[CANCER RESEARCH 41,3685-3690,September198110008-5472/81 /0041-0000$02.00

Epidemiological Correlations between Diet and Cancer Frequency1

PelayoCorreaLouisiana State University Medical Center, New Orleans, Louisiana 70112

fats alone were considered (25). Many studies primarily concerned with cancer have also included coronary heart diseasein their analysis because of its well-known correlation withcertain neoplasms (47).

Cancer correlation studies were greatly facilitated by thepioneer work of Segi, who collected and adjusted the cancerdeath rate to its now widely used ‘‘world'â€p̃opulation model(45). Lea (27) in 1967 correlated cancer death rates as adjusted for age by Segi with the availability of foods as provedby the FAQ2 publications. He was impressed by the fact thatneoplasms seem to fall into two groups. Group 1 was positivelycorrelated with the ingestion offat, sugar, animal protein, eggs,and milk. Prominent members of this group were cancers ofthe breast, ovary, large bowel, and prostate. Group 2 wasformed principally by cancers of the stomach and liver andshowed a negative association with such food items.

Wynder et al. (46, 47), while reporting on studies of analyticalepidemiology of colon cancer, concluded that dietary factorsand especially the high intake of fat appeared to be associatedwith the etiology of colon cancer. A positive correlation between death rates of colon cancer and myocardial infarctionwas reported, again pointing toward possibly related dietaryetiologies for both diseases.

Carroll et al. (4) found a positive correlation between breastcancer death rates and the intake of fat and calories. Theywere of the opinion that fat intake was the most relevantparameter.

Gregor et al. (13) correlated food intake with death rates forgastrointestinal cancer in an effort to explain the negativecorrelation between death rates of gastric cancer and coloncancer. They reported that animal protein intake correlatedpositively with the death rate of colon cancer and negativelywith gastric cancer. They corroborated previous findings byDunn and Buell (9), who reached similar conclusions about therole of diet in gastrointestinal cancer while studying time trendsin Japanese imigrants to California.

Hems (20) examined the relationship of dietary intake andbreast cancer in the pre- and postmenopausal periods. Heconcluded that the intake of sugar and fat accounted for threefourths of the intercountry variation in postmenopausal breastcancer, while for premenopausal cancer, genetic factors appeared to have a stronger influence.

Drasar and Irving (8) reexamined some of the mortality dataand added studies of cancer incidence in 37 countries ascorrelated with the FAO dietary intake data. They found nocorrelation of dietary items with gastric cancer but a positivecorrelation between breast cancer and colon cancer rates andtotal fat, animal protein, eggs, and sugar. Correlations withother indicators of affluence were also positive, such as income, the number of automobiles, and television sets. Nocorrelation with fiber intake was found.

Howell (22, 23) examined again the correlation between

2 The abbreviation used is: FAO, Food and Agriculture Organization.

SEPTEMBER1981 3685

Abstract

The literature concerning international correlations betweendietary items and cancer frequency is reviewed. An updatedcorrelation of the most recent data on cancer mortality andfood consumption is made. Strong and consistent correlationsare reported between death rates of cancers of the colon andbreast and the per capita consumption of total fat and ofnutrients derived from animal sources, especially beef, pork,eggs, and milk. Similar but less consistent correlations havebeen reported with cancers of the prostate, ovary, and endometrium. In addition, correlations between precursor lesions ofcoronary heart disease and colon cancer in New Orleansautopsy populations are reported. Some studies suggest thatmilk intake correlates better with atherosclerotic disease whilebeef intake correlates better with colon cancer. Negative correlations of colon cancer rates and vegetable consumption arereported. Colon cancer rates also show negative correlationswith stool weight, irrespective of the type of vegetable responsible for the increased bulk. Epidemiological data are consistent with the hypothesis that excessive beef and low vegetableconsumption are causally related to colon cancer. These fooditems probably do not have a direct carcinogenic role but ratherprovide a microenvironment favorable to the actions of carcinogens.

Introduction

This is an attempt to open a discussion on the subject ofdiet-cancer relationships based mostly on a brief review ofcorrelation studies. In addition, brief mention is made of studiesof the correlation between the precursor lesions of colon cancer and coronary heart disease.

Brief Review of Correlation Studies

The notion that nutrition and cancer might be interrelated isan old one. In modern times, one of its most articulate discussants has been Tannenbaum (41). His most prolific contributions are in the experimental field, but he also did somecorrelation studies, mostly based on the statistics of life insurance companies in which he found a positive associationbetween overweight and several types of cancer. He simulatedthis human situation in numerous animal experiments andestablished firmly that excessive nutrition enhances cancerdevelopment and progression (42).

Intercountry data on dietary intake were utilized on a largescale for correlation studies with coronary heart disease beforesimilar studies were done for neoplastic disease. An initialpositive correlation between coronary heart disease and totalfat intake was later found to be even stronger when saturated

I Presented at the workshop on Fat and Cancer, December 1 0 to 1 2, 1979,

Bethesda, Nd. work supported by Contract NOl -CP-53521 from the NationalCancerlnstitute, USPHS.

on April 24, 2020. © 1981 American Association for Cancer Research. cancerres.aacrjournals.org Downloaded from

P. Correa

colorectal cancer and diet by means of international dietarydata, data of a case-control study conducted by Haenszel (19),and data on food consumption within the United States. Hercorrelation studies were based on incidence and mortality ratesand again showed a positive association of colorectal cancerfrequently with fat and animal protein intakes. In her opinion,correlation studies did not provide an adequate base to consider one dietary component more suspect than the other. Incase-control studies, milk and eggs did not differentiate between cases and controls, and beef stood out as the food itemmost consistently associated with colon cancer. Howell alsoreported a strong negative correlation between rice consumption and the colon cancer rate.

Enstrom (11) failed to find positive correlations between timetrends and socioeconomic class on the one hand and cancerrates on the other. He based his analysis on data for UnitedStates populations which have become homogeneous withrespect to diet and cancer rates.

Armstrong and Doll (1) took advantage of the available newdata on cancer incidence, refined statistical techniques, andindicators of data reliability to critically reexamine the questionof diet-cancer correlations. They found gastric cancer to benegatively correlated with fat consumption; this negative association explained formerly reported associations with proteinconsumption. Meat and animal protein consumption was thevariable most highly correlated with colon cancer. Controllingfor this variable reduced substantially the correlations withother variables, including total fat, whereas no other variablereduced the correlation coefficient with meat to less than 0.70.In the case of cancer of the breast, corpus uteri, and ovary, onthe other hand, total fat intake provided the highest and mostconsistent correlation coefficients. Cereal and “pulses―showed negative association with these 3 endocrine-relatedcancers. Total fat consumption was also found to be positivelycorrelated with cancer of the prostate, testes, kidney, andnervous system, but some of these correlations were weak orinconstant.

Leveille (28) examined the time trends of colon cancer andfood consumption in Connecticut for I 935 to 1965. He foundthe by now well-known correlation with beef consumption andalso called attention to the fact that increases in fat and proteinin the diet are accompanied by other changes, notably by areduction in consumption of cereal and potatoes in the UnitedStates. He found a very strong negative correlation betweencolon cancer and cereals and potato consumption. Correlationsof this type have contributed to the present interest in studyingthe possible role of fiber in preventing colon cancer (26)originally proposed by Burkitt (3), based on observations ofhigh dietary fiber and low colon cancer frequency in Africa.

Hems (21) studied the correlation between diet and deathrates for breast cancer in 41 countries as well as the influenceof childbearing. He found a positive correlation with total fat,animal protein, and animal calories, but, because these 3 itemswere closely correlated with one another, it was not possible toassign an etiological role to one of them independently of theother 2. Differences in childbearing per se contributed little tothe international variation. He also reported a positive correlation between breast cancer rates and heights of women in 29countries. This confirmed previous results of case-control studies in Holland (7), Greece (43), Slovenia (37), and Brazil (33).Since nutrition influences height, this could be an indirect

indication of nutrition, but genetic factors most probably alsohave a strong influence on body height.

Gaskill et al. (14), based on a 1965 to 1966 household foodconsumption survey, analyzed the data for the main regions ofthe United States. They found again the positive association ofbreast cancer rates and milk consumption. In addition, theyfound a previously undetected negative correlation betweenbreast cancer rates and egg consumption. Egg consumptioncould be an indicator of poor socioeconomic status at thepresent time in the United States or could have some unknownbiological significance. The lack of consistency with otherinternational data should caution against assigning a causalrole to such a negative correlation. While consumption of eggshas declined in the United States since 1939, the availability ofother dairy products and meat has increased remarkably (28).This means that eggs are becoming relatively less important asa source of energy, and the negative correlation may be anexpression of the excessive intake of other types of food.

Enig et al. (10) provided a critique of the fat-cancer hypothesis and noted that the increase in fat consumption in the U. S.has been mainly due to an increase in vegetable fat, mostlycontaining trans-double bonds. They suggest that processedvegetable fats should be investigated as possible etiologicalagents. It should be noted that the marked increase in vegetable fat consumption has been taking place without a markedreduction in the consumption of other types of fat. This resultsin an excessive overall fat intake and makes it difficult to assignetiological roles to one particular type of fat to the exclusion ofthe other.

Liu et al. (29) based their correlation analysis on estimatesof the contents of cholesterol, fatty acids, and fiber on theitems reported in the food consumption tables of FAO. Theyfound that the correlation of colon cancer rates with cholesterolintake remained significant when adjustments were made forfiber and other fats; adjusting for cholesterol, on the otherhand, decreased most of the other correlations to nonsignificant levels.

The Role of Fiber

Several investigators have noted a negative correlation between fat and fiber intake. Simultaneously with an increase infat Consumption, there has been a decrease in the consumptionof fruits and vegetables in the United States (28). This trend isgenerally observed as the level of affluence of the populationunder study increases. Direct correlations of cancer rates withdietary fiber have not been consistently found (8). However,the calculation of ‘‘fiber'‘component of diet, based on international data, is far from satisfactory. It is well known that thereis a great variation in the type of vegetables consumed indifferent countries, and their content of fiber is either unknownor inaccurately estimated. While the definition fiber is stillcontroversial and the characterization of different types of fiberis under investigation, it remains true that populations with lowcolon cancer rates have bulkier diets than do those with highrates. Two independent studies in Hawaii (15) and Scandinavia(24) have shown that the daily stool weight is greater in lowrisk populations. This strengthens the observation made byLeveille that changing the energy intake from vegetable toanimal sources is a characteristic of populations at high riskfor cancer of certain organs, especially breast and colon. This

CANCERRESEARCHVOL. 413686

on April 24, 2020. © 1981 American Association for Cancer Research. cancerres.aacrjournals.org Downloaded from

GrossnationalproductwheatRiceMaizeBeansCattle meatPorkEggsMilkAnimal

oil andfatBeerAnimal

cabriesPro teinsFatFemaleheightColon0.67—0.34—0.67—0.680.540.600.750.480.640.620.840.490740.56Breast(female)0.660.34—0.50—0.66—0.700.580.620.750.550.640.560.840.480.750.63Prostate0.64—0.58—0.53—0.660.470.480.480.520.510.440.760.520.720.58AtherOsclerOtIC0.52—0.400.480.590.480.740.510.73heart

diseaseHeight0.70—0.42—0.660.710.640.480.580.470.690.61

Diet and Cancer

disease (0.41 ); prostate and arteriosclerotic heart disease(0.46).

Our findings confirmed what previous investigators havepointed out; diseases which have a better correlation withdietary data are cancers of the intestine, breast, and prostateand arteriosclerotic heart disease. Their correlations with totalfat intake and with sources of animal protein and fat, wellshown in Table 1, have also been extensively discussed byprevious investigators. The same diseases correlate well withthe physical quality of life index and with the gross nationalproduct, indicating that they are diseases of affluence. Affluence seems to bring with it dietary changes which result in anexcessive consumption of animal proteins. Leveille has calculated that the excess protein intake in the United States is morethan double the recommended dietary allowances (28).

Table 1 emphasizes the negative correlations of the diseasesunder study with the consumption of rice, corn, and beans,which may suggest a protective role for these food items. Asstated previously, the excessive intake of animal protein (mostlymeat) in affluent societies takes place simultaneously with adecrease in the consumption of vegetables (28). This makes itpossible at the present time to determine if the ‘‘protective―effect of rice, corn, and beans is by direct action or if it ismerely a sign of the damage caused by excessive meat. Thequestion may never be resolved, but its resolution becomessomewhat academic when one thinks that, in the past, dietarychanges in human populations simultaneously have reducedstarchy foods and increased meat consumption. This mayindicate that disease prevention could be accomplished byreversing both trends simultaneously. The role of starchy vegetables may be to satisfy the appetite and, therefore, limit theexcessive meat intake. Most habits are not suppressed butrather replaced.

Table 1 also shows a positive correlation between bodyheight and cancer of the colon, breast, and prostate. This hasbeen well described previously for breast cancer (7). Table 1also shows height to be correlated with affluence and withsources of animal protein and fat as well as negatively correlated with the consumption of rice and corn. It would bereasonable to assume that a reduction in protein intake and anincrease in the consumption of starchy vegetables might in thelong run affectthe average height of the population, a probablyvery unpopular result. On the other hand, it is hard to believethat an unlimited excess of protein consumption will result inunlimited increases in the height of the individuals in the community. The ideal situation should supply adequate energysources to satisfy the growing needs of the body and less thanexcessive nutrition after full growth has been achieved. Thisshould be a high priority challenge for our society atthe presenttime.

is well illustrated by a recent dietary survey conducted byFajardo (12) in rural areas of Colombia with very low incidenceof breast and colon cancer; in a typical village (Guaitanlla),82.5% of the calories and 76.4% of the protein came fromvegetablesources.

UpdatedCorrelations

In order to take a closer look at the role of vegetables incancer risk, we calculated single (Pearson) and rank (Spearman) correlation coefficients for disease rates (38, 39) ascompared to dietary information(l 3). The most recent availablecancer rates as age-adjusted by Segi were utilized for 1973and matched with diet data as published by FAO for the yearsof I 964 to 1966. This allows an 8- to 9-year lapse betweendietary data and cancer rates to partially accommodate thewell-known latency period needed for the development of neo

t plastic processes. In a total of 41 countries, mortality data anddetailed information for most dietary items were available. Theonly exception was the data on beans which appeared as aseparate item in only 15 of the countries under study. Datawere available from Mauritius, Canada, Costa Rica, Cuba,Dominican Republic, El Salvador, Mexico, Nicaragua, UnitedStates, Uruguay, Venezuela, Hong Kong, Israel, Japan, Singapore, Austria, Belgium, Bulgaria, Czechoslovakia, Denmark,Finland, France, West Germany, Greece, Hungary, Iceland,Ireland, Italy, Luxembourg, The Netherlands, Norway, Poland,Portugal, Rumania, Spain, Sweden, Switzerland, England, Yugoslavia, Australia, and New Zealand.

Correlation coefficients were calculated for males for cancers of the oral cavity, esophagus,stomach, intestines,andprostate (1973). Rates for breast and cervix were calculatedfor females. Additionally, rates for tuberculosis, infectious andparasitic diseases, and arteriosclerotic heart diseases werecalculated for males (1960 to 1961 ). Since body size is relatedIn part to nutrition, correlations were calculated with bodyheight. The latter data were available only for women in 27 ofthe countries under study (32).

Table I shows the correlation coefficients that were significant at the 0.05 level. No significant correlations were foundfor cancer of the oral cavity, esophagus, stomach, or cervix;for tuberculosis; or for infectious diseases. The only exceptionwasaweak(0.42)correlationbetweenesophagealcancerandrice consumption.Therewerealsosignificantcorrelationsbetweenthe followingdiseasesand cancersites:oral cavityandesophagus (0.78); stomach and arteriosclerotic heart disease(—0.47); Intestine and breast (0.90); intestine and prostate(0.73); intestine and arteriosclerotic heart disease (0.48);breast and prostate (0.77); breast and arteriosclerotic heart

Table 1Significant(p < 0.05) Pearson s correlation coefficients

Age-adjusted mortality rates (38) are correlated with per capita consumption of dietary item (13) and height.

SEPTEMBER1981 3687

on April 24, 2020. © 1981 American Association for Cancer Research. cancerres.aacrjournals.org Downloaded from

Disease death rates and consumption of milk andmeatDaily

intake (g)Truncated (35—64yr) de(per 100,000)ath

ratesAthero

scleroticheartdis-ColonBreastMilk

MeateasecancercancerArgentina207

2001 70 1550Finland87856385 639

Whites Blacks Whites Blacks

Low1915Medium34282.22.2High36352.43.0

P. Correa

The Milk versus Meat Controversy

Since milk, beef, pork, and eggs are the prominent sourcesof animal protein and fat in most wealthy societies, specialattention should be given to these items. Table 1 shows positivecorrelations of all of these items with the diseases underconsideration. The correlation coefficient between arteriosclerotic heart disease and egg consumption in our tabulations wasweakly positive (0.35) and not significant (p = 0.08). It shouldbe noted, however, that the recent drop in coronary heartdisease death rates in the United States has followed a decrease in the consumption of eggs and an increase in theconsumption of vegetable fat, and the possible causal linkagebetween the 2 events should be considered. The fact thatcancer rates have not dropped simultaneously with heart disease may indicate differences in either the pathogenesis or theetiology which should be investigated further. Most countrieshave similar patterns of consumption of animal fat and meat,and this accounts for the positive correlations with both items,which are practically impossible to separate in tabulations ofdata from all countries. A few countries have definite preferences for their source of animal protein, and this providessome opportunity for limited discriminatory analysis (2). Onesuch contrasting pattern is provided by Argentina and Finland,as shown in Table 2, which shows data on daily (1964 to 1966)per capita consumption of milk and meat (3) as well as thetruncated (ages 35 to 64 years) annual death rates (Finland,1960 to 1961 ; Argentina, 1962 to 1964) for coronary diseaseand cancer of the colon and breast (36, 39, 40). The high milkintake of the Finns is better reflected in their high heart diseaserates, while the high beef intake of the Argentinians is betterreflected in their high colon cancer rate. The rates of breastcancer, however, are high in both countries, probably indicating that either source of animal protein and fat may influenceits development. A similar situation seems to exist for prostaticcarcinoma; truncated rates for ages 35 to 74 years are 24.7for Argentina and 17.7 for Finland.

Correlations between Precursor Lesions

Colon cancer and coronary heart disease are the end pointsof prolonged, seemingly independent pathological processes.Stages previous to the final result can be identified and quantified in autopsy populations following methodology describedpreviously (5—31). We have estimated the area of the aortainvolved by atherosclerosis as well as the prevalence of colonicpolyps in 847 autopsies in New Orleans. Table 3 gives theprevalence of adenomatous polyps in males for categories ofatherosclerotic involvementofthe aorta. These categories weredefined for each age group according to previous investigations(31), and the ones represented in Table 3 represent a summaryfor all ages.

In New Orleans men, greater involvement with atherosclerosis is associated with higher polyp prevalence. This indicatesthat, in these populations, the factors responsible for bothlesions are either the same or similar in distribution. Givenpreviously discussed dietary associations, the latter explanation is favored, namely, that both dairy products and beef areexcessively consumed by New Orleans populations (35). It issuggested that applying these techniques to populations withcontrasting dietary habits, such as Argentina and Finland,

Table 2

Table 3Prevalence of adenomatous polyps according to atherosclerosis category

Prevalence of polyps (%) Relative riskDegree of aortic

involvement

might throw additional light on the subject. From their recentwork on atherosclerosis, Strong and collaborators have reported that, in the last 15 years, there has been a decrease inthe involvement of the aorta and coronary arteries by atherosclerosis. This correlates well with the decline in coronary heartdisease death rates that has been observed in the country. Nosimilar decrease has been observed in colon cancer deathrates or in the prevalence of colonic polyps. This suggests thatdietary changes may be taking place which tend to lowercoronary heart disease rates but do not affect colon cancerrates.

Case-Control Studies

A thorough discussion of the results of case-control studieswill not be attempted. They have been summarized recently(17, 44). Several of them, conducted in populations at high riskto colon cancer, have not found an association with meat orother suspect dietary items (17). This does not negate the roleof animal proteins and fat, because there is, in effect, anovermatching due to the fact that most members in our community eat excessive amounts of beef. It should also be remembered that at least 50% of people in the United States over 60years of age, when colon cancer is more frequent, carryadenomatous polyps in their colon. This means that at leastone-half of the controls will be carriers of a lesion which isconsidered a precursor of colon cancer. This may explain why,in populations with more variability in meat intake, positiveassociations between colon cancer and beef are found (19).

It should also be kept in mind that dietary items probably arenot direct carcinogens but rather are promoters of the actionof a carcinogen. Our epidemiology techniques take into account only the final product. In the absence of an initiator, nodegree of promotion will lead to cancer. In such circumstances,case-control studies may give contradictory results.

At least 2 case-control studies have shown an inverse association of colon cancer rates and fiber in the diet (16, 34).This has led to the very interesting speculations about the roleof certain indole-containing cruciferous plants in the inductionof presumably protective enzymes in the tissues (17). Population data suggest that greater stool bulk correlates negativelywith colon cancer rates, irrespective of the type of vegetableresponsible for the greater bulk (15, 24).

CANCERRESEARCHVOL. 413688

on April 24, 2020. © 1981 American Association for Cancer Research. cancerres.aacrjournals.org Downloaded from

Diet and Cancer

in two populations experiencing similar colon cancer risks. Lancet, 2: 80—81, 1974.

16. Graham, S., Dayal, H., Swanson, M., Mittelman, A., and Wilkinson, G. Dietin the epidemiology of cancer of the colon and rectum. J. Nati. Cancer Inst.,61: 709-714, 1978.

17. Graham, S., and Mettlin, C. Diet and colon cancer. Am. J. Epidemiol., 109:1-19, 1979.

18. Gregor, 0., Toman, R., and Frusona, F. Gastrointestinalcancerand nutrition.Gut, 10: 1031-1034, 1969.

19. Haenszel, W., Berg, J. W., Segi, M., Kurihara, M., and Locke, F. B. Largebowel cancer in Hawaiian Japanese. J. NatI. Cancer Inst., 51: 1765—1779,1973.

20. Hems, G. Epidemiologicalcharacteristicsof breast cancer in middle and lateage. Br. J. Cancer, 24: 226—234,1970.

21. Hems, G. The contribution of diet and childbearing to breast cancer rates.Br. J. Cancer, 37: 974—982,1978.

22. Howell, M. A. Factor analysis of international cancer mortality data and percapita food consumption. Br. J. Cancer, 29: 328—336,1974.

23. Howell, M. A. Diet as an etiological factor in the development of cancer ofthe colon and rectum. J. Chronic Dis., 28: 67—80,1975.

24. International Agency for Research on Cancer. Dietary fibre, transit time,fecal bacteria, steroids and colon cancer in 2 Scandinavian populations.Lancet, 2: 207—211, 1977.

25. Jolliffe, N., and Archer, M. Statisticalassociation between international heartdisease death rates and certain environmental factors. J. Chronic Dis., 9:636-652, 1959.

26. Kritchevsky, D., and Story, J. Dietary fiber and cancer. Curr. Concepts Nutr.,6: 41-54, 1977.

27. Lea, A. J. Neoplasms and environmental factors. Ann. R. Coil. Surg. EngI.,41: 432-438, 1967.

28. LevellIe, G. A. Issues in human nutrition and their probable impact on foodsof animal origin. J. Anim. Sci., 4 1: 723—731, 1975.

29. Liu, K., Stamler, J., Moss, D., Garside, 0. , Persky, V., and Soltero, I. Dietarycholesterol, fat and fibre, and colon cancer mortality. Lancet, 2: 782—785,1979.

30. MacMahon, B., Cole, P., Liu, T. M., Lowe, C. A., Mirra, A. P., Ravnihar, B.,Salber, E. J., Valaores, V. G., and Yuasa, S. Age at first birth and breastcancer risk. Bull. W. H. 0., 43: 209, 1970.

31 . McGill, H. C. The geographic pathology of atherosclerosis. Lab. Invest., 18:465—467,1968.

32. Meredith, H. V. Worldwide somatic comparisons among contemporary human groups of adult females. Am. J. Phys. Anthropol., 34: 89—132, 1971.

33. Mirra, A. P., Cole, P., and MacMahon, B. Breast cancer in an area of highparity: SãoPaulo, Brazil. Cancer Res., 31: 77—83,1971.

34. Modan, B., Barrell, V., Lubin, F., Modan, M., Greenberg, R. A., and Graham,S. Low fiber as an etiologic factor in cancer of the colon. J. NatI. CancerInst., 55: 15—18,1975.

35. Moore, M., Guzmán,M., Schilling, P., and Strong, J. P. Dietary-atherosclerosis study of deceased persons. J. Am. Diet. Assoc. , 70: 602—606,1977.

36. Puffer, R., and Griffith, W. Patterns of urban mortality. Washington, D.C.:Pan American Health Organization, 1967.

37. Ravnihar, B., MacMahon, B., and Lindtner, J. Epidemiologic features ofbreast cancer in Slovenia. Eur. J. Cancer, 7: 295—306,1971.

38. Segi, M., Age-adjusted Death Rates for Cancer for Selected Sites in 52Countries in 1973. Nagoya, Japan: Segi Institute of Cancer Epidemiology.

39. Segi, M., and Kurihara, M. Cancer Mortality for Selected Sites in 24Countries (1962—1963). Sendai, Japan: Tohoku University, 1966.

40. Segi, M., Kurihara, M., and Tsukahara, V. Mortality for Selected Causes in30 Countries(1 950—1961).Sendai, Japan: Tohoku University, 1966.

41 . Tannenbaum, A. Relationship of body weight to cancer incidence. Arch.Pathol., 30: 509-51 7, 1940.

42. Tannenbaum, A., and Silverstone, H. Nutrition and the genesis of tumors. In:A. W. Raven (ed), Cancer, Vol. 1, pp. 306-334. London: Butterworth &Co., Ltd., 1957.

43. United States Department of Agriculture Research Service. Household FoodConsumption Survey, 1965—1966,Report 18. Washington, D. C.: UnitedStates Government Printing Office, 1974.

44. Valaoras, V. G., MacMahon, B., Trichopoulus, 0., and Polychronopoulus,A.Lactation and reproductive histories of breast cancer patients in GreaterAthens. Int. J. Cancer, 4: 350—363,1969.

45. Waterhouse, J., Muir, C., Correa, P., and Powell, J. Cancer Incidence inFive Continents, Vol. 3, Publication 15. Lyon, France: International Agencyfor Research on Cancer, 1976.

46. Wynder, E. L., Kajitani, T., Dodo, H., and Takano, A. Environmental factorsof cancer of the colon and rectum. II. Japanese epidemiologic data. Cancer(Phila.), 23: 1210—1220,1970.

47. Wynder, E. L., and Shigematsu, T. Environmental factors of cancer of thecolon and rectum. Cancer(Phila.), 20: 1520—1561,1967.

3689

This brief review suggests that the best hypothesis availablefor testing today is that colon cancer is related to consumptionof excessive animal fat and protein, especially beef, and insufficient consumption of vegetables to increase food bulk. Sincechanges to reverse these trends in adults do not appear to behazardous, intervention trials should be considered seriously.The biggest difficulty is with the end point for evaluation of theresults, but recent progress in endoscopic techniques andmutagenesis assays offers alternatives to cancer as an endpoint.

Conclusions

I would like to propose that: (a) total fat and animal proteinstrongly correlate internationally with arteriosclerotic heart disease, colon cancer, and breast cancer; (b) similar but lessconsistent correlations are found with cancer of the ovary,endometrium, and prostate; (c) fat versus protein-independenteffects are difficult to discriminate in interpopulation correlations; (d) the available data suggest that fat correlates betterwith arteriosclerotic heart disease, and meat correlates betterwith colon cancer; (e) the fiber issue has not been resolved byinterpopulation correlation studies, but greater food bulk showsa good inverse correlation with colon cancer rates; ( f) meatconsumption appears to be excessive in the United Stateswhen compared to other countries and when compared tonutritional requirements; and ( g) high meat and low bulk appeared together in United States diets. They probably shouldbe reduced together in attempts to prevent the disease andreverse the trends of high cancer rates.

References

1. Armsfrong, B., and Doll, R. Environmental factors and cancer incidence indlfferentcountries, with specialreferenceto dietary practices. nt. J. Cancer,15:617—631,1975.

2. Berg, J. W., Haenszel, W., and Devesa, S. S. Epidemiology of gastrointestinal cancer. In: Proceedings. National Cancer Conference, Ed. 7, p. 459.Philadelphia: Lippincott Co., 1973.

3. Burkitt, 0. P. EpIdemiology of cancer of the colon and rectum. Cancer(Phila.), 28: 3-1 3, 1971.

4. Carroll, K. K., Gammel, E. B., and Plunkett, E. A. Dietary fat and mammarycancer. Can. Med. Assoc. J., 23: 590-594, 1968.

5. Correa, P., Duque, E., Cuello, C., and Haenszel, W. Polyps of the colon andrectum In Call, Colombia. nt. J. Cancer, 9: 86—96,1972.

6. Correa, P., Strong, J. P., Reif, A., and Johnson, W. The epidemiology ofcolorectal polyps. Cancer (Phila.), 39: 2258—2264,1977.

7. DeWaard, F. Breast cancer incidence and nutritional status with particularreference to body weight and height. Cancer Res., 35: 3351 —3356,1975.

8. Drasar, B. S., and Irving, D. Environmental factors and cancer of the colonand breast. Br. J. Cancer, 27: 167—172,1975.

9. Dunn, J. E., and Buell, P. Gastrointestinal cancer among ethnic groups inCalifornia. In: Proceedings of the Third World Congress of Gastroenterology,Tokyo, Japan, 1966.

10. EnIg, M. G., Munn, R. J., and Keeney, M. Dietary fat and cancer trends: acritique. Fed. Proc., 37: 2215—2220,1978.

11. Enstrom, J. E. Colorectal cancer and consumption of beef and fat. Br. J.Cancer,32:432—439,1975.

12. Fajardo, L. Colombia Dietary Surveys. Call, Colombia: Universidad del Valle,1979.

13. Food and Agriculture Organization. Food Balance Sheets 1964—1966.Rome, Italy: Food and Agriculture Organization, 1971.

14. GaskiII, S. P., McGulre, W. L., Osborne, C. K., and Stern, M. Breast cancermortality and diet In the United States. Cancer Res., 39: 3628-3637, 1979.

15. Glober, G. A., Klein, K. L., Moore, J. 0., and Abba, B. C. Bowel transit times

SEPTEMBER1981

on April 24, 2020. © 1981 American Association for Cancer Research. cancerres.aacrjournals.org Downloaded from

1981;41:3685-3689. Cancer Res   Pelayo Correa  FrequencyEpidemiological Correlations between Diet and Cancer

  Updated version

  http://cancerres.aacrjournals.org/content/41/9_Part_2/3685

Access the most recent version of this article at:

   

   

   

  E-mail alerts related to this article or journal.Sign up to receive free email-alerts

  Subscriptions

Reprints and

  .pubs@aacr.orgDepartment at

To order reprints of this article or to subscribe to the journal, contact the AACR Publications

  Permissions

  Rightslink site. Click on "Request Permissions" which will take you to the Copyright Clearance Center's (CCC)

.http://cancerres.aacrjournals.org/content/41/9_Part_2/3685To request permission to re-use all or part of this article, use this link

on April 24, 2020. © 1981 American Association for Cancer Research. cancerres.aacrjournals.org Downloaded from