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Influence of Diets High and Low in Animal Fat on Bowel Habit, Gastrointestinal Transit Time, Fecal Microflora, Bile Acid, and Fat Excretion

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Influence of Diets High and Low in Animal Fat on Bowel Habit, Gastrointestinal Transit Time, Fecal Microflora, Bile Acid, and Fat Excretion Influence of diets high and low in animal fat on bowel habit, gastrointestinal transit time, fecal microflora, bile acid, and fat excretion. J H Cummings, … , B S Drasar, M J Hill J Clin Invest. 1978;61(4):953-963. https://doi.org/10.1172/JCI109020. Research Article Epidemiological observations and animal experiments suggest that large bowel cancer is related to serveral factors. Among them, high dietary intakes of animal fat, the presence in the colon of relatively high levels of bile acids, specific patterns of intestinal microflora, slow transit through the gut, and low stool weights. Under metabolic conditions we have observed the effect on these variables of dietes containing 62 or 152 g/day of fat mainly of animal origin in six healthy young men over 4-wk periods. No change attributable to the diet was observed in the subjects' bowel habit, fecal weight, mean transit time through the gut, or in the excretion of dry matter. Total fecal bile acid excretion was significantly higher on the high fat diet (320 +/- 120 mg/day) than on the low fat diet (139.7) +/- 63 mg/day) t test = 7.78 P less than 0.001 as also was the total fecal fatty acid excretion, 3.1+/-0.71 and 1.14+/-0.35 g/day, respectively t test = 11.4 P less than 0.001). The fecal microflora including the nuclear dehydrogenating clostridia were unaltered by the dietary changes as was fecal beta-glucuronidase activity. Dietary changes which increase animal fat intake clearly influence fecal bile acid excretion in a way that would favor the development of large bowel cancer if current theories prove to be true. Dietary fat however […] Find the latest version: https://jci.me/109020/pdf Influence of Diets High and Low in Animal Fat on Bowel Habit, Gastrointestinal Transit Time, Fecal Microflora, Bile Acid, and Fat Excretion J. H. CUMMINGS and H. S. WIGGINS, Medical Research Council Dunn Nutrition Unit, Cambridge, England D. J. A. JENKINS and HELEN HOUSTON, Medical Research Council Gastroenterology Unit, Central Middlesex Hospital, London, England T. JIVRAJ, B. S. DRASAR, and M. J. HILL, Bacterial Metabolism Research Laboratory, Colindale Hospital, London, England A B S TR A C T Epidemiological observations and ani- INTRODUCTION mal experiments suggest that large bowel cancer is related to several factors. Among them, high dietary The high incidence of large bowel cancer found in intakes of animal fat, the presence in the colon of rela- "Western" or industrialized communities is associated tively high levels of bile acids, specific patterns of with high dietary intakes of fat, animal protein, and intestinal microflora, slow transit through the gut, and low intakes of dietary fiber (1-5). The hypothesis re- low stool weights. Under metabolic conditions we have lating low fiber consumption to large bowel cancer has aroused considerable interest, but at the present time observed the effect on these variables of diets con- on taining 62 or 152 g/day of fat mainly of animal origin in adequate data dietary fiber intake at the interna- six healthy young men over 4-wk tional level are not available to assess. The associa- periods. No change tion of high animal protein intake with colonic cancer attributable to the diet was observed in the subjects' is clear but no bowel habit, fecal weight, mean transit time through satisfactory mechanism has been pro- the or in posed to account for this apart from the association gut, the excretion of dry matter. Total fecal bile of high fat intakes in acid excretion was significantly higher on the high fat found commonly populations also diet (320±+120 mg/day) than on the low fat diet (139.7 consuming high animal protein intakes (6). For dietary +63 = < fat, however, there is both evidence of an epidemiolog- mg/day) t test 7.78 P 0.001 as also was the ical link with large bowel cancer and of a possible total fecal fatty acid excretion, 3.1+0.71 and 1.14±0.35 causal mechanism. g/day, respectively t test = 11.4 P < 0.001). The fecal microflora including the nuclear dehydrogenating Large bowel cancer is thought to be due to the pres- clostridia were unaltered by the dietary changes as was ence of carcinogens in the bowel lumen. Bile acids fecal /3-glucuronidase activity. Dietary changes which may be carcinogenic, may act as co-carcinogens, or may increase animal fat intake clearly influence fecal bile be degraded by colonic microflora to carcinogens (7-8). acid excretion in a way that would favor the de- When the stools of subjects from different countries velopment of large bowel cancer if current theories with contrasting large bowel cancer rates are compared prove to be true. Dietary fat however has no effect on the high colon cancer rates are associated with higher overall colonic function so other components of the diet fecal bile acid excretion and a greater preponderance must be responsible for the observed associations of of fecal anaerobic bacteria (9-11) including nuclear bowel cancer with slow transit and reduced bulk. dehydrogenating (ndh)l clostridia (12) although these fecal bacteriological changes are not consistently found (13, 14). In a comparison of subjects with colon cancer and Dr. Drasar's present address is London School of Hygiene and Tropical Medicine. 1 Abbreviations used in this paper: DF, dietary fiber; Receivedfor ptublication 2 Atugust 1977 and in revisedform HFD, high fat diet; LFD, low fat diet; MTT, mean transit 30 November 1977. time; ndh, nuclear dehydrogenating. J. Clin. Invest. © The American Society for Clinical Investigation, Inc., 0021-9738/78/0401-0953 $1.00 953 control patients with matched symptoms, 76% of the TABLE I cancer patients had a combination of ndh clostridia Daily Menus in their stool and >6 mglg fecal solids of bile acids whereas only 9% of the control patients showed Low fat diet Daily allowances glday this (15). Orange juice (tinned, natural If dietary fat and fecal bile acids are both causally unsweetened 200 related to large bowel cancer, a possible mechanism Comflakes 50 would be for dietary fat to increase fecal bile and Jam (raspberry) 25 acid excretion. Previous studies of the of Egg (medium size) 50 effect Sugar 100 dietary fat intake on bile acid excretion in man have Osborne biscuits 40 looked mainly at the effect of different types of fat Bread-white sliced 180 on fecal bile acids. It has been shown that diets high Butter 35 in polyunsaturates result in greater bile acid excretion Potato 150 Rice 150 in the stools than ones high in saturated fat (16, 17). Lettuce 20 Much less attention has been given to the role of dif- Cucumber 20 ferent levels of fat intake of similar fatty acid composi- Tomato 60 tion. Early studies of this problem showed that fecal Yogurt (plain) 140 bile acid excretion was unaltered by increasing dietary Skimmed milk 568 ml intake of saturated fat, usually as butter or hydrogenated Day 1 Day 2 Day 3 coconut fat (18-20). Recently, Hill (21) showed that four normal subjects on a hospital low fat diet decreased g g g their fecal bile acid concentration when compared with Plaice 75 Chicken 75 Beef 75 their normal diet. Green beans 100 Mixed veg. 50 Tomato 50 Because of the relationship between dietary fat and Apricots 120 Brussel 50 Broccoli 50 (tinned) sprouts Peaches 120 large bowel cancer we observed, in six normal people, Lamb 75 Fruit salad 120 (tinned) the effect of diets high and low in animal fat on fecal (tinned) Cottage 75 bile acid output and also on bowel habit, mean transit Tuna fish 75 cheese time (MTT) through the gut, and the fecal microflora because these factors are relevant to the large bowel Modifications for high fat diet cancer hypothesis (22). Daily allowances Cornflakes and rice-omitted METHODS Double cream-50 g added Bread-reduced to 60 g Subjects and study plan Butter-increased to 70 g Six healthy male medical students aged 21-24 were each Potato-reduced to 50 g studied for 10 wk. During two consecutive 4-wk periods they Whole milk replaced skimmed milk ate either a high fat or low fat diet in turn whereas during the first and last week of the study they maintained their Day 1 Day 2 Day 3 normal diets. Throughout these two ad lib. weeks of diet the Cheddar cheese students weighed and recorded all food and drink taken. The 100 design was such that three students ate the high fat diet first g Pork 100 g Lamb 100 g and three the low fat diet first. Volunteers lived in a student replaced lamb replaced chicken replaced cottage hostel on the grounds of the hospital and were expected to cheese continue their normal activities and life-style throughout the study. No subject received any medication before or during the study and alcohol was not allowed. All remained healthy puter program, based on the food tables of McCance and throughout. Widdowson (25). Dietary fat intake was 62 g/day on the low fat diet (LFD) Diets (Tables I-III) and 152 g/day on the high fat diet (HFD). This change to HFD was brought about by increasing the butter intake from 35 The diets were prepared in the metabolic diet kitchen, with to 70 g/day, substituting whole milk for skimmed milk, and most of the food required for the study being purchased in adding 50 g of double cream. These changes accounted for bulk at the start. Three 1-day menus of similar composition 74 g (82%) of the increase, the rest coming from the substi- were designed for each diet and were fed in rotation.
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