The sweet life: diet sugar concentration influences paracellular glucose absorption

Abstract

Small birds and bats face strong selection pressure to digest food rapidly in order to reduce digesta mass carried during flight. One mechanism is rapid absorption of a high proportion of glucose via the paracellular pathway (transfer between epithelial cells, not mediated by transporter proteins). Intestinal paracellular permeability to glucose was assessed for two nectarivorous passerines, the Australian New Holland honeyeater (Phylidonyris novaehollandiae) and African white-bellied sunbird (Cinnyris talatala) by measuring the bioavailability of radiolabelled, passively absorbed L-glucose. Bioavailability was high in both species and increased with diet sugar concentration (honeyeaters, 37 and 81% and sunbirds, 53 and 71% for 250 and 1000 mmol l L1 sucrose diets, respectively). We conclude that the relative contribution of paracellular to total glucose absorption increases with greater digesta retention time in the intestine, and paracellular absorption may also be modulated by factors such as intestinal lumen osmolality and interaction with mediated glucose uptake. The dynamic state of paracellular absorption should be taken into account in future studies.

Mistletoebirds and Xylose: Australian Frugivores Differ in Their Handling of Dietary Sugars

“…Silvereyes and singing honeyeaters showed greater bioavailability of both l-glucose and d-xylose on the more concentrated diet, where slower gut passage time would promote increased absorption via the paracellular route (likely because of increased contact time of digesta with absorptive surfaces), as has been previously described in three specialized nectarivores to date (McWhorter et al 2006;Napier et al 2008b). On the other hand, mistletoebirds did not vary f with diet concentration for either sugar.…”

“…Paracellular absorption provides a nonsaturable absorptive mechanism that matches absorption capacity to acute changes in dietary nutrient concentration (Afik et al 1997;Ferraris 2001). The relative contribution of paracellular to total glucose absorption in nectarivorous birds increases with an increase in diet sugar concentration, an effect that may be largely due to increased digesta retention time of more energy-dense nectars in the intestine (McWhorter et al 2006;Napier et al 2008b). Frugivorous birds and bats also rely extensively on the paracellular pathway for the absorption of glucose McWhorter et al 2010), but the effects of diet energy density and thus digesta transit or residence times have not been assessed in frugivorous species to date.…”

“…I where P is the steady-state feeding concentration of radiolabeled sugars in plasma (disintegrations per minute [dpm] mg Ϫ1 of plasma), S is the probe distribution space of radiolabeled sugars in plasma (mg of plasma), K el is the elimination rate constant for the removal of radiolabeled sugars from plasma and its excretion in urine (min Ϫ1 ), and I is the ingestion rate of radiolabeled sugars (dpm min Ϫ1 ; Karasov and Cork 1994;McWhorter et al 2006;Napier et al 2008b).…”

“…To vary food intake rate, birds received two diet sugar concentrations (0.25 and 1 mol L Ϫ1 hexose solutions) in separate feeding experiments. Both the order of trials and the treatments given were randomly assigned and followed published protocol (McWhorter et al 2006;Napier et al 2008b). Bioavailability (f) was calculated as…”

A Comparison of Pharmacokinetic Methods for In Vivo Studies of Nonmediated Glucose Absorption

“…Paracellular transport of glucose appears to account for a relatively small proportion of total glucose uptake (∼5%) in nonflying mammals such as rats (O'Rourke et al 1995;Uhing and Kimura 1995), dogs (Lane et al 1999;Pencek et al 2002Pencek et al , 2003, and humans (Fine et al 1993). Recent studies using uniform methodology have shown convincingly, however, that small birds (Karasov and Cork 1994;Levey and Cipollini 1996;Afik et al 1997;Chediack et al 2001Chediack et al , 2003Napier et al 2008b) and bats CaviedesVidal et al 2008) rely extensively on nonmediated mechanisms of absorption. In these animals, paracellular nutrient uptake supplements carrier-mediated absorption, allowing them to maintain high digestive efficiency in spite of generally smaller intestines, lower absorptive surface area, and relatively rapid digesta throughput (Caviedes-Vidal et al 2007).…”