Annals of Oncology 12: 327-330. 2001. © 2001 Kluwer Academic Publishers. Printed in the Netherlands.
Original article Changing socioeconomic correlates for cancers of the upper digestive tract^ i—
C. Bosetti,1 S. Franceschi,2 E. Negri,1 R.Talamini, 3 F.Tomei 4 & C. LaVecchia 1 ' 5 yfstituto di Ricerche Farmacologiche®Mario Negri, Milan, Itajyjj2 International Agency for Research on Cancer, Lyon, France; Centro di Riferimento Oncologico, Aviano (Pordenone); *Cattedra di Medicina del Lavoro, Universita La Sapienza', Rome; Istituto di Statistica Medica e Biometria, Universita degli Studi di Milano, Milan, Italy
Summary Cancers of the upper digestive tract have long I Background: Be been associated with low socio-economic levels. It has however been suggested that in recent times the social gradient for these cancers is leveling off. Patients and methods: Data from three case-control studies on oral, pharyngeal and oesophageal cancer conducted in Northern Italy during the periods 1984-1992 and 1992-1997 were combined and re-analyzed. Cases were subjects admitted to the major teaching and general hospitals in the areas under study with incident, histologically confirmed cancer of the oral cavity and pharynx (n = 1126) and oesophagus (n - 714). Controls were subjects admitted to the same hospitals for a wide spectrum of acute, non-neoplastic conditions, not related to smoking or alcohol consumption (n - 4642).
Results; In the 1980s a significant association was observed with low education and social class level. The multivariate odds ratios for oral, pharyngeal and oesophageal cancers combined was 1.78 for the lowest versus the highest educational level, and 1.75 for the lowest versus the highest social class. No consistent pattern of risk was observed with any of the socio-economic indicators considered in the studies conducted in the 1990s. Conclusions: The present study indicates that the socioeconomic correlates of cancers of the upper digestive tract have changed over the last few years in Italy, with a disappearance of the social gradient.^
Key words: case-control studies, oesophageal cancer, oral pharyngeal cancer, risk factors, socio-economic factors
Introduction
Patients and methods
Cancers of the oral cavity, pharynx and oesophagus have long been associated with low socio-economic levels, as shown by low education and social class indicators [1-5]. This pattern of risk is partly, but not completely, accounted for by the higher tobacco and alcohol consumption and poorer diet in lowest social classes [6]. In a case-control study on upper digestive tract neoplasms conducted in the 1980s in northern Italy [4] the relative risk (RR) was around 5 for the lowest versus the highest level of education for oral and pharyngeal cancer, and around 3 for oesophagus. Corresponding values for the two highest versus the two lowest social classes were around 2 for both sites. It has, however, been suggested, on the basis of descriptive data, that in France the incidence for oesophageal cancer has decreased in the last 20 years in those social groups which bore the highest risk in the past, with a consequent leveling off or disappearance of the social gradient in oesophageal cancer risk [7]. We have therefore systematically re-considered the socio-economic correlates of cancers of the upper digestive tract, using data from three case-control studies conducted in Italy in the 1980s and in the 1990s.
Data of the present analysis derive from three case-control studies of upper digestive tract neoplasms conducted in the provinces of Milan and Pordenone in northern Italy between 1984 and 1997, whose general design has been described in detail [8-11]. Briefly, the first study [8, 9] was conducted between 1984 and 1992, and included 528 (449 men. 79 women) oral and pharyngeal cancer cases, 410 (343 men, 67 women) squamous oesophageal cancer cases, and 2408 (1816 men, 592 women) controls under age 75. The second one [10] was conducted between 1992 and 1997 on 598 (512 men, 86 women) oral and pharyngeal cancer cases, and 1491 (1008 men, 483 women) controls younger than 78. The third one [11] was conducted in the same period on 304 (275 men, 29 women) squamous-cell oesophageal cancer cases and 743 (593 men, 150 women) controls under age 78. In all the studies, cases were subjects admitted to the major teaching and general hospitals in the areas under study with incident, histologically confirmed cancer. Controls were subjects admitted to the same hospitals as the cases for a wide spectrum of acute, non-neoplastic conditions, not related to smoking or alcohol consumption (including acute surgical conditions, orthopaedic and non-alcohol related traumas, skin, eye. ear or nose and miscellaneous disorders). Similar structured questionnaires were used by trained interviewers in all study centers, and administered to both cases and controls during their hospital stay. The questionnaires included information on sociodemographic characteristics, including education and occupation; general life-style habits, such as tobacco smoking and alcohol drinking; a food frequency questionnaire; personal medical history and family history of cancer. The questionnaires were tested for reproducibility and reliability [12].
328 Table I. Distribution of 528 oral and pharyngeal cancer cases, 410 oesophageal cancer cases and 2408 controls, according to education and social class, and corresponding odds ratios" (OR) and 95% confidence intervals (CI). Northern Italy, 1984-1992. Number of subjects
Educationc (years) >\2 7-11 <7
OR (95% CI)
Oral cavity and pharynx
Oesophagus
Controls
27 92 408
45 69 294
402 660 1336
lb 1.32(0.82-2.14) 2.24(1.44-3.49)
X2 trend (/'-value) Social class 1-2 3 4-5 Farmers Other or unknown
Oral cavity and pharynx
21.18 (<0.0001)
13 113 293 96 13
lb 2.12(1.13-4.00) 2.56(1.38-4.74) 4.92 (2.47-9.78) 1.74(0.74-4.13)
216 764 1159 147 122
23 114 220 27 26
X2 trendd (P-value)
23.92 ( < 0.0001)
Oesophagus
lb 0.90(0.59-1.37) 1.60(1.10-2.31) 12.05 ( < 0.001)
lb 1.35(0.81-2.22) 1.46(0.90-2.38) 1.47(0.75-2.87) 1.45(0.75-2.80) 2.15(0.14)
All
lb 1.08(0.78-1.51) 1.78(1.32-2.40) 24.48 ( < 0.0001)
lb 1.56(1.03-2.35) 1.75(1.17-2.62) 2.61 (1.60-4.24) 1.65(0.95-2.87) 15.19(<0.0001)
" Estimates from unconditional logistic regression models, including terms for age, sex, study center, alcohol and tobacco consumption. b Reference category. c The sum does not add up to the total because of some missing values. d Other or unknown excluded.
Table 2. Distribution of 598 oral and pharyngeal cancer cases and 1491 controls, 304 oesophageal cancer cases and 743 controls, according to education and social class, and corresponding odds ratios" (OR) and 95% confidence intervals (CI). Northern Italy, 1992-1997. Number of subjects
Education0 (years) £12 7-11 <7
OR (95% CI)
Oral cavity and pharynx
Controls
Oesophagus
Controls
Oral cavity and pharynx
53 130 410
194 400 896
22 65 216
98 189 454
lb 0.66(0.42-1.03) 0.79(0.52-1.20)
X2 trend (f-value) Social class 1-2 3 4-5 Farmers Other or unknown
0.10(0.75)
23 113 373 59 30
82 406 747 147 109
9 74 181 31 9
59 206 370 75 33
X2 trendd (P-value)
lb 0.66(0.37-1.19) 0.84(0.48-1.48) 0.69(0.36-1.35) 0.73(0.35-1.51) 0.02 (0.88)
(Desophagus
b
.31 (0.70-2.45) .61 (0.90-2.87) :>.99 (0.08)
b
.53 (0.67-3.50) .59(0.71-3.55) .59 (0.64^.00) .96 (0.60-6.42) ().63 (0.43)
All
lb 0.83(0.57-1.19) 1.01(0.72-1.43) 0.61 (0.44)
lb 0.88(0.54-1.53) 1.06(0.67-1.70) 0.96(0.55-1.66) 1.00(0.54-1.86) 0.59 (0.44)
" Estimates from unconditional logistic regression models, including terms for age, sex, study center, alcohol and tobacco consumption. b Reference category. c The sum does not add up to the total because of some missing values. d Other or unknown excluded.
Education was classified according to the number of years at school, and categorized into three groups corresponding approximately to primary, secondary and higher education. Social classes were defined according to the head of household's occupation, with a classification derived from that used by the British Registrar General [13], and reclassified in three categories, corresponding to the Registrar General's social classes 1 and 2 (professional, managerial and intermediate), social class 3 (skilled occupation), and social classes 4 and 5 (partly skilled and unskilled occupations). Farmers and subjects with other or unknown occupation were included in two further categories. Odds ratios (OR), and the corresponding 95% confidence intervals
(CI), were estimated using unconditional multiple logistic regression models [14], including terms for age, sex, study center, alcohol and tobacco consumption.
Results Table 1 gives the distribution of oral, pharyngeal and oesophageal cancer cases and controls collected in the 1980s, according to education and social class.
329 For both social-economic indicators a significant in- consumption [18, 19] are included. The changed social verse association was observed: the OR for both cancers pattern over the last few years indicates, therefore, that combined was 1.8 (95% CI: 1.3-2.4) for the lowest versus the differential exposure in the main risk factors for the the highest educational level, and 1.8 (95% CI: 1.2-2.6) upper digestive tract neoplasms has tended to decline for subjects in social class 4 and 5, versus those in social (i.e., from 38.8% to 28% current smokers, respectively, class 1 and 2. The OR was 2.6 for farmers. The associa- in the two studies, and from 13% to 9% heavy alcohol tion with low social-economic indicators was, however, drinkers), following a general decrease in alcohol and stronger for oral and pharyngeal, than for oesophageal tobacco consumption in Italy, mostly in men [20-22], and a more widespread availability of a more affluent and cancer. Table 2 gives comparable data for the studies con- varied diet. ducted in the 1990s. No consistent pattern of risk was observed with any of the socio-economic indicators considered, the OR being 1.0 (95% CI: 0.7-1.4) for the Acknowledgements lowest versus the highest educational level, and 1.1 (95% CI: 0.7-1.7) for subjects in social class 4 and 5, com- This work was conducted with the support of the Italian pared with those in the highest class. Likewise, the OR Association for Cancer Research, Milan. The authors for farmers was close to unity. The ORs were apparently, thank Mrs M. P. Bonifacino for editorial assistance. but not significantly, above unity for oesophageal cancer, but the estimates were unstable, since only nine cases were in the highest social class category. References Discussion The present study indicates that the social correlates of cancers of the upper digestive tract have changed over the last few years, with a disappearance of the social gradient previously reported. A similar pattern has been observed for oesophageal cancer in the department of Calvados, France [7], and has been partly attributed to the changed histological types, with a recent rise in adenocarcinomas [15, 16]. The present data, however, indicate that the changes in social correlates are observed also for oesophageal squamous-cell cancers. This pattern is also reflected in the descriptive epidemiology of cancers of the oral cavity, pharynx and oesophagus, which, after decades of rises, have started to level off or decline in several European countries, including Italy [17]. The studies included in the present analysis are hospital-based and have some of the related limitations [14]. Since the study designs were similar, however, these can hardly account for such large differences in results between studies as those observed with reference to the social class indicators considered. Moreover the characteristics of the controls were similar in the two studies in terms of education (56% in the lower educational level for the first study and 59% for the second one) and social class (48% and 49%, respectively, in social class 4-5). Among the strengths of the studies considered, moreover, there are the large datasets, the adoption of comparable and reproducible social class indicators, as well as the possibility of careful allowance for alcohol and tobacco consumption. Further allowance for total vegetable and fruit intake only marginally modified the estimates of the socio-economic indicators. Tobacco smoking and heavy alcohol drinking account for over 75% of oral, pharyngeal and oesophageal cancer cases in Italy, a proportion which reaches 85% when indicators of a poorer diet, such as low fruit and vegetable
1. Elwood JM, Pearson JCG, Skippen DH. Jackson SM. Alcohol, smoking, social and occupational factors in the aetiology of cancer of the oral cavity, pharynx and larynx. Int J Cancer 1984; 34: 603-12. 2. Papadimitriou C, Day N, Tzonou A et al. Biosocial correlates of colorectal cancer in Greece. Int J Epidemiol 1984; 13: 155-9. 3. Levi F, Negri E, La Vecchia C, Te VC. Socioeconomic groups and cancer risk at death in the Swiss Canton of Vaud. Int J Epidemiol 1988; 17:711-7. 4. Ferraroni M, Negri E. La Vecchia C et al. Socioeconomc indicators, tobacco and alcohol in the aetiology of digestive tract neoplasms. Int J Epidemiol 1989; 18: 556-62. 5. Fernandez E, Borrell C. Cancer mortality by educational level in the city of Barcelona. Br J Cancer 1999; 79: 684-9. 6. La Vecchia C, Tavani A, Franceschi S et al. Epidemiology and prevention of oral cancer. Oral Oncol 1997; 33: 302-12. 7. Launoy G, Desoubeaux N, Leprieur A et al. Major changes in social characteristics in oesophageal cancer patients in France. Int J Cancer 2000; 5: 895-7. 8. Franceschi S, Talamini R, Barra S et al. Smoking and drinking in relation to cancers of the oral cavity, pharynx, larynx, and esophagus in Northern Italy. Cancer Res 1990; 50: 6502-7. 9. La Vecchia C, Liati P, Decarli A et al. Tar yields of cigarettes and the risk of oesophageal cancer. Int J Cancer 1986; 38: 381-5. 10. Franceschi S, Favero A, Levi F et al. Energy intake and dietary pattern in cancer of the oral cavity and pharynx. Cancer Causes Control 1999; 10: 439-44. 11. BosettiC, La Vecchia C, Talamini Ret al. Food groups and risk of squamous cell esophageal cancer in northern Italy. Int J Cancer 2000; 87: 289-94. 12. D'Avanzo B, La Vecchia C, Katsouyanni K et al. Reliability of information on cigarette smoking and beverage consumption provided by hospital controls. Epidemiology 1996; 5: 312-5. 13. Leete R, Fox AJ. Registrar General's Social Classes: Origins and uses. Population Trends 1977; 8: 1-7. 14. Breslow NE, Day NE. Statistical Methods in Cancer Research. Vol 1. The Analysis of Case-Control Studies. IARC Scientific Publication No. 32. Lyon, France: IARC 1980. 15. Devesa SS, Blot WJ, Fraumeni JF. Changing patterns in incidence of esophageal and gastric carcinoma in the United States. Cancer 1998; 83: 2049-53. 16. Levi F, Randimbison L, La Vecchia C. Esophageal and gastric carcinoma in Vaud, Switzerland, 1976-1994. Int J Cancer 1998; 75: 160-1. 17. Levi F, Lucchini F, Negri E et al. Cancer mortality in Europe,
330
18.
19.
20. 21.
1990-1994, and an overview of trends from 1955 to 1994. Eur J Cancer 1999; 35: 1477-516. Negri E, La Vccchia C, Francechi S, Tavani A. Attributable risk for oral cancer in northern Italy. Cancer Epidemiol Biomark Prev 1993; 2: 189-93. Negri E, La Vecchia C, Franceschi S et al. Attributable risks for oesophageal cancer in northern Italy. Eur J Cancer 1992; 28A: 1167-71. La Vecchia C. Alcohol in the Mediterranean diet: Assessing risks and benefits. Eur J Cancer Prev 1995; 4: 3-5. Pagano R, La Vecchia C, Decarli A. Smoking in Italy, 1994. Tumori 1996; 82: 309-13.
22. Pagano R, La Vecchia C, Decarli A. Smoking in Italy, 1995. Tumori 1998; 84: 456-9. Received 16 August 2000; accepted 13 November 2000. Correspondence to: Dr C. Bosetti Istituto di Ricerche Farmacologiche 'Mario Negri' Via Eritrea 62 20157 Milan Italy ^ E-mail :)
[email protected]