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. 2019 Dec 27;98(1):skz393. doi: 10.1093/jas/skz393

Effects of Nutrient Restriction During Midgestation to Late Gestation on Maternal and Fetal Postruminal Carbohydrase Activities in Sheep

Ronald J Trotta 1, Manuel A Vasquez-Hidalgo 1, Kimberly A Vonnahme 1,b, Kendall C Swanson 1,✉
PMCID: PMC6986434  PMID: 31879771

Abstract

To examine the effects of nutrient restriction during midgestation to late gestation on maternal and fetal digestive enzyme activities, 41 singleton ewes (48.3 ± 0.6 kg of BW) were randomly assigned to dietary treatments: 100% (control; CON; n = 20) or 60% of nutrient requirements (restricted; RES; n = 21) from day 50 until day 90 (midgestation). At day 90, 14 ewes (CON, n = 7; RES, n = 7) were euthanized. The remaining ewes were subjected to treatments of nutrient restriction or remained on a control diet from day 90 until day 130 (late gestation): CON-CON (n = 6), CON-RES (n = 7), RES-CON (n = 7), and RES-RES (n = 7) and were euthanized on day 130. The fetal and maternal pancreas and small intestines were weighed, subsampled, and assayed for digestive enzyme activity. One unit (U) of enzyme activity is equal to 1 µmol of product produced per minute for amylase, glucoamylase, lactase, and trypsin and 0.5 µmol of product produced per minute for maltase and isomaltase. Nutrient restriction during midgestation and late gestation decreased (P < 0.05) maternal pancreatic and small intestinal mass but did not affect fetal pancreatic or small intestinal mass. Maternal nutrient restriction during late gestation decreased (P = 0.03) fetal pancreatic trypsin content (U/pancreas) and tended to decrease (P < 0.08) fetal pancreatic trypsin concentration (U/g), specific activity (U/g protein), and content relative to BW (U/kg of BW). Nutrient restriction of gestating ewes decreased the total content of α-amylase (P = 0.04) and tended to decrease total content of trypsin (P = 0.06) and protein (P = 0.06) in the maternal pancreas on day 90. Nutrient restriction during midgestation on day 90 and during late gestation on day 130 decreased (P = 0.04) maternal pancreatic α-amylase-specific activity. Sucrase activity was undetected in the fetal and maternal small intestine. Nutrient restriction during late gestation increased (P = 0.01) maternal small intestinal maltase and lactase concentration and tended to increase (P = 0.06) isomaltase concentration. Realimentation during late gestation after nutrient restriction during midgestation increased lactase concentration (P = 0.04) and specific activity (P = 0.05) in the fetal small intestine. Fetal small intestinal maltase, isomaltase, and glucoamylase did not respond to maternal nutrient restriction. These data indicate that some maternal and fetal digestive enzyme activities may change in response to maternal nutrient restriction.

Keywords: developmental programing, digestive enzymes, maternal nutrition, pancreas, small intestine, ruminant

Introduction

Maternal nutrition during gestation is a major determinant of fetal growth and development (Caton and Hess, 2010), and nutrient restriction during gestation can have adverse effects on maternal and fetal visceral tissues. Alterations in fetal visceral organ function during the prenatal phase can potentially have negative effects on postnatal growth (Yunusova et al., 2013). Splanchnic tissues in ruminants constitute less than 10% of BW but account for approximately 50% of total energy expenditure (McBride and Kelly, 1990; Caton et al., 2000) and are a major component defining maintenance requirements (Milligan and McBride, 1985). In ruminants, many studies have demonstrated that the gastrointestinal tract changes in response to pregnancy (Scheaffer et al., 2003, 2004a), stage of gestation (Caton et al., 2009; Meyer et al., 2010), and nutrient intake during gestation (Reed et al., 2007; Carlson et al., 2009). Changes in maternal and fetal visceral organ mass in response to nutrient restriction during gestation can potentially alter the maintenance energy requirements of both the dam and the fetus (Prezotto et al., 2014, 2016, 2018; Caton et al., 2019).

The pancreas and small intestine have important roles in postruminal nutrient digestion, and there is a limited amount of information on their function in response to nutritional adaptation (Harmon, 1993). Specifically, both tissues produce carbohydrases, or glycohydrolases, that are digestive enzymes that hydrolyze glycosidic linkages of saccharides. In nonpregnant ewes, Keomanivong et al. (2017a) found that ewes exposed to nutrient restriction for 60 d had decreased α-amylase activity. Furthermore, Awda et al. (2017) demonstrated that pancreatic exocrine function is affected by both nutrition and pregnancy in cows. Nutrient restriction of ewes during midgestation to late gestation decreased maternal α-amylase activity but had no effect on fetal pancreatic digestive enzymes (Keomanivong et al., 2016). In beef cows, nutrient restriction during midgestation to late gestation increased fetal α-amylase activity but decreased trypsin activity (Keomanivong et al., 2017b). There are no reports on the response of small intestinal carbohydrases (lactase, maltase, isomaltase, sucrase, glucoamylase) to nutrient restriction during pregnancy in ruminants. It was hypothesized that nutrient restriction during midgestation to late gestation may influence maternal and fetal postruminal digestive enzyme activities. Therefore, the objective of this experiment was to determine the effects of nutrient restriction of gestating ewes on maternal and fetal digestive enzyme activities in the pancreas and small intestine.

Materials and Methods

All animal care, surgical, and sample collection procedures were approved by the North Dakota State University Animal Care and Use Committee (Protocol #A18009).

Experimental design

Western whiteface ewe lambs (n = 90; <1 yr of age) were initially placed on pasture with ad libitum access to hay and water with 3 rams of proven fertility fitted with crayon marking harnesses. Mating was recorded every 12 h. On day 30 of gestation, ewes were transferred to the North Dakota State University Animal Nutrition and Physiology Center. Singleton pregnant ewes were identified between day 30 and day 40 of gestation via Doppler ultrasonography. Forty-one singleton ewes were fed a pelleted diet (Table 1) once daily and were housed at the North Dakota State University Animal Nutrition and Physiology Center in individual pens (0.91 × 1.2 m), in a temperature-controlled environment (14 °C), with a 12:12 h light-dark cycle. Targeted ME requirements were based on NRC (1985) recommendations for 60-kg pregnant ewes during midgestation to late gestation (140 g/d of ADG) and were adjusted to 2.36 Mcal of ME/d based on previous experiments using similar animals, diets, and housing (Neville et al., 2010b; Yunusova et al., 2013). Chemical composition of the diet was analyzed for N using method 988.05 (AOAC, 1990) with a Kjeltec Auto 1030 Analyzer (Foss Tecator AB, Höganäs, Sweden), NDF (assayed with a heat-stable amylase and expressed inclusive of residual ash), and ADF (expressed inclusive of residual ash; Van Soest et al., 1991). Dry matter, ash, ether extract, Ca, and P concentrations were analyzed using standard procedures (AOAC, 1990). Starch was analyzed using the methods of Herrera-Saldana and Huber (1989) using a microplate spectrophotometer (BioTek Instruments, Inc., Winooski, VT). Crude protein was calculated by multiplying N concentration × 6.25. Body weights were measured before the morning feeding every 14 d, and dietary allotments were adjusted accordingly.

Table 1.

Ingredient and chemical composition of the pelleted diet fed to gestating ewes

Ingredient composition, % of DM
 Alfalfa meal 33.4
 Beet pulp 28.9
 Wheat middlings 24.4
 Corn grain 9.3
 Soybean meal 4.0
Chemical composition
 DM, % 88.3
 OM, % of DM 94.0
 CP, % of DM 12.7
 NDF, % of DM 42.2
 ADF, % of DM 26.8
 Starch, % of DM 16.4
 EE1, % of DM 1.87
 Ca, % of DM 0.92
 P, % of DM 0.30
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1EE = ether extract.

Diet was formulated to meet NRC requirements (NRC, 1985).

The experimental design and description of treatment groups are presented in Fig. 1. On day 50 of gestation, 41 ewes carrying singletons (Mean initial BW = 48.3 ± 0.6 kg) were assigned to dietary treatments including: 100% of nutrient requirements (control; CON; n = 20) or 60% of nutrient requirements (restricted; RES; n = 21) from day 50 to day 90 of gestation (midgestation). At day 90, 14 ewes were euthanized (CON, n = 7; RES, n = 7), and the remaining ewes were subjected to treatments of nutrient restriction or remained on a control diet from day 90 until day 130 of gestation (late gestation; CON-CON, n = 6; CON-RES, n = 7; RES-CON, n = 7; and RES-RES, n = 7) and euthanized for sample collection.

Figure 1.

Figure 1.

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Schematic of experimental design. Forty-one singleton ewes were fed a pelleted diet formulated to meet NRC requirements (NRC, 1985) until day 50 of gestation. Dietary treatments were assigned from day 50 to day 90 (midgestation) and included 100% of nutrient requirements (control; CON; n = 20) or 60% of nutrient requirements (restricted; RES; n = 21) from day 50 to day 90 of gestation (midgestation). At day 90, 14 ewes were euthanized (CON, n = 7; RES, n = 7) and the remaining ewes either continued on CON or RES until day 130, or CON ewes were RES from days 90 to 130, or RES ewes were realimented to CON from days 90 to 130. This resulted in 4 additional treatment groups: CON-CON (n = 6), CON-RES (n = 7), RES-RES (n = 7), RES-CON (n = 7). All remaining ewes on day 130 of gestation were euthanized for sample collection.

Sample collection

On day 90 (n = 14) and day 130 (n = 27), ewes were weighed at 0700 and anesthesia was induced with 3 mg/kg of BW sodium pentobarbital. A jugular catheter was inserted to maintain anesthesia through intermittent infusion of sodium pentobarbital. The uterus was exposed with a midventral laparotomy for measurements of uteroplacental blood flow, blood collection, and fetal extraction as described by Lemley et al. (2012). The umbilical cord was identified, severed, and the fetus was removed. Ewes were then euthanized with an overdose of sodium pentobarbital and the carcass was eviscerated. Measurements of blood flow and nutrient and hormone concentrations in blood will be presented separately from this manuscript.

Gastrointestinal tracts were removed, weighed, and digestive organs were separated for individual weights and subsample collection. The pancreas and small intestine were trimmed of mesentery and adipose tissue and weighed. A subsample was collected from the body of the pancreas. A 1-m segment from the maternal small intestine was collected, after measuring 5 m distal to the pylorus. A mucosal scrape of the collected 1-m maternal small intestinal segment and the intact fetal small intestine (jejunum) were flash-frozen in isopentane (2-methylbutane, J. T. Baker, Center Valley, PA) that was super-cooled in liquid nitrogen and then stored at −80 °C until further analyses (Keomanivong et al., 2016).

Pancreatic digestive enzyme analysis

Pancreatic tissue (254 ± 14.3 mg) was weighed and diluted with 2.25 mL of 9 g/L NaCl solution in a 10-mL storage tube. Samples were homogenized (Kinematica Polytron PT 10/35; Brinkmann Instruments Inc., Westbury, NY), and protein concentration was measured using the bicinchoninic acid (BCA) procedure (Pierce BCA Protein Assay Kit; Cat no. 23225; Thermo Fisher Scientific Inc., Waltham, MA) with bovine serum albumin used as a standard diluted in saline (Smith et al., 1985). Activity of α-amylase was determined using the procedure of Wallenfels et al. (1978) that was adapted for analysis of pancreatic tissue. Alpha-amylase activity was assayed kinetically with a commercially available reagent (Amylase Reagent Set; Cat no. A533; Teco Diagnostics, Anaheim, CA) containing p-nitrophenyl-d-maltoheptaoside as the substrate. The reagent was reconstituted [0.225 mM p-nitrophenyl-d-maltoheptaoside; 6,250 U/L α-glucosidase (Saccharomyces cerevisiae); 2,500 U/L glucoamylase (Rhizopus sp.); 12.5 mM NaCl; 1.25 mM CaCl2; 12.5 mM buffer] with 24 mL of distilled water and pre-warmed to 39 °C in an incubator.

Trypsin activity was assayed kinetically using the methods described by Geiger and Fritz (1986) using N-α-benzoyl-dl-arginine-4-nitroanilide hydrochloride (CAS: 911-77-3, Thermo Fisher Scientific Inc., Waltham, MA) as the substrate. Five hundred microliters of the pancreas homogenate was combined with 500 µL of 200 U/L enterokinase (CAS: 9014-74-8, Sigma-Aldrich Co., St. Louis, MO) to activate trypsinogen (Glazer and Steer, 1977) in a 1.5-mL centrifuge tube. Tubes were incubated at 30 °C for 60 min in a water bath, followed by drenching in an ice bath. Analyses were adapted for use on a Synergy H1 microplate spectrophotometer (BioTek Instruments, Inc., Winooski, VT) at 39 °C. One unit (U) of enzyme activity equals 1 µmol product produced per min. Enzyme activity data are expressed as U/g pancreas (concentration), U/g protein (specific activity), kU/pancreas or U/pancreas (content), and U/kg BW (content relative to BW).

Small intestinal digestive enzyme analysis

Intestinal tissue (510 ± 28 mg) was weighed and diluted with 2.0 mL of 9 g/L NaCl solution in a 10-mL storage tube. Samples were homogenized (Kinematica Polytron PT 10/35; Brinkmann Instruments Inc., Westbury, NY) and protein concentration was measured using the BCA procedure, as described previously (Smith et al., 1985). The maternal and fetal small intestines were assayed for brush border carbohydrases: lactase, maltase, isomaltase, sucrase, and glucoamylase. Intestinal disaccharidases (lactase, maltase, isomaltase, sucrase) were assayed using modified methods of Dahlqvist (1964). Lactose, maltose, isomaltose, and sucrose were used as the substrates, respectively. Soluble starch was the substrate used to analyze for glucoamylase activity (Kidder et al., 1972). Five hundred microliters of the intestinal homogenate was combined with 500 µL of 25 mM potassium phosphate buffer (Turner and Moran, 1982) and 100 µL of 60 mM substrate solution in a 1.5-mL centrifuge tube. Tubes were incubated for 30 min at 39 °C in a water bath. The reaction was terminated by heating tubes for 2 min in a 90 °C water bath, followed by drenching in an ice bath. Tubes were then centrifuged at 4,000 × g for 20 min at 4 °C. Liberated glucose was measured using the hexokinase/glucose-6-phosphate dehydrogenase procedure (Farrance, 1987) on a microplate spectrophotometer at 39 °C. All assays were optimized to achieve maximal velocity through the linear concentration range. One unit (U) of enzyme activity equals 1 µmol glucose produced per minute for glucoamylase, lactase, and sucrase and 0.5 µmol glucose produced per minute for maltase and isomaltase. Blanks of each intestinal homogenate and substrate solution were quantified to account for endogenous glucose concentrations and subtracted from the total amount of product produced per minute. Enzyme activity data are expressed as U/g intestine (concentration) and U/g protein (specific activity).

Statistical analysis

Gastrointestinal weights and digestive enzyme data were analyzed using the GLM procedure of SAS (SAS 9.4, Cary, NC). The maternal data were analyzed as a completely randomized design for effects of treatment and the fetal data were analyzed as a randomized complete block design for effects of treatment and fetal sex (blocking factor). Because of the different statistical models and the biological differences between maternal and fetal tissues, no direct comparisons between maternal and fetal data were made. The LSMEANS statement was used to generate means for each treatment. Contrast statements were used to determine differences between treatments and stage of gestation, as described by Keomanivong et al. (2017a). A contrast statement for day of gestation (90 vs. 130; CON vs. CON-CON) was analyzed using control animals during midgestation and late gestation. To determine the effect of nutrient restriction during midgestation (MG on day 90), a contrast was analyzed for CON vs. RES on day 90. To determine the effect of nutrient restriction during midgestation or late gestation (MG on day 130), a contrast was analyzed for CON-CON and CON-RES vs. RES-CON and RES-RES on day 130. To determine the effect of nutrient restriction during late gestation (LG on d 130), a contrast was analyzed for CON-CON and RES-CON vs. CON-RES and RES-RES on day 130. To determine the interaction between treatment and stage of gestation, a midgestation × late-gestation treatment interaction (MG × LG) contrast statement was analyzed for CON-CON and RES-RES vs. CON-RES and RES-RES on day 130. Results were considered significant if P ≤ 0.05. Tendencies were declared when 0.05 < P ≤ 0.10.

Results

Body, pancreas, and small intestinal mass

Nutrient restriction during midgestation decreased maternal BW on day 90 (P = 0.02) and tended to decrease maternal BW on day 130 (P = 0.09; Table 2). Nutrient restriction during late gestation decreased (P = 0.002) maternal BW. Pancreatic mass from gestating ewes increased (P = 0.04) with day of gestation. However, nutrient restriction during midgestation decreased (P = 0.01) maternal pancreatic mass on day 90 and tended to decrease (P = 0.06) maternal pancreatic mass on day 130. Similarly, nutrient restriction during late gestation decreased (P = 0.01) maternal pancreatic mass. Pancreatic mass expressed per kg of BW tended to decrease (P = 0.07) with nutrient restriction during midgestation from tissues collected on day 90, but not day 130. Nutrient restriction during midgestation on day 90 and late gestation on day 130 decreased (P < 0.05) maternal small intestinal mass. Small intestinal mass tended to decrease (P = 0.09) with nutrient restriction during midgestation on day 130 and tended to decrease (P = 0.07) when expressed per kg of BW with nutrient restriction during late-gestation.

Table 2.

Effects of nutrient restriction and stage of pregnancy of gestating ewes on maternal BW, pancreatic, and small intestinal mass1

Stage of pregnancy2 Contrast P-value3
Midgestation Late gestation Day 90 Day 130
Item CON RES CON-CON CON-RES RES-CON RES-RES SEM4 Day MG on day 90 MG on day 130 LG on day 130 MG × LG
BW, kg 51.9 45.2 52.3 47.4 50.3 43.1 2.10 0.90 0.02 0.09 0.002 0.51
Pancreas, g 51.4 37.4 63.0 52.0 54.8 46.0 4.13 0.04 0.01 0.06 0.01 0.76
 g/kg BW 1.06 0.827 1.21 1.11 1.10 1.08 0.0927 0.29 0.07 0.36 0.50 0.66
Small intestine, g 692 594 653 555 629 465 34.9 0.42 0.05 0.09 <0.001 0.33
 g/kg BW 13.1 13.0 12.5 11.7 12.6 11.0 0.735 0.55 0.89 0.58 0.07 0.53
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1CON, control day 50 to 90; MG, midgestation; LG, late gestation; RES, restricted days 50 to 90; CON-CON, control days 50 to 130; CON-RES, control days 50 to 90, restricted days 90 to 130; RES-CON, restricted days 50 to 90, control days 90 to 130; RES-RES, restricted days 50 to 130; Trt, treatment.

2Midgestation, tissues collected on day 90; late gestation, tissues collected on day 130.

3Day, CON vs. CON-CON; MG on day 90, CON vs. RES; MG on day 130, CON-CON and CON-RES vs. RES-CON and RES-RES; LG on day 130, CON-CON and RES-CON vs. CON-RES and RES-RES; MG × LG, period treatment interaction (CON-CON and RES-RES vs. CON-RES and RES-CON).

4Standard error of the mean: (CON; n = 7), (RES, n = 7), (CON-CON; n = 6), (CON-RES; n = 7), (RES-CON; n = 7), (RES-RES; n = 7).

Fetal BW (g or g/kg ewe BW), pancreas mass (g), and small intestinal mass (g or g/kg fetal BW) increased (P < 0.04) with day of gestation (Table 3). Nutrient restriction during midgestation tended to decrease (P = 0.07) fetal small intestinal mass in tissues collected from day 90.

Table 3.

Effects of nutrient restriction and stage of pregnancy of gestating ewes on fetal BW, pancreatic, and small intestinal mass1

Stage of pregnancy2 Contrast P-value3
Midgestation Late gestation Day 90 Day 130
Item CON RES CON-CON CON-RES RES-CON RES-RES SEM4 Day MG on day 90 MG on day 130 LG on day 130 MG × LG
BW, g 617 562 3,492 3,403 3,671 3,425 213 <0.001 0.83 0.63 0.38 0.68
 g/kg ewe BW 12.8 12.4 66.4 72.1 73.1 77.7 4.54 <0.001 0.94 0.17 0.21 0.90
Pancreas, g 0.82 0.66 3.83 3.31 3.37 3.27 0.335 <0.001 0.70 0.45 0.30 0.47
 g/kg fetal BW 1.23 1.24 1.12 0.96 0.90 0.95 0.095 0.31 0.94 0.24 0.54 0.20
Small intestine, g 7.59 5.76 58.4 56.9 67.3 62.7 5.02 <0.001 0.76 0.14 0.51 0.72
 g/kg fetal BW 13.2 9.8 16.9 17.1 18.1 18.5 1.48 0.04 0.07 0.36 0.82 0.95
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1CON, control days 50 to 90; MG, midgestation; LG, late gestation; RES, restricted days 50 to 90; CON-CON, control days 50 to 130; CON-RES, control days 50 to 90, restricted days 90 to 130; RES-CON, restricted days 50 to 90, control days 90 to 130; RES-RES, restricted days 50 to 130; Trt, treatment.

2Midgestation, tissues collected on day 90; late gestation, tissues collected on day 130.

3Day, CON vs. CON-CON; MG on day 90, CON vs. RES; MG on day 130, CON-CON and CON-RES vs. RES-CON and RES-RES; LG on day 130, CON-CON and RES-CON vs. CON-RES and RES-RES; MG × LG, period treatment interaction (CON-CON and RES-RES vs. CON-RES and RES-CON).

4Standard error of the mean: (CON; n = 7), (RES, n = 7), (CON-CON; n = 6), (CON-RES; n = 7), (RES-CON; n = 7), (RES-RES; n = 7).

Pancreatic protein, α-amylase, and trypsin

Maternal pancreatic content of trypsin and protein tended to increase (P < 0.07) as gestation progressed (Table 4). Nutrient restriction during midgestation decreased (P = 0.02) maternal total pancreatic α-amylase content and tended to decrease (P = 0.06) total pancreatic protein and trypsin content in tissues collected from day 90. Nutrient restriction during midgestation decreased (P = 0.03) maternal pancreatic protein and tended to decrease (P < 0.08) α-amylase and trypsin activity expressed per kg of BW in tissues collected from day 90. Nutrient restriction during midgestation decreased (P = 0.04) maternal α-amylase activity (U/g and U/g protein) in tissues collected from day 90. Nutrient restriction of ewes during midgestation did not influence pancreatic protein or digestive enzyme activity in the maternal pancreas collected on day 130. Nutrient restriction during late gestation decreased (P = 0.05) pancreatic protein content expressed per kg of maternal BW. Nutrient restriction during late-gestation decreased (P = 0.04) maternal α-amylase specific activity and total pancreatic α-amylase content. The α-amylase:trypsin in maternal pancreas tended to decrease (P = 0.10) with nutrient restriction during late-gestation.

Table 4.

Effects of nutrient restriction and stage of pregnancy of gestating ewes on maternal pancreatic digestive enzyme activities and protein concentration1

Stage of pregnancy2 Contrast P-value3
Midgestation Late gestation Day 90 Day 130
Item CON RES CON-CON CON-RES RES-CON RES-RES SEM4 Day MG on day 90 MG on day 130 LG on day 130 MG × LG
Protein
 mg/g pancreas 100 95.9 107.1 118 116 126 9.37 0.60 0.73 0.37 0.25 0.92
 g/pancreas 5.11 3.58 6.67 6.16 6.37 5.71 6.35 0.07 0.06 0.51 0.31 0.89
 mg/kg BW 280 164 351 291 321 246 37.6 0.19 0.03 0.27 0.05 0.83
α-Amylase
 U/g pancreas 209 114 162 125 205 144 31.9 0.29 0.04 0.31 0.11 0.70
 U/g protein 1,936 1,187 1,461 1,052 1,770 1,164 257 0.18 0.04 0.39 0.04 0.67
 kU/pancreas 11.1 4.32 9.86 6.74 11.6 6.56 2.20 0.67 0.02 0.69 0.04 0.63
 U/kg BW 199 92.6 188 148 232 153 43.4 0.85 0.08 0.52 0.13 0.61
Trypsin
 U/g pancreas 7.01 5.69 6.08 5.73 5.79 6.62 0.835 0.42 0.25 0.70 0.77 0.46
 U/g protein 76.4 105 60.5 48.6 49.5 54.4 23.7 0.63 0.39 0.91 0.88 0.71
 kU/pancreas 0.338 0.218 0.391 0.299 0.314 0.306 0.0418 0.07 0.06 0.51 0.31 0.89
 U/kg BW 7.37 4.83 7.50 6.43 6.26 7.17 0.960 0.92 0.06 0.77 0.93 0.25
α-Amylase:trypsin 37.8 23.1 29.3 22.0 38.1 24.0 6.72 0.36 0.12 0.40 0.10 0.60
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1CON, control days 50 to 90; MG, midgestation; LG, late-gestation; RES, restricted days 50 to 90; CON-CON, control days 50 to 130; CON-RES, control days 50 to 90, restricted days 90 to 130; RES-CON, restricted days 50 to 90, control days 90 to 130; RES-RES, restricted days 50 to 130; Trt, treatment; U, unit of enzyme activity.

2Midgestation, tissues collected on day 90; late gestation, tissues collected on day 130.

3Day, CON vs. CON-CON; MG on day 90, CON vs. RES; MG on day 130, CON-CON and CON-RES vs. RES-CON and RES-RES; LG on day 130, CON-CON and RES-CON vs. CON-RES and RES-RES; MG × LG, period treatment interaction (CON-CON and RES-RES vs. CON-RES and RES-CON).

4Standard error of the mean: (CON; n = 7), (RES, n = 7), (CON-CON; n = 6), (CON-RES; n = 7), (RES-CON; n = 7), (RES-RES; n = 7).

Fetal pancreatic content (mg/pancreas or U/pancreas) of protein, α-amylase, and trypsin increased (P < 0.003) with day of gestation (Table 5). Fetal α-amylase activity and protein content expressed per kg of fetal BW (U/kg BW) increased (P < 0.04) with day of gestation. Fetal α-amylase concentration (U/g) increased (P = 0.05) as gestation progressed. Nutrient restriction during midgestation did not affect fetal pancreatic digestive enzyme activity or protein on day 90 or day 130. Nutrient restriction during late gestation did not affect fetal pancreatic protein or α-amylase activity. Nutrient restriction during late gestation decreased total pancreatic trypsin content (P = 0.03) and tended to decrease trypsin activity expressed per g of tissue (P = 0.07), g of protein (P = 0.08), and kg of BW (P = 0.06). Fetal pancreatic α-amylase:trypsin tended to increase (P = 0.07) with maternal nutrient restriction during late-gestation. There was a tendency (P = 0.07) for a midgestation × late-gestation treatment interaction for fetal α-amylase specific activity (U/g protein). Nutrient restriction during late gestation after an adequate diet during midgestation tended to decrease (P = 0.07) α-amylase-specific activity. However, nutrient restriction during late gestation after feeding of a restricted diet during midgestation tended to increase (P = 0.07) α-amylase-specific activity.

Table 5.

Effects of nutrient restriction and stage of pregnancy of gestating ewes on fetal pancreatic digestive enzyme activities and protein concentration1

Stage of pregnancy2 Contrast P-value3
Midgestation Late gestation Day 90 Day 130
Item CON RES CON-CON CON-RES RES-CON RES-RES SEM4 Day MG on day 90 MG on day 130 LG on day 130 MG × LG
Protein
 mg/g pancreas 42.7 41.6 51.6 58.8 64.5 57.3 6.79 0.27 0.89 0.39 0.99 0.24
 mg/pancreas 28.7 30.2 196 198 213 185 26.7 <0.001 0.97 0.95 0.57 0.52
 mg/kg BW 1.34 24.98 675 719 794 640 106 <0.001 0.85 0.85 0.56 0.30
α-Amylase
 U/g pancreas 11.7 18.51 27.3 20.3 25.3 32.6 6.44 0.05 0.38 0.40 0.97 0.21
 U/g protein 329 425 545 357 360 561 118 0.13 0.50 0.93 0.95 0.07
 U/pancreas 0.43 16.5 104 77.7 83.7 99.5 21.8 <0.001 0.54 0.97 0.79 0.28
 U/kg BW 14.2 21.8 30.1 20.3 22.9 29.6 6.30 0.04 0.33 0.87 0.78 0.15
Trypsin
 U/g pancreas 0.154 0.105 0.297 0.174 0.333 0.198 0.077 0.14 0.61 0.69 0.07 0.93
 U/g protein 3.35 2.64 5.82 3.08 4.88 3.44 1.29 0.12 0.66 0.81 0.08 0.57
 U/pancreas 0.140 0.058 1.13 0.628 1.11 0.587 0.250 0.003 0.79 0.90 0.03 0.96
 U/kg BW 0.172 0.132 0.323 0.181 0.306 0.178 0.080 0.11 0.69 0.86 0.06 0.88
α-Amylase:trypsin 164 277 101 201 85.4 264 83.5 0.54 0.28 0.77 0.07 0.60
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1CON, control days 50 to 90; MG, midgestation; LG, late gestation; RES, restricted days 50 to 90; CON-CON, control days 50 to 130; CON-RES, control days 50 to 90, restricted days 90 to 130; RES-CON, restricted days 50 to 90, control days 90 to 130; RES-RES, restricted days 50 to 130; Trt, treatment; U, unit of enzyme activity.

2Midgestation, tissues collected on day 90; Late-gestation, tissues collected on day 130.

3Day, CON vs. CON-CON; MG on day 90, CON vs. RES; MG on day 130, CON-CON and CON-RES vs. RES-CON and RES-RES; LG on day 130, CON-CON and RES-CON vs. CON-RES and RES-RES; MG × LG, period treatment interaction (CON-CON and RES-RES vs. CON-RES and RES-CON).

4Standard error of the mean: (CON; n = 7), (RES, n = 7), (CON-CON; n = 6), (CON-RES; n = 7), (RES-CON; n = 7), (RES-RES; n = 7).

Small intestinal protein and carbohydrases

Day of gestation did not affect maternal small intestinal protein concentration or carbohydrase activities (Table 6). Nutrient restriction did not affect protein concentration or glucoamylase activity in the maternal small intestine. Nutrient restriction during midgestation increased maternal maltase concentration (P = 0.02) and tended to increase (P = 0.07) isomaltase concentration. Nutrient restriction during midgestation increased maternal maltase specific activity (P = 0.05) and tended to increase (P = 0.08) lactase-specific activity. Nutrient restriction during midgestation did not influence maternal small intestinal carbohydrase activities on day 130. Nutrient restriction during late-gestation increased (P = 0.01) maltase and lactase concentrations and tended to increase (P = 0.06) isomaltase concentration. Maltase specific activity tended to increase (P = 0.08) and lactase-specific activity increased (P = 0.05) in ewes that were restricted during late-gestation. Sucrase activity was not detected in the maternal small intestine.

Table 6.

Effects of nutrient restriction and stage of pregnancy of gestating ewes on maternal digestive enzyme activities and protein concentration in the small intestine1

Stage of pregnancy2 Contrast P-value3
Midgestation Late gestation Day 90 Day 130
Item CON RES CON-CON CON-RES RES-CON RES-RES SEM4 Day MG on day 90 MG on day 130 LG on day 130 MG × LG
Protein
 mg/g intestine 97.9 109 127 136 128 131 14.5 0.15 0.56 0.88 0.67 0.84
Glucoamylase
 U/g intestine 3.06 2.48 2.71 3.51 2.60 3.61 0.635 0.69 0.49 0.99 0.14 0.86
 U/g protein 31.4 22.9 21.4 26.2 23.6 27.3 5.65 0.20 0.26 0.76 0.43 0.92
Maltase
 U/g intestine 4.64 6.86 6.04 8.19 6.73 8.43 0.703 0.15 0.02 0.49 0.01 0.73
 U/g protein 47.6 63.4 49.8 61.1 55.8 64.6 5.44 0.79 0.05 0.40 0.08 0.82
Isomaltase
 U/g intestine 2.22 3.13 3.05 3.53 3.08 3.91 0.363 0.11 0.07 0.56 0.06 0.61
 U/g protein 22.9 29.0 25.4 26.5 25.2 29.6 2.73 0.54 0.12 0.61 0.34 0.55
Lactase
 U/g intestine 2.27 3.89 2.37 5.27 2.59 3.52 0.750 0.92 0.11 0.29 0.01 0.17
 U/g protein 23.1 36.5 19.9 37.5 23.5 27.7 5.33 0.69 0.08 0.57 0.05 0.23
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1CON, control days 50 to 90; MG, midgestation; LG, late gestation; RES, restricted days 50 to 90; CON-CON, control days 50 to 130; CON-RES, control days 50 to 90, restricted days 90 to 130; RES-CON, restricted days 50 to 90, control days 90 to 130; RES-RES, restricted days 50 to 130; Trt, treatment; U, unit of enzyme activity.

2Midgestation, tissues collected on day 90; late gestation, tissues collected on day 130.

3Day, CON vs. CON-CON; MG on day 90, CON vs. RES; MG on day 130, CON-CON and CON-RES vs. RES-CON and RES-RES; LG on day 130, CON-CON and RES-CON vs. CON-RES and RES-RES; MG × LG, period treatment interaction (CON-CON and RES-RES vs. CON-RES and RES-CON).

4Standard error of the mean: (CON; n = 7), (RES, n = 7), (CON-CON; n = 6), (CON-RES; n = 7), (RES-CON; n = 7), (RES-RES; n = 7).

Nutrient restriction or stage of pregnancy did not affect fetal small intestinal protein concentration (Table 7). Day of gestation did not affect carbohydrase activity in the fetal small intestine. Nutrient restriction did not affect fetal glucoamylase, maltase, or isomaltase activities. There were significant midgestation treatment × late-gestation treatment interactions for lactase concentration (P = 0.04) and lactase-specific activity (P = 0.05) in the fetal small intestine. Nutrient restriction during late gestation after an adequate diet during midgestation increased (P < 0.05) lactase concentration and specific activity. Realimentation to an adequate diet during late gestation after nutrient restriction during midgestation increased (P < 0.05) fetal lactase concentration and specific activity. Sucrase activity was not detected in the fetal small intestine.

Table 7.

Effects of nutrient restriction and stage of pregnancy of gestating ewes on fetal digestive enzyme activities and protein concentration in the small intestine1

Stage of pregnancy2 Contrast P-value3
Midgestation Late gestation Day 90 Day 130
Item CON RES CON-CON CON-RES RES-CON RES-RES SEM4 Day MG on day 90 MG on day 130 LG on day 130 MG × LG
Protein
 mg/g intestine 84.2 84.9 83.0 80.0 90.1 85.1 5.54 0.86 0.91 0.26 0.42 0.84
Glucoamylase
 U/g intestine 0.66 0.53 0.57 0.60 0.64 0.50 0.106 0.51 0.29 0.88 0.52 0.41
 U/g protein 7.97 6.31 7.25 7.73 7.16 5.85 1.36 0.66 0.29 0.46 0.73 0.46
Maltase
 U/g intestine 0.53 0.47 0.51 0.55 0.70 0.57 0.090 0.87 0.61 0.24 0.56 0.27
 U/g protein 6.34 5.59 6.28 7.08 7.68 6.57 0.989 0.96 0.50 0.64 0.86 0.28
Isomaltase
 U/g intestine 0.35 0.34 0.36 0.38 0.40 0.37 0.035 0.70 0.77 0.78 0.80 0.46
 U/g protein 4.21 3.95 4.49 4.85 4.47 4.32 0.448 0.59 0.61 0.52 0.80 0.51
Lactase
 U/g intestine 20.5 13.7 27.5 36.0 45.1 32.5 5.51 0.29 0.28 0.19 0.68 0.04
 U/g protein 254 161 359 456 489 373 61.1 0.15 0.19 0.68 0.86 0.05
Open in a new tab

1CON, control days 50 to 90; MG, midgestation; LG, late gestation; RES, restricted days 50 to 90; CON-CON, control days 50 to 130; CON-RES, control days 50 to 90, restricted days 90 to 130; RES-CON, restricted days 50 to 90, control days 90 to 130; RES-RES, restricted days 50 to 130; Trt, treatment; U, unit of enzyme activity.

2Midgestation, tissues collected on day 90; late gestation, tissues collected on day 130.

3Day, CON vs. CON-CON; MG on day 90, CON vs. RES; MG on day 130, CON-CON and CON-RES vs. RES-CON and RES-RES; LG on day 130, CON-CON and RES-CON vs. CON-RES and RES-RES; MG × LG, period treatment interaction (CON-CON and RES-RES vs. CON-RES and RES-CON).

4Standard error of the mean: (CON; n = 7), (RES, n = 7), (CON-CON; n = 6), (CON-RES; n = 7), (RES-CON; n = 7), (RES-RES; n = 7).

Discussion

There have been numerous studies on the effects of nutrition on fetal development in livestock species (Reynolds and Vonnahme, 2017). In similar models, nutrient restriction during gestation has generally shown reductions in both maternal and fetal BW (Faichney and White, 1987; Scheaffer et al., 2004a; Reed et al., 2007), although exceptions do exist (Vonnahme et al., 2018). In the present study, nutrient restriction decreased maternal BW during both midgestation and late gestation similar to previous studies with beef cows (Meyer et al., 2010; Camacho et al., 2014) or ewes (Swanson et al., 2008d; Lemley et al., 2012; Meyer et al., 2012). However, fetal BW was not affected by maternal nutrient restriction in this study. This may be due to adaptation resulting from changes in uterine and umbilical blood flows (Lemley et al., 2012), nutrient transporter abundance (Dunlap et al., 2015), or net nutrient uteroplacental flux (Lemley et al., 2013).

Besides whole animal changes in BW, nutrient restriction can result in alterations at the tissue (Scheaffer et al., 2004a; Long et al., 2009; Meyer et al., 2013), cellular (Scheaffer et al., 2004b; Reed et al., 2007; Meyer et al., 2010), and molecular level (Neville et al., 2010b; McLean et al., 2017; Crouse et al., 2019) in ruminants. Specifically, the gastrointestinal tract is affected by nutrient restriction probably because of its relatively large consumption of total energy expenditure (Caton et al., 2000). In general, maternal pancreatic (Keomanivong et al., 2016, 2017b) and small intestinal (Meyer et al., 2010; Meyer and Caton, 2016) mass tends to change with plane of nutrition, whereas fetal pancreatic and small intestinal masses are less sensitive to changes in maternal diet (Meyer and Caton, 2016; Keomanivong et al., 2017a). However, fetal pancreatic mass has responded, not only to maternal diet but also maternal exposure to exogenous hormones (Keomanivong et al., 2016) or toxins, such as ergot alkaloids (Greene et al., 2019). Nutrient restriction decreased maternal, but not fetal, pancreatic, and small intestinal masses in the present study. Discrepancies across studies could be attributed to differences in species, diet, degree and length of nutrient restriction, stage of gestation, and parity.

Pancreatic (α-amylase) and small intestinal (maltase, isomaltase, glucoamylase) carbohydrases contribute to luminal and membrane-bound hydrolysis of starch to disaccharides and oligosaccharides to glucose. Small intestinal starch digestion in ruminants is potentially limited by deficient production of carbohydrases (Owens et al., 1986; Brake and Swanson, 2018). Pancreatic digestive enzymes respond to changes in nutrient intake (Kreikemeier et al., 1990) and changes in tissue mass (Wang et al., 1998; Swanson et al., 2002a). Although nonruminant digestive enzymes typically increase proportionally to substrate (Brannon, 1990), pancreatic digestive enzymes in ruminants respond differently to diet and luminal nutrient supply (Harmon, 1992). Moreover, postruminal carbohydrate supply as starch (Walker and Harmon, 1995; Wang and Taniguchi, 1998; Swanson et al., 2002b) or glucose (Swanson et al., 2002b) has been shown to decrease pancreatic α-amylase activity in ruminants. In contrast, postruminal protein (Swanson et al., 2002a, 2004; Richards et al., 2003; Trotta et al., 2020) or amino acid (Yu et al., 2013, 2014; Liu et al., 2018) supply can increase pancreatic α-amylase activity in ruminants. Although intestinal digesta flow or composition was not measured, it should be noted that these factors may influence changes in digestive enzyme activity. Because RES ewes received 60% of total nutrients, it is likely that less nutrients were flowing to the small intestine as a result of reduced intake and reduced digesta volume compared to CON ewes. Other factors such as rate of abomasal emptying, intestinal retention time, or osmolality could contribute to possible differences in digestive enzyme activity between CON and RES ewes.

Nutrient restriction during multiple physiological states has been shown to affect pancreatic exocrine function in ruminants by decreasing maternal (Keomanivong et al., 2016, 2017a), fetal (Keomanivong et al., 2017b), and offspring (day 48; Sun et al., 2017) α-amylase activity. Regulation of pancreatic exocrine function is complex (Swanson et al., 2000), and there are numerous neurohormonal signaling mechanisms involved in digestive enzyme synthesis and secretion (Swanson et al., 2003). Possible mechanisms for changes in digestive enzyme activity include changes in tissue mass, mRNA expression, protein concentrations or secretions, or post-translational modifications (Swanson et al., 2002a). In this study, nutrient restriction decreased maternal α-amylase activity, in part because of a reduction in tissue mass, as evident by the decrease in maternal α-amylase content. However, maternal trypsin activity was not influenced by nutrient restriction. Despite changes in pancreatic mass, regulatory alterations of pancreatic digestive enzymes seem to be more specific to α-amylase. Indeed, many studies in ruminants have found little or no change in pancreatic protease activities in response to nutritional adaptation (Swanson et al., 2000, 2004; Keomanivong et al., 2017b). In pregnant ewes, nutrient restriction from day 50 to day 130 of gestation decreased α-amylase (U/g, U/g protein, kU/pancreas, and U/kg BW) but only decreased trypsin when expressed as U/pancreas (Keomanivong et al., 2016) and data from the present study supports these observations. The downregulation in maternal α-amylase activity appears to be due to changes in both cellularity and tissue size (Swanson et al., 2008a,b,c). Decreases in maternal α-amylase activity may be related to conservation of energy by reducing protein synthesis as regulated via the mammalian target of rapamycin signaling pathway (Guo et al., 2018a,b, 2019), as acinar cells of the exocrine pancreas have the greatest rate of protein synthesis of any mammalian organ (Pandol, 2011).

In the fetal pancreas, pancreatic mass, total content of protein, α-amylase, and trypsin increased with day of gestation. These data support previous observations by Track et al. (1972) and Keomanivong et al. (2017a) in the fetal bovine pancreas. Interestingly, fetal trypsin activity was decreased with maternal nutrient restriction during late gestation. Similarly, maternal nutrient restriction of beef cows during early gestation to midgestation decreased trypsin-specific activity from fetal pancreas collected during late gestation (Keomanivong et al., 2017a). Reasons for decreased trypsin activity in fetal pancreas in response to nutrient restriction are unclear. Also, it is unclear if trypsin activity in RES animals returns to CON levels post-partum. Neville et al. (2010a) reported that lambs from ewes restricted during midgestation and late gestation did not differ in postweaning total tract N digestibility or N balance. Therefore, it is possible that decreases in fetal trypsin activity may not affect the capacity for adequate protein digestion during postnatal life. Additional management or environmental factors during postnatal life could potentially mitigate negative effects of nutrient restriction during gestation (Wu et al., 2006).

In this study, nutrient restriction during midgestation increased maternal maltase concentration by 41.7%, isomaltase concentration by 41.0%, and lactase concentration by 71.4%. During late gestation, nutrient restriction increased maternal glucoamylase concentration by 34.1%, maltase concentration by 30.2%, isomaltase concentration by 21.4%, and lactase concentration by 23.6%. Similar to the ewes in the present study, decreases in pancreatic digestive enzymes but increases in small intestinal disaccharidases were observed in nutrient-restricted broiler chickens (Palo et al., 1995). The observed increases in maternal small intestinal carbohydrase activities were probably a result of the 20.4% decrease in small intestinal mass. Reductions in maternal small intestinal mass but increases in small intestinal carbohydrase activities suggest a reduction in energy utilization by the portal-drained viscera (Freetly et al., 1995), which could result in an increase in digestive efficiency (Meyer et al., 2012; McLean et al., 2014). More information is needed on maternal small intestinal histomorphometry to understand how digestive and absorptive functions may be compromised with nutrient restriction.

Fetal brush border carbohydrases are imprinted early in development (Ferguson et al., 1973; Van Beers et al., 1995). Data from the present study demonstrate that fetal small intestinal carbohydrase activity are detectable (excluding sucrase) by the end of midgestation. It is unclear how early in prenatal development brush border enzyme activity is detectable in ruminants. Fetal brush border carbohydrases involved in small intestinal starch digestion were not affected by maternal nutrient restriction suggesting that maternal nutrient restriction should not be used as a developmental programming strategy to increase fetal brush border carbohydrase activities in sheep. Supporting these observations, Yunusova et al. (2013) found that offspring from nutrient-restricted ewes did not differ in jejunal maltase activity at day 180 post-partum.

One of the distinguishing physiological features of mammals is the ability to provide post-partum nutrition to the offspring via milk secretion from the mammary gland. Nutrient restriction of gestating ewes has been shown to decrease both colostrum and milk production weight and volume during early lactation (Swanson et al., 2008d; Meyer et al., 2011). Furthermore, lactose secretion (g/d) in both colostrum and milk were reduced in nutrient-restricted ewes, but was not affected when expressed as a percentage of milk output. These data indicate that nutrient restriction reduces lactose supply as a function of reduced milk production because of a reduction in mammary gland mass. Lactase produced in the mammalian intestine is the most important carbohydrase during early postnatal life because lactose is the primary carbohydrate ingested (Van Beers et al., 1995). In this study, there was a midgestation × late-gestation interaction for lactase activity in the fetal small intestine. These data indicate that nutrient restriction during midgestation followed by feeding a CON diet can increase fetal lactase activity. This may indicate that nutrient restriction during mid-gestation potentially could be used as a programming strategy to increase fetal lactase activity. However, the physiological consequences of increases in fetal lactase activity are not clear, as greater than 90% of intestinal lactose supply is digested in the small intestine in neonatal ruminants (Gilbert et al., 2015). Thus, improvements in fetal lactase activity may not result in improvements in growth performance post-partum. Regardless of treatment, fetal lactase activity was 60-fold greater on average than fetal maltase activity during late gestation.

There have been multiple reports (Walker, 1959; Shirazi-Beechey et al., 1989; Kreikemeier et al., 1990) that sucrase activity is absent in the ruminant small intestine. Furthermore, postruminal sucrose infusions do not induce mucosal sucrase activity in lambs (Swanson and Harmon, 1997). Likewise, in this study, sucrase activity was undetectable in the maternal and fetal small intestine. More focus on the transcriptional regulation and post-translational modification of sucrase-isomaltase is needed to better understand how the absence of sucrase activity may influence carbohydrate digestion in the ruminant small intestine.

Conclusions

Maternal BW, pancreatic mass, and small intestinal mass were decreased with nutrient restriction. Maternal pancreatic α-amylase activity decreased with nutrient restriction during both midgestation and late gestation. Fetal trypsin activity decreased with nutrient restriction during late gestation. Nutrient restriction increased carbohydrase activities in the maternal small intestine. However, fetal brush border carbohydrases involved in starch digestion were not influenced by nutrient restriction. Realimentation during late gestation after nutrient restriction during midgestation increased lactase activity in the fetal small intestine. These data indicate that some maternal and fetal postruminal carbohydrases may respond to nutrient restriction during midgestation and late gestation in ruminants. Additional work is needed to determine if changes in fetal postruminal digestive enzymes in response to maternal nutrient restriction influence digestive function or animal performance post-partum.

Conflict of interest

No potential conflict of interest was reported by the authors.

Acknowledgements

The authors thank Terry Skunberg and Justin Gilbertson of the NDSU Animal Nutrition and Physiology Center for assistance with animal care, and Jim Kirsch, Sheri Dorsam, and Taylor Czech for assistance with sample collection and analysis. This work was partially funded by Agriculture and Food Research Initiative (AFRI) Competitive (Grant no. 2016-67016-24884) from the USDA National Institute of Food and Agriculture (NIFA).

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