British journal of Dermatology (1991) 125, 580-582.
Skin cancer as a cause of death in Denmark ANNE 0STERLIND, HELLE HJALGRIM, BARBARA KULINSKY* AND GERDA FRENTZ* Danish Cancer Society. Danisii Cancer Registry, institute of Cancer Epidemiology.
Copenhagen
"Department of Plastic- and Reconstructive Surgery. Rigshospitalet. Copenhagen, Denmark
Accepted for publication 1 7 June 1991
Summary
Denmark has a well-established nation-wide registration system for cancer incidence and mortality. In 1984, 2984 new cases of non-melanoma skin cancer were notified to the Danish Cancer Registry and 40 deaths were attributed to this cause. An evaluation and validation of the death certificates indicate that the true number of deaths caused by non-melanoma skin cancer was 18. Basal cell and squamous cell carcinoma accounted for three and 15 of the deaths, respectively. The estimated lethality is 4-3% for squamous cell carcinoma and 0-12% for basal cell carcinoma.
Cancer of the skin, excluding malignant melanoma, is generally considered to be a non-fatal form of cancer. The nation-wide Danish Cancer Registry includes nonmelanoma skin cancer (NMSC). which is one of the most commonly reported cancers. In the period 1978-1982 some 2700 new cases of NMSC were notified to the registry each year and of these 400 were squamous cell carcinoma (SCC).' In the same period an average of 32 people per year were recorded with skin cancer as the underlying cause of death.' Following a review of death certificates we have estimated the true number of deaths that can be attributed to skin cancer in Denmark, and compared this to the recorded morbidity.
Methods The present study is based on all cases of NMSC in 1984 reported to the Danish Cancer Registry and on the deaths in 1984 that were classified as NMSC. The information in the Cancer Registry was coded according to ICD-0^ by a specific morphology code (NMSC: ICD0 = 173) and death certificates were coded according to ICD-8^ (NMSC: ICD-8 = 173). Half of the deaths were certified by hospital departments and in these cases further information was abstracted from hospital records and pathology reports. The other deaths were certified by practising physicians, to whom we mailed questionnaires. All the questionnaires were returned apart from one where the GP had died. In each case we collected information to verify the histological type of skin cancer, the site of the tumour. Correspondence: Dr A.0sterlind, Danish Cancer Society. Danish Cancer Registry, Institute of Cancer Epidemiology. Rosenvaengets Hovedvej 35, Box 839. DK-2100 Copenhagen, Denmark.
580
and information on other malignant and benign diseases that could potentially be involved as the cause of death.
Results Altogether, 2984 cases of NMSC (1545 in men, 1439 in women), were notified in 1984. Eighty-five per cent of the tumours were basal cell carcinomas (BCC), 12% were squamous cell carcinomas (SCC) and 3% of the tumours remained unspecified. The distribution of tumours according to sex and histological subtype is given in Table 1. In the same year the Danish Death Register recorded a total of 40 deaths with NMSC as the underlying cause. We obtained evidence of histological verification in 39 cases. Altogether, 22 patients did have NMSC and in 18 of these patients NMSC was also the underlying cause of death. In the other four patients with NMSC, death was caused by non-cutaneous cancers in two patients, cardio-pulmonary disease in one and post-operative surgical complications in the other patient. In the 17 patients for whom NMSC could not be confirmed, the cause of death was identified as other skin tumours (Table 2). Of the 18 deaths caused by NMSC, BCC and SCC accounted for three (17%) and 15 (83%) of the deaths, respectively. The mean survival for the 15 SCC deaths was 4-3 years and in all the patients the tumour had metastasized, primarily to the lungs. Five of the tumours were located to the external auditory meatus and when at this site the patients died at a fairly young age (mean 51-6 years) and all within 1 year from the time of diagnosis of the primary tumour. Two of the patients had received various treatments for psoriasis and developed multiple BCC and SCC skin cancers. For the three patients with
SKIN CANCER AS A CAUSE OF DEATH
581
Table 1. Incidence and lethality of non-melanoma skin cancer in Denmark. 1984
Number of deaths
Histological type
Males
Females
Total
Males
Females
Total
Estimated lethality* Total (%)
.Squamous cell carcinoma Basal cell carcinoma Other and unspecified
228 1271 46
121 1269 49
349 2540 95
10 1 0
5 2 0
15 3 0
4 30 012 0
Non-melanoma skin cancer
1545
1439
2984
II
7
18
0-60
Number of cases
* Lethality = ratio between number of deaths caused by non-melanoma skin cancer and number of new cases of non-melanoma skin cancer.
BCC. the cause of death was the result of local invasion and their mean survival was 9-6 years.
Discussion Denmark has a well-established nation-wide registration system for the incidence of and mortality from cancer. Because NMSC is relatively non-fatal compared to other malignancies, it was feasible to evaluate and validate all the death certificates for one year. This study has shown that the number of deaths in Denmark coded to NMSC as the underlying cause is greater than that which should properly be attributed to this cause. Instead of the 40 deaths coded as NMSC in 1984 the results indicate that the true number is 18. This discrepancy is mainly due to deaths caused by other malignant diseases located to the skin. Cutaneous malignant melanoma for example, was recorded on the death certificate as malignant neoplasm of the skin and therefore coded as NMSC. Additionally, patients with a non-fatal NMSC who died from another
Table 2. The true cause of death for 40 deaths notified to the Death Registry as caused by non-melanoma skin cancer in 1984
Skin cancer category after revision Non-melanoma skin cancer
Number of patients 18
The underlying cause of death, due to information from case records and questionnaires Non-melanoma skin cancer
2 1 1
Other cancers Non-cancer disease Complication to NMSC surgery
Other
7 5 1 4
Malignant melanomas Malignant fibrous histiocytoma Leiomyosarcoma Other cancers involving skin
Unknown
1
No information available
disease had skin cancer recorded on the death certificate as the underlying cause of death. The low validity of the deaths was mainly due to unspecified diagnoses on the death certificate, which were applied specific codes, and to a lesser extent to incorrect coding procedures in the Statistical Department of the National Board of Health (for example malignant melanoma and fibrous malignant histiocytoma had been coded as NMSC). Improved certification of the cause of death by the physician and validation of the coding procedures should increase the validity of this category as a cause of death. It is generally suspected that NMSC is underreported in cancer registry data.' There are no data available on the completeness of reporting of NMSC (i.e. SCC and BCC) in the Danish Cancer Registry, but we do not suspect its registration to be less complete than in other countries. In the present study 15 people died from SCC in 1984 and in the same year 349 new cases were notified to the Registry. This means that the lethality can be estimated as 4-3%, because the mortality/incidence ratio is regarded as an approximation given that the incidence is constant over time. In California in 19 5 9 the estimated lethality was 1-2%, but this figure was based on death certificates together with an estimated incidence of NMSC* The lethality calculated from hospitalbased material in the period 1937-55 from Denmark was 6' 5%.' The highest figure of 14-5% was reported for tumours located to the ear. which is corroborated by our data where four of the 15 deaths from SCC was caused by tumours of the external ear tract. Two of the 15 cases whose deaths were caused by SCC also had psoriasis that was treated for many years, and who developed multiple NMSC. both SCC and BCC. Although the numbers are too few for a conclusion to be drawn it suggests that patients with psoriasis who are intensively treated should be examined regularly.'' BCC is normally regarded as a benign non-fatal disease, in which metastases are extremely rare. Only some 100
582
A.0STERLrND et al.
Table 3. Lethality from non-melanoma skin cancer according to histological subtypes
Squamous cell carcinoma (95% Cn*
Basal cell carcinoma (95% CI)'
Dunn eta/., 1965" California. 1959
1-2%
0-2%
Jensen. 1967' Odense. 1937-1955
6-5%
0-4%
4-3% (2-2-6-4)
01% (0-0-0-3)
Author, place, and period
0sterIind et a;.. 1991 Denmark. 1984 (present study) * Binomial distribution
cases are reported in the literature.'' In our study, the estimated lethality was 0 1 2 % . The deaths from BCC were all due to local invasion by the tumours of vital organs. Similar population-based studies are rare because incidence data on BCC are seldom available. In the study
from California'* the estimated lethality was 0-2% and in the study from Denmark' it was 0-4% (Table 3). This series was hospital-based and the relatively high lethality figure may therefore be influenced by selection. Furthermore, the incidence of NMSC in Denmark has doubled since this investigation and the lethality of the disease may be less today than 30-40 years ago.
References 1 0sterlind A. Non-melanoma skin cancer in Denmark 1943-1 982. Ugeskr Uiecjer 1986; 148: 798-802. 2 World Health Organization. Manual of the Statistical Classification of Diseases. Injuries and Causes of Death 1965. 8th revision. Geneva. 1967. 3 World Health Organization. International Classification of Diseases for Oncology (ICD-0). 1st edn. Geneva. 1976. 4 Dunn JE. Levin EA. Liden G. Harzfeld L. Skin cancer as a cause of death. California Medicine 1965: 102: 361-3. 5 Jensen MS. Skin cancer. Dan Med Bull 1967: 14: 1 70-4. 6 Stern RS, Scotto J. Eears TR. Psoriasis and susceptibility to nonmelanoma skin cancer. / An] Acad Dennatol 1985: 12: 67-73. 7 Howat AJ. Levick PL. Metastatic basal cell carcinoma. Derniatolofiica 1987; 174: 132-4.
Skin cancer as a cause of death in Denmark ANNE 0STERLIND, HELLE HJALGRIM, BARBARA KULINSKY* AND GERDA FRENTZ* Danish Cancer Society. Danisii Cancer Registry, institute of Cancer Epidemiology.
Copenhagen
"Department of Plastic- and Reconstructive Surgery. Rigshospitalet. Copenhagen, Denmark
Accepted for publication 1 7 June 1991
Summary
Denmark has a well-established nation-wide registration system for cancer incidence and mortality. In 1984, 2984 new cases of non-melanoma skin cancer were notified to the Danish Cancer Registry and 40 deaths were attributed to this cause. An evaluation and validation of the death certificates indicate that the true number of deaths caused by non-melanoma skin cancer was 18. Basal cell and squamous cell carcinoma accounted for three and 15 of the deaths, respectively. The estimated lethality is 4-3% for squamous cell carcinoma and 0-12% for basal cell carcinoma.
Cancer of the skin, excluding malignant melanoma, is generally considered to be a non-fatal form of cancer. The nation-wide Danish Cancer Registry includes nonmelanoma skin cancer (NMSC). which is one of the most commonly reported cancers. In the period 1978-1982 some 2700 new cases of NMSC were notified to the registry each year and of these 400 were squamous cell carcinoma (SCC).' In the same period an average of 32 people per year were recorded with skin cancer as the underlying cause of death.' Following a review of death certificates we have estimated the true number of deaths that can be attributed to skin cancer in Denmark, and compared this to the recorded morbidity.
Methods The present study is based on all cases of NMSC in 1984 reported to the Danish Cancer Registry and on the deaths in 1984 that were classified as NMSC. The information in the Cancer Registry was coded according to ICD-0^ by a specific morphology code (NMSC: ICD0 = 173) and death certificates were coded according to ICD-8^ (NMSC: ICD-8 = 173). Half of the deaths were certified by hospital departments and in these cases further information was abstracted from hospital records and pathology reports. The other deaths were certified by practising physicians, to whom we mailed questionnaires. All the questionnaires were returned apart from one where the GP had died. In each case we collected information to verify the histological type of skin cancer, the site of the tumour. Correspondence: Dr A.0sterlind, Danish Cancer Society. Danish Cancer Registry, Institute of Cancer Epidemiology. Rosenvaengets Hovedvej 35, Box 839. DK-2100 Copenhagen, Denmark.
580
and information on other malignant and benign diseases that could potentially be involved as the cause of death.
Results Altogether, 2984 cases of NMSC (1545 in men, 1439 in women), were notified in 1984. Eighty-five per cent of the tumours were basal cell carcinomas (BCC), 12% were squamous cell carcinomas (SCC) and 3% of the tumours remained unspecified. The distribution of tumours according to sex and histological subtype is given in Table 1. In the same year the Danish Death Register recorded a total of 40 deaths with NMSC as the underlying cause. We obtained evidence of histological verification in 39 cases. Altogether, 22 patients did have NMSC and in 18 of these patients NMSC was also the underlying cause of death. In the other four patients with NMSC, death was caused by non-cutaneous cancers in two patients, cardio-pulmonary disease in one and post-operative surgical complications in the other patient. In the 17 patients for whom NMSC could not be confirmed, the cause of death was identified as other skin tumours (Table 2). Of the 18 deaths caused by NMSC, BCC and SCC accounted for three (17%) and 15 (83%) of the deaths, respectively. The mean survival for the 15 SCC deaths was 4-3 years and in all the patients the tumour had metastasized, primarily to the lungs. Five of the tumours were located to the external auditory meatus and when at this site the patients died at a fairly young age (mean 51-6 years) and all within 1 year from the time of diagnosis of the primary tumour. Two of the patients had received various treatments for psoriasis and developed multiple BCC and SCC skin cancers. For the three patients with
SKIN CANCER AS A CAUSE OF DEATH
581
Table 1. Incidence and lethality of non-melanoma skin cancer in Denmark. 1984
Number of deaths
Histological type
Males
Females
Total
Males
Females
Total
Estimated lethality* Total (%)
.Squamous cell carcinoma Basal cell carcinoma Other and unspecified
228 1271 46
121 1269 49
349 2540 95
10 1 0
5 2 0
15 3 0
4 30 012 0
Non-melanoma skin cancer
1545
1439
2984
II
7
18
0-60
Number of cases
* Lethality = ratio between number of deaths caused by non-melanoma skin cancer and number of new cases of non-melanoma skin cancer.
BCC. the cause of death was the result of local invasion and their mean survival was 9-6 years.
Discussion Denmark has a well-established nation-wide registration system for the incidence of and mortality from cancer. Because NMSC is relatively non-fatal compared to other malignancies, it was feasible to evaluate and validate all the death certificates for one year. This study has shown that the number of deaths in Denmark coded to NMSC as the underlying cause is greater than that which should properly be attributed to this cause. Instead of the 40 deaths coded as NMSC in 1984 the results indicate that the true number is 18. This discrepancy is mainly due to deaths caused by other malignant diseases located to the skin. Cutaneous malignant melanoma for example, was recorded on the death certificate as malignant neoplasm of the skin and therefore coded as NMSC. Additionally, patients with a non-fatal NMSC who died from another
Table 2. The true cause of death for 40 deaths notified to the Death Registry as caused by non-melanoma skin cancer in 1984
Skin cancer category after revision Non-melanoma skin cancer
Number of patients 18
The underlying cause of death, due to information from case records and questionnaires Non-melanoma skin cancer
2 1 1
Other cancers Non-cancer disease Complication to NMSC surgery
Other
7 5 1 4
Malignant melanomas Malignant fibrous histiocytoma Leiomyosarcoma Other cancers involving skin
Unknown
1
No information available
disease had skin cancer recorded on the death certificate as the underlying cause of death. The low validity of the deaths was mainly due to unspecified diagnoses on the death certificate, which were applied specific codes, and to a lesser extent to incorrect coding procedures in the Statistical Department of the National Board of Health (for example malignant melanoma and fibrous malignant histiocytoma had been coded as NMSC). Improved certification of the cause of death by the physician and validation of the coding procedures should increase the validity of this category as a cause of death. It is generally suspected that NMSC is underreported in cancer registry data.' There are no data available on the completeness of reporting of NMSC (i.e. SCC and BCC) in the Danish Cancer Registry, but we do not suspect its registration to be less complete than in other countries. In the present study 15 people died from SCC in 1984 and in the same year 349 new cases were notified to the Registry. This means that the lethality can be estimated as 4-3%, because the mortality/incidence ratio is regarded as an approximation given that the incidence is constant over time. In California in 19 5 9 the estimated lethality was 1-2%, but this figure was based on death certificates together with an estimated incidence of NMSC* The lethality calculated from hospitalbased material in the period 1937-55 from Denmark was 6' 5%.' The highest figure of 14-5% was reported for tumours located to the ear. which is corroborated by our data where four of the 15 deaths from SCC was caused by tumours of the external ear tract. Two of the 15 cases whose deaths were caused by SCC also had psoriasis that was treated for many years, and who developed multiple NMSC. both SCC and BCC. Although the numbers are too few for a conclusion to be drawn it suggests that patients with psoriasis who are intensively treated should be examined regularly.'' BCC is normally regarded as a benign non-fatal disease, in which metastases are extremely rare. Only some 100
582
A.0STERLrND et al.
Table 3. Lethality from non-melanoma skin cancer according to histological subtypes
Squamous cell carcinoma (95% Cn*
Basal cell carcinoma (95% CI)'
Dunn eta/., 1965" California. 1959
1-2%
0-2%
Jensen. 1967' Odense. 1937-1955
6-5%
0-4%
4-3% (2-2-6-4)
01% (0-0-0-3)
Author, place, and period
0sterIind et a;.. 1991 Denmark. 1984 (present study) * Binomial distribution
cases are reported in the literature.'' In our study, the estimated lethality was 0 1 2 % . The deaths from BCC were all due to local invasion by the tumours of vital organs. Similar population-based studies are rare because incidence data on BCC are seldom available. In the study
from California'* the estimated lethality was 0-2% and in the study from Denmark' it was 0-4% (Table 3). This series was hospital-based and the relatively high lethality figure may therefore be influenced by selection. Furthermore, the incidence of NMSC in Denmark has doubled since this investigation and the lethality of the disease may be less today than 30-40 years ago.
References 1 0sterlind A. Non-melanoma skin cancer in Denmark 1943-1 982. Ugeskr Uiecjer 1986; 148: 798-802. 2 World Health Organization. Manual of the Statistical Classification of Diseases. Injuries and Causes of Death 1965. 8th revision. Geneva. 1967. 3 World Health Organization. International Classification of Diseases for Oncology (ICD-0). 1st edn. Geneva. 1976. 4 Dunn JE. Levin EA. Liden G. Harzfeld L. Skin cancer as a cause of death. California Medicine 1965: 102: 361-3. 5 Jensen MS. Skin cancer. Dan Med Bull 1967: 14: 1 70-4. 6 Stern RS, Scotto J. Eears TR. Psoriasis and susceptibility to nonmelanoma skin cancer. / An] Acad Dennatol 1985: 12: 67-73. 7 Howat AJ. Levick PL. Metastatic basal cell carcinoma. Derniatolofiica 1987; 174: 132-4.
