J Clin Castroenterol 1990;12(2):222-7.
0 1990 Raven Press, Ltd., New York
Epidemiological Profile John H. Kurata, Editor
Esophageal Carcinoma in Indian Jews of Southern Israel An Epidemiologic Study H. s. Odes, M.B., J. Krawiec, M.D.
Ch.B.,
J. Gross, M.P.H., T. Lozover,
The incidence of esophageal cancer varies in different populations and localities. The varied composition of the immigrant population of southern Israel afforded us an opportunity to investigate the frequency of the disease. The results of a retrospective study (1961-1985) revealed a high mean age-adjusted incidence rate (per 10’) in immigrant Indian men (6.5 t 2.17) and Indian women (17.2 t 5.12). Rates in all non-Indian immigrants were significantly lower: men 2.7 t 1.19, women 2.1 t 0.24. The relative risk of developing the disease was significantly higher in Indians. The age at diagnosis was lower in Indian women (54.6 t 10.4 years) than Indian men and other immigrants (p < 0.05). The clinical features were similar in all cases. The risk factors in Indian men were not apparent; in women, the indiscrete use of spices might have raised the rate o f esophageal cancer. The disease is more frequent in Indian populations in several parts of the world, and vigilance is required on the part of physicians. Key Words: Esophageal cancer-Indian-Jews-Incidence.
M.D.,
H. Vardi,
M.SC.,
and
The incidence rates of esophageal carcinoma vary in different geographical areas, being very high in the Honor Province of China, the Caspian area of Iran, the Turkmenistan area of Russia, and the Transkei in Southern Africa (1). By contrast, the incidence is low in the United States, Europe, and Israel (2-4). Studies of the epidemiology of this neoplasm can help to characterize populations at higher risk, as well as to define possible causative factors. The Beer Sheva and Ashkelon districts (total population 450,700 in 1985, mean population 318,460 during 1961-1985) account for most of the land area of the southern half of Israel. Fifty-eight percent of the Jewish population of this region is composed of immigrants from Europe, the Americas, North Africa, and Asia (5). Seventy percent of all Jewish migrants from India live in this region. There were 2,098 Indian Jews living in these districts in 1961, and their number increased steadily in the first decade of the study period; this population reached 7,569 in 1971 and 8,461 in 1985. The average Indian population in the period 1961-1985 was 6,782. In a report from the Soroka Medical Center (Beer Sheva) a decade ago, esophageal carcinoma was more common in Jewish immigrants from India than from other countries (6). The present study, which is an extension of our earlier limited survey, reports the incidence of esophageal carcinoma in the entire geographical area of southern Israel (with the exclusion of Eilat).
From the Gastroenterology Unit, Department of Internal Medicine (H.S.O., T.L., J.K.), and the Epidemiology and Health Sciences Evaluation Unit (J.G., H.V.), Soroka Medical Center and Faculty of Health Sciences, Ben Gurion University of the Negev, Beer Sheva, Israel. Address correspondence and reprint requests to Dr. H. S . Odes, Gastroenterology Unit, Soroka Medical Center, PO Box 151, Beer Sheva, 84101, Israel.
METHODS A retrospective study of esophageal carcinoma was carried out in the Jewish population of southern Israel
222
223
ESOPHAGEAL CARCINOMA IN INDIAN JEWS
YEAR A
I
197,
FIG. 1. (A) Incidence rate (crude) of esophageal cancer in Indian migrants (men, E;women, @ ) in southern Israel during the period 1961-1 985. (B) Incidence rate (crude) of esophageal cancer in other migrants (men, 0 ; women, m) in southern Israel during the period 1961-1 985.
lQ8! 5 I 0
I
I
5
10
I
I
I
15 20 25 CASES/100,000
I
I
30
35
I
40
YEAR B
197
i 4
5 0.0
from 1961 to 1985. Cases in permanent residents of the region were traced from clinical, radiologic, endoscopic, and pathologic records at the Soroka Medical Center in Beer Sheva and the Barzilai Hospital in Ashkelon, the only two hospitals serving the whole region. In addition, local residents with esophageal carcinoma treated elsewhere in the country were located from the files of the Central Cancer Registry in Jerusalem. Cases with adenocarcinoma arising in the upper stomach and infiltrating the esophagus were specifically excluded from the study (five such patients were detected). In 30% of the cases, it was possible to interview patients and/or relatives in order to study etiologic factors, including diet. As there were no statistically significant differences between the various non-Indian immigrant groups, their results are pooled as “others.” Results are expressed as the mean 2 standard deviation (SD). Incidence data were computed per 10’ population and are expressed as the crude rates as well as the age-adjusted rates (calculated by the direct method using the total population of Israel as the standard population). Data were processed utilizing SPSS-X (release 2.2), and the statistical analysis
0.5
1.0 CASES/ 100,000
1.5
2.0
included Student’s t test and the chi-square method. Differences were considered significant at p < 0.05.
RESULTS
In the 25-year study period, there were 108 patients with esophageal carcinoma. All of these cases occurred in the immigrant population. Of these, 22 cases (8 men, 14 women) occurred in Indian immigrants and 86 cases (54 men, 32 women) in immigrants from Europe and U.S.A. (42%) and North Africa, Near and Middle East (58%). Accordingly, the mean fema1e:male ratios in the period 1961-1985 were: Indian 1.75, others 0.59. As the Indian population was relatively small, the annual crude incidence rates in the Indians were much higher than in others (Fig. 1). The mean annual age-adjusted incidence rates (see methods) J Clin Gastroenterol, Vol. 12, No. 2,1990
H . S . ODES ET AL
224
TABLE 1. Mean annual age-adjusted” incidence rates of esophageal cancer in Indian and other immigrants in southern Israel during 1961-1985 Incidence rate per 1O5 population
Age group
Total
(years)
Men
Women
Indian
Others
Indian
Others
Indian
Others
30-44 45-59 60
4.2b 25.0’ 30.8
0.2 2.7 13.9
0.0 23.3’ 27.6
0.2 3.7 18.4
7.3’ 26.9’ 33.0
0.2 1.8 9.9
All (30+)
15.6’
3.8
13.5
4.9
17.1’
2.8
To standard Israel population. p < 0.05 Indian versus others.
a
’
over the entire period 1961-1985 were as follows: in men, Indian 6.5 i 2.17, others 2.7 ? 1.19 (p < 0.05); in women, Indian 17.2 i 5.12, others 2.1 i 0.24 (p < 0.05). Examination of the mean annual age-adjusted incidence rates per age group (30 years and older) revealed significant differences, particularly in the 45-59-year age group (Table 1). The greater age-adjusted incidence rate in Indian women was noted in all age groups over 30 years. The relative risk (295% confidence intervals) of esophageal carcinoma in Indians compared with others was as follows: Indian total population 4.1 2 3.2 (p < 0.05); Indian women 6.2 ? 3.0 (p < 0.05); Indian men 2.8 i. 2.9 (p value not significant). A further striking difference between Indians and others was detected in the age at time of diagnosis of esophageal carcinoma. In all populations, there were no cases under the age of 30 years. The Indians had a younger age at diagnosis than the controls, whose disease developed later in life (Fig. 2). In the whole population, the mean age at diag-
%
6o
r
nosis was 64.8 2 11.2 years (Table 2). The age at diagnosis in Indian migrants, 57.5 t 10.9 years, was significantly lower than in others, 66.7 i 10.6 years (p < 0.05); this difference was the result of the younger age of occurrence of esophageal carcinoma in Indian women, 54.6 ? 10.4 years, compared with other women, 66.2 i 10.5 years (p < 0.05). Indian women with esophageal carcinoma were on average 8 years younger than Indian men, who in turn were 4 years younger than other men. The mean age at diagnosis was about the same in other men and women. The mean ages in each patient group did not fluctuate significantly over the time period of the study; the Indian patients were consistently younger than controls. The frequency of the symptoms and signs in our patients is given in Table 3. Dysphagia was the most common symptom in all patient groups. Other features noted frequently were weight loss, anorexia, and pain. Lesions were located most commonly in the lower third of the esophagus (Indians 55%,
OF CASES
50 40
FIG. 2. Age at diagnosis of esophageal cancer in Indian (=) and other ( ) migrant groups during 1961-1985. There were no cases in subjects under 30 years of age.
30 20 10 A
30-44
45-69
60-74
AGE AT DIAGNOSIS (YRS) J Clin Gastroenterol, Vol. 12, No. 2, 1990
75+
ESOPHAGEAL CARCINOMA I N INDIAN JEWS TABLE 2. Mean age i SD at diagnosis in Indian and other immigrants Migrant group
Total (years)
Men (years)
Women (years)
All persons Indian Others
64.8 ? 11.2 57.5 2 10.9” 66.7 t 10.6’
66.4 ? 10.7 62.6 2 10.5 66.9 ? 10.7
62.6 2 11.7 54.6 i 10.4c 66.2 2 10.5d
225
ly spiced with curry, ginger, saffron, cloves, peppers, and cinnamon. Indian men usually had their main meals at their places of work (often factories), and their exposure to these spices was likely to be less. In other patients, there were 48% smokers and 27% drinkers. No specific dietary habits were discerned in this group.
a versus b, p < 0.05. c versus d, p < 0.01,
DISCUSSION
others 54%), with the middle third being the next most common site (Indians 28%, others 35%). Keratinizing and nonkeratinizing squamous carcinoma was the most frequent tumor (Indian 91%, others 79%), followed by undifferentiated carcinoma, sarcoma, and melanoma (Indian 9%, others 15%). True esophageal adenocarcinoma was found in 6% of controls. Treatment was similar in both groups; 64% of Indians were subjected to surgical treatment and 50% received radiotherapy; in others, the figures were 46% and 47%, respectively. Chemotherapy was offered in 17% of Indians and 11% of others. The life expectancy was somewhat better in controls than in Indians: in 51 patients that died in 1961-1985, the mean survival time was 0.3 years in Indians and 0.8 years in others. Appropriate data on social and dietary risk factors were obtained in 44% of cases (this low figure being the result of the retrospective nature of the study). The socioeconomic status of controls was significantly better than that of Indian Jews (p < 0.005). Four male Indian patients (50%) were characterized as heavy smokers and drinkers; in control men, the rate of smoking and drinking was 59%. Neither smoking nor drinking was observed in the female Indian patients, whose distinguishing risk factor appeared to be in their diet. Eighty percent of Indian women ate traditional Indian home-cooked foods, most often boiled vegetables and rice, heaviTABLE 3. Presenting features of esophageal carcinoma in Indians and others Indian Features Dysphagia Weight loss Anorexia Pain Anemia Vomiting Hoarseness Couqh
Others
Men Yo
Women
Men
Women
Oh
%
%
76 38 38 19 0 13 0
72 36 36 29 14 0 0
0
0
60 35 50 11 7 11 4 4
62 19 19 31 9 12 9 6
Our study has confirmed that the previously reported low rate (2.340’) and the male preponderance (fema1e:male ratio 0.63) of esophageal carcinoma in Israel (4) do not apply to the immigrants from India, who have a high rate of incidence of this neoplasm, with more cases occurring in women than in men. Furthermore, the lesion develops about one decade earlier in Indian women compared with Indian men and all non-Indian subjects. In the non-Indian immigrants (others), however, the frequency of esophageal cancer and the male: female ratio were similar to the previous data from Israel (4). No cases of esophageal carcinoma were found in the native-born population, probably because this group was comparatively much younger in age than the immigrants. Shani and Modan (4) observed that Asian immigrants had a relatively higher incidence of esophageal cancer in the under 60 age group than European and American immigrants; their Asian patients derived principally from regions in Iran that have a known high frequency of this neoplasm. Odes and Krawiec (6) reported that Indian Jews constituted 9 of 21 cases of esophageal cancer in Beer Sheva; the incidence rates, however, were not determined. Our present study, carried out in all of southern Israel, confirms that Indian Jews have a several-fold higher incidence of esophageal carcinoma than other immigrants. As the disease in southern Israel was detected in the immigrants, we examined the rate and characteristics of esophageal cancer in their countries of origin. Cancer of the esophagus is very common in certain regions of the Indian subcontinent (2). The vast majority of Indian Jews, as well as most of our cases of esophageal cancer, originated from the greater Bombay area on the west coast of India. This locality has been studied in detail: Malhotra (7) found that esophageal carcinoma was the third most common gastrointestinal malignancy (1 1% of cancers) in Bombay-seven times more frequent in men than women. Desai et al. (8) reported in 1969 that the age-adjusted incidence rate in Bombay was J Clin Gastroentcrol, V o / . 12, N o . 2,1990
H . S. ODES ET AL. 14.4 in men and 11.0 in women. Jussawalla (9) in 1981 reported an age-adjusted incidence rate of 15.2 in men and 10.8 in women in Bombay. Crude incidence rates from Bombay, reported by Gangadharan (10) in 1974, were lower, with frequencies of 6.1 in men and 5.1 in women; however, similar crude rates were given by Jussawalla (9). Crude incidence rates by Malhotra (7) were 4.5, 3.5, and 2.4 in the total populations in western, southern, and northern India, respectively. In Manipur, eastern India, men with cancer of the esophagus outnumbered women in the ratio of 1.36; incidence data were not reported (11). Most or all of these cases from India, were not Jewish. In comparison with these data, the incidence in male and female Indian Jews in Israel is higher still (Table 1). As already noted, incidence rates in all non-Indian immigrant groups were low. Men outnumber women with esophageal cancer in almost all countries, including such high incidence areas as Malaysia (Chinese), Natal (Africans), Zimbabwe, certain provinces of France, urban black populations in the United States, Brazil (San Paulo), and Hawaii (2,3,12-14). The exceptions are Natal Indians, where the age-adjusted incidence rates were 5.5 in men and 12.9 in women, Malaysian Indians with rates of 5.6 and 5.9, respectively, and Malaysian Chinese with rates of 1.2 and 3.0 (2,14). Interestingly, we found that in Israel, the fema1e:male ratio in Indians with esophageal carcinoma was 1.75, which is markedly different from the fema1e:male ratio in Bombay (7-9). It will be important to follow this relationship in the future. In the “others,” the fema1e:male ratio was
0 1990 Raven Press, Ltd., New York
Epidemiological Profile John H. Kurata, Editor
Esophageal Carcinoma in Indian Jews of Southern Israel An Epidemiologic Study H. s. Odes, M.B., J. Krawiec, M.D.
Ch.B.,
J. Gross, M.P.H., T. Lozover,
The incidence of esophageal cancer varies in different populations and localities. The varied composition of the immigrant population of southern Israel afforded us an opportunity to investigate the frequency of the disease. The results of a retrospective study (1961-1985) revealed a high mean age-adjusted incidence rate (per 10’) in immigrant Indian men (6.5 t 2.17) and Indian women (17.2 t 5.12). Rates in all non-Indian immigrants were significantly lower: men 2.7 t 1.19, women 2.1 t 0.24. The relative risk of developing the disease was significantly higher in Indians. The age at diagnosis was lower in Indian women (54.6 t 10.4 years) than Indian men and other immigrants (p < 0.05). The clinical features were similar in all cases. The risk factors in Indian men were not apparent; in women, the indiscrete use of spices might have raised the rate o f esophageal cancer. The disease is more frequent in Indian populations in several parts of the world, and vigilance is required on the part of physicians. Key Words: Esophageal cancer-Indian-Jews-Incidence.
M.D.,
H. Vardi,
M.SC.,
and
The incidence rates of esophageal carcinoma vary in different geographical areas, being very high in the Honor Province of China, the Caspian area of Iran, the Turkmenistan area of Russia, and the Transkei in Southern Africa (1). By contrast, the incidence is low in the United States, Europe, and Israel (2-4). Studies of the epidemiology of this neoplasm can help to characterize populations at higher risk, as well as to define possible causative factors. The Beer Sheva and Ashkelon districts (total population 450,700 in 1985, mean population 318,460 during 1961-1985) account for most of the land area of the southern half of Israel. Fifty-eight percent of the Jewish population of this region is composed of immigrants from Europe, the Americas, North Africa, and Asia (5). Seventy percent of all Jewish migrants from India live in this region. There were 2,098 Indian Jews living in these districts in 1961, and their number increased steadily in the first decade of the study period; this population reached 7,569 in 1971 and 8,461 in 1985. The average Indian population in the period 1961-1985 was 6,782. In a report from the Soroka Medical Center (Beer Sheva) a decade ago, esophageal carcinoma was more common in Jewish immigrants from India than from other countries (6). The present study, which is an extension of our earlier limited survey, reports the incidence of esophageal carcinoma in the entire geographical area of southern Israel (with the exclusion of Eilat).
From the Gastroenterology Unit, Department of Internal Medicine (H.S.O., T.L., J.K.), and the Epidemiology and Health Sciences Evaluation Unit (J.G., H.V.), Soroka Medical Center and Faculty of Health Sciences, Ben Gurion University of the Negev, Beer Sheva, Israel. Address correspondence and reprint requests to Dr. H. S . Odes, Gastroenterology Unit, Soroka Medical Center, PO Box 151, Beer Sheva, 84101, Israel.
METHODS A retrospective study of esophageal carcinoma was carried out in the Jewish population of southern Israel
222
223
ESOPHAGEAL CARCINOMA IN INDIAN JEWS
YEAR A
I
197,
FIG. 1. (A) Incidence rate (crude) of esophageal cancer in Indian migrants (men, E;women, @ ) in southern Israel during the period 1961-1 985. (B) Incidence rate (crude) of esophageal cancer in other migrants (men, 0 ; women, m) in southern Israel during the period 1961-1 985.
lQ8! 5 I 0
I
I
5
10
I
I
I
15 20 25 CASES/100,000
I
I
30
35
I
40
YEAR B
197
i 4
5 0.0
from 1961 to 1985. Cases in permanent residents of the region were traced from clinical, radiologic, endoscopic, and pathologic records at the Soroka Medical Center in Beer Sheva and the Barzilai Hospital in Ashkelon, the only two hospitals serving the whole region. In addition, local residents with esophageal carcinoma treated elsewhere in the country were located from the files of the Central Cancer Registry in Jerusalem. Cases with adenocarcinoma arising in the upper stomach and infiltrating the esophagus were specifically excluded from the study (five such patients were detected). In 30% of the cases, it was possible to interview patients and/or relatives in order to study etiologic factors, including diet. As there were no statistically significant differences between the various non-Indian immigrant groups, their results are pooled as “others.” Results are expressed as the mean 2 standard deviation (SD). Incidence data were computed per 10’ population and are expressed as the crude rates as well as the age-adjusted rates (calculated by the direct method using the total population of Israel as the standard population). Data were processed utilizing SPSS-X (release 2.2), and the statistical analysis
0.5
1.0 CASES/ 100,000
1.5
2.0
included Student’s t test and the chi-square method. Differences were considered significant at p < 0.05.
RESULTS
In the 25-year study period, there were 108 patients with esophageal carcinoma. All of these cases occurred in the immigrant population. Of these, 22 cases (8 men, 14 women) occurred in Indian immigrants and 86 cases (54 men, 32 women) in immigrants from Europe and U.S.A. (42%) and North Africa, Near and Middle East (58%). Accordingly, the mean fema1e:male ratios in the period 1961-1985 were: Indian 1.75, others 0.59. As the Indian population was relatively small, the annual crude incidence rates in the Indians were much higher than in others (Fig. 1). The mean annual age-adjusted incidence rates (see methods) J Clin Gastroenterol, Vol. 12, No. 2,1990
H . S . ODES ET AL
224
TABLE 1. Mean annual age-adjusted” incidence rates of esophageal cancer in Indian and other immigrants in southern Israel during 1961-1985 Incidence rate per 1O5 population
Age group
Total
(years)
Men
Women
Indian
Others
Indian
Others
Indian
Others
30-44 45-59 60
4.2b 25.0’ 30.8
0.2 2.7 13.9
0.0 23.3’ 27.6
0.2 3.7 18.4
7.3’ 26.9’ 33.0
0.2 1.8 9.9
All (30+)
15.6’
3.8
13.5
4.9
17.1’
2.8
To standard Israel population. p < 0.05 Indian versus others.
a
’
over the entire period 1961-1985 were as follows: in men, Indian 6.5 i 2.17, others 2.7 ? 1.19 (p < 0.05); in women, Indian 17.2 i 5.12, others 2.1 i 0.24 (p < 0.05). Examination of the mean annual age-adjusted incidence rates per age group (30 years and older) revealed significant differences, particularly in the 45-59-year age group (Table 1). The greater age-adjusted incidence rate in Indian women was noted in all age groups over 30 years. The relative risk (295% confidence intervals) of esophageal carcinoma in Indians compared with others was as follows: Indian total population 4.1 2 3.2 (p < 0.05); Indian women 6.2 ? 3.0 (p < 0.05); Indian men 2.8 i. 2.9 (p value not significant). A further striking difference between Indians and others was detected in the age at time of diagnosis of esophageal carcinoma. In all populations, there were no cases under the age of 30 years. The Indians had a younger age at diagnosis than the controls, whose disease developed later in life (Fig. 2). In the whole population, the mean age at diag-
%
6o
r
nosis was 64.8 2 11.2 years (Table 2). The age at diagnosis in Indian migrants, 57.5 t 10.9 years, was significantly lower than in others, 66.7 i 10.6 years (p < 0.05); this difference was the result of the younger age of occurrence of esophageal carcinoma in Indian women, 54.6 ? 10.4 years, compared with other women, 66.2 i 10.5 years (p < 0.05). Indian women with esophageal carcinoma were on average 8 years younger than Indian men, who in turn were 4 years younger than other men. The mean age at diagnosis was about the same in other men and women. The mean ages in each patient group did not fluctuate significantly over the time period of the study; the Indian patients were consistently younger than controls. The frequency of the symptoms and signs in our patients is given in Table 3. Dysphagia was the most common symptom in all patient groups. Other features noted frequently were weight loss, anorexia, and pain. Lesions were located most commonly in the lower third of the esophagus (Indians 55%,
OF CASES
50 40
FIG. 2. Age at diagnosis of esophageal cancer in Indian (=) and other ( ) migrant groups during 1961-1985. There were no cases in subjects under 30 years of age.
30 20 10 A
30-44
45-69
60-74
AGE AT DIAGNOSIS (YRS) J Clin Gastroenterol, Vol. 12, No. 2, 1990
75+
ESOPHAGEAL CARCINOMA I N INDIAN JEWS TABLE 2. Mean age i SD at diagnosis in Indian and other immigrants Migrant group
Total (years)
Men (years)
Women (years)
All persons Indian Others
64.8 ? 11.2 57.5 2 10.9” 66.7 t 10.6’
66.4 ? 10.7 62.6 2 10.5 66.9 ? 10.7
62.6 2 11.7 54.6 i 10.4c 66.2 2 10.5d
225
ly spiced with curry, ginger, saffron, cloves, peppers, and cinnamon. Indian men usually had their main meals at their places of work (often factories), and their exposure to these spices was likely to be less. In other patients, there were 48% smokers and 27% drinkers. No specific dietary habits were discerned in this group.
a versus b, p < 0.05. c versus d, p < 0.01,
DISCUSSION
others 54%), with the middle third being the next most common site (Indians 28%, others 35%). Keratinizing and nonkeratinizing squamous carcinoma was the most frequent tumor (Indian 91%, others 79%), followed by undifferentiated carcinoma, sarcoma, and melanoma (Indian 9%, others 15%). True esophageal adenocarcinoma was found in 6% of controls. Treatment was similar in both groups; 64% of Indians were subjected to surgical treatment and 50% received radiotherapy; in others, the figures were 46% and 47%, respectively. Chemotherapy was offered in 17% of Indians and 11% of others. The life expectancy was somewhat better in controls than in Indians: in 51 patients that died in 1961-1985, the mean survival time was 0.3 years in Indians and 0.8 years in others. Appropriate data on social and dietary risk factors were obtained in 44% of cases (this low figure being the result of the retrospective nature of the study). The socioeconomic status of controls was significantly better than that of Indian Jews (p < 0.005). Four male Indian patients (50%) were characterized as heavy smokers and drinkers; in control men, the rate of smoking and drinking was 59%. Neither smoking nor drinking was observed in the female Indian patients, whose distinguishing risk factor appeared to be in their diet. Eighty percent of Indian women ate traditional Indian home-cooked foods, most often boiled vegetables and rice, heaviTABLE 3. Presenting features of esophageal carcinoma in Indians and others Indian Features Dysphagia Weight loss Anorexia Pain Anemia Vomiting Hoarseness Couqh
Others
Men Yo
Women
Men
Women
Oh
%
%
76 38 38 19 0 13 0
72 36 36 29 14 0 0
0
0
60 35 50 11 7 11 4 4
62 19 19 31 9 12 9 6
Our study has confirmed that the previously reported low rate (2.340’) and the male preponderance (fema1e:male ratio 0.63) of esophageal carcinoma in Israel (4) do not apply to the immigrants from India, who have a high rate of incidence of this neoplasm, with more cases occurring in women than in men. Furthermore, the lesion develops about one decade earlier in Indian women compared with Indian men and all non-Indian subjects. In the non-Indian immigrants (others), however, the frequency of esophageal cancer and the male: female ratio were similar to the previous data from Israel (4). No cases of esophageal carcinoma were found in the native-born population, probably because this group was comparatively much younger in age than the immigrants. Shani and Modan (4) observed that Asian immigrants had a relatively higher incidence of esophageal cancer in the under 60 age group than European and American immigrants; their Asian patients derived principally from regions in Iran that have a known high frequency of this neoplasm. Odes and Krawiec (6) reported that Indian Jews constituted 9 of 21 cases of esophageal cancer in Beer Sheva; the incidence rates, however, were not determined. Our present study, carried out in all of southern Israel, confirms that Indian Jews have a several-fold higher incidence of esophageal carcinoma than other immigrants. As the disease in southern Israel was detected in the immigrants, we examined the rate and characteristics of esophageal cancer in their countries of origin. Cancer of the esophagus is very common in certain regions of the Indian subcontinent (2). The vast majority of Indian Jews, as well as most of our cases of esophageal cancer, originated from the greater Bombay area on the west coast of India. This locality has been studied in detail: Malhotra (7) found that esophageal carcinoma was the third most common gastrointestinal malignancy (1 1% of cancers) in Bombay-seven times more frequent in men than women. Desai et al. (8) reported in 1969 that the age-adjusted incidence rate in Bombay was J Clin Gastroentcrol, V o / . 12, N o . 2,1990
H . S. ODES ET AL. 14.4 in men and 11.0 in women. Jussawalla (9) in 1981 reported an age-adjusted incidence rate of 15.2 in men and 10.8 in women in Bombay. Crude incidence rates from Bombay, reported by Gangadharan (10) in 1974, were lower, with frequencies of 6.1 in men and 5.1 in women; however, similar crude rates were given by Jussawalla (9). Crude incidence rates by Malhotra (7) were 4.5, 3.5, and 2.4 in the total populations in western, southern, and northern India, respectively. In Manipur, eastern India, men with cancer of the esophagus outnumbered women in the ratio of 1.36; incidence data were not reported (11). Most or all of these cases from India, were not Jewish. In comparison with these data, the incidence in male and female Indian Jews in Israel is higher still (Table 1). As already noted, incidence rates in all non-Indian immigrant groups were low. Men outnumber women with esophageal cancer in almost all countries, including such high incidence areas as Malaysia (Chinese), Natal (Africans), Zimbabwe, certain provinces of France, urban black populations in the United States, Brazil (San Paulo), and Hawaii (2,3,12-14). The exceptions are Natal Indians, where the age-adjusted incidence rates were 5.5 in men and 12.9 in women, Malaysian Indians with rates of 5.6 and 5.9, respectively, and Malaysian Chinese with rates of 1.2 and 3.0 (2,14). Interestingly, we found that in Israel, the fema1e:male ratio in Indians with esophageal carcinoma was 1.75, which is markedly different from the fema1e:male ratio in Bombay (7-9). It will be important to follow this relationship in the future. In the “others,” the fema1e:male ratio was
