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© 2007 American Society for Nutrition J. Nutr. 137:2580S-2584S, November 2007

Inulin and Oligofructose: Health Benefits and Claims-A Critical Review

Overview of Experimental Data on Reduction of Colorectal Cancer Risk by Inulin-Type Fructans1–4,

Beatrice L. Pool-Zobel* and Julia Sauer

Department of Nutritional Toxicology, Institute for Nutrition, Friedrich-Schiller-University, D-07743 Jena, Germany

* To whom correspondence should be addressed. E-mail: b8pobe{at}uni-jena.de.


   ABSTRACT
TOP
 ABSTRACT
Introduction
 LITERATURE CITED
 
Colorectal cancer is related to diet, lifestyle, physical inactivity, and obesity. The responsible carcinogens cause mutations or enhance cell growth. Inulin-type fructans may counteract the effects via their gut flora-mediated fermentation products in vitro and in vivo. Important products formed by fermentation of inulin-type fructans with human gut flora are short-chain fatty acids. Of these, butyrate and propionate inhibit growth of colon tumor cells and histone deacetylases. Butyrate also causes apoptosis, reduces metastasis in colon cell lines, and protects from genotoxic carcinogens by enhancing expression of enzymes involved in detoxification. Fermentation supernatants of inulin have similar growth-inhibitory effects on colon adenoma and carcinoma cells and induce histone hyperacetylation by inhibiting histone deacetylases. In animal models inulin-type fructans prevent and retard colorectal carcinogenesis. Several studies reported the reduction of chemically induced preneoplastic lesions or tumors in the colon of rodents treated with inulin-type fructans. The human intervention study (SYNCAN project) sought to provide the experimental evidence for risk reduction by inulin-type fructans in humans. One group of polypectomized people at high risk for colon cancer and another of colon cancer volunteers after curative resection were given a synbiotic preparation. There were clear functional effects of the synbiotic because numerous different cancer risk markers were favorably altered. In conclusion, there is considerable experimental evidence that inulin modulates parameters of colon cancer risks in human colon cells, in animals, and in a human intervention trial. The involved mechanisms possibly include reduction of exposure to risk factors and suppression of tumor cell survival.


   Introduction
TOP
 ABSTRACT
 Introduction
LITERATURE CITED
 
The evolution of colorectal cancer (CRC)5 is a complicated multistep process involving specific molecular genetic alterations in tumor suppressor genes, protooncogenes, and genes encoding proteins for DNA repair (1). Some of these genetic lesions may be inherited and are the most decisive type of susceptility factors (2). The alterations can also be caused during the lifetime of an individual by exogenous and endogenous chemicals with genotoxic potential (3). They have their source in the general environment, in nutrition, and subsequently in various processes of metabolically endogenous conversion (4). This leads to a considerable burden of toxic and genotoxic factors in the gut lumen. Fecal samples, for instance, have been shown to contain bile acids, amines, sulfates, and bacterial toxins (5); additional products of bacterial biotransformation (6); nondigested food residues and excretable metabolites; and genotoxic compounds (7).

Several dietary or biliary compounds can be transformed by anaerobic gut bacteria to genotoxic products. For instance, heterocyclic amines, which are pyrolysis products from fried protein-containing foods that undergo biotransformation in the liver, can be reactivated by eubacteria and chlostridia in the colon by the bacterial ß-glucuronidase (8,9). Collectively, chronic exposure to such substances may initiate the process of colorectal carcinogenesis or enhance its progression.

Protective factors from nutrition, such as foods containing inulin-type fructans, may lead to other fecal compounds that are more related to cancer prevention, such as the SCFA, of which butyrate has been shown to have numerous biological effects. This product of gut flora-mediated fermentation induces apoptosis of tumor cells (10) and protects cells from genotoxic insult by elevating phase II detoxification (11). The SYNCAN-project has investigated some of these mechanisms in more detail, as is outlined below.

In vitro studies

In a series of experiments performed in vitro with cultured cell lines, we first investigated the composition and the effects of a fermentation supernatant obtained after anaerobic incubation of Synergy (a prebiotic mixture of oligofructose and inulin) with samples of feces-derived human gut flora (12). A subgroup of fermentation samples representing different regions of the large intestine were prepared as described (13). As shown in Figure 1, the butyrate concentration was markedly increased in vessel 3, which mimics the type of fermentation occurring in the distal colon. It is also apparent from Figure 1 that especially the fermentation products formed in vessel 3 impaired the survival of HT29 tumor cells and were the most efficient inhibitors of cell proliferation. At the same time, markers indicative of the intestinal barrier function were modulated because transepithelial electrical resistance was lowered, and mannitol flux increased. There was also a trend for fermentation products to inhibit invasion (12). Together, the information obtained thus far strongly indicates that fermentation supernatants derived from Synergy impair growth, survival, and progression of human tumor cell lines, all mechanisms that are associated with suppressing activity and secondary cancer prevention (14,15).


Figure 1
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  		FIGURE 1  Concentration of the 3 main SCFA in the fermentation sample of Synergy 1 in 3 different vessels of an in vitro fermentation system and the effects of the supernatants from vessels 2 and 3 on human tumor cells. Results have been published previously (13).

 
An important mechanism by which butyrate causes biological effects in colon carcinoma cells has been proposed to be the hyperacetylation of histones by inhibition of histone deacetylases (16). Histone acetylation influences gene transcription by loosening histone-DNA contacts, thus making the DNA accessible for transcription factors. Imbalance in histone acetylation can lead to transcriptional dysregulation and silencing of genes that are involved in control of cell-cycle progression, differentiation, apoptosis, and cancer development. Recent studies have shown that butyrate and propionate enhanced histone acetylation in HT29 colon adenocarcinoma cells. Together, these SCFA could possibly mediate important processes related to an altered transcriptional gene activation and thus contribute to biological effects possibly related to cancer progression or prevention (17).

Next, we were interested in effects of inulin fermentation products in primary cells. In particular, it was of interest to assess activities that would prohibit the formation of initiated cells or, in other words, prevent the onset of carcinogenesis. For this, we continued our efforts of the last decades (18–20) to refine methods for obtaining primary, nontransformed healthy colon cells and keeping them alive in vitro for a reasonable period of time. Our newest development now is to use surgical samples from which we isolate the epithelial layer and either prepare epithelial tissue strips or isolate intact cells (21). These primary cells, as isolated cells in suspension culture, retain their viability for ~1 h. However, if intact tissue strips are incubated in vitro and then individual cells are isolated, sufficiently viable cells with >50–70% survival can still be recovered after 12 h of in vitro culture. Thus, it is now also possible to perform in vitro, cell-based studies for up to 12 h (22). Using these in vitro cultivation techniques, a first aim was to assess survival of primary colon cells exposed to the Synergy fermentation supernatants (SFS) and to corresponding controls. Figure 2 shows effects of these samples on mitochondrial metabolic activity. There is a marked increase of metabolic activity in primary colon cells treated with SFS. This increase indicates that the fermentation compounds are utilized by the colon cells, an effect that possibly reflects trophic effects. The enhanced metabolism, however, is not caused in a similar manner by butyrate, which has previously been reported to be a survival factor for primary colon cells (23). Figure 2 also shows that the effects are also not caused by a mixture of SCFA composed to mimic the SFS. Instead, it rather seems that the feces supernatant is supplying survival factors that "last" for only 12 h but not for 24 h. Thus, the SFS seems to be more potent in increasing survival of primary colon cells on account of as yet unknown compounds of fecal origin but not because of the SCFA. It will be of interest to identify and characterize those fecal survival factors in more detail in the future.


Figure 2
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  		FIGURE 2  Metabolic activity of primary human colon cells after incubation with a Synergy 1 fermentation supernatant, a butyrate control, the feces control, and a mixture of SCFA mimicking the concentrations in the fermentation supernatant for 4 to 24 h. Results are from Sauer et al. (22).

 
The studies also provide the experimental basis for determining various additional biological effects caused by SFS in primary human colon cells. One of the first applications was to study altered patterns of gene expression caused by SFS, SCFA, and the corresponding controls. In particular, we have investigated expression of genes related to drug metabolism (20), stress response (24), proliferation, and apoptosis (Scharlau, unpublished data). The study of glutathione S-transferases (GSTs) was of particular interest because it seems likely that induced expression of GSTs will result in the protection of cells from genotoxic insult by specific chemicals (25), especially because these particular enzymes are more involved in deactivation than in activation and because they are inducible (25,26). However, experimental verification of the hypothesis is needed. Butyrate has been shown to induce several types of GSTs in primary human colon cells (20). Recent studies have now shown that butyrate is also able to enhance expression of catalase but inhibits cyclooxygenase 2 and superoxide dismutase 2 (24). Figure 3 shows that there is an induction of catalase, determined both on mRNA level using real-time PCR and on enzyme activity level. This increased catalase activity could result in reduced concentration of its genotoxic substrate hydrogen peroxide (H2O2). In rat colon cells H2O2 is less genotoxic (see Fig. 4) in butyrate-pretreated cells than in the controls (27). It will now be of interest to determine whether butyrate pretreatment of human colon cells also results in a lower genotoxicity of H2O2 and how SFS are able to elicit similar effects.


Figure 3
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  		FIGURE 3  Modulation of catalase expression in primary human colon cells on mRNA level using real-time PCR (left side) and on protein level measuring enzyme activity (right side).

 

Figure 4
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  		FIGURE 4  Effects of a butyrate preincubation for 15 min on H2O2-induced DNA damage detected with the comet assay in colonic epithelial cells. Adapted from Abrahamse et al. (27).

 
In vivo studies

A number of studies report the effects of inulin-type fructans on chemically induced preneoplastic lesions (aberrant crypt foci) or tumors in the colon of rats and mice; these are reviewed in detail by Pool-Zobel (28). Thus, this present contribution only briefly summarizes the most important outcomes of these studies. Inulin-type fructans reduced tumor incidence in APCmin mice and reduced growth and metastasizing properties of implanted tumor cells in mice. The most pronounced effects were reported for inulin-type fructans (designed for favorable fermentation in the colon lumen) and especially longer-chain inulin components (optimal effectiveness at 10% wt:wt in diet), animals fed a high-fat Western-style diet, intervention together with probiotic bacteria (synbiotic preparations), and intervention throughout the whole carcinogenesis process (28). The effects have been reported to be associated with gut flora-mediated fermentation and production of butyrate. The results are meaningful according to the PASSCLAIM7 evaluation (26) because aberrant crypt foci are a valuable biomarker in rodents, providing a quantitative assessment of the development of colon cancer in this species. The presence of adenomas and adenocarcinomas, their size, and multiplicity are directly linked to cancer, and the final resulting mortality is a hard endpoint resulting from tumor progression. In conclusion, the studies on chemically induced preneoplasia and tumors in the colon of rats point to a clear-cut nontoxic effect of inulin-type fructans leading to a marked reduction of colon cancer incidence in animals exposed to the experimental colon carcinogens.

As a part of the SYNCAN-study this animal model was used to compare the efficacies of intervention with Synergy (prebiotic), Bifidobacterium lactis Bb12 plus Lactobacillus rhamnosus GG (probiotics), and the combination of both (synbiotic). Rats treated with Synergy as prebiotic or synbiotic had fewer carcinogen-induced tumors, both adenomas and cancers (29). The model was also used to validate the biomarker fecal water genotoxicity. For this, feces were obtained from azoxymethane-treated rats at 2, 4, and 8 mo after the beginning of the study. Fecal waters were prepared and analyzed for DNA-damaging potential using the single-cell microgelelectrophoresis "comet" assay (30). This study found a clear-cut reduction of genotoxicities of fecal waters from synbiotic-treated rats after 4 and 8 mo (Fig. 5). This biomarker is of interest, and the PASSCLAIM group concludes that cytotoxicity and particularly genotoxicity of fecal water have a good mechanistic link with colon carcinogenesis and hence provide potentially valuable noninvasive methods for assessing CRC risk in human subjects (26). However, there is a need for more extensive validation of these endpoints.


Figure 5
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  		FIGURE 5  Reduction of fecal water genotoxicity in azoxymethane-treated rats after intervention with synbiotics (30).

 
In the human intervention study, the synbiotic treatment resulted in a reduction of the DNA-damaging capacity of fecal water in polyp patients at the end of the intervention period but not in the cancer patients, as shown in Figure 6. The data had been previously reported to be nonsignificant with other statistical methods but here were reevaluated with a paired t-test (31). Another human study (32) detected a decline of toxic bile acids in fecal samples after a 3-mo intervention with oligofructoses, a finding that confirms some of our observations. Another related biomarker of interest measured in the human SYNCAN trial was the changes of DNA damage in colon cells of patients receiving the synbiotic intervention. Colonic biopsies were available from the same groups of patients from which fecal water had been obtained. The differences in the extents of DNA damage for polyp patients and for cancer patients are shown in Figure 7. Again, the polyp patients seem to profit more from the intervention because there was a clear reduction of DNA damage after synbiotic treatment but not after placebo administration. According to the PASSCLAIM diet-related cancer group, the determination of DNA damage provides a useful tool to investigate the effects of diet in different human tissues that are relevant for diet-associated tumor occurrence (26). The modulation of DNA damage also reflects reasonably well the modulated exposure to genotoxic compounds that cause the damage. Therefore, the reduction of DNA damage will indicate a reduced exposure, which in turn is related to a decrease of risk. The results may be more meaningful than those of the fecal water genotoxicity, and, together with the other data from this SYNCAN trial, they do indicate that the intervention is reducing exposure to genotoxic compounds in the gut.


Figure 6
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  		FIGURE 6  Fecal water genotoxicity in polyp patients after a 12-wk intervention with synbiotics (31). Fecal samples were obtained before, during, and after the intervention. The study included polypectomized and colon cancer patients.

 

Figure 7
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  		FIGURE 7  In the 12-wk randomized, double blind, placebo-controlled trial of a synbiotic food composed of Synergy 1 and the probiotics LGG and BB12, colorectal biopsies were taken before and after the intervention from colon cancer patients and polypectomized patients. DNA damage was measured in colon cells of the biopsies after intervention with synbiotics (31).

 
In conclusion, there are now data available that in vitro fermentation products of Synergy, one of the most effective inulin-type fructans, modulate parameters related to CRC initiation and progression in a favorable and beneficial way. In animal experiments in vivo, tumors are inhibited and fecal water genotoxicity is reduced after intervention. In humans, fecal water genotoxicity is also reduced, and, moreover, damage to colon cells is inhibited.

Thus, for the time being we may conclude "SYNCAN," meaning that SYNbiotic intervention CAN reduce exposure, which in turn is related to a decrease of colon cancer risks. In rats numerous studies show that it prevents the development of chemically induced colon tumors. Whether it can prevent CRC in humans will now have to be ascertained in long-term prospective studies with cancer development as an endpoint.


   FOOTNOTES
 
1 Published in a supplement to The Journal of Nutrition. Presented at the conference "5th ORAFTI Research Conference: Inulin and Oligofructose: Proven Health Benefits and Claims" held at Harvard Medical School, Boston, MA, September 28–29, 2006. This conference was organized and sponsored by ORAFTI, Belgium. Guest Editors for the supplement publication were Marcel Roberfroid, Catholique University of Louvain, Brussels, Belgium and Randal Buddington, Mississippi State University, USA. Guest Editor disclosure: M. Roberfroid and R. Buddington, support for travel to conference provided by ORAFTI. Back

2 Author disclosures: B. L. Pool-Zobel and J. Sauer, no conflicts of interest. Back

3 This work was supported by the EU-sponsored SYNCAN project (QLK-1999-346) and the German Research Foundation (DFG, PO284/8-1,2). Back

4 In these proceedings, the term inulin-type fructan shall be used as a generic term to cover all ß–(2<-1) linear fructans. In any other circumstances that justify the identification of the oligomers vs. the polymers, the terms oligofructose and/or inulin or eventually long-chain or high-molecular-weight inulin will be used, respectively. Even though the oligomers obtained by partial hydrolysis of inulin or by enzymatic synthesis have a slightly different DPav (4 and 3.6, respectively), the term oligofructose shall be used to identify both. Synergy will be used to identify the 30/70 mixture (wt:wt) of oligofructose and inulin HP, otherwise named oligofructose-enriched inulin. Back

5 Abbreviations used: CRC, colorectal cancer; GST, glutathione S-transferase; SFS, Synergy fermentation supernatant. Back

7 Process for Assessment of Scientific Support for Claims on Food. Back


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