Review | Published:

The bifidogenic effect of inulin and oligofructose and its consequences for gut health

European Journal of Clinical Nutrition volume 63, pages 12771289 (2009) | Download Citation

Abstract

The bifidogenic effect of inulin and oligofructose is now well established in various studies, not only in adult participants but also in other age groups. This bifidogenic shift in the composition of the colonic microbiota is likely the basis for the impact of these prebiotic compounds on various parameters of colonic function. Mainly from animal and in vitro studies and also from some human trials, there are indications, for instance, that inulin-type fructans may reduce the production of potentially toxic metabolites and may induce important immune-mediated effects. This review discusses how these changes in the composition and activity of the colonic microbiota may affect gut health in healthy people, including in those who may experience some form of gastrointestinal discomfort.

Introduction

The large intestine is one of the most densely populated ecosystems in nature. The number of microbes and the biodiversity of the intestinal microbiota are enormous. In scientific literature, estimates are between 500 and 1000 different bacterial species with a total weight of about 1.5 kg (Xu and Gordon, 2003). This may be an overestimation, and other experts estimate bacterial mass to be about 100–200 g wet weight (Cummings et al., 1987; Belenguer et al., 2008). Most of the species are difficult or impossible to cultivate, but with new analysis techniques based on nucleic acids, proteomics and metabolomics, more insight into the diversity, the genera involved, their metabolic activities, and their functions and effects on health of the host is being obtained.

Through these studies, it becomes more and more evident that the metabolism in the colon has a major impact on human physiology. The colon is not just an organ for absorption of water and salts, or for storage of undigested material, but instead the many microbial conversions of undigested material lead to a variety of important physiological effects. Among these conversions, the production of short-chain fatty acids (SCFA) through fermentation of non-digested carbohydrates has a predominant role. This fermentation not only leads to acetate, propionate and butyrate as the main SCFAs but also to lactate, an important intermediate in the formation of SCFA. These products of carbohydrate fermentation are thought to be beneficial to host health, whereas those of protein breakdown and amino acid fermentation, which include ammonia, phenols, indoles, thiols, amines and sulphides, are not (de Graaf and Venema, 2008). Therefore, PASSCLAIM, an EU programme that included the consensus of many experts, defined what it felt was a healthy, or balanced, flora as one that is predominantly saccharolytic, and comprises significant numbers of bifidobacteria and lactobacilli (Cummings et al., 2004). Non-digestible carbohydrates that are able to generate such a bifidogenic shift in the colonic microbiota are called prebiotics. Originally, prebiotics were defined by Gibson and Roberfroid (1995) as ‘non-digestible food ingredients that beneficially affect the host by selectively stimulating the growth and/or activity of one or a limited number of bacterial species in the colon, and thus improve host health’ ‘and well-being’ (Gibson et al., 2004).

Inulin, oligofructose or fructo-oligosaccharide (FOS) are the best studied prebiotics. Inulin is a generic term to cover all β(2–1) linear fructans, with a variable degree of polymerization. On account of the presence of the β(2–1) bonds, inulin is not digestible by digestive enzymes in the small intestine; it reaches the colon intact, wherein it is fermented to SCFA and gases by colonic bacteria. Chicory inulin shows a degree of polymerization of 2–60; its partial enzymatic hydrolysis product is oligofructose or FOS with a degree of polymerization of 2–10. FOS from sucrose is produced by the enzymatic transfer of fructosyl groups from sucrose. This product consists of short fructan chains up to a degree of polymerization of 5.

In this review, we present an overview of the effects of inulin and oligofructose from chicory on the composition and activity of the colonic microbiota as they emanate from studies with human volunteers. Next, we will discuss how these changes may affect gut health in healthy people. To put the results of different types of studies into perspective, we first discuss the possible relevance of changes in several biomarkers for gut health below.

The effects of these prebiotics in people with gut diseases (for example, see MacFarlane et al., 2008; Hedin et al., 2007; Heilpern and Szilagyi, 2008) are beyond the scope of this review.

Biomarkers for gut health

The potential benefits ascribed to the activity of the colon microbiota are listed in Table 1. The composition of the intestinal microbiota is characteristic of each individual, and there are large inter-individual variations (for example, see Zoetendal et al., 2006). Roughly, the intestinal bacteria can be divided into three categories (Figure 1) based on their potential pathogenic effects: (a) lactobacilli and bifidobacteria; (b) potentially pathogenic bacteria, such as certain species of clostridia, and (c) other commensal bacteria, such as Bacteroides, that may have both positive and negative features. Although definite evidence is lacking, it is generally assumed that a gut microbiota, in which lactobacilli and bifidobacteria dominates, is beneficial to health. The genera Bifidobacterium and Lactobacillus do not contain any known pathogens, and they are primarily carbohydrate-fermenting bacteria, unlike other groups such as Bacteroides and clostridia that are also proteolytic and amino acid fermenting. It should be noted that the composition and activity of the colonic microbiota are affected by several external factors, as depicted in Figure 2.

Table 1: Potential benefits of the intestinal microbiota
Figure 1
Figure 1

Schematic presentation of the most abundant species and genera of the human colonic microbiota. The numbers at the arrow indicate approximate numbers of the different genera (Log 10 scale per gram of faeces). *The harmful or beneficial effects of these bacteria or clusters are largely unknown. Cluster IV contains Ruminococcus spp. and Faecalibacterium prausnitzii, Cluster IX Veillonella spp. and Cluster XIVa Roseburia spp. Diagram adapted from Gibson and Roberfroid (1995) and Thomas and Flower (2006).

Figure 2
Figure 2

Factors affecting the composition and metabolic activity of the intestinal microbiota; based on data from Guigoz et al. (2008); Woodmansey (2007); Holdeman et al. (1976) among others.

Obviously, intestinal transit time, frequency of defecation and stool weight are important biomarkers of overall colonic function. In addition, there is a wide range of measurement techniques to monitor other markers of gut health, such as the measurement of changes in metabolite profile (SCFA, lactate; de Graaf and Venema, 2008), several parameters of colonization resistance against pathogens and the integrity of the intestinal lining or immunomodulation (Cummings et al., 2004; Albers et al., 2005). In addition, a battery of intermediate biomarkers for colon cancer is available, including the activity of certain faecal enzymes and the modulation of genotoxicity of faecal water (Klinder et al., 2004; Rafter et al., 2007). The scheme in Figure 3 represents the cascade of physiological effects that can be induced by consumption of either inulin-type fructans or probiotic bacteria or a combination of both, the so-called synbiotics. The various steps in this scheme show at which stages in this cascade of physiological events parameters are available as possible biomarkers. One of the hypotheses, for instance, is that a faster intestinal transit gives less opportunity for the formation of potentially harmful substances and for interaction with the intestinal cells (Pool-Zobel, 2005).

Figure 3
Figure 3

Microbiota-dependent mechanisms of physiological effects induced by inulin/oligofructose or probiotic bacteria. SCFA, short-chain fatty acids (acetate, propionate, butyrate); IBD, inflammatory bowel disease; IBS, irritable bowel syndrome. Adapted from Vos et al. (2007).

It is important to note that alterations in a single biomarker cannot provide definite proof of a health benefit or reduced risk of disease, but the evidence becomes stronger when data on various biomarkers—from different types of studies—are all in the same direction. Besides, various biomarkers can provide clues to the underlying mechanisms. Given the fact that gut-associated immune function is extremely complex and there are large inter-individual variations in many immune functions even among the healthy, caution should be taken in making general statements about the impact of changes in certain immune parameters. Combining markers with high and medium suitability is currently the best approach to measure immunomodulation in human nutrition intervention studies (Albers et al., 2005).

Effects on the composition and metabolic activity of the colon microbiota

Microbiota composition

An overview of studies in human volunteers on the effects of consumption of chicory-derived fructans on faecal microbiota composition is presented below. In these studies, changes in composition were detected both with classical plate-counting techniques (for example, see Gibson et al., 1995; Bouhnik et al., 2007) and with modern techniques based on reverse transcriptase PCR (for example, see ten Bruggencate et al., 2006) or fluorescent in situ hybridization (for example, see Kolida et al., 2007). The results are given for three groups: (a) infants, (b) adult participants and (c) elderly people (aged 65 and above). Details of studies in these three age groups are compiled in Tables 2, 3 and 4. When relevant, data from studies with oligofructose from sources other than chicory are mentioned in the text as well.

Table 2: Overview of studies on the effects of fructans from chicory on faecal flora composition in infants
Table 3: Effects of inulin or oligofructose from chicory on colonic microbiota composition in adult participants
Table 4: Effects of inulin or oligofructose from chicory on colonic microbiota composition in elderly participants

Infants

As can be seen in Table 2, most, but not all, studies in infants revealed bifidogenic effects with consumption of chicory-derived fructans at daily dosages ranging from 1.25 to 4 g, and in some of these studies, besides the increase in Bifidobacterium spp. an increase in Lactobacillus spp. and other favourable changes in microbiota composition were also noted. With a mixture of oligofructose and native inulin, a bifidogenic effect has been found in children aged about 6 months at a consumption rate of about 1.7 g/day (Brunser et al., 2006a), whereas for the same mixture applied in an enteral formula, there was no significant effect, but a trend towards an increase in numbers of bifidobacteria in paediatric cancer patients aged 1–12 years (Zheng et al., 2006). Another study showed significant bifidogenic effects in formula-fed babies of an average of 12 weeks of age, consuming 1.5 g/day of native inulin (Kim et al., 2007). A slightly lower dosage of native inulin of 1.25 g/day gave similar results in infants, aged about 8 months, after weaning (Yap et al., 2008). In the latter study also, a decrease in clostridia was observed at all dosages tested. Some studies using oligofructose did not show significant changes in faecal microbiota composition. In one study, on supplementation with 1 g/l FOS the number of Bifidobacterium was increased significantly after 1 week, but this effect did not persist after 3 weeks, and it also was not found with an intake of 3 g/l FOS (Euler et al., 2005). In a long-lasting study (up to 12 weeks) the investigators could not find any changes at a similar daily intake of oligofructose (Bettler and Euler, 2006). Other investigators also reported a non-significant trend towards bifidogenic effects in children aged 6–24 months consuming 2 g of oligofructose per day (Waligora-Dupriet et al., 2007).

Short-chain FOS from sucrose seemed to be ineffective for a bifidogenic effect in formula-fed babies in dosages up to 3 g/day (Guesry, 2000).

Many data regarding the prebiotic effects in formula-fed babies have been published for a 9:1 mixture of galacto-oligosaccharides (GOS) and long-chain inulin (confusingly called GOS/FOS mixture). There is one study with this mixture in which no significant differences in percentage of bifidobacteria were found (after 16 weeks) with a consumption level of 6 g/l (Bakker-Zierikzee et al., 2005), but all other studies do show the bifidogenic effect. One study in term infants consuming either 4 g/l or 8 g/l of this mixture in the formula indicated a dose-dependent increase in Bifidobacterium, whereas Lactobacillus changed with the same increase at both levels of intake (Moro et al., 2002). A number of studies reported that this prebiotic GOS/FOS mixture is able to induce a microbiota that closely resembles the microbiota of breast-fed infants, at the level of the different species of both Bifidobacterium and Lactobacillus (Knol et al., 2005; Rinne et al., 2005; Haarman and Knol, 2006). Scholtens et al. (2006a) showed that this also happens in older children during weaning, when the mixture was added to solid food. These authors speculated that GOS was responsible for growth stimulation of Bifidobacterium, whereas inulin stimulated the growth of Lactobacillus. One study with GOS alone showed it to elicit a bifidogenic effect in formula-fed babies when given in a dosage of 2.4 g/l (Ben et al., 2004).

Adult participants

A large number of studies in adult participants consistently show significant bifidogenic changes in the composition of the colonic microbiota after consumption of inulin or oligofructose from chicory (Table 3). The lowest dosage showing a bifidogenic effect was 5 g/day for inulin (Bouhnik et al., 2007; Kolida et al., 2007) and oligofructose (Menne et al., 2000; Rao, 2001) and 9 g/day for long-chain inulin (Harmsen et al., 2002). As a bifidogenic effect is also found with short-chain FOS from sucrose (for example, see Bouhnik et al., 2006), it seems to be independent of chain length.

Roberfroid et al. (1998) argued that the daily dose is not a determinant of the prebiotic effect, but the magnitude of the bifidogenic effect is mainly influenced by the number of bifidobacteria present in the colon before supplementation with the prebiotic begins. This seems to be the case in many studies with adult volunteers (Roberfroid et al., 1998; Tuohy et al., 2001a; Kolida et al., 2007; De Preter et al., 2008b) and infants (Kim et al., 2007; Yap et al., 2008). This phenomenon may explain why in a few studies no bifidogenic effects were observed, for instance, in a study using 10 g/day long-chain inulin (Bouhnik et al., 2004), whereas another study did show such an effect at 9 g/day of the same type of fructan (Harmsen et al., 2002). Moreover, one should realize that a small increase in log numbers may represent a large increase in numbers of bacteria: an increase from log 7 to log 8 represents a much smaller increase than that from log 9.2 to log 9.6. Therefore, it cannot be speculated which type of fructan (or for that matter, which type of prebiotic) is the most bifidogenic.

Not surprisingly, a bifidogenic effect can be found with inulin derived from chicory as well as from Jerusalem artichoke (Kleessen et al., 2007).

In some studies, a decrease in potentially pathogenic species, such as Clostridium spp., was also found (for example, see Gibson et al., 1995; Rao, 2001; see Table 3).

All data given above were obtained with faecal samples and thus are applicable for the bacteria present in the lumen of the colon. From the data by Langlands et al. (2004) it seems that inulin also has a bifidogenic effect on the mucosa-associated microbiota.

Elderly people

In elderly persons, the content of bifidobacteria decreases, whereas that of enterobacteria and clostridia increases (Hopkins and MacFarlane, 2002; Woodmansey, 2007). It might, therefore, be expected that in elderly, the bifidogenic effects of inulin could be more pronounced. As can be seen in Table 4, a bifidogenic effect is observed at roughly the same dosages as in younger adults, and in some—but not all—studies inulin consumption was found to affect other genera as well.

Inulin supplementation of 20 or 40 g/day has been shown to significantly increase the amount of bifidobacteria in constipated elderly women (Kleessen et al., 1997). This finding confirmed earlier data from a preliminary study in a group of eight constipated elderly men, taking 40 g of inulin per day (Kleessen et al., 1994). A bifidogenic effect was also reported in a study with patients suffering from antibiotic-associated diarrhoea. These patients consumed 12 g/day of oligofructose (Lewis et al., 2005b).

In healthy elderly participants, a combination of 6 g/day of an inulin/oligofructose mixture with two types of Bifidobacterium spp. was found to increase the total number of bifidobacteria in faecal samples (Bartosch et al., 2005). In another study, it was shown that 8 g/day of short-chain FOS from sucrose also caused an increase in Bifidobacterium spp. in patients admitted to nursing homes (Guigoz et al., 2002).

Although data are limited, it can be concluded that in elderly like in other age groups, the bifidogenic effect is probably not dependent on the chain length of the fructan. Data are too limited to conclude whether the order of magnitude of the bifidogenic effect is greater than that in younger people.

Metabolic activity of gut microbiota

Many studies show that concomitant with a bifidogenic change in the composition of the colon flora, the metabolic activity changes with consumption of inulin-type fructans. The available data on the effects on faecal metabolites and specific enzyme activities, and on several immune parameters are briefly summarizsed below. As explained above, it must be realized that the relevance of changes in various biomarkers for gut health is not fully understood.

Changes in faecal metabolites and enzyme activity

In experimental animal studies, it is well documented that inulin consumption leads to increased SCFA concentrations (Nilsson and Nyman, 2007). Supplementation with inulin has also been shown to increase bile acid secretion in rats (Levrat et al., 1994) and in hamsters (Trautwein et al., 1998).

A number of studies in human volunteers who consumed oligofructose in dosages varying from 13 to 20 g/day revealed an increase in faecal concentrations of lactate, (ten Bruggencate et al., 2006), acetate (van Dokkum et al., 1999), or total SCFA, acetate and propionate (Grasten et al., 2003). In one study (Causey et al., 2000), only a non-significant trend for increased acetate and total SCFA was found in faecal samples of volunteers consuming 20 g/day of inulin. It must be noted, however, that changes in these fermentation products are difficult to detect, as most of the SCFA will be absorbed from the colon (Belenguer et al., 2008). Not surprisingly, therefore, other investigators could not find changes in faecal SCFA concentrations after inulin consumption (Gibson et al., 1995).

With respect to bile acid secretion and inulin consumption, human data are only limited. A Korean study (Lee et al., 2004) reported a lowered deoxycholate concentration in faeces of postmenopausal women consuming 8 g/day of inulin, whereas van Dokkum et al. (1999) showed similar data in healthy men consuming 15 g/day of inulin or oligofructose.

Both in vitro and in vivo studies have shown that inulin can direct colon metabolic activity towards less proteolysis. With an in vitro model of the proximal colon, van Nuenen et al. (2003) showed that independent of chain length, inulin lowered the production of ammonia, p-cresol and iso-SCFA, especially in conditions when the colon pathogen Clostridium difficile was present.

In a human volunteer study with oligofructose-enriched inulin de Preter et al. (2007, 2008a) showed that together with an increase in faecal bifidobacteria, the production of colonic ammonia and p-cresol was reduced.

Faecal β-glucuronidase activity may be lowered after consumption of FOS from sucrose (Buddington et al., 1996) or inulin (Bouhnik et al., 2007; de Preter et al., 2008). Some reports also show a diminished activity of other enzymes, such as nitroreductase or glycocholic acid hydroxylase (Buddington et al., 1996). These data are not totally consistent, as with 12.5 g/day of FOS from sucrose, no change in nitroreductase, azoreductase or β-glucuronidase was found (Bouhnik et al., 1996b), and in another study in elderly participants consuming 20 or 40 g/day of inulin, no effects on β-glucuronidase or β-glucosidase were observed (Kleessen et al., 1997). The impact of these changes in enzyme activity in relation to gut health is not clear, but it has been suggested that these enzymes are involved in the conversion of procarcinogens into carcinogens.

In a series of publications, ten Bruggencate et al. (2004) reported that oligofructose and inulin consumption in rats caused an increase in cytotoxicity of faecal water. The physiological relevance of these findings remains to be clarified, as in human trials, consumption of oligofructose at 20 g/day (ten Bruggencate et al., 2006) or more (up to 30 g/day; Scholtens et al., 2006b) did not affect the cytotoxicity of faecal water and intestinal permeability.

Effects on immune parameters

Both animal and human studies suggest that inulins may have immune-modulatory effects, but so far data are limited and the results should be interpreted carefully.

A clear outcome of animal studies is that the intestinal immune system and, especially, the immune cells associated with the Peyer's patches are responsive to a dietary supplement of inulin/oligofructose and/or their metabolites (Seifert and Watzl, 2007). For instance, it has been shown that inulin supplementation of rat feed leads to increased production of IL-10 and interferon-gamma from Peyer's patches (Roller et al., 2004). This may be related to a fermentation product of inulin, as it has been reported that butyrate suppresses lymphocyte proliferation, reduces cytokine expression and enhances IL-10 production in rats. However, as Peyer's patches are located in the small intestine, whereas fructans are fermented mainly in the large intestine, it could be speculated that microbiota-independent mechanisms may also have a role in the observed effects (Vos et al., 2007).

Data from a recent trial in mice suggest that a diet supplemented with an inulin/oligofructose mixture stimulates mucosal immunity and seems to improve the efficacy of an oral Salmonella vaccine (Benyacoub et al., 2008). The combined application of inulin/oligofructose with two probiotic bacterial species was found to induce different effects from those of the individual supplements, but it did not simply result in additive or synergistic effects on intestinal immune functions in rats (Roller et al., 2004).

According to Seifert and Watzl (2007), the first results from human intervention studies suggest that the intake of inulin and oligofructose has beneficial effects on the gut-associated lymphoid tissue. At the level of the systemic immune system, however, only minor effects have been observed in healthy adult human participants. In contrast, data from studies in infants suggest that supplementation with a prebiotic mixture positively affects postnatal immune development and increases faecal secretory IgA. The effects on immunological processes at the level of the gut-associated lymphoid tissue may be associated with significant health benefits in infants and in patients with intestinal inflammatory diseases.

Immune modulation in infants

The limited human data on the antiallergic potential of inulin/oligofructose are based on the GOS/FOS mixture described earlier (Niers et al., 2007). Moro et al. (2006) showed a reduced incidence of atopic dermatitis in children administered this prebiotic mixture during the first 6 months of life. However, according to a Cochrane review (Osborn and Sinn, 2007) data are too limited to draw firm conclusions. Further trials are needed to determine whether the reduction in eczema that has been reported in high-risk infants is reproducible and whether it would persist over a longer period of time.

The results of a vaccination study in 8-month-old infants are also interesting. Infants who received 1 g of a 30/70 mixture of native inulin and oligofructose in 25 g cereal for 10 weeks showed higher IgG antibody titres after measles vaccination compared with the control group that did not receive the prebiotic. To further elucidate the mechanism by which prebiotics change the immune response after vaccination, studies on cellular immune reaction and with different types of vaccines are needed (Haschke et al., 2001).

In a review on the efficacy of inulin and oligofructose in paediatric applications, Veereman (2007) concludes that the bifidogenic effect probably is not the only mechanism involved, but it may be key to important immune-mediated effects.

Immune modulation in elderly people

Guigoz et al. (2002) noted that with the consumption of 8 g/day of FOS from sucrose, some inflammatory response markers decreased. In healthy elderly people, they showed a decreased phagocytic activity of granulocytes and monocytes, as well as a decreased expression of interleukin-6 mRNA in peripheral blood monocytes after 3 weeks of FOS consumption. In a later study by the same research group, these changes in immune parameters were confirmed with supplementation of 2–4 g/day FOS for 12 weeks in a group of older persons at risk of malnutrition (Schiffrin et al., 2007).

Bunout et al. (2002) investigated the effect of prebiotics on the response to vaccination in elderly. A mixture of inulin and oligofructose (70/30; 6 g/day) did not lead to a changed immunological response in the volunteers aged >70 y. No changes in secretory IgA could be found, nor an effect on the antibody titre after vaccination with influenza or pneumococcal vaccines.

Possible role of inulin and oligofructose in alleviating gastrointestinal discomfort

We discuss the results from studies with healthy human volunteers—without medication—who may experience some form of gastrointestinal discomfort below.

People with a low defecation frequency (mildly constipated participants)

Constipation is a widespread phenomenon in western populations, especially in women and in the elderly (Higgins and Johanson, 2004; Peppas et al., 2008).

Recent data from studies with infants show that oligofructose increases stool frequency (Euler et al., 2005) and/or leads to softer stools (Moore et al., 2003; Bongers et al., 2007), whereas inulin consumption in formula-fed babies had a positive effect on stool mass at a consumption of about 1.5 g/day with a trend for softer consistency (Kim et al., 2007). The same effects have been reported for the GOS/FOS mixture, as described by Knol et al. (2005).

Consumption of GOS also led to a higher frequency of defecation and a lower faecal pH in formula-fed babies (Ben et al., 2004).

A number of studies in constipated adult participants report favourable results with supplementation of inulin. Native inulin at 20 g/day was shown to increase stool frequency (Causey et al., 2000), whereas a comparable effect was found in two other studies using long-chain inulin at a consumption level of 15 g/day (den Hond et al., 2000) or 10 g/day FOS (Chen et al., 2000). A study involving 35 elderly constipated persons also showed significantly improved stool frequency. Stools were soft, but diarrhoea was not observed. Furthermore, all patients reported the absence of nausea and headaches, complaints that often accompany constipation (Kleessen et al., 1997). According to Elia and Cummings (2007) these favourable results are surprising, as the meta-analysis of studies in healthy participants revealed no significant increase in stool output for a range of prebiotics. In contrast, one study in nine healthy young men did show an increase in daily stool output with a high consumption level of inulin (50 g/day). The increase in stool output could be ascribed to a significant increase in faecal bacterial weight and to a significant increase in water content (Castiglia-Delavaud et al., 1998).

It seems therefore that the stool bulking effect of inulin or oligofructose is rather low (see also Salminen et al., 1998), and that the improved bowel habits are based on other features such as softer stool consistency and increased stool frequency.

People with a higher risk of gastrointestinal infection

Diarrhoeal diseases in children

Duggan et al. (2003) could not find an effect on diarrhoea prevalence from oligofructose consumption in Peruvian infants. The investigators suggested that children who are already receiving oligosaccharides through breast milk may experience no further benefit. An investigation in Indonesia seems to indicate that prebiotic consumption may have a positive effect on the risk and duration of diarrhoeal infections in infants (Widjojo et al., 2006), but the data are not totally consistent and firm conclusions cannot be drawn. In another Indonesian study in children aged 1–14 years, consumption of FOS from sucrose (2.5–5 g/day) shortened the duration of diarrhoeal episodes, and stools had a lower pH, indicative of increased fermentation and formation of SCFA (Juffrie et al., 2007).

In a clinical trial using a synbiotic preparation of inulin in combination with soy polysaccharides and L. rhamnosus, duration of diarrhoea was found to be shortened in children suffering from acute diarrhoea. Whether this effect can be attributed to the prebiotic, probiotic or both, is impossible to say. The extra consumption of iron and zinc also complicates the drawing of unequivocal conclusions (Agustina et al., 2007).

Interestingly, a recent prospective, placebo-controlled trial in which healthy term infants with a parental history of atopy who were fed either GOS/FOS (8 g/l)- or placebo-supplemented hypoallergenic formula, showed a reduced number of infectious episodes and reduced incidence of recurring, particularly respiratory, infections during the first 6 months of life (Arslanoglu et al., 2007). A follow-up study showed that this effect persisted for a year without dietary intervention (Arslanoglu et al., 2008). The authors speculate that an immune modulating effect through the bifidogenic change in faecal microbiota composition may be responsible for this prolonged protective effect.

Travellers’ diarrhoea

Episodes of diarrhoea are often associated with travel to high-risk areas (in Central America, the Far East, India and parts of Africa). Current estimates are that 60 million travellers from the West visit high-risk areas annually, and 30–50% of these have episodes of diarrhoea. Cummings et al. (2001) reported that 10 g oligofructose daily alone could not prevent traveller's diarrhoea. Participants reported less episodes of diarrhoea, but the difference with the control group was not significant (P=0.08). Later analysis showed that those participants taking oligofructose experienced less severe attacks of diarrhoea than the placebo group (MacFarlane et al., 2006). Interestingly, a post-study questionnaire revealed that participants taking oligofructose noticed significant improvement in well-being during their holiday, although they reported more flatulence.

Conclusions

The bifidogenic effect of inulin and oligofructose—when taken in relatively small amounts of around 5–15 g/day—is well established in different age groups. The bifidogenic effect seems to be independent of chain length of inulin-type fructans and a clear dose–response relationship has not been found. The order of magnitude of the bifidogenic response is likely to be more dependent on the initial number of bifidobacteria before the supplementation is started. Apart from the bifidogenic shift in the composition of the colon microbiota, there is emerging evidence—mainly from animal and in vitro studies and also from some human studies—for the potential of inulin to influence colonic function. There are indications to support the hypothesis that inulin-type fructans may reduce the production of potentially toxic metabolites by suppressing specific enzyme activities in the colon. In addition, they may increase the concentration of compounds that could be beneficial for the host.

There are also indications for a beneficial influence of inulin-type fructans on gut health and well-being, and the data for improved bowel habit require further substantiation. Similarly, the positive effect of these fructans on immunological processes needs further support. Preliminary data suggest, for instance, that a prebiotic mixture may reduce the incidence of atopic dermatitis in infants, as well as have favourable effects in young children at risk of diarrhoeal disease and in adult people suffering from travellers’ diarrhoea. The bifidogenic effect probably is not the only mechanism involved, but it may be the key to important immune-mediated effects. Available data are too limited, however, to draw firm conclusions. Clearly, further research is needed, not only to see whether the promising data can be confirmed and quantified in different target groups but also to get a clear picture of the physiological meaning of changes in faecal enzyme activity and in various immune parameters.

Conflict of interest

D Meyer is employed as a scientific and regulatory affairs manager with Sensus, a manufacturer of inulin and oligofructose, and M Stasse-Wolthuis has carried out consultancy work for Sensus, as well as for other food companies and non-governmental organizations.

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Acknowledgements

This paper is based on the results of an international workshop held in Utrecht on 29 and 30 November 2007. We wish to thank Chairman Professor Joseph Hautvast and all the participants. We are especially grateful to Professor John Cummings and Professor Ian Rowland for the detailed comments they provided on the earlier manuscript.

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  1. Sensus, Roosendaal, The Netherlands

    • D Meyer
  2. Stasse Consultancy, Udenhout, The Netherlands

    • M Stasse-Wolthuis

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https://doi.org/10.1038/ejcn.2009.64

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