Clinical and Ultrasonographic Characterization of Hidradenitis Suppurativa in Female Patients: Impact of Early Recognition of the Disease
Abstract
:1. Introduction
2. Patients and Methods
3. Results
3.1. Total Population
3.2. Patients with Early- vs. Adult-Onset HS
Clinical Features
3.3. Treatment Approach
3.4. Ultrasonographic Features
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Zouboulis, C.C.; del Marmol, V.; Mrowietz, U.; Prens, E.P.; Tzellos, T.; Jemec, G.B. Hidradenitis Suppurativa/Acne Inversa: Criteria for Diagnosis, Severity Assessment, Classification and Disease Evaluation. Dermatology 2015, 231, 184–190. [Google Scholar] [CrossRef]
- Nguyen, T.V.; Damiani, G.; Orenstein, L.A.V.; Hamzavi, I.; Jemec, G.B. Hidradenitis suppurativa: An update on epidemiology, phenotypes, diagnosis, pathogenesis, comorbidities and quality of life. J. Eur. Acad. Dermatol. Venereol. 2021, 35, 50–61. [Google Scholar] [CrossRef]
- Morss, P.; Porter, M.; Savage, K.; Santillan, M.R.; Giannotti, N.; Kimball, A. Investigating race and gender in age at onset of hidradenitis suppurativa. J. Eur. Acad. Dermatol. Venereol. 2020, 34, e139–e141. [Google Scholar] [CrossRef] [PubMed]
- Sabat, R.; Jemec, G.B.E.; Matusiak, Ł.; Kimball, A.B.; Prens, E.; Wolk, K. Hidradenitis suppurativa. Nat. Rev. Dis. Primers 2020, 6, 18. [Google Scholar] [CrossRef]
- Abu Rached, N.; Gambichler, T.; Ocker, L.; Dietrich, J.W.; Quast, D.R.; Sieger, C.; Seifert, C.; Scheel, C.; Bechara, F.G. Screening for Diabetes Mellitus in Patients with Hidradenitis Suppurativa—A Monocentric Study in Germany. Int. J. Mol. Sci. 2023, 24, 6596. [Google Scholar] [CrossRef]
- Cuenca-Barrales, C.; Montero-Vilchez, T.; Krajewski, P.K.; Szepietowski, J.C.; Matusiak, L.; Arias-Santiago, S.; Molina-Leyva, A. Sexual Dysfunction and Quality of Life in Patients with Hidradenitis Suppurativa and Their Partners. Int. J. Environ. Res. Public Health 2022, 20, 389. [Google Scholar] [CrossRef]
- Özkur, E.; Karadağ, A.S.; Üstüner, P.; Aksoy, B.; Eşme, P.; Çalışkan, E.; Akoğlu, G.; Kalkan, G.; Demirseren, D.D.; Polat, M.; et al. Clinical and demographic features of hidradenitis suppurativa: A multicentre study of 1221 patients with an analysis of risk factors as-sociated with disease severity. Clin. Exp. Dermatol. 2021, 46, 532–540. [Google Scholar] [CrossRef]
- Bettoli, V.; Ricci, M.; Zauli, S.; Virgili, A. Hidradenitis suppurativa-acne inversa: A relevant dermatosis in paediatric patients. Br. J. Dermatol. 2015, 173, 1328–1330. [Google Scholar] [CrossRef]
- Molina-Leyva, A.; Cuenca-Barrales, C. Adolescent-Onset Hidradenitis Suppurativa: Prevalence, Risk Factors and Disease Features. Dermatology 2019, 235, 45–50. [Google Scholar] [CrossRef] [PubMed]
- Dessinioti, C.; Tzanetakou, V.; Zisimou, C.; Kontochristopoulos, G.; Antoniou, C. A retrospective study of the characteristics of patients with early-onset compared to adult-onset hidradenitis suppurativa. Int. J. Dermatol. 2018, 57, 687–691. [Google Scholar] [CrossRef] [PubMed]
- Braunberger, T.L.; Nicholson, C.L.; Gold, L.; Do, A.F.N.; Jacobsen, G.; Parks-Miller, A.; Hamzavi, I.H. Hidradenitis suppurativa in children: The Henry Ford experience. Pediatr. Dermatol. 2018, 35, 370–373. [Google Scholar] [CrossRef]
- Vaiopoulos, A.G.; Nikolakis, G.; Zouboulis, C.C. Hidradenitis suppurativa in paediatric patients: A retrospective monocentric study in Germany and review of the literature. J. Eur. Acad. Dermatol. Venereol. 2020, 34, 2140–2146. [Google Scholar] [CrossRef]
- Offidani, A.; Molinelli, E.; Sechi, A.; Brisigotti, V.; Campanati, A.; Raone, B.; Neri, I.; Patrizi, A. Hidradenitis suppurativa in a prepubertal case series: A call for specific guidelines. J. Eur. Acad. Dermatol. Venereol. 2019, 33 (Suppl. 6), 28–31. [Google Scholar] [CrossRef]
- Abu Rached, N.; Gambichler, T.; Dietrich, J.W.; Ocker, L.; Seifert, C.; Stockfleth, E.; Bechara, F.G. The Role of Hormones in Hidradenitis Suppurativa: A Systematic Review. Int. J. Mol. Sci. 2022, 23, 15250. [Google Scholar] [CrossRef] [PubMed]
- Deckers, I.E.; van der Zee, H.H.; Boer, J.; Prens, E.P. Correlation of early-onset hidradenitis suppurativa with stronger genetic sus-ceptibility and more widespread involvement. J. Am. Acad. Dermatol. 2015, 72, 485–488. [Google Scholar] [CrossRef]
- Rosi, E.; Fastame, M.T.; Scandagli, I.; Di Cesare, A.; Ricceri, F.; Pimpinelli, N.; Prignano, F. Insights into the Pathogenesis of HS and Therapeutical Approaches. Biomedicines 2021, 9, 1168. [Google Scholar] [CrossRef] [PubMed]
- Gierek, M.; Kitala, D.; Łabuś, W.; Szyluk, K.; Niemiec, P.; Ochała-Gierek, G. Impact of Hidradenitis Suppurativa Surgical Treatment on Health-Related Life Quality. J. Clin. Med. 2022, 11, 4327. [Google Scholar] [CrossRef] [PubMed]
- Organization for Economic Co-Operation and Development (OECD). The Heavy Burden of Obesity: The Economics of Prevention; Country Note to the Report the Heavy Burden of Obesity: Italy; OECD Health Policy Studies, OECD Publishing: Paris, France, 2019. [Google Scholar]
- Kurzen, H.; Kurzen, M. Secondary prevention of hidradenitis suppurativa. Dermatol. Rep. 2019, 11, 8243. [Google Scholar] [CrossRef]
- Molinelli, E.; Brisigotti, V.; Campanati, A.; Sapigni, C.; Giacchetti, A.; Cota, C.; Offidani, A. Efficacy of oral zinc and nicotinamide as maintenance therapy for mild/moderate hidradenitis suppurativa: A controlled retrospective clinical study. J. Am. Acad. Dermatol. 2020, 83, 665–667. [Google Scholar] [CrossRef]
- Choi, F.; Lehmer, L.; Ekelem, C.; Mesinkovska, N.A. Dietary and metabolic factors in the pathogenesis of hidradenitis suppurativa: A systematic review. Int. J. Dermatol. 2020, 59, 143–153. [Google Scholar] [CrossRef]
- Wortsman, X. Strong validation of ultrasound as an imaging biomarker in hidradenitis suppurativa. Br. J. Dermatol. 2021, 184, 591–592. [Google Scholar] [CrossRef]
- Wortsman, X.; Rodriguez, C.; Lobos, C.; Eguiguren, G.; Molina, M.T. Ultrasound Diagnosis and Staging in Pediatric Hidradenitis Suppurativa. Pediatr. Dermatol. 2016, 33, e260–e264. [Google Scholar] [CrossRef]
- Wortsman, X.; Moreno, C.; Soto, R.; Arellano, J.; Pezo, C.; Wortsman, J. Ultrasound in-depth characterization and staging of hid-radenitis suppurativa. Dermatol. Surg. 2013, 39, 1835–1842. [Google Scholar] [CrossRef] [PubMed]
- Caposiena Caro, R.D.; Solivetti, F.M.; Bianchi, L. Power Doppler ultrasound assessment of vascularization in hidradenitis suppura-tiva lesions. J. Eur. Acad. Dermatol. Venereol. 2018, 32, 1360–1367. [Google Scholar] [CrossRef] [PubMed]
- Kokolakis, G.; Wolk, K.; Schneider-Burrus, S.; Kalus, S.; Barbus, S.; Gomis-Kleindienst, S.; Sabat, R. Delayed Diagnosis of Hidradenitis Suppurativa and Its Effect on Patients and Healthcare System. Dermatology 2020, 236, 421–430. [Google Scholar] [CrossRef] [PubMed]
- Loget, J.; Saint-Martin, C.; Guillem, P.; Kanagaratnam, L.; Becherel, P.A.; Nassif, A.; Fougerousse, A.C.; Siham, M.; Girard, C.; Barthelemy, H.; et al. Misdiagno-sis of hidradenitis suppurativa continues to be a major issue. The R-ENS Verneuil study. Ann. Dermatol. Venereol. 2018, 145, 331–338. [Google Scholar] [CrossRef] [PubMed]
- Saunte, D.; Boer, J.; Stratigos, A.; Szepietowski, J.; Hamzavi, I.; Kim, K.; Zarchi, K.; Antoniou, C.; Matusiak, L.; Lim, H.; et al. Diagnostic delay in hidradenitis suppurativa is a global problem. Br. J. Dermatol. 2015, 173, 1546–1549. [Google Scholar] [CrossRef]
- Di Cesare, A.; Nikolakis, G.; Kanni, T.; Giamarellos-Bourboulis, E.J.; Matusiak, L.; Szepietowski, J.C.; Zouboulis, C.C.; Prignano, F. Iden-tification of clinical features affecting diagnostic delay in paediatric hidradenitis suppurativa: Results from a multicentre obser-vational study. Br. J. Dermatol. 2022, 187, 428–430. [Google Scholar] [CrossRef]
- Cuenca-Barrales, C.; Montero-Vílchez, T.; Szepietowski, J.; Matusiak, L.; Molina-Leyva, A. Sexual impairment in patients with hidradenitis suppurativa: A systematic review. J. Eur. Acad. Dermatol. Venereol. 2021, 35, 345–352. [Google Scholar] [CrossRef]
- Marzano, A.V.; Genovese, G.; Casazza, G.; Moltrasio, C.; Dapavo, P.; Micali, G.; Sirna, R.; Gisondi, P.; Patrizi, A.; Dini, V.; et al. Evidence for a ‘window of opportunity’ in hidradenitis suppurativa treated with adalimumab: A retrospective, real-life multicentre cohort study. Br. J. Dermatol. 2021, 184, 133–140. [Google Scholar] [CrossRef]
- Garg, A.; Neuren, E.; Cha, D.; Kirby, J.S.; Ingram, J.R.; Jemec, G.B.; Esmann, S.; Thorlacius, L.; Villumsen, B.; del Marmol, V.; et al. Evaluating patients’ unmet needs in hidradenitis suppurativa: Results from the Global Survey Of Impact and Healthcare Needs (VOICE) Project. J. Am. Acad. Dermatol. 2020, 82, 366–376. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Garg, A.; Neuren, E.; Strunk, A. Hidradenitis Suppurativa Is Associated with Polycystic Ovary Syndrome: A Population-Based Analysis in the United States. J. Investig. Dermatol. 2018, 138, 1288–1292. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Phan, K.; Charlton, O.; Smith, S.D. Hidradenitis suppurativa and polycystic ovarian syndrome: Systematic review and me-ta-analysis. Australas J. Dermatol. 2020, 61, e28–e33. [Google Scholar] [CrossRef] [PubMed]
- Lewis, F.; Messenger, A.G.; Wales, J. Hidradenitis suppurativa as a presenting feature of premature adrenarche. Br. J. Dermatol. 1993, 129, 447–448. [Google Scholar] [CrossRef]
- Rosi, E.; Fastame, M.T.; Silvi, G.; Guerra, P.; Nunziati, G.; Di Cesare, A.; Scandagli, I.; Ricceri, F.; Prignano, F. Hidradenitis Suppurativa: The Influence of Gender, the Importance of Trigger Factors and the Implications for Patient Habits. Biomedicines 2022, 10, 2973. [Google Scholar] [CrossRef]
- Bukvić Mokos, Z.; Miše, J.; Balić, A.; Marinović, B. Understanding the Relationship Between Smoking and Hidradenitis Suppurati-va. Acta Dermatovenerol. Croat. 2020, 28, 9–13. [Google Scholar]
- Garg, A.; Papagermanos, V.; Midura, M.; Strunk, A. Incidence of hidradenitis suppurativa among tobacco smokers: A popula-tion-based retrospective analysis in the U.S.A. Br. J. Dermatol. 2018, 178, 709–714. [Google Scholar] [CrossRef] [Green Version]
- Balgobind, A.; Finelt, N.; Strunk, A.; Garg, A. Association between obesity and hidradenitis suppurativa among children and ado-lescents: A population-based analysis in the United States. J. Am. Acad. Dermatol. 2020, 82, 502–504. [Google Scholar] [CrossRef] [Green Version]
- Gierek, M.; Ochała-Gierek, G.; Kitala, D.; Łabuś, W.; Bergler-Czop, B. Hidradenitis suppurativa: Bacteriological study in surgical treatment. Adv. Dermatol. Allergol. 2022, 39, 1101–1105. [Google Scholar] [CrossRef]
- Rosi, E.; Pescitelli, L.; Ricceri, F.; Di Cesare, A.; Novelli, A.; Pimpinelli, N.; Prignano, F. Clindamycin as unique antibiotic choice in Hid-radenitis Suppurativa. Dermatol. Ther. 2019, 32, e12792. [Google Scholar] [CrossRef]
- Molinelli, E.; De Simoni, E.; Candelora, M.; Sapigni, C.; Brisigotti, V.; Rizzetto, G.; Offidani, A.; Simonetti, O. Systemic Antibiotic Therapy in Hidradenitis Suppurativa: A Review on Treatment Landscape and Current Issues. Antibiotics 2023, 12, 978. [Google Scholar] [CrossRef]
- Bettoli, V.; Manfredini, M.; Massoli, L.; Carillo, C.; Barozzi, A.; Amendolagine, G.; Ruina, G.; Musmeci, D.; Libanore, M.; Curtolo, A.; et al. Rates of antibiotic resistance/sensitivity in bacterial cultures of hidradenitis sup-purativa patients. J. Eur. Acad. Dermatol. Venereol. 2019, 33, 930–936. [Google Scholar] [CrossRef] [PubMed]
- Nazzaro, G.; Passoni, E.; Calzari, P.; Barbareschi, M.; Muratori, S.; Vearldi, S.; Marzano, A.V. Color Doppler as a tool for correlating vascularization and pain in hidradenitis suppurativa lesions. Ski. Res. Technol. 2019, 25, 830–834. [Google Scholar] [CrossRef]
- Crisan, D.; Wortsman, X.; Alfageme, F.; Catalano, O.; Badea, A.; Scharffetter-Kochanek, K.; Sindrilaru, A.; Crisan, M. Ultrasonography in dermatologic surgery: Revealing the unseen for improved surgical planning. JDDG J. Der Dtsch. Dermatol. Ges. 2022, 20, 913–926. [Google Scholar] [CrossRef] [PubMed]
- Caro, R.D.C.; Solivetti, F.M.; Candi, E.; Bianchi, L. Clinical and Power-Doppler ultrasound features related with persistence of fistulous tracts under treatment with adalimumab in hidradenitis suppurativa: 4 years of follow-up. Dermatol. Ther. 2021, 34, e14804. [Google Scholar] [CrossRef]
- Kraiewski, P.k.; Jfri, A.; Ochando-Ibernçn, G.; Martorell, A. Ultrasonographic railway signs in tunnel sas a new indipendent risk factor of adalimumab failure in hidradenitis suppurativa. J. Am. Acad. Dermatol. 2023, 88, 732–734. [Google Scholar] [CrossRef] [PubMed]
- Gierek, M.; Bergler-Czop, B.; Słaboń, A.; Łabuś, W.; Ochała-Gierek, G. Laser speckle contrast analysis (LASCA): A new device in the diagnosis and monitoring of surgical treatment of hidradenitis suppurativa. Adv. Dermatol. Allergol. 2023, 40, 253–258. [Google Scholar] [CrossRef]
- Manfredini, M.; Chello, C.; Ciardo, S.; Guida, S.; Chester, J.; Lasagni, C.; Bigi, L.; Farnetani, F.; Bettoli, V.; Pellacani, G. Hidradenitis sup-purativa: Morphologic and vascular study of nodular inflammatory lesions by means of optical coherence tomography. Exp. Dermatol. 2022, 31, 1076–1082. [Google Scholar] [CrossRef]
- Gierek, M.; Łabuś, W.; Słaboń, A.; Ziółkowska, K.; Ochała-Gierek, G.; Kitala, D.; Szyluk, K.; Niemiec, P. Co-Graft of Acellular Dermal Matrix and Split Thickness Skin Graft—A New Reconstructive Surgical Method in the Treatment of Hidradenitis Suppurativa. Bioengineering 2022, 9, 389. [Google Scholar] [CrossRef]
- Reshetylo, S.; Narla, S.; Bakker, C.; Freeman, T.; Farah, R.S.; Hamzavi, I.H.; Goldfarb, N. Systematic review of photodynamic therapy for the treatment of hidradenitis suppurativa. Photodermatol. Photoimmunol. Photomed. 2023, 39, 39–50. [Google Scholar] [CrossRef]
- Shukla, R.; Karagaiah, P.; Patil, A.; Farnbach, K.; Ortega-Loayza, A.G.; Tzellos, T.; Szepietowski, J.C.; Giulini, M.; Schepler, H.; Grabbe, S.; et al. Surgical Treatment in Hidradenitis Suppurativa. J. Clin. Med. 2022, 11, 2311. [Google Scholar] [CrossRef] [PubMed]
All (n = 53) | Early Onset (n = 22) | Adult Onset (n = 31) | p | |
---|---|---|---|---|
Age at visit, years ° | 30 (22–43) | 26 (18–30) | 32 (27–49) | 0.0005 § |
Age of onset, years ° | 19 (14–25) | 14 (11–16) | 25 (20–34.2) | <0.0001 § |
Age at diagnosis, years ° | 25 (20–35) | 18 (14–24) | 27 (22.8–43) | <0.0001 § |
HS duration, years ° | 7 (4–16) | 11 (5–22) | 4 (3–15) | 0.11 § |
Delay in diagnosis, years ° | 3.5 (1–9) | 6 (2–9.5) | 2 (1–6) | 0.16 § |
Family history, n (%) | 7 (13.2) | 5 (22.7) | 2 (6.5) | 0.11 # |
Smoking, n (%) | ||||
Never smoked | 17 (32) | 7 (31.8) | 10 (32.3) | |
Former smokers | 4 (7.5) | 2 (9.1) | 2 (6.3) | |
Active smokers | 32 (60.4) | 13 (59.1) | 19 (61.3) | 0.95 * |
Personal history acne, n (%) | 15 (28.3) | 6 (27.3) | 9 (29) | >0.9999 # |
First menstruation age, n (%) | 12 (11–13) | 11.5 (10–13) | 13 (12–13.8) | 0.0226 § |
Menses abnormalities, n (%) | 13 (24.5) | 9 (40.9) | 4 (12.9) | 0.0264 # |
BMI kg/m2 ° | 25.2 (21.3–28.5) | 25.7 (23.5–29.8) | 25.2 (20.8–28.3) | 0.57 § |
BMI > 25, n (%) | 31 (58.5) | 14 (63.3) | 17 (54.8) | 0.58 # |
BMI > 30, n (%) | 11 (20.8) | 4 (18.2) | 7 (22.6) | 0.75 # |
All (n = 53) | Early Onset (n = 22) | Adult Onset (n = 31) | P | |
---|---|---|---|---|
Hurley, n (%) | ||||
I | 18 (33.4) | 5 (22.7) | 13 (41.9) | |
II | 21 (39.6) | 9 (40.9) | 12 (38.7) | |
III | 14 (26.4) | 8 (36.3) | 6 (19.4) | 0.24 * |
IHS4 ° | 6 (3.3–11.8) | 8.5 (3.8–12) | 5.5 (3–10) | 0.35 § |
Region involved in HS (n) | ||||
Axillae | 28 (52.8) | 12 (54.5) | 16 (51.6) | >0.9999 # |
Inguinal | 34 (64.2) | 17 (77.3) | 17 (54.8) | 0.15 # |
Gluteal | 16 (31.4) | 7 (31.8) | 9 (29) | >0.9999 # |
Trunk | 8 (15.1) | 2 (9.1) | 6 (19.4) | 0.45 # |
Ano-genital | 18 (33.4) | 11 (50) | 7 (22.6) | 0.0459 # |
Type of lesions (n) | ||||
Nodules | 35 (66) | 16 (72.7) | 19 (61.3) | 0.56 # |
Abscesses | 39 (73.6) | 18 (81.8) | 21 (67.7) | 0.35 # |
Fistulas/tunnel | 29 (54.7) | 14 (63.4) | 15 (48.4) | 0.40 # |
Number of lesions ° | ||||
Nodules | 1 (0–3) | 1.5 (0–3) | 1 (0–3) | 0.73 § |
Abscesses | 1 (0–2) | 1 (0.75–2.25) | 1 (0–2) | 0.86 § |
Fistulas/tunnel | 1 (0–1) | 1 (0–1.25) | 0 (0–1) | 0.39 § |
Number of affected areas ° | 3 (2–5) | 3.5 (2–5) | 2 (2–4) | 0.09 § |
Previous HS treatments, n (%) | ||||
Only topical agents | 13 (24.5) | 6 (27.3) | 7 (22.6) | 0.75 # |
Systemic agents | ||||
Conventional | 44 (83.1) | 17 (77.3) | 27 (87.1) | 0.46 # |
Biologics | 10 (18.9) | 6 (27.3) | 4 (12.9) | 0.29 # |
Actual HS treatment, n (%) | ||||
Only Topical agents | 28 (52.8) | 11 (50) | 17 (45.9) | 0.59 # |
Systemic agents | ||||
Conventional | 14 (26.4) | 3 (13.6) | 11 (35.5) | 0.11 # |
Biologics | 11 (20.8) | 8 (36.4) | 3 (9.7) | 0.0486 # |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Di Cesare, A.; Rosi, E.; Amerio, P.; Prignano, F. Clinical and Ultrasonographic Characterization of Hidradenitis Suppurativa in Female Patients: Impact of Early Recognition of the Disease. Life 2023, 13, 1630. https://doi.org/10.3390/life13081630
Di Cesare A, Rosi E, Amerio P, Prignano F. Clinical and Ultrasonographic Characterization of Hidradenitis Suppurativa in Female Patients: Impact of Early Recognition of the Disease. Life. 2023; 13(8):1630. https://doi.org/10.3390/life13081630
Chicago/Turabian StyleDi Cesare, Antonella, Elia Rosi, Paolo Amerio, and Francesca Prignano. 2023. "Clinical and Ultrasonographic Characterization of Hidradenitis Suppurativa in Female Patients: Impact of Early Recognition of the Disease" Life 13, no. 8: 1630. https://doi.org/10.3390/life13081630
APA StyleDi Cesare, A., Rosi, E., Amerio, P., & Prignano, F. (2023). Clinical and Ultrasonographic Characterization of Hidradenitis Suppurativa in Female Patients: Impact of Early Recognition of the Disease. Life, 13(8), 1630. https://doi.org/10.3390/life13081630