Maternal high-fat diet increases independent feeding in pre-weanling rat pups

Abstract

In laboratory settings, the adult offspring of rodent dams that are maintained on high-fat diet (HFD) before conception and/or during pregnancy/lactation display an increased incidence of obese phenotypic markers, including increased body weight and adiposity, reduced leptin sensitivity, and impaired glucose tolerance. In rat pups raised by dams consuming HFD, these obese markers emerge during the first postnatal week. Since the week-old offspring of HFD dams consume excess amounts of milk during experimental tests of independent feeding (i.e., intake away from the dam), we hypothesized that maternal diet affects suckling and/or independent ingestion by pups in the home-cage environment. In the present study, this hypothesis was tested by conducting detailed analyses of ingestive behaviors expressed by pups in the home cage. Pups raised by dams consuming HFD displayed an earlier onset of independent feeding and more amounts of calorie intake from solid food during the third postnatal week compared to pups raised by dams consuming regular chow, with no diet-related differences in suckling behavior. Independent ingestion by pups in both diet groups was most frequently observed after nursing, with offspring of HFD dams engaged more frequently in post-nursing independent feeding episodes compared to offspring of chow-fed dams, particularly when the prior nursing episode was nutritive (i.e., including milk receipt by pups). We conclude that early-life exposure to HFD enhances the facilitative effect of nutritive suckling on independent feeding in pups, promoting increased caloric intake from solid food in the home-cage environment.

Keywords: High-fat diet; Independent feeding; Nursing; Obesity; Offspring; Suckling.

Figure 1

Operational definitions for four categories of independent feeding in relation to nursing. (i) Feeding after nursing: feeding episode observed within 40 min after the termination of nursing. (ii) Feeding during nursing: feeding episode observed while the dam nursed other pups. (iii) Feeding out of nursing: feeding episode observed more than 40 min after termination of the prior nursing bout, with no simultaneous nursing of other pups. (iv) Feeding after unidentified nursing: feeding episode ongoing at the beginning of the observation period, with the prior nursing bout terminating at an unknown time.

Figure 2

Body weight in male (A) and female (B) offspring of HFD- vs. CHOW-fed dams. HFD pups of both sexes were heavier than CHOW pups at P7, P14, and P21 (*p < 0.05). On P1, male CHOW pups weighed slightly but significantly more than male HFD pups (^#p < 0.05).

Figure 3

Home-cage caloric intake from solid food, and dam’s feeding time postpartum. (A) Cumulative caloric intake (dams plus pups) was similar in CHOW and HFD groups. (B) During the third postnatal week, rats in HFD groups consumed more total calories from solid food compared to CHOW groups (*p < 0.05). (C) HFD dams spent similar total amounts of time engaged in feeding during the second and third postnatal weeks.

Figure 4

Suckling and independent feeding by pups. (A) The total number of stretching responses (indicative of milk receipt) was similar in CHOW and HFD pups from P7–P20. (B) During the third postnatal week, the total amount of time spent engaged in independent feeding was higher in HFD vs. CHOW pups as indicated by AUC (inset), although this difference did not reach significance. HFD pups cumulatively spent more time engaged in independent feeding on P17 and P18 compared to CHOW pups (*p < 0.05).

Figure 5

Independent feeding categorized in relation to nursing during the third postnatal week (see text and Figure 1 for operational definitions). HFD pups spent more time engaged in independent feeding after nursing compared to feeding in the other nursing-related categories (^#p < 0.05), and also spent more time for feeding independently after nursing than CHOW pups (*p < 0.05).

Figure 6

The proportion of observed nursing episodes followed by pup independent feeding during the third postnatal week. A higher proportion of nursing episodes was followed by pup independent feeding (within 40 min) in HFD vs. CHOW litters (*p < 0.05).

Figure 7

Pup independent feeding after nursing during the third postnatal week. (A) Total duration of pup independent feeding at each 5-min timepoint for 40 min after nursing. The AUC (inset) indicates that HFD pups spent more time engaged in independent feeding than CHOW pups (*p < 0.05), although the time-binned group difference was significant only at the 20 min time point. (B) Cumulative time spent engaged in independent feeding after nursing. HFD pups spent more time feeding independently than CHOW pups, with a significant group difference emerging 25 min after nursing (*p < 0.05 from 25–40 min).

Figure 8

Cumulative time spent by pups in independent feeding during the third week postnatal, categorized as occurring either before or after a nursing bout. Pups (HFD and CHOW groups combined, because of no interaction with maternal diet) spent more time feeding independently within the 10-min period after nursing than before nursing (*p < 0.05).

Figure 9

Independent feeding by pups after a nutritive vs. non-nutritive suckling episode (i.e., with or without stretching responses indicative of milk receipt). Regardless of maternal diet, the duration of independent feeding after nursing was greater when the nursing episode included milk receipt by pups (^#p < 0.05 vs. duration without milk receipt). HFD pups displayed more independent feeding after milk receipt compared to CHOW pups (*p < 0.05), whereas there was no diet group difference in independent feeding after nursing that induced no milk receipt in pups.