Barriers to Care among Patients with Sarcoidosis: A Qualitative Study

Abstract

Rationale: Lower-income patients with sarcoidosis experience worse outcomes than those with higher incomes. The reasons for these disparities are not well understood.

Objectives: To identify patient-reported barriers to and facilitators of self-empowered care among patients with sarcoidosis residing in high- and low-median-income zip-code areas.

Methods: Patients with biopsy-proven sarcoidosis who had received pharmacologic treatment within the past year and who were cared for in a sarcoidosis clinic of a large, urban medical system were included. Focus groups were stratified by high- and low-median-income zip-code areas. Transcriptions were analyzed using grounded theory.

Results: Five focus groups were created; two included patients living in zip-code areas with high median incomes ($84,263; interquartile range [IQR], $79,334–$89,795), and three included patients living in zip-code areas with low median incomes ($27,470; IQR, $22,412–27,597). Patients with sarcoidosis from low-income and high-income zip-code areas reported remarkably similar experiences. Patients reported that sarcoidosis was a burden owing to its disease manifestations and the adverse effects of treatment, which led to a compromised ability to perform their activities of daily living at home or at work. Reported barriers to care included perceived inadequate knowledge about sarcoidosis among providers, communication barriers with providers, and the high cost of treatment. Patients from low-income zip-code areas experienced discrimination related to race and income, which served to compound their mistrust. Patients sought to overcome these barriers through self-empowerment, including independent learning, self-advocacy, medication nonadherence, and use of alternative therapies.

Conclusions: Patients with sarcoidosis who lived in high- and low-income zip-code areas expressed similar overall concerns regarding sarcoidosis care. However, patients from low-income zip-code areas more frequently expressed concerns about racial and income-based discrimination. Patients from both groups addressed these barriers through self-empowerment, which included not adhering to prescribed therapies. Future work should focus on the effects of culturally and socioeconomically congruent, community-engaged interventions for quality of life of patients with sarcoidosis.

Sarcoidosis is an inflammatory disorder of unknown cause that can affect any organ system (1). The clinical course is highly variable, with some patients experiencing minimal effects and others progressing to end-stage organ failure and death (1). Sarcoidosis can be devastating for minority and low-income patients. For example, Black individuals are approximately three times as likely as White individuals to have sarcoidosis diagnosed (2) and are almost 10 times as likely to die of sarcoidosis (3). In addition, patients of lower socioeconomic status have more severe disease at presentation (4), have greater progression of pulmonary disease (5), are more likely to develop comorbidities after a diagnosis of sarcoidosis (6), and have worse quality of life (6). At present, the reason for these disparate outcomes is unclear.

Given what is known regarding health disparities in other diseases, it is reasonable to assume that observed disparities in sarcoidosis are not due simply to biological differences by race and income but to a complex web of social and environmental factors that serve as barriers to care (7). This hypothesis is supported by past work showing a strong relationship between zip-code markers of socioeconomic status and patient outcomes across a range of diseases (8–10). To understand how these factors could be affecting patients with sarcoidosis, we employed a community-based participatory research approach. This methodology seeks to recognize the community as a unit of identity, build on the strengths of the community, and facilitate collaborative partnerships with the community at all phases of research (11). We met with patients with sarcoidosis whose stories informed us that their needs differed by socioeconomic status but that the approach to their management was often the same. We hypothesized that building focus groups of patients from high- and low-income zip-code areas would allow us to identify unique barriers to care on the basis of socioeconomic status and to identify the strategies that they employed to overcome these barriers.

Methods

Participants

This qualitative study was conducted between October 2019 and January 2020. All patients were receiving care at the sarcoidosis clinic of a large, urban health system in Cleveland, Ohio. Individuals were classified as having “highly probable” or “at least probable” sarcoidosis on the basis of the 2014 World Association of Sarcoidosis and Other Granulomatous Diseases organ assessment tool (12) and had received a systemic antisarcoidosis medication within the prior year prescribed by a sarcoidosis specialist. We focused on patients who received pharmacologic treatment to ensure that our sample contained those whose disease severity was significant enough for them to have had substantial interactions with the medical system. Focus groups were stratified by the median income of the patients’ zip-code areas as determined by the U.S. census (13). We did not inquire about individuals’ incomes before conducting the focus-group sessions to avoid offending eligible individuals and consequently suppressing recruitment. We included patients living in zip-code areas with the highest median income within 25 miles of our center as well as the zip-code areas with the lowest median income within 10 miles of our center to limit transportation barriers. We identified 522 patients who had received a diagnosis of sarcoidosis and resided in our target zip-code areas (301 from high-income zip-code areas and 221 from low-income zip-code areas). Of these, 223 patients were receiving immunosuppressive therapy (123 from high-income zip-code areas and 100 from low-income zip-code areas). Upon closer chart review, we excluded patients who had not undergone a biopsy for diagnosis and those who were prescribed immunosuppressive therapy for conditions other than sarcoidosis (56 from high-income zip-code areas and 23 from low-income zip-code areas). We mailed letters explaining the study and offering the opportunity to opt out to the remaining 67 patients from high-income zip-code areas and 77 patients from low-income zip-code areas who met study criteria. No one opted out, and all patients were called to discuss the study further and complete enrollment. Twenty-two patients from high-income zip-code areas and 31 patients from low-income zip-code areas agreed over the phone to participate. Of these, 10 from high-income zip-code areas and 20 from low-income zip-code areas attended the scheduled focus-group sessions. Patients were compensated $75 for participating.

Setting

The focus-group sessions were held in the community at locations near patients’ neighborhoods to provide a familiar location to put patients at ease. Community partners were compensated for use of their facility.

Questionnaire

Before the focus-group sessions, patients completed an anonymous questionnaire that asked them to identify their sex, race, ethnicity, current income, which of their organs was/were affected by sarcoidosis, and which sarcoidosis-specific medications they had ever used.

Procedures

An interview guide containing open-ended questions was developed with input from a patient with sarcoidosis, qualitative methodologists, and clinicians who regularly care for patients with sarcoidosis (see the online supplement). The groups were moderated by a male pulmonologist with expertise in sarcoidosis (L.J.H.) and a female social worker with sarcoidosis (G.L.). Notes were taken by a female trained research observer (R.S.) during each focus-group session and were incorporated into the analysis. All members of the study team underwent training in qualitative methodology, which included focus-group moderation and data analysis. Sessions were recorded and transcribed verbatim by a professional focus-group session transcriber. Groups were scheduled for 2 hours, with the first half hour set aside for the participants to eat a meal and get to know each other. We held two groups with respondents from exclusively high-income zip-code areas (5 respondents/group) and three groups with respondents from exclusively low-income zip-code areas (one group of 10 respondents and two groups of 5 respondents each).

We analyzed the transcripts with grounded theory (14, 15) analysis using the constant comparison method in conjunction with theoretical sampling. The analysis began with each member of the study team (L.J.H., G.L., R.S., and J.D.T.) independently reviewing transcripts from the first two groups to immerse themselves in the data. After an overview of the breadth, context, and relationship among study data was developed, each transcript was reread in more detail, with codes assigned to key concepts that illustrated the emerging framework of sarcoidosis care. The team met, discussed, and refined the codes and jointly created a finalized coding structure. Team members independently applied the finalized coding structure to all transcripts after each focus-group session. Any additional codes that emerged were discussed and added to the existing coding structure or merged with existing codes. Focus-group sessions were held until thematic saturation was achieved and no new codes surfaced. The Cleveland Clinic Institutional Review Board approved this study (institutional review board [IRB] 19-804).

Results

We conducted five focus-group sessions comprising 30 adults (Table 1). Of the 26 participants who completed the preinterview survey, 17 (65%) were Black and 8 (35%) were non-Hispanic White. Self-reported income ranged from less than $25,000 per year in 8 (31%) patients to more than $100,000 per year in 4 (15%) patients. Patients residing in low-income zip-code areas reported lower yearly household incomes (3 of 16 reporting income >$50,000) than patients residing in high-income zip-code areas (7 of 10 reporting income >$50,000) (Table 1). Participants from high-income zip-code areas were predominantly White (8 [80%]), whereas participants from low-income zip-code areas were predominantly Black (15 [94%]). Patients recruited from low-income zip-code areas came from zip-code areas with lower median household incomes ($27,470 [interquartile range (IQR), $22,412–$27,597] vs. $84,263 [IQR, $79,334–$89,795]), lower median owner-occupied house prices ($54,700 [IQR, $49,500–$58,002] vs. $218,750 [IQR, $202,500–$269,600]), higher rates of poverty (35% [IQR, 34%–38%] vs. 5% [IQR, 4%–6%]), and higher proportions of Black residents (89% [IQR, 74%–90%] vs. 4% [IQR, 3%–10%]) (see Table E1 in the online supplement). The overall study population had significant disease burden, with 18 (69%) reporting extrapulmonary manifestations, 22 (85%) reporting prior steroid use, and 20 (77%) reporting treatment with a steroid-sparing medication (Table 1).

Table 1.

Self-reported participant demographics and disease characteristics

	High Income (n = 10)	Low Income (n = 16)*
Salary
>$100,000	2	2
$50,000–100,100	5	1
$25,000–50,000	2	4
<$25,000	1	7
Refused to respond	0	2
Race
White	8	0
Black	2	15
Refused to respond	0	1
Organ involvement
Pulmonary	9	14
Extrapulmonary	6	12
Ocular	2	7
Cutaneous	1	6
Neurologic	2	3
Cardiac	1	6
Other	2	0
Medication use
Steroid	8	14
Steroid-sparing	7	13
Methotrexate	5	12
Hydroxychloroquine	3	1
Leflunomide	2	1
Azathioprine	0	1
Infliximab	1	4
Adalimumab	0	1
Repository corticotropin	1	0

^*Four patients in the low-income zip-code groups refused to complete the survey. A total of 20 patients from low-income zip-code areas participated in the focus-group sessions.

Three major themes emerged from the focus-group sessions: 1) the burden of sarcoidosis (Table 2), 2) barriers to sarcoidosis care (Table 3), and 3) self-empowerment to overcome the barriers to care (Table 4). Overall, we discovered remarkably similar experiences regardless of participants’ median zip-code area income. Each of these themes and their subthemes are described subsequently with illustrative quotations from the focus groups.

Table 2.

Burden of sarcoidosis: subthemes and representative quotes

Subtheme by Zip-Code Income	Illustrative Quote
Traumatic diagnosis
High	“Initially I was diagnosed with severe bronchitis . . . My doctor . . . goes ‘Well, it’s just being stubborn’ . . . I said ‘Is this common sense? Something is not right’” (group 1, participant 4).
Low	“I kept going to the emergency room and they kept sending me home” (group 4, participant 4).
Impact of organ dysfunction
High	“I have developed severe small-fiber neuropathy, which has resulted in literally head-to-toe pain, constantly, and that’s why I’m in a wheelchair now 24/7, and have been for nine and a half years” (group 1, participant 2).
Low	“I lost my sight from it you know . . . It started hitting my lungs about four or five years ago, and then I started getting heart problems. I’d never been sick in my life . . .” (group 3, participant 2).
Non–organ-related symptoms
High	“I’m just tired . . . Why am I always tired? I think it’s important to talk to people. You guys are all tired, so maybe its normal” (group 2, participant 2).
Low	“I mean, I’m pretty sure all of us have some kind of depression <several agree>” (group 3, participant 7).
Adverse effects of treatment
High	“Prednisone [is] the Devil’s candy. Just the side effects with the skin and nails . . . I never ate like that” (group 2, participant 1).
Low	“They keep telling me to wait a little bit longer, to try to give it time for the methotrexate to work . . . trading it off from one thing to have the symptoms of being sick to your stomach and everything else” (group 5, participant 5).
Compromised roles
High	“I wasn’t able to work, just to be able to cope with not working and the loss of your friends at work and your income, essentially your whole life” (group 2, participant 3).
Low	“I feel like I’ve become a burden on my kids” (group 3, participant 4).

Similar causes of morbidity from sarcoidosis were seen between patients from high-income zip-code areas and patients from low-income zip-code areas.

Table 3.

Barriers to care: subthemes and representative quotes

Subtheme by Zip-Code Income	Illustrative Quote
Provider knowledge gaps
High	“I ended up with fifteen doctors . . . and only one of them knew anything about sarcoidosis” (group 2, participant 3).
Low	“Medical doctors should know something about sarcoidosis so when a patient do come into their office, ‘I got this terrible cough,’ because a lot of doctors, in my own experience, they never heard of sarcoidosis” (group 4, participant 1).
Poor patient–provider communication
High	“You can be taking medication that ‘Hey, you know this doesn’t really work for me’ and no one’s listening to you” (group 2, participant 4).
Low	“I think the appointment were more depressing for me cause you gotta keep going to the doctor and don’t nobody got an answer and it’s just ‘take this medicine’” (group 4, participant 4).
Cost of care
High	“That [medication] had to be approved [by the insurer] and so that added another six weeks or so [to waiting for symptom relief]. I was feeling pretty bad because I had been that long without that medication that was helping [my symptoms]” (group 1, participant 3).
Low	“I’m [paying] $1,738 a month for my prescriptions” (group 5, participant 2).
Mistrust: quality of care
High	“He [the doctor] answered a lot of my questions, but . . . I had a knot in my stomach when I left his office because . . . he wanted me on like all kind of steroids and I’ve never been on a steroid” (group 1, participant 3).
Low	“I was on those pills. The doctor never even consulted me about them, and the next thing I know, I’m getting all these hip pains” (group 4, participant 5).
Mistrust: income-based discrimination
Low	“I don’t think I get the same as someone that can afford it” (group 4, participant 3).
Low	“Don’t nobody care about me, but me . . . if you never had to go to the doctor, they don’t make any money off of you . . . I don’t want them to get rich off of me” (group 5, participant 2).
Mistrust: racial incongruity
Low	“My doctors are Caucasian, so I can’t talk to them the way I want to talk to them . . . it’s just like they’re just there” (group 3 [low income], participant 1).
Low	“I’ve had bad experiences with some doctors. I don’t know if it was racial, but they treated me different when I did ask them questions, like ‘who are you?’” (group 5, participant 5).

Mistrust related to income-based discrimination and racial incongruity were unique barriers for patients from low-income zip-code areas.

Table 4.

Self-empowerment: subthemes and representative quotes

Subtheme by Zip-Code Income	Illustrative Quote
Knowledge acquisition
High	“I’m online on a support group . . . It’s very supportive and informational” (group 1, participant 3).
Low	“I had one of my church members look sarcoidosis up, and I kind of read through it and it was telling me everything I was going through” (group 5, participant 1).
Self-advocacy
High	“Basically, I’m the one with all the information, and so as soon as I walk in ‘Okay, this and this and this has been happening, and this is what I’m taking’” (group 1, participant 1).
Low	“I’m always up on them doctors’ faces . . . When I was an inpatient taught me to take an interest in my own health” (group 4, participant 3).
Medication nonadherence
High	“I even try to be my own doctor. Like I’ll just stop a med and he’ll [the doctor] be like ‘Why did you do that?’ . . . because I read up a lot. So, if I get to seeing side effects or stuff that don’t sit right with me. That kind of scare me” (group 2, participant 5).
Low	“So I feel that it [methotrexate] should’ve been reduced but they [doctors] all said ‘No stay on it.’ . . . I’ve been concerned for at least the last six months . . . I was thinking about maybe I should just reduce myself” (group 4, participant 2).
Initiating alternative therapies
High	“Aquatherapy has also helped me a lot” (group 1, participant 2).
Low	“I stopped eating red meat and I started working out . . . so then I started feeling a little better, and I said ‘Forget this prednisone’ ” (group 5, participant 3).
Mindfulness and spirituality
High	“I think, for me, it’s been about trying to empower myself . . . I meditate to help control really a lot of the ups and downs with anxiety” (group 1, participant 4).
Low	“I believe in the power of prayer, waking up and meditating for a few minutes and just clearing my head” (group 3, participant 8).

Similar self-empowerment strategies were seen between patients from high-income zip-code areas and patients from low-income zip-code areas.

Burden of Sarcoidosis

Patients shared the challenges of having sarcoidosis, which ranged from the initial impediments associated with obtaining a diagnosis to the significant morbidity of the disease and from this significant morbidity to the adverse effects associated with treatment. Participants identified depression and fatigue as persistent, severe, and significant drivers of their impaired quality of life. Our respondents expressed the burden of their disease by how compromised they were in their ability to complete activities of daily living both at home and at work.

Many patients described a traumatic diagnosis as their initial experience with sarcoidosis. Participants reported suffering with a prolonged period of unexplained symptoms. The challenges of their symptoms were compounded by a perceived lack of motivation from their doctors to identify the underlying cause. This led to a damaged patient–provider relationship and mistrust before the diagnosis of sarcoidosis had been made.

In this cohort of patients who underwent treatment for sarcoidosis, there was significant morbidity. Notable related conditions included pulmonary fibrosis, heart failure, and neurologic complications. Patients in all groups reported the non–organ-related symptoms of depression and fatigue. Many were not aware that these symptoms could be related to sarcoidosis and expressed some relief at learning that others with the disease were experiencing these symptoms as well.

Patients reported frequent and debilitating adverse effects from the medications used to treat their sarcoidosis. Although most comments were related to corticosteroids, patients also mentioned adverse effects of receiving steroid-sparing medications.

Patients conveyed the severity of sarcoidosis in ways that differed from those of their physicians. Patients defined the severity of their sarcoidosis by how it compromised their ability to perform their daily roles of living at home and at work, not by severity of organ involvement. Limitations in their activities were often attributed to fatigue and depression rather than to end-organ dysfunction.

Barriers to Care

In addition to having a chronic disease with severe manifestations, patients in each of the groups reported difficulties in obtaining high-quality care because of the difficulty of finding knowledgeable providers, poor communication with their healthcare team, and the high costs of care. These barriers led to significant mistrust. All groups reported mistrust related to not believing they were heard by their providers. Patients in low-income zip-code groups reported additional mistrust related to feeling discriminated against owing to lack of ability to pay and race.

In all of our groups, participants shared stories of healthcare practitioners who were unfamiliar with sarcoidosis. Patients believed that these provider knowledge gaps led to inappropriate treatments and delays in care. Even when they were able to find a provider who was informed regarding sarcoidosis, patients reported that they struggled with poor patient–provider communication. This led to patients feeling that their doctor was simply prescribing medication without making the effort to address their individual concerns. Mistrust in the healthcare system was solidified by the high cost of care (a notable barrier mentioned in all groups), regardless of median zip-code area income.

These barriers to care resulted in significant mistrust of the medical system by the respondents. Across all groups, there was significant skepticism that the quality of care that patients were receiving was optimal. Patients did not believe that they could trust their care team to tell them all of their options or to fully educate them on the potential side effects of treatment. In our groups from low-income zip-code areas, there was an additional layer of mistrust related to differences in socioeconomic status between provider and patient. Respondents reported fears that they were being discriminated against because of having a low income. In addition, racial incongruity between patients and providers led to mistrust through communication difficulties and perceived racism. In our interviews, mistrust emerged as the final, common pathway among barriers related to communication, lack of knowledge, and high costs.

Self-Empowerment

Patients from all zip-code areas sought to empower themselves to take control of their own care and combat disability from sarcoidosis, the toxic effects of treatment, and mistrust stemming from challenges in accessing care. The key first step identified by all groups was knowledge acquisition. Patients sought outside information from the Internet, support groups, and local church groups. Armed with this knowledge, patients felt confident in using self-advocacy to improve their care. When disagreements between patients and providers could not be resolved, patients used medication nonadherence to take control of their care. Notably, there was no mention of nonadherence owing to lack of understanding of the prescribed treatment regimen in any of our groups. Instead, nonadherence was viewed as a means of avoiding side effects or improving poor health. In addition, many respondents initiated alternative therapies to improve their health, with reported improved outcomes from dietary modifications, exercise, and physical therapy. Throughout this whole process, respondents sought to care for their mental and spiritual well-being through self-directed mindfulness, meditation, and participation in their local communities of faith.

Discussion

This is, to our knowledge, the first study to systematically gather patients’ opinions and feedback regarding sarcoidosis care. In this focus-group study of patients’ perceptions regarding care of their sarcoidosis, we found several barriers to optimal care and identified several approaches that patients use to overcome those barriers. Study patients reported significant morbidity from symptoms of fatigue and depression, the common occurrence of adverse effects from prescribed medications, challenges with accessing high-quality care, and a need to self-advocate to improve their care. This study provides important insights into what mediates these perceptions, as well as solutions that would potentially benefit all patients with sarcoidosis.

To our surprise, we found a largely shared experience across patients with sarcoidosis, regardless of socioeconomic status. This suggests that the barriers to sarcoidosis care are systemic and deeply rooted. For example, patients in all five of our groups identified the high costs of care as a significant hurdle. Although this has been demonstrated in other studies (6, 16), the frequency with which this issue was raised highlights how substantial a problem it is for all patients. In fact, many patients expressed that cost frequently dictated which treatments they decided to pursue. Future studies should investigate the relationship between costs and treatment decisions and subsequent outcomes.

In line with past reports (17), patients frequently reported a conscious decision to not adhere to therapies offered by their providers. Interestingly, nonadherence was most often used as a means to improve overall health, avoid therapies that appeared to offer no benefit, and improve quality of life by reducing treatment-related adverse effects. Patients reported frequently not including their providers in this decision-making process because they believed that their providers were not listening to them or sufficiently prioritizing their needs.

The primary difference that we noted between the high- and low-income zip-code groups was an increased perception of discrimination among those in the low-income groups. Participants from low-income zip-code areas were predominantly Black, making it difficult to determine whether the concerns that were expressed were associated with race, socioeconomic status, or both. However, there is a burgeoning body of literature exploring the high prevalence of discrimination felt by minority patients during interactions with healthcare systems (18, 19). Participants from low-income zip-code areas also referred to a lack of racial congruence with members of their treatment team as a barrier to communication. Such challenges with communication have been demonstrated among patients with other diseases and have been associated with reduced treatment adherence and provider trust (20). In this study, we found that patients countered this lack of support by reaching out to members of their own community, especially their faith community. Diversifying the pool of providers who care for patients with sarcoidosis would likely have a substantial impact on patient outcomes (21). Interventions aimed at bridging cultural gaps, such as patient advocates (22), peer mentoring (23), or patient support groups (24), may also have a role in improving communication and reducing mistrust among affected patients.

Patients were disappointed by a lack of recommendations regarding alternative therapies to manage their sarcoidosis. Patients reported symptoms such as fatigue and depression that were not recognized by their providers. In addition, providers offered little assistance in dealing with the adverse effects of medications. This, coupled with the perceived reliance on pharmacologic therapy by their treatment team, led to patients concluding that providers were prescribing medications for financial gain. This, in turn, led to greater patient mistrust of providers. Patients in all groups expressed an interest in learning about nutritional alternatives, complementary medicine, and behavioral interventions. Given the noted toxicity of prednisone (25) and its limited efficacy in treating sarcoidosis (26), this study suggests that further research in nonpharmacologic therapies would be of great interest to our patients and may improve patient–provider relationships. These results also suggest that a multidisciplinary approach to delivering high-quality sarcoidosis care is needed, as has been used in other respiratory diseases such as cystic fibrosis (27) and interstitial lung diseases (28).

Strengths and Limitations

Our study has limitations. Our focus groups were not stratified by self-reported income. However, we recruited from zip-code areas with widely divergent socioeconomic demographics and demonstrated a difference in self-reported race and income among our groups. Patients from high-income zip-code areas were predominantly White, and participants from low-income zip-code areas were predominantly Black, which made it difficult for us to determine whether race, socioeconomic status, or both were factors influencing patient responses. However, the fact that patients from all zip-code areas reported similar challenges suggests that the needs of most patients with sarcoidosis are not being met. This was a single-center study, and our results may not be generalizable to care delivered to patients with sarcoidosis elsewhere. Patients in this study received their care at a specialized sarcoidosis center in a large, academic healthcare system. This highlights that, even with state-of-the-art sarcoidosis management, the needs of minority and low-income populations are not being fully met. In addition, we chose to only recruit individuals who had required treatment for sarcoidosis in the past. Up to 50% of patients have mild manifestations of disease and do not require any therapy (1). We made the decision to focus our efforts on the patients who likely have the most contact with the healthcare system, but our results may not be representative of the population with milder symptoms or those who refuse pharmacologic therapy. Finally, the individuals we recruited may have been more actively engaged in their care or may have had more extreme opinions than the general population with sarcoidosis. The feedback provided by these groups necessitates further study to determine the prevalence of their concerns.

Conclusions

Our results have implications for caregivers and administrators who wish to improve the quality of sarcoidosis care. Engaging and partnering with patients may lead to the development of interventions that improve communication and foster trust. This, in turn, may lead to improvements in patient quality of life while decreasing sarcoidosis-related complications and healthcare use.