The effect of COVID-19 disease on patients diagnosed with skin cancer in the

dermatology clinic
Alper Alyanak 1, *, Nurhan Döner Aktaş 1, Büşra Emir 2, Türkan Güray 1 and Ayşe Yazıcı 3
1 Department of Dermatology, Izmir Katip Çelebi University, Medical Faculty, Atatürk Research and Education Hospital,
Izmir, Turkey.
2 Department of Biostatistics, Izmir Katip Çelebi University Medical Faculty, Izmir, Turkey.
3 Department of Pathology, Izmir Katip Çelebi University, Medical Faculty, Atatürk Research and Education Hospital, Izmir,

Turkey.

World Journal of Advanced Research and Reviews, 2024, 22(01), 018–026

Publication history: Received on 20 February 2024; revised on 27 March 2024; accepted on 30 March 2024

Article DOI: https://doi.org/10.30574/wjarr.2024.22.1.1006

Abstract
Objective: We aimed to define the impact of the pandemic on patients presenting to dermatology clinic with skin cancer.

Methods: In our study, the characteristics of patients who attended our dermatology clinic before six months and after
six months of March 11, 2020, and whose biopsies diagnosed as basal cell carcinoma (BCC), squamous cell carcinoma
(SCC), and malignant melanoma (MM) were evaluated and compared regarding before and after COVID-19 pandemic

Results: Patients with BCC attending to the dermatology clinic were found to be younger in the pandemic period
(p<0.05). Gender, duration of skin tumors, primary lesions, and their locations were found to be not statistically
significant (p>0.05).

Conclusion: Patients with suspicious skin lesions could be encouraged to visit a hospital with appropriate COVID-19
protection. Alternatively, teledermatology could be used to evaluate whether the lesions should be excised or biopsied.

Keywords: Skin cancer; COVID-19; Hospital application; Biopsy

1. Introduction
COVID-19 disease was the most important threat to health when the World Health Organisation declared the novel
coronavirus (COVID-19) outbreak as a global pandemic on March 11, 2020. In Türkiye, after March 11, 2020, people
other than students and the working class refrain from going outside for about 1 year until vaccinations were completed.
In that period hospitals were accepting patients other than COVID-19 illnesses, but the applications to hospitals were
low compared to the previous year. Our aim was to define the effect of the pandemic on the applications of patients with
skin cancer to dermatology clinic.

2. Material and Methods

In our study, the characteristics of patients, who applied to Izmir Atatürk Research and Education Hospital dermatology
clinic, and from whom skin biopsies were taken, and resulted as basal cell carcinoma (BCC), squamous cell carcinoma
(SCC), and malignant melanoma (MM) were evaluated from the records of our clinic. The biopsies taken six months


Corresponding author: Alper Alyanak
Copyright © 2024 Author(s) retain the copyright of this article. This article is published under the terms of the Creative Commons Attribution Liscense 4.0.
 World Journal of Advanced Research and Reviews, 2024, 22(01), 018–026

before and six months after March 11, 2020, were searched from the records. The evaluated patients’ features were age,
gender, duration of the skin tumor ( if it was recorded), primary lesion, and location of the lesion.

This study was conducted under the Helsinki criteria after approval by the Izmir Katip Çelebi University Ethics
Committee (approval number: 249, date 27.05.2021).

2.1. Statistical Analysis

The data were evaluated in the statistical package program IBM SPSS Statistics 25.0 (IBM Corp., Armonk, New York,
USA). The normal distribution of the data of numerical variables was evaluated with the Shapiro-Wilk normality test
and Q-Q graphs. Categorical variables were given as frequency and percentage. Descriptive statistics were given as Mean
± Standard Deviation and Median (IQR) values. Mann Whitney U test was used to compare two independent groups of
continuous variables for which the assumption of normal distribution was not met. The relationship between
categorical variables was evaluated with the Continuity Correction test in 2 x 2 tables and the Pearson Chi-Square test
in r x c tables. A value of p<0.05 was considered statistically significant.

2.2. Ethics committee approval

This study was conducted under the Helsinki criteria after approval by the Izmir Katip Çelebi University Ethics
Committee (approval number: 249, date 27.05.2021).

3. Results
Between March 11, 2020, and September 11, 2019, the number of skin biopsies taken in our dermatology clinic was
1613; between March 11, 2020, and September 11, 2020, the number of skin biopsies taken in our dermatology clinic
was 564. Out of the total 2177 biopsies, 233 were diagnosed as basal cell carcinoma, squamous cell carcinoma, and
malignant melanoma.

Diagnosed with BCC, there was a total of 159 patients, 84 women, and 75 men. The average age was 70.57±12.59 (mean
± sd) for women and 69.47±13.88 (mean ± sd) for men. Out of 159 patients, there was a total of 38 patients, 22 women
and 16 men, with a known duration of the disease. Duration of disease was 4.02±5.21 years (mean ± sd) in women and
2.80±2.89 years (mean ± sd) in men. There were 119 patients between March 2020 and September 2019, and 40
patients between March 2020 and September 2020. The primary lesions and their numbers were as follows: papule,
nodule, plaque, ulcerated papule, ulcerated nodule, ulcerated plaque, and multiple lesions; 48, 40, 8, 1, 42, 3, and 17,
respectively. Locations of lesions and their numbers were as follows: nose, ear, forehead, cheek, trunk (hip, front trunk,
back trunk, waist, neck), chin, upper lip, around the eyes (eyelids and canthal regions), temple, upper extremity (hand,
arm), scalp, different regions; 62, 6, 12, 24, 10, 5, 2, 9, 9, 3, 6, and 11, respectively. Descriptive data of the patients with
basal cell carcinoma were given in Table 1. Statistical analysis revealed that patients who applied to our dermatology
clinic after March 11, 2020, were younger compared to the patients who applied before the pandemic (p<0.05) (Table
2).

Table 1 Descriptive data of patients with basal cell carcinoma

n (%)
Gender
Female 84 (52.8)
Male 75 (47.2)
Age
Female (Mean ± SD) 70.57±12.59
Male (Mean ± SD) 69.47±13.88
Time (year)
Female (Mean ± SD) (n = 22) 4.02±5.21
Male (Mean ± SD) (n = 16) 2.80±2.89

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Group
March 2020- September 2019 119 (74.8)
March 2020- September 2020 40 (25.2)
Primary lesion
Papule 48 (30.2)
Nodule 40 (25.2)
Plaque 8 (5.0)
Ulcerated papule 1 (0.6)
Ulcerated nodule 42 (26.4)
Ulcerated plaque 3 (1.9)
More than one lesion 17 (10.7)
Location
Nose 62 (39.0)
Ear 6 (3.8)
Forehead 12 (7.5)
Cheek 24 (15.1)
Trunk (hip, front trunk, back trunk, waist, neck) 10 (6.3)
Chin 5 (3.1)
Upper lip 2 (1.3)
Around the eyes (eyelids and canthal regions) 9 (5.7)
Temple 9 (5.7)
Upper extremity (hand, arm) 3 (1.9)
Scalp 6 (3.8)
Different regions 11 (6.9)

Table 2 Statistical analysis of features of patients with BCC according to the start of the pandemic

Before March 11, 2020, six After March 11, 2020, six
months months
Mean ± SD Mean ± SD
n n
Variables Median (IQR) Median (IQR) p value
71.24 ± 12,38 66.53 ± 14.95
Age 119 40 0.037+
73.00 (16.00) 67.50 (17.00)
2.79 ± 3.95 5.81 ± 5.12
Time (year) 29 9 0.100+
1.00 (2.00) 4.00 (8.70)
n (%) n (%)
Gender 0.616*
Female 61 (51.3) 23 (57.5)
Male 58 (48.7) 17 (42.5)

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Primary lesion 0.336++

Papule 40 (33.6) 8 (20.0)
Nodule 28 (23.5) 12 (30.0)
Plaque 5 (4.2) 3 (7.5)
Ulcerated papule 0 (0.0) 1 (2.5)
Ulcerated nodule 30 (25.2) 12 (30.0)
Ulcerated plaque 2 (1.7) 1 (2.5)
More than one lesion 14 (11.8) 3 (7.5)
Location 0.726++
Nose 43 (36.1) 19 (47.5)
Ear 4 (3.4) 2 (5.0)
Forehead 8 (6.7) 4 (10.0)
Cheek 20 (16.8) 4 (10.0)
Trunk (hip, front trunk, back trunk,
9 (7.6) 1 (2.5)
waist and neck)
Chin 4 (3.4) 1 (2.5)
Upper lip 2 (1.7) 0 (0.0)
Around the eyes (eyelids and canthal
5 (4.2) 4 (10.0)
regions)
Temple 8 (6.7) 1 (2.5)
Upper extremity (hand, arm) 2 (1.7) 1 (2.5)
Different regions 9 (7.6) 2 (5.0)
Scalp 5 (4.2) 1 (2.5)
SD: Standard Deviation; IQR: Interquartile Range; + Mann Whitney U test; * Continuity Correction Test; ++ Pearson Chi-Square test

Diagnosed with SCC, there was a total of 68 patients, 34 women and 34 men. The average age was 74.59±11.62 (mean
± sd) for women and 69.76±13.65 (mean ± sd) for men. Out of 68 patients, there was a total of 30 patients, 17 women
and 13 men, with a known duration of the disease. Duration of disease was 1,15±1,33 (mean ± sd) in women and
1.21±2.65 years (mean ± sd) in men. There were 47 patients between March 2020 and September 2019 and 21 patients
between March 2020 and September 2020. The primary lesions and their numbers were as follows: papule, nodule,
plaque, ulcerated papule, ulcerated nodule, ulcerated plaque, multiple lesions; 14, 19, 6, 2, 13, 8, and 6, respectively.
Locations of lesions and their numbers were as follows: nose, ear, forehead, cheek, around the eyes, temple, scalp, upper
limb (hand, arm), trunk (hip, front trunk, back trunk, waist, neck), perineal, lips, lower extremity (leg, foot), and different
regions; 7, 1, 4, 13, 2, 2, 4, 8, 4, 5, 4, 8, and 6, respectively. Descriptive data of the patients with squamous cell carcinoma
were given in Table 3. There were not any statistically significant differences between the groups according to the six-
month time frames (Table 4).

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Table 3 Descriptive data of patients with squamous cell carcinoma

n (%)
Gender
Female 34 (50,0)
Male 34 (50,0)
Age
Female (Mean ± SD) 74.59±11.62
Male (Mean ± SD) 69.76±13.65
Time (year)
Female (Mean ± SD) (n = 17) 1.15±1.33
Male (Mean ± SD) (n = 13) 1.21±2.65
Group
March 2020- September 2019 47 (69.1)
March 2020- September 2020 21 (30.9)
Primary lesion
Papule 14 (20.6)
Nodule 19 (27.9)
Plaque 6 (8.8)
Ulcerated papule 2 (2.9)
Ulcerated plaque 8 (11.8)
Ulcerated nodule 13(19.1)
More than one lesion 6 (8.8)
Location
Nose 7 (10.3)
Ear 1 (1.5)
Forehead 4 (5.9)
Cheek 13 (19.1)
Around the eyes (eyelids and canthal regions) 2 (2.9)
Temple 2 (2.9)
Scalp 4 (5.9)
Upper limb (hand, arm) 8 (11.8)
Trunk (hip, front trunk, back trunk, waist, neck) 4 (5.9)
Perineal 5 (7.4)
Lips 4 (5.9)
Lower extremity (leg, foot) 8 (11.8)
Different regions 6 (8.8)

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Table 4 Statistical analysis of features of patients with SCC according to the start of the pandemic

Before March 11, 2020, six After March 11, 2020, six
months months
Mean ± SD Mean ± SD
n n
Variables Median (IQR) Median (IQR) p value
72,43 ± 12,94 71,62 ± 12,83
Age 47 21 0,676+
73,00 (15,00) 70,00 (18,00)
1.42 ± 2.21 0.40 ± 0.11
Time (year) 23 7 0.096+
0.60 (0.70) 0.40 (0.20)
n (%) n (%)
Gender 1.000*
Female 23 (48.9) 11 (52.4)
Male 24 (51.1) 10 (47.6)
Primary lesion 0.270++
Papule 7 (14.9) 7 (33.3)
Nodule 12 (25.5) 7 (33.3)
Plaque 4 (8.5) 2 (9.5)
Ulcerated papule 2 (4.3) 0 (0.0)
Ulcerated nodule 10 (21.3) 3 (14.3)
Ulcerated plaque 8 (17.0) 0 (0.0)
More than one lesion 4 (8.5) 2 (9.5)
Location 0.392++
Nose 3 (6.4) 4 (19.0)
Ear 1 (2.1) 0 (0.0)
Forehead 2 (4.3) 2 (9.5)
Cheek 10 (21.3) 3 (14.3)
Around the eyes (eyelids and canthal
0 (0.0) 2 (9.5)
regions)
Temple 2 (4.3) 0 (0.0)
Different regions 4 (8.5) 2 (9.5)
Scalp 4 (8.5) 0 (0.0)
Upper limb (hand, arm) 5 (10.6) 3 (14.3)
Trunk (hip, front trunk, back trunk,
3 (6.4) 1 (4.8)
waist, neck)
Perineal 3 (6.4) 2 (9.5)
Lips 3 (6.4) 1 (4.8)
Lower extremity (leg, foot) 7 (14.9) 1 (4.8)
SD: Standard Deviation; IQR: Interquartile Range; + Mann Whitney U test; * Continuity Correction Test; ++ Pearson Chi-Square test

Diagnosed with malignant melanoma, there was a total of 6 patients, 2 women and 4 men. The average age was
79.50±4.95 (mean ± sd) for women and 57.75±8.14 (mean ± sd) for men. Out of 6 patients, there were 5 patients, with

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a known duration of the disease. Duration of disease was 0.60±0.56 (mean ± sd) in women and 0.67±0.29 years (Mean
± SD) in men. There were 5 patients between March 2020 and September 2019, and 1 patient between March 2020 and
September 2020. The primary lesions and their numbers were as follows: papule, nodule, ulcerated nodule, and
ulcerated plaque; 1, 3, 1, and 1, respectively. Locations of lesions and their numbers were as follows: trunk, foot; 2, 4,
respectively. Descriptive data of the patients with malignant melanoma were given in Table 5. The number of patients
with melanoma was low, and we did not perform statistical analysis.

Table 5 Descriptive data of patients with malignant melanoma

n (%)
Gender
Female 2 (33.3)
Male 4 (66.7)
Age
Female (Mean ± SD) 79.50±4.95
Male (Mean ± SD) 57.75±8.14
Time (year)
Female (Mean ± SD) (n = 2) 0.60±0.56
Male (Mean ± SD) (n = 3) 0.67±0.29
Group
March 2020- September 2019 5 (83.3)
March 2020- September 2020 1 (16.7)
Primary lesion
Papule 1 (16.7)
Nodule 3 (50.0)
Ulcerated nodule 1 (16.7)
Ulcerated plaque 1 (16.7)
Location
Trunk 2 (33.3)
Lower extremity (foot) 4 (66.7)

4. Discussion
The proportion of all skin biopsies taken was found to fall approximately one-third in our study, and a similar amount
of fall was also seen for the skin cancers. The effect of the pandemic was expected to be the reason for this decrease. It
was mentioned that, according to data obtained from Google Trends, during COVID-19, there was a
decline in online search activity for skin cancer and melanoma, with a particular decline in search activity
in March, April, and May [1]. It was stated that patients' interests shifting to that of COVID-19 is the reason for a
reduction in online health and information-seeking behavior for skin cancer and melanoma, and could therefore be
a factor that contributed to the observed decrease in skin cancer referrals [1].

In our study, we found patients with BCC applied to dermatology clinic were younger in the pandemic period. In the
study of Lallas et al. with 598 patients with skin cancer, patients with melanoma and basal cell carcinoma were found
to be significantly younger at the time of diagnosis in 2020 compared to those in previous years [2]. It was reported that
patients with squamous cell carcinoma also showed a similar trend [2]. Authors associated patients being young with
the growing concerns among older adults about COVID-19 [2]. In the pandemic, COVID -19 disease-associated deaths
were reported to rise with age: 0.1% to 0.2% for individuals aged 20 to 44 years, 0.5% to 0.8% for individuals aged 45

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to 54 years, 1.4% to 2.6% for individuals aged 55 to 64 years, 2.7% to 4.9% for individuals aged 65 to 74 years, 4.3% to
10.5% for individuals aged 75 to 84 years, and 10.4% to 27.3% for individuals aged ≥85 years [3]. In our study the
number of patients with SCC and MM was low, and that could be the reason for not finding statistical significance in our
patients with SCC.

We did not find significant differences in sex regarding the applications before and after the pandemic. In Lallas et al.’s
study, a higher than anticipated percentage of women was reported during the pandemic period and the authors
associated this with the men's growing concern over the serious COVID-19 consequences [2]. In Koh et al.’s study in
1992, about melanoma first detection in patients, men were reported as less likely than women to find their lesions (42
percent vs. 66 percent), and it was speculated that women might be more aware of potential changes to their skin [4].
Women with skin cancer predominance in the literature [2] after the pandemic could be the effect of both the pandemic
and the tendency to detect skin cancer compared to men.

We did not find significant differences in primary lesion types and their locations before and after the pandemic. In the
study from Ireland, it was stated that the Breslow thickness of melanomas increased during 2020's first two halves, and
that was attributed to delayed presentations caused by recurrent lockdowns and the shutdown of medical services [5].

In the literature, there are studies, conducted before the pandemic, and hence the effects of the pandemic were not
evaluated, concerning the factors affecting patients with skin cancers to apply to doctors. In our study, we did not
interview with the patients to ask which factors led them to apply dermatology clinic. In Koh et al.’s study, a survey of
216 patients with melanoma was performed, and about half of melanomas were reported to be found by the patients
themselves, in 25% of the cases, the spouse, a different family member, in the remaining 25% of cases, a
medical professional's physical examination was mentioned to reveal the lesion [4]. Regarding suspicious pigmented
lesions, 40 people were interviewed in Walter et al.’s study, it was reported that when a change was noticed by the
patient, a small size typically indicated a lack of seriousness, and the choice to seek assistance was influenced by the co-
occurrence of two or more changes, rapid growth, pain or lump [6]. In the same study, about half of the
interviewees were reported to have no worries about their moles and had never thought that a mole could be a sign of
a minor or serious illness; these individuals were described as being encouraged to seek assistance by worried spouses
or other family members, or a medical professional had observed a lesion during a consultation for a different reason
[6]. Future awareness campaigns were recommended to focus on the higher-risk demographics, like elderly men or
single people, and encourage family and friends to be responsible in recognizing changes in moles and
minimizing delays in seeking medical attention [6]. In De Giorgi et al.’s study, 802 melanoma patients were evaluated,
and the authors reported that self-detection was linked to a higher likelihood of a thick melanoma
and, consequently, a worse prognosis [7]. Self-examination with the help of a full-length mirror and a hand-held mirror
was recommended for detection of early melanoma [8].

There could be also false beliefs that keep patients from going to a hospital. In a study, a survey was carried out for 123
patients who had visited the Plastic Surgery Clinic within the last 5 years due to tumors on their face; when asked
if they thought that excising a lesion suspected of being neoplastic would accelerate the spread of the disease, 67
patients said "definitely yes" or "rather yes," while 45 patients were unsure, and eleven patients disagreed with this
statement [9]. Fear of surgery was cited by the majority of the study participants (n = 85) as the most significant factor
contributing to the delay in starting treatment; the authors have stated, that social education is necessary to help people
understand the risks associated with skin cancer development [9]. By informing patients that the surgery can be
performed under local anesthesia or sedation, their fear of general anesthesia, and hence surgery could be alleviated.

Skin cancer treatment could be postponed according to the guidelines. For melanoma, according to NCCN (National
Comprehensive Cancer Network) recommendation, patients with T0 to T1 tumors may postpone treatment for up to
three months if after biopsy no macroscopic residual disease remains; patients with ≥T2 disease may postpone
treatment for up to three months if biopsy margins are negative [3]. Regarding SCC, according to ACMS (American
College of Mohs Surgery), patients with small, well-differentiated cutaneous SCC and cutaneous SCC in situ may
postpone treatment for up to three months; it was stated that prioritization should be given to patients with tumors
that are enlarging, causing symptoms, or ulcerating; those with perineural involvement; those with
poorly differentiated tumors; and those with patient-specific risk factors (such as an immunocompromised state) [3].
For BCC, it was stated that, if the patient is not experiencing severe symptoms, treatment of BCC tumors can
be postponed for a minimum of three months [3]. Our patients’ treatments were scheduled according to the guidelines.

Telemedicine to screen skin cancer was reported to be useful in determining which skin lesions carry high-risk features
and which patients should be invited to the hospital to be treated as soon as possible in the COVID-19 pandemic [10].
Melanoma diagnosis delay could affect a patient’s survival more than the risk of COVID-19 disease transmission. It was

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reported that a delay of three months in diagnosing invasive melanoma was predicted to reduce the long-term 10-year
cancer-specific net survival by 3.13% to 12.56% in patients aged 30-39 to 80+ years old, respectively [11].

5. Conclusion
In our study, we found patients with BCC in the pandemic period were younger than before the pandemic, compatible
with the literature. Society could be educated about skin cancer symptoms, skin examination, and about false beliefs not
being true. Patients with suspicious skin lesions could be encouraged to visit a hospital with appropriate protection
from COVID-19 or teledermatology could be used to evaluate whether the suspicios lesions should be excised, biopsied,
followed, or patients invited to the hospital for physical examination.

Compliance with ethical standards

Disclosure of conflict of interest

No conflict of interest to be disclosed.

Statement of ethical approval

This study was conducted under the Helsinki criteria after approval by the Izmir Katip Çelebi University Ethics
Committee (approval number: 249, date 27.05.2021).

Statement of informed consent

Informed consent was obtained from all individual participants included in the study.

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