Burden of skin disease and associated socioeconomic status in Europe: An ecologic study from the Global Burden of Disease Study 2017.

INTRODUCTION: Dermatoses contribute to a large burden of global disease, but the relationship between socioeconomic status and the effect of dermatologic conditions in Europe is not well understood.
METHODS: We selected Global Burden of Disease Study data sets to analyze disability-adjusted life-years (DALYs) and the annual rate of change of dermatoses between 1990 and 2017 in 43 European countries. The principal country-level economic factor used was gross domestic product per capita from the World Bank. Statistical analysis was performed with Spearman ρ correlation.
RESULTS: Wealthier European countries had higher DALYs for melanoma, basal cell carcinoma, psoriasis, atopic dermatitis, acne, seborrheic dermatitis, alopecia, asthma, contact dermatitis, and viral skin disease. Poorer countries had higher DALYs of squamous cell carcinoma, urticaria, decubitus ulcers, pruritus, scabies, tuberculosis, and syphilis. Thirteen European countries were in the top 10th percentile globally for annual increase in skin and subcutaneous disease burden.
CONCLUSION: The majority of European countries have experienced an increase in skin and subcutaneous diseases in recent decades relative to the rest of the world, but the burden of individual dermatoses in Europe varies by country and socioeconomic status. DALYs can potentially serve as a purposeful measure for directing resources to improve the burden of skin disease in Europe.

Understanding the regional effect of dermatologic disease is critical to developing a concerted and sustained global effort toward reducing this burden.

A relationship exists between socioeconomic status, geographic location, and certain dermatoses. Resources should be directed at countries with high disability-adjusted life-years to create influential interventions in Europe.

Introduction

Skin conditions are one of the leading contributors to the global burden of disease. They affect people of all cultures and ages and are associated with substantial morbidity. Skin and subcutaneous diseases were the fourth leading cause of nonfatal disease burden and disability worldwide in 2010 and 2013, emphasizing dermatology's expanding role and importance in global health., Skin disease burden can be measured with disability-adjusted life-years (DALYs), calculated as the sum of the years lost because of premature death and years lost because of living with disability. The burden of dermatoses has been steadily increasing; the total DALYs globally caused by skin and subcutaneous diseases increased from 1.21% in 1990 to 1.76% in 2017. Certain cutaneous disorders have been shown to cause a disproportionate number of DALYs in relation to their corresponding prevalence, such as fungal skin diseases, atopic dermatitis, and scabies.

Socioeconomic factors play a major role in skin disease morbidity and quality of life. The Socio-Demographic Index was developed to identify where countries or other geographic areas are in their aspects of development. It is a composite average of income per capita, average educational attainment, and fertility rate and expressed on a scale of 0 to 1. Socioeconomic burden in part depends on health care delivery models, the availability of therapy for skin diseases, and the cost of medications. Across geographic borders, the burden of skin disease varies. For example, Western Europe experiences a greater burden from psoriasis and acne vulgaris, and additionally it shows the highest total rate of DALYs from skin disease compared with Central and Eastern Europe.

Although skin disease is prevalent throughout Europe, the relationship between socioeconomic status and skin burden of disease is not well understood. Understanding the geographic variations in skin disease burden provides information that can help address these inequalities. This observational study compared the relationship between socioeconomic status and burden of skin disease in Europe in 2017 and investigated the annual percentage change of common skin diseases between 1990 and 2017.

Methods

Data source

The principal country-level economic factor used to measure socioeconomic status was 2017 data for gross domestic product per capita from the World Bank. Information on the DALYs of the most common dermatoses was obtained from the latest publicly available Global Burden of Disease Study 2017 data sets, which provide data to compare the effect of diseases, injuries, and risk factors across age groups, sexes, countries, and regions from 1990 to the present for greater than 350 diseases in 195 countries. The Global Burden of Disease Study project is led by the Institute for Health Metrics and Evaluation at the University of Washington and collaborates with greater than 145 countries and 3600 researchers worldwide. A detailed protocol is available from the institute on how data are obtained, incorporated, calculated, and published in the Global Burden of Disease Study.

Study design

This study was an ecologic observational analysis including the entire European population. Individual European country demographics are provided (Table I). A global map of the percentage change of age-standardized prevalence rates of skin and subcutaneous disease per 100,000 population from 1990 to 2017 of all 195 Global Burden of Disease Study countries is provided (Fig 1). Age-standardized DALYs per 100,000 of skin and subcutaneous diseases, melanoma, and nonmelanoma skin cancers were also compared with the absolute Socio-Demographic Index values of 43 European countries in 2017 (Figs 2 and 3).

Table I

European country profiles

Country	Population	Per-capita GDP, $	Fertility rate	Educational attainment, years	Female life expectancy, years	Male life expectancy, years	Mortality <5	Mortality <1
Albania	2.8M	11,466	1.9	10.2	82.1	75.0	12.7	10.7
Andorra	80.0K	69,202	1.2	13.3	85.1	80.6	1.9	1.1
Armenia	3.0M	8505	1.6	12.1	78.7	72.4	9.6	8.1
Austria	8.8M	45,465	1.5	13.0	84.0	79.4	3.4	2.9
Azerbaijan	10.2M	16,349	2.0	11.3	74.7	67.2	35.2	30.9
Belarus	9.5M	18,282	1.6	12.4	78.8	66.1	6.5	5.1
Belgium	11.3M	42,569	1.7	14.1	83.8	78.9	3.6	3.0
Bosnia and Herzegovina	3.4M	10,762	1.3	10.5	79.1	74.3	6.4	5.6
Bulgaria	7.1M	18,957	1.5	13.5	78.6	71.3	7.7	6.5
Croatia	4.3M	22,271	1.4	13.2	81.6	75.4	4.3	3.6
Cyprus	1.3M	31,531	1.0	13.2	85.2	78.5	2.9	2.5
Czech Republic	10.6M	32,611	1.6	13.5	82.0	76.3	2.9	2.3
Denmark	5.7M	45,244	1.7	15.0	82.7	78.8	3.7	3.3
Estonia	1.3M	28,542	1.6	14.2	82.1	73.7	3.0	2.2
Finland	5.5M	40,215	1.6	14.5	84.3	78.6	2.2	1.8
France	65.7M	38,992	1.8	13.7	85.7	79.8	3.9	3.1
Georgia	3.7M	9486	2.0	12.8	77.3	68.4	11.1	9.5
Germany	83.3M	45,446	1.4	13.0	83.0	78.3	3.6	3.0
Greece	10.4M	25,232	1.4	12.4	83.6	78.4	4.5	3.8
Hungary	9.7M	26,491	1.4	12.8	80.2	73.2	4.8	4.1
Iceland	337.5K	47,062	1.8	15.1	85.9	79.8	2.2	1.5
Ireland	4.9M	64,037	1.8	13.1	83.7	80.0	3.4	3.0
Italy	60.6M	35,079	1.3	12.6	85.3	80.8	3.2	2.7
Kazakhstan	17.9M	23,781	2.4	11.4	76.4	67.5	14.1	11.3
Latvia	1.9M	24,227	1.6	13.6	79.9	70.2	4.9	4.0
Lithuania	2.8M	28,645	1.6	13.7	80.2	69.6	4.8	3.9
Luxembourg	590.5K	97,887	1.5	14.0	83.3	80.0	2.1	1.7
Malta	434.5K	36,920	1.5	12.5	83.0	78.9	6.0	5.4
Moldova	3.7M	4915	1.3	11.9	77.4	68.2	14.4	12.7
Montenegro	626.3K	15,716	1.7	13.0	78.9	74.1	4.0	3.3
Netherlands	17.0M	48,405	1.7	14.5	83.1	79.9	3.9	3.3
North Macedonia	2.2M	13,628	1.5	11.9	79.7	73.9	9.6	8.6
Norway	5.3M	63,501	1.7	14.1	84.2	80.5	2.6	2.0
Poland	38.4M	26,735	1.3	13.8	81.8	74.1	4.4	3.8
Portugal	10.7M	28,158	1.3	10.9	84.2	78.5	3.4	2.8
Romania	19.4M	22,535	1.6	12.8	79.0	71.6	8.7	7.3
Russia	146.2M	24,427	1.6	12.5	77.2	66.8	7.4	6.0
Serbia	8.9M	13,959	1.4	11.8	77.9	73.6	5.0	4.4
Slovakia	5.4M	30,067	1,4	13.6	80.6	74.1	5.9	5.0
Slovenia	2.1M	31,251	1.5	13.8	84.2	77.9	2.2	1.7
Spain	46.4M	34,908	1.4	11.9	85.8	80.2	3.2	2.6
Sweden	10.0M	46,388	1.8	13.7	84.2	80.8	2.7	2.3
Switzerland	8.6M	56,296	1.5	12.9	85.7	82.1	3.8	3.3
Turkey	80.5M	22,903	1.8	10.1	83.1	75.2	14.2	11.5
Ukraine	44.7M	8548	1.4	13.1	76.5	64.7	9.5	7.5
United Kingdom	66.6M	39,708	1.7	12.8	82.7	79.2	4.4	3.8

All data are from 2017. Mortality rates less than 1 and less than 5 are measured in deaths per 1,000 live births. Total fertility rate is the average number of children a woman would deliver during her lifetime.

GDP, Gross domestic product; K, thousand; M, million.

Fig 1

Percentage change in age-standardized prevalence rate of skin and subcutaneous disease per 100,000 population from 1990 to 2017.

Fig 2

Age-standardized disability-adjusted life-years rates from skin and subcutaneous disease by Socio-Demographic Index score for European countries in 2017. DALY, Disability-adjusted life-year; SDI, Socio-Demographic Index.

Fig 3

Age-standardized disability-adjusted life-years rates from melanoma (blue) and nonmelanoma skin cancer (orange) by Socio-Demographic Index score for European countries in 2017. DALY, Disability-adjusted life-year; SDI, Socio-Demographic Index.

Statistical analysis

Three broad categories of dermatoses were analyzed for each European country: neoplastic, inflammatory, and infectious. Statistical analysis of correlations (Spearman ρ) was performed with SPSS Statistics (version 25.0, IBM Corp, Armonk, NY). Statistical significance was set at P < .05. European countries were organized in a heat table by gross domestic product per capita by least wealthy (top rows) to most wealthy (bottom rows) and DALYs ranking of each country were numerically ranked from 1 (highest DALYs, red) to 195 (lowest DALYs, blue) for each disease analyzed (Fig 4). A positive correlation between gross domestic product per capita and DALYs ranking showed that as a country's gross domestic product per capita increased, the DALYs ranking approached 195 (lower DALYs), whereas a negative correlation signified that as gross domestic product per capita increased, the DALYs ranking approached 1 (higher DALYs). Additionally, by using the DALYs per 100,000 in European countries and all 195 countries worldwide between 1990 and 2017, we measured the annual percentage change of skin and subcutaneous diseases, melanoma, nonmelanoma skin cancer, basal cell carcinoma (BCC), squamous cell carcinoma (SCC), lip and oral cancer, seborrheic dermatitis, contact dermatitis, pruritus, pyoderma, decubitus ulcer, cellulitis, fungal infection, and tuberculosis (Table II).

Fig 4

European countries ordered with rows from highest (least wealthy) to lowest (most wealthy) and each country numerically ranked in the world from 1 (highest disability-adjusted life-years, red) to 195 (lowest disability-adjusted life-years, blue) for each disease in 2017. ACN, Acne; ALO, alopecia areata; AST, asthma; ATO, atopic dermatitis; BCC, basal cell carcinoma; B&H, Bosnia and Herzegovina; CEL, cellulitis; CON, contact dermatitis; DEC, decubitus ulcer; FUN, fungal skin disease; LEI, leishmaniasis; MEL, melanoma; NMS, nonmelanoma skin cancer; ORA, oral/lip cancer; PRU, pruritus; PSO, psoriasis; PYO, pyoderma; Rep, Republic; SCA, scabies; SCC, squamous cell carcinoma; SEB, seborrheic dermatitis; SYP, syphilis; TUB, tuberculosis; UK, United Kingdom; URT, urticaria; VIR, viral skin disease.

Table II

Notable top 10th percentile world rankings of European countries by annual percentage change from 1990 to 2017, measured in disability-adjusted life-years per 100,000

Disease	European country	World ranking
Skin and subcutaneous disease	Malta	1
	Portugal	6
	Germany	7
	Cyprus	9
	Spain	10
	Belgium	11
	Netherlands	13
	Italy	14
	Greece	15
	Austria	16
	Greenland	17
	Norway	18
	Finland	19
Melanoma	Lithuania	5
	Belarus	9
	Greece	12
	Latvia	15
	Portugal	16
	Bulgaria	17
	Ukraine	19
Nonmelanoma skin cancer	Bosnia and Herzegovina	8
	Macedonia	13
	Latvia	14
BCC	Portugal	2
	Romania	3
	Poland	4
	Germany	5
	Netherlands	11
	Serbia	13
	Slovenia	15
	Cyprus	16
	Latvia	17
SCC	Bosnia and Herzegovina	8
	Macedonia	13
	Latvia	14
Lip and oral cancer	Romania	6
	Ukraine	19
Seborrheic dermatitis	Greenland	3
Contact dermatitis	Albania	5
Pruritus	Albania	3
	Bosnia and Herzegovina	7
Pyoderma	Ukraine	11
	Belgium	13
	Netherlands	20
Decubitus ulcer	Bosnia and Herzegovina	20
Cellulitis	Ukraine	10
	United Kingdom	16
Fungal infection	Malta	3
	Lithuania	5
	Greece	6
	Slovenia	8
	Portugal	9
	Croatia	11
	Italy	12
	Spain	13
	Latvia	14
	Bulgaria	16
	Estonia	17
	Finland	18
	Bosnia and Herzegovina	20
Tuberculosis	Ukraine	3
	Russia	10
	Belarus	11
	Lithuania	16

BCC, Basal cell carcinoma; SCC, squamous cell carcinoma.

Results

European countries were shown to have a cluster of high skin and subcutaneous disease burden when the global map of percentage change in age-standardized prevalence rate from 1990 to 2017 was examined (Fig 1). In comparison of the geographic regions of Europe, Western Europe showed a higher percentage change compared with Eastern European countries.

When age-standardized DALYs rates caused by skin and subcutaneous diseases in 2017 were compared, several European countries, such as Norway, Sweden, France, Greenland, and the United Kingdom, had higher-than-expected age-standardized DALYs rates according only to their Socio-Demographic Index score (Fig 2). Other countries, including Macedonia, Montenegro, Slovak Republic, Lithuania, and Slovenia, had lower-than-expected age-standardized DALYs rates. A similar comparison was performed of age-standardized DALYs rates caused by melanoma and nonmelanoma skin cancer and associated Socio-Demographic Index score in 2017 across the same countries (Fig 3). Norway, Sweden, Denmark, Slovenia, and the Netherlands were among the countries with a higher-than-expected age-standardized DALYs rate caused by melanoma, whereas others such as Montenegro, Cyprus, Spain, and Malta had a much lower-than-expected rate. The difference in age-standardized DALYs rates was not as prevalent when nonmelanoma skin cancer was assessed.

For the neoplastic category, there was a positive correlation between DALYs rankings and gross domestic product per capita for SCC (0.68) (Fig 4). In contrast, there was a negative correlation for BCC (–0.54) and melanoma (–0.31). For the inflammatory category, there was a positive correlation between DALYs rankings and gross domestic product per capita for urticaria (0.73), decubitus ulcer (0.61), and pruritus (0.70) and a negative correlation for acne (–0.88), psoriasis (–0.89), atopic dermatitis (–0.81), seborrheic dermatitis (–0.72), alopecia (–0.66), asthma (–0.68), and contact dermatitis (–0.67). Last, for the infectious category, there was a positive correlation between DALYs rankings and gross domestic product per capita for scabies (0.74), tuberculosis (0.75), and syphilis (0.38) and a negative correlation for viral skin diseases (–0.76).

Between 1990 and 2017, 13 European countries were in the top 10th percentile in the world for annual percentage change in skin and subcutaneous disease, including Malta (first), Portugal (sixth), Germany (seventh), and Cyprus (ninth) (Table II). Lithuania (fifth) and Belarus (ninth) ranked in the top 10 globally for annual percentage change in melanoma DALYs, whereas Bosnia and Herzegovina (eighth) was within the top 10 for nonmelanoma skin cancer. Regarding BCC, Portugal (second), Romania (third), Poland (fourth), and Germany (fifth) were part of the top 10 countries, whereas Bosnia and Herzegovina (eighth) was ranked in the top 10 for SCC. Fungal infections were highly prevalent in Europe, with 13 countries composing the top 20 countries worldwide for annual change: Malta (third), Lithuania (fifth), Greece (sixth), Slovenia (eighth), and Portugal (ninth) were in the top 10. Additionally, 4 European countries made up the top 10th percentile for annual change in tuberculosis, with Ukraine ranked third.

Discussion

Our results showed that wealthier European countries had higher DALYs of BCC, melanoma, acne, psoriasis, atopic dermatitis, seborrheic dermatitis, alopecia, asthma, contact dermatitis, and viral skin diseases. On the other hand, European countries with lower socioeconomic status had higher DALYs of SCC, urticaria, decubitus ulcer, pruritus, scabies, tuberculosis, and syphilis.

European countries with a higher gross domestic product per capita have been strongly associated with increased risk of melanoma and nonmelanoma skin cancer.12, 13, 14 It is suggested this risk is due to increased ultraviolet exposure from more frequent sun-seeking trips in more affluent regions. Although high socioeconomic status is strongly associated with BCC risk, this association is weaker in SCC. BCC arises de novo with no precursor lesions, whereas SCC precursor lesions include actinic keratoses and Bowen disease, suggesting that their etiologies may differ. Additionally, SCC has been shown to be associated with occupational sun exposure (high lifetime cumulative exposure to ultraviolet radiation), whereas melanoma and BCC have been associated with recreational or nonoccupational sun exposure., Our results show that SCC is higher in poorer European countries, which may be explained by an increase of outdoor working environments.

Poverty is a major risk factor for poor health because of the lack of decent living standards, sanitation, and clean water. Resource-poor environments cause high morbidity rates, especially for transmissible skin diseases. Common and treatable transmissible skin diseases are associated with household crowding and lack of hygiene, which are reflections of low socioeconomic status., Our results demonstrated that countries with lower gross domestic product per capita had higher DALYs of many infectious dermatoses, such as scabies, tuberculosis, and syphilis, which could be due to housing and living situation discrepancy.

We found psoriasis burden to be greatest in high-income European countries. Previous studies of patients in the United States and France have shown a significant association between lower educational level and poor control and severity of psoriasis., In contrast, a recent study examining psoriasis on a global scale showed a higher burden of psoriasis in high-income countries, with Western Europe ranking second in a regional comparison of psoriasis prevalence.

It has been reported that higher socioeconomic status is associated with a higher prevalence and DALYs of atopic diseases. A link between atopic diseases and particulate air pollution from motor vehicles has been previously shown. Furthermore, individuals living in a metropolitan area and higher educational levels have been associated with a higher prevalence of eczema. The “hygiene hypothesis” proposes that the increased prevalence of allergic diseases in more developed countries is explained by improved living conditions, antibiotic use, and childhood vaccinations, resulting in the reduction of infections. The immunologic mechanism underlying the hygiene hypothesis is not well understood, but one mechanism suggests that the lack of microbial burden in developed countries redirects the typical immunoresponse from a strong T helper cell type 1 immunity toward a T helper cell type 2 phenotype, predisposing the host to allergic disorders. Our results support these findings because wealthier European countries presented with higher DALYs caused by atopic dermatitis, which is possibly explained by the increased prevalence in the region.

Limitations of the Global Burden of Disease Study have been described, including inconsistent reporting of mortality by skin disease in assessing DALYs. Disability reflects only symptoms such as itch and appearance including disfigurement, not capturing other complications such as secondary infection and mental illness. There are also potential limitations inherent in our descriptive study design and population, including the ecologic fallacy. It is possible that there are confounding intrinsic or extrinsic systematic differences between individuals of different countries, such as Fitzpatrick skin types or environmental factors such as climate or air pollution. Future studies with an analytic approach on an individual level may be warranted before potential public health solutions are addressed. Despite these limitations, understanding the relationship between socioeconomic status on geographic burden of common skin diseases is a valuable step in developing measurable, influential, and sustainable interventions to reduce disease morbidity in both resource-rich and -poor countries.

Dermatologic diseases pose significant burdens on the health status and quality of life for patients. Europe in particular is heavily affected by skin and subcutaneous diseases; 13 European countries are in the top 10th percentile for annual change in these diseases worldwide. To adequately address these issues, efforts should be focused on dermatoses with the highest DALYs in their respective countries.