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Table of Contents
ORIGINAL ARTICLE
Year : 2022  |  Volume : 40  |  Issue : 2  |  Page : 94-99

The seroconversion rate of QuantiFERON-TB gold in-tube test in psoriatic patients receiving anti-interleukin-23 monoclonal antibodies


1 Department of Dermatology, National Taiwan University Hospital, Taipei, Taiwan
2 Department of Dermatology, National Taiwan University Hospital; Department of Dermatology, College of Medicine, National Taiwan University, Taipei, Taiwan

Date of Submission21-Sep-2021
Date of Decision18-Mar-2022
Date of Acceptance22-Mar-2022
Date of Web Publication29-Jun-2022

Correspondence Address:
Dr. Tsen-Fang Tsai
Department of Dermatology, National Taiwan University Hospital, Taipei; Department of Dermatology, College of Medicine, National Taiwan University, Taipei
Taiwan
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ds.ds_18_22

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  Abstract 


Background: Biologic therapies have become the gold standard for the treatment of moderate-to-severe psoriasis and psoriatic arthritis. However, concerns for opportunistic infections exist, especially for tuberculosis (TB) in endemic areas. Previously, tumor necrosis factor inhibitors were reported to carry higher risks of latent TB infection (LTBI) reactivation or new active TB, followed by anti-interleukin (IL)-12/23 and IL-17 agents in Taiwan. Objectives: The objective of the study is to provide real-world clinical rate of seroconversion of serial QuantiFERON-TB gold in-tube (QFT-GIT) tests, for detection of LTBI and newly-acquired TB, in psoriasis patients while receiving IL-23 inhibitors in an intermediate TB burden country. Methods: The local risk management plan required regular monitoring of TB while receiving biologics for psoriasis. This retrospective cohort evaluated consecutive psoriasis patients who received guselkumab or risankizumab between 2015 and 2021 in a tertiary referral center in Taiwan. Results: A total of 144 patients were included, with negative baseline QFT-GIT in 88% and positive in 13%. After receiving at least 6 months of anti-IL-23 drugs, persistently seropositive was found in 15 patients (10%), persistently seronegative in 125 patients (87%), seroconversion in 1 patient (0.6%), and seroreversion in 3 patients (1.9%). The seroconversion rate was 1% (1/127) in individuals under anti-IL-23 medications for at least 12 months. No case of LTBI reactivation was identified. Conclusion: In psoriasis patients under anti-IL-23 therapy, serial interferon-gamma release assays demonstrated a low seroconversion rate (<1%). Anti-IL-23 agents may be a favorable choice for psoriasis patients with a higher risk of TB infection and LTBI reactivation or those who reside in endemic regions.

Keywords: Anti-interleukin-23, guselkumab, interferon-gamma release assays, latent tuberculosis infection, QuantiFERON-TB gold in-tube test, risankizumab, Taiwan, tuberculosis


How to cite this article:
Huang YW, Tsai TF. The seroconversion rate of QuantiFERON-TB gold in-tube test in psoriatic patients receiving anti-interleukin-23 monoclonal antibodies. Dermatol Sin 2022;40:94-9

How to cite this URL:
Huang YW, Tsai TF. The seroconversion rate of QuantiFERON-TB gold in-tube test in psoriatic patients receiving anti-interleukin-23 monoclonal antibodies. Dermatol Sin [serial online] 2022 [cited 2022 Dec 7];40:94-9. Available from: https://www.dermsinica.org/text.asp?2022/40/2/94/349023




  Introduction Top


Biologics have become the treatment choices for patients with moderate to severe psoriasis. Current biologics approved for psoriasis include anti-interleukin (IL)-12/23 antibody, anti-IL-17 or anti-IL-17A, anti-IL-23 agents, and tumor necrosis factor-α (TNF-α) inhibitors. Guselkumab and risankizumab are immunoglobulin G1 monoclonal antibodies that inhibit IL-23 by selectively binding to its p19 subunit.[1],[2]

Biological agents showed favorable efficacy and safety profiles in clinical trials.[3] However, screening and monitoring for tuberculous infection and viral hepatitis are required during clinical trials and often in clinical practice.[4],[5],[6],[7] Anti-IL-23 agents were found to be better than the other drugs with respect to safety in a meta-analysis of pivotal trials.[8] However, meta-analysis results do not reliably reflect the real safety of biologics in psoriasis,[9] and real-world data are still needed to validate the safety. For example, tuberculosis (TB), especially reactivation of latent TB infection (LTBI), is an important safety concern due to its high prevalence in some countries, but pivotal studies of biologics enrolled patients mainly from low TB burden countries.[10],[11]

The use of TNF-α inhibitors is associated with an increased risk of LTBI reactivation, while the risk is lower for IL-17 and 23 inhibitors.[11],[12] Previous studies of TNF-α inhibitors reported an annual seroconversion rate of serial QuantiFERON-TB gold in-tube (QFT-GIT) tests between 0.38% and 18% in psoriatic patients,[13],[14],[15],[16],[17],[18] and the data from Taiwan were 14.29%.[19] A retrospective analysis of ustekinumab, an IL-12/23 inhibitor, showed a lower seroconversion rate at 7.3%.[20] The risk of LTBI was reported to be lower in IL-17 and IL-23 antagonists.[11] TB screening before biologic therapy is recommended by several guidelines and consensuses, but the need for subsequent monitoring is variable.[21],[22],[23] For IL-17 monoclonal antibodies, there was no case of reactivated LTBI detected during the long-term follow-up up to 52 weeks in a pooled analysis of phase II and phase III clinical studies of secukinumab.[24] The postmarketing study demonstrated seroconversion to be 1.3% in patients with at least 11 months of cumulative exposure to secukinumab or ixekizumab in Taiwan.[25]

Puig et al. reported the safety of guselkumab in psoriasis patients with latent TB, and no cases of active TB, including reactivation of LTBI, were documented up to 2 years of treatment.[26] This study evaluates the real-world experience of QFT-GIT status in Taiwanese patients with psoriasis treated with anti-IL-23 monoclonal antibodies, including guselkumab and risankizumab.


  Materials and Methods Top


Patients

All consecutive psoriasis patients who had received anti-IL-23 agents for at least 6 months with serial QFT-GIT tests who visited our clinic between March 2015 and June 2021 were enrolled. According to the local risk management plan in Taiwan, baseline QFT-GIT was required before the initiation of biologics which will be repeated at least once annually during biological treatment. The baseline QFT-GIT was defined as the latest test result before the initiation of anti-IL-23 therapies. The latest result of QFT-GIT test during the treatment course was recorded, defining the follow-up result. The duration of anti-IL-23 therapy was retrieved from the medical records, and patients with <6 months of IL-23 inhibitors exposure were excluded. The study has been approved by the Research Ethics Committee of National Taiwan University Hospital (201904124RINC).

The immediately-before (1 month before the observed period) and concurrent systemic therapies during IL-23 inhibitors were documented, including cyclosporine, methotrexate, nonsteroidal anti-inflammatory agents (NSAIDs), leflunomide, sulfasalazine, corticosteroid, or other target agents (tofacitinib, etanercept, adalimumab, ustekinumab, golimumab, ixekizumab, and secukinumab).

QuantiFERON-TB gold in-tube for latent tuberculosis infection

QFT-GIT tests were performed in all the patients in this cohort to evaluate the status of TB infection. QFT-GIT contained three peptide antigens, mycobacterial proteins TB7.7, ESAT-6, and CFP-10(p4). The values of interferon-γ (IFN-γ) were calculated by subtracting the obtained value with nil antigens. A positive result was defined as IFN-γ ≥0.35 IU/ml. A positive control (mitogen) was defined as value ≥0.5 IU/ml and negative result as 0 < IFN-γ <0.35 IU/ml. IFN-γ of nil antigen >8 IU/ml or positive control value <0.5 IU/ml was defined as indeterminate result.

The primary outcomes, in reference to the baseline and the follow-up QFT-GIT results, are divided into four categories, persistent positive, persistent negative, seroconversion, and seroreversion. Seroconversion refers to the QFT-GIT result turning negative to positive, while seroreversion refers to a negative QFT-GIT result during follow-up despite a positive baseline test.

Statistical analysis

Statistical analysis was performed using Microsoft Excel 2016 (Microsoft Corporation, Seattle, WA, USA). Fisher exact test was applied for group comparisons. Statistical significance was defined as P < 0.05. Fisher exact test was applied for groups comparison. Significance statistical results were defined as P < 0.05.


  Results Top


Patient characteristics

[Table 1] presents the characteristics of the cohort. A total of 144 individuals were enrolled, including 119 receiving guselkumab and 25 receiving risankizumab. The mean age was 49.5 years old (standard deviation [SD] 13.2 years), with a female-to-male ratio of 25/119. Psoriatic arthritis was noted in 56 (39%) patients, and a history of erythroderma was documented in 24 (17%). The follow-up duration ranged from 6.0 to 77.1 months (mean 26.5 months, median 19.2 months; SD 17.6 months), with cumulative exposure to anti-IL-23 therapy at 3819 person-months. 127 (88%) patients were treated with anti-IL-23 therapy for more than 1 year. Most (81%) of the patients had failed to reach adequate response to at least one of the following biologic agents: etanercept, adalimumab, secukinumab, ixekizumab, brodalumab, ustekinumab. Twenty-seven patients (19%) were biologic-naïve. Immediately-before treatment with systemic or biologic therapy was found in 42% of the patients, and concomitant therapy was given in 17%. Among 61 patients with immediately-before therapy, methotrexate (n = 29) was the most commonly prescribed medication. NSAID was the most frequent concurrent medication during anti-IL-23 therapy, found in 14 out of 25 patients with concomitant medication.
Table 1: Demographics and final outcomes of patients receiving anti-interleukin-23 therapy

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QuantiFERON-TB gold in-tube results and primary outcomes

[Table 1] summarizes the primary outcomes, and a flow chart with baseline and follow-up QFT-GIT results were shown in [Figure 1]. At baseline, 126 patients (88%) and 18 patients (13%) showed negative and positive results, respectively. All the seropositive patients initiated prophylactic therapy before or received starting biologic treatment, and biologics were given concomitantly during the treatment course. Isoniazid was given for 9 months. The duration between baseline and follow-up QFT-GIT was 12–65 months. The primary outcomes showed constant seropositive in 15 patients (10%), constant seronegative in 125 patients (87%), seroconversion in one patient (1%), and seroreversion in three patients (2%). In patients with at least 1 year of exposure to anti-IL-23 therapy, the seroconversion rate was 1% (1/127). Seroconversion was observed in one patient after 6 months of exposure to guselkumab.
Figure 1: Results of serial QuantiFERON-TB gold in-tube tests in patients receiving anti-interleukin-23 drugs, guselkumab and risankizumab.

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A subanalysis of patients with or without concomitant therapy, with or without immediately-before treatment, and biologic-naïve or not were performed to determine if these characteristics are significantly different between the persistently seronegative group and seroconversion group. However, none of the P values reach a significant level, as shown in [Table 2].
Table 2: Comparison of persistently seronegative group and seroconversion group

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  Discussion Top


IL-23 induces proliferation, maturation, and maintenance of Th17 cells, playing critical roles in the immunopathogenesis of psoriasis.[27] Biological medications targeting anti-IL-23, including guselkumab, risankizumab, tildrakizumab, and mirikizumab, effectively clear psoriatic lesions.[28] Although the inhibition of critical immune mediators may elevate the risk of infections, the safety profiles of anti-IL-23 agents are generally more favorable than anti-IL-17 agents.[29]

Previous Taiwanese studies showed seroconversion rates of psoriasis patients receiving TNF-α inhibitors, ustekinumab, and IL-17 inhibitors as 14.29%, 7.3%, and 1.3%, respectively.[19],[20],[25] This study further confirms the low risk of TB for anti-IL-23 agents in Taiwan.

In terms of TB, TNF has an important function in granuloma formation, and TNF inhibitors may disrupt the granuloma formation, thus rendering patients a higher TB rate.[30] As for IL-23, its role in TB is less explored. In vitro studies have established that IL-23 is critical for the Th17 pathway, which induces immunologic cascades that respond to infection with Mycobacterium TB.[31],[32] In prior studies, IL-23 promotes multifunctional CD4 T cell responses after immunization with the Mycobacterium TB subunit vaccine H1 DDA/TDB independently of IL-17A.[33] IL-12-and IL-23-dependent induction of IFN-γ is associated with the immunity to mycobacteria.[34] However, data from clinical trials and real-world practice found a low risk of TB. No cases of reactivation of LTBI or active TB were reported during guselkumab therapy for up to 2 years.[26] Two cases of LTBI were reported in the risankizumab group in the pivotal phase III studies (UltIMMA-1 and UltIMMA-2).[35] In a pooled analysis of nine phase II and phase III clinical trials, there were eight events (0.4/100 person-year) of LTBI.[36] In the IMMhance study, none of the 31 patients with latent TB became active TB during a follow-up period of 55 weeks despite not receiving anti-TB medication.[37]

Routine pretreatment LTBI and subsequent annual interferon-gamma release assays (IGRA) testing remained to be recommended in current practice.[21],[22],[23] Based on the observation that IL-23 inhibitors demonstrated a relatively lower TB risk compared to TNF-α inhibitors, pretreatment screening and yearly testing afterward for LTBI only for patients with high risk and at the discretion of the dermatologist was suggested in a recently revised joint guideline.[38] Recently, some experts advocated time for this paradigm change.[11] The benefits of using TB prophylactic medication have to be balanced with the risk of toxicity of anti-TB medication and the possibility of drug-resistant TB.

Seroconversion of QFT-GIT was observed in only one patient in our study, which was documented after 6 months of exposure to guselkumab. The TB antigen increased from 0.275 to 0.49 IU/mL. This 63-year-old man had been diagnosed with psoriasis for 32 years. He had received multiple systemic therapies, including acitretin, methotrexate, phototherapy, and ustekinumab. He received methotrexate 1 month before the initiation of guselkumab, but there was no concomitant medication. He denied a contact history with a person with TB. Chest X-ray showed normal findings, and sputum culture yielded a negative result. A 9-month isoniazid (INH) therapy for LTBI was subsequently given. As for patients in the persistently seropositive group, all patients in our study received INH therapy before IL-23 inhibitor initiation, and the subsequent treatment showed no evidence of active TB.

Seroreversion of QFT-GIT tests was common in psoriasis under biological therapy. In one report of 11 years of follow-up, QFT-GIT results converted from positive to negative in 34 (39.5%) of 86 patients after starting biologic therapy, especially in patients treated with TNF-α inhibitors and in patients who received INH.[39] Previously, seroreversion of QFT-GIT tests was reported in 17 (56.7%) of 30 patients after 8 months of anti-TB medication.[40] In our report, three patients (1.9%) showed seroreversion, with TB antigen decreasing from 2.30 to 0.406, 0.459 to 0.266, and 2.86 to 0.23 IU/mL, which may be explained by the effective prior anti-TB treatment.[41]

The retrospective nature, lack of control group, and the background intermediate TB burden limit generalizability of our findings. Although QFT-GIT tests are widely used, false-negative results have been reported.[42] Additional data from higher TB burden countries is needed to elucidate the impact of IL-23 inhibitors on the risk of TB.


  Conclusions Top


Serial IGRAs in psoriasis patients using IL-23 inhibitors showed a low seroconversion rate (1%) in Taiwan. Compared to TNF-α inhibitors and anti-IL-12/23 agents, anti-IL-23 antibodies carry a minor risk of TB infection and LTBI reactivation for psoriatic patients receiving biologic treatment. The need for serial QFT-GIT tests may be reexamined in patients receiving an-IL-23 inhibitors.

Financial support and sponsorship

Nil.

Conflicts of interest

Dr. Tsai has conducted clinical trials and has received honoraria for serving as a consultant or speaking fee for Pfizer Ltd, Serono International SA (now Merck Serono International SA), UniPharma/Biogen Idec, Galderma, Celgene, Novartis Pharmaceuticals Corp, Janssen-Cilag Pharmaceutica, and AbbVie. Also, an editorial board member at Dermatologica Sinica, had no role in the peer review process of or decision to publish this article. The other author declared no conflicts of interest in writing this paper.



 
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