March 1988, p. 93-98. Vol. 4, No. i. ESOPHAGEAL CANCER MORTALITY: RELATIONSHIP WITH ALCOHOL INTAKE. AND CIGARETTE SMOKING IN ITALY.
Eur. J. Epidemiol. 0392-2990
Vol. 4, No. i
March 1988, p. 93-98
ESOPHAGEAL CANCER MORTALITY: RELATIONSHIP WITH ALCOHOL INTAKE AND CIGARETTE SMOKING IN ITALY F. LA ROSA 1, A. CRESCI, G. SALTALAMACCHIA and
C. ORPIANESI V. MASTRANDREA
Dipartimento di Igiene dell'Universit~ di Perugia - Via del Giochetto, 06100 Perugia, Italy.
Key words: E s o p h a g e a l c a n c e r - M o r t a l i t y - A l c o h o l - T o b a c c o . This p a p e r examines changes with time in age-adjusted m o r t a l i t y f r o m esophageal ,cancer for the years 1950-1981, in relation to changes in smoking habits and alcohol consumption. In b o t h sexes the age-adjusted death rates have shown no m a r k e d t i m e variation. I n s t e a d in the same p e r i o d there have been m a r k e d t e m p o r a l variations in o o n s u m p t i o n of alcohol and tobacco which are considered risk factors associated w i t h esophageal cancer. The male cohort v a r i a t i o n seems to indicate some fluctuations in m o r t a l i t y before 1921 and a progressive increase after this year. I n females the death rates are very low and the cohort v a r i a t i o n is prati,cally constant. The progressive increase of cohort v a r i a t i o n in esophageal cancer m o r t a l i t y for m e n b o r n a f t e r 1921 coincides w i t h a progressive increase in h a r d alcohol consumption. I n the s a m e p e r i o d there has also been a progressive increase in tobacco c o n s u m p t i o n b u t this begun at the t u r n of this century.
INTRODUCTION throughout the world suggests that a number of risk factors both exogenous causative factors a n d s o m e k i n d s of h o s t s u s c e p t i b i l i t y a r e i n v o l v e d (1, 22, 31, 34). I n w e s t e r n c o u n t r i e s , a m o n g the exogenous risk factors, alcohol intake and s m o k i n g h a b i t s s e e m to h a v e t h e g r e a t e s t imp o r t a n c e (5, 8, 28, 32). T h i s p a p e r a t t e m p t s to i n t e r p r e t t h e m o r t a l i t y t r e n d s f r o m e s o p h a g e a l c a n c e r , f r o m 1950 to 1981 in I t a l y , in r e l a t i o n to p a t t e r n s o f a l c o h o l a n d t o b a c c o c o n s u m p t i o n . To o b t a i n m o r e r e l i a b l e a n d c o m p a r a b l e i n f o r m a t i o n o n e s o p h a g e a l cancer mortality, several methods of calculation were u s e d : 1) A d j u s t e d m o r t a l i t y f o r all a g e s a n d f o r t h e a g e g r o u p 0-64 y e a r s , 2) F i v e - y e a r a g e - s p e c i f i c , 45-84 y e a r s , d e a t h r a t e s , 3) A n a l y s e s of v a r i a t i o n in c o h o r t , a g e a n d p e r i o d of d e a t h b y i n d i r e c t s t a n d a r d i z a t i o n m e t h o d (9, 15).
Patterns and trends of the incidence and mortality from esophageal cancer vary considerably in t h e d i f f e r e n t c o u n t r i e s o f t h e w o r l d . I n s o m e a r e a s it is a l e a d i n g c a u s e o f d e a t h , w h i l e in o t h e r s it is o n e o f t h e l e a s t c o m m o n (5, 20, 22, 26). U s u a l l y in w e s t e r n c o u n t r i e s t h e r a t e s a r e low except for the Western French provinces which have a very high mortality rate similar to t h o s e o f s o m e a r e a s in Asia, A f r i c a a n d C e n t r a l o r S o u t h e r n A m e r i c a (26, 28). D u r i n g t h e l a s t 30 y e a r s o r so, t h e t i m e t r e n d s in w e s t e r n c o u n t r i e s have not been homogeneous. Only France has s h o w n a d r a m a t i c i n c r e a s e in r a t e s - - c l o s e to 50% - - w h i l e in o t h e r c o u n t r i e s , t h e m o r t a l i t y f r o m c a n c e r o f t h e e s o p h a g u s h a s r e m a i n e d cons t a n t o r h a s d e c r e a s e d s l o w l y o v e r t i m e (25, 26). T h i s d i v e r s i t y in p a t t e r n s a n d t r e n d s o b s e r v e d 1 C o r r e s p o n d i n g author. 93
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MATERIALS
AND
ulation over the periods (9). The age variations were also obtained using the SMR: the procedure is very similar to that of period variation computing the values for e4ery row rather than for every column. Thus we obtained a period-standardized ratio, and the last age group (80-84 years) was the standard for age variation (15). All indices are also scaled to have a weighted geometric mean of unity for the p u r p o s e of possible comparisons. In interpretation of indices, the first (1870) and last three (1940-1950) cohorts are disregarded to limit the r a n d o m variability relative to final periods. The data on tobacco c o n s u m p t i o n (1901-1981) was obtained f r o m official publications of the Administration of the State Monopolies or f r o m unpublished material kindly provided by the same Administration .(19). The data on alcohol intake are from official publications (4, 11, 12). Those relative to 1981 are derived f r o m unpublished data of the National Health Council.
METHODS
The main source of data for this study was that published by the National Institute of Statistics (ISTAT) in Rome. The data on esophageal cancer deaths between 1950 and 1981, from official ISTAT publications, are r e p o r t e d according to the Ninth Revision of the International Classification of Diseases (ICD) (33) (Malignant neoplasm of esophagus, 150). The populations are those registered in the 1951, 1961, 1971 and 1981 census reports, and for intercensal years, they have been estimated from registry variations supplied either from official publications or directly by ISTAT. The mortality rates per 100,000 inhabitants -computed for all ages and for the age group 0-64 years-were calculated on a five-year basis, and adjusted for age using the direct method, taking the world population model (32) as standard. Analysis of variation of cohort, age and period of death were p e r f o r m e d by the indirect standardization m e t h o d (9, 15). This m e t h o d consists of indirect age-standardization by period of death and birth cohort, calculating a standardized period mortality ratio and a standardized cohort mortality ratio. The first ratio measures the variation between periods, the second the variation between b i r t h cohorts, even if the two ratios ignore the potential c o h o r t effect and the potential period effect respectively. The SMRs were calculated on five-year basis. The cohorts considered were f r o m 1875 to 1935. The 1950-54 period was used as the standard for period variation, while for cohort variation, we used a weighted average of the age-specific rates and the combined pop-
TABLE
1. - -
Tables 1 and 2 and Figure 1 give the esophageal cancer mortality rates in Italy over the 1950-1981 period. For men, the all-age-adjusted death rate rises slightly until 1969 and thereafter, with some fluctuations, remains above 4.50 per 100,000 inhabitants. F r o m the 1950's to 1981 the adjusted rate in males u n d e r 65 years increases. In females the rates are very low, and they show fairly constant trends. In males the cohort~variation rises until 1895, then decreases until 192t, and after this year rises
Malignant neoplasms of esophagus (150 ICD no.) in Italy. Age-specific death rates (45-84 years) per 100,000 inhabitants, crude and adjusted rates (AADR) for all ages and for 0-64, mean number of deaths, from 1950 to 1981. Males.
Age group 4549 50-54 55-59 60-64 65-69 70-74 75-79 80-84 Crude rate AADR all AADR 0-64 mean number of deaths
RESULTS
Calendar
period
1950-54
1955-59
1960-64
1965-69
1970~74
1975-79
1980-81
2.38 6.21 11.61 18.40 25.76 30.74 36.59 29.40 3.98 3.77 1.88
2.37 5.72 11.14 19.62 28.12 35.74 4'0.67 38.68 4.47 4.03 1.88
2.40 5.66 11.94 19.82 30.46 41.22 45.50 43.14 5.15 4.37 1.90
2.84 5.46 11.93 21.02 30.46 39.41 50.79 52.46 5.61 4.57 2.03
3.39 7.13 12.00 20.42 27.98 37.61 47.76 49.82 5.95 4.54 2.14
4.96 8.52 14.56 19.91 26.63 34.54 48.15 52.70 6.46 4.75 2.42
5.16 9.95 14.29 20.44 26.75 33.90 39.21 55.06 6.62 4.74 2.51
926
1073
1279
1439
1581
1777
1832
94
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Esophageal cancer mortality in italy.
T A B L E 2. - - Malignant n e o p l a s m s of esophagus (150 ICD nrO.) in Italy. Age-specific death rates (45-84 years) p e r 100,000 inhabitants, crude and a d j u s t e d rates (AADR) for all ages and for 0-64 years, m e a n n u m b e r of deaths, f r o m 1950 to 1981. Females. Age group
C a 1e n d a r
45-49 50-54 55-59 60-64 65-69 70-74 75-79 80-84 Crude rate AAD,R all AADR 0-64 mean number of deaths
1950-54
1955-59
1960-64
1965-69
1970-74
1975-79
1980~81
0.60 1.03 2.13 2.71 4.96 7.59 9.79 13.27 1.04 0.84 0.35
0.54 1.18 1.92 2.93 4.52 7.92 11.61 12.67 1.14 0.85 0.34
0.69 0.97 1.65 3.26 4.95 7.63 10.77 13.72 1.27 0.87 0.35
0.41 0.95 1.75 2.99 4.49 7.24 9.94 14.83 1.30 0.82 0.32
0.53 0.96 1.65 2.63 4.44 6.81 10.64 13.82 1.39 0.80 0.30
0.56 1.10 1.78 2.88 4.36 6.64 11.29 14.43 1.57 0.85 0.34
0.46 0.82 2.03 2.39 4.39 7.33 9.21 16.94 1.62 0.81 0.29
254
284
330
348
386
452
473
TABLE 3. Mean yearly c o n s u m p t i o n .of total tobacco*, cigarettes, wine, b e e r and h a r d alcohol by person over 14 years of age in Italy, 190:1-1981.
M
g all L
@
4-
Year
3-2-
av'
1-
m
"O
1901 1911 1921 1931 1941 1951 1956 1961 1966 1971 1976 1981
0-64
Ill
II~
................................
all
. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
0--64
" !
p e r i o d
(
I ......
I
I
I
I
c a l e n d a r period Figure 1. - Mortality from esophageal cancer in Italy, 1950-1981. Age-adjusted rates for all ages and 0-64 years.
g r a m s of total cigarettes tobacco 732 805 1043 875 1050 1106 1310 1536 1767 1861 2168 2274
37 115 415 452 714 870 1103 1428 1637 1766 2106 2228
wine
159.0 175.1 162.5 143.0 113.2 114.5 142.1 145.0 154.5 149.1 131.1 119.8
liters of beer hard alcohol 1.2 2.3 3.8 4.0 3.9 4.2 4.6 8.2 13.7 16.0 18.3 22.0
0.8 0.8 0.8 0.6 0.4 0.9 1.2 1.6 2.1 2.4 7.2 12.8
* Total tobacco: cigarettes, shag, cigars and snuff. p r o g r e s s i v e l y . T h e p e r i o d v a r i a t i o n is p r a c t i c a l l y c o n s t a n t o v e r t h e s t u d i e d y e a r s , a n d t h e a g e varia t i o n i n c r e a s e s s t e a d i l y w i t h age ( f i g u r e 2). In females the cohort variation follows the m a l e t r e n d u n t i l 1915 a n d t h e n r e m a i n s p r a c t i c a l l y c o n s t a n t . T h e p e r i o d v a r i a t i o n is s i m i l a r to t h a t in m a l e s a n d t h e a g e v a r i a t i o n i n c r e a s e s s h a r p l y w i t h age. T a b l e 3 gives t h e c o n s u m p t i o n o f t o t a l t o b a c c o and cigarettes, and that of wine, beer and hard a l c o h o l p e r I t a l i a n i n h a b i t a n t o v e r 14 y e a r s , f r o m 1901 to 1981. T h e c o n s u m p t i o n o f t o t a l t o b a c c o r o s e d r a m a t i c a l l y f r o m 732 g r a m s in 1901 to 2274
in 1981, as d i d t h e n u m b e r of c i g a r e t t e s s m o k e d , f r o m 37 t o 2228. B e e r i n t a k e h a s i n c r e a s e d s i n c e 1901, a n d w i n e c o n s u m p t i o n r o s e till a b o u t 1966 a n d a f t e r w a r d s d e c r e a s e d . H o w e v e r o u r d a t a do n o t r e f l e c t t h e c o n s u m p t i o n of p r i v a t e l y p r o d u c e d wines. The hard alcohol intake shows a decrease u p to 1941 a n d a m a r k e d i n c r e a s e o v e r t h e l a s t 40 y e a r s . T h e o f f i c i a l d a t a o n t o b a c c o a n d a l c o h o l cons u m p t i o n do n o t give a r e l i a b l e e s t i m a t e of t h e a c t u a l a m o u n t c o n s u m e d in I t a l y . I l l e g a l i m p o r t s of manufactured cigarettes probably provided a 95
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Eur. J. Epidemiol.
SMR
SMI~ °cohort
age
period.
2.0.
I
/
8-
1.5_
6-
1.0-
4-
0.5-
2-
0.0
8'7o ' le 1880
'
1900
1 '1o
!
1920
calendar
I
1930
I
1940
I
1950
I
1960
year
'I
1970
1
1980
I
//,.
l o/.
.,/""
O3() 40
5'0 6'0 7() 80
.age~ a t d e a t h
Figure 2. - Esophageal cancer mortality in Italy. Standardized Mortality Ratios (SMR) relative to cohort, period and age variations. Males ( ) and Females (. . . . . ). countries with low mortality (25, 26) such as Scotland, England and Wales, Ireland, the U.S.A. and Canada. I n s t e a d in the same period there have been m a r k e d temporal variations in the c o n s u m p t i o n of alcohol and tobacco which are considered risk factors associated with esophageal cancer. Unfortunately the lack of data over the studied period on alcohol c o n s u m p t i o n by sex and age groups does not allow a m o r e careful analysis, However, as far as Italy is concerned certain c o m m e n t s are suggested by the comparison of trends in the c o n s u m p t i o n of alcohol and tobacco and c u r r e n t trends in esophageal cancer mortality in different male b i r t h cohorts (separating changes associated with period of b i r t h and period of death). In fact the male c o h o r t variation indicates some fluctuations in mortality before 1921 and a progressive increase after this. In females the death rates by b i r t h c o h o r t are very low and the c o h o r t variation is practically constant. Similar results, in the t r e n d of the cohort variation, are reported by other a u t h o r s (6, 10), who have calculated the effect by the age-periodc o h o r t statistical model described by O s m o n d and Gardner (21). The progressive increase in the esophageal standardized cohort mortality ratio for men b o r n after 1921 coincides with a progressive increase in h a r d alcohol consumption. I n the same period there has also been a progressive increase in tobacco consumption, b u t this increase had already begun at the t u r n of this century.
substantial fraction of tobacco c o n s u m p t i o n and illegal distillation of h a r d alcohol in some regions of n o r t h Italy probably constituted a good share of alcohol consumed. Nevertheless the data on tobacco sold and the estimates on alcohol sales, r e p o r t e d here could give a good indication of temporal trends. The data on separate c o n s u m p t i o n (by sex and age groups) of tobacco and alcohol are available only for more recent years. It was assessed that, in 1983, the p r o p o r t i o n s of non- m o d e r a t e and heavy drinkers were respectively 22.5, 52.8 and 24.7% in males and 47.4, 50.2 and 2.4% in females, and that the heavy drinkers were more c o m m o n a m o n g the middle aged (45-64) than in y o u n g e r or older age groups (14, 17). I n the same year the p r o p o r t i o n s of non-smokers, ex-smokers and smokers were respectively 40.9, 13.5 and 45.6 in males and 8.0, 2.3 and 17.7 in females (14). In 1980 they were 35.8, 10.0 and 54.3 in males and 81.9, 1.4 and 16.7 in females (13). The latest inf o r m a t i o n on cigarette c o n s u m p t i o n per sex is referred to 1957, when cigarette c o n s u m p t i o n by female smokers was less than 10% of the total (24). DISCUSSION
The results of this investigation d e m o n s t r a t e that in Italy the age adjusted death rates from esophageal cancer in b o t h sexes have shown no m a r k e d time variations f r o m 1950 to 1981. This pattern is similar to that f o u n d in other western 96
Vol. 4, 1988
Esophageal cancer mortality in Italy.
The data presented above lead one to postulate an association between the trends in esophag e a l cancer and the increase in c o n s u m p t i o n of h a r d alcohol, whereas it is difficult to etablish, f r o m our data, w h e t h e r tobacco c o n s u m p t i o n is, associated with this type of cancer. It might be that tobacco c o n s u m p t i o n has a certain significance when associated with h a r d alcohol intake. This hypothesis, which a t t e m p t s to explain the trends in m o r t a l i t y f r o m esophageal cancer in Italy, appears plausible .even if we c o m p a r e our data with those of other a u t h o r s (1, 2, 22, 27, 31). Pottern et al. (22) emphasize the risk associated with the use of alcohol beverages, a risk which increases with the a m o u n t and hardness of liquors. The same a u t h o r s ( 2 2 ) e s t i m a t e that, for esophageal cancer, in the period 1970-75, there is an excess of 81% deaths attributable to alcoholic beverage c o n s u m p t i o n a m o n g blacks in Washington De. B u t c h (2), examining secular trends in England and Wales, finds no association between esophageal cancer and cigarette smoking, while he affirms that death rates are positively correlated to alcohol consumption. The a u t h o r notes a fall in rates a m o n g y o u n g e r m e n and w o m e n f r o m 1911-1915 to a b o u t 1951-1960 and the subsequent rise f r o m a b o u t 1960 onwards, With reference to alcoholic intake he believes that this risk, 2-.3 years p r i o r to death, is significant in terms of , p r o m o t i o n ,,. I n Berlin's opinion this,interval seems too short (1), even if the relative risk falls fairly rapidly after stopping consumption of alcoho! (5, 18). I n conclusion, the time trends in mortality f r o m esophageal cancer in I t a l y can be partially explained by changes, over a period of time, in tobacco smoking and alcohol intake, even considering the s h o r t c o m i n g s deriving f r o m our use of alcohol and tobacco c o n s u m p t i o n data relative to the whole population It would be interesting t o make a clearer distinctioh between the respective effects of these two risk factors by considering them singly and separately by sex and age groups. To this end it has been suggested that probing investigation should be c o n d u c t e d in Italy in areas with a high incidence and those with a low incidence for this type of cancer. I n fact, c o m p a r i n g the mortality f r o m esophageal cancer in different Italian regions, some a u t h o r s (3, 7, 16)) have f o u n d a high ratio between some n o r t h e r n and some s o u t h e r n regions. This has been related to different levels of c o n s u m p t i o n of wine and h a r d liquors (7, 23).
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Acknowledgements This work was supported by the Italian Ministry of Education. 97
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