Pattern changes of cutaneous dermatoses among Iraqi women preceding and during the COVID-19 pandemic

Background: We compared the pattern of cutaneous dermatoses among Iraqi females of all ages between 4 months preceding the coronavirus disease 2019 (COVID-19) pandemic, and the same months 1 year later within the COVID-19 pandemic. Methods: This was a cross-sectional study, that targeted all female patients attending an outpatient clinic for dermatology and venereology in Al-Kindy teaching hospital, Baghdad between October 2019 to the end of January 2020, and the same 4-month duration 1 year later (October 2020 to the end of January 2021) after the COVID-19 peak period had passed and there was no or partial curfew to exclude seasonal impact. Results: A total of 2657 female-patients of all ages were enrolled in this study with 1314 females during the 4 months pre COVID-19, and 1343 females during the pandemic. The mean age of patients presented before the pandemic was 27.2±16.6 years, while the mean age of patients during the pandemic was 28.1±15.6 years with no statistically significant difference in mean ages (P >0.05). Hair loss in general with telogen effluvium specifically increased significantly. Cutaneous contagious viral infections were reduced significantly and specifically of these molluscum contagiosum and condylomata accuminata. Other forms of infections including bacterial and parasitic were also reduced while dermatophytosis was increased but not to a significant level. Acne vulgaris, rosacea, lichen planus, urticaria, pityriasis rosea, seborrheic dermatitis, and vitiligo were increased, but psoriasis, alopecia areata, other types of dermatitis, and melasma were reduced but none to a significant level. Conclusions: The COVID-19 pandemic resulted in changes in the pattern of diseases presented to an out-patient clinic for dermatology and venereology. This could be either related to COVID-19 infection or stress associated with the pandemic, because of curfew, or wearing facemasks which may cause a decrease or increase in certain diseases.

The Republic of Iraq officially reported the first confirmed case of COVID-19 on February 24, 2020 in Al-Najaf government and after that it started to increase in all cities of Iraq, and many measurements including total and partial curfew on week-ends had been taken in order to limit spread of infection. 3 The pattern of diseases including dermatological diseases started changing during the era of COVID-19 pandemic and a lot had been changed since then, 4 At that time, hygiene measures included face masks, different type of alcohol-based hand sanitizers, in liquid or gel forms, and diluted chlorine bleach for surfaces.
The aim of this study was to investigate the changes in the profile of dermatological diseases among Iraqi females of all ages before and during the COVID-19 pandemic.

Ethical approval
The study was approved by scientific committee (Research Ethics Committee) of Al-Kindy college of medicine, university of Baghdad. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards (Code: 2019/C081). All patients attending the Al-Kindy teaching hospital in Baghdad are routinely informed that their data could be used for medical research, and their personal information would not be disclosed. In cases below the age of 18 years, the patients care giver would be responsible for giving the approval. If patients do not consent, their data is not shared.

Study design and setting
This study involved a cross-sectional survey carried out in the out-patient clinic for dermatology and venereology in Al-Kindy teaching hospital, Baghdad. The data was collected from the medical records of all enrolled female patients who attended the out-patient clinic for 8 months, 4 of them before the first COVID-19 case was diagnosed in Iraq (from October 2019 to the end of January 2020), and the other four months 1 year later (from October 2020 to the end of January 2021) to exclude seasonal impact.

Participants
The data were collected retrospectively from all female patients attending the dermatology out-patient's clinic during the study period. Inclusion criteria included female patients of any age who were examined by the same dermatologist and had been given a definitive diagnosis. Exclusion criteria was if a definitive diagnosis had not been recorded.

Variables
The study variables included patients' age and the definite dermatological diagnosis for each patient.

Data sources and measurement
Diagnosis was made by clinical examination. Some cases required specific investigation in the form of dermoscopic and wood-light examination, scraping test, routine histopathological examination and immunohistochemistry for selected cases to confirm diagnosis.

Bias
This study mainly faced two types of bias: selection bias and information bias. Some degree of selection bias was evident because the cases enrolled were examined by the same dermatologist, which was done to ensure that the steps of examination and diagnosis was offered to all patients had similar quality, the other cause of selection bias that this was a

REVISED Amendments from Version 2
Added a note about the main hygiene measures used in Iraq at time of sample collection and clarified more about the term "uncommon dermatoses" that was utilized in the current study.
Any further responses from the reviewers can be found at the end of the article single center study. Information bias was limited because the data entry was double checked and that any case without a clear and definite diagnosis was excluded from the study.

Statistical analysis
The collected data were analyzed by Statistical Package for the Social Sciences (SPSS), version 22. The descriptive analysis focused on frequencies, and percentages, and percent change. While the Chi-square (goodness of fit) test was used to find the associations between variables and significance of percent change. A P-value ≤ 0.05 was considered statistically significant.

Results
A total of 2657 female patients were enrolled in this study with 1314 before the COVID-19 pandemic, and 1343 1-year into the pandemic. 14 The mean age of patients during the period before COVID-19 was 27.2 AE 16.6 years, while the mean age of patients during the pandemic was 28.1 AE 15.6 years. There was no significant difference between the mean age of the patients before and during the COVID-19 pandemic (P-value > 0.05). Table 1 shows that hair loss in general was significantly increased during COVID-19 pandemic. Viral infections in general reduced significantly, while diseases like lichen planus, pityriasis rosea, urticaria, rosacea, vitiligo, acne vulgaris, cutaneous fungal infections, and cutaneous leishmaniasis all increased. On the other hand, bacterial and parasitic infections, psoriasis, pruritis, melasma, and dermatitis were decreased but not to a significant level. Uncommon dermatosis included more than 80 different dermatoses like cases with pemphigus vulgaris, bullous pemphigoid, dermatitis herpetiformis, erythema multiforme, and pityriasis rubra pilaris. 14 Cutaneous viral infections in general reduced significantly during COVID era, specially molluscum contagiosum and condylomata accuminata, while herpes zoster increased but it was not significant ( Table 2). There was a reduction in the percentage of the most common forms of cutaneous bacterial infections after the peak of the COVID-19 pandemic, but it was not statistically significant (Table 3). Dermatophytosis increased while cutaneous candidiasis decreased but neither were statistically significant (Table 4).   Parasitic infections including scabies and pediculosis decreased during COVID-19 pandemic but also not statistically significant (Table 5).
Hair loss in general and telogen effluvium specifically increased significantly from the pre COVID-19 period. Cases of female baldness, trichotillomania, and acquired hair shaft anomaly had increased, and cases of alopecia areata and traction alopecia had decreased, however, these changes were not statistically significant (Table 6).
Seborrheic dermatitis and to little extent contact dermatitis increased, while all other types of dermatitis were reduced, and all are not statistically significant (Table 7).

Discussion
There are many cutaneous manifestations that appeared to be associated with COVID-19 infection. [5][6][7] To the best of our knowledge, this is the only study investigating the pattern of dermatologic diseases among Iraqi women who presented to an outpatient dermatological clinic in the 4 months before COVID-19 outbreak and compared to the same 4 months one year later that were not in the partial or complete curfew. In this study we choose only female patients of all ages because we believe that females are more aware of their skin and hair than males in our society.
Kutlu and Metin 2020 from Turkey compared 2 months (April and May 2019) to the same months in 2020 which were at the beginning of the era of COVID-19. They found that wart, molluscum contagiosum, and dermatophytosis were significantly decreased while scabies increased over this time period. 4 Also Turkmen et al. 2021 founded a highly significantly increase in scabies during pandemic months and an increase in herpes zoster but there was a reduction in wart, while other cutaneous infections was not changed. 7 In our study all types of cutaneous infections and infestations which are contagious like viral, bacterial, and parasitic had decreased but not to a significant level except for molluscum contagiosum and condylomata accuminata which may have been due to closure and curfew, decreasing of extra-marital sexual activity, and decreased families visiting each other. Although herpes zoster is considered to be viral infection, it was probably increased as it results from reactivation of a latent virus and not a new infection.
Dermatophytosis in our study had increased 1 year after the start of the pandemic but not to a significant level mostly because many families bought pets to their children during a period of ban, and these were the source of most dermatophytosis in our cases.
Kutlu and Metin found that telogen effluvium and Alopecia areata increased significantly, 4 however, Turkmen et al.
reported only alopecia areata was increased significantly and telogen effluvium was not changed, 7 while in our study hair loss in general with telogen effluvium specifically was increased significantly because of fever due to COVID-19 infection which is considered an important cause of telogen effluvium. 8 Alopecia areata cases may have decreased because it is a chronic disease and asymptomatic so patients may have postponed visiting a dermatologic clinic to avoid COVID-19 infection.
Lichen planus, pityriasis rosea, and urticaria were increased during COVID-19 era but not to a significant level; the reason may be because pityriasis rosea and urticaria have been reported in many studies to be associated with COVID-19 infection as a direct or indirect cause, 5,9 but lichen planus was not, and because these diseases are itchy and their cutaneous lesions are usually generalized, patients may have worried about their illness and if it is related to COVID-19 infection or not. Psoriasis and melasma are usually chronic diseases, sometimes asymptomatic, so some patients might have postponed attending to dermatology clinic, which may explain the reduction in frequency of these disease during the COVID-19 pandemic; however, Kutlu and Metin and Turkmen et al. reported that psoriasis frequency increased significantly during the COVID-19 pandemic. 4,7 Acne vulgaris and rosacea had increased during the pandemic but also not to a significant level. This increase may have been due to wearing a face mask to reduce the risk of contamination; Han C in 2020 reported an increased flare of acne caused by long time mask wearing during the pandemic, and they attributed that to long-time mask wearing which could increase the flare of acne due to higher temperature and humidity on the surface of facial skin caused by expired air and the perspiration, 10 this could also explain the increase in rosacea.
All types of dermatitis decreased except seborrheic dermatitis but not to a significant level. This may be due to the fact that most acne patients have some sort of seborrheic dermatitis, so because acne was increasing, seborrheic dermatitis increased too. Singh M and Abtahi B during COVID-19 (March through April 2020) found that there was an increase of irritant contact dermatitis among the general population likely due to overuse of antiseptic agents and frequent hand and face washing. [11][12][13] Limitations of the study There are some limitations to our study. These are that this research was a single center study and data was only measured over a short period (October to January) which cannot cover all dermatological diseases that could increase or decrease in a certain season.

Conclusions
The COVID-19 pandemic resulted in changes in the diseases presented to an out-patient clinic for dermatology and venereology. This could be either related to infection with COVID-19 or stress associated with the pandemic or because of closure and wearing mask.

Open Peer Review
the subject and the structure of the work are not particularly original, since many papers have been published about it. The interest is mainly linked to the geographic area of the authors.
The main other criticisms are as follows: Since public hygiene measures aimed at preventing COVID-19 are different in different countries and have changed over time, those concerning the area under study should be specified in the introduction.

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The reason why only female patients were included in the study should be specified, and the data possibly compared with those relating to male patients.

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The number of patients included in the two groups is surprisingly similar: the authors should better specify how the two groups were formed. Furthermore, it is not clear whether it is possible that the same patient is placed in both groups, if she had access to dermatological services before and after COVID-19.

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Since among the pathologies that have undergone to a significant reduction there is that of "uncommon dermatoses", and that this includes dermatoses of different origin, it should be stratified, to understand which pathology is actually responsible for the variation.

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Similarly, it is possible to group the pathologies on the basis of the cause (i.e. inflammatory, immunological genesis, etc.). This should in particular replace Table 7, the function of which is unclear.

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The relationship between cases with telogen effluvium and COVID-19 infection should be clarified, specifying how many patients had COVID-19, and the temporal relationship of the infection to hair loss.

Is the work clearly and accurately presented and does it cite the current literature? Partly
Is the study design appropriate and is the work technically sound? Partly

If applicable, is the statistical analysis and its interpretation appropriate? Partly
Are all the source data underlying the results available to ensure full reproducibility? Partly

Are the conclusions drawn adequately supported by the results? Partly
Competing Interests: No competing interests were disclosed.

Reviewer Expertise: Dermatology
I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.