Contrasting effects of viscous and particulate fibers on colonic fermentation in vitro and in vivo, and their impact on intestinal water studied by MRI in a randomized trial

TY - JOUR

T1 - Contrasting effects of viscous and particulate fibers on colonic fermentation in vitro and in vivo, and their impact on intestinal water studied by MRI in a randomized trial

AU - Gunn, David

AU - Murthy, Rajani

AU - Major, Giles

AU - Wilkinson-Smith, Victoria

AU - Hoad, Caroline

AU - Marciani, Luca

AU - Remes-Troche, Jose

AU - Gill, Sammie

AU - Rossi, Megan

AU - Harris, Hannah

AU - Ahn-Jarvis, Jennifer

AU - Warren, Fred

AU - Whelan, Kevin

AU - Spiller, Robin

PY - 2020/9/1

Y1 - 2020/9/1

N2 - BACKGROUND: Wheat bran, nopal, and psyllium are examples of particulate, viscous and particulate, and viscous fibers, respectively, with laxative properties yet contrasting fermentability. OBJECTIVES: We assessed the fermentability of these fibers in vitro and their effects on intestinal function relevant to laxation in vivo using MRI. METHODS: Each fiber was predigested prior to measuring gas production in vitro during 48-h anaerobic incubation with healthy fecal samples. We performed a randomized, 3-way crossover trial in 14 healthy volunteers who ingested 7.5 g fiber twice on the day prior to study initiation and once with the study test meal. Serial MRI scans obtained after fasting and hourly for 4 h following meal ingestion were used to assess small bowel water content (SBWC), colonic volumes, and T1 of the ascending colon (T1AC) as measures of colonic water. Breath samples for hydrogen analysis were obtained while patients were in the fasted state and every 30 min for 4 h following meal ingestion. RESULTS: In vitro, the onset of gas production was significantly delayed with psyllium (mean ± SD: 14 ± 5 h) compared with wheat bran (6 ± 2 h, P = 0.003) and was associated with a smaller total gas volume (P = 0.01). Prefeeding all 3 fibers for 24 h was associated with an increased fasting T1AC (>75% of values >90th centile of the normal range). There was a further rise during the 4 h after psyllium (0.3 ± 0.3 s P = 0.009), a fall with wheat bran (-0.2 ± 0.2 s; P = 0.02), but no change with nopal (0.0 ± 0.1 s, P = 0.2). SBWC increased for all fibers; nopal stimulated more water than wheat bran [AUC mean (95% CI) difference: 7.1 (0.6, 13.8) L/min, P = 0.03].Breath hydrogen rose significantly after wheat bran and nopal but not after psyllium (P < 0.0001). CONCLUSION: Both viscous and particulate fibers are equally effective at increasing colonic T1 over a period of 24 h. Mechanisms include water trapping in the small bowel by viscous fibers and delivery of substrates to the colonic microbiota by more fermentable particulate fiber. This trial was registered at clinicaltrials.gov as NCT03263065.

AB - BACKGROUND: Wheat bran, nopal, and psyllium are examples of particulate, viscous and particulate, and viscous fibers, respectively, with laxative properties yet contrasting fermentability. OBJECTIVES: We assessed the fermentability of these fibers in vitro and their effects on intestinal function relevant to laxation in vivo using MRI. METHODS: Each fiber was predigested prior to measuring gas production in vitro during 48-h anaerobic incubation with healthy fecal samples. We performed a randomized, 3-way crossover trial in 14 healthy volunteers who ingested 7.5 g fiber twice on the day prior to study initiation and once with the study test meal. Serial MRI scans obtained after fasting and hourly for 4 h following meal ingestion were used to assess small bowel water content (SBWC), colonic volumes, and T1 of the ascending colon (T1AC) as measures of colonic water. Breath samples for hydrogen analysis were obtained while patients were in the fasted state and every 30 min for 4 h following meal ingestion. RESULTS: In vitro, the onset of gas production was significantly delayed with psyllium (mean ± SD: 14 ± 5 h) compared with wheat bran (6 ± 2 h, P = 0.003) and was associated with a smaller total gas volume (P = 0.01). Prefeeding all 3 fibers for 24 h was associated with an increased fasting T1AC (>75% of values >90th centile of the normal range). There was a further rise during the 4 h after psyllium (0.3 ± 0.3 s P = 0.009), a fall with wheat bran (-0.2 ± 0.2 s; P = 0.02), but no change with nopal (0.0 ± 0.1 s, P = 0.2). SBWC increased for all fibers; nopal stimulated more water than wheat bran [AUC mean (95% CI) difference: 7.1 (0.6, 13.8) L/min, P = 0.03].Breath hydrogen rose significantly after wheat bran and nopal but not after psyllium (P < 0.0001). CONCLUSION: Both viscous and particulate fibers are equally effective at increasing colonic T1 over a period of 24 h. Mechanisms include water trapping in the small bowel by viscous fibers and delivery of substrates to the colonic microbiota by more fermentable particulate fiber. This trial was registered at clinicaltrials.gov as NCT03263065.

KW - Bran

KW - Colon

KW - Fiber

KW - Intestine

KW - MRI

KW - Nopal

KW - Psyllium

KW - Water

UR - http://www.scopus.com/inward/record.url?scp=85090175631&partnerID=8YFLogxK

U2 - 10.1093/ajcn/nqaa173

DO - 10.1093/ajcn/nqaa173

M3 - Article

C2 - 32619212

AN - SCOPUS:85090175631

SN - 0002-9165

VL - 112

SP - 595

EP - 602

JO - The American journal of clinical nutrition

JF - The American journal of clinical nutrition

IS - 3

ER -