Impact of the COVID-19 Pandemic on Melanoma Diagnosis in Romania—Data from Two University Centers
Abstract
:1. Introduction
2. Materials and Methods
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Conforti, C.; Zalaudek, I. Epidemiology and Risk Factors of Melanoma: A Review. Dermatol. Pract. Concept. 2021, 11, e2021161S. [Google Scholar] [CrossRef]
- Dzwierzynski, W.W. Melanoma Risk Factors and Prevention. Clin. Plast. Surg. 2021, 48, 543–550. [Google Scholar] [CrossRef] [PubMed]
- Elmas, Ö.F.; Demirbaş, A.; Düzayak, S.; Atasoy, M.; Türsen, Ü.; Lotti, T. Melanoma and COVID-19: A Narrative Review Focused on Treatment. Dermatol. Ther. 2020, 33, e14101. [Google Scholar] [CrossRef] [PubMed]
- Mishra, K.; Barnhill, R.L.; Paddock, L.E.; Fine, J.A.; Berwick, M. Histopathologic Variables Differentially Affect Melanoma Survival by Age at Diagnosis. Pigment Cell Melanoma Res. 2019, 32, 593–600. [Google Scholar] [CrossRef] [PubMed]
- Weiss, S.A.; Hanniford, D.; Hernando, E.; Osman, I. Revisiting Determinants of Prognosis in Cutaneous Melanoma. Cancer 2015, 121, 4108–4123. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Boutros, M.; Moujaess, E.; Kourie, H.R. Cancer Management during the COVID-19 Pandemic: Choosing between the Devil and the Deep Blue Sea. Crit. Rev. Oncol. Hematol. 2021, 167, 103273. [Google Scholar] [CrossRef]
- Slotman, E.; Schreuder, K.; Nijsten, T.; Wakkee, M.; Hollestein, L.; Mooyaart, A.; Siesling, S.; Louwman, M. The Impact of the COVID-19 Pandemic on Keratinocyte Carcinoma in the Netherlands: Trends in Diagnoses and Magnitude of Diagnostic Delays. J. Eur. Acad. Dermatol. Venereol. 2022, 36, 680–687. [Google Scholar] [CrossRef]
- Ricci, F.; Fania, L.; Paradisi, A.; Di Lella, G.; Pallotta, S.; Sobrino, L.; Panebianco, A.; Annessi, G.; Abeni, D. Delayed Melanoma Diagnosis in the COVID-19 Era: Increased Breslow Thickness in Primary Melanomas Seen after the COVID-19 Lockdown. J. Eur. Acad. Dermatol. Venereol. 2020, 34, e778–e779. [Google Scholar] [CrossRef]
- Shannon, A.B.; Sharon, C.E.; Straker, R.J.; Miura, J.T.; Ming, M.E.; Chu, E.Y.; Karakousis, G.C. The Impact of the COVID-19 Pandemic on the Presentation Status of Newly Diagnosed Melanoma: A Single Institution Experience. J. Am. Acad. Dermatol. 2021, 84, 1096–1098. [Google Scholar] [CrossRef]
- Rashid, S.; Tsao, H. Effect of the COVID-19 Pandemic on Delayed Skin Cancer Services. Dermatol. Clin. 2021, 39, 627–637. [Google Scholar] [CrossRef]
- Venables, Z.C.; Ahmed, S.; Bleiker, T.O.; Broggio, J.; Kwiatkowska, M.; Levell, N.J.; Millington, G.W.M.; Paley, L.; Payne, E.; Proby, C.; et al. The Impact of the COVID-19 Pandemic on Skin Cancer Incidence and Treatment in England, 2020. Br. J. Dermatol. 2021, 185, 460–462. [Google Scholar] [CrossRef] [PubMed]
- Earnshaw, C.; Hunter, H.; McMullen, E.; Griffiths, C.; Warren, R. Reduction in Skin Cancer Diagnosis, and Overall Cancer Referrals, during the COVID-19 Pandemic. Br. J. Dermatol. 2020, 183, 792–794. [Google Scholar] [CrossRef] [PubMed]
- Marson, J.W.; Maner, B.S.; Harding, T.P.; Meisenheimer, J.; Solomon, J.A.; Leavitt, M.; Levin, N.J.; Dellavalle, R.; Brooks, I.; Rigel, D.S. The Magnitude of COVID-19′s Effect on the Timely Management of Melanoma and Nonmelanoma Skin Cancers. J. Am. Acad. Dermatol. 2021, 84, 1100–1103. [Google Scholar] [CrossRef] [PubMed]
- Lallas, A.; Kyrgidis, A.; Manoli, S.-M.; Papageorgiou, C.; Lallas, K.; Sotiriou, E.; Vakirlis, E.; Sidiropoulos, T.; Ioannides, D.; Apalla, Z. Delayed Skin Cancer Diagnosis in 2020 Because of the COVID-19–Related Restrictions: Data from an Institutional Registry. J. Am. Acad. Dermatol. 2021, 85, 721–723. [Google Scholar] [CrossRef]
- Tejera-Vaquerizo, A.; Nagore, E. Estimated Effect of COVID-19 Lockdown on Melanoma Thickness and Prognosis: A Rate of Growth Model. J. Eur. Acad. Dermatol. Venereol. 2020, 34, e351–e353. [Google Scholar] [CrossRef]
- Gualdi, G.; Porreca, A.; Amoruso, G.F.; Atzori, L.; Calzavara-Pinton, P.; De Tursi, M.; Di Buduo, A.; Di Marino, P.; Fabroncini, G.; Fantini, F.; et al. The Effect of the COVID-19 Lockdown on Melanoma Diagnosis in Italy. Clin. Dermatol. 2021, 39, 911–919. [Google Scholar] [CrossRef]
- Gisondi, P.; Cazzaniga, S.; Di Leo, S.; Piaserico, S.; Bellinato, F.; Pizzolato, M.; Gatti, A.; Eccher, A.; Brunelli, M.; Saraggi, D.; et al. Impact of the COVID-19 Pandemic on Melanoma Diagnosis. J. Eur. Acad. Dermatol. Venereol. 2021, 35, e714–e715. [Google Scholar] [CrossRef]
- Cariti, C.; Merli, M.; Avallone, G.; Rubatto, M.; Marra, E.; Fava, P.; Caliendo, V.; Picciotto, F.; Gualdi, G.; Stanganelli, I.; et al. Melanoma Management during the COVID-19 Pandemic Emergency: A Literature Review and Single-Center Experience. Cancers 2021, 13, 6071. [Google Scholar] [CrossRef]
- Trepanowski, N.; Chang, M.S.; Zhou, G.; Ahmad, M.; Berry, E.G.; Bui, K.; Butler, W.H.; Chu, E.Y.; Curiel-Lewandrowski, C.; Dellalana, L.E.; et al. Delays in Melanoma Presentation during the COVID-19 Pandemic: A Nationwide Multi-Institutional Cohort Study. J. Am. Acad. Dermatol. 2022, 87, 1217–1219. [Google Scholar] [CrossRef]
- Gedeah, C.; Damsin, T.; Absil, G.; Somja, J.; Collins, P.; Rorive, A.; Marchal, N.; Seidel, L.; Nikkels, A.F. The Impact of COVID-19 on the New Diagnoses of Melanoma. Eur. J. Dermatol. 2021, 31, 565–567. [Google Scholar] [CrossRef]
- Martinez-Lopez, A.; Diaz-Calvillo, P.; Cuenca-Barrales, C.; Montero-Vilchez, T.; Sanchez-Diaz, M.; Buendia-Eisman, A.; Arias-Santiago, S. Impact of the COVID-19 Pandemic on the Diagnosis and Prognosis of Melanoma. J. Clin. Med. 2022, 11, 4181. [Google Scholar] [CrossRef] [PubMed]
- Molinier, R.; Roger, A.; Genet, B.; Blom, A.; Longvert, C.; Chaplain, L.; Fort, M.; Saiag, P.; Funck-Brentano, E. Impact of the French COVID-19 Pandemic Lockdown on Newly Diagnosed Melanoma Delay and Severity. J. Eur. Acad. Dermatol. Venereol. 2022, 36, e164–e166. [Google Scholar] [CrossRef] [PubMed]
- Weston, G.K.; Jeong, H.S.; Mu, E.W.; Polsky, D.; Meehan, S.A. Impact of COVID-19 on Melanoma Diagnosis. Melanoma Res. 2021, 31, 280–281. [Google Scholar] [CrossRef]
- Davis, C.H.; Ho, J.; Greco, S.H.; Koshenkov, V.P.; Vidri, R.J.; Farma, J.M.; Berger, A.C. COVID-19 Is Affecting the Presentation and Treatment of Melanoma Patients in the Northeastern United States. Ann. Surg. Oncol. 2022, 29, 1629–1635. [Google Scholar] [CrossRef] [PubMed]
- Tejera-Vaquerizo, A.; Paradela, S.; Toll, A.; Santos-Juanes, J.; Jaka, A.; López, A.; Cañueto, J.; Villegas-Romero, I.; Fernández-Pulido, C.; Perandones, H.; et al. Effects of COVID-19 Lockdown on Tumour Burden of Melanoma and Cutaneous Squamous Cell Carcinoma. Acta Derm. Venereol. 2021, 101, adv00525. [Google Scholar] [CrossRef] [PubMed]
- Conforti, C.; Lallas, A.; Argenziano, G.; Dianzani, C.; Di Meo, N.; Giuffrida, R.; Kittler, H.; Malvehy, J.; Marghoob, A.A.; Soyer, H.P.; et al. Impact of the COVID-19 Pandemic on Dermatology Practice Worldwide: Results of a Survey Promoted by the International Dermoscopy Society (IDS). Dermatol. Pract. Concept. 2021, 11, e2021153. [Google Scholar] [CrossRef]
- Conic, R.Z.; Cabrera, C.I.; Khorana, A.A.; Gastman, B.R. Determination of the Impact of Melanoma Surgical Timing on Survival Using the National Cancer Database. J. Am. Acad. Dermatol. 2018, 78, 40–46.e7. [Google Scholar] [CrossRef]
- Nolan, G.S.; Dunne, J.A.; Kiely, A.L.; Pritchard Jones, R.O.; Gardiner, M.; RSTNCOVID: Skin Collaborative; Jain, A. The Effect of the COVID-19 Pandemic on Skin Cancer Surgery in the United Kingdom: A National, Multi-Centre, Prospective Cohort Study and Survey of Plastic Surgeons. Br. J. Surg. 2020, 107, e598–e600. [Google Scholar] [CrossRef]
- Kaufman, H.W.; Chen, Z.; Niles, J.; Fesko, Y. Changes in the Number of US Patients With Newly Identified Cancer Before and During the Coronavirus Disease 2019 (COVID-19) Pandemic. JAMA Netw. Open 2020, 3, e2017267. [Google Scholar] [CrossRef]
- IJzerman, M.; Emery, J. University of Is a Delayed Cancer Diagnosis a Consequence of COVID-19? Available online: https://pursuit.unimelb.edu.au/articles/is-a-delayed-cancer-diagnosis-a-consequence-of-COVID-19 (accessed on 31 October 2022).
- Rutter, M.D.; Brookes, M.; Lee, T.J.; Rogers, P.; Sharp, L. Impact of the COVID-19 Pandemic on UK Endoscopic Activity and Cancer Detection: A National Endoscopy Database Analysis. Gut 2021, 70, 537–543. [Google Scholar] [CrossRef]
- Saab, R.; Obeid, A.; Gachi, F.; Boudiaf, H.; Sargsyan, L.; Al-Saad, K.; Javakhadze, T.; Mehrvar, A.; Abbas, S.S.; Al-Agele, Y.S.A.; et al. Impact of the Coronavirus Disease 2019 (COVID-19) Pandemic on Pediatric Oncology Care in the Middle East, North Africa, and West Asia Region: A Report from the Pediatric Oncology East and Mediterranean (POEM) Group. Cancer 2020, 126, 4235–4245. [Google Scholar] [CrossRef] [PubMed]
- COVIDSurg Collaborative Elective Surgery Cancellations Due to the COVID-19 Pandemic: Global Predictive Modelling to Inform Surgical Recovery Plans. Br. J. Surg. 2020, 107, 1440–1449. [CrossRef]
- Arenbergerova, M.; Lallas, A.; Nagore, E.; Rudnicka, L.; Forsea, A.; Pasek, M.; Meier, F.; Peris, K.; Olah, J.; Posch, C. Position Statement of the EADV Melanoma Task Force on Recommendations for the Management of Cutaneous Melanoma Patients during COVID-19. J. Eur. Acad. Dermatol. Venereol. 2021, 35, e427–e428. [Google Scholar] [CrossRef] [PubMed]
- Raza, S.A.; Cannon, D.; Nuttall, G.; Ali, F.R. Exploring the Implications of the First COVID-19 Lockdown on Patients with Melanoma: A National Survey. Clin. Exp. Dermatol. 2022, 47, 114–116. [Google Scholar] [CrossRef] [PubMed]
- Chuchu, N.; Dinnes, J.; Takwoingi, Y.; Matin, R.N.; Bayliss, S.E.; Davenport, C.; Moreau, J.F.; Bassett, O.; Godfrey, K.; O’Sullivan, C.; et al. Teledermatology for Diagnosing Skin Cancer in Adults. Cochrane Database Syst. Rev. 2018, 2018, CD013193. [Google Scholar] [CrossRef]
- Villani, A.; Fabbrocini, G.; Costa, C.; Scalvenzi, M. Melanoma Screening Days During the Coronavirus Disease 2019 (COVID-19) Pandemic: Strategies to Adopt. Dermatol. Ther. 2020, 10, 525–527. [Google Scholar] [CrossRef]
Month | Pre-COVID-19 n (%) | COVID-19 n (%) | Change n (%) |
---|---|---|---|
March | 21 (6.2%) | 40 (14.5%) | +19 (+90.4%) |
April | 32 (9.4%) | 12 (4.4%) | −20 (−62.5%) |
May | 28 (8.2%) | 15 (5.5%) | −13 (−46.4%) |
June | 43 (12.6%) | 21 (7.6%) | −22 (−51.1%) |
July | 34 (10.0%) | 30 (10.9%) | −4 (−11.7%) |
August | 21 (6.2%) | 18 (6.5%) | −3 (−14.2%) |
September | 25 (7.3%) | 23 (8.4%) | −2 (−8%) |
October | 37 (10.9%) | 26 (9.5%) | −11 (−29.7%) |
November | 26 (7.6%) | 23 (8.4%) | −3 (−11.5%) |
December | 30 (8.8%) | 21 (7.6%) | −9 (−30%) |
January | 19 (5.6%) | 17 (6.2%) | −2 (−10.5%) |
February | 25 (7.3%) | 29 (10.5%) | + 4 (−16%) |
Total | 341 (100.0%) | 275 (100.0%) | −66 (−19.3%) |
Characteristics | Pre-COVID-19 | COVID-19 | p-Value | |
---|---|---|---|---|
Median Breslow index (mm)(SD) | 1.37 (0.5–3.5) | 2.20 (0.7–5.11) | 0.004 | |
Median mitotic count (/mm2)(SD) | 3 (1–7) | 4 (1–10) | 0.002 | |
Histological subtype (n%) | ||||
SSM | 258 (75.7%) | 188 (68.4%) | 0.126 | |
NM | 60 (17.6%) | 71 (25.8%) | ||
LMM | 11 (3.2%) | 6 (2.2%) | ||
ALM | 8 (2.3%) | 5 (1.8%) | ||
Other types | 4 (1.2%) | 5 (1.8%) | ||
Ulceration (n%) | No | 229 (67.2%) | 163 (59.3%) | 0.053 |
Yes | 112 (32.8%) | 112 (40.7%) | ||
Vascular/lymphatic invasion (n%) | No | 324 (95%) | 254 (92.4%) | 0.234 |
Yes | 17 (5%) | 21 (7.6%) | ||
Neural invasion (n%) | No | 332 (97.4%) | 269 (97.8%) | 0.918 |
Yes | 9 (2.6%) | 6 (2.2%) | ||
pT staging (n%) | ||||
Tis | 59 (17.3%) | 39 (14.2%) | 0.036 | |
T1a | 86 (25.2%) | 56 (20.4%) | ||
T1b | 26 (7.6%) | 15 (5.5%) | ||
T2a | 34 (10.0%) | 23 (8.4%) | ||
T2b | 12 (3.5%) | 12 (4.4%) | ||
T3a | 21 (6.2%) | 18 (6.5%) | ||
T3b | 39 (11.4%) | 24 (8.7%) | ||
T4a T4b | 11 (3.2%) | 13 (4.7%) | ||
52 (15.2%) | 70 (25.5%) | |||
Not specified | 1 (0.3%) | 5 (1.8%) | ||
pT staging group (n%) | Thin melanoma (Tis, T1) | 172 (50.4%) | 115 (41.8%) | 0.04 |
Thick melanoma (T2, T3, T4) | 169 (49.6%) | 160 (58.2%) | ||
Total | 341 (100%) | 275 (100%) |
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Ungureanu, L.; Apostu, A.P.; Vesa, Ș.C.; Cășeriu, A.E.; Frățilă, S.; Iancu, G.; Bejinariu, N.; Munteanu, M.; Șenilă, S.C.; Vasilovici, A. Impact of the COVID-19 Pandemic on Melanoma Diagnosis in Romania—Data from Two University Centers. Int. J. Environ. Res. Public Health 2022, 19, 15129. https://doi.org/10.3390/ijerph192215129
Ungureanu L, Apostu AP, Vesa ȘC, Cășeriu AE, Frățilă S, Iancu G, Bejinariu N, Munteanu M, Șenilă SC, Vasilovici A. Impact of the COVID-19 Pandemic on Melanoma Diagnosis in Romania—Data from Two University Centers. International Journal of Environmental Research and Public Health. 2022; 19(22):15129. https://doi.org/10.3390/ijerph192215129
Chicago/Turabian StyleUngureanu, Loredana, Adina Patricia Apostu, Ștefan Cristian Vesa, Alexandra Elena Cășeriu, Simona Frățilă, Gabriela Iancu, Nona Bejinariu, Maximilian Munteanu, Simona C. Șenilă, and Alina Vasilovici. 2022. "Impact of the COVID-19 Pandemic on Melanoma Diagnosis in Romania—Data from Two University Centers" International Journal of Environmental Research and Public Health 19, no. 22: 15129. https://doi.org/10.3390/ijerph192215129