Abstract
Understanding the effects of age on the epidemiology of diseases primarily affecting the skin is important to the practice of dermatology, both for proper allocation of resources and for optimal patient-centered care. To fully appreciate the effect that age may have on the population-based calculations of incidence of diseases primarily affecting the skin in Olmsted County, Minnesota, and worldwide, we performed a review of all relevant Rochester Epidemiology Project–published data and compared them with similar reports in the worldwide English literature. Using the Rochester Epidemiology Project, population-based epidemiologic studies have been performed to estimate the incidence of specific skin diseases over the past 50 years. In older persons (>65 y), nonmelanoma skin cancer, lentigo maligna, herpes zoster, delusional infestation, venous stasis syndrome, venous ulcer, and burning mouth syndrome were more commonly diagnosed. In those younger than 65 years, atypical nevi, psoriatic arthritis, pityriasis rosea, herpes progenitalis, genital warts, alopecia areata, hidradenitis suppurativa, infantile hemangioma, Behçet disease, and sarcoidosis (isolated cutaneous, with sarcoidosis-specific cutaneous lesions and with erythema nodosum) had a higher incidence. Many of the incidence rates by age group of diseases primarily affecting the skin derived from the Rochester Epidemiology Project were similar to those reported elsewhere.
Keywords: epidemiology, skin diseases, statistical review
Introduction
As the world population grows and changes, so too does disease incidence (new disease over time in a population) change. For diseases that primarily affect the skin, incidence trends in the literature over time and by category may help us to coordinate the appropriate allocation of resources in clinical practice, patient-centered care, and research in dermatology. Therefore, an understanding of which skin diseases are more prominent with age is important.
For instance, it is well established in the literature that nonmelanoma skin cancers are more common in the elderly. The incidence of melanoma skin cancer, however, has increased markedly in younger age groups, especially among women (1), and the incidence of nonmelanoma skin cancer is also increasing in this younger age group. Diseases for which incidences are less commonly reported in the literature and which are perhaps less researched (although no less important for our patients and professions), such as hidradenitis suppurativa, appear to be more common in men and women in their twenties (2). The mechanisms whereby a person’s age influences the function and integrity of the integumentary system have yet to be fully elucidated, but exposure to extrinsic factors such as UV radiation and tobacco, genetics, endocrine and hormonal dysregulation, and inflammation may all influence the multifaceted pathogenesis of disease in skin over time (3). For diseases such as hidradenitis suppurativa, an epidemic of obesity and weight gain may affect the age-related incidence of this disease.
The Rochester Epidemiology Project (REP) is an extensive medical records linkage system founded in 1966, whereby the medical records of almost all residents of Olmsted County, Minnesota, United States, may be used for the epidemiologic study of disease over the past 50 years (4,5). Although there are some limitations in the generalizability of data cultivated from the REP owing to a less racially and ethnically diverse population, the ability to obtain a multitude of health information from a population of approximately 150,000 people in a well-defined geographic region has been helpful.
In 2 previous publications, incidences of diseases primarily affecting the skin were reported 1) without subcategorization and 2) subsequently stratified by sex (6,7), with a comparison to reports from the world literature in 1 of the studies (7). The purpose of our study is to better understand age-specific incidence rates (IRs) of diseases that primarily affect the skin in Olmsted County and, similarly, age-specific IRs worldwide.
Materials and Methods
The highest IRs (per 100,000 person-years) by age group for diseases primarily affecting the skin were collected from all of the REP studies in Olmsted County, Minnesota, generated between 1966 and June 2016. Studies in which these data were included as a figure(s), rather than numerically defined, were excluded. Studies reporting appropriate data but with fewer than 10 patients in the analysis were also excluded from our study. The following parameters were recorded for each report fitting our inclusion criteria: source, study period, skin disease, age, number of cases, age group, and highest IR per 100,000 person-years by age and sex, similar to previous studies (6,7).
We subsequently performed a search of the worldwide English-language literature describing age-specific IRs for diseases that primarily affect the skin during our study period of 1966 through June 2016 by using PubMed. If appropriate data were present but analyses were performed on 10 or fewer patients, the study was not included in our review. Some studies reported only overall IRs by age group with no subclassification by sex, and vice versa; these studies were included. Similar to a previous publication (7), we limited our world literature review to 5 publications per disease in each of 5 main categories (which were also used in previous publications [6,7]): 1) skin cancer, 2) connective tissue diseases, 3) papulosquamous diseases including psoriatic arthritis, 4) infections and infestations, and 5) other skin diseases. For each disease, we chose to limit our search to a maximum of 5 most-relevant publications.
We used the following search terms for the English-language literature via PubMed: incidence AND age-specific incidence AND basal cell carcinoma OR squamous cell carcinoma OR atypical nevi OR lentigo maligna OR cutaneous melanoma OR systemic lupus erythematosus (SLE) (definite, suspected, or combined), OR mixed connective tissue disease OR primary Sjögren syndrome OR psoriasis OR psoriatic arthritis OR pityriasis rosea OR herpes zoster OR herpes progenitalis OR condyloma acuminatum (genital warts) OR cutaneous nontuberculous mycobacterial infection OR delusional infestation OR alopecia areata OR hidradenitis suppurativa OR infantile hemangioma OR Behçet disease OR venous stasis syndrome OR burning mouth syndrome OR leukocytoclastic vasculitis OR sarcoidosis (isolated cutaneous, or systemic with sarcoidosis-specific cutaneous lesions or systemic with erythema nodosum).
We abstracted the same parameters from each of the studies meeting our criteria as outlined above and additionally included study method and geographic area. We found no comparative studies meeting our criteria for the following diseases: atypical nevi, mixed connective tissue disease, pityriasis rosea, herpes progenitalis, cutaneous nontuberculous mycobacterial infection, delusional infestation, hidradenitis suppurativa, infantile hemangioma, burning mouth syndrome, leukocytoclastic vasculitis, and sarcoidosis; either studies were not found, age-specific IRs were not reported, or age-specific IRs were presented as figures rather than numerically reported.
Results
Results from REP studies are summarized in Table 1. In general, nonmelanoma skin cancer, lentigo maligna, herpes zoster, delusional infestation, venous stasis syndrome, venous ulcer, and burning mouth syndrome were more commonly diagnosed in the elderly. In contrast, persons younger than 65 years in Olmsted County were more likely to have atypical nevi, psoriatic arthritis, pityriasis rosea, herpes progenitalis, genital warts, alopecia areata, hidradenitis suppurativa, infantile hemangioma, Behçet disease, and sarcoidosis (isolated cutaneous, with sarcoidosis-specific cutaneous lesions and with erythema nodosum).
Table 1.
Source | Study Period | Skin Disease | Age, y | N | Highest Incidence Rate Per 100,000 Person-Years by Age and Sex
|
|||||
---|---|---|---|---|---|---|---|---|---|---|
Age Group, y | Both Sexes | Age Group, y | Female | Age Group, y | Male | |||||
Skin Cancer | ||||||||||
Chuang et al (8) | 1976–1984 | BCC | All | 657 | ≥85 | 950.2 | ≥85 | 927.8 | 75–84 | 1,043.4 |
Christenson et al (9) | 1976–2003 | BCC | ≤40 | 417 | 36–39 | 93 | 36–39 | 99.6 | 36–39 | 86.1 |
Christenson et al (9) | 1976–2003 | SCC | ≤40 | 68 | 36–39 | 17.4 | 36–39 | 12.5 | 36–39 | 22.6 |
Chuang et al (8) | 1976–1984 | SCC | All | 169 | ≥85 | 446.3 | ≥85 | 371.1 | ≥85 | 706.5 |
Gray et al (10) | 1984–1992 | SCC | All | 511 | ≥85 | 874 | ≥85 | 758.4 | ≥85 | 1,286 |
Adaji et al (11) | 2000–2005 | Atypical nevi | All | 631 | 30–39 | 143.1 | 30–39 | 155.5 | 30–39 | 130.4 |
Mirzoyev et al (12) | 1970–2007 | Lentigo maligna | ≥18 | 145 | 70–79 | 28.5 | ≥80 | 12.6 | 70–79 | 51.9 |
Popescu et al (13) | 1950–1985 | CMM | All | 107 | ≥70 | 23.5 | ≥70 | 16.8 | ≥70 | 37.3 |
Resseguie et al (14) | 1950–1974 | CMM | All | 42 | ≥60 | 8.8 | 40–59 | 8 | ≥60 | 15.5 |
Connective Tissue Disease | ||||||||||
Kurland et al (15)a | 1951–1967 | SLE | All | 29 | 45–64 | 9.2 | ≥65 | 13.6 | 45–64 | 12.4 |
Michet et al (16) | 1950–1979 | Definite SLE | All | 258 | ≥65 | 4.8 | 25–44 | 6.3 | ≥65 | 4.5 |
Michet et al (16) | 1950–1979 | Suspected SLE | All | 21 | ≥65 | 4.8 | ≥65 | 7.5 | N/A | N/A |
Nobrega et al (17) | 1950–1959 | Combined SLE | All | 8 | 45–54 | 5.1 | ≥55 | 7.5 | 45–54 | 5.8 |
Nobrega et al (17) | 1960–1965 | Combined SLE | All | 17 | 45–54 | 15.6 | ≥55 | 14.5 | 45–54 | 34.8 |
Ungprasert et al (18) | 1985–2014 | Mixed connective tissue disease | ≥18 | 50 | 60–69 | 3 | 60–69 | 4.3 | 60–69 | 1.6 |
Pillemer et al (19)b | 1976–1992 | Primary Sjögren syndrome | All | 53 | All | 3.2 | 55–64 | 22.7 | ≥75 | 8.7 |
Nannini et al (20) | 1976–2005 | Primary Sjögren syndrome | ≥18 | 105 | 65–74 | 12.7 | 65–74 | 21.8 | ≥75 | 7.5 |
Papulosquamous Disease Including Psoriatic Arthritis | ||||||||||
Icen et al (21) | 1970–2000 | Psoriasis | ≥18 | 1,633 | 60–69 | 94.2 | 50–59 | 90.7 | 60–69 | 115.3 |
Bell et al (22)c | 1980–1983 | Psoriasis | All | 132 | 60–69 | 112.6 | 60–69 | 126.5 | ≥70 | 130.6 |
Wilson et al (23) | 1969–1999 | Psoriatic arthritis | ≥18 | 147 | 50–59 | 9.6 | 50–59 | 10.5 | 30–39 | 12.2 |
Shbeeb et al (24) | 1982–1991 | Psoriatic arthritis | ≥20 | 66 | ≥20 | 6.59 | 40–59 | 13.38 | 20–39 | 10.8 |
Chuang et al (25) | 1969–1978 | Pityriasis rosea | All | 939 | 20–24 | 454 | 20–24 | 523.2 | 20–24 | 305 |
Infections and Infestations | ||||||||||
Guess et al (26) | 1960–1981 | Herpes zoster | <20 | 173 | 15–19 | 63 | 15–19 | 58 | 15–19 | 71 |
Yawn et al (27) | 1996–2001 | Herpes zoster | ≥22 | 1,669 | ≥80 | 1,140 | ≥80 | 910 | ≥80 | 1,070 |
Kawai et al (28)d | 2000–2007 | Herpes zoster | All | 8,017 | ≥80 | 1,070 | All | 3.44 | All | 2.61 |
Chuang et al (29) | 1965–1979 | Herpes progenitalis | All | 392 | 20–24 | 197 | 20–24 | 210 | 20–24 | 170 |
Chuang et al (30) | 1950–1978 | Condyloma acuminatum | All | 746 | 20–24 | 298 | 20–24 | 322 | 20–24 | 247 |
Wentworth et al (31) | 1980–2009 | Cutaneous nontuberculous mycobacterial infection | All | 40 | ≥60 | 2.2 | N/A | N/A | N/A | N/A |
Bailey et al (32) | 1976–2010 | Delusional infestation | All | 64 | ≥80 | 10 | ≥80 | 7.2 | ≥80 | 16.2 |
Other Skin Diseases | ||||||||||
Safavi et al (33) | 1975–1989 | Alopecia areata | All | 292 | 30–39 | 29.3 | 50–59 | 31.4 | 30–39 | 31.3 |
Mirzoyev et al (34) | 1990–2009 | Alopecia areata | All | 530 | 30–39 | 30.1 | 20–29, 40–49 | 27.1 | 30–39 | 37.2 |
Vazquez et al (2) | 1968–2008 | Hidradenitis suppurativa | All | 268 | 20–29 | 13.3 | 20–29 | 18.4 | 20–29 | 7.4 |
Anderson et al (35)e | 1976–2010 | Infantile hemangioma | ≤3 | 999 | ≤3 | 1,640 | 60–89 days | 7,910 | 60–89 days | 3,410 |
Calamia et al (36) | 1960–2005 | Behçet disease | ≥18 | 13 | 18–29 | 0.75 | 18–29 | 1.14 | 30–39 | 0.59 |
Heit et al (37) | 1966–1990 | Venous stasis syndrome | ≥15 | 1,131 | ≥85 | 349.7 | ≥85 | 364.8 | ≥85 | 306.3 |
Heit et al (37) | 1966–1990 | Venous ulcer | ≥15 | 263 | ≥85 | 124.9 | ≥85 | 134.7 | ≥85 | 96.7 |
Kohorst et al (38) | 2000–2010 | Burning mouth syndrome | All | 169 | 80–89 | 48.1 | 70–79 | 70.3 | 70–79 | 18.4 |
Arora et al (39) | 1996–2010 | Leukocytoclastic vasculitis | All | 84 | 60–69 | 9.7 | 60–69 | 9.3 | ≥70 | 10.9 |
Ungprasert et al (40) | 1976–2013 | Isolated cutaneous sarcoidosis | ≥18 | 26 | 40–49 | 1.5 | 40–49 | 2.3 | 60–69 | 1.4 |
Ungprasert et al (40) | 1976–2013 | Systemic sarcoidosis with sarcoidosis-specific cutaneous lesions | ≥18 | 36 | 40–49 | 2 | 50–59 | 3.4 | 40–49 | 1.7 |
Ungprasert et al (40) | 1976–2013 | Systemic sarcoidosis with erythema nodosum | ≥18 | 26 | 40–49 | 1.5 | 40–49 | 2 | 30–39 | 1.1 |
Abbreviations: BCC, basal cell carcinoma; CMM, cutaneous malignant melanoma; N/A, not available; SCC, squamous cell carcinoma; SLE, systemic lupus erythematosus.
Standardized to the 1960 census.
Hole punched in the manuscript copy, but data were not obscured.
Standardized to the 1980 Rochester census.
Highest incidence rate for both sexes was originally reported as cases/1,000 person-years and has been adjusted to cases/100,000 person-years.
ncidence rates were originally reported as cases/100 person-years and have been adjusted to cases/100,000 person-years.
Table 2 summarizes the literature published in English on non-REP studies. In general, nonmelanoma skin cancer was diagnosed more commonly in persons older than 70 years. Malignant melanoma and melanoma in situ were diagnosed more frequently in those older than 65 years. Herpes zoster and venous leg ulcer were also more common in the elderly. In contrast, lentigo maligna, SLE, psoriatic arthritis, pityriasis rosea, genital warts, and Behçet disease were more likely to be diagnosed in persons younger than 65 years.
Table 2.
Source | Study Period |
Skin Disease |
Method | Location | Age, y | N | Highest Incidence Rate Per 100,000 Person-Years by Age and Sex |
|||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Age Group, y |
Both Sexes |
Age Group, y |
Female | Age Group, y |
Male | |||||||
Skin Cancer | ||||||||||||
de Vries et al (41) | 1998–2000 | BCC | Review of incident data using the Eindhoven Cancer Registry | Southeast Netherlands | All | 23,511 | N/A | N/A | ≥70 | 340 | ≥70 | 533 |
Bielsa et al (42) | 2006–2007 | BCC | Review of diagnosed cases registered by dermatologists in Barcelona’s Nord county | Spanish Mediterranean | All | 936 | 80–84 | 2,197 | 80–84 | 1,523 | ≥85 | 3,910 |
Celic et al (43) | 2003–2005 | BCC | Data collection by questionnaire designed by Croatia committee of dermatology and venereology of ministry of health and social welfare | Croatia | All | 7,244 | N/A | N/A | ≥80 | 326.8 | ≥80 | 652.3 |
Sella et al (44) | 2006–2011 | BCC | Data collected from MHS, with histology and laboratory confirmation | Israel | All | 16,079 | ≥80 | 999 | All | 158 | All | 225 |
Hoey et al (45) | 1993–2002 | BCC | Data collected from NICR in the province, with pathology confirmed | Northern Ireland | All | 14,442 | N/A | N/A | ≥70 | 405 | ≥70 | 579 |
Sella et al (44) | 2006–2011 | SCC | Data collected from MHS, with histology and laboratory confirmation | Israel | All | 4,767 | ≥80 | 612 | All | 41 | All | 78 |
Hoey et al (45) | 1992–2002 | SCC | Data collected from NICR in the province, with pathology confirmed | Northern Ireland | All | 6,401 | N/A | N/A | ≥70 | 209 | ≥70 | 401 |
Staples et al (46) | 2002 | SCC | Face-to-face interviews conducted by market research company | Australia | All | 286 | ≥70 | 2,972 | ≥70 | 2,146 | ≥70 | 3,979 |
Karagas et al (47) | 1979–1980 | SCC | Physicians and pathology laboratory in New Hampshire and bordering regions; reported cases during time period | New Hampshire, Vermont | All | 160 | N/A | N/A | ≥75 | 84.3 | ≥75 | 331.1 |
Karagas et al (47) | 1993–1994 | SCC | Physicians and pathology laboratory in New Hampshire and bordering regions; reported cases during time period | New Hampshire | All | 779 | N/A | N/A | ≥75 | 361 | ≥75 | 1,239 |
Sella et al (44) | 2006–2011 | Invasive melanoma | Data collected from MHS, with histology and laboratory confirmation | Israel | All | 1,264 | 70–79 and ≥80 | 64 | All | 16 | All | 19 |
Hoey et al (45) | 1993–2002 | MM | Data collected from NICR in the province, with pathology confirmed | Northern Ireland | All | 1,866 | N/A | N/A | ≥70 | 35 | ≥70 | 35 |
Howlett et al (48)a | 1998–2002 | MM | New cases were registered with Nova Scotia Cancer Registry | Nova Scotia | All | 925 | N/A | N/A | ≥65 | 44.9 | ≥65 | 80 |
Cossu et al (49) | 1992–2011 | MM | Epi data obtained from local tumor registry of the Italian association for tumor registries | North Sardinia, Italy | All | 532 | N/A | N/A | 75–79 | 10.7 | ≥85 | 20.4 |
Hoejberg et al (50) | 2012 | MM | NORDCAN database used to collect cancer incidence in Nordic countries | Denmark | All | 2,046 | N/A | N/A | 0–69 | 803 | 0–69 | 665 |
Sella et al (44) | 2006–2011 | MIS | Data collected from MHS, with histology and laboratory confirmation | Israel | All | 714 | 70–79 | 40 | All | 8 | All | 12 |
Weinstock et al (51)b | 2002–2009 | MIS | Cross-sectional study of Medicare part B claims for beneficiaries ≥65 y | USA | ≥65 | N/A | 75–85 | 75.2 | >65 | 37.7 | >65 | 100.7 |
Wang et al (52)c | 1992–2011 | MIS | Data collected from SEER database | USA | All | 49,313 | >65 | 22.72 | All | 5.77 | All | 7.95 |
Helvind et al (53) | 2008–2012 | MIS | Data from the Danish Melanoma Group Database | Denmark | All | 1,615 | N/A | N/A | >60 | 1.96 | >60 | 2.6 |
Iannacone et al (54)d | 1982–2010 | MIS | Data collected from the Queensland cancer registry | Queensland, Australia | 15–24 | 192 | 20–24 | 9.2 | 20–24 | 9.8 | 20–24 | 8.6 |
Wang et al (52)c | 1992–2011 | Lentigo maligna melanoma | Data collected from SEER database | USA | All | 49,313 | >65 | 7.69 | All | 0.77 | All | 2.21 |
Newell et al (55)e | 1973–1981 | Lentigo maligna | Data collected from SEER database | USA | >30 | 1,107 | >30 | N/A | >30 | 0.6 | >30 | 0.8 |
Greveling (56)f | 1989–2013 | Primary lentigo maligna | Data collected using the Netherlands Cancer Registry and PALGA: Dutch Pathology registry | Netherlands | All | 10,545 | All | 3.84 (2013) | All | 4.16 (2013) | All | 3.57 (2013) |
Greveling (56)f | 1989–2013 | Lentigo maligna melanoma | Data collected using the Netherlands Cancer Registry and PALGA: Dutch Pathology registry | Netherlands | All | 2,989 | All | 1.19 (2013) | All | 1.18 (2013) | All | 1.25 (2013) |
Holman et al (57) | 1975–1976 | Pre-MM | Hospital records of Western Australia residents using a computerized hospital morbidity reporting system; histopathology records used to confirm incident cases | Western Australia | All | 120 | N/A | N/A | 40–49 | 16.3 | ≥80 | 22.1 |
Connective Tissue Disease | ||||||||||||
Lerang et al (58) | 1999–2008 | SLE | Data collected from the national population register | Norway | >16 | 116 | 16–19 | 4.6 | N/A | N/A | N/A | N/A |
Hochberg (59) | 1970–1977 | SLE | Medical record review from 19, 14, and 5 hospitals in Baltimore, within Baltimore city limits, and in Baltimore county, respectively | Baltimore, Maryland | All | 302 | 25–34 | 7.69 | 45–54 white | 7.23 white | 35–44 white | 1.21 white |
Hochberg (59) | 1970–1977 | SLE | Medical record review from 19, 14, and 5 hospitals in Baltimore, within Baltimore city limits, and in Baltimore county, respectively | Baltimore, Maryland | All | 302 | 25–34 | 7.69 | 25–34 black | 21.57 black | 55–64 black | 5.06 black |
See et al (60) | 2005–2009 | SLE | Data collected from the Taiwan NHIRD | Taiwan | All | 358 | All | 7.2 | All | 12.8 | All | 1.5 |
Weng et al (61) | 2005–2007 | Primary Sjögren syndrome | Data collected using the incidence of reported disease through the Bureau of National Health Insurance of Taiwan | Taiwan | >15 | 3,352 | 65–74 | 13.5 | 55–64 | 23.4 | 65–74 | 4 |
See et al (60) | 2005–2009 | Primary Sjögren syndrome | Data collected from the Taiwan NHIRD | Taiwan | All | 583 | All | 11.8 | All | 20.1 | All | 3.3 |
Papulosquamous Disease Including PA | ||||||||||||
Huerta et al (62) | 1996–1997 | Psoriasis | Data collected using the United Kingdom General Practice Research Database | United Kingdom | All | 3,994 | 50–59 | 16.7 | 50–59 | 17.2 | 70–79 | 22.4 |
Kaipiainen-Seppanen (63) | 1990 | PA | Nationwide sickness insurance database in Finland | Finland | >16 | 65 | 45–54 | 11.8 | 45–54 | 9 | 45–54 | 10 |
Soriano et al (64) | 2000–2006 | PA | Data collected from the Hospital Italiano Medical Care Program | Buenos Aires, Argentina | >18 | 35 | 45–64 | 11.6 | 45–64 | 7.7 | 45–64 | 18.1 |
Soderlin et al (65)g | 1999–2000 | PA | Prospective population-based annual incidence study. General practitioners in participating centers referred patients to the rheumatology department in Vaxjo | Southern Sweden | >16 | 151 | >16 | 1.1 | >16 | 1.2 | >16 | 0.5 |
Savolainen et al (66) | 2000 | PA | Survey study of patients with at least 1 peripheral joint with synovitis or signs of inflammation at a visit | Finland | All | 199 | Adults | 23 | N/A | N/A | N/A | N/A |
Alamanos et al (67) | 1982–1991 | PA | Patients referred to rheumatology clinics in Ioannina University Hospital and Ioannina General Hospital | Northwest Greece | All | 221 | All (45–64) | 1.96 | All (45–64) | 2.18 | All (45–64) | 1.74 |
Alamanos et al (67) | 1992–2001 | PA | Patients referred to rheumatology clinics in Ioannina University Hospital and Ioannina General Hospital | Northwest Greece | All | 221 | All | 3.76 | All | 3.8 | All | 3.73 |
Kyriakis et al (68) | 1995–2002 | Pityriasis rosea | Hospital-based cross-sectional study | Athens, Greece | All | 479 | 31–35 | 17.5 | 21–25 | 20.2 | 6–10 | 16 |
Infections and Infestations | ||||||||||||
Brisson et al (69) | 1991–2000 | Herpes zoster | Data collected from the Royal College of General Practitioners Weekly Returns Service | England and Wales | All | 224,818 | ≥65 | 932 | N/A | N/A | N/A | N/A |
Civen et al (70)h | 2007–2010 | Herpes zoster | Surveillance site for varicella and zoster with reports by schools and healthcare providers every 2 wk using a standard questionnaire | Antelope Valley, CA | 0–19 | 229 | 10–19 | 78.2 | N/A | N/A | N/A | N/A |
Esteban-Vassalo et al (71) | 2005–2012 | Herpes zoster | Cross-sectional study from the Madrid Regional Public Health System, electronic records in primary care | Madrid, Spain | All | 211,650 | ≥75 (2012) | 1,127.74 (2012) | 65–74 (2011) | 1,190.07 (2011) | ≥75 (2012) | 1,021.94 (2012) |
Hillebrand et al (72) | 2005–2009 | Herpes zoster | Retrospective cohort study of health insurance members | Germany | All | 215,959 | ≥85 | 9.4 | All | 8.3 | All | 5.5 |
Mullooly et al (73) | 1997–2002 | Herpes zoster | Incidence rates from Kaiser Permanente Health Plan | USA | All | 369 | All | 215 | ≥80 | 1,194.30 | All | 1,256.70 |
Camenga et al (74)i | 2000–2005 | Genital warts | Enrollees of Northern California Kaiser Permanente | USA | 11–29 | 181,264 | 20–24 | 470 | 20–24 | 630 | 20–24 | 270 |
Bollerup et al (75) | 2008 | Genital warts | Data collected from Danish National Patient Registry + prescription medications for genital warts | Denmark | All | 117,792 | N/A | N/A | 18–19 | 1,808 | 22–25 | 1,828 |
Bollerup et al (75) | 2013 | Genital warts | Data collected from Danish National Patient Registry + prescription medications for genital warts | Denmark | All | 117,792 | N/A | N/A | 22–25 | 774 | 22–25 | 1,247 |
Persson et al (76)j | 1989–1990 | Genital warts | Data collected from all clinics treating STDs in Boris | Sweden | 10–60 | 440 | 20–24 | 1,200 | 15–19 | 1,400 | 25–29 | 640 |
Pirotta et al (77)j | 2000–2006 | Genital warts | Cross-sectional database collection with Bettering the Evaluation of Care and Health database | Australia | All | 64,600 | All | 168 | 20–24 | 861 | 25–29 | 740 |
Other Skin Diseases | ||||||||||||
See et al (60) | 2005–2009 | Behçet disease | Data collected from the Taiwan NHIRD | Taiwan | All | 42 | All | 0.9 | All | 1.1 | All | 0.6 |
Mohammad et al (78) | 1997–2010 | Behçet disease | Study among 3 health care districts in Sweden using a clinical registry | Southern Sweden | ≥15 | 20 | 25–34 | 0.5 | ≥15 | 0.1 | ≥15 | 0.3 |
Margolis et al (79)k | 1988–1996 | Venous leg ulcer | Data collected from the general practice research database for Philadelphia and Baltimore | Northeast USA | 65–95 | 65 | N/A | N/A | 91–95 | 0.02 | 91–95 | 0.03 |
Abbreviations: BCC, basal cell carcinoma; Epi, epidemiology; MHS, Maccabi Health Care Services; MIS, melanoma in situ; MM, malignant melanoma; N/A, not available; NHIRD, National Health Insurance Research Dataset; NICR, Northern Ireland population-based cancer registry; PA, psoriatic arthritis; SCC, squamous cell carcinoma; SEER, Surveillance, Epidemiology, and End Results Program; SLE, systemic lupus erythematosus; STDs, sexually transmitted diseases.
Based on 1991 standard population.
Rate/100,000 Medicare beneficiaries.
Age-standardized using the US 2000 census population.
Data based on the 1970 US male or female population.
European standardized rate.
Age-standardized to the 2000 World Standard Population.
Incidence was originally reported as cases per million (2003 Taiwan population) and has been adjusted to cases/100,000 person-years.
Data were originally reported as cases per million and has been adjusted to cases/100,000 person-years.
Based on US census data.
Rates were originally reported as cases per 1,000 person-years and have been adjusted to cases/100,000 person-years.
Rates were originally reported as cases per 100 person-years and have been adjusted to cases/100,000 person-years.
Discussion
Skin Cancer
In Olmsted County, nonmelanoma skin cancer, including basal cell and squamous cell carcinoma, was more commonly diagnosed in persons older than 85 years, except in one study in which IRs were generated in a population younger than 40 years (8–10). World literature reports were similar; both nonmelanoma skin cancers were most commonly diagnosed after age 70 years (41–45).
REP studies highlighted an increased likelihood of diagnosis of cutaneous malignant melanoma in Olmsted County in persons older than 60 years, with the highest reported incidence for women occurring in the 40- to 59-year-old age group in one study (13,14). In the world literature, the highest incidence of malignant melanoma and melanoma in situ was in those aged 65 years and older (44–51). Of note, premalignant melanoma in a study in western Australia was more commonly diagnosed in men older than 80 years, whereas women were most commonly aged 40 to 49 years (57). In Olmsted County, lentigo maligna was more commonly diagnosed in those aged 70 years and older (12). Incidence reports in the world literature of lentigo maligna and lentigo maligna melanoma by age group are not as definitive; more studies outlining incidence by age may be of benefit to improve our epidemiologic knowledge of these specific skin diseases (52,55,56).
Connective Tissue Diseases
Age group does not as easily delineate trends in incidence of connective tissue diseases from the REP. This may be partly due to the different definitions used to describe a diagnosis of SLE, including SLE, definite SLE, suspected SLE, and combined SLE. In general, the highest incidences of SLE occurred in those older than 45 years in Olmsted County (15–18). Two world studies showed the highest incidence of SLE by age group to be in persons ages 16 to 19 years and 35 to 44 years, respectively, with contrasting age groups by sex and race in a study from Baltimore, Maryland (58,59). For mixed connective tissue disease, the highest incidence was reported in persons aged 60 to 69 years in Olmsted County.
Patients in Olmsted County with primary Sjögren syndrome were more likely to receive a diagnosis after age 75 years if male and between 55 and 75 years if female (19, 20). Similarly, in Taiwan, those aged 65 to 74 years were more likely to have primary Sjögren syndrome (61).
Papulosquamous Diseases
In Olmsted County, psoriasis was more commonly diagnosed in persons aged 60 to 69 years in 2 REP-derived studies, with the highest incidence occurring in men at a later age than in women, whereas for psoriatic arthritis the opposite was true; more men had a psoriatic arthritis diagnosis at an earlier age (21–24). Similar findings were noted elsewhere for psoriatic arthritis (63,64,67).
Pityriasis rosea was uniformly more common in 20- to 24-year-olds in both men and women in Olmsted County (25). In Athens, Greece, most diagnoses were made in persons aged 31 to 35 years and between the ages of 21 and 25 years and 6 and 10 years in female and male patients, respectively (68).
Skin Infections and Infestations
Herpes zoster in Olmsted County was diagnosed predominantly in those aged 80 years and older in the 2 studies in which the population comprised adults (27,28). Similarly, the incidence of herpes zoster in adults in the world literature was highest in persons older than or equal to 65, 75, and 85 years, depending on the study (69, 71–73). Herpes progenitalis in Olmsted County was most commonly diagnosed in women of childbearing age, 20 to 24 years; the same was true for genital warts (29,30). The incidence of genital warts was comparatively highest in persons of reproductive potential in Northern California, Denmark, Sweden, and Australia (74–77).
Cutaneous nontuberculous mycobacterial infection was most commonly diagnosed in those older than 60 years; delusional infestation was typically diagnosed in persons older than 80 years in Olmsted County (31,32).
Other Skin Diseases
In REP studies, alopecia areata was more commonly diagnosed in persons aged 30 to 39 years (33,34). Hidradenitis suppurativa was more commonly diagnosed in those aged 20 to 29 years (2). Behçet disease was more commonly diagnosed between the ages of 18 and 29 years in Olmsted County, with an increased age at diagnosis for men (30–39 years) (36). Similarly, a study performed in southern Sweden demonstrated Behçet disease as diagnosed most commonly in the 25- to 34-year-old age group for combined sexes (78).
In Olmsted County, venous stasis syndrome and venous ulcer were most commonly diagnosed in men and women older than 85 years (37). Results were similar worldwide, with diagnosis in men and women more commonly after age 90 years (79).
Burning mouth syndrome was most commonly diagnosed after age 80 years, leukocytoclastic vasculitis after age 60 years, and sarcoidosis after age 40 years in Olmsted County (38–40). Interestingly, men had systemic sarcoidosis with specific cutaneous lesions and with erythema nodosum earlier than women, whereas isolated cutaneous sarcoidosis was more commonly diagnosed in women at an earlier age (40).
Study Strengths and Limitations
We recognize several strengths and limitations of our study. The REP is extremely useful for obtaining standardized data in a population over time. We believe that this compilation of data in comparison with international studies is helpful for recognition of skin disease in the elderly across the globe, with consideration toward allocation of future resources. The specific limitations regarding the use of REP studies are further outlined in a previous publication (6). We recognize that our method of article selection and search criteria may introduce bias into our review and may not provide a wholly comprehensive picture of the age-related incidence of certain diseases. Also, whereas choosing 5 articles may be suitable for frequently occurring diseases, further investigation and reporting of IRs in rarer diseases would be valuable. We also recognize the difficulty in comparing REP studies with studies from the world literature, specifically because of differences in study design, population characteristics, age groups, and eligibility criteria reported in each study. Also, reporting IRs as standardized or crude rates may or may not affect how data compare between REP and world literature studies. Meta-analyses and meta-regression analyses were not performed because of scarcity of data pertaining to age-related incidences for certain diseases. Future studies and analyses may contribute to a more comprehensive appreciation of age-related incidence rates regarding this topic, as well as provide information about bias across studies. Future studies may also evaluate the effects of obesity and weight gain on the incidence of diseases primarily affecting the skin, which is outside the scope of the current review. We do also recognize that the extent of this review, as well as the time period used for the collection of data, is large, which reflects the large amounts of data available for comparison through the REP. Using a study period of 1966 through June 2016 is a limitation of our study in that more recent trends in IRs may not be as accurately portrayed. We included the dates of relevant studies and note that for some diseases a stricter time period would have excluded studies for rarer diseases. In addition, our use of the REP is a limitation in that certain diseases common in the elderly, such as actinic keratosis and chronic actinic dermatitis, were not included in our review.
Conclusion
We describe several reports of diseases primarily affecting the skin subcategorized by age group, particularly examining data accumulated by the REP from 1966 to the present and gathering comparative data within the world literature. Our results indicate that several of these skin diseases may have increased incidences within certain age group categories. Despite differences in study methodologies and designs, we found similarities in skin diseases by age group between the REP and world literature studies. Nonmelanoma skin cancers, herpes zoster, and venous ulcer were found to be of highest incidence in the elderly, whereas psoriatic arthritis, pityriasis rosea, genital warts, and Behçet disease were less likely to be diagnosed in the elderly. We believe that further subcategorization of diseases that primarily affect the skin encourages appropriate use of resources in our field and advancement in the knowledge of dermatologic disease for research, optimal patient-centered care, and population health initiatives. We also believe that highlighting those diseases for which incidence subcategorization by age is scarce indicates that further study in these areas may be undertaken.
Acknowledgments
This study was made possible using the resources of the Rochester Epidemiology Project, which is supported by the National Institute on Aging of the National Institutes of Health under Award Number R01AG034676. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Abbreviations
- IR
incidence rate
- REP
Rochester Epidemiology Project
- SLE
systemic lupus erythematosus
Footnotes
Authorship Disclosure: No relevant financial or nonfinancial relationships to disclose.
Publisher: To expedite proof approval, send proof via email to scipubs@mayo.edu.
References
- 1.Nikolaou V, Stratigos AJ. Emerging trends in the epidemiology of melanoma. Br J Dermatol. 2014;170:11–9. doi: 10.1111/bjd.12492. [DOI] [PubMed] [Google Scholar]
- 2.Vazquez BG, Alikhan A, Weaver AL, et al. Incidence of hidradenitis suppurativa and associated factors: a population-based study of Olmsted County, Minnesota. J Invest Dermatol. 2013;133:97–103. doi: 10.1038/jid.2012.255. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Kanaki T, Makrantonaki E, Zouboulis CC. Biomarkers of skin aging. Rev Endocr Metab Disord. 2016;17:433–42. doi: 10.1007/s11154-016-9392-x. [DOI] [PubMed] [Google Scholar]
- 4.Rocca WA, Yawn BP, St Sauver JL, et al. History of the Rochester Epidemiology Project: half a century of medical records linkage in a US population. Mayo Clin Proc. 2012;87:1202–13. doi: 10.1016/j.mayocp.2012.08.012. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Melton LJ., 3rd History of the Rochester Epidemiology Project. Mayo Clin Proc. 1996;71:266–74. doi: 10.4065/71.3.266. [DOI] [PubMed] [Google Scholar]
- 6.Andersen LK, Davis MD. The epidemiology of skin and skin-related diseases: a review of population-based studies performed by using the Rochester Epidemiology Project. Mayo Clin Proc. 2013;88:1462–7. doi: 10.1016/j.mayocp.2013.08.018. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Andersen LK, Davis MD. Sex differences in the incidence of skin and skin-related diseases in Olmsted County, Minnesota, United States, and a comparison with other rates published worldwide. Int J Dermatol. 2016;55:939–55. doi: 10.1111/ijd.13285. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Chuang TY, Popescu A, Su WP, Chute CG. Basal cell carcinoma: a population-based incidence study in Rochester, Minnesota. J Am Acad Dermatol. 1990;22:413–7. doi: 10.1016/0190-9622(90)70056-n. [DOI] [PubMed] [Google Scholar]
- 9.Christenson LJ, Borrowman TA, Vachon CM, et al. Incidence of basal cell and squamous cell carcinomas in a population younger than 40 years. JAMA. 2005;294:681–90. doi: 10.1001/jama.294.6.681. [DOI] [PubMed] [Google Scholar]
- 10.Gray DT, Suman VJ, Su WP, et al. Trends in the population-based incidence of squamous cell carcinoma of the skin first diagnosed between 1984 and 1992. Arch Dermatol. 1997;133:735–40. [PubMed] [Google Scholar]
- 11.Adaji A, Gaba P, Lohse CM, Brewer JD. Incidence of atypical nevi in Olmsted County: an epidemiological study. J Cutan Pathol. 2016;43:557–63. doi: 10.1111/cup.12709. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Mirzoyev SA, Knudson RM, Reed KB, et al. Incidence of lentigo maligna in Olmsted County, Minnesota, 1970 to 2007. J Am Acad Dermatol. 2014;70:443–8. doi: 10.1016/j.jaad.2013.11.008. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Popescu NA, Beard CM, Treacy PJ, et al. Cutaneous malignant melanoma in Rochester, Minnesota: trends in incidence and survivorship, 1950 through 1985. Mayo Clin Proc. 1990;65:1293–302. doi: 10.1016/s0025-6196(12)62140-5. [DOI] [PubMed] [Google Scholar]
- 14.Resseguie LJ, Marks SJ, Winkelmann RK, Kurland LT. Malignant melanoma in the resident population of Rochester, Minnesota. Mayo Clin Proc. 1977;52:191–5. [PubMed] [Google Scholar]
- 15.Kurland LT, Hauser WA, Ferguson RH, Holley KE. Epidemiologic features of diffuse connective tissue disorders in Rochester, Minn., 1951 through 1967, with special reference to systemic lupus erythematosus. Mayo Clin Proc. 1969;44:649–63. [PubMed] [Google Scholar]
- 16.Michet CJ, Jr, McKenna CH, Elveback LR, et al. Epidemiology of systemic lupus erythematosus and other connective tissue diseases in Rochester, Minnesota, 1950 through 1979. Mayo Clin Proc. 1985;60:105–13. doi: 10.1016/s0025-6196(12)60294-8. [DOI] [PubMed] [Google Scholar]
- 17.Nobrega FT, Ferguson RH, Kurland LT, Hargraves MM. Lupus erythematosus in Rochester, Minnesota, 1950-1965: a preliminary study. In: Bennett PH, Wood PHN, editors. Proceedings of the Third International Symposium on Population Studies of the Rheumatic Diseases. New York (NY): Excerpta Medica; 1966. pp. 259–66. (Excerpta Medica International Congress Series No. 148). [Google Scholar]
- 18.Ungprasert P, Crowson CS, Chowdhary VR, et al. Epidemiology of mixed connective tissue disease, 1985-2014: a population-based study. Arthritis Care Res (Hoboken) 2016;68:1843–48. doi: 10.1002/acr.22872. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Pillemer SR, Matteson EL, Jacobsson LT, et al. Incidence of physician-diagnosed primary Sjogren syndrome in residents of Olmsted County, Minnesota. Mayo Clin Proc. 2001;76:593–9. doi: 10.4065/76.6.593. [DOI] [PubMed] [Google Scholar]
- 20.Nannini C, Jebakumar AJ, Crowson CS, et al. Primary Sjogren’s syndrome 1976-2005 and associated interstitial lung disease: a population-based study of incidence and mortality. BMJ Open. 2013;3:e003569. doi: 10.1136/bmjopen-2013-003569. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Icen M, Crowson CS, McEvoy MT, et al. Trends in incidence of adult-onset psoriasis over three decades: a population–based study. J Am Acad Dermatol. 2009;60:394–401. doi: 10.1016/j.jaad.2008.10.062. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Bell LM, Sedlack R, Beard CM, et al. Incidence of psoriasis in Rochester, Minn, 1980-1983. Arch Dermatol. 1991;127:1184–7. [PubMed] [Google Scholar]
- 23.Wilson FC, Icen M, Crowson CS, et al. Time trends in epidemiology and characteristics of psoriatic arthritis over 3 decades: a population-based study. J Rheumatol. 2009;36:361–7. doi: 10.3899/jrheum.080691. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Shbeeb M, Uramoto KM, Gibson LE, et al. The epidemiology of psoriatic arthritis in Olmsted County, Minnesota, USA, 1982-1991. J Rheumatol. 2000;27:1247–50. [PubMed] [Google Scholar]
- 25.Chuang TY, Ilstrup DM, Perry HO, Kurland LT. Pityriasis rosea in Rochester, Minnesota, 1969 to 1978. J Am Acad Dermatol. 1982;7:80–9. doi: 10.1016/s0190-9622(82)80013-3. [DOI] [PubMed] [Google Scholar]
- 26.Guess HA, Broughton DD, Melton LJ, 3rd, Kurland LT. Epidemiology of herpes zoster in children and adolescents: a population-based study. Pediatrics. 1985;76:512–7. [PubMed] [Google Scholar]
- 27.Yawn BP, Saddier P, Wollan PC, et al. A population-based study of the incidence and complication rates of herpes zoster before zoster vaccine introduction. Mayo Clin Proc. 2007;82:1341–9. doi: 10.4065/82.11.1341. Erratum in: Mayo Clin Proc 2008; 83: 255. [DOI] [PubMed] [Google Scholar]
- 28.Kawai K, Yawn BP, Wollan P, Harpaz R. Increasing incidence of herpes zoster over a 60-year period from a population-based study. Clin Infect Dis. 2016;63:221–6. doi: 10.1093/cid/ciw296. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29.Chuang TY, Su WP, Perry HO, et al. Incidence and trend of herpes progenitalis: a 15-year population study. Mayo Clin Proc. 1983;58:436–41. [PubMed] [Google Scholar]
- 30.Chuang TY, Perry HO, Kurland LT, Ilstrup DM. Condyloma acuminatum in Rochester, Minn., 1950-1978. I. Epidemiology and clinical features. Arch Dermatol. 1984;120:469–75. [PubMed] [Google Scholar]
- 31.Wentworth AB, Drage LA, Wengenack NL, et al. Increased incidence of cutaneous nontuberculous mycobacterial infection, 1980 to 2009: a population-based study. Mayo Clin Proc. 2013;88:38–45. doi: 10.1016/j.mayocp.2012.06.029. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32.Bailey CH, Andersen LK, Lowe GC, et al. A population-based study of the incidence of delusional infestation in Olmsted County, Minnesota, 1976-2010. Br J Dermatol. 2014;170:1130–5. doi: 10.1111/bjd.12848. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33.Safavi KH, Muller SA, Suman VJ, et al. Incidence of alopecia areata in Olmsted County, Minnesota, 1975 through 1989. Mayo Clin Proc. 1995;70:628–33. doi: 10.4065/70.7.628. [DOI] [PubMed] [Google Scholar]
- 34.Mirzoyev SA, Schrum AG, Davis MD, Torgerson RR. Lifetime incidence risk of alopecia areata estimated at 2.1% by Rochester Epidemiology Project, 1990-2009. J Invest Dermatol. 2014;134:1141–2. doi: 10.1038/jid.2013.464. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Anderson KR, Schoch JJ, Lohse CM, et al. Increasing incidence of infantile hemangiomas (IH) over the past 35 years: correlation with decreasing gestational age at birth and birth weight. J Am Acad Dermatol. 2016;74:120–6. doi: 10.1016/j.jaad.2015.08.024. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Calamia KT, Wilson FC, Icen M, et al. Epidemiology and clinical characteristics of Behçet’s disease in the US: a population-based study. Arthritis Rheum. 2009;61:600–4. doi: 10.1002/art.24423. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Heit JA, Rooke TW, Silverstein MD, Mohr DN, et al. Trends in the incidence of venous stasis syndrome and venous ulcer: a 25-year population-based study. J Vasc Surg. 2001;33:1022–7. doi: 10.1067/mva.2001.113308. [DOI] [PubMed] [Google Scholar]
- 38.Kohorst JJ, Bruce AJ, Torgerson RR, et al. A population-based study of the incidence of burning mouth syndrome. Mayo Clin Proc. 2014;89:1545–52. doi: 10.1016/j.mayocp.2014.05.018. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Arora A, Wetter DA, Gonzalez-Santiago TM, et al. Incidence of leukocytoclastic vasculitis, 1996 to 2010: a population-based study in Olmsted County, Minnesota. Mayo Clin Proc. 2014;89:1515–24. doi: 10.1016/j.mayocp.2014.04.015. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Ungprasert P, Wetter DA, Crowson CS, Matteson EL. Epidemiology of cutaneous sarcoidosis, 1976-2013: a population-based study from Olmsted County, Minnesota. J Eur Acad Dermatol Venereol. 2016;30:1799–1804. doi: 10.1111/jdv.13760. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.de Vries E, Louwman M, Bastiaens M, et al. Rapid and continuous increases in incidence rates of basal cell carcinoma in the southeast Netherlands since 1973. J Invest Dermatol. 2004;123:634–8. doi: 10.1111/j.0022-202X.2004.23306.x. [DOI] [PubMed] [Google Scholar]
- 42.Bielsa I, Soria X, Esteve M, Ferrandiz C, Skin Cancer Study Group of Barcelones Nord Population-based incidence of basal cell carcinoma in a Spanish Mediterranean area. Br J Dermatol. 2009;161:1341–6. doi: 10.1111/j.1365-2133.2009.09468.x. [DOI] [PubMed] [Google Scholar]
- 43.Celic D, Lipozencic J, Jurakic Toncic R, et al. The incidence of basal cell carcinoma in Croatia: an epidemiological study. Acta Dermatovenerol Croat. 2009;17:108–12. [PubMed] [Google Scholar]
- 44.Sella T, Goren I, Shalev V, et al. Incidence trends of keratinocytic skin cancers and melanoma in Israel 2006-11. Br J Dermatol. 2015;172:202–7. doi: 10.1111/bjd.13213. [DOI] [PubMed] [Google Scholar]
- 45.Hoey SE, Devereux CE, Murray L, et al. Skin cancer trends in Northern Ireland and consequences for provision of dermatology services. Br J Dermatol. 2007;156:1301–7. doi: 10.1111/j.1365-2133.2007.07936.x. [DOI] [PubMed] [Google Scholar]
- 46.Staples MP, Elwood M, Burton RC, et al. Non-melanoma skin cancer in Australia: the 2002 national survey and trends since 1985. Med J Aust. 2006;184:6–10. doi: 10.5694/j.1326-5377.2006.tb00086.x. [DOI] [PubMed] [Google Scholar]
- 47.Karagas MR, Greenberg ER, Spencer SK, et al. Increase in incidence rates of basal cell and squamous cell skin cancer in New Hampshire, USA. New Hampshire Skin Cancer Study Group. Int J Cancer. 1999;81:555–9. doi: 10.1002/(sici)1097-0215(19990517)81:4<555::aid-ijc9>3.0.co;2-r. [DOI] [PubMed] [Google Scholar]
- 48.Howlett AL, Dewar RA, Morris SF. The epidemiology of cutaneous malignant melanoma in Nova Scotia. Can J Plast Surg. 2006;14:211–4. doi: 10.1177/229255030601400409. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 49.Cossu A, Casula M, Cesaraccio R, et al. Epidemiology and genetic susceptibility of malignant melanoma in North Sardinia, Italy. Eur J Cancer Prev. 2017;26:263–7. doi: 10.1097/CEJ.0000000000000223. [DOI] [PubMed] [Google Scholar]
- 50.Hoejberg L, Gad D, Gyldenkerne N, Bastholt L, Academy of Geriatric Cancer Research (AgeCare) Trends in melanoma in the elderly in Denmark, 1980-2012. Acta Oncol. 2016;55(Suppl 1):52–8. doi: 10.3109/0284186X.2015.1114677. [DOI] [PubMed] [Google Scholar]
- 51.Weinstock MA, Lott JP, Wang Q, et al. Skin biopsy utilization and melanoma incidence among Medicare beneficiaries. Br J Dermatol. 2017;176:949–54. doi: 10.1111/bjd.15077. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 52.Wang Y, Zhao Y, Ma S. Racial differences in six major subtypes of melanoma: descriptive epidemiology. BMC Cancer. 2016;16:691. doi: 10.1186/s12885-016-2747-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 53.Helvind NM, Holmich LR, Smith S, et al. Incidence of in situ and invasive melanoma in Denmark from 1985 through 2012: a national database study of 24,059 melanoma cases. JAMA Dermatol. 2015;151:1087–95. doi: 10.1001/jamadermatol.2015.1481. [DOI] [PubMed] [Google Scholar]
- 54.Iannacone MR, Youlden DR, Baade PD, et al. Melanoma incidence trends and survival in adolescents and young adults in Queensland, Australia. Int J Cancer. 2015;136:603–9. doi: 10.1002/ijc.28956. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55.Newell GR, Sider JG, Bergfelt L, Kripke ML. Incidence of cutaneous melanoma in the United States by histology with special reference to the face. Cancer Res. 1988;48:5036–41. [PubMed] [Google Scholar]
- 56.Greveling K, Wakkee M, Nijsten T, et al. Epidemiology of lentigo maligna and lentigo maligna melanoma in the Netherlands, 1989-2013. J Invest Dermatol. 2016;136:1955–60. doi: 10.1016/j.jid.2016.06.014. [DOI] [PubMed] [Google Scholar]
- 57.Holman CD, Mulroney CD, Armstrong BK. Epidemiology of pre-invasive and invasive malignant melanoma in Western Australia. Int J Cancer. 1980;25:317–23. doi: 10.1002/ijc.2910250303. [DOI] [PubMed] [Google Scholar]
- 58.Lerang K, Gilboe I, Garen T, et al. High incidence and prevalence of systemic lupus erythematosus in Norway. Lupus. 2012;21:1362–9. doi: 10.1177/0961203312458168. [DOI] [PubMed] [Google Scholar]
- 59.Hochberg MC. The incidence of systemic lupus erythematosus in Baltimore, Maryland, 1970-1977. Arthritis Rheum. 1985;28:80–6. doi: 10.1002/art.1780280113. [DOI] [PubMed] [Google Scholar]
- 60.See LC, Kuo CF, Chou IJ, et al. Sex- and age-specific incidence of autoimmune rheumatic diseases in the Chinese population: a Taiwan population-based study. Semin Arthritis Rheum. 2013;43:381–6. doi: 10.1016/j.semarthrit.2013.06.001. [DOI] [PubMed] [Google Scholar]
- 61.Weng MY, Huang YT, Liu MF, Lu TH. Incidence and mortality of treated primary Sjogren’s syndrome in Taiwan: a population-based study. J Rheumatol. 2011;38:706–8. doi: 10.3899/jrheum.100883. [DOI] [PubMed] [Google Scholar]
- 62.Huerta C, Rivero E, Rodriguez LA. Incidence and risk factors for psoriasis in the general population. Arch Dermatol. 2007;143:1559–65. doi: 10.1001/archderm.143.12.1559. [DOI] [PubMed] [Google Scholar]
- 63.Kaipiainen-Seppanen O. Incidence of psoriatic arthritis in Finland. Br J Rheumatol. 1996;35:1289–91. doi: 10.1093/rheumatology/35.12.1289. [DOI] [PubMed] [Google Scholar]
- 64.Soriano ER, Rosa J, Velozo E, et al. Incidence and prevalence of psoriatic arthritis in Buenos Aires, Argentina: a 6-year health management organization-based study. Rheumatology (Oxford) 2011;50:729–34. doi: 10.1093/rheumatology/keq369. [DOI] [PubMed] [Google Scholar]
- 65.Soderlin MK, Borjesson O, Kautiainen H, et al. Annual incidence of inflammatory joint diseases in a population based study in southern Sweden. Ann Rheum Dis. 2002;61:911–5. doi: 10.1136/ard.61.10.911. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 66.Savolainen E, Kaipiainen-Seppanen O, Kroger L, Luosujarvi R. Total incidence and distribution of inflammatory joint diseases in a defined population: results from the Kuopio 2000 arthritis survey. J Rheumatol. 2003;30:2460–8. [PubMed] [Google Scholar]
- 67.Alamanos Y, Papadopoulos NG, Voulgari PV, et al. Epidemiology of psoriatic arthritis in northwest Greece, 1982-2001. J Rheumatol. 2003;30:2641–4. [PubMed] [Google Scholar]
- 68.Kyriakis KP, Palamaras I, Terzoudi S, et al. Epidemiologic characteristics of pityriasis rosea in Athens Greece. Dermatol Online J. 2006;12:24. [PubMed] [Google Scholar]
- 69.Brisson M, Edmunds WJ. Epidemiology of Varicella-Zoster Virus in England and Wales. J Med Virol. 2003;70(Suppl 1):S9–14. doi: 10.1002/jmv.10313. [DOI] [PubMed] [Google Scholar]
- 70.Civen R, Marin M, Zhang J, et al. Update on incidence of herpes zoster among children and adolescents after implementation of varicella vaccination, Antelope Valley, CA, 2000 to 2010. Pediatr Infect Dis J. 2016;35:1132–6. doi: 10.1097/INF.0000000000001249. [DOI] [PubMed] [Google Scholar]
- 71.Esteban-Vasallo MD, Gil-Prieto R, Dominguez-Berjon MF, et al. Temporal trends in incidence rates of herpes zoster among patients treated in primary care centers in Madrid (Spain), 2005-2012. J Infect. 2014;68:378–86. doi: 10.1016/j.jinf.2013.09.035. [DOI] [PubMed] [Google Scholar]
- 72.Hillebrand K, Bricout H, Schulze-Rath R, et al. Incidence of herpes zoster and its complications in Germany, 2005-2009. J Infect. 2015;70:178–86. doi: 10.1016/j.jinf.2014.08.018. [DOI] [PubMed] [Google Scholar]
- 73.Mullooly JP, Riedlinger K, Chun C, et al. Incidence of herpes zoster, 1997-2002. Epidemiol Infect. 2005;133:245–53. doi: 10.1017/s095026880400281x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 74.Camenga DR, Dunne EF, Desai MM, et al. Incidence of genital warts in adolescents and young adults in an integrated health care delivery system in the United States before human papillomavirus vaccine recommendations. Sex Transm Dis. 2013;40:534–8. doi: 10.1097/OLQ.0b013e3182953ce0. [DOI] [PubMed] [Google Scholar]
- 75.Bollerup S, Baldur-Felskov B, Blomberg M, et al. Significant reduction in the incidence of genital warts in young men 5 years into the Danish Human Papillomavirus Vaccination Program for girls and women. Sex Transm Dis. 2016;43:238–42. doi: 10.1097/OLQ.0000000000000418. [DOI] [PubMed] [Google Scholar]
- 76.Persson G, Andersson K, Krantz I. Symptomatic genital papillomavirus infection in a community:incidence and clinical picture. Acta Obstet Gynecol Scand. 1996;75:287–90. doi: 10.3109/00016349609047103. [DOI] [PubMed] [Google Scholar]
- 77.Pirotta M, Stein AN, Conway EL, et al. Genital warts incidence and healthcare resource utilisation in Australia. Sex Transm Infect. 2010;86:181–6. doi: 10.1136/sti.2009.040188. [DOI] [PubMed] [Google Scholar]
- 78.Mohammad A, Mandl T, Sturfelt G, Segelmark M. Incidence, prevalence and clinical characteristics of Behcet’s disease in southern Sweden. Rheumatology (Oxford) 2013;52:304–10. doi: 10.1093/rheumatology/kes249. [DOI] [PubMed] [Google Scholar]
- 79.Margolis DJ, Bilker W, Santanna J, Baumgarten M. Venous leg ulcer: incidence and prevalence in the elderly. J Am Acad Dermatol. 2002;46:381–6. doi: 10.1067/mjd.2002.121739. [DOI] [PubMed] [Google Scholar]