Effects of COVID-19 Pandemic on the Diagnosis of Melanoma and Keratinocyte Carcinomas: a Systematic Review and Meta-analysis

Authors

  • Pablo Díaz-Calvillo Department of Dermatology, Virgen de las Nieves University Hospital, Granada, Spain; Instituto de Investigación Biosanitaria ibs.GRANADA, Granada, Spain
  • Daniel Muñoz-Barba Department of Dermatology, Virgen de las Nieves University Hospital, Granada, Spain; Instituto de Investigación Biosanitaria ibs.GRANADA, Granada, Spain
  • Clara Ureña-Paniego Department of Dermatology, Virgen de las Nieves University Hospital, Granada, Spain; Instituto de Investigación Biosanitaria ibs.GRANADA, Granada, Spain
  • Lara Valeska Maul Department of Dermatology, University Hospital of Basel, Basel, Switzerland
  • Sara Cerminara Department of Dermatology, University Hospital of Basel, Basel, Switzerland
  • Lisa Kostner Department of Dermatology, University Hospital of Basel, Basel, Switzerland
  • Antonio Martínez López Department of Dermatology, Virgen de las Nieves University Hospital, Granada, Spain; Instituto de Investigación Biosanitaria ibs.GRANADA, Granada, Spain
  • Salvador Arias-Santiago Department of Dermatology, Virgen de las Nieves University Hospital, Granada, Spain; Instituto de Investigación Biosanitaria ibs.GRANADA, Granada, Spain; Department of Dermatology, University of Granada, Granada, Spain

DOI:

https://doi.org/10.2340/actadv.v104.19460

Keywords:

melanoma, squamous cell carcinoma, basal cell carcinoma, COVID-19

Abstract

Since December 2019, the COVID-19 pandemic has profoundly affected healthcare. The real effects of the COVID-19 pandemic on skin cancer are still unclear, more than 3 years later. This study aims to summarise the pandemic’s impact on skin cancer diagnosis and outcome. A systematic review and meta-analysis was conducted, selecting studies comparing skin cancer diagnosis and prognosis post-pandemic with pre-pandemic data. A total of 27 papers were reviewed including 102,263 melanomas and 271,483 keratinocyte carcinomas. During the initial pandemic months (January–July 2020), melanoma surgeries dropped by 29.7% and keratinocyte carcinomas surgeries by 50.8%. Early pandemic tumours exhibited greater thickness and stage. In a long-term period beyond the initial months, melanoma surgeries decreased by 9.3%, keratinocyte carcinomas by 16.6%. No significant differences were observed in the Breslow thickness of melanomas after the start of the pandemic (mean difference 0.06, 95% confidence interval –0.46, 0.58). Melanomas operated on post-pandemic onset had an increased risk of ulceration (odds ratio 1.35, 95% confidence interval 1.22–1.50). Keratinocyte carcinomas showed increased thickness and worsened stage post-pandemic. However, studies included were mostly retrospective and cross-sectional, reporting diverse data. This review indicates that the pandemic likely caused delays in skin cancer diagnosis and treatment, potentially impacting patient outcomes.

Downloads

Download data is not yet available.

References

World Health Organization (WHO). Novel Coronavirus (2019-nCoV) situation reports. 2023 [cited 2023 17 Sep]. Available from: www.who.int/emergencies/diseases/novel-coronavirus-2019/situation-reports.

Ferrante G, Camussi E, Piccinelli C, Senore C, Armaroli P, Ortale A, et al. Did social isolation during the SARS-CoV-2 epidemic have an impact on the lifestyles of citizens? Epidemiol Prev 2020; 44: 353-362.

Rogers MC, Wallace MM, Wheless L, Dewan AK. Impact of the COVID-19 pandemic on inpatient dermatology consult patterns at a tertiary care hospital: a retrospective cohort study. J Am Acad Dermatol 2021; 84: 156-158.

https://doi.org/10.1016/j.jaad.2020.09.060 DOI: https://doi.org/10.1016/j.jaad.2020.09.060

Teuscher M, Diehl K, Schaarschmidt ML, Weilandt J, Sasama B, Ohletz J, et al. Effects of the COVID-19 pandemic on care of melanoma patients in Berlin, Germany: the Mela-COVID survey. Eur J Dermatol 2022; 31: 521-529.

https://doi.org/10.1684/ejd.2021.4098 DOI: https://doi.org/10.1684/ejd.2021.4098

Aggarwal P, Knabel P, Fleischer Jr, AB. United States burden of melanoma and non-melanoma skin cancer from 1990 to 2019. J Am Acad Dermatol 2021; 85: 388-395.

https://doi.org/10.1016/j.jaad.2021.03.109 DOI: https://doi.org/10.1016/j.jaad.2021.03.109

Garbe C, Keim U, Amaral T, Berking C, Eigentler TK, Flatz L, et al. Prognosis of patients with primary melanoma stage I and II according to American Joint Committee on Cancer Version 8 validated in two independent cohorts: implications for adjuvant treatment. J Clin Oncol 2022; 40: 3741-3749.

https://doi.org/10.1200/JCO.22.00202 DOI: https://doi.org/10.1200/JCO.22.00202

Renzi C, Mastroeni S, Passarelli F, Mannooranparampil TJ, Caggiati A, Potenza C, et al. Factors associated with large cutaneous squamous cell carcinomas. J Am Acad Dermatol 2010; 63: 404-411.

https://doi.org/10.1016/j.jaad.2009.09.044 DOI: https://doi.org/10.1016/j.jaad.2009.09.044

Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021; 372: n71.

https://doi.org/10.1136/bmj.n71 DOI: https://doi.org/10.1136/bmj.n71

Tools., T.N.I.o.H.S.Q.A. Quality assessment tool for observational cohort and cross-sectional studies. 2020 [cited 2023 1 April]. Available from: https://www.nhlbi.nih.gov/health-topics/study-quality-assessment-tools.

Amin MB, Greene FL, Edge SB, Compton CC, Gershenwald JE, Brookland RK, et al. The Eighth Edition AJCC Cancer Staging Manual: Continuing to build a bridge from a population-based to a more "personalized" approach to cancer staging. CA Cancer J Clin 2017; 67: 93-99.

https://doi.org/10.3322/caac.21388 DOI: https://doi.org/10.3322/caac.21388

Troesch A, Hoellwerth M, Forchhammer S, Del Regno L, Lodde G, Turko P, et al. The impact of the COVID-19 pandemic on the diagnosis of cutaneous melanomas: a retrospective cohort study from five European skin cancer reference centres. J Eur Acad Dermatol Venereol 2023; 37: 922-931.

https://doi.org/10.1111/jdv.18953 DOI: https://doi.org/10.1111/jdv.18953

Aabed H, Bloanca V, Crainiceanu Z, Bratosin F, Citu C, Diaconu MM, et al. The impact of SARS-CoV-2 pandemic on patients with malignant melanoma at a Romanian Academic Center: a four-year retrospective analysis. Int J Environ Res Public Health 2022; 19: 8499.

https://doi.org/10.3390/ijerph19148499 DOI: https://doi.org/10.3390/ijerph19148499

Davis CH, Ho J, Greco SH, Koshenkov VP, Vidri RJ, Farma JM, et al. COVID-19 is affecting the presentation and treatment of melanoma patients in the northeastern United States. Ann Surg Oncol 2022; 29: 1629-1635.

https://doi.org/10.1245/s10434-021-11086-8 DOI: https://doi.org/10.1245/s10434-021-11086-8

Hurley CM, Wrafter L, Dhannoon A, Regan H, Regan PJ. Optimising the management of malignant melanoma during COVID-19. JPRAS Open 2022; 31: 72-75.

https://doi.org/10.1016/j.jpra.2021.09.004 DOI: https://doi.org/10.1016/j.jpra.2021.09.004

Jeremic J, Sudecki B, Radenovic K, Mihaljevic J, Radosavljevic I, Jovanovic M, et al. Impact of the COVID-19 pandemic on melanoma diagnosis: increased Breslow thickness in primary melanomas: a single center experience. Int J Environ Res Public Health 2022; 19: 16806.

https://doi.org/10.3390/ijerph192416806 DOI: https://doi.org/10.3390/ijerph192416806

Kleemann J, Meissner M, Özistanbullu D, Balaban Ü, Old O, Kippenberger S, et al. Impact of the Covid-19 pandemic on melanoma and non-melanoma skin cancer inpatient treatment in Germany: a nationwide analysis. J Eur Acad Dermatol Venereol 2022; 36: 1766-1773.

https://doi.org/10.1111/jdv.18217 DOI: https://doi.org/10.1111/jdv.18217

Kostner L, Cerminara SE, Pamplona GSP, Maul JT, Dummer R, Ramelyte E, et al. Effects of COVID-19 lockdown on melanoma diagnosis in Switzerland: increased tumor thickness in elderly females and shift towards stage IV melanoma during lockdown. Cancers (Basel) 2022; 14: 2360.

https://doi.org/10.3390/cancers14102360 DOI: https://doi.org/10.3390/cancers14102360

Lamm R, Lyons W, So W, Willis AI. Advanced-stage melanoma at presentation following the peak of the pandemic: a COVID-19 cancer canary in a coal mine. World J Surg 2022; 46: 1820-1825.

https://doi.org/10.1007/s00268-022-06623-9 DOI: https://doi.org/10.1007/s00268-022-06623-9

Martinez-Lopez A, Diaz-Calvillo P, Cuenca-Barrales C, Montero-Vilchez T, Sanchez-Diaz M, Buendia-Eisman A, et al. Impact of the COVID-19 pandemic on the diagnosis and prognosis of melanoma. J Clin Med 2022; 11: 4181.

https://doi.org/10.3390/jcm11144181 DOI: https://doi.org/10.3390/jcm11144181

Sangers TE, Wakkee M, Kramer-Noels EC, Nijsten T, Louwman MWJ, Jaspars EH, et al. Limited impact of COVID-19-related diagnostic delay on cutaneous melanoma and squamous cell carcinoma tumour characteristics: a nationwide pathology registry analysis. Br J Dermatol 2022; 187: 196-202.

https://doi.org/10.1111/bjd.21050 DOI: https://doi.org/10.1111/bjd.21050

Shahid S, Gao J, Corriero AC, Roszpopa J, Miranda BH. A study of the effects of delayed patient presentation on cutaneous SCC progression. J Plast Reconstr Aesthet Surg 2022; 75: 722-729.

https://doi.org/10.1016/j.bjps.2021.09.015 DOI: https://doi.org/10.1016/j.bjps.2021.09.015

Silvia C, Denis C, Mario C, Luigi V, Federico T, Marcello C. Impact of COVID-19 pandemic on non-melanoma skin cancer's tumor burden and care: a multi-center study based in northern Italy. J Plast Reconstr Aesthet Surg 2022; 75: 3616-3621.

https://doi.org/10.1016/j.bjps.2022.06.037 DOI: https://doi.org/10.1016/j.bjps.2022.06.037

Slotman E, Schreuder K, Nijsten TEC, Wakkee M, Hollestein L, Mooyaart A, et al. 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.

https://doi.org/10.1111/jdv.17976 DOI: https://doi.org/10.1111/jdv.17976

Ungureanu L, Apostu AP, Vesa SC, Caseriu AE, Fratila S, Iancu G, et al. 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 DOI: https://doi.org/10.3390/ijerph192215129

Anichini A, Asero S, Bersanelli M, Caracò C, De Giorgi V, Di Giacomo AM, et al. The effect of COVID-19 emergency in the management of melanoma in Italy. Dermatol Reports 2021; 13: 8972.

https://doi.org/10.4081/dr.2021.8972 DOI: https://doi.org/10.4081/dr.2021.8972

Asai Y, Nguyen P, Hanna TP. Impact of the COVID-19 pandemic on skin cancer diagnosis: a population-based study. PLoS One 2021; 16: e0248492.

https://doi.org/10.1371/journal.pone.0248492 DOI: https://doi.org/10.1371/journal.pone.0248492

Berry W, Tan K, Haydon A, Shackleton M, Mar VJ. Reduced melanoma referrals during COVID-19 lockdown. Aust J Gen Pract 2021; 50.

https://doi.org/10.31128/AJGP-COVID-45 DOI: https://doi.org/10.31128/AJGP-COVID-45

Cocuz IG, Cocuz ME, Niculescu R, Șincu MC, Tinca AC, Sabău AH, et al. The impact of and adaptations due to the COVID-19 pandemic on the histopathological diagnosis of skin pathologies, including non-melanocyte and melanoma skin cancers: a single-center study in Romania. Medicina (Kaunas) 2021; 57: 533.

https://doi.org/10.3390/medicina57060533 DOI: https://doi.org/10.3390/medicina57060533

Ferrara G, De Vincentiis L, Ambrosini-Spaltro A, Barbareschi M, Bertolini V, Contato E, et al. Cancer diagnostic delay in northern and central Italy during the 2020 lockdown due to the coronavirus disease 2019 pandemic. Am J Clin Pathol 2021; 155: 64-68.

https://doi.org/10.1093/ajcp/aqaa177 DOI: https://doi.org/10.1093/ajcp/aqaa177

Filoni A, Del Fiore P, Cappellesso R, Dall'Olmo L, Salimian N, Spina R, et al. Management of melanoma patients during COVID-19 pandemic in an Italian skin unit. Dermatol Ther 2021; 34: e14908.

https://doi.org/10.1111/dth.14908 DOI: https://doi.org/10.1111/dth.14908

Gualdi G, Porreca A, Amoruso GF, Atzori L, Calzavara-Pinton P, De Tursi M, et al. The effect of the COVID-19 lockdown on melanoma diagnosis in Italy. Clin Dermatol 2021; 39: 911-919.

https://doi.org/10.1016/j.clindermatol.2021.05.015 DOI: https://doi.org/10.1016/j.clindermatol.2021.05.015

Guven DC, Sahin TK, Yildirim HC, Cesmeci E, Incesu FGG, Tahillioglu Y, et al. Newly diagnosed cancer and the COVID-19 pandemic: tumour stage migration and higher early mortality. BMJ Support Palliat Care 2021 Oct 28 (Online ahead of print).

https://doi.org/10.1136/bmjspcare-2021-003301 DOI: https://doi.org/10.1136/bmjspcare-2021-003301

Hamel R, Pollard B, Council ML. Impact of COVID-19 on dermatologic surgery: experience of a Midwestern academic practice. Arch Dermatol Res 2023; 315: 85-87.

https://doi.org/10.1007/s00403-021-02284-1 DOI: https://doi.org/10.1007/s00403-021-02284-1

Hoellwerth M, Kaiser A, Emberger M, Brandlmaier M, Laimer M, Egger A, et al. COVID-19-induced reduction in primary melanoma diagnoses: experience from a dermatopathology referral center. J Clin Med 2021; 10: 4059.

https://doi.org/10.3390/jcm10184059 DOI: https://doi.org/10.3390/jcm10184059

Seretis K, Boptsi E, Boptsi A, Lykoudis EG. The impact of treatment delay on skin cancer in COVID-19 era: a case-control study. World J Surg Oncol 2021; 19: 350.

https://doi.org/10.1186/s12957-021-02468-z DOI: https://doi.org/10.1186/s12957-021-02468-z

Tejera-Vaquerizo A, Paradela S, Toll A, Santos-Juanes J, Jaka A, López A, et al. Effects of COVID-19 lockdown on tumour burden of melanoma and cutaneous squamous cell carcinoma. Acta Derm Venereol 2021; 101: adv00525.

https://doi.org/10.2340/00015555-3890 DOI: https://doi.org/10.2340/00015555-3890

Valenti M, Pavia G, Gargiulo L, Facheris P, Nucca O, Mancini L, et al. Impact of delay in follow-up due to COVID-19 pandemic on skin cancer progression: a real-life experience from an Italian hub hospital. Int J Dermatol 2021; 60: 860-863.

https://doi.org/10.1111/ijd.15501 DOI: https://doi.org/10.1111/ijd.15501

Dergiades T, Milas C, Mossialos E, Panagiotidis T. Effectiveness of government policies in response to the first COVID-19 outbreak. PLOS Glob Public Health 2022; 2: e0000242.

https://doi.org/10.1371/journal.pgph.0000242 DOI: https://doi.org/10.1371/journal.pgph.0000242

Baumann BC, MacArthur KM, Brewer JD, Mendenhall WM, Barker CA, Etzkorn JR, et al. Management of primary skin cancer during a pandemic: multidisciplinary recommendations. Cancer 2020; 126: 3900-3906.

https://doi.org/10.1002/cncr.32969 DOI: https://doi.org/10.1002/cncr.32969

Chen RC, Haynes K, Du S, Barron J, Katz AJ. Association of cancer screening deficit in the United States with the COVID-19 Pandemic. JAMA Oncol 2021; 7: 878-884.

https://doi.org/10.1001/jamaoncol.2021.0884 DOI: https://doi.org/10.1001/jamaoncol.2021.0884

Renzi C, Mastroeni S, Mannooranparampil TJ, Passarelli F, Caggiati A, Potenza C, et al. Delay in diagnosis and treatment of squamous cell carcinoma of the skin. Acta Derm Venereol 2010; 90: 595-601.

https://doi.org/10.2340/00015555-0966 DOI: https://doi.org/10.2340/00015555-0966

Toma AO, Prodan M, Reddyreddy AR, Seclaman E, Crainiceanu Z, Bloanca V, et al. The epidemiology of malignant melanoma during the first two years of the COVID-19 pandemic: a systematic review. Int J Environ Res Public Health 2022; 20: 305.

https://doi.org/10.3390/ijerph20010305 DOI: https://doi.org/10.3390/ijerph20010305

Li X, Li Z, Yi X, Gao X, Yang Z, Huang X, et al. A population-based cohort study for presence of ulceration among cutaneous malignant melanoma subgroups of patients. Front Oncol 2022; 12: 929600.

https://doi.org/10.3389/fonc.2022.929600 DOI: https://doi.org/10.3389/fonc.2022.929600

Moynihan R, Sanders S, Michaleff ZA, Scott AM, Clark J, To EJ, et al. Impact of COVID-19 pandemic on utilisation of healthcare services: a systematic review. BMJ Open 2021; 1: e045343.

https://doi.org/10.1136/bmjopen-2020-045343 DOI: https://doi.org/10.1136/bmjopen-2020-045343

Pasquali P, Romero-Aguilera G, Moreno-Ramirez D. Teledermatology before, during, and after the COVID-19 pandemic. Actas Dermosifiliogr (Engl Ed) 2021; 112: 324-329. DOI: https://doi.org/10.1016/j.adengl.2021.01.040

https://doi.org/10.1016/j.ad.2020.11.008 DOI: https://doi.org/10.1016/j.ad.2020.11.008

Published

2024-03-14

How to Cite

Díaz-Calvillo, P., Muñoz-Barba, D., Ureña-Paniego, C., Maul, L. V., Cerminara, S., Kostner, L., Martínez López, A., & Arias-Santiago, S. (2024). Effects of COVID-19 Pandemic on the Diagnosis of Melanoma and Keratinocyte Carcinomas: a Systematic Review and Meta-analysis. Acta Dermato-Venereologica, 104, adv19460. https://doi.org/10.2340/actadv.v104.19460