A substantial proportion of patients in the gastroenterology clinic relate their symptoms to intestinal gas. Typically bloating, abdominal distension, and flatulence are attributed to intestinal gas. Studies showed that 15%–20% of the general population in US and Europe experience these symptoms [1
] and the proportion increases up to 90% in patients with functional digestive symptoms, i.e., without detectable abnormalities by conventional testing, particularly in patients with irritable bowel syndrome (IBS) [3
]. Since the cause of these symptoms is uncertain, the current treatments are of limited efficacy [4
Most of the gas in the digestive tract is produced in the colon by intestinal microbiota in the process of fermentation of meal residues that escape small bowel absorption [5
]. Particularly, it has been shown that some food components, such as resistant starches, cellulose, or pectins, are incompletely absorbed in the small bowel and enter the colon [6
]. The physiological role of the different gases and volatile compounds produced by colonic microbiota is incompletely understood, but some products of fermentation play a positive role as anti-inflammatory, anti-oxidative, and neuroprotective agents.
Within subjects, the volume of gas output varies in relation to the diet [9
]. However, there is a great inter-individual variability, and gas evacuation in subjects maintained on a similar diet may differ substantially. This depends mainly on the composition and metabolic activity of the individuals’ colonic microbiota [5
]. Hence, the volume of gas production and anal evacuation is determined by two main factors: the diet, particularly the amount of fermentable residues reaching the colon, and the individual composition and activity of the colonic microbiota. Indeed, human gut microbiota encodes for a large variety of carbohydrate-active enzymes [10
] and this may vary between subjects.
A previous study [9
] showed that a diet rich in fermentable residues significantly increased the volume and the number of anal gas evacuations, and induced gas-related symptoms in healthy subjects. This challenge diet included legumes among other high-residue foodstuffs. Legumes contain high levels of indigestible alpha-galactosides that are exclusively fermented by resident microbiota, releasing gas [11
A fermented milk product containing Bifidobacterium animalis
CNCM I-2494 and lactic acid bacteria has been shown to improve symptoms and well-being in women with mild digestive complaints [12
], and to improve bloating, digestive discomfort, and reduce abdominal distension in IBS-C patients [16
]. The response to this product seems to be related to the metabolic activity of the gut microbiota [18
In the present study, we hypothesized that a fermented milk product containing the same B. lactis CNCM I-2494 and lactic acid bacteria may reduce subjective and objective components of flatulence in healthy subjects challenged by a diet rich in fermentable residues.
Our pilot, proof-of-concept study indicates that consumption of a fermented milk product with B. lactis CNCM I-2494 and lactic acid bacteria may improve the tolerance of a challenge diet rich in fermentable residues in healthy subjects, suggesting that probiotics may render healthy individuals more resilient to dietary diversions.
As in previous studies [9
], healthy subjects without digestive symptoms on their habitual diet became symptomatic when challenged with a flatulogenic diet. The challenge diet induced predominant symptoms that are commonly attributed to intestinal gas, such as abdominal bloating, distension, and flatulence, and had also a negative impact on digestive well-being. These sensations were associated with a substantial increase in the number of anal gas evacuations measured by an event marker. This method has been previously used with reproducible and consistent results [9
]; furthermore, it was shown that marked evacuations exhibited a very good correlation with direct recording of anal gas outflow obtained simultaneously (R > 0.95; p
< 0.05) [25
]. The effects of the challenge diet increased over the 3-days administration period, as opposed to the stability of repeated measurements on the habitual diet in the pretreatment phase; however, the daily increments became gradually smaller conceivably tending towards a plateau with longer administration. The challenge diet did not affect normal bowel habit; a similar result was observed in a previous study showing that a 3-day high-residue diet increased the fecal output, a parameter not measured in the present study, without changes in stool frequency and consistency [26
It has been shown that patients with functional gut disorders complaining of gas-related symptoms exhibit the same symptoms and also a number of anal gas evacuations above the normal range [9
]; hence, the challenge diet in healthy subjects to some extent mimicked this clinical condition.
This experimental model of gut discomfort was used in the present study to test the effect of a fermented milk product with B. lactis CNCM I-2494 and lactic acid bacteria in healthy subjects. In this model, consumption of the FMP over a 4-week period had a positive impact on the 3 parameters that were affected by the challenge diet: the FMP reduced gas-related symptoms, reduced the number of anal gas evacuations, and improved digestive well-being. The FMP induced these effects without affecting normal bowel habit in healthy subjects, a response analogous to that of the challenge diet.
In previous studies, the effect of different dietary interventions on intestinal gas production was detected by changes in the number of daily anal gas evacuations measured over several days, as well as by changes in the volume of gas evacuated per anus measured during the postprandial period after a probe meal [9
]. In the present study, the FMP reduced the number of anal gas evacuations, but no effect on the gas volume evacuated after the probe meal was detected, conceivably because the probe meal had a high content of residues, and the potential effect of probiotics was overflown by the abundance of fermentable substrates within the colonic biomass. Proof of a modulatory effect of a FMP with the same B. lactis
CNCM I-2494 on intestinal gas production was provided by a previous study showing a reduction in postprandial hydrogen breath excretion after a nutrient meal containing lactulose in IBS patients [18
No differences in the volume of intestinal gas measured by abdominal MRI were detected during the FMP administration. In a previous study, 3-day dietary interventions comparing high-fiber (35 g/d) versus low-fiber (8 g/d) diets did not result in significant changes in colonic gas volume measured by MRI during fasting [26
]. Intestinal gas homeostasis is tightly regulated to maintain the volume of intraluminal gas constant under different conditions. Indeed, over 70% of the gas produced in the process of microbiota fermentation of meal residues is absorbed into the blood and eliminated by breath [28
], and another part of the gas produced is disposed by gas-consuming microorganisms [5
In a previous study, a FMP with B. lactis
CNCM I-2494 reduced the Prevotella/Bacteroides
ratio metabolic potential in IBS patients [18
]. These results were not reproduced in the present study using a different dietary challenge in healthy subjects. However, we identified some bacterial genera that were potentially associated with the reduction in symptoms and anal gas evacuations during FMP consumption. Some of these specific genera are linked with the metabolism of hydrogen, including Methanobrevibacter
, and Desulfovibrionaceae
that might reflect a trade-off in the balance between gas-producing and gas-consuming microorganisms. For these analyses, we applied first machine learning to evaluate whether microbiota features could predict flatulence variation; then, we evaluated the most important features with Spearman correlation. We acknowledge that the microbial signal is weak and this could be related to the two sets of statistical methods used. Furthermore, our results must be considered only as hypothesis generating since no multiplicity adjustments were performed according to the exploratory nature of the study.
The reduction of symptoms and changes in the gas evacuation pattern associated to FMP administration could be not only related to microbiota metabolism of intraluminal substrates, but also to an effect of probiotics on gut sensitivity and/or on the handling of contents. A FMP with the same B. lactis
CNCM I-2494 was previously shown to reduce visceral sensitivity to colorectal distension in a rat model [29
] and to modulate the activity of brain regions that control central processing of emotion and sensation in healthy women [30
]; furthermore, the same product accelerated orocecal and colonic transit in patients with IBS-C along with a reduction in symptoms and objective abdominal distension [16
We acknowledge that in the absence of a control arm, a possible placebo effect on subjective perception cannot be excluded. However, participants were not aware of the potential effects, whether beneficial or deleterious, that the challenge diet or the FMP could produce.