Effect of vertical sleeve gastrectomy on food selection and satiation in rats

Abstract

Vertical sleeve gastrectomy (VSG) is a restrictive procedure that reduces food intake to produce weight loss. Here we assess volume and nutrient effects on the ingestive behavior of VSG and sham surgery animals. Rats given access to Ensure or pelleted chow were used to determine if liquid foods would adversely affect weight loss after surgery. Volume effects were studied by altering the caloric density of Ensure, and dietary preferences for fat and carbohydrate (sucrose) were assessed using a two-bottle test. c-Fos was used to measure neuronal activation in the nucleus of the solitary tract and area postrema in response to intragastric infusions of water, sucrose, or Intralipid. The degree of colocalization with catecholaminergic neurons was also assessed. VSG rats did not show the expected preference for a liquid diet over chow and lacked dietary preferences for fat seen in shams. Preferences for carbohydrate/sucrose solutions were unaffected by surgery. Meal size was reduced by VSG; however, VSG rats were able to alter their volume of intake to compensate for changes in caloric density, and intragastric infusions of water produced similar levels of neuronal activation among VSG, sham, and pair-fed rats. In comparison, nutrient-induced c-Fos activation was substantially increased by VSG. Colocalization between c-Fos and catecholaminergic-expressing neurons was similar among rats treated with water, sucrose, or Intralipid. VSG alters nutrient sensing in a manner that lowers the threshold for satiety and reduces fat preference to induce and maintain weight loss.

Fig. 1.

The two cohorts of rats used in the present study and details of the experiments each group was assigned to. VSG, vertical sleeve gastrectomy.

Fig. 2.

A: mean daily food intake (kcal) of sham (open circles, n = 20) and VSG (filled triangles, n = 19) rats before and after surgery. Food intake was significantly reduced by VSG rats up until postoperative day 35 (P < 0.05). B: body weight of VSG, pair-fed (filled circles, n = 20), and ad libitum-fed sham animals over the same period (*P < 0.05). C: lean tissue mass 3 days before (open bars) and 4 wk after (filled bars) surgery. D: fat mass before and after surgery (*P < 0.05). Differences between VSG and pair-fed animals were nonsignificant, P > 0.05.

Fig. 3.

A: the ratio of Ensure liquid diet (filled bars) to solid rat chow (open bars) consumed over the last 3 days of a food preference study. Sham-operated rats (n = 10) consumed more of their daily calories from Ensure, as expected (P < 0.001). However, contrary to our initial hypothesis, VSG rats (n = 7) showed no preference for the liquid diet over pelleted chow (P > 0.05). ns, Not significant. B: daily food intake shows that sham-operated rats exhibited this preference throughout the experiment, whereas VSG rats initially preferred chow to Ensure (P < 0.05), before eventually consuming similar amounts of each diet (P > 0.05). *P < 0.05, **P < 0.01, and ***P < 0.001.

Fig. 4.

A and B: daily food intake in rats maintained on Ensure liquid diet (days 100–129), chow diet (days 130–183), and then Ensure again (days 183–209). On the Ensure diet, average daily food intake was significantly lower in VSG (n = 5) rats (filled triangles) relative to sham (n = 8) (open circles) (P < 0.05). In animals fed solid chow, differences in food intake were nonsignificant (P > 0.05). C: sham-operated rats (open bars) lost more weight on chow (P < 0.05) and were more susceptible to diet-induced weight gain on the Ensure diet than VSG rats (filled bars, P < 0.05). D: differences in body weight between sham and VSG rats were maintained on each diet, P < 0.05. D, day. *P < 0.05, **P < 0.01, and ***P < 0.001.

Fig. 5.

A: rats compensated for a decrease in calories by volume by increasing their volume of intake during the Ensure + H₂O condition (hatched bars) compared with Ensure alone (open bars), P < 0.05. B: VSG rats (n = 7) compensated almost perfectly by eating a similar amount of calories in each condition, P > 0.05. Ad libitum (n = 10) and pair-fed (n = 10) rats increased their volume of intake in the Ensure + H₂O condition but ate significantly fewer calories compared with Ensure alone, P < 0.05. *P < 0.05 compared with Ensure.

Fig. 6.

Preferences for sucrose were unaltered by VSG (filled triangles, n = 7, P < 0.05) (A); however, preferences for corn oil were significantly reduced compared with ad libitum sham rats (open circles, n = 10, P < 0.05) (B). At the highest concentrations tested, the total intake (kcal) of both sucrose (C) and corn oil (D) was also reduced by VSG (filled bars) compared with sham rats (open bars), P < 0.05. *P < 0.05 compared with sham.

Fig. 7.

Left, quantification of c-Fos induced by water (2 ml), sucrose (4 kcal), or Intralipid (4 kcal). c-Fos levels were similar among groups treated with water but significantly higher in VSG rats treated with sucrose or Intralipid, P < 0.05. Right, micrographs (x10) showing c-Fos in the nucleus of the solitary tract (NTS) and area postrema (AP) of sham, VSG, and pair-fed rats treated with Intralipid (4 kcal). Differences between treatments in sham and pair-fed rats were nonsignificant, P > 0.05, n = 6–7/group. *P < 0.05 compared with sham. #P < 0.05 compared with pair fed (scale bar = 100 μm).

Fig. 8.

Micrograph (x10) showing c-Fos (red)- and dopamine β-hydroxylase (DBH) (green)-expressing neurons in the NTS just rostral to obex in a VSG rat given an intragastric infusion of water (scale bar 100 μm).

Fig. 9.

Micrograph (x10) showing c-Fos (red)- and DBH (green)-expressing neurons in the NTS just rostral to obex in a VSG rat given an intragastric infusion of sucrose (scale bar 100 μm).

Fig. 10.

The number of DBH-positive (A) and c-Fos-positive (B) cells and the percentage of DBH-containing neurons expressing c-Fos (C) in sham and pair-fed (PF) rats given an intragastric infusion of water (n = 3/3) and VSG rats given an intragastric infusion of water (n = 5), sucrose (n = 5), or Intralipid (n = 5). *P < 0.05 compared with rats given water.