Employing Adalimumab in Treatment of Moderate-to-Severe Hidradenitis Suppurativa: Real-Life Multicenter Data from the Czech Republic

Smetanova, Alzbeta; Marques, Emanuel; Kojanova, Martina; Arenberger, Petr; Strosova, Daniela; Fialova, Jorga; Arenbergerova, Monika

doi:https://doi.org/10.1155/2023/3640285

Dermatologic Therapy

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Abstract Introduction Methods Results Discussion Data Availability Conflicts of Interest Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2023 | Article ID 3640285 | https://doi.org/10.1155/2023/3640285

Employing Adalimumab in Treatment of Moderate-to-Severe Hidradenitis Suppurativa: Real-Life Multicenter Data from the Czech Republic

Alzbeta Smetanova,¹Emanuel Marques,¹Martina Kojanova,²Petr Arenberger,¹Daniela Strosova,³Jorga Fialova,²and Monika Arenbergerova¹

Academic Editor: Qiuning Sun

Received03 Nov 2022

Revised03 Jan 2023

Accepted17 Feb 2023

Published15 Mar 2023

Abstract

Adalimumab is the only approved biologic treatment for moderate-to-severe hidradenitis suppurativa, nonetheless, long-term data from real-life setting are still limited. The objective of this observational multicenter study was to evaluate the effectiveness, safety, and drug survival of adalimumab in patients with hidradenitis suppurativa included in the BIOREP registry. A total of 299 patients who initiated adalimumab therapy for hidradenitis suppurativa from 2011 to November 2021 were included. The Dermatology-Life-Quality-Index (DLQI), pain scale, the number of abscesses, inflammatory nodules and draining tunnels, and International Hidradenitis Suppurativa Severity Score System (IHS4) were recorded in the 0^th, 3^rd, and 6^th months; then every 6 months during the ongoing adalimumab treatment. Studied patients underwent treatment for up to 48 months, with the average duration of treatment lasting 2.3 years. The mean age of the patients was 44.9 years, 79% were smokers or ex-smokers, 54.8% were obese, and 26.4% were overweight, the mean BMI was 30.8. The mean time from diagnosis to initiation adalimumab therapy was 9.1 years. The number of patients with severe IHS4 dropped from the initial 249 (83.3%) to 65 (30.1%) after 12 months and this trend was maintained up to the 48^th month. A decreasing number of inflammatory lesions were rapid and sustained and correlated to the improvement of patients’ quality of life, the mean DLQI score dropped from 17.6 to 8.5 after 3 months and to 5, 7 after 48 months. No unexpected risk signals were observed. Our long-term study demonstrates the effectiveness and safety of adalimumab in a real-life setting.

1. Introduction

Hidradenitis suppurativa (HS) is a chronic inflammatory skin disease that severely impairs patients’ quality of life. It is characterized by recurrent painful nodules, abscesses, and draining sinus tracts most commonly in the axillary, inguinal, and anogenital regions Reference [1]. Chronic inflammation and dysregulated epithelial differentiation, especially of hair follicle keratinocytes, which leads to follicular hyperkeratosis, dilatation, and rupture, have been involved in the pathogenesis of HS [2]. Cardiovascular diseases risk factors including central obesity, history of smoking, metabolic syndrome, dyslipidemia, and hypertension are more prevalent among HS patients compared to the general population [3]. At the same time, HS is associated with other immune-mediated diseases, such as inflammatory bowel disease and spondyloarthropathy (Nguyen TV, Damiani G) and high rates of depression and anxiety have been reported in HS patients [4].

In a recent review, the prevalence of HS in the American and European populations varies from 0.7% to 1.2% [5]. The onset of the disease is usually shortly after puberty, and HS is more common in women compared to men (>2 : 1). It is not clear whether menopause induces remission [1, 6]. Delayed diagnosis led to irreversible scarring and significantly impacted patient’s physical and mental health and his ability to integrate into everyday work and social life [7]. In a recent multicenter study, the therapeutic delay correlated to lack of response to adalimumab [8].

According to the recommendations of the Czech State Institute for Drug Control, fully human monoclonal antibody blocking tumor necrosis alfa-adalimumab, is the only approved biological drug for the treatment of moderate-to-severe HS. Treatment is reimbursed only for adult patients and adolescents over 12 years of age who have active moderate-to-severe form of HS and not responded to or are intolerant to 3 months of oral antibiotic therapy [9].

Clinical trials demonstrated safety and effectiveness of adalimumab [10]. However, comprehensive long-term data from the common clinical practice of HS are still limited [11–13].

The aim of this observational, multicenter study was to describe the patient cohort of 299 patients from the Czech Republic treated for moderate-to-severe HS with adalimumab as well as data related to drug survival, effectiveness, and health-related quality using long-term data from the BIOREP registry.

2. Methods

In this retrospective multicenter study, data from the nationwide BIOREP registry (established in May 2005) were used. BIOREP is a web-based database of patients with psoriasis, hidradenitis suppurativa (2011), and atopic dermatitis (2018) treated with biologics or targeted therapy. In the Czech Republic, biological therapy is administered at 37 specialized centres, 35 of which are included in the BIOREP registry. Adalimumab for HS was administered in 18 centres at the time of the analysis.

The study was conducted in accordance with the Helsinki Declaration of 1964 and all subsequent amendments, and all patients provided a written informed consent. Patient-level data used for this analysis were deidentified, and Institutional Review Board approval was not required for this study. Permission to use data from the BIOREP registry was obtained. Patients with HS who received at least one dose of adalimumab were analyzed. The cut-off date for our analysis was 15^th of November 2021. Patients were treated according to the standard treatment regimen of adalimumab: 160 mg at baseline and 80 mg at week 2, followed by 40 mg weekly from week 4 or 80 mg every other week in maintenance phase [14, 15].

Patients’ demographic and baseline clinical characteristics were collected including age, the age at onset of HS, gender, weight, height and body mass index (BMI), occupation, smoking status, alcohol consumption, family history of HS, patients’ comorbidities, duration and severity of the disease, previous treatment, standardized measures of health status; Dermatology Life Quality Index (DLQI), pain according to visual analogue scale (VAS), number of abscesses, inflammatory nodules and draining tunnels, and International Hidradenitis Suppurativa Severity Score System (IHS4). This validated scoring system was calculated by the number of nodules1 + number of abscesses2 + number of draining tunnels4 with a total score: ≤3—mild, 4–10—moderate, and ≥11—severe [16] Level of white blood cell count and C-reactive protein (CRP) was analysed when available. In addition, the age at onset of adalimumab treatment was recorded.

2.1. Treatment Assessment

Disease severity was assessed using IHS4 at baseline, month 3, 6, and then every 6 months. The HS lesions were counted and included number of inflammatory nodules, abscesses, and draining fistulas.

The Dermatology Life Quality Index (DLQI) questionnaire and the Visual Analogue Scale for pain (VAS) which are instruments widely accepted to evaluate QoL in HS, were collected at baseline and month 3, 6, and then every 6 months.

2.2. Statistical Analysis

Collected parameters were summarized using descriptive statistics. Categorical outcomes were evaluated by the number and percentage in each category and continuous outcomes were assessed by mean and standard deviation (SD). The persistence on adalimumab was defined as the time from initiation of adalimumab treatment to the discontinuation, temporary termination, or switch of the treatment. Patients were censored in case they were lost to follow-up or in case no more follow-up visits were available. The persistence was assessed using Kaplan–Meier survival curves, which take into account right-censored data. Differences between survival curves were tested using the log-rank test at the significance level of 5.0%. Statistical analyses were performed using Stata software [17].

3. Results

3.1. Demographics and Clinical Characteristics

A total of 299 patients with moderate-to-severe HS were enrolled, 133 women (44.5%) and 166 men (55.5%) with a mean age of 44.9 years (SD 12.9). At baseline the HS status of patients was evaluated. Hurley stage I was shown in 1%, Hurley stage II in 37%, and Hurley stage III in 58%. The mean age at the time of diagnosis of HS was 33.6 years (SD 13.1), the mean age at the initiation of adalimumab treatment was 42.7 years (SD 12.7). The mean duration from diagnosis to the initiation of adalimumab was 9.1 years (SD 9.1). A total of 51 patients (17.1%) had a family history of HS. Almost 80% of patients were current smokers or ex-smokers with an average of 13.8 cigarettes smoked per day. More than half of the patients worked full-time, 22.4% were on disability pension, 6.7% were retired, 4.3% were studying, 4.3% worked half-time, 4.0% were unemployed, and 3.7% were on long-term incapacity for work (Tables 1 and 2).

A total of 176 patients (58.9%) suffered from at least one comorbidity. The most common of them were arterial hypertension (26.4%) and diabetes mellitus type II (13.7%). A total of 9.0% had dyslipidemia, 5.4% depression, almost 3% anxiety disorder and 2.3% Crohn’s disease or ulcerative colitis. Obesity was found in 164 patients (54.8%), 79 patients (26.4%) were found to be overweight (Table 1).

The previous therapy consisted of systemic antibiotic use (94.3% of patients), retinoids (25.1%), autogenous vaccine therapy (7.0%), and systemic corticosteroids (2.3%). The most affected region at the baseline was genitofemoral area (84.3% of patients) and axillary area (73.6% of patients) (Table 1).

3.2. Adalimumab Treatment

Out of 299 patients, a total of 216 patients (72.2%) completed 12 months of treatment, 137 patients (45.8%) completed 24 months, and 46 patients (15.4%) completed 48 months of adalimumab treatment. In total, 96.0% of analysed patients received Humira and 4.0% of patients were treated by biosimilars of adalimumab.

The mean VAS score was 5.2 (SD 2.7) at baseline. In terms of inflammatory serum markers, the mean baseline level of white blood cell count was 10.6 × 10⁹ (SD 2.9), and a total CRP serum level was 20.3 mg/ml (SD 22.3) (Table 2).

During the adalimumab treatment, there was a substantial reduction in number of abscesses, nodules and draining fistulas, IHS4, and DLQI scores (Figure 1). At baseline, the HS status was assessed as severe in 249 patients (83.3%) based on IHS4 scoring and moderate or mild in 37 patients (12.4%) (Table 2). The proportion of patients with severe IHS4 score decreased from 83.3% to 39.6% after 3 months and to 30.1% patients after 12 months of adalimumab treatment and remained stable for the rest of follow-up (Figure 2).

The improvement in IHS4 correlated with the number of active HS lesions. The mean number of inflammatory nodules at baseline was 8.2, the mean number of draining fistulas was 5.0, and the mean number of abscesses was 3.0. The improvement was observed after only 3 months of treatment, mean values decreased to 3.5 of inflammatory nodules, 1.9 fistulas, and 1.1 abscesses. After 12 months of treatment the mean values were as follows: inflammatory nodules 2.8, draining fistulas 1.4, and abscesses 0.7. The number of active lesions was stable at low levels during the patients´ visits up to 48 months of treatment. A minor increase in the number of draining tunnels (1.5 after 30 months and 1.6 after 48 months of treatment) could be observed (Figure 1).

Decreasing number of inflammatory lesions correlated to the improvement of patients’ quality of life, reflected in the DLQI questionnaire. A mean DLQI score was 17.6 (SD 7.3) at baseline, dropped to 8.5 (SD 6.5) after 3 months and to 6.1 (SD 6.0) after 12 months of treatment and remained stable during observation period (Table 2, Figure 1).

Furthermore, we analysed the course of BMI level during the treatment, at baseline the mean BMI was 30.8 (SD 5.9), with a slightly decreasing trend to 30.2 (SD 5.0) at 24 months, 29.9 (SD 5.4) at 30 months, and 28.9 (SD 5.9) at 48 months.

3.3. Treatment Discontinuation

From all 299 analysed patients, 233 patients (77.9%) were still treated at the time of the data lock point. A total of 66 patients (22.1%) discontinued, temporarily terminated or switched the treatment; 17 due to lack of effectiveness (5.7%); 15 for adverse events (5.0%); 10 due to surgical procedure (3.3%); 7 for noncooperation (2.3%); 7 due to other reasons (2.3%); patient’s choice in 5 (1.7%); 4 due to pregnancy (1.3%); and one patient committed suicide (0.3%) (Figure 3).

Ten of 66 patients (3.3% of all treated) temporarily interrupted the therapy due to adverse events (AEs), namely, COVID-19 infection (n = 2; 0.7%), and the following were observed in single patients: bronchopneumonia, upper respiratory tract infection, nonspecific influenza-like illness, nephritis, nonspecific urethritis, squamous cell carcinoma of the skin, latent tuberculosis infection, and neurological disorder.

Permanent discontinuation due to AEs was in 5 of 66 patients: squamous cell carcinoma of the skin (n = 1), lung carcinoma (n = 1), severe bronchopneumonia (n = 1), skin rash (n = 1), and not identified event (n = 1) (Table 2).

The mean duration of adalimumab treatment was 2.3 years (SD 1.7) for all analysed patients. In patients who discontinued the treatment, the mean duration was 1.7 years (SD 1.4). The mean duration of treatment in treated patients was 2.4 years (SD 1.8).

3.4. Drug Survival of Adalimumab

The persistence on adalimumab treatment was assessed using the Kaplan–Meier survival estimates. Adalimumab persistence rates were 92.5%, 80.5%, 71.0%, and 66.7% after 12, 24, 36, and 48 months of treatment, respectively (Figure 4(a)).

(a)

(b)

(c)

Survival estimates were also analysed according to the smoking status: patients, who never smoked and those, who were currently smoking or previously smoked. No statistically significant differences were observed between these two groups () (Figure 4(b)). For nonsmokers the persistence rates were 91.2% after 12 months of treatment, 84.5% after 24 months, and 80.4% after 36 and 48 months of treatment. For smokers and ex-smokers, the persistence rates were 93.3%, 80.0%, 69.2%, and 64.0% after 12, 24, 36, and 48 months of treatment, respectively.

The persistence on treatment was also analysed by the BMI category: patients with normal BMI (BMI ≤ 25) and patients with overweight or obese patients (BMI > 25). The persistence rates using the Kaplan–Meier method showed lower survival in overweight or obese patients, although the difference was not statistically significant () (Figure 4(c)). The persistence rates were 95.9%, 85.7%, 75.0%, and 71.3% for patients with normal BMI after 12, 24, 36, and 48 months of treatment; and 91.8%, 79.4%, 70.2%, and 65.6% for patients with overweight or obese patients.

3.5. Adalimumab Safety Profile

A total of 24 (8.0%) adverse events were reported (Table 2). The most frequently recorded were infections (4.7%). Malignancies were reported in 1.0% and skin disorders in 1.3%. One percent of AEs was cholangitis (0.3%), cerebrovascular disease (0.3%), and latent tuberculosis (0.3%). Serious AEs included 3 of 14 reported infections (1.0%) and 1 of 3 reported malignancies (0.3%).

4. Discussion

The results of this multicenter retrospective study demonstrate the effectiveness and safety of adalimumab in the real-world setting.

The analysis of the demographic data showed higher percentage of male patients in our cohort (55%) similarly to other study confirming the fact, that men have increased disease severity [18].

The long duration of disease before initiation of biologic therapy (9.1 years) pose a problem in HS likewise to other chronic inflammatory skin diseases, including psoriasis, moreover a common feature is diagnostic delay in HS and the average interval from self-reported onset of symptoms to diagnosis is 7.2 years [19].

In our cohort, approximately 80% of the patients were active smokers or ex-smokers, which is in accordance to the meta-analysis [20] reporting that patients with HS are about 4 times (OR, 4.26) more likely to be smokers. However, our cohort shows even higher percentage of smokers when compared to the other HS registries [21]. This has proven to be unsurprising, as it correlates with the fact that the Czech Republic is among the 7 countries in the world with the highest amounts of cigarettes smoked per person [22].

The IHS4 severity score is recognized as simple and practical validation system which was adapted for daily practice and has been used in several clinical trials [16, 23, 24]. We used this scoring system to assess therapeutical response in our cohort.

During the adalimumab treatment, there was a substantial reduction in number of abscesses, nodules and draining fistulas, IHS4 and DLQI scores. The proportion of patients with severe IHS4 dropped from 249 (83.3%) at initial baseline to 65 (30.1%) after 12 months; this trend was maintained up to the 48^th month. The results are comparable to the response observed in the SOLACE and OLE study, which also collected real-world data [12, 25]. To our knowledge, our study offers real-world data with the longest mean duration of treatment of 2.3 years, and a maximum treatment period of 48 months. In most of patient cases, the clinical response to adalimumab has been sustained. The long-term response in our cohort may be also explained by the slightly improvement of patients BMI levels during the treatment. It has been proven that elevated BMI in HS is associated with decreased response to adalimumab therapy [26].

Adalimumab persistence rates in our cohort were 92.5%, 80.5%, 71.0%, and 66.7% after 12, 24, 36, and 48 months of treatment, respectively, which was higher than in other one-center study with a median survival probability of 74.1% after one year [27].

Survival estimates were also analysed according to the smoking status and BMI. Although no statistically significant differences were observed, there was observable better treatment persistence in patients who never smoked contrast to those who were smokers or ex-smokers. The difference was also observed between obese and nonobese patients.

Adalimumab discontinuation occurred in 22.1% of patients, with the main reason being loss of treatment efficacy.

The safety profile of adalimumab in the analysed group of patients was good and in accordance with other real-world data [28]. A total of 8.0% AEs were reported. The most frequent mild AEs were infections (4.7%) and skin disorders (1.3%); the serious AEs included severe infections (1%) and malignancies (0.3%).

The limitations of our study include its retrospective design and the absence of a control group, which is typical in studies that use realworld data. Under discussion could also be the evaluation of efficacy with IHS4 only. IHS4 was recognized as validated and simple to use scoring system for clinical research and daily practice (14). In addition, the correlation between IHS4 and Hidradenitis Suppurativa Clinical Response (HiSCR) was described by Caposiena and Gulliver (12, 27). Notwithstanding these limitations, our study is the long follow-up period with a large number of patients in a real-world and provide evidence that adalimumab achieves IHS4 and DLQI improvement with some sustainability of response.

Data Availability

The data used to support the findings of this study are available from the corresponding author upon request.

Conflicts of Interest

AS, EM, and DS declare, that they have nothing to disclose. MK has served as consultants, speakers, or investigators for Abbvie, Amgen, Eli-Lilly, Janssen, Leo Pharma, Novartis, Pfizer, Sanofi, and UCB. PA has served as consultant, speaker, or investigator for Abbvie, Amgen, BMS, Eli Lilly, Janssen, Leo Pharma, L´Oréal, MSD, Novartis, Pfizer, Pierre Fabre, Sanofi and UCB. JF has served as consultants, speakers, or investigators for Abbvie, Amgen, Eli-Lilly, Janssen, Leo Pharma, Novartis, Pfizer, Sanofi, and UCB. MA received honoraria from Abbvie, MSD, BMS, Novartis, L´Oréal, and Pierre Fabre.

Acknowledgments

The authors wish to thank all of the dermatologists and collaborators who participated in the creation of BIOREP for their efforts and dedication to the project. The authors would also like to thank BIOREP Group Members: Zdenek Antal, Petr Arenberger, Jirina Bartonova, Linda Blahova, Petra Brodska, Petra Cetkovska, Martin Cetkovsky, Dominika Diamantova, Olga Filipovska, Petra Gkalpakioti, Spyridon Gkalpakiotis, Martina Grycova, Jiri Horazdovsky, Katerina Hrazdirova, Eduard Hrncir, Hana Janatova, Jaromira Janku, Renata Kopova, Dora Kovandova, Iva Lomicova, Alena Machovcova, Hana Malikova, Miroslav Necas, Helena Nemcova, Jitka Osmerova, Zuzana Plzakova, Marie Policarova, Tomas Pospisil, Miloslav Salavec, Ivana Strouhalova, David Stuchlik, Alena Stumpfova, Jaroslav Sevcik, Jan Sternbersky, Jiri Stork, Katerina Svarcova, Katerina Tepla, Martin Tichy, Yvetta Vantuchova, and Ivana Vejrova. This work was supported by the Cooperatio 39-Oncology and hematology, Charles University grant.

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Copyright © 2023 Alzbeta Smetanova et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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