J Chron Dis 1975, Vol. 28, pp. 349-358. Pergamon Press. Printed
in Great Britain
STOMACH AND COLON CANCER MORTALITY AMONG PUERTO RICANS IN NEW YORK CITY AND PUERTO RICO* MARY MONK and M. ELLEN WARSHAUER
Department
of Community and Preventive Medicine, New York Medical College, Fifth Avenue at 106th Street, New York, New York 10029 (Received in revised.form 18 November 1974)
EPIDEMIOLOGIC studies comparing migrant and nonmigrant populations have multiplied in recent years, the principal reason, of course, being the opportunity to study the relative importance of environmental and constitutional factors [l-6]. In stomach cancer, the evidence indicates that early environmental exposure or constitutional factors may be more important than recent environmental conditions, since mortality rates for migrants tend to be closer to those in their home country than to those in the country to which they moved. In colon cancer, on the other hand, migrants tend to die at rates prevalent in their host rather than in their native country. This finding implies that a recent exposure to a condition or factor in the host country may be important in the development of colon cancer. Indeed, the diet in countries with high colon cancer rates has already been indicted for its role in this disease; studies completed and in progress suggest to many a guilty verdict [7-IO]. A study of Puerto Rican migrants to New York City affords an opportunity to examine changes in stomach cancer mortality, which is higher in Puerto Rico than in New York, and changes in colon cancer mortality, which is lower in Puerto Rico [ Ill. Puerto Ricans in New York are different in a number of respects from migrants from other countries to the United States [12]. First, the vast majority of Puerto Ricans came to New York after World War II, whereas migrants from Europe and the Orient came in largest numbers before 1924. Second, Puerto Ricans frequently travel back and forth between New York and Puerto Rico, staying for unknown lengths of time in one place or the other. Thus, it is not easy to know for how long a Puerto Rican dying in New York may have been exposed to a particular environmental condition. Migrants from other areas tend to have stayed continuously in the United States since their first entry. *This investigation was supported in part by Grant No. 1N 96A from the American Cancer Society and by General Research Support Grant RR-05398 from the General Research Support Branch, Division of Research Resources, National Institutes of Health. 349
MARY MONK and M. ELLENWARSHAUER
350
Despite these unique characteristics of Puerto Ricans in New York, we felt that comparisons among Puerto Ricans in New York, Puerto Ricans in Puerto Rico, and other population groups in New York might add to an understanding of stomach and colon cancer. METHODS
Since the middle 1950’s, the New York City Department of Health has tabulated separately deaths among Puerto Rican-born persons. Since the number of deaths from colon or stomach cancer was quite small until about 1960, we have confined our analysis to deaths in three periods-1958-1962, 1963-1967, and 1968-1971. Deaths from the two cancers were obtained for Puerto Ricans, other whites and nonwhites, by age and sex, for these three periods, and rates were calculated using the 1960 and 1970 census figures and an intercensal estimate. The Cancer Control Division in Puerto Rico kindly sent us the numbers of persons dying from stomach and colon cancer in Puerto Rico for the years 1965-1971. Data for the period before 1965 were ;available in Cancer in Puerto Rico, 1950-1964 [l 11. Population data for Puerto Rico were obtained from the 1960 and 1970 United States censuses and estimated for 1965. On the New York City death certificate, the number of years the deceased person had lived in New York City immediately prior to death is recorded. This information was abstracted for every Puerto Rican who died from colon cancer between 1958 and 1971. Because of the large numbers involved, it was abstracted only in the 3-yr periods around 1960, 1965 and 1970 for those Puerto Ricans dying of stomach cancer. RESULTS
Table 1 shows the population distribution by age of the different groups in 1970. The whites were older than all the other groups, while the Puerto Rican-born in New York had the smallest proportion under 25 yr. Except for whites, all groups had a larger population in 1970 than in 1960. In all groups, the proportion of the population 65 yr TABLE 1. 1970 POPULATION AGE DISTRIBUTION (IN PERCENTAGES) FOR WHITES,NONWHITESAND PUERTORICAN-BORN RESIDENTS OF NEW YORK CITY AND FORRESIDENTS OF PUERTORICO New York Whites
/\sc
Non-Whites
City Puerto
Rican-Born
Puerto
Rico
36.9%
49.6%
32.7%
55.9%
25 - 44
22.6
28.5
43.7
22.6
45 - 54
12.7
IO.1
12.1
a.4
55 - 64
13.0
6.5
7.0
6.6
65 - 74
9.7
3.7
3.1
4.0
75 or
5.'1
1.6
1.4
2.5
100.0%
100.0%
100.0%
24
years
or
more
Total Population
less
100.0
5,605,633
1,815,929
473,300
2,712,033
Stomach
and Colon Cancer Mortality
351
and older increased in the lo-yr period. Table 2 presents the number of deaths from colon and stomach cancer in the three different periods. It should be noted that there were very few colon cancer deaths among Puerto Rican males in New York in the carlicst period. TABLE 2. NCMUER CITY
UE DEATHS PROM STOMACH AND COLON CANCER FOR GIVEN PERIODS IN Ntw YORK AND
PUERTO
RICO
BY SEX, POPULATlON
New Time
Period
White
York
AND TIME PERIOD
City
Non-White Males
GROUP
Puerto - Stomach
Rican-Born
Puerto
Rico
Cancer
1958-62
3,837
528
122
1,373
1563-67
3,062
509
Ill
1,450
1968-71
2,031
411
96
1,108
Females
- Stomach
Cancer
191;8-62
2,449
314
71
663
1963-67
2,030
325
77
683
1968-71
1,351
228
81
544
Males
-
Colon
Cancer
1958-62
4,502
295
I9
180
1963-67
4,710
373
44
200
lY68-71
3,696
342
43
199
Females
-
Colon
Cancer
1958-62
4,569
364
44
225
1963-67
4,516
466
61
280
1968-71
3,627
396
61
249
Table 3 compares the annual age-adjusted rates of the different groups for the three periods. In stomach cancer, the rates have decreased over time by about one-third for all groups except Puerto Rican-born women in New York who showed little change. In the earliest period, it is clear that Puerto Ricans in New York had rates of stomach cancer substantially below those for Puerto Ricans in Puerto Rico and higher than those of other whites in New York. This pattern was maintained in 1970. In comparison with nonwhites, the Puerto Ricans in New York had somewhat lower rates of stomach cancer. In colon cancer, a different picture emerges. Puerto Rican-born men in New York had a 90 per cent increase in colon cancer death rates from the 1960 to 1965 period, whereas all other groups changed relatively little over that time. Between 1965 and 1970, no group showed much change. In 1960, the rates for Puerto Ricans in New York
MARY MONK and M. ELLEN WARSHAUER
352
were much lower than those for other whites and nonwhites and about the same as those for Puerto Ricans in Puerto Rico. By 1970, the New York Puerto Ricans still had much lower rates than other New York residents but somewhat higher rates than island Puerto Ricans.
TABLE 3. AVERAGEANNUAL AGE-ADJUSTED MORTALI~ RATES*(PER 100,000)FORSTOMACH AND COLON CANCERIN NEW YORK Cm AND PUERTORICO BY SEX,POPULATIONGROUPAND TIMEPERIOD
New York City
Time Period
White
Non-White
Puerto Rican-Born
Puerto Rico
Males - Stomach Cancer 1958-62
24.3
36.0
31.2
45.4
1963-67
19.4
27.3
23.0
40.3
1968-71
16.6
23.0
21.0
33.3
Females - Stomach Cancer
1958-62
12.7
17.7
13.2
22.7
1963-67
10.1
13.5
11.6
18.4
1968-71
8.1
11.8
12.8
15.6
Males - Colon Cancer 1958-62
27.6
19.9
4.8
5.9
1963-67
29.7
20.0
9.0
5.5
1968-71
30.1
19.0
9.3
5.9
Females - Colon Cancer 1958-62
23.7
20.3
8.1
7.3
1W-67
22.6
19.2
9.1
7.8
1968-71
21.9
16.1
9.5
7.1
*Indirect adjustment,
New York State rates for 1965 used as standard
It should be noted that the rates for other whites in New York City include both native and foreign-born persons. The proportion of foreign-born approached 25 per cent among persons 45-64 yr and 50 per cent among persons 65 yr and over in New York in 1970. The foreign-born in New York City have higher rates of stomach cancer than native whites [13, 141.Thus, if only native-born whites had been considered in Table 3, the rates for stomach cancer for other whites in New York would have been lower and the difference between Puerto Rican migrants and other whites in New York would have been larger, a difference about the same as the difference between Puerto Ricans in New York and in Puerto Rico. Colon cancer rates were nearly the same in New York City for foreign-born and native-born whites [14].
Stomach and Colon Cancer Mortality
353
Age-specific rates for the two groups of Puerto Ricans and for whites are shown in Tables 4 and 5. (For purposes of clarity, the age-specific rates for nonwhites are not shown in these tables. Changes in age-specific rates for nonwhites over time paralleled the changes for age-adjusted rates.) Most of the rates for Puerto Ricans under 45 yr are based on numbers of less than 20 and in the earliest period, the colon cancer rates for Puerto Rican men at any age are based on numbers less than 10. Statistically significant differences between Puerto Ricans in New York City and in Puerto Rico are noted in these tables. TABLE
4.
AGE-SPECIFICMORTALITYRA~S(PER~~~,~~~)FORSTOMACHCANCER,BYSEXANDPOPULATION GROUP IN THREE TIME PERIODS
Males
Females
25 - 44 Years Time Period
White
PR/NYC
PR/PR
White
lg56-62
2.8
2.5”
4.6
1.9
1963-67
1.9
2.2”
3.7
1.4
1.7 >ft*
3.0
1968-71
1.4
4.oa
2.7
1.1
1.5 hC
1.4*
PR/NYC
-43””
PR/PR
3.7
45 - 64 Years 1958-62
31.9
36.9
64.5+
1411
20.5
27.9
1963-67
24.2
28.4
53.3t
Il.9
15.6
21.3
1968-71
22.3
23.8
43.5+
9.7
13.1
23.ot
65 Years or
More
1958-62
144.0
236.0
271.2
84.3
79.8
13O.b
1W-67
123.7
146.7
252.4+
65.9
65.7
117.y
1968-71
100.3
127.5
210.9+
52.2
go.0
92.5
*Based on 10 to lg deaths **Based on g or fewer deaths tDifference
between Puerto Ricans
in New York and in Puerto Rico is significant
at p - 0.01 or less
Table 4 shows that the general picture for stomach cancer is much the same for the older age groups, 45-64 and 65 yr or more, as for the total group. In the earliest period, stomach cancer rates for Puerto Rican men in New York are lower than those for men in Puerto Rico and higher than for other whites. By 1970, rates for all groups had decreased at about the same rate. For women, there is less consistency; the rates for the oldest group of Puerto Ricans in New York increased from the 1965 to 1970 period as did, to a lesser extent, the rates for Puerto Ricans in Puerto Rico in the 45-64 age group. But in all instances, rates for women in New York were lower than for women in Puerto Rico.
354
MARY
and M.ELLENWARSHAUER
MONK
For colon cancer (Table 5), the rates for Puerto Rican women in New York and in Puerto Rico began at about the same level in 1960 but diverged slightly by 1970 with the New York rates becoming higher. For men, this was true only for the age group 65 yr and older. In 1960, Puerto Rican men in New York aged 45-64 yr had lower rates of colon cancer than did island Puerto Ricans, but by 1970 had higher rates.
TABLE 5. AGE-SPECIFICMORTALITY RATES(PER 100,000)FOR CROUP
IN THREE
TIME
COLON
CANCER,
BY SEX AND
POPULATION
PERIODS
Males
Females
25 - 44 Years -PR/PR
PR/NYC
Time Period
White
1958-62
2.8
, . , 3""
1963-67
2.5
1968-71
2.5
White
Pp./NYC
.5""
3.3
. 855
, .a XJ:
, . 2:‘:
2.4
1.2 :t"
1 6 :>:t
1.7
2.8
-35""
PR/PR
, ,O” 1.4 0.7";:
45 - 64 Years -1958-62
36.8
1963-67
38.7
1968-71
38.1
7.8+
34.9
12.0
10.2
10.6 +
6.5
32.4
12.3
9.9
Il.6 -c
6.7
32.7
14.1
a.7
3.9
!:A
65 y ears or More 1958-62
170.9
35.0 *;t
36.6
138.0
45.9 +
42.8
1963-67
187.5
49.9 *
33.7
135.8
52.6
44.3
1968-71
192.0
54.6 *
35.3
129.7
53.7
46.2
"Based on IO to 19 deaLhs C::Based on y or fewer deaths +Difference
between Puerto Ricans
in New York and in Puerto Rico is significant
et P = 0.05 or less
Table 6 shows the average number of years Puerto Ricans dying in New York had lived in New York. The accuracy of these data is unknown; this item is not coded for routine use by the health department. The death certificate presumably shows the number of years the deceased lived in New York immediately prior to death. Consequently, a person who had moved to New York at age 20, moved away at 50 yr of age, returned at age 55, and died at 65 in New York should have 10 yr recorded as the time he lived in New York before death. It is, of course, possible that 40 or 45 yr would be recorded. Since Puerto Ricans do move back and forth between New York and Puerto Rico, the use of this information as an accurate measure of time in New York is questionable but it gives some idea of length of exposure to the New York environment.
Stomach TABLE 6.
and Colon
Cancer
335
Mortality
AVERAGE NUMBEROF YEARS LIVEDIN NEW YORK CITY BEFOREDEATH FOR PUERTO RICANS
DYING
OF STOMACH
AND COLON
CANCER,
BY AGE AT DEATH,
SEX AND
PERIOD
OF DEATH
Average Years in New York Period
Sex
Age
1360
Males
45-64
18.4
65+
15.0
21.0
45-64
21.8
20.0
65+
10.2
21.8
45-64
18.3
65+
23.1
31.7
45-64
18.7
22.4
24.0
28.3
Females
1970
Males
Females
65+
Stomach Ca.
yrs.
yrs.
Colon Ca.
20.3
31.5
yrs.
yrs.
Table 6 shows that Puerto Ricans dying from colon cancer had been living in New York for 20-30 yr before their deaths. Those who died from stomach cancer had lived in New York for a shorter time before death. This shorter time lived in New York for stomach cancer decedents reflects to some extent the shorter survival rate for stomach cancer than colon cancer, but the data suggest that colon cancer decedents came to New York around 1940, whereas stomach cancer decedents came somewhat later. Whether the period lived in New York is considered long enough for an environmental carcinogen to become operative is open to question. DISCUSSION
In some respects these data for Puerto Rican migrants parallel data for other migrants to the United States. In New York City in 1950 [14] and in the United States as a whole in 1950 and 1960 [l, 2, 41, migrants from many European countries and from Japan died from stomach cancer at rates that were lower than those of nonmigrants but higher than those of native-born whites in the United States. The rates tended to be closer to those in their birthplace ,than to those in the United States. We estimated that Puerto Rican migrants to New York City had rates of stomach cancer about midway between those for nonmigrants and native-born whites in New York. In 1960, colon cancer death rates for many European migrants to the United States were higher than those of nonmigrants and the same as or somewhat higher than native-born whites [4]. Puerto Rican male migrants, however, died from colon cancer at the same rate as did nonmigrants in 1960; in 1965, their rate had nearly doubled but showed little change thereafter. Female migrants’ rates rose only a small amount between 1960 and 1970. This change for men and not for women has also been reported for some Japanese migrants [15]. Both the male and female migrants, however, had rates in 1970 that were only l/2-1/3 those of other whites in New York City. The smaller relative changes that occur among European migrants in stomach cancer compared with changes in colon cancer have been interpreted as showing that stomach cancer is less responsive to current environmental factors than is colon cancer.
356
MARY MONK and M. ELLEN WARSHAUER
Thus, the mortality from stomach cancer remains closer to levels in one’s birthplace and that from colon cancer changes to levels in one’s new residence. These Puerto Rican data seem to show the opposite. By 1960, Puerto Rican migrants had rates of stomach cancer lower than in Puerto Rico while rates of colon cancer were no different from Puerto Rican rates, this despite the fact that migrants dying from stomach cancer had lived in New York for a shorter time than colon cancer decedents. The colon cancer rates for male migrants did increase in 1965 but not in 1970 and were still much lower than for other whites in the latter period. It would appear then that for Puerto Rican migrants stomach cancer is more responsive to recent environmental exposures than is colon cancer. We have considered a number of possible reasons for this unexpected finding. For instance, diagnostic practices and treatment in New York may differ from those in Puerto Rico with the differences being greater for one cancer than the other [16]. Truly comparable data for New York and Puerto Rico about the bases for death certification of the two cancers were not available. Indirect evidence from a variety of sources [6, 11, 13, 171, however, indicates that in the 1960 period there were probably more histologically confirmed cancers in New York than in Puerto Rico and proportionately more for stomach cancer than for colon cancer. Survival rates for both cancers in the United States were about twice those in Puerto Rico in the period 1950-1960 [ 11,173 ; by 1970, survival rates in Puerto Rico were much closer to those in the United States-about 80 per cent of the United States rates [18, 19-j.Thus, while there are differences between New York and Puerto Rico in diagnosis and survival, we do not believe they can completely account for our findings of relatively greater changes at an earlier time for stomach cancer than for colon cancer. We also considered the possibility that the changes in diets of Puerto Rican migrants were different from the changes of other migrants who came to New York. It seems to us that Puerto Ricans were probably no more or less resistant to changing their diet than the earlier European migrants although the relative ease of travel to and from Puerto Rico may have made it easier to continue early dietary patterns. On the other hand, during the late 1940’s and through the 1960’s, some meats and meat products were relatively plentiful and cheap in New York compared to Puerto Rico, and there is no reason to believe that Puerto Rican migrants did not increase their consumption of these foods, thought by some to cause colon cancer. There is also the possibility that Puerto Rican migrants were a selected groupselected in the sense of being at lower risk for stomach cancer than other Puerto Ricans and at a similar risk for colon cancer before they left for New York. Thus, they would have had lower rates of stomach cancer even if they had remained in Puerto Rico. (This, of course, may be true for European migrants as well.) Colon cancer rates would not increase over those of nonmigrants until some factor in the new environment had an opportunity to operate. Studies of Puerto Rican migrants have not, however, revealed any apparent outstanding selective factor in migration [12]. The recency of migration and the young age of the Puerto Rican migrants are probably the most important factors in attempting to explain the rates and trends we found for colon and stomach cancer. Even though many Puerto Ricans have lived in New York for 30 yr or more, the greatest number came here beginning in the late 1940’s. The numbers over 45 yr of age are still quite small and, as mentioned before, the movement back and forth may lessen the effect of any environmental exposure.
Stomach and Colon Cancer Mortality
357
There is also the possibility that Puerto Ricans go back to their homes on the island to retire or die. Perhaps the most reasonable position at this time would be to wait and see what happens to cancer mortality of Puerto Ricans by the 1980’s. These data for 1960 and 1970 indicate that Puerto Ricans may differ from other groups in their response to factors involved in colon and stomach cancer. Careful follow-up of Puerto Rican migrants over time may clarify the relative importance of these factors. SUMMARY
Stomach cancer mortality rates for Puerto Rican migrants to New York City were lower than those for Puerto Ricans in Puerto Rico and higher than for other whites in New York City for the time periods 1958-1962, 1963-1967 and 1968-1971. It is estimated that they were midway between the rates for native-born whites in New York and those for nonmigrant Puerto Ricans. Colon cancer mortality rates for Puerto Rican migrants to New York were about the same as those in Puerto Rico in the 1960 period; in 1965, male rates for migrants rose nearly 90 per cent and remained at that rate in 1970. Female migrant rates rose slightly from 1960 to 1970, while in Puerto Rico rates for colon cancer for both sexes remained about the same. Colon cancer rates for other whites in New York were in all three time periods two to three times higher than those for Puerto Rican migrants. The greater relative change in stomach cancer mortality compared to colon cancer for Puerto Rican migrants is different from the change reported for migrants to the United States from European or Oriental countries. The Puerto Rican data suggest that stomach cancer rather than colon cancer is more responsive to recent environmental exposure. The recency of migration of Puerto Ricans and the small numbers of deaths from these cancers may, however, account for these contradictory findings. REFERENCES 1. 2. 3. 4. 5. 6. I. 8. 9. 10. 11. 12. 13. B
Haenzel W: Cancer mortality among the foreign-born in the United States. J Nat Can Inst 26: 37-132, 1961 Haenzel W, Kurihara M: Studies of Japanese migrants-I. Mortality from cancer and other diseases among Japanese in the United States. J Nat Can Inst 40: 43-68, 1968 Kmet J: The role of migrant population in studies of selected cancer sites: a review. J Chron Dis 23: 305-324, 1970 Lilienfeld AM, Levin ML, Kessler II: Cancer in the United States, Mortality Among the Foreignborn and in Their Countries of Origin. Chapter 7, Cambridge, Mass: Harvard Univ Press, 1972 King H, Haenzel W: Cancer mortality among foreign-born and native-born Chinese in the United States. J Cluon Dls 26: 623-646, 1973 Haenzel W, Dawson E: A note on mortality from cancer of the colon and rectum in the United States. Cancer 18: 265-272, 1965 Burkitt D: Related disease-related cause? Lancet 2: 1229-1231, 1969 Hill MJ, Drasar BS, Aries V, Crowther JS, Hawksworth G, Williams REO: Bacteria and aetiology of cancer of the large bowel. Lancet 1: 95-100, 16 Jan 1971 Drasar BS, Irving D: Environmental factors and cancer of the colon and rectum. Br J Can 27 : 167-172, 1973 Berg J, Howell M, Silverman S: Dietary hypotheses and diet-related research in the etiology of colon cancer. Hlth Serv Reps 88: 915-924, 1973 Martinez E (ed.): Cancer in Puerto Rico: 1950-1964. San Juan, Central Cancer Registry, Division of Cancer Control, Dept of Health, 1967 Sandis EE: Characteristics of Puerto Rican migrants to, and from, the United States. Int Mig Rev 4: 22-42, 1970 Terris M, Hall C: Decline in mortality from gastric cancer in native-born and foreign-born residents of New York City. J Nat Can Inst 31: 155-162, 1963
358 14. 15. 16. 17. 18. 19.
MARY MONK and M. ELLEN WARSHAUER Seidman H: Cancer mortality in New York City for country-of-birth, religious and socioeconomic groups. Envir Res 4: 390429, 1971 Stemmerman GB: Cancer of the colon and rectum discovered at autopsy in Hawaiian Japanese. Cancer 19: 1567-1572, 1966 Doll R: Worldwide distribution of gastrointestinal cancer. Nat Can Inst Monograph 25: 173-190, 1966 Cutler SJ, Ederer F (eds.): Part I. End Results in Cancer. In, End results and mortality trends in cancer. Nat Can Inst Monograph 6: US Dept HEW, 1961 End Results in Cancer, Report No 4. Nat1 Inst Hlth Publ. US Dept HEW, Nat1 Cancer Inst. Bethesda, Md, 1972 Cancer in Puerto Rico, 1970. Dept of Health, Cancer Control Program, San Juan, Puerto Rico
in Great Britain
STOMACH AND COLON CANCER MORTALITY AMONG PUERTO RICANS IN NEW YORK CITY AND PUERTO RICO* MARY MONK and M. ELLEN WARSHAUER
Department
of Community and Preventive Medicine, New York Medical College, Fifth Avenue at 106th Street, New York, New York 10029 (Received in revised.form 18 November 1974)
EPIDEMIOLOGIC studies comparing migrant and nonmigrant populations have multiplied in recent years, the principal reason, of course, being the opportunity to study the relative importance of environmental and constitutional factors [l-6]. In stomach cancer, the evidence indicates that early environmental exposure or constitutional factors may be more important than recent environmental conditions, since mortality rates for migrants tend to be closer to those in their home country than to those in the country to which they moved. In colon cancer, on the other hand, migrants tend to die at rates prevalent in their host rather than in their native country. This finding implies that a recent exposure to a condition or factor in the host country may be important in the development of colon cancer. Indeed, the diet in countries with high colon cancer rates has already been indicted for its role in this disease; studies completed and in progress suggest to many a guilty verdict [7-IO]. A study of Puerto Rican migrants to New York City affords an opportunity to examine changes in stomach cancer mortality, which is higher in Puerto Rico than in New York, and changes in colon cancer mortality, which is lower in Puerto Rico [ Ill. Puerto Ricans in New York are different in a number of respects from migrants from other countries to the United States [12]. First, the vast majority of Puerto Ricans came to New York after World War II, whereas migrants from Europe and the Orient came in largest numbers before 1924. Second, Puerto Ricans frequently travel back and forth between New York and Puerto Rico, staying for unknown lengths of time in one place or the other. Thus, it is not easy to know for how long a Puerto Rican dying in New York may have been exposed to a particular environmental condition. Migrants from other areas tend to have stayed continuously in the United States since their first entry. *This investigation was supported in part by Grant No. 1N 96A from the American Cancer Society and by General Research Support Grant RR-05398 from the General Research Support Branch, Division of Research Resources, National Institutes of Health. 349
MARY MONK and M. ELLENWARSHAUER
350
Despite these unique characteristics of Puerto Ricans in New York, we felt that comparisons among Puerto Ricans in New York, Puerto Ricans in Puerto Rico, and other population groups in New York might add to an understanding of stomach and colon cancer. METHODS
Since the middle 1950’s, the New York City Department of Health has tabulated separately deaths among Puerto Rican-born persons. Since the number of deaths from colon or stomach cancer was quite small until about 1960, we have confined our analysis to deaths in three periods-1958-1962, 1963-1967, and 1968-1971. Deaths from the two cancers were obtained for Puerto Ricans, other whites and nonwhites, by age and sex, for these three periods, and rates were calculated using the 1960 and 1970 census figures and an intercensal estimate. The Cancer Control Division in Puerto Rico kindly sent us the numbers of persons dying from stomach and colon cancer in Puerto Rico for the years 1965-1971. Data for the period before 1965 were ;available in Cancer in Puerto Rico, 1950-1964 [l 11. Population data for Puerto Rico were obtained from the 1960 and 1970 United States censuses and estimated for 1965. On the New York City death certificate, the number of years the deceased person had lived in New York City immediately prior to death is recorded. This information was abstracted for every Puerto Rican who died from colon cancer between 1958 and 1971. Because of the large numbers involved, it was abstracted only in the 3-yr periods around 1960, 1965 and 1970 for those Puerto Ricans dying of stomach cancer. RESULTS
Table 1 shows the population distribution by age of the different groups in 1970. The whites were older than all the other groups, while the Puerto Rican-born in New York had the smallest proportion under 25 yr. Except for whites, all groups had a larger population in 1970 than in 1960. In all groups, the proportion of the population 65 yr TABLE 1. 1970 POPULATION AGE DISTRIBUTION (IN PERCENTAGES) FOR WHITES,NONWHITESAND PUERTORICAN-BORN RESIDENTS OF NEW YORK CITY AND FORRESIDENTS OF PUERTORICO New York Whites
/\sc
Non-Whites
City Puerto
Rican-Born
Puerto
Rico
36.9%
49.6%
32.7%
55.9%
25 - 44
22.6
28.5
43.7
22.6
45 - 54
12.7
IO.1
12.1
a.4
55 - 64
13.0
6.5
7.0
6.6
65 - 74
9.7
3.7
3.1
4.0
75 or
5.'1
1.6
1.4
2.5
100.0%
100.0%
100.0%
24
years
or
more
Total Population
less
100.0
5,605,633
1,815,929
473,300
2,712,033
Stomach
and Colon Cancer Mortality
351
and older increased in the lo-yr period. Table 2 presents the number of deaths from colon and stomach cancer in the three different periods. It should be noted that there were very few colon cancer deaths among Puerto Rican males in New York in the carlicst period. TABLE 2. NCMUER CITY
UE DEATHS PROM STOMACH AND COLON CANCER FOR GIVEN PERIODS IN Ntw YORK AND
PUERTO
RICO
BY SEX, POPULATlON
New Time
Period
White
York
AND TIME PERIOD
City
Non-White Males
GROUP
Puerto - Stomach
Rican-Born
Puerto
Rico
Cancer
1958-62
3,837
528
122
1,373
1563-67
3,062
509
Ill
1,450
1968-71
2,031
411
96
1,108
Females
- Stomach
Cancer
191;8-62
2,449
314
71
663
1963-67
2,030
325
77
683
1968-71
1,351
228
81
544
Males
-
Colon
Cancer
1958-62
4,502
295
I9
180
1963-67
4,710
373
44
200
lY68-71
3,696
342
43
199
Females
-
Colon
Cancer
1958-62
4,569
364
44
225
1963-67
4,516
466
61
280
1968-71
3,627
396
61
249
Table 3 compares the annual age-adjusted rates of the different groups for the three periods. In stomach cancer, the rates have decreased over time by about one-third for all groups except Puerto Rican-born women in New York who showed little change. In the earliest period, it is clear that Puerto Ricans in New York had rates of stomach cancer substantially below those for Puerto Ricans in Puerto Rico and higher than those of other whites in New York. This pattern was maintained in 1970. In comparison with nonwhites, the Puerto Ricans in New York had somewhat lower rates of stomach cancer. In colon cancer, a different picture emerges. Puerto Rican-born men in New York had a 90 per cent increase in colon cancer death rates from the 1960 to 1965 period, whereas all other groups changed relatively little over that time. Between 1965 and 1970, no group showed much change. In 1960, the rates for Puerto Ricans in New York
MARY MONK and M. ELLEN WARSHAUER
352
were much lower than those for other whites and nonwhites and about the same as those for Puerto Ricans in Puerto Rico. By 1970, the New York Puerto Ricans still had much lower rates than other New York residents but somewhat higher rates than island Puerto Ricans.
TABLE 3. AVERAGEANNUAL AGE-ADJUSTED MORTALI~ RATES*(PER 100,000)FORSTOMACH AND COLON CANCERIN NEW YORK Cm AND PUERTORICO BY SEX,POPULATIONGROUPAND TIMEPERIOD
New York City
Time Period
White
Non-White
Puerto Rican-Born
Puerto Rico
Males - Stomach Cancer 1958-62
24.3
36.0
31.2
45.4
1963-67
19.4
27.3
23.0
40.3
1968-71
16.6
23.0
21.0
33.3
Females - Stomach Cancer
1958-62
12.7
17.7
13.2
22.7
1963-67
10.1
13.5
11.6
18.4
1968-71
8.1
11.8
12.8
15.6
Males - Colon Cancer 1958-62
27.6
19.9
4.8
5.9
1963-67
29.7
20.0
9.0
5.5
1968-71
30.1
19.0
9.3
5.9
Females - Colon Cancer 1958-62
23.7
20.3
8.1
7.3
1W-67
22.6
19.2
9.1
7.8
1968-71
21.9
16.1
9.5
7.1
*Indirect adjustment,
New York State rates for 1965 used as standard
It should be noted that the rates for other whites in New York City include both native and foreign-born persons. The proportion of foreign-born approached 25 per cent among persons 45-64 yr and 50 per cent among persons 65 yr and over in New York in 1970. The foreign-born in New York City have higher rates of stomach cancer than native whites [13, 141.Thus, if only native-born whites had been considered in Table 3, the rates for stomach cancer for other whites in New York would have been lower and the difference between Puerto Rican migrants and other whites in New York would have been larger, a difference about the same as the difference between Puerto Ricans in New York and in Puerto Rico. Colon cancer rates were nearly the same in New York City for foreign-born and native-born whites [14].
Stomach and Colon Cancer Mortality
353
Age-specific rates for the two groups of Puerto Ricans and for whites are shown in Tables 4 and 5. (For purposes of clarity, the age-specific rates for nonwhites are not shown in these tables. Changes in age-specific rates for nonwhites over time paralleled the changes for age-adjusted rates.) Most of the rates for Puerto Ricans under 45 yr are based on numbers of less than 20 and in the earliest period, the colon cancer rates for Puerto Rican men at any age are based on numbers less than 10. Statistically significant differences between Puerto Ricans in New York City and in Puerto Rico are noted in these tables. TABLE
4.
AGE-SPECIFICMORTALITYRA~S(PER~~~,~~~)FORSTOMACHCANCER,BYSEXANDPOPULATION GROUP IN THREE TIME PERIODS
Males
Females
25 - 44 Years Time Period
White
PR/NYC
PR/PR
White
lg56-62
2.8
2.5”
4.6
1.9
1963-67
1.9
2.2”
3.7
1.4
1.7 >ft*
3.0
1968-71
1.4
4.oa
2.7
1.1
1.5 hC
1.4*
PR/NYC
-43””
PR/PR
3.7
45 - 64 Years 1958-62
31.9
36.9
64.5+
1411
20.5
27.9
1963-67
24.2
28.4
53.3t
Il.9
15.6
21.3
1968-71
22.3
23.8
43.5+
9.7
13.1
23.ot
65 Years or
More
1958-62
144.0
236.0
271.2
84.3
79.8
13O.b
1W-67
123.7
146.7
252.4+
65.9
65.7
117.y
1968-71
100.3
127.5
210.9+
52.2
go.0
92.5
*Based on 10 to lg deaths **Based on g or fewer deaths tDifference
between Puerto Ricans
in New York and in Puerto Rico is significant
at p - 0.01 or less
Table 4 shows that the general picture for stomach cancer is much the same for the older age groups, 45-64 and 65 yr or more, as for the total group. In the earliest period, stomach cancer rates for Puerto Rican men in New York are lower than those for men in Puerto Rico and higher than for other whites. By 1970, rates for all groups had decreased at about the same rate. For women, there is less consistency; the rates for the oldest group of Puerto Ricans in New York increased from the 1965 to 1970 period as did, to a lesser extent, the rates for Puerto Ricans in Puerto Rico in the 45-64 age group. But in all instances, rates for women in New York were lower than for women in Puerto Rico.
354
MARY
and M.ELLENWARSHAUER
MONK
For colon cancer (Table 5), the rates for Puerto Rican women in New York and in Puerto Rico began at about the same level in 1960 but diverged slightly by 1970 with the New York rates becoming higher. For men, this was true only for the age group 65 yr and older. In 1960, Puerto Rican men in New York aged 45-64 yr had lower rates of colon cancer than did island Puerto Ricans, but by 1970 had higher rates.
TABLE 5. AGE-SPECIFICMORTALITY RATES(PER 100,000)FOR CROUP
IN THREE
TIME
COLON
CANCER,
BY SEX AND
POPULATION
PERIODS
Males
Females
25 - 44 Years -PR/PR
PR/NYC
Time Period
White
1958-62
2.8
, . , 3""
1963-67
2.5
1968-71
2.5
White
Pp./NYC
.5""
3.3
. 855
, .a XJ:
, . 2:‘:
2.4
1.2 :t"
1 6 :>:t
1.7
2.8
-35""
PR/PR
, ,O” 1.4 0.7";:
45 - 64 Years -1958-62
36.8
1963-67
38.7
1968-71
38.1
7.8+
34.9
12.0
10.2
10.6 +
6.5
32.4
12.3
9.9
Il.6 -c
6.7
32.7
14.1
a.7
3.9
!:A
65 y ears or More 1958-62
170.9
35.0 *;t
36.6
138.0
45.9 +
42.8
1963-67
187.5
49.9 *
33.7
135.8
52.6
44.3
1968-71
192.0
54.6 *
35.3
129.7
53.7
46.2
"Based on IO to 19 deaLhs C::Based on y or fewer deaths +Difference
between Puerto Ricans
in New York and in Puerto Rico is significant
et P = 0.05 or less
Table 6 shows the average number of years Puerto Ricans dying in New York had lived in New York. The accuracy of these data is unknown; this item is not coded for routine use by the health department. The death certificate presumably shows the number of years the deceased lived in New York immediately prior to death. Consequently, a person who had moved to New York at age 20, moved away at 50 yr of age, returned at age 55, and died at 65 in New York should have 10 yr recorded as the time he lived in New York before death. It is, of course, possible that 40 or 45 yr would be recorded. Since Puerto Ricans do move back and forth between New York and Puerto Rico, the use of this information as an accurate measure of time in New York is questionable but it gives some idea of length of exposure to the New York environment.
Stomach TABLE 6.
and Colon
Cancer
335
Mortality
AVERAGE NUMBEROF YEARS LIVEDIN NEW YORK CITY BEFOREDEATH FOR PUERTO RICANS
DYING
OF STOMACH
AND COLON
CANCER,
BY AGE AT DEATH,
SEX AND
PERIOD
OF DEATH
Average Years in New York Period
Sex
Age
1360
Males
45-64
18.4
65+
15.0
21.0
45-64
21.8
20.0
65+
10.2
21.8
45-64
18.3
65+
23.1
31.7
45-64
18.7
22.4
24.0
28.3
Females
1970
Males
Females
65+
Stomach Ca.
yrs.
yrs.
Colon Ca.
20.3
31.5
yrs.
yrs.
Table 6 shows that Puerto Ricans dying from colon cancer had been living in New York for 20-30 yr before their deaths. Those who died from stomach cancer had lived in New York for a shorter time before death. This shorter time lived in New York for stomach cancer decedents reflects to some extent the shorter survival rate for stomach cancer than colon cancer, but the data suggest that colon cancer decedents came to New York around 1940, whereas stomach cancer decedents came somewhat later. Whether the period lived in New York is considered long enough for an environmental carcinogen to become operative is open to question. DISCUSSION
In some respects these data for Puerto Rican migrants parallel data for other migrants to the United States. In New York City in 1950 [14] and in the United States as a whole in 1950 and 1960 [l, 2, 41, migrants from many European countries and from Japan died from stomach cancer at rates that were lower than those of nonmigrants but higher than those of native-born whites in the United States. The rates tended to be closer to those in their birthplace ,than to those in the United States. We estimated that Puerto Rican migrants to New York City had rates of stomach cancer about midway between those for nonmigrants and native-born whites in New York. In 1960, colon cancer death rates for many European migrants to the United States were higher than those of nonmigrants and the same as or somewhat higher than native-born whites [4]. Puerto Rican male migrants, however, died from colon cancer at the same rate as did nonmigrants in 1960; in 1965, their rate had nearly doubled but showed little change thereafter. Female migrants’ rates rose only a small amount between 1960 and 1970. This change for men and not for women has also been reported for some Japanese migrants [15]. Both the male and female migrants, however, had rates in 1970 that were only l/2-1/3 those of other whites in New York City. The smaller relative changes that occur among European migrants in stomach cancer compared with changes in colon cancer have been interpreted as showing that stomach cancer is less responsive to current environmental factors than is colon cancer.
356
MARY MONK and M. ELLEN WARSHAUER
Thus, the mortality from stomach cancer remains closer to levels in one’s birthplace and that from colon cancer changes to levels in one’s new residence. These Puerto Rican data seem to show the opposite. By 1960, Puerto Rican migrants had rates of stomach cancer lower than in Puerto Rico while rates of colon cancer were no different from Puerto Rican rates, this despite the fact that migrants dying from stomach cancer had lived in New York for a shorter time than colon cancer decedents. The colon cancer rates for male migrants did increase in 1965 but not in 1970 and were still much lower than for other whites in the latter period. It would appear then that for Puerto Rican migrants stomach cancer is more responsive to recent environmental exposures than is colon cancer. We have considered a number of possible reasons for this unexpected finding. For instance, diagnostic practices and treatment in New York may differ from those in Puerto Rico with the differences being greater for one cancer than the other [16]. Truly comparable data for New York and Puerto Rico about the bases for death certification of the two cancers were not available. Indirect evidence from a variety of sources [6, 11, 13, 171, however, indicates that in the 1960 period there were probably more histologically confirmed cancers in New York than in Puerto Rico and proportionately more for stomach cancer than for colon cancer. Survival rates for both cancers in the United States were about twice those in Puerto Rico in the period 1950-1960 [ 11,173 ; by 1970, survival rates in Puerto Rico were much closer to those in the United States-about 80 per cent of the United States rates [18, 19-j.Thus, while there are differences between New York and Puerto Rico in diagnosis and survival, we do not believe they can completely account for our findings of relatively greater changes at an earlier time for stomach cancer than for colon cancer. We also considered the possibility that the changes in diets of Puerto Rican migrants were different from the changes of other migrants who came to New York. It seems to us that Puerto Ricans were probably no more or less resistant to changing their diet than the earlier European migrants although the relative ease of travel to and from Puerto Rico may have made it easier to continue early dietary patterns. On the other hand, during the late 1940’s and through the 1960’s, some meats and meat products were relatively plentiful and cheap in New York compared to Puerto Rico, and there is no reason to believe that Puerto Rican migrants did not increase their consumption of these foods, thought by some to cause colon cancer. There is also the possibility that Puerto Rican migrants were a selected groupselected in the sense of being at lower risk for stomach cancer than other Puerto Ricans and at a similar risk for colon cancer before they left for New York. Thus, they would have had lower rates of stomach cancer even if they had remained in Puerto Rico. (This, of course, may be true for European migrants as well.) Colon cancer rates would not increase over those of nonmigrants until some factor in the new environment had an opportunity to operate. Studies of Puerto Rican migrants have not, however, revealed any apparent outstanding selective factor in migration [12]. The recency of migration and the young age of the Puerto Rican migrants are probably the most important factors in attempting to explain the rates and trends we found for colon and stomach cancer. Even though many Puerto Ricans have lived in New York for 30 yr or more, the greatest number came here beginning in the late 1940’s. The numbers over 45 yr of age are still quite small and, as mentioned before, the movement back and forth may lessen the effect of any environmental exposure.
Stomach and Colon Cancer Mortality
357
There is also the possibility that Puerto Ricans go back to their homes on the island to retire or die. Perhaps the most reasonable position at this time would be to wait and see what happens to cancer mortality of Puerto Ricans by the 1980’s. These data for 1960 and 1970 indicate that Puerto Ricans may differ from other groups in their response to factors involved in colon and stomach cancer. Careful follow-up of Puerto Rican migrants over time may clarify the relative importance of these factors. SUMMARY
Stomach cancer mortality rates for Puerto Rican migrants to New York City were lower than those for Puerto Ricans in Puerto Rico and higher than for other whites in New York City for the time periods 1958-1962, 1963-1967 and 1968-1971. It is estimated that they were midway between the rates for native-born whites in New York and those for nonmigrant Puerto Ricans. Colon cancer mortality rates for Puerto Rican migrants to New York were about the same as those in Puerto Rico in the 1960 period; in 1965, male rates for migrants rose nearly 90 per cent and remained at that rate in 1970. Female migrant rates rose slightly from 1960 to 1970, while in Puerto Rico rates for colon cancer for both sexes remained about the same. Colon cancer rates for other whites in New York were in all three time periods two to three times higher than those for Puerto Rican migrants. The greater relative change in stomach cancer mortality compared to colon cancer for Puerto Rican migrants is different from the change reported for migrants to the United States from European or Oriental countries. The Puerto Rican data suggest that stomach cancer rather than colon cancer is more responsive to recent environmental exposure. The recency of migration of Puerto Ricans and the small numbers of deaths from these cancers may, however, account for these contradictory findings. REFERENCES 1. 2. 3. 4. 5. 6. I. 8. 9. 10. 11. 12. 13. B
Haenzel W: Cancer mortality among the foreign-born in the United States. J Nat Can Inst 26: 37-132, 1961 Haenzel W, Kurihara M: Studies of Japanese migrants-I. Mortality from cancer and other diseases among Japanese in the United States. J Nat Can Inst 40: 43-68, 1968 Kmet J: The role of migrant population in studies of selected cancer sites: a review. J Chron Dis 23: 305-324, 1970 Lilienfeld AM, Levin ML, Kessler II: Cancer in the United States, Mortality Among the Foreignborn and in Their Countries of Origin. Chapter 7, Cambridge, Mass: Harvard Univ Press, 1972 King H, Haenzel W: Cancer mortality among foreign-born and native-born Chinese in the United States. J Cluon Dls 26: 623-646, 1973 Haenzel W, Dawson E: A note on mortality from cancer of the colon and rectum in the United States. Cancer 18: 265-272, 1965 Burkitt D: Related disease-related cause? Lancet 2: 1229-1231, 1969 Hill MJ, Drasar BS, Aries V, Crowther JS, Hawksworth G, Williams REO: Bacteria and aetiology of cancer of the large bowel. Lancet 1: 95-100, 16 Jan 1971 Drasar BS, Irving D: Environmental factors and cancer of the colon and rectum. Br J Can 27 : 167-172, 1973 Berg J, Howell M, Silverman S: Dietary hypotheses and diet-related research in the etiology of colon cancer. Hlth Serv Reps 88: 915-924, 1973 Martinez E (ed.): Cancer in Puerto Rico: 1950-1964. San Juan, Central Cancer Registry, Division of Cancer Control, Dept of Health, 1967 Sandis EE: Characteristics of Puerto Rican migrants to, and from, the United States. Int Mig Rev 4: 22-42, 1970 Terris M, Hall C: Decline in mortality from gastric cancer in native-born and foreign-born residents of New York City. J Nat Can Inst 31: 155-162, 1963
358 14. 15. 16. 17. 18. 19.
MARY MONK and M. ELLEN WARSHAUER Seidman H: Cancer mortality in New York City for country-of-birth, religious and socioeconomic groups. Envir Res 4: 390429, 1971 Stemmerman GB: Cancer of the colon and rectum discovered at autopsy in Hawaiian Japanese. Cancer 19: 1567-1572, 1966 Doll R: Worldwide distribution of gastrointestinal cancer. Nat Can Inst Monograph 25: 173-190, 1966 Cutler SJ, Ederer F (eds.): Part I. End Results in Cancer. In, End results and mortality trends in cancer. Nat Can Inst Monograph 6: US Dept HEW, 1961 End Results in Cancer, Report No 4. Nat1 Inst Hlth Publ. US Dept HEW, Nat1 Cancer Inst. Bethesda, Md, 1972 Cancer in Puerto Rico, 1970. Dept of Health, Cancer Control Program, San Juan, Puerto Rico
