The Low Incidence of Colorectal Cancer

in a ‘High-Risk” Population:
Its Correlation with Dietary Habits

PAUL ROZEN, MD, SHLOMO M. HELLERSTEIN, MD, AND CRYSTAL HORWITZ,’ PHD

In Israel, the incidence of colorectal cancer is highest in European-American-born Jews, although this
incidence is lower than that found in European-born Jews living in the United States. A significantly
lower-than-expected incidence was found in a specific kibbutz established by immigrants of European
origin. Matched population samples from this kibbutz and the city of Tel Aviv revealed significant
differences in dietary habits. The kibbutz members ate more unavailable carbohydrate and ascorbic acid
and had a higher dietary polyunsaturated to saturated fat (P/S)ratio than the city dwellers. Both groups
ate more crude fiber, less saturated fat, and less beef than has been reported from America and European
countries. This kibbutz diet seems to have prevented large bowel cancer, parallels the “prudent” diet
of Wynder, and possibly indicates the feasibility of colorectal cancer prevention.
Cancer 482692-2695, 1981.

T HE HIGH A N D , I N SOME CASES, rising incidence of

colorectal cancer in many countries having a west-
ern European-American lifestyle has led to a concerted
search for its possible causes. I n addition to genetic
influences, in most cases it is believed that environ-
mental factors, especially dietary, play a dominant
role.’.* Most of these studies, as to be expected, have
been retrospective and have pointed out the possible
roles of ch~lesterol,~ fat,4 meat,’ fiber,6 and vitamins’
as causative or protective agents. However, few inves-
tigators in this field have proposed preventive dietary
recommendation^.^*^.^
Within a program for the early detection of large
bowel tumors, we have deliberately sought populations
assumed to be at high risk because of their demographic
or epidemiologic characteristics.”*” One such group is
the European or American-born immigrant to Israel
who has approximately 2% times the risk of developing
From the Departments of Gastroenterology and *Dietetics, Mu-
nicipal-Governmental Medical Center, Ichilov Hospital and the Tel
Aviv University Sackler School of Medicine, Tel Aviv, Israel.
Supported by the Israel Cancer Fund (Canada) and the Israel Can-
cer Association.
Address for reprints: P. Rozen, MD, Ichilov Hospital, Weizmann
Street, Tel Aviv, Israel.
The authors thank the members, medical staff and Head Nurse,
Hava Givoni, of Kibbutz Givat Brenner for their cooperation; N.
Levin of the Ministry of Health, Jerusalem and M. Modan of the C.
Sheba Medical Center for their assistance in analyzing the data; Dr.
D. Schottenfeld, New York, for reviewing the manuscript. The dietary
data on the Tel Aviv residents are part of a larger unpublished survey
by Drs. Gilat and Horwitz on dietary factors in gallstone disease.
Accepted for publication November 8, 1980.
this malignancy compared with those coming from Asia
or Africa.I2 Tel Aviv has a high incidence of colorectal
cancer because of its large proportion of elderly im-
migrants from Europe or America.” However, when
we extended the screening program (to be reported else-
where) to a nearby kibbutz (communal farm) composed
of a similar population, we were surprised by its low
incidence of colorectal cancer. It became apparent, that
for the last 20 years, the kibbutz members have kept
to a low-animal-fat, high-residue diet in an attempt to
prevent arteriosclerotic heart disease. This provided a
unique opportunity to compare the dietary habits and
colorectal cancer rates in these two populations.
Patients and Methods
The kibbutz is situated on the coastal plain, a 20-
minute drive from Tel Aviv. It was founded 51 years
ago, mainly by Eastern European and German-born
immigrants. The population ( 1600 residents, including
990 full members) has remained stable for the last 20
years. They have a mixed economy based on agricul-
ture, light industry, and tourism. Their standard of liv-
ing is comparable to that of an urban middle-class fam-
ily, as determined by on-site inspection and comparison
of their per capita income with national figures.
Large Bowel Cancer Rate
In the kibbutz population, the large bowel cancer rate
was ascertained by reviewing the medical records at the

0008-543)3/81/ I21 5/2692 $0.70 0 American Cancer Society

2692
No. 12 COLORECTAL
CANCERAND DIETARYHABITS . Rozen et al. 2693

TABLEI . Characteristics of the Tel Aviv and Kibbutz by the National Water Carrier; its contents are uniform
Population Samples
throughout central Israel.
Tel Aviv Kibbutz The dietary habits of 88 Tel Aviv residents, matched
~~~ ~

as closely as possible to the kibbutz group by age, sex,

Number 88 75
Males %! 48.9 46.7
social level, years in Israel, and country of birth, were
Age (years) (mean f SD) 55.8 f 10.7 58.3 f 10.4 ascertained by the same team of dieticians using the
Years in Israel same interview technique. They were chosen at random
(mean f SD) 36.3 f 14.4 40.2 t 9.5
Years in Kibbutz
from the hospital staff and outpatients, excluding those
(mean f S D ) - 36.8 f 10.2 with chronic gastrointestinal disorders or those keeping
European or American to any special diet. To prevent any bias by the inter-
origin, 95 I00 86.3
Weight, kg (mean f SD) 70.6 f 11.9 66.1 k 10.3 viewer~,’~ they were told that the project concerned
Height (cm) (mean f S D ) 165.3 ? 7.3 162.8 i 7.5 gallbladder disease.

Data Analysis
on-site clinic and adjacent hospital. The expected num-
ber of colorectal cancer cases was calculated according The dietary constituents were evaluated by a com-
to the mean age, sex, and ethnic-specific incidence rates puter program using local and international tables for
in Israel for the period 1967-1974.’* food values.I6-’* The accuracy of this technique was
confirmed by hand calculation of random individual
samples. Statistical tests used included the chi-square
Dietary Habits
test with the “Yates’ correction,” and the separate vari-
The diet of 75 kibbutz members was ascertained by ance estimate t test. Statistical comparison of the ob-
personal interview. A dietician trained in performing served number of colorectal cancer patients to the ex-
field-surveys reviewed the food intake, habits, and idio- pected number was based on Poisson 95% confidence
syncrasies of this group by the frequency questionnaire limits.
method.I3 Every tenth member appearing on an alpha-
betical list of adults over the age of 40 years was in- Results
terviewed. It should be noted that there is a central
kitchen and dining hall where the members eat standard During the last 20 years, only two cases of colorectal
fare. Eating light meals in the living quarters is also cancer has occurred among the kibbutz members. The
possible, and this was taken into account. The daily per number of cases expected during the same period, had
capita consumption of foodstuffs of the kibbutz mem- the incidence resembled that of the total Israeli popu-
bers was also calculated by using their central pur- lation of European-American origin adjusted for age
chasing records for the years 1972- 1973, 1978- I979. and sex, was 6.5. The observed number of cases, 2, was
This allowed us to detect changes in dietary habits, to significantly lower than the expected, P = 0.04.
confirm the results of the dietary survey, and to compare The characteristics of the two compared populations,
them with national figures.I4Drinking water is provided kibbutz members and Tel Aviv controls, are given in
Table 1. There are no significant differences between
the two groups. The Tel Aviv controls were heavier than
TABLE
2. Daily Per Capita Intake of Nutrients Where No the kibbutz members but also taller, and thus the rel-
Significant Differences were Found*
ative body weight (RBW) was the same.
Tel Aviv Kibbutz The dietary survey results are summarized in Tables
2 and 3. no significant differences were found between
Energy, cals 21 18.2 f 554.7 2209 t 1022.9
Total fat (8) 89.8 ? 31 93.8 t 44.8 the two sample groups in daily caloric, total fat, avail-
Monounsaturated able carbohydrate, tryptophan, sodium, cholesterol, and
fatty acids (g) 31.8 f 12.5 32 t 12 monosaturated fatty acid intake. The Tel Aviv residents
Cholesterol (mg) 415.3 f 206.1 433.9 +- 240.8
Carbohydrate (g) ate more protein, and their nicotinamide intake was
(available) 232.1 f 75 254.3 f 155.8 larger, in both cases P = 0.05. The source of calories
Protein (g) 91.9 t 20.4 84.6 ? 24.7 for the Tel Aviv residents was from protein 1890, fat
N icotinamide
(mg) 20.8 f 7.6 18.6 2 5.2 38% and carbohydrates 44%. The equivalent values for
Tryptophan (mg) 1043.5 f 236.5 1004.3 t 309 the kibbutz group were 16%, 38%, and 4690, respec-
Sodium ( m g ) t 2517.8 f 2505.1 2700.3 rt 2292.6 tively.
* Values expressed as mean rt SD. More poultry than beef was eaten by both the kibbutz
t Excluding added salt. members and the Tel Aviv residents and also by the
2694 CANCERDecember 15 1981 Vol. 48

3.
TABLE Daily Per Capita Intake of Nutrients Where Significant Differences were Found*

Tel Aviv Kibbutz Significance

Carbohydrate (g)
(unavailable) 6.8 * 2.9 9.6 1- 4.0 P < 0.01
Saturated fat (g) 32.4 1- 13.3 27.7 rt 13.4 P < 0.05
Polyunsaturated fat (8) 19.6 rt 9.9 26.0 ? 11.4 P < 0.01
P / S ratio 0.7 rt 0.4 1.0 rt 0.4 P < 0.01
Ascorbic acid (mg) 93.5 k 52.6 214.2 1- 114.2 P < 0.01
Carotene ( p g ) 1334.3 * 819.7 1980.8 * 895.9 P < 0.01
Retinol ( p g ) 538.5 rt 258.4 333.4 rt 186.0 P < 0.01
Thiamine (mg) 0.79 1- 0.19 1.22 1- 0.44 P < 0.01
RiboRavin (mg) 1.371- 0.42 1.65 1- 0.6 P < 0.01
Iron (mg) 11.9 & 3.2 15.1 ? 4.6 P < 0.01
Potassium (mg) 2320.7 f 616.6 3453.7 rt 964.2 P < 0.01
Magnesium (mg) 207.0 f 65.1 262.8 1- 93.5 P < 0.01
Calcium (mg) 707.8 +_ 341.0 862.1 f 382.0 P = 0.01
* Values expressed as mean f SD.

nation. The survey showed that the mean daily con- analyzed. 197920-24In most cases, conclusions were drawn
sumption of cooked poultry was 53 g, beef 41 g, and from experimental ~ t u d i e s ~epidemiologic
.~, studies of
fish 14 g by each of the kibbutz group. The equivalent national food habits,25retrospective dietary analyses of
Tel Aviv figures were 86 g, 39 g, and 8 g. A published colon cancer comparison of dietary habits
national sample for 1975- 1976 showed a daily per cap- of selected groups within a geographic area,**and rural-
ita consumption of 57 g of poultry, 42 g of beef, and urban and migrant studies.4,15*25,29,30 Those who believe
17 g of fish.I4 Interestingly, for the same period, the that specific dietary factors are related to the etiology
calculated (from purchasing records) daily per capita of colon cancer have frequently found it difficult to
consumption of all the kibbutz residents was 79 g of prove their point. ‘
Some are willing to propose
3,496,20.2333

cooked poultry, 27 g of beef, and 16 g of fish. The dif-
ference between these and the dietary survey figures are
explained by the fact that the children are offered
mainly poultry while the adults are given a choice of
beef or poultry.
Markedly significant differences between the two
groups were found in the daily intake of the following
nutrients: the kibbutz members had a greater intake of
unavailable carbohydrates (“crude fiber”), potassium,
magnesium, calcium, iron, carotene, thiamine, ribofla-
vin, ascorbic acid, polyunsaturated fats, and a greater
P/S ratio, while the Tel Aviv residents had a higher
intake of retinol and saturated fats.
The per capita daily food consumption of both groups
was compared with present and previously published
national and calculated kibbutz figures.14 There was a
tendency in the kibbutz, over a period of seven years,
to eat more meat and poultry (a 17% rise) and more
fruit and vegetables (a 25% rise). Intake of other food-
stuffs showed little change. National figures for beef
and poultry intake were virtually identical to those
found in a survey seven years before, though fish con-
sumption had fallen by 25%.
Discussion
The etiology of large bowel cancer has been the sub-
ject of many recent review^.'^,'^ The etiologic impor-
tance of various dietary factors has been extensively
a preventive diet, while others feel that changing na-
tional habits is difficult and unjustified considering the
present state of k n ~ w l e d g e . ’ ~ , ~ ~ , ~ ~ * ~ ’ * ~ *
In the United States, Jews of European origin are at
an increased risk of developing colon cancer.33In Israel,
however, similar Jews of European-American origin
have only a “medium” incidence of large bowel cancer
compared with the rest of the world.I2 This has been
correlated with Israeli dietary habits, namely total di-
etary fat,“ cholesterol intake,3 and indirectly with crude
fiber c o n ~ u m p t i o nOur
. ~ ~ dietary survey, from both the
Tel Aviv and kibbutz populations, demonstrate that
they eat less beef, cholesterol, saturated fat (and have
a better P/S ratio), and more crude fiber than has been
quoted for the American and other population^.'^^+^ In
fact, the intake of meat and fat were even lower 25-30
years ago because of food shortages and rationing.14
Poultry is the main source of animal protein and has
not been a food associated, so far, with the etiology of
bowel cancer.22
The kibbutz we have examined is unique in that the
population has kept to a uniform diet for an extensive
period of time and has a low incidence of colon cancer.
Their diet is significantly richer in fiber, vitamins, and
minerals due to a higher intake of fruit and vegetables
than the Tel Aviv controls. On the other hand, both
groups had a similar caloric, total fat, and protein in-
take. This almost laboratory-model state reemphasizes
the importance of unavailable carbohydrate (“fiber”)
No. 12 CANCER
COLORECTAL HABITS
AND DIETARY
in prevention of colorectal cancer. The opposite, a low-
fiber diet, was shown by Modan et al. to be common
in a retrospective analysis of Israeli patients with large
bowel cancer.34 The protective value of other factors
such as ascorbic acid’” or fresh vegetables*’ may also
play a part. The etiologic dietary agents are most likely
multifactorial, and the total amount and balance be-
tween them provides the environmental milieu influ-
encing carcinogenesis.6 At the present state of knowl-
edge, these factors seem to include a high caloric intake,
high fat, high-protein ( ? beef); low fresh fruit, low veg-
etable (? fiber, ? vitamins) diet. It may well be that a
diet, similar to the “prudent” diet recommended by
, ~ been unwittingly tried out in this kibbutz
W ~ n d e rhas
population and has proven its worth as far as colon
cancer is concerned. However, further observations on
larger populations are needed before final conclusions
can be deduced about its place in colorectal cancer pre-
vent ion.
ADDENDUM
Advances in the understanding of dietary fiber and improved food
tables (Paul AA, Southgate DAT, McCance, and Widdowsons: The
composition of foods. London: HMSO, 1978.) have allowed us to
recalculate the total dietary fiber, “unavailable carbohydrate.” The
mean ? SD daily intake of total dietary fiber was 23.6 ? 9.1 g in
the kibbutz group, and only 18.7 * 5.8 g in the Tel-Aviv residents,
P < 0.01.
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