Fecal
of volunteers
J. Hentges,3
Ten
volunteers
meatless
diet,
a high-beef
contents high-beef
were diet.
essentially High-beef
flora
of the
volunteers.
diets
in total
numbers
differences indicate
in the that
possible
is discussed.
completed
diet,
and
There
counts
were
of the
protein
influence Am.
American
Journal
of Clinical
Nutrition
a 4-month same
control
the same in all four protein consumption no
of anaerobic,
animal
the
of animal I
(‘lin.
genera has
fat consumption
Nutr.
31: OCTOBER
differences or aerobic
individual
consumption
diet diet,
31: Sl23-S124,
series
consisting
each
hasting
of a control 1 month.
Fat
diet, and
a
fiber
diets, but protein content was doubled during the had little effect on the composition of the intestinal
significant
facultative,
A systematic study was initiated in our laboratory to examine the effect of a highbeef diet on the bacterial and chemical composition of human feces ( 1 ). Ten student volunteers were placed on a dietary regimen for 4 months that included a typically American diet (which served as the control), a meatless diet, a high-beef diet, and again the control diet, each of 1-month duration. Fat and fiber contents were essentially the same in all four diets, but the protein content was doubled during the high-beef diet. Great variations in bacterial counts were obtained among the volunteers (2). Despite these variations, the mean counts of the major groups of organisms were remarkably similar under all dietary conditions, with the exception of cbstridia and filamentous fungi whose numbers were erratic. Dietary change appeared to have little effect on counts at the species and subspecies level. However, in most cases tests for significance could not be performed at this level because of the irregular appearance of individual species and subspecies among the isolates. Where tests for significance could be performed, differences in counts between meatless and high-beef diets were observed in only a few instances. The results of this study differed from those reported by Hill et al. (3). There were no significant differences between the high-meat and meatless diets in the total numbers of anaerobic, facultative, or aerobic organisms isolated from the feces of volunteers, nor were there major differences in the counts of the The
diets1’2
Ph.D.
ABSTRACT
The
on controlled
little
and
between organisms
species
effect on the
on
the
of bacteria the
high-beef
isolated, fecal
metabolic
nor
and were
encountered.
bacterial activities
profile of intestinal
meatless
there
major
The
data
in humans. bacteria
1978.
individual genera and species of organisms encountered. Some increase in the ratio of anaerobic bacteria to facultative and aerobic organisms was observed during the high-meat diet as compared with the mealtless diet, but this ratio was not of the same magnitude reported by Hill et at. (3). There was no increase in the concentrations of acid or neutral steroids or their metabohites in the feces of the volunteers during the high-meat diet. On the contrary, the concentrations of cholesterol metabolites in the feces were significantly lower during the high-meat diet as compared to the meatless diet. These data indicate that high-animal protein consumption produces no major effects on the bacterial and steroid composition of the feces. However, it should be emphasized that we examined only the effect of high-meat protein consumption on the composition of the feces. The fat content in all diets was held constant. There is evidence that animal fat consumption influences the concentration of steroids in the feces. Hill (4) showed that the acid steroid concentration in the feces of volunteers declined greatly and that the neutral steroid concentration declined slightly when fat meat in the diet was replaced by lean meat. The proportion of secondary bile acids ‘From the Department of Microbiology, University of Missouri, School of Medicine, Columbia, Missouri 65201. 2Supported by Contract NOl-CP-33335 from the National Cancer Institute. Professor and Chairman of Microbiology.
1978,
pp. S123-S124.
Printed
in U.S.A.
S123
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S123/4656077 by Boston University Libraries user on 14 January 2019
David
flora
S 124
HENTGES
feces. These studies suggest that the taxonomic criteria used may be inadequate in assessing the influence of diet on the intestinal flora. It is apparent that a positive correlation exists between high meat consumption and colon cancer risk. High levels of steroid conversion products that function as carcinogenic or cocarcinogenic agents occur in the feces of colon cancer patients and of individuals who consume a great deal of meat. The high steroid levels appear to be the result of animal fat consumption rather than protein consumption. Although diet does not necessarily influence the composition of the intestinal flora, there is evidence that it has an impact on the bacteria that are largely responsible for formation of steroid conversion products. Of primary importance in investigating the etiology of colon cancer is an understanding ofthe influence ofdietary constituents on the enzymic activities of intestinal bacteria, irrespective of species.
a
References 1. HENTGES,
D. J., G. C. BURTON, M. A. FLYNN, J. A. C. W. GEHRKE, K. 0. GERHARDT, B. R. MAIER, R. K. TSUTAKAWA AND R. L. WIx0M. Effect of a high beef diet on bacterial flora and chemical components of human feces: a summary of results. Proceedings of the Third International Symposium on the Detection and Prevention of Cancer, New York, 1977, in press. HENTGES, D. J., B. R. MAIER, G. C. BURTON, M. A. FLYNN AND R. K. TSUTAKAWA. Effect ofa high beef diet on the fecal bacterial flora of humans. Cancer Res. 37: 368, 1977. HILL, M. J., B. S. DRASAR, V. ARIES, J. S. CROWTHER, G. HAWKSWORTH AND R. E. 0. WILLIAMS. Bacteria and aetiology of cancer of large bowel. Lancet 1: 95, 1971. HILL, M. J. The Effect of some factors on the faecal concentration of acid steroids, neutral steroids and urobilins. J. Pathol. 104: 239, 1971. REDDY, B. S., J. H. WEISBURGER AND E. L. WYNDER. Effect of high risk and low risk diets for colon carcinogenesis on fecal microflora and steroids in man. J. Nutr. 105: 878, 1975. MooRE, W. E. C., AND L. V. HOLDEMAN. Discussion of current bacteriological investigations of the relationships between intestinal flora, diet, and colon cancer. Cancer Res. 35: 3418, 1975. FINEGOLD, S. M., H. R. ATFEBERY AND V. L. SuTFRANZ,
2.
3.
4.
5.
6.
7.
TER.
Effect
of Japanese
27:
1456,
8. DRASAR, and large 1976.
of diet and
on
human
American
fecal diets.
flora: Am.
1974. B. S., AND D. J. A. JENKINS. bowel cancer. Am. J. Chin.
comparison
J. Clin.
Nutr.
Bacteria,
diet, 1410,
Nutr.
29:
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S123/4656077 by Boston University Libraries user on 14 January 2019
was greatest during the fat meat consumption when the concentration of total bile acids was high. Hill speculated that the secondary bile acid are products of the dehydroxylation of primary fecal bile acids by intestinal bacteria. Reddy et a!. (5) compared the effects of a high-fat, high-meat, mixed Western diet with a nonmeat diet on the flora and steroid content of the feces of human volunteers. The protein content of both diets was nearly the same, but the fat content was 15% greater in the mixed Western diet than in the nonmeat diet. Although differences in bacterial counts between the two diets were not striking, total anaerobic counts and counts of several mdividual genera of anaerobes were significantly greater during the mixed Western diet than during the nonmeat diet. Fecal excretion of secondary bile acids and cholesterol metabohites was also greater during consumption of the mixed Western diet. It was concluded from these studies that high dietary fat intake affects the composition of the intestinal flora and the level of steroid conversion products in the feces. Major differences in flora composition between highand low-risk groups were not observed, however, by Moore and Holdeman (6) or by Finegold et al. (7). In their studies, the composition ofthe intestinal flora of highrisk populations, including polyp patients, North Americans, and Japanese-Americans on Western-type diets, was compared with the composition of the flora of low-risk populations, including rural Japanese, Africans of the Tswana tribe, and Japanese-Americans eating a traditional Japanese diet. Although there were some minor quantitative variations, no organisms characteristic of high- or low-risk populations were detected. Organisms commonly present in individuals on high-risk diets were also present in individuals on low-risk diets. Similar results were obtained during an investigation of the influence of various dietary supplements on the composition of the fecal flora of student volunteers (8). The subjects consumed their usual diets. At intervals, the diets were supplemented for 2-week periods with either unabsorbable plant polysaccharides, fiber (in the form of bananas), olive oil, or medium-chain triglycerides. None of the supplements appreciably altered the types or numbers of bacteria isolated from the
of volunteers
J. Hentges,3
Ten
volunteers
meatless
diet,
a high-beef
contents high-beef
were diet.
essentially High-beef
flora
of the
volunteers.
diets
in total
numbers
differences indicate
in the that
possible
is discussed.
completed
diet,
and
There
counts
were
of the
protein
influence Am.
American
Journal
of Clinical
Nutrition
a 4-month same
control
the same in all four protein consumption no
of anaerobic,
animal
the
of animal I
(‘lin.
genera has
fat consumption
Nutr.
31: OCTOBER
differences or aerobic
individual
consumption
diet diet,
31: Sl23-S124,
series
consisting
each
hasting
of a control 1 month.
Fat
diet, and
a
fiber
diets, but protein content was doubled during the had little effect on the composition of the intestinal
significant
facultative,
A systematic study was initiated in our laboratory to examine the effect of a highbeef diet on the bacterial and chemical composition of human feces ( 1 ). Ten student volunteers were placed on a dietary regimen for 4 months that included a typically American diet (which served as the control), a meatless diet, a high-beef diet, and again the control diet, each of 1-month duration. Fat and fiber contents were essentially the same in all four diets, but the protein content was doubled during the high-beef diet. Great variations in bacterial counts were obtained among the volunteers (2). Despite these variations, the mean counts of the major groups of organisms were remarkably similar under all dietary conditions, with the exception of cbstridia and filamentous fungi whose numbers were erratic. Dietary change appeared to have little effect on counts at the species and subspecies level. However, in most cases tests for significance could not be performed at this level because of the irregular appearance of individual species and subspecies among the isolates. Where tests for significance could be performed, differences in counts between meatless and high-beef diets were observed in only a few instances. The results of this study differed from those reported by Hill et al. (3). There were no significant differences between the high-meat and meatless diets in the total numbers of anaerobic, facultative, or aerobic organisms isolated from the feces of volunteers, nor were there major differences in the counts of the The
diets1’2
Ph.D.
ABSTRACT
The
on controlled
little
and
between organisms
species
effect on the
on
the
of bacteria the
high-beef
isolated, fecal
metabolic
nor
and were
encountered.
bacterial activities
profile of intestinal
meatless
there
major
The
data
in humans. bacteria
1978.
individual genera and species of organisms encountered. Some increase in the ratio of anaerobic bacteria to facultative and aerobic organisms was observed during the high-meat diet as compared with the mealtless diet, but this ratio was not of the same magnitude reported by Hill et at. (3). There was no increase in the concentrations of acid or neutral steroids or their metabohites in the feces of the volunteers during the high-meat diet. On the contrary, the concentrations of cholesterol metabolites in the feces were significantly lower during the high-meat diet as compared to the meatless diet. These data indicate that high-animal protein consumption produces no major effects on the bacterial and steroid composition of the feces. However, it should be emphasized that we examined only the effect of high-meat protein consumption on the composition of the feces. The fat content in all diets was held constant. There is evidence that animal fat consumption influences the concentration of steroids in the feces. Hill (4) showed that the acid steroid concentration in the feces of volunteers declined greatly and that the neutral steroid concentration declined slightly when fat meat in the diet was replaced by lean meat. The proportion of secondary bile acids ‘From the Department of Microbiology, University of Missouri, School of Medicine, Columbia, Missouri 65201. 2Supported by Contract NOl-CP-33335 from the National Cancer Institute. Professor and Chairman of Microbiology.
1978,
pp. S123-S124.
Printed
in U.S.A.
S123
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S123/4656077 by Boston University Libraries user on 14 January 2019
David
flora
S 124
HENTGES
feces. These studies suggest that the taxonomic criteria used may be inadequate in assessing the influence of diet on the intestinal flora. It is apparent that a positive correlation exists between high meat consumption and colon cancer risk. High levels of steroid conversion products that function as carcinogenic or cocarcinogenic agents occur in the feces of colon cancer patients and of individuals who consume a great deal of meat. The high steroid levels appear to be the result of animal fat consumption rather than protein consumption. Although diet does not necessarily influence the composition of the intestinal flora, there is evidence that it has an impact on the bacteria that are largely responsible for formation of steroid conversion products. Of primary importance in investigating the etiology of colon cancer is an understanding ofthe influence ofdietary constituents on the enzymic activities of intestinal bacteria, irrespective of species.
a
References 1. HENTGES,
D. J., G. C. BURTON, M. A. FLYNN, J. A. C. W. GEHRKE, K. 0. GERHARDT, B. R. MAIER, R. K. TSUTAKAWA AND R. L. WIx0M. Effect of a high beef diet on bacterial flora and chemical components of human feces: a summary of results. Proceedings of the Third International Symposium on the Detection and Prevention of Cancer, New York, 1977, in press. HENTGES, D. J., B. R. MAIER, G. C. BURTON, M. A. FLYNN AND R. K. TSUTAKAWA. Effect ofa high beef diet on the fecal bacterial flora of humans. Cancer Res. 37: 368, 1977. HILL, M. J., B. S. DRASAR, V. ARIES, J. S. CROWTHER, G. HAWKSWORTH AND R. E. 0. WILLIAMS. Bacteria and aetiology of cancer of large bowel. Lancet 1: 95, 1971. HILL, M. J. The Effect of some factors on the faecal concentration of acid steroids, neutral steroids and urobilins. J. Pathol. 104: 239, 1971. REDDY, B. S., J. H. WEISBURGER AND E. L. WYNDER. Effect of high risk and low risk diets for colon carcinogenesis on fecal microflora and steroids in man. J. Nutr. 105: 878, 1975. MooRE, W. E. C., AND L. V. HOLDEMAN. Discussion of current bacteriological investigations of the relationships between intestinal flora, diet, and colon cancer. Cancer Res. 35: 3418, 1975. FINEGOLD, S. M., H. R. ATFEBERY AND V. L. SuTFRANZ,
2.
3.
4.
5.
6.
7.
TER.
Effect
of Japanese
27:
1456,
8. DRASAR, and large 1976.
of diet and
on
human
American
fecal diets.
flora: Am.
1974. B. S., AND D. J. A. JENKINS. bowel cancer. Am. J. Chin.
comparison
J. Clin.
Nutr.
Bacteria,
diet, 1410,
Nutr.
29:
Downloaded from https://academic.oup.com/ajcn/article-abstract/31/10/S123/4656077 by Boston University Libraries user on 14 January 2019
was greatest during the fat meat consumption when the concentration of total bile acids was high. Hill speculated that the secondary bile acid are products of the dehydroxylation of primary fecal bile acids by intestinal bacteria. Reddy et a!. (5) compared the effects of a high-fat, high-meat, mixed Western diet with a nonmeat diet on the flora and steroid content of the feces of human volunteers. The protein content of both diets was nearly the same, but the fat content was 15% greater in the mixed Western diet than in the nonmeat diet. Although differences in bacterial counts between the two diets were not striking, total anaerobic counts and counts of several mdividual genera of anaerobes were significantly greater during the mixed Western diet than during the nonmeat diet. Fecal excretion of secondary bile acids and cholesterol metabohites was also greater during consumption of the mixed Western diet. It was concluded from these studies that high dietary fat intake affects the composition of the intestinal flora and the level of steroid conversion products in the feces. Major differences in flora composition between highand low-risk groups were not observed, however, by Moore and Holdeman (6) or by Finegold et al. (7). In their studies, the composition ofthe intestinal flora of highrisk populations, including polyp patients, North Americans, and Japanese-Americans on Western-type diets, was compared with the composition of the flora of low-risk populations, including rural Japanese, Africans of the Tswana tribe, and Japanese-Americans eating a traditional Japanese diet. Although there were some minor quantitative variations, no organisms characteristic of high- or low-risk populations were detected. Organisms commonly present in individuals on high-risk diets were also present in individuals on low-risk diets. Similar results were obtained during an investigation of the influence of various dietary supplements on the composition of the fecal flora of student volunteers (8). The subjects consumed their usual diets. At intervals, the diets were supplemented for 2-week periods with either unabsorbable plant polysaccharides, fiber (in the form of bananas), olive oil, or medium-chain triglycerides. None of the supplements appreciably altered the types or numbers of bacteria isolated from the
