Health Disparities in Pediatric Rheumatology.

Potential societal, institutional, individual care, and familial determinants of health disparities among youths with pediatric rheumatic diseases. This conceptual framework is based on Reifsnider et al.’s modified Bronfenbrenner social-ecological model⁵.

Characteristically health disparities affect socially disadvantaged populations who experience barriers to optimal health created by historically-embedded practices of systemic racism and individual and institutional discrimination based on racial/ethnic group, religion, socioeconomic status (SES), gender, mental health, disability, sexual orientation and geographic region². Social determinants of health are personal, social, economic, and environmental factors that shape an individual’s health². These factors are primary drivers of health and healthcare disparities among socially disadvantaged racial/ethnic, gender, and socioeconomic groups⁶. Despite their critical role in other health outcomes, research in social determinants of health in pediatric rheumatology treatment delivery and disease outcomes remains sparse. Robust health and healthcare disparity research is crucial to the development of appropriate changes in practice and health policy to address health equity in pediatric rheumatology.

Disparities in childhood-onset SLE (cSLE)

Health disparities in childhood-onset systemic lupus erythematosus (cSLE) have received more attention in pediatric rheumatology research than disparities in most other rheumatologic diseases. This attention is warranted as cSLE can be a deadly disease, more so with sub-optimal treatment. In young adults SLE is even more deadly than in other age ranges ⁷ and cSLE is more deadly compared to adult-onset SLE⁸. Morbidity associated with cSLE is particularly high in young adults of minority race/ethnicities. In the US, SLE ranks as the 5th cause of death among Black and Hispanic females ages 10–25 years old⁹.

Despite the attention given to disparities along race/ethnicity, major gaps in the cSLE literature exist for other social determinants of health. Few studies have examined income, education, and other factors associated with systemic barriers to health equity.

Disparities in Health in cSLE

There are striking differences in prevalence across race/ethnicities for SLE both in pediatric and adult populations. The prevalence of cSLE is especially high in indigenous peoples around the globe, including Native American/First Nation Canadians, Maori people of New Zealand, and the Aboriginal people of Australia^10–14. The highest prevalence of cSLE, like SLE, is documented in Native American and First Nation Canadians. The prevalence in Native American children is around 13 per 100,000 and at least 3 times that of the general population^{10, 11}. Black, Hispanic/Latino, and Asian youth have higher prevalence than white youth¹⁰.

The largest effort to identify disparities across race/ethnicity in SLE was through the LUMINA study (Lupus in Minorities: Nature versus Nurture) in the US¹⁵. While this study primarily examined adults, a proportion of participants were pediatric age. Research out of the LUMINA study established that both Hispanic and Black Americans had worse disease activity scores, worse patient reported outcomes, and worse organ involvement (specifically cardiac and renal). In line with this, Hispanic and Black Americans were more likely to be treated with more steroids and cyclophosphamide, likely indicating worse disease^16–22.

Indeed, differences in cSLE disease severity between Black and white youth is evident from several other studies, as well. Studies in cSLE have consistently demonstrated that Black youth are more likely to have the most severe forms of organ involvement associated with SLE, including renal, neurologic, and cardiac disease^23–25. Furthermore, Black youth with cSLE are more likely to have SLE organ-related disease than even Black adults with adult-onset SLE, with more renal, neurologic, hematologic and ocular manifestations^{26, 27}.

Worldwide, non-white youth with cSLE have worse disease outcomes compared to white youth. Black youth from low-resource areas demonstrate the highest rates of end-organ disease and morbidity. In the PULSE cohort from South Africa, Black South African children had more end-organ damage (63% vs 23%) than Black American youth from the Childhood Arthritis and Rheumatology Research Alliance (CARRA) registry, and more Black youth from the PULSE cohort required renal transplantation (8% vs. <1%)²⁸.

Frequent hospitalizations in cSLE are associated with increased morbidity and mortality and disparities in hospitalizations of cSLE patients based on race/ethnicity have also been identified, with Black and Hispanic youth being overrepresented⁷. Demographic factors associated with increased length of stay in the hospital include other race than white or Black and urban location, after accounting for important clinical factors such as lupus nephritis⁷. Mortality data from the National Vital Statistics System of the National Center for Health Statistics shows that the Black/white mortality rate was 5.7 for patients aged 0–24 in 1995– 1997 which increased to 6.7 in 2015–2017²⁹. Another recent national study of youth enrolled in Medicaid (an indicator of low income) showed that Black race and hospital location in the Southern US were among the strongest risk factors for hospitalization mortality, even after accounting for lupus nephritis and young adult age (age 18–20)⁷. The mortality of Black youth with end-stage renal disease (ESRD) from lupus nephritis is twice that of their white counterparts¹⁰.

Disparities in Healthcare in cSLE

Health disparities observed in cSLE may be related to or a direct result of disparities in healthcare, specifically disparities in access and treatment. However, few studies to date have examined disparities in quality of care, access in care, and treatment in cSLE. The studies to date that have attempted to examine these questions indicate important disparities in healthcare along race/ethnicity and income. A study of the CARRA registry found that delays in diagnosis of >1 year were more likely in youth with cSLE from low-income families and that youth living in a state with a high density of pediatric rheumatologists were more likely to be seen expeditiously³⁰. Youth with ESRD from lupus nephritis in the US Renal Data System were less likely to receive renal transplants if they were Black, Hispanic, older, or on Medicaid¹⁰.

Among the co-morbidities in SLE that are highly associated with worse quality of life, are mental health disorders. Approximately a third of youth with cSLE have clinically significant symptoms of depression and/or anxiety³¹. While in studies of single-center cohorts Black youth appear to be more affected³², in a large study of a national Medicaid sample, Black youth were less likely to be diagnosed with depression or anxiety and less likely to receive pharmacotherapy³³. Beyond affecting quality of life, this disparity may have important implications on SLE disease outcomes. Depression symptoms are associated with worse medication adherence in youth³⁴ and among cSLE youth with mental health disorders, mental health treatment, including the use of pharmacotherapy, improves adherence³⁵.

Disparities in Juvenile Idiopathic Arthritis (JIA)

Juvenile idiopathic arthritis is the most common pediatric rheumatologic disease and is associated with an increased risk for morbidity and disability³⁶. According to the International League of Associations for Rheumatology (ILAR) JIA is comprised of seven subtypes that vary by clinical characteristic, and classically by the number of affected joints and extraarticular symptoms³⁷.

Health Disparities in JIA

Overall, the global prevalence rate for JIA is 132 per 100,000³⁸. Conversely, annual incidence rates for JIA range from 16 to 113 per 100,000 depending on the country and underlying population. Prevalence rates for rheumatoid factor (RF)-positive polyarticular JIA among American Indian/First Nations youth may be particularly high, but studies are scarce^{11, 39, 40}. In the large US multi-center CARRA Registry, approximately 93% of youth diagnosed with JIA (N=4682) identified as white, and 11% as Hispanic ethnicity; only 5% identified as Black and 3% as Asian⁴¹.

When stratified by race and ethnicity, a greater percentage of white youth reported oligoarthritis, whereas a higher proportion of African American (16%) and Hispanic (21%) youths were more likely to present with systemic manifestations compared to white (7%) and non-Hispanic (8%) youth⁴¹. Furthermore, although rates of polyarthritis were comparable by race/ethnicity, higher proportions of both Black (26%) and Hispanic (23%) youths with JIA were RF-positive compared to 9% of both white and non-Hispanic comparator groups⁴¹.

Similar distributions were observed by global region, with the highest frequencies of systemic arthritis reported among traditionally less-developed regions of Southeast Asia, Latin America, and Africa and the Middle East, ranging from approximately 30% to slightly less than 20% compared to areas of Europe and North America (<10%), with the highest frequencies of RF-positive polyarthritis in Latin America and Southeast Asia⁴².

Despite similar prevalence rates of polyarticular JIA among white and Black youth, Black youth had 1.9 times greater odds of joint damage⁴¹ and persistently greater physician- and patient/caregiver-assessed disease activity and JIA-related pain⁴³ than white counterparts. Social constructs of race/ethnicity and SES are strongly interrelated in the US⁴⁴, in both of these studies, Black youths were more likely to report indicators of low SES, including annual household income less than $50,000 and reliance on public health insurance. Similarly, children with Medicaid were more likely to present with polyarticular and/or systemic JIA features, as well as present with more active disease and pain than children with private health insurance⁴⁵.

Increased disease activity and morbidity can result in greater disability and reduced quality of life. Low SES, compared to high SES, has been associated with increased disability and decreased quality of life as measured by higher Childhood Health Assessment Questionnaire (CHAQ) scores and worse illness perception^{45, 46}. Similarly, among Egyptian youths with JIA, low SES was also associated with impaired health related quality of life (HRQoL) compared to high SES individuals⁴⁷. Living on a reservation, rather than American Indian race, was correlated with increased JIA-related disability, supporting the role of SES and place-based factors in race/ethnicity-based health disparities⁴⁸.

Healthcare Disparities in JIA

Early and aggressive treatment of JIA^49–51 has been shown to improve treatment response and outcomes, so responsive access to care and quality treatment is necessary. However, disparities in access to care and treatment among youth with JIA has been largely understudied and instead inferences are often made from adults with rheumatoid arthritis, healthcare practices in other countries, and other pediatric subspecialties⁵².

In the US, urbanicity is often characterized by greater racial/ethnic heterogeneity, as well as areas of concentrated poverty and economic disadvantage, due to historical practices of segregation^{53, 54}, these pockets of increased socioeconomic disadvantage facilitate physical and socioeconomic barriers to access to quality healthcare. In general, children with public insurance are more likely to be denied a subspecialty appointment and experience severe delays in specialty appointments compared to children with private insurance⁵⁵. Outside of the U.S., high parental educational attainment⁵⁶, private insurance⁵⁷, and shorter distance to travel^{57, 58} were all associated with earlier access to a rheumatologist for treatment of JIA symptoms.

Biologic disease-modifying antirheumatic drugs (DMARDs) are instrumental in the treatment of JIA, particularly among severe cases. Studies have demonstrated that use of biologic DMARDs early in the disease process can better reduce disease activity and facilitate early disease management compared to conventional treatments^{51, 59}. Whereas disparities in biologic DMARD use has been reported among Black adults with rheumatoid arthritis compared to white counterparts⁶⁰, these disparities have not been fully elucidated among youth with JIA. Although not designed to examine differences across socio-demographics, studies have reported both higher⁶¹ and lower⁶² biologic DMARD use among Black children.

Disparities in Other Diseases in Pediatric Rheumatology

Outside of cSLE and JIA there is very sparse literature involving other pediatric rheumatologic diseases aimed to help identify health and healthcare disparities. Few studies of juvenile dermatomyositis youth show a continued pattern of Black and Hispanic youth and youth from low-income families faring worse, both with delays in diagnosis, increased length of stay during hospitalization and higher rates of calcinosis^63–65. Of concern is the growing literature indicating important health disparities in adult patients with some of these diseases, including ones with high morbidity and mortality such as systemic sclerosis^66–70 and sarcoidosis^71–74 .

Disparities in Transitional Care

The transition period from pediatric care to adult care is particularly challenged by changes and increased barriers to healthcare access. In certain disease in pediatric rheumatology, such as SLE, the age group in which patients transition is particularly medically vulnerable and plagued by increased mortality and poor outcomes^{29, 75, 76}. Among youth with general chronic disease, young adults who are Black or Hispanic, of lower SES and non-English speakers are less likely to be adequately prepared to transition⁷⁷.

There are limited studies in rheumatology that investigate racial and ethnic differences during transition. A recent study of a large cohort of privately insured young adults with cSLE found no difference across racial and ethnic groups in a successful transfer, defined as visit with an adult rheumatology/nephrology within 12 months after the last pediatric subspecialist visit⁷⁸. A smaller study of youth with cSLE found that lower education and white race was associated with gaps in care during transition⁷⁹.

There is high variability in the transition process across pediatric rheumatology practices despite both pediatric transition guidelines⁸⁰ and guidelines specific for pediatric rheumatology^{81, 82}. Only 8% of pediatric rheumatologists are very familiar the American Academy of Pediatrics transition policy and less than half report following their department’s own formal transition policy⁸³. Potentially, this variability may be a source of disparities, however this area has yet to be adequately investigated.

Interventions to Eliminate Health & Healthcare Disparities

The development and implementation of effective interventions to mitigate health and healthcare disparities requires an iterative process of identifying, monitoring , and addressing disparities (Fig. 2)⁸⁴. Interventions to decrease the gaps in health disparities created by inequities in healthcare are multifactorial and target individual, community, and macro-environmental factors related to federal policies and systems⁸⁵.

Figure 2. Addressing Health Disparities in Pediatric Rheumatologic Diseases.

A proposed iterative framework to address health disparities through evidence-based methods. This is modified form a conceptual framework developed by Rashid et al⁸⁴.

An example of federal programming that successfully targeted disparities² is the State Children’s Health Insurance Program (sCHIP), federally-funded medical insurance for low-income children. The initiation sCHIP was associated with an increase in access to medical care for Black and Hispanic children by 10% and 21%, respectively. Following program initiation racial/ethnic disparities in unmet needs (delayed or foregone preventive, acute, specialty, emergency care, and required prescriptions) were eliminated with unmet needs at 19% for all racial/ethnic groups. At minimum, pediatric rheumatologists can work with other healthcare workers, such as nurses and social workers, to secure insurance for patients⁸⁶.

At an institution and practice level, interventions are aimed to standardize care, improve provider education, and implement practices that affect vulnerable populations. A study of the implementation of an integrated care management program was developed and used in multihospital system in Boston to address social needs in vulnerable adult patients with medically and psychologically complex SLE⁸⁷. Addressing social determinants of health is an important mechanism of mitigating healthcare disparities and the use of a social needs assessment tools has been proposed as an initial step of promoting health equity⁸⁸.

In pediatric rheumatology, as is seen widely in medicine, clinicians do not always deliver the recommended care despite multiple guidelines^89–92. In a recent study done by Burman et al. the investigators created a pediatric lupus care index (p-LuCI) which includes standard of care assessments or interventions that should be done at specified times⁹³. Care and completion of the p-LuCI after intervention varied based on patient and clinician characteristics. Hispanic ethnicity was associated with higher likelihood of completion, over Black and white patients.

Encouragingly, in an implementation study in JIA toward a treat-to-target approach using a clinical decision support tool by Chang et al. demonstrated overall improvement in clinical Juvenile Arthritis Disease Activity Scores (cJADAS) and a gap in score improvement between races favored improvement in Black children⁶². Importantly, though, it did not close the disparity gap in cJADAS scores between Black and white children. It is possible, that prior to the implementation Black patients did not obtain sufficiently aggressive therapy. Standardization of care through tools utilizing and leveraging electronic medical records is a way to diminish the impact of potential implicit or explicit biases a provider may have that lead to disparities in care.

One critical means of increasing access to care is to increase the limited pediatric rheumatology workforce. Because of a dearth in pediatric rheumatologists, many youth must seek care with an adult rheumatologist who is not as highly trained in specific pediatric rheumatic diseases or as familiar with the clinical nuances required to optimally treat this population ^{94, 95}. Furthermore, there is a mismatch of more senior pediatric rheumatologists leaving the workforce than trainees entering. By 2030 there is projected to be a remarkable deficit of 50% in the number of pediatric rheumatologists in the US. The Southeast, South Central and Southwest regions of the US are expected to be most affected⁹⁶.

With efforts to grow the workforce, an important consideration will be to increase the number of pediatric rheumatologists from underrepresented demographics. Key strategies put forth by the U.S. Department of Health and Human Services’ Office of Minority Health to address disparities include increase cultural competency of healthcare workers, support initiatives to increase a diverse work force and promote community interventions⁹⁷.

Little has been reported recently on the demographic make-up of pediatric rheumatologists, but a study from 2000 indicated that 95% of the workforce is white⁹⁵. The adult workforce, which often services pediatric rheumatology patients, is also highly non-diverse. In a study looking at adult rheumatologists, underrepresented in medicine (URIM) trainees, which include Black or African American, American Indian or Alaska Native, Native Hawaiian or other Pacific Islander, Hispanic or Latino, have increased in most internal medicine subspecialties, but not rheumatology, which remains under 12%⁹⁷.

Discordance in race between clinicians and patients is a risk factor for negative patient-physician interactions and disparate care. One study found that Black SLE patients report more hurried communication and a perception of providers using more difficult words than white patients⁹⁸. Further investigations on rheumatologists’ implicit biases and the effect on patient treatment and outcomes are needed.

Among key strategies to address healthcare disparities put forth by the US Department of Health and Human Services’ Office of Minority Health is the education of healthcare workers toward improved cultural competency⁹⁷. This includes education about healthcare disparities. Education about healthcare disparities for rheumatology trainees and faculty is highly variable and proposed curriculum to address gaps in knowledge is currently being developed⁹⁹.

Areas for Future Studies

Historically, one of the challenges in identifying disparities in pediatric rheumatic diseases stems from a body of literature that is largely based on small single-centered studies without a wide enough lens or enough power to detect differences across sociodemographic groups such as race/ethnicity. Over the past decade, investigators have utilized administrative datasets and the CARRA registry, which has led to a deeper understanding of disparities impacting this patient population. However, there are still not enough studies in pediatric rheumatology that have examined even the most basic social determinants of health, such as income-level and poverty¹⁰⁰. The continued use of large datasets and registries, such as the CARRA registry, will help advance the field in further identifying disparities in not only the more common pediatric rheumatic diseases, but the rarer diseases, as well. This research will help guide the development of targeted provider- and institution-level interventions and system-level advocacy. Critical to the success of this, will be ensuring that registries are representative of a diverse group of patients and are not unintentionally or systematically excluding hard-to-reach populations.

Indeed, currently there is a distinct gap in the literature regarding many underrepresented populations. In the US literature, Native Americans and American Indian youth are almost entirely absent. Despite this, in the few studies that have specifically investigated Native American youth, they are at higher risk for many rheumatic diseases, including cSLE and polyarticular JIA¹¹. Furthermore, there are populations for which even the prevalence of disease is unknown due to a lack of rheumatologists. This particularly affects the continent of Africa^{101, 102}.

A recent systematic review of the participation of underrepresented patients in research in SLE and Rheumatoid Arthritis found that trust in the patient physician relationship, inclusion/exclusion criteria that make Black and Hispanic ineligible, community engagement have been barriers to inclusive research in rheumatology¹⁰³. These need to be carefully addressed in research in pediatric rheumatology and are critical to further identify and address disparities.

If intervention studies do not include diverse populations or intentionally exclude groups based on language, resources, acceptability, or other barriers, they have the potential to exacerbate health disparities. Recently, several studies in pediatric rheumatology have implemented technology-based programs and web-based programs for peer support and self-management support. Two studies from the University of Toronto have shown that implementing these tools can lead to important improvements in quality of life and self-management for youth with JIA^{104, 105}. As these interventions are further tested for efficacy, it is critical that testing is specifically designed to be inclusive of participants across demographics, languages, and resources. This is especially important for technology-based interventions. A study by Sun et al., indicates that non-white, rural, low-income and Spanish speaking families in rheumatology were less likely to access electronic patient portals¹⁰⁶.If intervention studies do not include diverse populations or are intentionally excluding groups based on language and resources, they have the potential to increase health disparities. Recently, several studies in pediatric rheumatology have implemented technology-based programs and web-based programs for peer support and self-management support. Two studies from the University of Toronto have shown that implementing these tools can lead to important improvements in quality of life and self-management for youth with JIA^{104, 105}. As these interventions are further tested of efficacy, it is critical that testing is specifically designed to inclusive of participants across demographics, languages, and resources. This is especially important for technology-based interventions. A study by Sun et al, indicates that youth from non-white, rural, low-income and Spanish speaking families were less likely to access electronic patient portals¹⁰⁶.

Healthcare disparities among LGBTQ+ (lesbian, gay, bisexual, transgender, questioning and queer) youth in rheumatology needs further investigation. Adolescents reporting minoritized sexual orientation increased from 7.9% in 2009 to 14.3 in 2017¹⁰⁷. These youth are at increased risk for substance abuse, mental health disorders, and are 3 times more likely to attempt suicide^{107, 108}. Hence, this is an area that should be included in research into disparities in pediatric rheumatology and sexual orientation and gender identity should be addressed in clinical encounters with adolescents in the pediatric rheumatology clinic.

Summary

Critical health and healthcare disparities related to race/ethnicity, SES, and geography have been identified in the most prevalent pediatric rheumatic diseases. However, significant gaps in knowledge exist regarding health disparities associated with rarer pediatric rheumatologic diseases and within highly underrepresented demographics. Of particular note, is the lack of literature investigating health disparities (or even health outcomes) in Native American/First Nations youth with rheumatic disease. This group is almost entirely absent from research in pediatric rheumatology. Alarmingly, this is a population is subject to some of the worst health disparities in general health and common chronic diseases¹⁰⁹ and with particularly high prevalence of pediatric rheumatic disease with high morbidity and disability, such as SLE and polyarticular JIA^{10, 11}.

Important health disparities in Black Americans have been identified and widely recognized over the past several decades in the general U.S. population, resultant from centuries of systemic and systematic racism. Hence, it is no surprise that the most evident health disparities in pediatric rheumatology are in Black youth. In SLE, which is arguably the most studied disease in pediatric rheumatology with regards to health disparities, disparities in mortality—the most critical and most basic indicator of health—have not only persisted in the U.S. but have worsened over time. Currently in the US, SLE ranks 5th in causes of death for Black and Hispanic 10–25-year-old females⁹. Similarly, Black youth and low SES youth with SLE, JIA, and other rheumatologic disease are more likely to experience greater disease activity and increased morbidity into adulthood.

This highlights the urgent need to address and mitigate health and healthcare disparities within pediatric rheumatology at the familial, individual treatment, institutional, and societal levels. Identification of health disparities is not enough. Very little research in pediatric rheumatology has tackled interventions to promote health equity and close gaps in health disparities. The few studies that have investigated strategies to implement more standardized treatment and examined their impact on health disparities have had limited success in mitigating gaps in health care disparities, let alone gaps in health outcomes. Interventions that specifically target and uplift the care of vulnerable populations may be needed to attain health equity, rather than focusing on provision of equal care. Strategies that address health and healthcare disparities on different levels—including practice level changes, improving trainee education to address implicit bias, implementing equitable representation in pediatric rheumatology literature and research, and passing equity-focused healthcare policy—are crucial to ensuring optimal health and well-being among youth with rheumatic diseases.

Key Points:

• Health disparities in pediatric rheumatic diseases are prevalent across racial/ethnic groups, socioeconomic groups and geographic areas.

• While health disparities in youth with SLE and JIA have been identified, significant gaps in knowledge on disparities in other childhood rheumatologic diseases exist.

• Standardizing care is a strategy to decrease disparities but improved understanding of healthcare disparities in this population is necessary to develop appropriate interventions to decrease healthcare inequity in pediatric rheumatology.

Synopsis.

Health and healthcare disparities in pediatric rheumatology are prevalent across racial/ethnic groups, socioeconomic groups, and geographic areas from a socially disadvantaged backgrounds affecting, access to care, disease severity, morbidity, mortality, quality of life and mental health. There is literature on JIA and SLE with significant gaps in studies looking at health and healthcare disparities of other pediatric rheumatic diseases. Understanding of why healthcare disparities exist will ultimately inform the innovation and implementation of policies and interventions on a federal, local, and individual levels.