Abstract
Background
Generalized pustular psoriasis (GPP) is a rare, chronic, often unpredictable, severe multisystemic autoinflammatory skin disease from which patients can experience flares, episodes of widespread eruptions of painful, sterile pustules often accompanied by systemic symptoms. The impact of GPP flares and underlying GPP severity on the healthcare resource utilization (HCRU) is not well characterized.
Objective
To quantify HCRU among US GPP patients by flare status and underlying severity.
Methods
Outpatient electronic health record (EHR) data (2017-2023) from the OMNY Health platform were linked with claims. Patients were indexed at first EHR GPP diagnosis code and followed for 1 year. GPP flares were identified from a previously developed algorithm. All-cause hospitalizations, emergency department/urgent care (ED/UC), and outpatient visits were summarized by flare status and underlying severity. Pharmacy and total gross charges were described by number of flares.
Results
A total of 335 patients were included. Patients who flared in the follow-up period (n = 205) had more hospitalizations than patients who did not flare (n = 130; 12.2% vs 6.9%; mean: 0.26 vs 0.09). ED/UC visits were similar between groups (22.9% vs 27.7%; mean: 0.54 vs 0.45), while outpatient visits were greater among patients who did not flare (69.8% vs 78.5%; mean: 5.37 vs 6.56). For patients with 0, 1, and ≥2 flares with HCRU, mean pharmacy charges ($19,887, $25,180, and $57,674, respectively) and total gross charges ($29,196, $40,079, and $52,940, respectively) increased monotonically.
Conclusion
GPP patients who flared and had more severe disease had greater HCRU and charges.
Keywords: generalized pustular psoriasis, flare, healthcare resource utilization, charges, real-world data
Introduction
Generalized pustular psoriasis (GPP) is a chronic rare skin disorder characterized by generally distributed eruptions of sterile pustules arising on inflamed skin.1,2 Accompanying symptoms are variable and may include leukocytosis, scaling, skin pain, itching, burning, and high fever.3,4 Additionally, autoimmune comorbid conditions and laboratory abnormalities are often associated with GPP. In the acute phase, GPP patients may experience periodic flares, which are unpredictable episodes of extensive, sterile pustular eruptions, often accompanied by potentially life-threatening systemic complications, including sepsis and respiratory, heart, liver, and kidney failure.3-6 A survey of dermatologists from the Corrona Registry reported that GPP patients flares can typically last between 2-4 weeks, with 41% of dermatologists reporting flares can last up to 1-3 months. 7 Treatments for GPP flares are limited with AAD-NPF guidelines for off-label treatments reflecting low-strength recommendations consisting of B or C ratings. Broad consensus-based treatment goals include clearance of pustules, erythema, scaling and crust, skin lesions, and prevention of new flares. 8 Currently, spesolimab is the only FDA approved treatment specifically for GPP, 9 which demonstrated efficacy in reducing the number of visible pustules among patients experiencing a GPP flare. 10 Furthermore, spesolimab is also approved for subcutaneous administration in patients with GPP who are not experiencing a disease flare.
Although electronic health records (EHRs) and administrative claims databases can be useful for understanding the burden of GPP on the healthcare system, the rarity of GPP and lack of standard documentation for flares and disease severity measures makes it difficult assess factors that impact health care resource utilization. As a result, few studies examining the impact of GPP flares and disease severity on healthcare resource utilization (HCRU) and associated charges have been published. The objective of this study is to quantify HCRU, pharmacy charges and total charges among GPP patients identified in outpatient dermatology clinics in the United States by documented flare status and underlying disease severity.
Methods
Study Design and Data Sources
This non-interventional cohort study was a retrospective analysis of EHR data from United States-based outpatient dermatology clinics and claims data from January 2017 to January 2023. De-identified patient-level EHR data from 6 specialty dermatology networks in the OMNY Health deidentified real-world data platform were accessed. In addition to standard structured EHR fields, this data source included clinical measures of GPP disease activity (i.e., body surface area, physician global assessment of severity, pain visual analogue scale) for a subset of patient encounters and access to encounter-level unstructured clinical notes. Furthermore, the patient-level data were tokenized and linked to a claims data source to access information on HCRU and associated charges delivered inside and outside the dermatology clinics.
Participants
Patients were included if they met the following criteria: (1) ever had an EHR diagnosis code for GPP (International Classification of Diseases, 10th Edition [ICD-10]: L40.1), (2) were at least 12 years of age at the time of their first GPP diagnosis code, (3) had at least 30 days of EHR data before their first GPP diagnosis code, (4) had accessible clinical notes to determine GPP flare status, and (5) had available linkable claims with at least 1 year of follow-up data. GPP flare status at each encounter was determined from a supervised-learning algorithm based on natural language processing of clinical notes and structured procedure codes from the EHR data. 11 Flare episodes were defined as 45 days in length, in line with clinical observations and previously published literature.3,4 Patients were indexed at the date of their first GPP diagnosis code. The pre-index period was defined as the time prior to the index date for which the patient had data and was used to characterize the study population.
The follow-up period was defined as up to 1 year after the index date and was used to determine the occurrence and frequency of GPP flares and to assess HCRU and associated charges. HCRU outcomes were all-cause hospitalizations, emergency department and urgent care (ED/UC) visits, and outpatient visits in the follow-up period. Charges associated with pharmacy claims and total charges (i.e., charges associated with any claim) were also assessed in the follow-up period.
Statistical Analysis
Descriptive statistics were used to characterize the study population overall and by subsequent flare status in the follow-up period. HCRU outcomes were summarized for GPP patients by flare status and by underlying disease severity at index GPP diagnosis code as determined from the physician global assessment of severity among patients who had a baseline rating. Pharmacy and total gross charges (i.e., charges for all services including pharmacy) were described by number of flares (0, 1, or ≥2) observed in the follow-up period.
Results
Of approximately 7.4 million patients from specialty dermatology networks with available EHR data, 1672 had at least 1 diagnosis code for GPP during the study period, 1660 of whom were at least 12 years of age, 823 of whom had at least 30 days of data in the pre-index period, and 638 of whom had accessible clinical notes. Linkable claims with at least 1 year of follow-up data were available for 335 of these patients, comprising the study population; 205 (61%) experienced at least 1 flare episode (160 with 1 flare and 45 with ≥2 flares).
Most patients were female (75%), white (89%), and not Hispanic or Latino (95%) with an average age of 58 years (standard deviation: 15). Common medical histories and comorbid conditions included plaque psoriasis (45%), cardiovascular disease (33%), systemic infection (32%), and skin infection (20%). Patients who experienced a GPP flare were more likely to be less than 65 years of age (70% vs 57%), nonwhite (16% vs 6%), and Hispanic or Latino (9% vs 0%), have a physician global assessment rating of severe disease (16% vs 7%), have greater GPP percent body surface area (mean: 14% vs 7%), and experience more pain (31% vs 18% with visual analogue scale ≥3). No notable differences by flare status were observed for other index variables (Table 1).
Table 1.
Patient Characteristics at Index GPP Diagnosis Code.
| Characteristic | Study Population (N = 335) | Experienced a GPP Flare (N = 205) | Did Not Experience a GPP Flare (N = 130) |
|---|---|---|---|
| Gender, N (%) | |||
| Female | 249 (74.8) | 153 (75.4) | 96 (73.8) |
| Male | 84 (25.2) | 50 (24.6) | 34 (26.2) |
| Age, mean (SD), years | 58 (15) | 57 (15) | 60 (14) |
| Age (years), N (%) | |||
| 12 to 17 | 2 (0.6) | 2 (1.0) | 0 (0.0) |
| 18 to 34 | 25 (7.5) | 20 (9.8) | 5 (3.8) |
| 35 to 49 | 60 (17.9) | 38 (18.5) | 22 (16.9) |
| 50 to 64 | 130 (38.8) | 83 (40.5) | 47 (36.2) |
| ≥65 | 118 (35.2) | 62 (30.2) | 56 (43.1) |
| Race, N (%) | |||
| Black or African American | 14 (8.3) | 11 (12.4) | 3 (3.8) |
| White | 150 (88.8) | 75 (84.3) | 75 (93.8) |
| Other | 5 (3.0) | 3 (3.4) | 2 (2.5) |
| Ethnicity, N (%) | |||
| Hispanic or Latino | 6 (4.9) | 6 (8.5) | 0 (0.0) |
| Not Hispanic or Latino | 117 (95.1) | 65 (91.5) | 52 (100.0) |
| Medical histories and comorbid conditions, N (%) | |||
| Anxiety | 49 (14.6) | 30 (14.6) | 19 (14.6) |
| Cancer | 43 (12.8) | 23 (11.2) | 20 (15.4) |
| Cardiovascular disease | 109 (32.5) | 62 (30.2) | 47 (36.2) |
| Hidradenitis suppurativa | 10 (3.0) | 8 (3.9) | 2 (1.5) |
| Palmoplantar pustulosis | 35 (10.4) | 21 (10.2) | 14 (10.8) |
| Plaque psoriasis | 152 (45.4) | 88 (42.9) | 64 (49.2) |
| Psoriatic arthritis | 18 (5.4) | 10 (4.9) | 8 (6.2) |
| Skin infection | 66 (19.7) | 41 (20.0) | 25 (19.2) |
| Systemic infection | 107 (31.9) | 64 (31.2) | 43 (33.1) |
| Percent body surface area, No. | 67 | 43 | 24 |
| Mean (SD) | 12 (16) | 14 (19) | 7 (8) |
| Median (Q1, Q3) | 5 (2, 13) | 6 (4, 20) | 4 (2,10) |
| Physician global assessment of severity at index, N (%) | |||
| Clear | 2 (2.7) | 0 (0.0) | 2 (6.7) |
| Almost clear | 11 (14.9) | 6 (13.6) | 5 (16.7) |
| Mild | 15 (20.3) | 11 (25.0) | 4 (13.3) |
| Moderate | 37 (50.0) | 20 (45.5) | 17 (56.7) |
| Severe | 9 (12.2) | 7 (15.9) | 2 (6.7) |
| Pain 10-point visual analogue scale, N (%) | |||
| 0 | 34 (59.6) | 21 (60.0) | 13 (59.1) |
| 1 | 4 (7.0) | 0 (0.0) | 4 (18.2) |
| 2 | 4 (7.0) | 3 (8.6) | 1 (4.5) |
| ≥3 | 15 (26.3) | 11 (31.4) | 4 (18.2) |
Abbreviations: GPP, generalized pustular psoriasis; Q1, first quartile; Q3, third quartile; SD, standard deviation; VAS, visual analogue scale.
Note: Race, ethnicity, and disease activity metrics were available for a subset of patients; statistics were based on nonmissing data. Medical histories and comorbid conditions are not mutually exclusive.
Healthcare Resource Utilization
Patients who experienced a flare episode in the 1-year follow-up period were more likely to be hospitalized than patients who did not experience a flare episode (12.2% vs 6.9%). Similarly, flares were associated with increased mean number of hospitalizations (0.26 vs 0.09 overall; 2.12 vs 1.33 among patients with at least 1 hospitalization) and associated mean charges ($1207 vs $455 overall; $9895 vs $6573 among patients with at least 1 hospitalization). Although the proportion of patients who had an ED/UC visit was smaller for patients who experienced a flare episode (22.9% vs 27.7%), they had greater mean number of ED/UC visits (0.54 vs 0.45 overall; 2.36 vs 1.64 among patients with at least 1 ED/UC visit) and associated mean charges ($840 vs $769 overall; $3662 vs $2776 among patients with at least 1 ED/UC visit). Outpatient visits were more prevalent among patients who did not experience a flare episode (78.5%) compared to patients who did (69.8%); however, outpatient charges were similar by flare status ($5113 vs $5867 overall; $7330 vs $7478 among patients with at least 1 outpatient visit). Compared to patients rated as having clear, almost clear, or mild GPP (n = 37), patients who were rated as having moderate or severe GPP (n = 55) were more likely to have a hospitalization (10.9% vs 0%) and ED/UC visit (20.0% vs 5.4%) and had a slightly higher likelihood of having an outpatient visit (67.3% vs 62.2%) in the follow-up period (Table 2).
Table 2.
All-Cause Healthcare Resource Utilization by Flare Status in the Follow-Up Period and by Index Disease Severity.
| Description | Flare Status | Index GPP Severity | ||
|---|---|---|---|---|
| Patients with ≥1 Flare (N = 205) | Patients with No Flares (N = 130) | Moderate, Severe (N = 55) | Clear, Almost Clear, Mild (N = 37) | |
| Hospitalizations | ||||
| Patients with ≥1 hospitalization, n (%) | 25 (12.2%) | 9 (6.9%) | 6 (10.9%) | 0 (0.0%) |
| Number of hospitalizations overall, mean (SD) | 0.26 (0.93) | 0.09 (0.36) | 0.13 (0.39) | 0.00 (0.00) |
| Number of hospitalizations among patients with ≥1 hospitalization, mean (SD) | 2.12 (1.81) | 1.33 (0.50) | 1.17 (0.41) | NA |
| ED/UC visits | ||||
| Patients with ≥1 ED/UC visit, n (%) | 47 (22.9%) | 36 (27.7%) | 11 (20.0%) | 2 (5.4%) |
| Number of ED/UC visits overall, mean (SD) | 0.54 (1.66) | 0.45 (0.92) | 0.38 (0.97) | 0.05 (0.23) |
| Number of ED/UC visits among patients with ≥1 ED/UC visit, mean (SD) | 2.36 (2.79) | 1.64 (1.05) | 1.91 (1.38) | 1.00 (0.00) |
| Outpatient visits | ||||
| Patients with ≥1 outpatient visits, n (%) | 143 (69.8%) | 102 (78.5%) | 11 (20.0%) | 2 (5.4%) |
| Number of outpatient visits overall, mean (SD) | 5.37 (9.03) | 6.56 (9.93) | 0.47 (1.12) | 0.05 (0.23) |
| Number of outpatient visits among patients with ≥1 outpatient visit, mean (SD) | 7.70 (9.95) | 8.6 (10.52) | 2.36 (1.36) | 1.00 (0.00) |
Abbreviations: ED/UC, emergency department or urgent care; GPP, generalized pustular psoriasis.
Note: Index GPP severity was based on physician global assessment of severity at index GPP diagnosis code.
Pharmacy and Total Charges
Direct monotonic relationships were observed between number of flares and both mean pharmacy charges and total gross charges. For patients who experienced 0, 1 and ≥2 flares in the follow-up period, mean pharmacy charges, respectively, were $13,678, $15,580, and $38,450 overall, and $19,887, $25,180, and $57,674 among patients with at least 1 pharmacy claim. Similar trends were observed for total gross charges with mean values ranging from $26,501 to $48,234 overall and from $29,196 to $52,940 among patients with at least 1 charge for any service (Figure 1).
Figure 1.
Mean pharmacy and total gross charges by number of GPP flares in the follow-up period.
During the 1-year follow-up period, patients with moderate or severe GPP had approximately 5 times overall mean pharmacy charges ($24,666 vs $5078) and 3.5 times overall total gross charges ($10,042 vs $36,222) compared to patients with clear, almost clear, or mild GPP at index diagnosis code. Similar results were observed for patients with at least 1 documented pharmacy or charge or any service (Figure 2).
Figure 2.
Mean pharmacy and total gross charges by physician global assessment of severity at index GPP diagnosis.
Discussion
The burden of GPP on various healthcare systems has been studied.12-17 Recent analyses using claims data concluded that GPP patients had higher all-cause outpatient, inpatient, and ED visits and longer mean duration length of stay compared to those with plaque psoriasis.18,19 An additional study examining the economic burden of GPP utilizing IQVIA PharMetric Plus US claims database found that the adjusted total direct costs per patient per month for GPP were 35% higher compared to a matched plaque psoriasis cohort and more than the 5 times the costs compared to a matched general population cohort. 17 Furthermore, a long-term case series study of GPP patients demonstrated that 36% of GPP patients had at least 1 hospitalization with a median rate of 0.5 hospitalizations per year. 20 Our study, however, specifically examined the impact of GPP flares and disease severity on healthcare resource utilization and associated charges in a large sample of GPP patients in the real-world dermatology setting.
Results from our study show that GPP patients who experienced a flare had a distinct demographic and clinical profile (younger, nonwhite, Hispanic or Latino, greater underlying disease activity). Furthermore, these patients who flared represented a greater overall burden to the healthcare system as measured by more hospitalizations and ED/UC visits and 1.5 times the mean pharmacy charges and total gross charges in the 1 year following index GPP diagnosis code. Burden on the patient and healthcare system was more pronounced for patients with ≥2 flares (2-3 times mean pharmacy charges; 1.5-2 times mean total gross charges compared to patients with no flares) and for patients rated as moderate or severe (4-5 times mean pharmacy charges; 3.5 times mean total gross charges compared to less severe patients).
Although this is the first US-based study examining HCRU by flare status, the overall findings of this study focusing on patients who flare are similar to prior studies examining HCRU and the economic burden of GPP. Crowley et al 18 and Sobell et al 19 published parallel analyses examining HCRU in GPP patients over a 1-year follow-up period in different databases with different populations. Our results for all GPP patients were very similar to those of Sobell et al for hospitalizations (8.7% vs 12.2% patients; mean number: 2.0 vs 1.9) and ED/UC visits (21.3% vs 24.6%; mean number: 2.2 vs 2.0). Results for outpatient visits were different (mean number: 7.7 vs 17.0), which may be a consequence of their inclusion criterion of at least 2 outpatient visits with GPP diagnosis codes. Crowley et al reported higher utilization for all resources; however, their population was older on average (54.7% ages ≥65 years vs 12.4% in Sobell et al and 35.2% in our study). Charges for the overall GPP population were similar to cost analyses (transformed from monthly to annually) presented by Hanna et al 17 where mean pharmacy costs and total costs per patient per year (vs charges in our study) were $21,828 (vs $25,745) and $38,100 (vs $36,553), respectively.
While patients who experienced a flare may have subsequently been treated more actively and been less likely to have had an ED/UC visit (given the lower proportion of patients), they utilized this resource more than patients who did not experience a flare (given the higher mean number of ED/UC visits). Patients who experienced a flare may have been less likely to have outpatient visits because they tended to present with greater severity and have greater utilization of ED/UC services than patients who did not experience a flare.
This study had several limitations. Data were from US-based outpatient practices only, which included patients who were referred or had access to specialists who were more likely to diagnosis and treat GPP. These patients may also be sicker than other patients experiencing care in more general settings and may be more likely to require biologics and other systemic treatments. Only patients with the GPP diagnosis code (ICD-10: L40.1) were included. Given that GPP is a rare disease, underdiagnosis in the real-world setting is possible, which may have resulted in the underestimation of number of flares and flare rate in the follow-up period. The establishment of GPP flares in EHR data was based on an algorithm using natural language processing of clinical notes and structured procedure codes. Although GPP-specific diagnosis statuses indicating worsening or uncontrolled condition were available for encounters used in algorithm training, the algorithm was not fully validated with clinically adjudicated chart review. Documentation and coding of GPP and GPP flares may not have been comprehensive or consistent between healthcare providers, leading to variability. Prescription orders and administrations were observed in EHR data and may not have represented whether therapies were taken by the patient. Indication of medications was defined by the presence of prescription data and label conventions and may not have represented actual use of medication. Nonetheless, the results of this study highlight the importance of understanding GPP flares in terms of patient demographic and clinical characteristics and the increased patient and economic burden associated with number of flares and underlying disease severity. Managing GPP patients to prevent flares and treat emerging flares are important to reducing HCRU and associated charges.
Footnotes
The author(s) declared the following potential conflicts of interest with respect to the research, authorship, and/or publication of this article: The authors met criteria for authorship as recommended by the International Committee of Medical Journal Editors (ICMJE). Megan Noe was an employee of Brigham and Women’s Hospital at the time of study completion but is now employed by Sanofi. She has received research grants from Boehringer Ingelheim and Bristol Myers Squib. She is a consultant for Boehringer Ingelheim and Argenx and received honoraria. She was a senior editor for the Journal of Psoriasis and Psoriatic Arthritis during the presentation of this manuscript. Layla Lavasani and Marianne Laouri are full-time employees of Boehringer Ingelheim. Lawrence Rasouliyan is an employee of OMNY Health, a company contracted by Boehringer Ingelheim to provide data and research services. Jamie Rhoads received research grants from Genentech. She is a consultant for Eli Lilly and Company, Boehringer Ingelheim, and Argenx. Boehringer Ingelheim was given the opportunity to review the manuscript for medical and scientific accuracy as well as intellectual property considerations.
Funding: The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: The study was supported and funded by Boehringer Ingelheim. The authors met criteria for authorship as recommended by the International Committee of Medical Journal Editors (ICMJE). Boehringer Ingelheim was given the opportunity to review the manuscript for medical and scientific accuracy as well as intellectual property considerations.
Ethical Statement
Ethics and Consent
Our institution does not require ethics approval for reporting secondary research.
ORCID iDs
Megan H. Noe https://orcid.org/0000-0001-8481-4711
Lawrence Rasouliyan https://orcid.org/0000-0002-0445-6123
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