Skin carcinoma and malignant melanoma in Slovenia 
C/inica/ study 
TRENDS IN INCIDENCE OF SKIN AND LIP CARCINOMAS 
AND MALIGNANT MELANOMA OF THE SKIN IN 
SLOVENJA 
V. Pompe-Kirn, A. Kansky and l. Planinšič 
ABSTRACT 
The incidence of skin and lip carcinomas as well as malignant melanoma of skin is greatly varying in the world. Reliable cancer 
incidence data can be obtained only in regions where population-based cancer registries are operating. In Slovenia the Cancer 
Registry has been operating since 1950 at the Institute of Oncology in Ljubljana. The average annual crude incidence rate per 
100000 ofskincarcinomas was during the period 1950-195214.4 inmales, and 19.4 infemales; it rose to 20.9 inmales and25.8 
in females during the 1986-1988 period. The crude rate for lip carcinoma was 6.2 in males and 1.4 in females in this first period, 
and it was 2.2 in males and 0.8 in females in the last period of observation; for malignantmelanoma it increased from O. 7 in males 
and 0.8 in females to 5.0 in males and 5.2 in females. Trends in crude and cumulative incidence rates in the 1974-1988 period 
were analysed in details. In cruderates the trendfor skin carcinoma was stable (-0.1 % inmales and -0.4% in females), for male 
lip carcinoma it was decreasing (-6.1 % ), whereas in malignant melanoma it was increasing in males (7.5% ), and in females 
(7 .8% ). When cumulative rates till the age 74 were tak:en into account, a decrease of skin carcinoma in females was evident (-
2.1 % ) , the decrease of male lip carcinoma was steeper (-7 .3 % ), whereas in malignant melanoma the increase was greater in male s 
(8.2% ), and lower in females (7 .1 % ). Cohort-analyses showed in skin carcinoma in males a tendency of higher rates in younger 
birth-cohorts up to the age of 70 only; in male lip cancer younger birth-cohorts were less affected in all age groups, whereas in 
malignant melanoma younger birth-cohorts were more affected in both sexes in almost ali age groups. 
KEYWORDS: 
skin and lip carcinomas, malignant melanoma, incidence, Slovenia 
INTRODUCTION 
Accurate population studies based on incidence figures for 
carcinoma and malignant melanoma (MM) of the skin are 
relatively few, most of the studies are unreliable from an 
epidemiological point of view because they are based on 
selected series of cases observed by clinicians or by 
acta dermatovenerologica A.P.A. 2-92 
pathologists ( 1 ). Among the first adequate approaches to this 
problem were the studies by MacDonald and MacDonald and 
Bubendorf (2,3). With a larger number of population-based 
cancer registries data on the incidence of malignant skin 
tumors in various countries became more reliable. 
There is an ample evidence that carcinoma of the skin and 
41 
Skin carcinoma and malignant melanoma in S/ovenia 
lips are not evenly distributed in various populations. A 
number of reports show that the incidence is greater in 
geographical areas with expressed insolation and high 
proportion of population engaged in outdoor activities. Such 
observation concerns specially people of Caucasian origin. 
The most susceptible are the fair-skinned people with blue 
irises, red hair and freckles. People of Irish and Scottish 
descent are particularly endangered as it was observed in 
Australia and the USA (4). An extremely high incidence of 
non-melanotic skin cancer was established among the whites 
in Australia: an investigation covering a population sample 
of30 976 people (Carlton South, Victoria) gave a standardized 
incidence of 823 per 100 000 inhabitants. The rate for basal 
carcinoma (BCC) was 657 and for squamous celi carcinoma 
(SCC) 166, giving aBCCto SCCratio of about4: 1 (5). Inthe 
USA an incidence of 71.5 for men and 4 7 .2 for women was 
observed in Minnesota which is a rather northem country and 
whose populationhas a relatively low actinic exposure (6). In 
contrary to this a much higher incidence of 3 79 (539 for men 
and 259 for women) was detected in the area of Dallas and 
Forth Worth which are characterized by high insolation (7). 
In United Kingdom an annual incidence of 100 is suggested 
(1). 
The incidence of carcinoma of the lips differs also a great 
deal between different population cohorts. White farmers 
seem again to be most endangered (8). According to Whelan 
et al. (9), thehighest age-standardized incidence was detected 
inmales inNewfoundland where itreaches 15.1, and in South 
Ireland 11.6. In females the disease is rare, the highest 
incidence being reported for South Australia 1.6 per 100 000. 
It is worth to mention that in certain countries, e.g. in former 
East Germany (10) and in Polland (11) a clear tendency to 
decrease is expressed. 
The highest age standardized incidence of MM of the skin 
was again observed in Australia; in Queensland it reaches 
30.9 in males and 28.5 in females, whereas the figures for 
New South Wales are 17.1 formalesand 16.1 forfemales (9). 
In the USA the incidence rate for MM rose from 4.5 in 1970 
to 11.2 in 1987 (12). From Denmark too an elevated number 
of patients with cutaneous MM was reported between 1943 
and 1982: 3509 men and 5305 women, yielding a fivefold to 
sixfold increase of the age standardized incidence rate (13). 
In Finland the incidence rose during the 1953 to 1973 period 
from 1.3 to 3.8 for men and from 1.5 to 3.5 for women (14). 
The main factors contributing to the development of 
cutaneous carcinomas may be listed as follows: 1) exposure 
to UV light, 2) exposure to other carcinogens, 3)genetic 
disposition, 4)viruses, 5)old age etc. Various mechanisms 
may induce cancer, e.g. physical and chemical damages to 
DNA, liberation of deoxyribonucleases from lysosomes, 
impaired or exhausted DNA repair in keratinocytes, 
suppression of cellular immunity, the presence of oncogens. 
It is highly probable that similar contributing factors are 
42 
operational in MM, but this remains to be proved. 
Reliable cancer incidence data can be obtained only in 
regions where population-based cancer registry is operating. 
In Slovenia the Cancer Registry has been operating since 
1950 at the Institute of Oncology in Ljubljana. In the present 
article detailed data on the incidence of skin and lip carcinomas 
as well as skin MM in Slovenia are presented. In addition, the 
recent knowledge in carcinogenesis for these three cancers is 
shortly reviewed. 
Carcinogenesis 
In man UV radiation, specially the so-called UV B range, 
including 290 to 320 nm wave lengths, is believed to be the 
most important skin carcinogen. A dose which provokes a 
given tumor end point represents a cumulative figure deri ved 
from many exposures. Blum demonstrated the quantitative 
nature of tumor response in the ears ofhaired mice and Forbes 
in hairless mice (15). Data from animal studies indicate that 
both fractionation and attenuated delivery ofUV increase the 
carcinogenic effectiveness of given dose. 
On molecular leve! the process of photocarcinogenesis is 
characterized by absorption of UV light by a molecule, so-
called chromophore: DNA, RNA, proteins (keratin, collagen, 
elastin), porphyrin and other substances. During this process 
photoproducts, e.g. thymine dimers, otherpyrimidine adducts, 
free radicals, DNA crosslinks with proteins and other 
substances are being formed .The enzymatic DNA repair 
which normally follows the UV-induced damage is often 
deficient in photocarcinogenesis (16). Histological changes 
may be divided in acute and chronic. The acute damage 
includes spongiosis of theepidermis, celi edema, v acuolisation 
and eosinophilia of cytoplasm, pyknosis of nuclei in the 
keratinocytes (sunbum cells) . The main chronic damage is 
represented by elastosis of the dermis, parakeratosis and 
atrophy of the epidermis, dilatation of superficial capillaries, 
followed by atypia of keratinocytes. hnmediately after a 
single exposure to the UV B radiation, a dose-dependent 
arrest of mitotic activity for 6-24 hours, followed by a 
reactive proliferation on days 2-7, can be observed ( 17). 
Besides keratinocytes, melanocytes and fibroblasts too are 
important targets of the UV carcinogenesis. 
Further factors which may contribute to the development 
of skincarcinomas are methylcholantrene, benzpyrene, certain 
tars, ionizing radiation and others. Many hereditary traits are 
poten ti ali y relev ant in skin carcinogenesis, e .g. the amount of 
pigment in the skin, enzymatic DNA repair system, the 
number of melanocytic nevi and others. The role of human 
papilloma viruses in skin carcinogenesis, specially the HPV 
16 and 18 has stili not been unequivocally proven for non-
immunosuppressed individuals . Inherited or acquired 
immunosuppressio~ is also an important contributing factor. 
The increased incidence of skin carcinomas in elderly people 
acta dermatovenerologica A.P A. 2-92 
Skin carcinoma and malig11011t melanoma in Slove11ia 
25-------------------~ 
§ 
g 20 
~ 
w 
§ 15 
a: u 
1 
~ 10 
a: 
~ 
i:j 5 
a: 
I 
1-
0-'--,----,--r--.-r---r--.-----r--.-------,--,---,--,---' 
50-52 53-55 56'58 59-61 62-64 65-67 68-70 71-73 74-76 77-79 80-82 83-85 86-88 
YEAR 
1- UPCANCER --- MAUGNANT MELANOMA - OTHEA SKIN CANCERS 
Figure 1: 
lncidence of lip cancer, malignant melanoma, and other skin 
cancers in males; Slovenia, 1950-1988 
is most probabl y due to an exhausted DNA repair mechanism 
and an impaired cellular immunity. 
There is convincing evidence that UV light and heredity 
play an important role in the genesis of MM. A number of 
investigations in experimental animals has shown that after 
exposure to UV light precursor melanocytes become activated 
and start to proliferate (18,19). Certain clinical studies make 
the information available of convincing trends towards 
increasing risk of MM with increased exposure to the sun (20, 
21 ,22). Heredity seems to be also a contributory factor: blue 
eyes, fair or red hair, pale complexion. Since the report by 
Cowly (23) more cases of familial occunence of MM were 
observed; it is believed that the inheritance is polygenic (24). 
The presence ofbenign melanocytic nevi has been documented 
in 16 epidemiological studies on MM. Therisk with increasing 
number of nevi has general! y been higher in the category with 
the greatest number of nevi, the relative tisk being higher 
than 10. Other factors such as occupational exposure to 
chemicals, ionizing radiation, use of steroid hormones, diet 
and others from present evidence have only week effects if 
any (25). 
MATERIAL AND METHODS 
Data from the Cancer Registry of Slovenia conceming 
non-melanoma skin cancer, lip cancer and malignant 
melanoma of the skin were analysed. Time trends for the 
1950-1988 period were studied, birth cohort analysis for the 
1964-1988 period, and an analysis ofhistologic types in non-
melanoma skin cancer for the 1984-1988 period was done. 
The Cancer Registry covers a two million population of 
acta dermatove11erologica AP.A. 2-92 
30-r-------------------~ 
§ 25 
8 
~ 
~ 20 
w 
" ~ u 
w 15 
~ 
w 
~ 10 
~ 
~ 
~ 5 
~ 
50-52 53-55 56-58 59-61 62-64 65-67 68-70 71-73 74-76 77-79 80-82 83-85 86-88 
YEAR 
1-UPCANCER -- MAUGNANT MELANOMA - OTHER SKIN CANCERS 1 
Figure 2: 
lncidence of lip cancer, malignant melanoma, and other skin 
cancers infemales; Slovenia, 1950-1988 
Republic Slovenia. Registration is compulsory, strict data 
protection measures are respected when analysing the data. 
Non-melanoma skin cancer (other skin cancers) were 
registered since 1950 as ali other cancer sites. They were 
classified according to the 8th revision of the Intemational 
Classification of diseases under the number 173. According 
to the data of the Cancer Registry 98% ofnon-melanoma skin 
cancer cases were carcinomas. Registration of these 
carcinomas was certainlynot as complete asforbreast orlung 
cancer, but in Slovenia there were no privatefacilities to treat 
skin cancer, and at least ali inadiated cases were notified to 
the Registry because there were only three institutions in 
Slovenia with radiation treatrnent facilities. Some surgically 
treated lesions with favorable prognosis escaped the 
registration, however. In figures non-melanoma skin cancer 
is marked as "other skin" cancers. 
For data analysis, standard descriptive epidemiological 
methodology was used (18) . 
In birth-cohort analysis age-specific incidence rates are 
plotted according to the year of birth. This analysis shows 
whether persons bom in certain year carry with them 
throughout their life a relatively higher or lower rate of the 
disease studied. 
RESULTS 
Time trends of crude incidence rates are shown on figures 
1 and 2. Three year averages were used to overcome the 
annual chance peaks. The crude rate of carcinomas was 14.4 
in the 1950-1952 peti.od and rose to 20.9 in 1986-1988. 
Conesponding values forfemales changedfrom 19 .4 to 25 .8. 
43 
Ski11 carci11oma arul maligMnt melanoma in S/ovenia 
250•- -------------------
200 
g 150 
g 
iii-
i 100 
50 
20 25 30 35 40 45 50 55 60 65 70 75 80+ 
AGE 
1 &1Ql LIP CANCER - MALIGNANT MELANOMA ~ OTHER SKIN CANCERS 
Figure 3: 
A ve rage annual incidence of lip cance r, malig nant melanoma, 
and other skin cancers in males by age; Slovenia, 1984-1988 
Carcinoma of the lips in males showed a steady decline of 
crude rates from 6.2 in 1950-1952 to 2.2 in 1986-1988. In 
females the corresponding values were 1.4 and 0.8. The 
crude rate of malignant melanoma rose from 0.7 during 
1950-1952 to 5.0 in 1986-1988 inmales, and from0.8 to 5.2 
in females. 
Taking into account the possibility that in the first years of 
cancer registration in Slovenia,the underreporting of cases 
250 
1 FEMALES 1 
200 
o 
150 o o 
o o 
ii) . 
i 100 
50 
o 
20 25 30 35 40 45 50 55 60 65 70 75 80+ 
AGE 
1 &1Ql LIP CANCER - MAUGNANT MELANOMA ~ OTHER SKIN CANCERS 
Figure 4: 
Average annual incidence of lip cancer, malignant melanoma, 
and other skin cancers infemales by age; Slovenia, 1984-
1988 
44 
1+--..--- -----~-..------------j 
--B-
1934 
---+--
1929 ...... 
1924 
-><---
1919 
----1914 --1909 
m • ~ a w M w ~ ro n w+ 
AGE 
Figure 5: 
Age-specific incidence of other skin cancers in males by birth 
cohorts; Slovenia, 1964-1988 
was greaterthen later-on, acloser look to the 1974-1988 tirne 
period was given. During this 15-year period the crude rates 
of skin cancer remained more or less stable in both sexes with 
an average annual percentage change of -0.1 % for males and 
of -0.4% for females; the rates of lip cancer in males were 
decreasing with an average annual percentage change of -
6.1 %, whereas the rates of malignant melanoma were 
increasing in both sexes with an average annual percentage 
change of7.5% and 7.8%. 
Cruderates do not take into account the eldering of Slov ene 
population during the analysed tirne period. As all studied 
cancer sites are more common in older age groups (figures 3 
--B--
1934 
---+--
1929 ...... 
1924 
-><---
1919 
----1914 
---1909 
1+--.----r-~-.---,---,---r-~--1 
m • ~ a w M M ~ ro n oo+ 
AGE 
Figure 6: 
Age-specific incidence of other skin cancers infemales by 
birth cohorts; Slovenia, 1964-1988 
acta dermatovenerologica A.P.A. 2-92 
Skin carcinoma and malignant melanoma in Slovenia 
100 
8 g 
10 
~ 
~ 
--&-
1 MALES 1 
1934 
--+-
1929 __... 
1924 
........ 
1919 
----1914 
1909 
• ~ % oo ~ oo m ro ~ oo+ 
AGE 
Figure 7: 
Age-specific incidenceof lip cancer in males by birthcohorts; 
Slovenia, 1964-1988 
and 4), this eldering of Slovene population influenced the 
crude rates and their trend. So, when cumulative rates till the 
age 74 only were taken into account, the calculated average 
annual percentage changes were slightly different. In other 
skin cancers in females the decrease was more evident 
(-2.1 % ), and so it was in male lip cancer (-7.3% ); in malignant 
melanoma in males the increase was greater (8.2% ), whereas 
in females it was lower (7 .1 % ). 
These results provoked us to analyse the data for the three 
cancer sites by birth cohorts for six five-years periods. In 
other skin cancers in males in younger birth-cohorts a tendency 
100---------------------, 
§ 
g 10 
t 
--&-
1934 
--+-
1929 __... 
1924 
........ 
191 9 
----1914 
---,..... 
1909 
• ~ % oo ~ oo m ro ~ oo+ 
AGE 
Figure 8: 
Age-specific incidence of malignant melanoma in males by 
birth cohorts; Slovenia, 1964-1988 
acta dermatovenerologica A.P.A. 2-92 
100 
--&-
j FEMALES 1 1934 
--+-
1929 __... 
1924 
........ 
1919 
8 ----~ 1914 10 -----u) 1909 
~ 
1-t--.----~----,-----,-------,---,----,-------,----,------, 
m • ~ % oo ~ oo m ro ~ oo+ 
AGE 
Figure 9: 
Age-specific incidence of malignant melanoma infemales by 
birth cohorts; Slovenia, 1964-1988 
of higher rates was expressed up to the age of 70 years, 
whereas in females a tendency oflowerrates in these cohorts 
was indicated up to the age of 80 years (Figures 5 and 6). In 
male lip cancer younger birth-cohorts were les s affected than 
the older ones in all age groups (Figures 7), whereas in 
malignant melanoma younger birth-cohorts were more 
affected in both sexes (Figures 8 and 9). 
In the period 1984-1988, 26% of non-melanoma skin 
cancers were squamous cell carcinomas, 69% basal cell 
carcinomas, 1 % adenocarcinomas , 2% non specified 
carcinomas, and 2% were other malignancies, e.g. some 
140 
120 
100 
o o 80 o o o 
u) 60 .... 
~ 
40 
20 
o 
MALES 
No. of cases: 670 basal cen 
252 squamous cel! 
Aatio: 2.7 
30 35 40 45 50 55 60 65 70 75 80+ 
AGE 
1 ~ BASAL - SOUAMOUS 1 
Figure 10: 
Average annual incidence of basal-celi and squamous-cell 
skin carcinoma by age in males; Slovenia, 1984-1988 
45 
Skin carcinoma and malignant melanoma in S/ovenia 
angiosarcomas, non-Hodgkin's lymphomas, etc .. OnFigures 
10 and 11 the age-specific incidence rates for squamous-cell 
and basal-cell carcinomas are given. Despite higher absolute 
numbers in females, the rates were higher in males. The 
reason is that there are more women older than 50 years in the 
Slovene population. 
140 
120 FEMALES 
No. of cases: 907 basal celi 
323 squamous cell 
100 Ratio: 2.8 
o 
o o 80 o 
o 
iii 
~ 60 
a: 
40 
20 
o 
30 35 40 45 50 55 60 65 70 75 80+ 
AGE 
,~ BASAL -SQUAMOUS 1 
Figure 11 : 
Average annual incidence of basal-celi and squamous-cell 
skin carcinoma by age infemales; Slovenia, 1984-1988 
DISCUSSION 
The incidence of skin carcinoma in Slovenia is Iower than 
in Minnesota (6) or Iowa (7) and essentially lower than in 
Australia (5). The age-specific rates disclose that the highest 
values were in the age group over 80 years which corresponds 
to the data in the Minnesota study.lnteresting is that in 
Slovenia birth-cohorts show opposite tendencies in males 
and females. In contrast to the relatively steady trend of BCC 
and SCC in Slovenia, in British Columbia, which is relatively 
low sunlight area, the age standardized incidence rate rose 
during the 1973-1987 period for BCC from 70. 7 to 120-4. in 
males and from 61.5 to 92.2 in females. The increase for SCC 
wasfrom 16.6to31.2inmales andfrom9.4to 16.9 infemales 
(19). The ratio BCC to SCC was in our study 2.7 for males 
and 2.8 for females which seems to be in the normal range. 
However, higher ratios are mentioned in the literature: 4: 1 in 
Queensland, 6: 1 in Minneapolis and San Francisco and even 
9: 1 in certain areas of USA (20). 
The steady decline of carcinoma of lips in Slovenia my be 
explained by the fact that the number of people engaged in 
outdoor activities was constantly dwindling. Birth-cohort 
analysis support this statement. 
There was a steep increase in malignant melanoma 
incidence in the studied period in crude and cumulati ve rates 
in Slovenia too; birth-cohort analysis indicate that more 
recent birth-cohorts experienced higher incidence rates in 
each age. This fact is possibl y related to a marked increase in 
sunbathing habits. Despite this increase Slovenia is in 
comparison with other countries in the world still on the 
lower side. 
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AUTHORS' ADDRESSES 
Vera Pompe-Kirn M. D., Ph. D., professor of cancer epidemiology, 
Head Cancer Registry, Institute of Oncology, Zaloška 2, 61000 Ljubljana, Slovenia 
Aleksej Kansky M. D., Ph. D., professor of dermatology, 
Štihova 26, 61000 Ljubljana, Slovenia 
Ivan Planišič M. D., Ph. D., professor of dermatology, Dpt. of Dermatology, 
University C!inical Center, Zaloška 2, 61000 Ljubljana, Slovenia 
acta dermatove11erologica A.P A. 2-92 47