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Racial Differences in Perceptions of Psoriasis Therapies: Implications for Racial Disparities in Psoriasis Treatment

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

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

    Center for Clinical Epidemiology and Biostatistics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
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  • Whitney T. Eriksen
    Affiliations
    Department of Family Medicine and Community Health, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
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  • Valerie T. Raziano
    Affiliations
    Department of Dermatology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
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  • Claire Bocage
    Affiliations
    Department of Family Medicine and Community Health, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
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  • Lynn Hur
    Affiliations
    Department of Family Medicine and Community Health, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
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  • Ruchi V. Shah
    Affiliations
    Rowan University School of Osteopathic Medicine, Stratford, New Jersey, USA
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  • Joel M. Gelfand
    Affiliations
    Department of Dermatology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA

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

    Center for Clinical Epidemiology and Biostatistics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
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  • Frances K. Barg
    Affiliations
    Department of Biostatistics, Epidemiology and Informatics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Center for Clinical Epidemiology and Biostatistics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA

    Department of Family Medicine and Community Health, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
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Open ArchivePublished:February 06, 2019DOI:https://doi.org/10.1016/j.jid.2018.12.032
      In the United States, black patients are less likely than white patients to receive biologic treatment for their psoriasis. We conducted a qualitative free-listing study to identify patient-generated factors that may explain this apparent racial disparity in psoriasis treatment by comparing the perceptions of biologics and other psoriasis therapies between white and black adults with psoriasis. Participants included 68 white and black adults with moderate to severe psoriasis who had and had not received biologic treatment. Each participant was asked to list words in response to verbal probes querying five psoriasis treatments: self-injectable biologics, infliximab, methotrexate, apremilast, and phototherapy. Salience scores indicating the relative importance of each word were calculated, and salient words were compared across each race/treatment group. Participants who had experience with biologics generally associated positive words with self-injectable biologics. Among biologic-naïve participants, “apprehension,” “side effects,” and “immune suppression” were most salient. “Unfamiliar” and “dislike needles” were salient only among black participants who were biologic naïve. Participants were generally unfamiliar with the other psoriasis therapies except phototherapy. Unfamiliarity with biologics, particularly among black, biologic-naïve patients, may partly explain the existing racial disparity in biologic treatment for psoriasis and might stem from lack of exposure to or poor understanding of biologics.

      Introduction

      Psoriasis is a chronic systemic inflammatory disease, primarily of the skin, that affects approximately 7.5 million Americans (
      National Psoriasis Foundation
      Statistics.
      ). Moderate to severe psoriasis, in particular, has major negative effects on the physical and psychosocial well-being of those affected (
      • Rapp S.R.
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      • Exum M.L.
      • Fleischer Jr., A.B.
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      Psoriasis causes as much disability as other major medical diseases.
      ) and is associated with cardiometabolic (
      • Azfar R.S.
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      • Shin D.B.
      • Troxel A.B.
      • Margolis D.J.
      • Gelfand J.M.
      Increased risk of diabetes mellitus and likelihood of receiving diabetes mellitus treatment in patients with psoriasis.
      ,
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      • Neimann A.L.
      • Shin D.B.
      • Wang X.
      • Margolis D.J.
      • Troxel A.B.
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      ,
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      • Dommasch E.D.
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      • Azfar R.S.
      • Kurd S.K.
      • Wang X.
      • et al.
      The risk of stroke in patients with psoriasis.
      ,
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      • Shin D.B.
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      • Kimmel S.E.
      • Mehta N.N.
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      Prevalence of metabolic syndrome in patients with psoriasis: a population-based study in the United Kingdom.
      ,
      • Mehta N.N.
      • Azfar R.S.
      • Shin D.B.
      • Neimann A.L.
      • Troxel A.B.
      • Gelfand J.M.
      Patients with severe psoriasis are at increased risk of cardiovascular mortality: cohort study using the General Practice Research Database.
      ,
      • Wan M.T.
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      • Hubbard R.A.
      • Noe M.H.
      • Mehta N.N.
      • Gelfand J.M.
      Psoriasis and the risk of diabetes: a prospective population-based cohort study.
      ) and other comorbid diseases (
      • Chiesa Fuxench Z.C.
      • Shin D.B.
      • Ogdie Beatty A.
      • Gelfand J.M.
      The risk of cancer in patients with psoriasis: a population-based cohort study in the Health Improvement Network.
      ,
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      • Denburg M.R.
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      • Gelfand J.M.
      The risk of IgA nephropathy and glomerular disease in patients with psoriasis: a population-based cohort study.
      ,
      • Kurd S.K.
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      • Crits-Christoph P.
      • Gelfand J.M.
      The risk of depression, anxiety, and suicidality in patients with psoriasis: a population-based cohort study.
      ,
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      • Chiesa Fuxench Z.C.
      • et al.
      Risk of incident liver disease in patients with psoriasis, psoriatic arthritis, and rheumatoid arthritis: a population-based study.
      ,
      • Takeshita J.
      • Shin D.B.
      • Ogdie A.
      • Gelfand J.M.
      Risk of serious infection, opportunistic infection, and herpes zoster among patients with psoriasis in the United Kingdom.
      ,
      • Wan J.
      • Wang S.
      • Haynes K.
      • Denburg M.R.
      • Shin D.B.
      • Gelfand J.M.
      Risk of moderate to advanced kidney disease in patients with psoriasis: population based cohort study.
      ,
      • Yeung H.
      • Takeshita J.
      • Mehta N.N.
      • Kimmel S.E.
      • Ogdie A.
      • Margoli D.J.
      • et al.
      Psoriasis severity and the prevalence of major medical comorbidity: a population-based study.
      ) that may be modulated by psoriasis treatment (
      • Ahlehoff O.
      • Skov L.
      • Gislason G.
      • Gniadecki R.
      • Iversen L.
      • Bryld L.E.
      • et al.
      Cardiovascular outcomes and systemic anti-inflammatory drugs in patients with severe psoriasis: 5-year follow-up of a Danish nationwide cohort.
      ,
      • Bissonnette R.
      • Harel F.
      • Krueger J.G.
      • Guertin M.C.
      • Chabot-Blanchet M.
      • Gonzalez J.
      • et al.
      TNF-α antagonist and vascular inflammation in patients with psoriasis vulgaris: a randomized placebo-controlled study.
      ,
      • Bissonnette R.
      • Kerdel F.
      • Naldi L.
      • Papp K.
      • Galindo C.
      • Langholff W.
      • et al.
      Evaluation of risk of major adverse cardiovascular events with biologic therapy in patients with psoriasis.
      ,
      • Mehta N.N.
      • Shin D.B.
      • Joshi A.A.
      • Dey A.K.
      • Armstrong A.W.
      • Duffin K.C.
      • et al.
      Effect of 2 psoriasis treatments on vascular inflammation and novel inflammatory cardiovascular biomarkers: a randomized placebo-controlled trial.
      ,
      • Wu J.J.
      • Guerin A.
      • Sundaram M.
      • Dea K.
      • Cloutier M.
      • Mulani P.
      Cardiovascular event risk assessment in psoriasis patients treated with tumor necrosis factor-α inhibitors versus methotrexate.
      ,
      • Wu J.J.
      • Joshi A.A.
      • Reddy S.P.
      • Batech M.
      • Egeberg A.
      • Ahlehoff O.
      • et al.
      Anti-inflammatory therapy with tumour necrosis factor inhibitors is associated with reduced risk of major adverse cardiovascular events in psoriasis.
      ,
      • Wu J.J.
      • Sundaram M.
      • Cloutier M.
      • Gauthier-Loiselle M.
      • Guerin A.
      • Singh R.
      • et al.
      The risk of cardiovascular events in psoriasis patients treated with tumor necrosis factor-α inhibitors versus phototherapy: an observational cohort study.
      ,
      • Yang Z.S.
      • Lin N.N.
      • Li L.
      • Li Y.
      The effect of TNF inhibitors on cardiovascular events in psoriasis and psoriatic arthritis: an updated meta-analysis.
      ). Psoriasis is also associated with a large economic burden of up to $135 billion in total costs (in 2013 dollars), of which up to $35.4 billion is attributed to indirect costs that are largely due to lost work productivity (
      • Brezinski E.A.
      • Dhillon J.S.
      • Armstrong A.W.
      Economic burden of psoriasis in the United States: a systematic review.
      ). Therefore, it is important on both individual and societal levels that patients with psoriasis receive adequate and effective treatment.
      Despite a growing number of increasingly efficacious therapeutic options (primarily biologics) for treating moderate to severe psoriasis, most patients remain undertreated with only topical medications or no treatment at all (
      • Lebwohl M.G.
      • Bachelez H.
      • Barker J.
      • Girolomoni G.
      • Kavanaugh A.
      • Langley R.G.
      • et al.
      Patient perspectives in the management of psoriasis: results from the population-based Multinational Assessment of Psoriasis and Psoriatic Arthritis Survey.
      ). Considering that, in the United States, psoriasis may be more severe (
      • Gelfand J.M.
      • Stern R.S.
      • Nijsten T.
      • Feldman S.R.
      • Thomas J.
      • Kist J.
      • et al.
      The prevalence of psoriasis in African Americans: results from a population-based study.
      ) and have a greater negative impact on quality of life (
      • Shah S.K.
      • Arthur A.
      • Yang Y.C.
      • Stevens S.
      • Alexis A.F.
      A retrospective study to investigate racial and ethnic variations in the treatment of psoriasis with etanercept.
      ) among racial/ethnic minority patients than white patients, undertreatment may disproportionately affect minority and other marginalized or disadvantaged individuals with psoriasis. For example, among Medicare recipients, black beneficiaries with moderate to severe psoriasis are 70% less likely to receive biologic treatment for their psoriasis than white beneficiaries, independent of other demographic and socioeconomic factors, comorbidities, and differences in Medicare plans (
      • Takeshita J.
      • Gelfand J.M.
      • Li P.
      • Pinto L.
      • Yu X.
      • Rao P.
      • et al.
      Psoriasis in the US Medicare population: prevalence, treatment, and factors associated with biologic use.
      ). A clinic-based study of patients with psoriasis in the United States also found similar racial differences in psoriasis treatment with biologics (
      • Kerr G.S.
      • Qaiyumi S.
      • Richards J.
      • Vahabzadeh-Monshie H.
      • Kindred C.
      • Whelton S.
      • et al.
      Psoriasis and psoriatic arthritis in African-American patients—the need to measure disease burden.
      ). As biologic therapies increasingly become the mainstay of treatment for patients with more severe psoriasis, it is important to identify why black patients are less likely than white patients to receive highly efficacious biologics for their skin disease and rectify any existing treatment disparity. Thus, our study aimed to understand psoriasis patients’ perceptions of biologics and other common or new psoriasis treatments by leveraging qualitative research methods that are aimed at generating testable hypotheses for why a racial disparity in biologic treatment for psoriasis exists in the United States.

      Results

      Participants

      The sociodemographic and clinical characteristics of 68 participants with moderate to severe psoriasis according to race/treatment groups are summarized in Table 1. Median age ranged from 48 to 55 years and was similar across race/treatment groups. Participants were predominantly female (70.6% of all participants). Most participants resided in Northeastern US and were affiliated with the University of Pennsylvania Health System. Significantly more black participants were of lower income and education levels than white participants. Differences in primary medical insurance were also seen across race/treatment groups.
      Table 1Participant characteristics
      CharacteristicsWhite/Biologic (n = 19)White/No Biologic (n = 17)Black/Biologic (n = 16)Black/No Biologic (n = 16)P-Value
      Age in years, median (IQR)48 (35–66)50 (36–62)54 (46.5–62)55 (46.5–66.5)0.54
      Female, n (%)12 (63.2)11 (64.7)14 (87.5)11 (68.8)0.39
      Annual household income, n (%)0.005
       <$50,0006 (31.6)3 (17.6)10 (62.5)10 (62.5)
       ≥$50,00012 (63.2)12 (70.6)3 (18.7)3 (18.7)
       Prefer not to answer1 (5.2)2 (11.8)3 (18.7)3 (18.7)
      Education, n (%)<0.001
       Less than bachelor’s degree4 (21.0)3 (17.6)12 (75.0)11 (68.8)
       Bachelor’s degree or more15 (79.0)14 (82.4)4 (25.0)5 (31.2)
      Employment, n (%)0.14
       Unemployed/unable to work5 (26.3)0 (0)4 (25.0)2 (12.5)
       Part time2 (10.5)5 (29.4)1 (6.2)1 (6.2)
       Full time9 (47.4)9 (52.9)6 (37.5)7 (43.8)
       Retired1 (5.3)2 (11.8)5 (31.3)5 (31.3)
       Other2 (10.5)1 (5.9)0 (0)1 (6.2)
      Marital status, n (%)0.08
       Single6 (31.6)6 (35.3)5 (31.3)5 (31.3)
       Married/domestic partner11 (57.9)11 (64.7)6 (37.5)5 (31.3)
       Divorced/separated/widowed1 (5.3)0 (0)5 (31.3)5 (31.3)
       Other1 (5.3)0 (0)0 (0)0 (0)
       Prefer not to answer0 (0)0 (0)0 (0)1 (6.3)
      Residence in US Northeast, n (%)14 (73.7)10 (58.8)14 (87.5)15 (93.8)0.08
      Primary medical insurance, n (%)0.004
       Commercial8 (42.1)15 (88.2)9 (56.3)7 (43.8)
       Medicare/Medicaid9 (47.4)1 (5.9)7 (43.7)5 (31.3)
       Other0 (0)1 (5.9)0 (0)1 (6.2)
       None2 (10.5)0 (0)0 (0)0 (0)
       Prefer not to answer0 (0)0 (0)0 (0)3 (18.7)
      Abbreviation: IQR, interquartile range.
      Psoriasis history and characteristics, with the exception of treatment history, were similar across all race/treatment groups (Table 2). Compared with participants who had experience with biologics, biologic-naïve participants were more likely to be currently receiving phototherapy or topical therapy only and were less likely to have received oral systemic therapy in the past.
      Table 2Psoriasis history
      CharacteristicsWhite/Biologic (n = 19)White/No Biologic (n = 17)Black/Biologic (n = 16)Black/No Biologic (n = 16)P-Value
      Age in years at psoriasis onset, n (%)0.46
       <4016 (84.2)11 (64.7)11 (68.8)10 (62.5)
       ≥403 (15.8)6 (35.3)5 (31.2)6 (37.5)
      Psoriasis duration in years, median (IQR)21 (14–34)10 (7–22)8 (5.5–32.5)9 (2.25–25)0.83
      Current psoriasis severity, n (%)0.88
       None/very little5 (26.3)3 (17.7)3 (18.8)3 (18.8)
       Mild5 (26.3)3 (17.7)2 (12.5)3 (18.8)
       Moderate6 (31.6)8 (47.1)7 (43.8)4 (25.0)
       Severe3 (15.8)3 (17.7)4 (25.0)6 (37.5)
      Psoriatic arthritis, n (%)9 (47.4)4 (23.5)6 (37.5)3 (18.8)0.28
      Primary medical provider for psoriasis, n (%)0.53
       Dermatologist15 (79.0)16 (94.1)15 (93.8)15 (93.8)
       Rheumatologist3 (15.8)1 (5.9)1 (6.3)0 (0)
       Other1 (5.3)0 (0)0 (0)1 (6.2)
      Dermatology life quality index, median (IQR)7 (1–11)5 (2–9)9 (2.5–15.5)5.5 (2–13.5)0.62
      Current treatment, n (%)
       Phototherapy0 (0)8 (47.1)2 (12.5)8 (50.0)<0.001
       Oral systemic1 (5.3)4 (23.5)1 (6.3)2 (12.5)0.44
       Biologic13 (68.4)0 (0)12 (75.0)0 (0)<0.001
       Topicals only1 (5.3)7 (41.2)1 (6.3)5 (31.3)0.02
       Other1 (5.3)0 (0)1 (6.3)0 (0)0.86
       None3 (15.8)0 (0)1 (6.3)1 (6.3)0.36
      Past treatment, n (%)
       Phototherapy12 (63.2)10 (58.8)11 (68.8)12 (75.0)0.82
       Oral systemic13 (68.4)4 (23.5)9 (56.3)1 (6.3)<0.001
       Biologic16 (84.2)0 (0)15 (93.8)0 (0)<0.001
       Topicals only0 (0)4 (23.5)0 (0)3 (18.8)0.02
       Other3 (15.8)1 (5.9)1 (6.3)0 (0)0.46
       None1 (5.3)2 (11.8)0 (0)1 (6.3)0.73
      Abbreviation: IQR, interquartile range.

      Free-listing results

      Self-injectable biologics

      Salient words for self-injectable biologics varied across race/treatment groups (Figure 1a). Positive feelings (“positive,” “effective,” “convenient”) were salient only among participants who had experience with biologic treatment, but they were mixed with some negative perceptions, particularly among the white/biologic group. Among biologic-naïve participants, feelings of apprehension and concerns about potential adverse effects and immune suppression were salient. Lack of familiarity with self-injectable biologics, dislike of needles, and concern about side effects were each strongly salient for the black/biologic-naive group only; “side effects” was also moderately salient for the white/biologic-naive group. Additionally, only black participants linked “injection,” which included the descriptive terms “shots” and “needles,” with self-injectable biologics.
      Figure thumbnail gr1
      Figure 1Salient items from free-lists for psoriasis therapies by race/treatment groups. For each psoriasis therapy, words are listed in order of salience from most to least salient: (a) self-injectable biologics, (b) infliximab, (c) methotrexate, (d) apremilast, and (e) phototherapy. Words in boldface are strongly salient; words in plain text are moderately salient. Words are listed twice if strongly salient in one group and moderately salient in another.
      Considering baseline differences in income and education among the race/treatment groups, we also compared free-list data for self-injectable biologics between higher and lower income and education groups (Table 3). “Unfamiliar” was not salient among any of the four groups. However, for both the lower income and education groups, “injection” was identified as the only salient item, whereas apprehension and concerns about adverse effects and immune suppression were salient for both the higher income and education groups.
      Table 3Salient items
      Words in boldface are strongly salient; words in plain text are moderately salient.
      from free-lists of psoriasis therapies by income and education level
      Psoriasis TherapyIncome
      Participants who did not provide income information (n = 9) were excluded from analysis.
      Education
      Higher (n = 30)Lower (n = 29)Higher (n = 38)Lower (n = 30)
      Self-injectable biologicsside effectsinjectionapprehensioninjection
      apprehensionside effects
      negativeimmune suppression
      immune suppression
      Infliximabunfamiliarunfamiliarunfamiliarunfamiliar
      inexperienced
      Apremilastunfamiliarunfamiliarunfamiliarunfamiliar
      commercials
      inexperienced
      Methotrexateunfamiliarunfamiliarunfamiliarunfamiliar
      side effectsside effectsside effectsside effects
      risk
      ineffective
      Phototherapyinconvenientlightinconvenientlight
      positivenegativepositive
      lighteffective
      side effectsbooth
      unfamiliar
      side effects
      ineffective
      1 Words in boldface are strongly salient; words in plain text are moderately salient.
      2 Participants who did not provide income information (n = 9) were excluded from analysis.

      Infliximab

      The most salient word associated with infliximab was “unfamiliar” across all race/treatment (Figure 1b), income, and education groups (Table 3). Lack of experience with infliximab treatment was also strongly salient for each of the black/biologic and lower education groups.

      Methotrexate

      “Unfamiliar” was strongly salient for methotrexate across all race/treatment (Figure 1c), income, and education groups (Table 3). Among white/biologic and black/biologic participants, who were also more likely to have been treated with methotrexate in the past, additional strongly salient items included “side effects” for both groups and “ineffective” for the white/biologic group. Moderately salient items among participants with history of biologic treatment were generally negative in nature among whites and positive among blacks.

      Apremilast

      Similar to infliximab and methotrexate, “unfamiliar” was also strongly salient for apremilast across all race/treatment (Figure 1d), income, and education groups (Table 3). Specifically, for the white/biologic group, reference to commercials for apremilast was strongly salient. “Commercials” remained strongly salient among whites compared with blacks, regardless of biologic treatment status (data not shown) and was also moderately salient for those in the higher education group.

      Phototherapy

      “Inconvenient” was the most salient item for phototherapy among white participants, regardless of biologic treatment history, whereas it was the least moderately salient item for the black/biologic group and was not at all salient for the black/biologic-naïve group (Figure 1e). When all white and black participants were compared, “inconvenient” remained a strongly salient item for the former, whereas “light” and “positive” were salient items for the latter (data not shown). Similarly, among participants who had experience with biologic treatment, negative feelings and “inconvenient” were strongly salient compared with biologic-naïve participants, for whom positive feelings and “effective” were strongly salient (data not shown). A comparison of salient items between participants who were currently receiving versus not receiving phototherapy was performed as well and showed a mix of both positive and negative words. The most salient words associated with those currently receiving phototherapy were positive or neutral, whereas negative or neutral items were most salient for those not currently receiving phototherapy (data not shown). “Inconvenience” was also the most and only strongly salient item for the higher income and education groups (Table 3). The term “light,” which included descriptors of phototherapy (e.g., “UV-ray,” “lights,” “sun lamp”) was strongly salient among all black participants and those in the lower income and education groups.

      Discussion

      In our free-listing study of white and black patients with moderate to severe plaque psoriasis, we identified differences in perceptions and understanding of psoriasis therapies by race and treatment history that show potential reasons for the existing racial disparity in biologic treatment for psoriasis. Most strikingly, we found that for self-injectable biologics, lack of familiarity was a uniquely salient item among black participants who were biologic naïve. Unfamiliarity with self-injectable biologics among this group was unlikely to be due to patients never having been treated with biologics, because “unfamiliar” was not a salient item among white participants who were also biologic naïve. Similarly, in analyses that compared participants by income and education levels, lack of familiarity with self-injectable biologics did not emerge as a salient item, suggesting that neither of these measures of socioeconomic status were primary drivers of our findings among the black/biologic-naïve group. Collectively, these results indicate that black patients with psoriasis, in particular, are less aware of biologics as therapeutic options despite biologics being highly efficacious treatments for psoriasis. We hypothesize that greater unfamiliarity with biologics among black versus white patients may be an important modifiable cause of the racial disparity in biologic treatment for psoriasis that we have previously observed (
      • Takeshita J.
      • Gelfand J.M.
      • Li P.
      • Pinto L.
      • Yu X.
      • Rao P.
      • et al.
      Psoriasis in the US Medicare population: prevalence, treatment, and factors associated with biologic use.
      ).
      “Dislike needles” and “side effects” were also uniquely strongly salient items for self-injectable biologics among the black/biologic-naïve group. This suggests that preference to avoid needles and greater concern about adverse effects among the black/biologic-naive group compared with other race/treatment groups for whom these items were not strongly salient may also drive different biologic treatment patterns. The idea that the risk-benefit balance for biologics may be different between whites and blacks is supported by a single study of rheumatoid arthritis patients that found blacks to be more risk averse than whites when considering treatment with disease-modifying antirheumatic drugs (
      • Constantinescu F.
      • Goucher S.
      • Weinstein A.
      • Smith W.
      • Fraenkel L.
      Understanding why rheumatoid arthritis patient treatment preferences differ by race.
      ).
      Although treatment differences due to patient preferences alone do not constitute a disparity, it is important to remember that patient preferences are not always based on an accurate or adequate comprehension of health care. In fact, preferences that are founded on an inaccurate or inadequate understanding can be a source of disparity (
      Institute of Medicine
      Unequal treatment: confronting racial and ethnic disparities in health care.
      ). We cannot definitively determine from our study if the identified salient themes among race/treatment groups are based on similar levels of understanding of biologics. However, among the salient items for self-injectable biologics, purely descriptive terms, as captured under the item “injection,” were highly salient among black but not white participants and also among participants of lower income and education levels. Among all salient items, a predominance of descriptive terms, some of which were provided in the free-listing prompts, over other words or phrases that express a feeling or represent deeper knowledge may support a hypothesis that the understanding of biologics was less comprehensive among black, lower income, and lower education participants than white, higher income, and higher education participants. A similar pattern of descriptive salient terms (i.e., “light”) among black, lower income, and lower education participants was noted for phototherapy, even though a numerically higher percentage of black participants were currently receiving phototherapy.
      Lack of familiarity with treatment was the most or second most salient item for all other psoriasis therapies (methotrexate, apremilast, infliximab), except for phototherapy. In contrast to self-injectable biologics, lack of familiarity with these other treatments was a similar theme across all race/treatment groups and, at least in part, was likely related to the fact that few participants were currently receiving methotrexate, infliximab, or apremilast in our study.
      As with all studies, there are limitations to consider. The main limitation is that most study participants were from Northeastern US and had been seen at a single large, urban academic health center. Because the intent of qualitative research is hypothesis generation rather than generalizability, our findings may not be representative of all patients with psoriasis throughout the United States who may be seen in different medical settings or who may have chosen not to participate in our study. However, many participants had a long history of psoriasis for which they had received care from multiple providers across different locations over their skin disease course. Second, there were differences in income and education level between the white and black participants that may explain our results. However, our additional analyses by income and education level suggest that our findings for the biologics are not entirely due to socioeconomic status differences. Third, our study was designed to identify differences in perceptions of psoriasis therapies by race/treatment groups, primarily for biologics. Therefore, perceptions of other therapies and differences across other group categorizations require further study. Finally, because there are many potential causes of treatment disparities, understanding not only each patient’s experiences and perceptions but also the medical provider and health system factors that may contribute to disparities is important in future work.
      In conclusion, we hypothesize that racial disparities in biologic treatment for psoriasis in the United States may be due to a greater level of unfamiliarity with biologics, preference to avoid needles, and fear of side effects among black patients compared with whites. Poor familiarity with biologics may stem from having less exposure to the treatments (e.g., not being offered a biologic by a medical provider or not seeing advertisements for biologics, among other reasons) or from lack of recognition or understanding of biologics as treatments for psoriasis even when patients have been offered treatment with or have received information about them. Therefore, we propose that efforts to improve exposure to and understanding of biologic therapeutic options for psoriasis among black patients may be essential to minimizing existing disparities in treatment for this common and chronic inflammatory skin disease that is associated with major comorbid disease burden. Future studies aimed at testing our hypothesis may involve developing and quantitatively testing, in a randomized controlled trial, treatment decision aids or other educational efforts to improve awareness of psoriasis therapies, especially biologics, among black patients with psoriasis. Such studies are critical to advancing efforts to reduce psoriasis treatment disparities and improve outcomes for all.

      Materials and Methods

      Study overview and design

      We designed a qualitative study that used free-listing to understand and compare perceptions of biologics and other common or newer psoriasis therapies among white and black individuals with moderate to severe plaque psoriasis who have and have not received biologic treatment. Free-listing is a standard, systematic interviewing method that is well established in anthropologic research and has been more recently applied to medical research (
      • Ahmad F.S.
      • Barg F.K.
      • Bowles K.H.
      • Alexander M.
      • Goldberg L.R.
      • French B.
      • et al.
      Comparing perspectives of patients, caregivers, and clinicians on heart failure management.
      ,
      • Andrew G.
      • Patel V.
      • Ramakrishna J.
      Sex, studies or strife? What to integrate in adolescent health services.
      ,
      • Barg F.K.
      • Keddem S.
      • Ginsburg K.R.
      • Winston F.K.
      Teen perceptions of good drivers and safe drivers: implications for reaching adolescents.
      ,
      • Bennett I.
      • Switzer J.
      • Aguirre A.
      • Evans K.
      • Barg K.
      ‘Breaking it down’: patient-clinician communication and prenatal care among African American women of low and higher literacy.
      ,
      • Fiks A.G.
      • Gafen A.
      • Hughes C.C.
      • Hunter K.F.
      • Barg F.K.
      Using freelisting to understand shared decision making in ADHD: parents’ and pediatricians’ perspectives.
      ,
      • Patterson A.E.
      • Winch P.J.
      • Gilroy K.E.
      • Doumbia S.
      Local terminology for medicines to treat fever in Bougouni District, Mali: implications for the introduction and evaluation of malaria treatment policies.
      ,
      • Schrauf R.W.
      • Sanchez J.
      Using freelisting to identify, assess, and characterize age differences in shared cultural domains.
      ). Free-listing allows one to identify how people with shared experiences (e.g., a disease such as psoriasis) perceive or define a topic (e.g., psoriasis treatments) (
      • Dongre A.
      • Deshmukh P.
      • Kalaiselvan G.
      • Upadhyaya S.
      Application of qualitative methods in health research: an overview.
      ,
      • Weller S.C.
      • Romney A.K.
      Systematic data collection.
      ). This method involves asking respondents (e.g., individuals with psoriasis) to list all words that come to mind when they think of a specific word or phrase (e.g., biologics) (
      • Dongre A.
      • Deshmukh P.
      • Kalaiselvan G.
      • Upadhyaya S.
      Application of qualitative methods in health research: an overview.
      ). Through free-listing, salient or important words and phrases are identified and considered to define a topic or domain (i.e., a set of items or things that are of the same category) of interest based on the principles that the most relevant items will be mentioned more frequently and earlier than less important or relevant items (
      • Bernard H.R.
      • Pertti J.P.
      • Werner O.
      • Boster J.
      • Romney A.K.
      • Johnson A.
      • et al.
      The contruction of primary data in cultural anthropology.
      ,
      • Borgatti S.
      Cultural consensus theory.
      ,
      • Handwerker W.P.
      • Borgatti S.P.
      Reasoning with numbers.
      ,
      • Weller S.C.
      • Romney A.K.
      Systematic data collection.
      ). Salient words identified from free-lists can also be compared among different groups of people. The free-listing study was embedded within a longer, in-depth, semistructured interview study aimed at understanding the experience of psoriasis and its treatments from the patient perspective. This study was conducted in accordance with the Declaration of Helsinki and approved by the institutional review board of the University of Pennsylvania. Every participant provided informed consent; written consent was obtained for in-person interviews, and verbal consent was obtained for telephone interviews.

      Study sample

      Study participants were recruited both locally and nationally. Local recruitment was primarily from dermatologist referrals from outpatient clinics affiliated with and/or patient responses to study advertisements within the University of Pennsylvania Health System. National recruitment was primarily from individual responses to study advertisements sent to members of the National Psoriasis Foundation, with select additional recruitment by dermatologists of psoriasis patients seen at the University of California–San Francisco, Johns Hopkins University, Howard University, and Cooper University dermatology clinics. Inclusion criteria were as follows: (i) at least 18 years of age, (ii) self-report of current or prior diagnosis of moderate to severe plaque psoriasis from a dermatologist for at least 6 months, (iii) self-identified race as either white or black, (iv) resides in the United States, and (v) is or has been under the care of a dermatologist or rheumatologist for psoriasis. Moderate to severe psoriasis was defined by at least one of the following: (i) study referral from a dermatologist who confirmed a history of moderate to severe psoriasis or (ii) self-report of current or prior treatment with or recommendation by a dermatologist to be treated with phototherapy, oral systemic, or biologic therapy for psoriasis. Individuals were excluded if they did not speak English. Participants were interviewed either in person or via telephone; interview mode has not been shown to affect semi-structured interview responses (
      • Gravlee C.C.
      • Bernard H.R.
      • Maxwell C.R.
      • Jacobsohn A.
      Mode effects in free-list elicitation: comparing oral, written, and web-based data collection.
      ,
      • Vogl S.
      Telephone versus face-to-face interviews: mode effect on semistructured interviews with children.
      ).
      As is standard for qualitative studies, we used a purposive sampling strategy in selecting consecutive study participants who indicated interest in participating in our study. Considering the study objective to understand racial disparities in the biologic treatment of psoriasis, we aimed to achieve an approximately equal number of white and black participants who have and have not received biologic treatment for their psoriasis. Sampling in qualitative research is continued until data saturation is reached, which indicates that no new information or important themes arise (
      • Dongre A.
      • Deshmukh P.
      • Kalaiselvan G.
      • Upadhyaya S.
      Application of qualitative methods in health research: an overview.
      ). We evaluated for saturation by analyzing the free-list data when 80% and 100% of the data had been collected. No new salient words were identified between the two analyses, and the sample was considered to be sufficient. Each participant was provided $40 for his/her study participation.

      Data collection

      The research team developed a free-list interview guide (see Supplementary Appendix S1 online) based on their expertise and input from clinical experts in psoriasis. The guide included an initial description of the study, instructions for free-listing, and an example exercise to allow study participants to practice with a question unrelated to the study. The guide included a written script for the interviewer to maintain consistency across interviews. Participants were asked to provide a verbal list of words in response to five questions about specific psoriasis therapies (self-injectable biologics, infliximab, methotrexate, apremilast, and phototherapy) by asking, “What words come to mind when you think of ‘X’ as a psoriasis treatment?” where X represents each of the psoriasis therapies of interest. Infliximab was queried separately from the other biologics due to being administered intravenously rather than being self-injectable. The brand names for self-injectable biologics, infliximab, and apremilast were used. An optional prompt with a short description of each therapy was provided to those who expressed initial unfamiliarity. The questions were designed to identify perceptions and understanding of biologics and other commonly used or newer therapies for moderate to severe psoriasis among individuals with the disease.
      Interviews were conducted from May 2017 through January 2018. All interviews were performed by one of two members of the research team (WTE or VTR) who were trained in conducting semi-structured interviews. The free-listing portion of the interview typically lasted up to 10 minutes. The interviewers met regularly with the principal investigator (JT) and anthropologist qualitative methods expert (FKB) to address any questions regarding the interview process. Interviews also included questions about participants’ sociodemographic characteristics, psoriasis history, and skin disease-related quality of life as measured by the Dermatology Life Quality Index (
      • Bronsard V.
      • Paul C.
      • Prey S.
      • Puzenat E.
      • Gourraud P.A.
      • Aractingi S.
      • et al.
      What are the best outcome measures for assessing quality of life in plaque type psoriasis? A systematic review of the literature.
      ,
      • Finlay A.Y.
      • Khan G.K.
      Dermatology Life Quality Index (DLQI)—a simple practical measure for routine clinical use.
      ).

      Data management and analysis

      Each study participant’s word lists were transcribed and evaluated independently by three research team members (WTE, CB, and LH) to group similar ideas into standardized single words or phrases while maintaining the order in which words were mentioned. For example, in response to biologics, the single standard word “injection” was used to represent each mention of “needle,” “needles,” and “shot.” Standardized and ordered word lists were reviewed and validated by the principal investigator, revised as necessary, and entered as text files into Anthropac 4.98 (Analytic Technologies, Lexington, KY). For the primary analysis, a text file of word lists was created for each of the five questions about psoriasis treatments and each race/treatment group, indicating the participant’s combination of race and treatment history with biologics (white/biologic, white/no biologic, black/biologic, and black/no biologic), for a total of 20 text files. In additional analyses, text files of word lists for each of the five psoriasis treatments and each of the following race, education, and income groups were also created: white and black race, higher (≥$50,000) and lower (<$50,000) annual household income, and higher (bachelor’s degree or higher) and lower (less than a bachelor’s degree) education level.
      A salience index (Smith S) for each item (i.e., word or theme) in each list was calculated in Anthropac using the following formula: S = {∑ [(LRj + 1)/L]}/n, where L is the length of each list, Rj is the rank of item j in the list, and n is the number of lists in the sample (
      • Borgatti S.P.
      Elicitation techniques for cultural domain analysis.
      ,
      • Smith J.J.
      • Borgatti S.P.
      Salience counts and so does accuracy: correcting and updating a measure for free-list-item salience.
      ). The Smith S is a numeric measure of item importance that identifies salient items that represent those that are most important for defining a domain of interest (e.g., biologics) among members of a group (e.g., individuals with psoriasis). Salience values theoretically range from 0.0 (an item that is never mentioned in any list) to 1.0 (the first item on every list). Salience scores remained linked to their corresponding items and were sorted from high to low and plotted as scree plots, with the y-axis representing Smith S values. The plots were examined to identify the elbow that indicates the transition from a steep to a flattened slope. All items linked to salience scores greater than or equal to the elbow value were considered salient (
      • Borgatti S.P.
      Elicitation techniques for cultural domain analysis.
      ). Among salient items, those with the highest S values and largest spatial separation from words with lower values were considered strongly salient, and the remaining words were considered moderately salient. The primary analysis compared salient items among participants in the white/biologic, white/no biologic, black/biologic, and black/no biologic race/treatment groups. In additional analyses, we also compared salient words between the following participant groups: white and black race, higher and lower annual household income, and higher and lower education level.

      Conflict of Interest

      JT receives research grants 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 and Novartis. JMG served as a consultant for BMS, Boehringer Ingelheim, GSK, Janssen Biologics, Novartis, Regeneron, UCB (DSMB), Sanofi, and Pfizer, receiving honoraria; receives research grants (to the Trustees of the University of Pennsylvania) from AbbVie, Janssen, Novartis, Sanofi, Celgene, Ortho Dermatologics, and Pfizer; and received payment for continuing medical education work related to psoriasis that was supported indirectly by Eli Lilly and Ortho Dermatologics. JMG is a co-patent holder of resiquimod for the treatment of cutaneous T-cell lymphoma. The other authors state no conflict of interest.

      Acknowledgments

      This study was supported by a grant from the National Institute of Arthritis and Musculoskeletal and Skin Diseases K23-AR068433 (to JT). Funding sources had no role in the design and conduct of the study; collection, management, analysis, and interpretation of data; preparation, review, or approval of the manuscript; or decision to submit the manuscript for publication.
      We are grateful to Warren R. Heymann, Wilson Liao, and Ginette A. Okoye for their assistance with study recruitment and to our study participants for sharing their time and thoughts with us.
      An abstract of the data contained in this article was presented at the International Investigative Dermatology 2018 Meeting (May 2018) and the American Public Health Association 2018 Annual Meeting (November 2018).

      Supplementary Materials

      Supplementary Appendix S1. Free-listing interview guide
      Cosentyx: Novartis, East Hanover, NJ; Enbrel: Amgen, Thousand Oaks, CA; Humira: AbbVie, North Chicago, IL; Otezla: Celgene, Summit, NJ; Remicade: Janssen Biotech, Horsham, PA; Siliq: Ortho Dermatologics, Bridgewater, NJ; Stelara: Janssen Biotech, Horsham, PA; Taltz: Eli Lilly, Indianapolis, IN; Tremfya: Janssen Biotech, Horsham, PA.
      1Cosentyx: Novartis, East Hanover, NJ; Enbrel: Amgen, Thousand Oaks, CA; Humira: AbbVie, North Chicago, IL; Otezla: Celgene, Summit, NJ; Remicade: Janssen Biotech, Horsham, PA; Siliq: Ortho Dermatologics, Bridgewater, NJ; Stelara: Janssen Biotech, Horsham, PA; Taltz: Eli Lilly, Indianapolis, IN; Tremfya: Janssen Biotech, Horsham, PA.

      I’d like to start with a word association exercise about different psoriasis therapies. I will name a psoriasis treatment, and I’d like you to tell me any and all words that come to your mind about that treatment. If you can, please try to use single words. If you are not familiar with the treatment, you can say, “I don’t know.” Before we begin, let’s try a practice exercise together.
      What words come to mind when you think of the beach? Now, let’s do the same exercise with psoriasis treatments.
      Q1: What words come to mind when you think of phototherapy as a psoriasis treatment?
      Reminder: Phototherapy is a form of artificial sunlight that is usually administered 2–3 times a week (not a tanning bed).
      Q2: What words come to mind when you think of methotrexate as a psoriasis treatment?
      Reminder: Methotrexate is an oral pill. Methotrexate is often taken as multiple pills once a week at home.
      Q3: What words come to mind when you think of Otezla (apremilast)?
      Reminder: Otezla is an oral pill that is taken twice a day at home.
      Q4: What words come to mind when you think of self-injectable medications or biologics, for example, Enbrel, Humira, Stelara, Cosentyx, Taltz, Siliq, and Tremfya?
      Reminder: These medications are shots that you can give yourself at home anywhere from 2 times a week to every 3 months depending on the specific medication.
      Q5: What words come to mind when you think of Remicade (infliximab)?
      Reminder: This is a medication (biologic) that is administered as an infusion through your vein in the doctor’s office about every 8 weeks.

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