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(Journal of Nutrition. 1999;129:1428S-1430S.)
© 1999 The American Society for Nutritional Sciences


Supplement

Nondigestibility Characteristics of Inulin and Oligofructose in Humans1

Henrik B. Andersson2, Lars H. Ellegård and Ingvar G. Bosaeus

Department of Clinical Nutrition, Institute of Internal Medicine, Göteborg University, SE 413 45 Göteborg, Sweden

2To whom correspondence should be addressed.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 Inulin and oligofructose
 Other dietary fiber studies...
 CONCLUSION
 REFERENCES
 
The ileostomy model is considered to be a reliable model to reflect small bowel absorption. Studies in ileostomy subjects have shown that inulin and oligofructose pass through the small bowel without degradation and without influencing the absorption of nitrogen, fat, starch, calcium, magnesium or zinc. Inulin and oligofructose do not have any considerable effect on cholesterol absorption or bile acid excretion.


KEY WORDS: • oligofructose • cholesterol • nitrogen • zinc • iron • humans


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 Inulin and oligofructose
 Other dietary fiber studies...
 CONCLUSION
 REFERENCES
 
This review focuses on the effect of different fiber on ileal excretion in ileostomy subjects. It provides a comparison between short-term balance techniques performed with inulin and oligofructose (Ellegård et al. 1997Citation ) and five earlier studies using different high fiber products or diets (Bosaeus and Andersson 1987Citation , Bosaeus et al. 1992Citation , Ellegård and Bosaeus 1991Citation , Langkilde et al. 1993Citation , Lia et al. 1995Citation ).


    Inulin and oligofructose
 TOP
 ABSTRACT
 INTRODUCTION
 Inulin and oligofructose
 Other dietary fiber studies...
 CONCLUSION
 REFERENCES
 
Ellegård et al. (1997)Citation performed a double blind crossover study with inulin and oligofructose in 10 patients with conventional ileostomy due to ulcerative colitis. The mean serum cholesterol of the subjects was 6.3 mmol/L. Subjects test diets were prepared in a metabolic kitchen for 3 d. The basal diet with added sucrose (7 g) compared with a diet fortified with of 17 g of inulin, (19.4 g of Raftiline ST) or 17 g of oligofructose (19 g of Raftilose P95). Inulin and oligofructose were digested only to a small extent in the small intestine. The recovery in the ileostomy effluent amounted to 88% [95% confidence interval (CI), 76–100%] and 89% (64–114%) for inulin and oligofructose, respectively. Similar figures have been reported (Bach Knudsen and Hessov 1995Citation ) and are comparable to the recovery of 88% obtained with wheat bran in our earlier ileostomy studies (Sandberg et al. 1981Citation ). The nondigested fructans increased dry matter excretion by nearly 15 g, with an energy content of almost 17 kJ/g, equivalent to the energy value of carbohydrates. No change in the mean daily ileal excretion of nitrogen (2.2, 2.3 and 2.2 g), fat (8.7, 9.6 and 9.3 mmol), or starch (8.8, 9.1 and 8.6 g) occurred in subjects fed the three diets. Moreover, the mean values for the ileal excretion of calcium, magnesium and zinc did not differ among dietary treatments. Mean mineral excretions were 29.3, 29.8 and 31.2 mmol of calcium, 11.1, 10.9 and 10.8 mmol of magnesium and 119, 147 and 116 µmol of zinc per 24 h, respectively. The ileostomy model offers a sensitive method to determine short-term excretion of cholesterol, which averaged 506, 504 and 510 mg per 24 h for the three diets, respectively, and the mean cholesterol absorption, measured with an isotope-labeled cholesterol technique, which averaged 63, 60 and 62%, respectively. No significant differences in bile acid excretion between the three periods were detected (480 mg, 453 mg and 326 mg, respectively). This study suggests that inulin has little or no influence on the absorption of nutrients and minerals in the small bowel. Nevertheless, several questions about this study emerged, including the following: How reliable are these figures? It must be questioned whether the recovery from the ileostomy bags corresponds to the flow from the small to the large bowel. Earlier experience of the sensitivity of excretion figures for sterols in the ileostomy model may provide some clues.


    Other dietary fiber studies with the ileostomy model
 TOP
 ABSTRACT
 INTRODUCTION
 Inulin and oligofructose
 Other dietary fiber studies...
 CONCLUSION
 REFERENCES
 
Although studies in ileostomy subjects have been performed earlier (Werch and Ivy 1940Citation ), reliable results of specific analyses of the ileostomy contents could not be obtained until we introduced studies using a controlled diet in the late 1970s that minimized bacterial degradation by frequent collection and immediately freezing of the contents. This is now referred to as the ileostomy model. Advantages and disadvantages have recently been reviewed (Andersson 1992Citation , Andersson and Bosaeus 1993Citation ).

The main advantage of the ileostomy model is that the intestinal transit time is so short that the effluent corresponding to one day's intake is completely excreted before the next morning (Englyst and Cummings 1986Citation , Sandberg et al. 1981Citation ). The within-patient, within-diet and day-to-day variations are small, making short-term balance studies feasible. The standard error of the mean for nitrogen and calcium cumulative balances, was similar for a 4-d balance period in ileostomy subjects (1.5 and 1.0 mmol/24 h, respectively) compared with that for 52 d in subjects with an intact large bowel (1.5 and 1.9 mmol/24 h, respectively) (Tornquist et al. 1986Citation ). The CV between days for dry matter excretion in ileostomy subjects is ~5% (Ellegård and Bosaeus 1991Citation ).

Collection of ileostomy contents is relatively easy to perform for ileostomy subjects because handling of ileostomy excreta is a routine matter for these subjects. In contrast, constant supervision and encouragement are needed to obtain complete fecal collections from normal healthy persons. The ileostomy model could be criticized because ileostomy subjects have lost the ileocecal valve together with a minimal part of the distal ileum. Furthermore, the bacterial flora differ from those of the normal distal ileum. The number of bacteria in the terminal ileum of ileostomy subjects has been estimated to be 107–108 per gram compared with 105–106 per gram in the normal ileum (Finegold et al. 1970Citation ).

A number of studies, however, support the idea that there is only a small microbial degradation in the ileostomy bags when they are handled properly. Thus, degradation of bile acids and neutral steroids is minimal (Bosaeus et al. 1986Citation , Bosaeus and Andersson 1987Citation ). Furthermore, there is no or minimal degradation of non-starch polysaccharide (NSP) components from pectin, bran or starchy foods (Englyst and Cummings 1987Citation , Englyst and Kingman 1990Citation , Schweizer et al. 1990Citation ). Less then 5 mmol/L of short-chain fatty acids are found in ileal samples (Cummings and Englyst 1991Citation ). The pH of the ileostomy content is generally in the range of 7–8. Moreover, to determine whether significant fermentation occurs in the terminal ileum, two ileostomy subjects have been studied both with and without the antibiotic Metronidazole (Englyst and Cummings 1987Citation ). No significant difference was observed in the recovery of non-starch polysaccharides (NSP), starch or resistant starch with or without the antibiotic. Consequently, the ileostomy model can be used for determination of small-intestinal digestion of carbohydrates without interference from any substantial bacteriological degradation.

It could also be questioned whether the transit through the small bowel in the proctocolectomized subject differs from that of the normalsubject. However, transit time through the stomach and small intestine of ileostomy subjects is similar to that observed in healthy subjects (Holgate and Read 1983Citation , Malagelada et al. 1984Citation ). Moreover, the so-called ileal brake, whereby fat in the terminal ileum may influence gastric emptying rate and the intestinal transit time, also seems to be operative in ileostomy subjects (Soper et al. 1990Citation ).

The function of the distal ileum seems to remain intact in patients in whom there is only a small resection of the distal ileum, as after proctocolectomy for ulcerative colitis. Ileal excretion from patients operated for Crohn's disease does not reflect the normal excretion to the large bowel. The excretion of bile acids from the ileostomy is seldom increased above 1 g/24 h. Bile acid excretion was found to be 410 ± 72 (mean ±SEM) mg/24 h in a well-controlled group of nine ileostomy subjects (Ellegård and Bosaeus 1991Citation ), which equals fecal losses. These nine subjects had a mean serum cholesterol level of 6.0 mmol/l, within the normal range of healthy subjects consuming a Western diet.

Two studies have also been performed to show that there is no difference between the immediate response to a diet change on ileal excretion and to the excretion pattern after some weeks of consuming the same diet (Zhang et al. 1991Citation , Zhang et al. 1992Citation ). The immediate response to the diet appears thus to remain in long-term studies. Moreover, the reduction in serum cholesterol induced by oat bran in ileostomy subjects was similar to that of normal persons (Andersson and Bosaeus 1993Citation ).

Earlier studies in ileostomy subjects have shown a correlation between the serum cholesterol–lowering property of a dietary fiber product and small bowel excretion (Andersson 1992Citation ). Citrus pectin (Bosaeus et al. 1986Citation ) and oat bran (Lia et al. 1995Citation ), which are known to reduce serum cholesterol, increased ileal bile acid excretion. Wheat bran, without effect on serum lipids, did not induce any significant change in sterol excretion (Bosaeus et al. 1986Citation ). Ileostomy studies with 3 d for each dietary period, with the same number of subjects, given 15 g pectin or 15 g of mixed dietary fibers from unrefined food, could detect changes in sterol excretion of 15% (Andersson and Bosaeus 1993Citation ). It seems unlikely that inulin and oligofructose in similar doses (Ellegård et al. 1997Citation ) would induce any considerable effect on sterol excretion from the small bowel.


    CONCLUSION
 TOP
 ABSTRACT
 INTRODUCTION
 Inulin and oligofructose
 Other dietary fiber studies...
 CONCLUSION
 REFERENCES
 
From our study performed on inulin and oligofructose in ileostomy subjects (Ellegård et al. 1997Citation ), in relation to our earlier experience with ileostomy subjects, three conclusions can be reached. First, inulin or oligofructose passes through the small bowel without degradation and without influencing the absorption of nutrients or minerals (calcium, magnesium and zinc). Second, inulin and oligofructose do not appear to have any considerable effect on cholesterol and bile acid excretion in the small bowel. Finally, one of the physiologic effects of inulin and oligofructose is to supply substrate for fermentation in the colon.


    FOOTNOTES
 
1 Presented at the conference Nutritional and Health Benefits of Inulin and Oligofructose held May 18–19, 1998 in Bethesda, MD. This symposium was supported in part by educational grants from the National Institutes of Health Office of Dietary Supplements, the U.S. Department of Agriculture and Orafti Technical Service. Published as a supplement to The Journal of Nutrition. Guest editors for the symposium publication were John A. Milner, The Pennsylvania State University, and Marcel Roberfroid, Louvain University, Brussels, Belgium. Back


    REFERENCES
 TOP
 ABSTRACT
 INTRODUCTION
 Inulin and oligofructose
 Other dietary fiber studies...
 CONCLUSION
 REFERENCES
 

1. Andersson H. The ileostomy model for the study of carbohydrate digestion and carbohydrate effects on sterol excretion in man. Eur. J. Clin. Nutr. 1992;46:S69-S76

2. Andersson H., Bosaeus I. Sterol balance studies in man. A critical review. Eur J Clin. Nutr. 1993;47:153-159[Medline]

3. Bach Knudsen K. E., Hessov I. B. Recovery of inulin from Jerusalem artichoke (Helianthus tuberosus L.) in the small intestine of man. Br. J. Nutr. 1995;74:101-113[Medline]

4. Bosaeus I., Andersson H. Short-term effect of two cholesterol-lowering diets on sterol excretion in ileostomy patients. Am. J. Clin. Nutr. 1987;45:54-59[Abstract/Free Full Text]

5. Bosaeus I., Belfrage L., Lindgren C., Andersson H. Olive oil instead of butter increases net cholesterol excretion from the small bowel. Eur. J. Clin. Nutr. 1992;46:111-115[Medline]

6. Bosaeus I., Carlsson N.-G., Sandberg A.-S., Andersson H. Effect of wheat bran and pectin on bile acid and cholesterol excretion in ileostomy patients. Hum. Nutr. Clin. Nutr. 1986;40C:429-440[Medline]

7. Cummings J. H., Englyst H. N. Measurement of starch fermentation in the human large intestine. Can. J. Physiol. Pharmacol. 1991;69:121-129[Medline]

8. Ellegård L., Andersson H., Bosaeus I. Inulin and oligofructose do not influence the absorption of cholesterol, or the excretion of cholesterol, Ca, Mg, Zn, Fe, or bile acids but increase energy excretion in ileostomy subjects. Eur. J. Clin. Nutr. 1997;51:1-5[Medline]

9. Ellegård L., Bosaeus I. Sterol and nutrient excretion in ileostomists on prudent diets. Eur. J. Clin. Nutr. 1991;45:451-457[Medline]

10. Englyst H. N., Cummings J. H. Digestion of polysaccharides of potato in the small intestine of man. Am. J. Clin. Nutr. 1987;45:423-431[Abstract/Free Full Text]

11. Englyst H. N., Kingman S. M. Dietary fiber and resistant starch: a nutritional classification of plant polysaccharides. Kritchevsky D. Anderson J. A. eds. Dietary Fiber, Chemistry, Physiology and Health Effects 1990:49-65 Plenum Press New York, NY.

12. Englyst H. N., Cummings J. H. Digestion of the carbohydrates of banana (Musa paradisiaca sapientum) in the human small intestine. Am. J. Clin. Nutr. 1986;44:42-50[Abstract/Free Full Text]

13. Finegold S. M., Sutter V. L., Boyle J. D., Shimada K. The normal flora of ileostomy and transverse colostomy effluents. J. Infect. Dis. 1970;122:376-381[Medline]

14. Holgate A. M., Read N. W. Relationship between small bowel transit time and absorption of a solid meal; influence of metoclopramide, magnesium sulfate and lactulose. Dig. Dis. Sci. 1983;28:812-819[Medline]

15. Langkilde A. M., Andersson H., Bosaeus I. Sugar-beet fibre increases cholesterol and reduces bile acid excretion from the small bowel. Br. J. Nutr. 1993;70:757-766[Medline]

16. Lia Å., Hallmans G., Sandberg B., Åhman P., Andersson H. Oat (ß-glucan) increases bile acid excretion and a fiber-rich barley fraction increases cholesterol excretion in ileostomy subjects. Am. J. Clin. Nutr. 1995;62:1245-1251[Abstract/Free Full Text]

17. Malagelada J. R., Robertson J. S., Brown M. L., Remington M., Duenes J. A., Thomforde G. M., Carryer P. W. Intestinal transit of solid and liquid components of a meal in health. Gastroenterology 1984;87:1255-1263[Medline]

18. Sandberg A.-S., Andersson H., Hallgren B., Hasselblad K., Isaksson B. Experimental model for in vivo determination of dietary fibre and its effect on the absorption of nutrients in the small intestine. Br. J. Nutr. 1981;45:283-294[Medline]

19. Schweizer T. H., Andersson H., Langkilde A. M., Reimann S., Torsdottir I. Nutrients excreted in ileostomy effluents after consumption of mixed diets with beans or potatoes. II. Starch, dietary fibre and sugars. Eur. J. Clin. Nutr. 1990;44:567-575[Medline]

20. Soper N. J., Chapman N. J., Kelly K. A., Brown M. L., Phillips S. F., Vay Liang W.G.O. The "ileal brake" after ileal pouch-anal anastomosis. Gastroenterology 1990;98:111-116[Medline]

21. Tornquist H., Rissanen A., Andersson H. Balance studies in patients with intestinal resection, how long is enough?. Br. J. Nutr. 1986;56:11-16[Medline]

22. Werch S. C., Ivy A. C. On the fate of ingested pectin. Am. J. Clin. Nutr. 1940;8:101-105

23. Zhang J.-X., Hallmans G., Andersson H., Bosaeus I., Åman P., Tidehag P., Stenling R., Lundén E., Dahlgren S. Effects of oat bran on plasma cholesterol and bile acid excretion in nine subjects with ileostomies. Am. J. Clin. Nutr. 1992;56:99-105[Abstract/Free Full Text]

24. Zhang J.-X., Lundin E., Andersson H., Bosaeus I., Dahlgren S., Hallmans G., Stenling R., Åman P. Brewers' spent grain, serum lipids and fecal sterol excretion in human subject with ileostomies. J. Nutr. 1991;121:778-784




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