Effects of butyrate on apoptosis in the pig colon and its consequences for skatole formation and tissue accumulation1

Abstract

Evidence exists that butyrate inhibits apoptosis of colon crypt cells in vivo so that less tryptophan from cell debris is available for skatole formation by microbes in the pig colon. In this study, potato starch containing a high proportion of resistant starch was fed to test the hypothesis that increased butyrate formation will occur in the colon and contribute to reduced epithelial cell apoptosis, thus leading to reduced skatole formation and absorption. Two groups of six barrows were provided with catheters in the jugular vein and fed either a ration with pregelatinized starch (high ileal digestibility; controls) or potato starch (low ileal digestibility; PS) as the main carbohydrate. All pigs were fed 31 MJ of metabolizable energy and 381 g of crude protein per day. The controls were fed for 19 d. The PS group received the same control ration for 10 d, and then changed to the PS ration. The total feeding period of PS consisted of a 5 d adaptation period followed by another 19 d. In the continously sampled feces, pH, short chain fatty acids, and skatole were determined. Skatole was additionally measured in blood plasma that was sampled daily. After killing barrows at the end of the feeding period, fat tissue for skatole measurement and colon tissue for histological quantification of mitosis and apoptosis were obtained. Feeding potato starch led to a rapid 2.2 fold increase of fecal butyrate when compared both with the control period of the PS group and the control group (P < 0.001). PS feeding resulted in a decrease in pH from 7.3 to 5.3 (P < 0.001) and apoptosis from 2.06 cells/crypt to 0.90 cells (P < 0.01), whereas there was no change in mitosis. Consequently, skatole decreased both in feces (controls vs PS group: 120.0 vs 1.9 microg/g; P < 0.001) and in blood plasma (1.6 vs 0.2 ng/mL; P < 0.001). The mean concentration of skatole in fat tissue was 167 ng/g tissue in controls, and below the detection limit (0.8 ng/g) in the PS group (P < 0.001). It is concluded that butyrate-dependent inhibition of apoptosis in the colon due to potato starch feeding efficiently inhibits skatole production in barrows. Because of the depressed skatole levels, improved sensory quality of pork is possible.

Is resistant starch protective against colorectal cancer via modulation of the WNT signalling pathway?

“…A similar earlier study also reported a reduction in apoptosis in the colon of pigs fed a potato starch diet and, interestingly, these researchers reported significantly higher faecal butyrate concentrations following the RS diet (81) .…”

Performances, meat quality and boar taint of castrates and entire male pigs fed a standard and a raw potato starch-enriched diet

“…In contrast, other researchers offered RPS for 2 or 3 weeks (Andersson et al, 2005;Lö sel and Claus, 2005;Zamaratskaia et al, 2005a) and obtained a complete wash-out of skatole from the adipose tissue; however, skatole concentration in the adipose tissue of control entire males was lower than in our study. Claus et al (2003) measured a marked reduction in the adipose tissue accompanied by minimal skatole levels in the faeces and very low levels in the plasma by day four after RPS feeding. The skatole breakdown in the liver can be efficient and fast as the half-life of skatole in the adipose tissue is about 12 h .…”

“…The production of skatole greatly depends on the composition of the diet and the intestinal microflora (Jensen et al, 1995;Claus et al, 2003). Important quantities of butyrate are produced when RPS is fermented in the large intestine (Martin et al, 2000;Mentschel and Claus, 2003), which reduces epithelial cell apoptosis .…”

In vitro production of short-chain fatty acids from resistant starch by pig faecal inoculum

“…In particular, acetate reaches muscle tissues where it contributes to energy supply, whereas propionate is converted to glucose in the liver . Finally, butyrate is considered as the most important SCFA that can stimulate development, growth and renewal of intestinal cells (Bach Knudsen et al, 2012) and can reduce epithelial cell apoptosis, thus leading to decreased skatole formation and absorption (Claus et al, 2003). Not only the amount of RS reaching the large intestine has great importance, but also its composition and physical structure may affect SCFA fermentation patterns (Brouns et al, 2002) and absorption (van der Meulen et al, 1997;Regmi et al, 2011).…”