Psyllium husk, derived from the seeds of Plantago ovata
, consists of highly branched and gel-forming arabinoxylan, a polymer rich in arabinose and xylose which has limited digestibility in humans. However, several members of the intestinal microbiota can utilize these oligosaccharides and their constituent sugars as an energy source [1
], and therefore, psyllium can be considered to have prebiotic potential. In general, the health-promoting effects of prebiotics include supporting the growth of bacteria beneficial to the host and increasing the production of short-chain fatty acids (SCFA) such as butyrate and propionate previously shown to be positive for colonic health [6
]. Another property of psyllium is that it is capable of retaining water in the small intestine, and thereby, increasing water flow into the ascending colon. The resulting increase in the fluidity of colonic content may explain the success of psyllium husk in treating constipation [7
]. In addition to the relief of symptoms through softening of stool and increasing stool frequency, the increase of free water alters the environmental conditions of the colon.
The effects of psyllium husk on host physiology have already been described, however, the effect that it has on the microbial ecosystem has not been well characterised. The effect of psyllium on microbial composition has been studied in an in vitro model mimicking the healthy intestine where it was shown that the microbial composition was not strongly affected. [10
] However, there was an indication that the bacterial fermentation of fibres increased colonic levels of SCFAs. Moreover, a recent trial observed that psyllium supplementation protected mice from colitis by reducing the inflammatory response. This response was found to be largely microbiota dependent [11
In this study, we aimed to determine the effect of psyllium husk supplementation on the intestinal microbiota of both healthy subjects and patients with chronic idiopathic constipation using two separate randomised, placebo-controlled intervention studies. The samples for this study come from two linked, published clinical trials [12
] where the effect of psyllium husk on colonic volume and intestinal water content was tested on first healthy adult subjects and then adults with chronic constipation. Here, we built on the results reported previously by concentrating on the microbial composition alterations introduced by psyllium supplementation. We aimed to understand how altered gut environmental conditions induced by psyllium husk affected the microbiota composition. Here, we showed that in healthy controls there was a very small change in the microbiota, however, there was a larger change in the microbial composition of the constipated patients.
In this study, we utilized two clinical trials to investigate the effects of psyllium husk ingestion on the faecal microbiota composition of both healthy controls and patients with idiopathic constipation [12
]. We showed that the environmental changes (change in transit time, faecal water content and the concentration of SCFAs) introduced by the psyllium husk were substantial in both patient groups. However, the healthy subjects showed very little change in their faecal microbial composition, whereas several key members of the microbial ecosystem were altered in the constipated patients.
There were detectable microbial differences between healthy and constipated patients at baseline, including significantly higher levels of Desulfovibrio
ssp. in the constipated patients. Interestingly, in a recent study, a member of the Desulfovibrio
genus was shown to reduce transit in an in vivo model [17
]. It has also been shown that this taxon produces hydrogen sulphide, which is known to decrease inflammation in the GI tract and to inhibit motility [18
]. The association of Desulfovibrio
spp. with constipated patients is a new finding that may be followed up by studies on the relevance of this organism to GI health and its effect on orchestrating motility.
Another genus level taxon that showed significant difference between the study groups was Lachnospira
, with an over four-fold higher level in the healthy than in the constipated subjects. Additionally, we detected a significant increase of this taxon in these patients after psyllium supplementation and we found positive associations between increased faecal water content and acetate levels. It is known that several members from Lachnospira
genus are capable of producing lactate and acetate. Lactate may be further metabolized into butyrate or propionate. It has been shown that low concentration of butyrate contributes to constipation by inhibiting mucin secretion [20
]. Therefore, decreased levels of these SCFAs produces could contribute to the disease state of constipation.
Psyllium husk has long been used as a treatment for constipation; however, the changes it produces in the composition of the intestinal microbiota have so far not been addressed. We showed that the intestinal microbiota composition of healthy individuals was less affected by the psyllium supplementation than those of the constipated patients. This is in line with previous findings on psyllium supplementation [21
] as well as the general understanding where the microbial composition of healthy subjects is regarded to be resistant to environmental changes [22
]. It should be noted that the constipated patients had a larger environmental change, as reflected by the change in colonic T1, an Magnetic Resonance Imaging (MRI) time constant reflecting fluidity of the colonic chyme [12
], than the healthy subjects; the degree of microbial change may be a reflection of this. We showed that in both studies there was an increase of Veillonella
, an organism typically more abundant in the small intestine [23
]. There were also changes in other small intestinal taxa [24
], such as Sutterella
(belonging to the Proteobacteria phylum), which increased in abundance after psyllium supplementation in the constipated subjects. Sutterella
bacteria are slow growing organisms [25
], and therefore, their higher abundance with faster transit could be an indication that these bacteria are washed out of the small intestine and become detectable in greater numbers in faeces. Therefore, we hypothesize that the increase in both of these bacterial taxa is secondary to the supplementation of psyllium and change in the colonic environment rather than increased colonic growth of the bacteria belonging to these taxa.
The supplementation of psyllium significantly increased the numbers of commensals such as Phascolarctobacterium
] and Faecalibacterium
] in the constipated patients. These same organisms have also been shown to have increased abundance after consumption of a polydextrose fibre [29
have also been previously associated with faster colonic transit [30
] and Faecalibacterium
with loose stools [31
]. In our study, the increase in Faecalibacterium
was also associated with higher stool water content and the increase of both Phascolarctobacterium
with larger amounts of acetate in stools. Interestingly, Faecalibacterium
converts sugars and acetate into butyrate–an important molecule for intestinal health used by the colonocytes as an energy resource. The favourable change in the acetate concentration may be explained by the increase in abundance of these genera.
Another bacterial genus affected by the psyllium supplementation in the constipated patients was Christensenella
, which decreased almost two-fold in abundance after psyllium treatment. Previously, Christensenella
had been associated with hard stools [31
], and interestingly, we were able to show a similar trend, since in our study, this genus was negatively associated with increased faecal water content.
In conclusion, we showed that consumption of psyllium husks introduced small but significant changes in the intestinal microbiota of both healthy and constipated patients. This change was more pronounced in the constipated patients. Organisms associated with intestinal short-chain fatty acid production such as Faecalibacterium ssp. were increased, an effect that suggests a potential health benefit from psyllium supplementation. Several candidate mechanisms for such an effect were present, such as changes in gut transit and increased intestinal water content. These data support potential health benefits for such mechanisms in addition to their role in the relief of constipation symptoms.