Jejunal Glucose Uptake and Oxygen Consumption in Turkey Poults Selected for Rapid Growth 1

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1 Jejunal Glucose Uptake and Oxygen Consumption in Turkey Poults Selected for Rapid Growth 1 Y. K. FAN,*,2 J. CROOM,,3 V. L. CHRISTENSEN, B. L. BLACK, A. R. BIRD,*,3 L. R. DANIEL,4 B. W. MCBRIDE, and E. J. EISEN* Departments of *Animal Science, Poultry Science, and Zoology, North Carolina State University, Raleigh, North Carolina , and Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario, N1G 2W1 Canada ABSTRACT Two lines of turkey poults, one selected for rapid growth at 16 wk of age (F line) and the other a randombred control line (RBC2) were used to investigate the effect of selection for rapid growth on jejunal O 2 consumption and glucose transport as well as wholebody O 2 consumption. All trials used unsexed poults and were designed as a randomized complete block with day and line as independent variables. In Trial 1, 120 turkey poults, fed a standard starter ration (25.5% CP), were used to examine the effect of selection on feed intake, body weight gain, and efficiency from hatching (Day 0) to 13 d of age. At Day 14, 36 of 60 birds from each line were killed to measure intestinal length and weight and jejunal O 2 consumption after 18 h of feed deprivation. Compared with the RBC2 line, the F line had relatively shorter but heavier small intestinal segments when adjusted by 18 h feed-deprived body Received for publication February 10, Accepted for publication August 14, The use of trade names in this publication does not imply endorsement by the North Carolina Agricultural Research Service of the products named or similar ones not mentioned. 2Present address: National Chung-Hsing University, Taichung, Taiwan. 3To whom correspondence should be addressed. 4Present address: CSIRO, Division of Human Nutrition, Adelaide 5000, Australia. weight (FBW; P < 0.001). The F line consumed more O 2 over the entire jejunum adjusted to FBW than RBC2 line (43.8 vs 34.6 nmol O 2 /min g FBW; P < 0.001). Jejunal ouabain- and cycloheximide-sensitive O 2 consumption were greater (P < 0.05) in the F line. In Trial 2, d-old poults from each line were used to measure in vitro jejunal glucose transport rate. There was no difference in glucose transport of the jejunum (nanomoles per minute per gram of FBW) between the lines. In Trial 3, 20 poults from each line were used to measure whole-body O 2 consumption at 7 to 10 d of age. The F and RBC2 lines had similar whole-body O 2 consumption rate per gram of FBW. These data suggest that selection of turkeys for rapid growth at 16 wk of age did not increase efficiency of jejunal glucose uptake in 14-d-old turkey poults. (Key words: turkey, small intestine, glucose active transport, respiration, genetic selection) INTRODUCTION Selection for larger body weight has changed the rate of development of body organs and tissues in the chicken (Katanbaf et al., 1988). Birds selected for high growth rate have a rapid rate of development of supply organs such as the gastrointestinal tract and liver during the 1st wk of life (Lilja, 1983). Previous studies have indicated that selection for rapid growth rate results in changes in the length and weight of the small intestine, the number of enterocytes per villus, villus size and surface area, and the rates of turnover and migration of 1997 Poultry Science 76: enterocytes from crypt to villus tip (Katanbaf et al., 1988; Smith et al., 1990). The gastrointestinal tract is the major site of nutrient uptake and accounts for 23 to 36% of whole body energy expenditure and 23 to 38% of whole-body protein synthesis in the broiler chick (Summers, 1991). Changes in small intestinal growth or anatomy due to genetic selection may significantly impact the energetic efficiency of body growth (Croom et al., 1993). The functional changes in the intestinal tract in response to genetic selection have not been elucidated in turkeys. The objective of this study was to investigate whether selection for rapid growth in turkeys has affected glucose absorption, O 2 consumption, and whole body respiration in the jejunum of 14-d-old poults. MATERIALS AND METHODS Experimental Design A randomized complete block design was used in each of three trials. Two turkey lines described by Anthony et 1738

2 GROWTH AND INTESTINAL FUNCTION 1739 al. (1991) and McCartney (1964) were used; one was selected for rapid growth at age 16 wk (F line) and the other was a randombred control line (RBC2). The blocks consisted of days in which poults from each line were randomly sampled. In Trial 1, feed intake, body weight gain, and feed efficiency were measured by using a cage with five birds as the experimental unit. The data associated with intestinal traits measured on individual poults, in Trials 2 and 3, were regarded as experimental units. Animals and Diets The newly hatched poults were provided by the North Carolina State University Department of Poultry Science Field Research Laboratory. All poults were cared for and treated according to the guidelines of the Institutional Animal Care and Use Committee of North Carolina State University. Poults were housed in an electrical brooder battery that maintained the ambient temperature at 38 C for the 1st wk and 35 C for the 2nd wk. In Trial 1, 60 unsexed birds from each line were used for performance, organ weights and jejunal O 2 consumption measurements as well as biochemical analyses. The birds consumed ad libitum a starter ration (corn-soybean meal, 25.5% CP, 3.9% fat, and 2,794 kcal ME/kg) and water. From hatching (Day 0) to Day 13, body weight and feed consumption were recorded. In Trial 2, 16 unsexed 14-d-old birds from each line were used for measuring jejunal glucose transport and jejunal histomorphometric parameters. In Trial 3, 20 unsexed 7- to 10-d-old poults from each line were used for whole-body O 2 consumption. Jejunal Sample Collection On Day 14, birds in Trials 1 and 2 were killed by cervical dislocation after an 18-h feed deprivation period, and the abdominal cavity exposed. Two cuts, one at the gizzardduodenal junction, the other at the ileocecal junction, were made to excise the entire small intestine. The small intestine was immediately placed in ice-cold physiological saline. The pancreas, mesenteric tissue, and adipose tissue were removed. The duodenum (pyloric sphincter to bile duct), jejunum (bile duct to yolk stalk), and ileum (yolk stalk to cecum) of the small intestine were identified and separated. The three intestinal segments were blotted dry and their weights and unstretched lengths measured. After flushing the lumen with 10 ml ice-cold physiological saline, 6 cm of mid-jejunum was cut and placed in an ice-cold O 2 measurement incubation buffer (see below) 5Sigma Chemical Co., St. Louis, MO YSI Model 5300, Yellow Springs Instruments, Yellow Springs, OH Techmar Co., Cincinnati, OH Hoefer Scientific Instruments, San Francisco, CA Pierce Chemical, Rockford, IL Model El 309, BioTek Instruments, Winooski, VT until measurement of O 2 consumption in Trial 1 or in glucose transport buffer (see below) until measurement of glucose transport in Trial 2. In Trials 1 and 2, an additional 4-cm sample of jejunal tissue adjacent to the mid-jejunum was stored in a capped vial at 20 C for biochemical assays. In Trial 2, an additional 2-cm sample of jejunal tissue adjacent to the mid-jejunum was prepared for histomorphometric analyses. All sampling procedures were completed within 15 min after death. Jejunal Oxygen Consumption The jejunum of each bird was longitudinally cut and divided into four 20- to 40-mg pieces. The remainder of the jejunal sample was scraped free of mucosa with the edge of a glass microscope slide leaving intact the serosa, including muscularis externa. The serosa was also cut into four 20- to 40-mg pieces. The O 2 consumption rates of intact jejunal tissue and jejunal serosa were monitored in constantly stirred O 2 consumption incubation buffer containing 11 g M199, g HEPES,5 and 0.36 g NaHCO 3 in 1 L of deionized water at 37 C using an incubation chamber6 fitted with an O 2 electrode6 as described by McBride and Milligan (1985). The O 2 consumption rate of mucosa was estimated by the difference between the O 2 consumption rate of intact jejunal tissue and the O 2 consumption rate of serosa. The ouabain (2.0 mm buffer concentration5) and cycloheximide (6.8 mm buffer concentration5)-sensitive O 2 concentration rates of intact jejunal tissue, serosa, or mucosa were used to estimate the O 2 consumption necessary to sustain Na+/K+-adenosine triphosphatase (ATPase) and protein synthesis, respectively, in various jejunal tissues. Biochemical Assays Jejunal samples were thawed and rinsed in ice-cold physiological (0.9% NaCl wt/vol) saline and blotted dry before scraping off mucosa from serosa and muscularis externa with the edge of a glass microscope slide. The dry matter content of jejunal mucosa and serosa as well as intact jejunum were determined by placing tissue in a forced-air oven for 48 h at 80 C. About 20 mg of mucosa was homogenized for 30 s in cold buffer (2.5 ml; ph 7.4, 10 mmol/l Tris, 1 mmol/l EDTA and 1 mmol NaCl/L) with a Janke and Kunkel homogenizer.7 The DNA content of the mucosal homogenate was determined fluorimetrically using a TKO 100 fluorimeter8 with calf thymus DNA as a standard.8 After homogenizing 20 mg of mucosa for 30 s in 2.5 ml ice-cold NaCl (2 g/l), protein in the mucosal homogenate was precipitated by addition of trichloroacetic acid (100 TCA g/l) and subsequently centrifuged at 800 g for 15 min at 4 C. The total protein content of the resulting pellet was measured using the absorbance of bicinchoninic acid complexed with Cu+9 at 550 nm after resuspending in 2 ml of 2 g/l NaCl. Absorbance was read by an automated microtiter plate reader,10 and protein content estimated using bovine serum albumin as the standard.

3 1740 Glucose Uptake Assay Active glucose uptake by jejunal rings was measured using a modification of the technique described by Reynolds (1995). Jejunal rings, 2-mm wide, were cut from a mid-jejunum sample with a special device designed for this purpose (Bird et al., 1994). After cutting, jejunal rings of each poult were placed in a beaker of glucose transport buffer. Glucose transport buffer (GTB) contained 140 mm NaCl, 4.8 mm KCl, 2.5 mm CaCl 2, 1.2 mm KH 2 PO 4, 1.2 mm MgSO 4, 1.2 mm MgSO 4,25mMHEPES, 0.5 mm b- hydroxybutyrate, and 2.5 mm L-glutamine (ph 7.4). A beaker with three jejunal rings in 2 ml GTB and a duplicate set of beakers containing 0.8 mm, methyl a-dglucopyranoside, 3H-L-glucose (15 Ci/mmol11) and 14C-methyl a-d-glucopyranoside (0.1 Ci/mmol12) in addition to 2 ml GTB were incubated in a Dubnoff Shaking Incubator.13 The beakers were incubated for 10 min at 37 C with a shaking speed of 60 cycles per minute. The assay was started by transferring the rings individually into the isotope-containing beakers at timed intervals. The jejunal rings were incubated for 15 min at 37 C with a shaking speed of 100 cycles per minute. The assay was terminated by rinsing the rings in 3 ml of ice-cold 300 mm mannitol. Jejunal rings were then immersed in 2 ml of TCA (25 g TCA/L) and incubated for 60 min at room temperature to extract the two isotopes. The extracted jejunal rings were removed, blotted dry, and weighed. The TCA extract was centrifuged for 5 min at 2,000 g, and 1 ml of supernate was added to 10 ml of ScientiVerse Bio- HP14 in a Packard Tri-carb 300 liquid scintillation counter set to count 3H and 14C windows. The 3H-L-glucose was used to measure amount of glucose that would adhere to the rings. The 14C-methyl a-d-glucose was used to measure the active uptake of the tissue. Histomorphometric Analysis The jejunal segments used for histological morphometric measurement were fixed in Carnoy s solution for 4 h, sequentially dehydrated, and stored in 70% (vol/vol) ethanol until being embedded with paraffin. Embedded tissue was cut into 5-mm slices and stained with Feulgen reagent and counter-stained with 0.05% Fast Green. A computerized microscopic image analyzer15 was used to determine histomorphometric parameters such as villus height, villus width at its base, villus planar perimeter length, crypt depth, external muscle layer thickness, and height of enterocytes at mid-villus (Bird et al., 1994). Ten jejunal villi were examined from each poult. The criterion for selection of histological sections for examination was 11EI Dupont, Wilmington, DE Amersham Life Sciences Inc., Arlington Heights, IL Precision Dubnoff Metabolic Shaking Incubator, Chicago, IL Fisher Scientific, Pittsburgh, PA Optimas Corp., Bothell, WA Columbus Instruments International Corp., Columbus, OH FAN ET AL. based on the presence of an intact lamina propria, and villi were chosen that were perpendicularly sectioned through the midline axis. Whole-Body Oxygen Consumption The details of the calibration of the measuring system, the measurement procedures, and the calculation of the whole-body O 2 consumption rate were the same as described by Fan et al. (1996) for mice, except that the air flow to the chamber was 0.8 L/min and the activity of the poults was not recorded. For each measuring day, five birds from each line were used to measure whole-body respiration. Each poult was measured twice, consecutively, and the average was taken. Poults were placed in an O 2 -ECO system measurement chamber16 for at least 60 min prior to measuring respiration. Immediately after the repeated measurements, the BW of the poult was recorded. Statistical Analysis The data of each trial were statistically analyzed using the GLM procedure of SAS (SAS Institute, 1988). The model included the effects of block, line, and error. The MANOVA option was used to examine the partial correlations among the variables using cage as experimental unit in Trial 1 and individual poult as the experimental unit in Trial 2. Tukey s test was used to test the significance of differences between means of lines (Steel and Torrie, 1980). RESULTS Feed intake, daily body weight gain, and feed efficiency of the poults at various intervals between hatching and 13 d of age are presented in Table 1. The F line consumed more feed during Days 0 to 6 and 6 to 13, resulting in a 28% increase in feed intake compared to RBC2. The daily BW gains of the two lines were similar at 0 to 6 d and then diverged between 6 to 13 d, which resulted in a 26% cumulative increase in the BW of the F compared to the RBC2 line between 0 and 13 d of age. Although the feed efficiencies of the two lines between Days 0 to 6 and 0 to 13 were not statistically different (P > 0.16), the F line tended (P < 0.067) to have a higher feed efficiency between Days 6 and 13. The weight and length of the small intestines in poults at 14 d of age are presented in Table 2. The F line had a 23% greater 18-h feed-deprived body weight (FBW). Additionally, F line poults had a heavier, longer, and denser duodenum, jejunum, ileum, and small intestine (P < 0.001). After adjustment by FBW, the F line had a shorter (P < 0.05) but heavier (P < 0.001) small intestine (Table 2). Neither the proportions of jejunal serosa and mucosa on a wet basis nor the dry matter contents of intact jejunal and mucosal tissues were different between the F

4 GROWTH AND INTESTINAL FUNCTION 1741 TABLE 1. Feed intake, daily body weight gain, and feed efficiency of poults at 0 to 13 d of age in Trial 1 1 Initial body weight, g/bird Daily feed, g 0 to 6 d to 13 d to 13 d Daily gain, g 0 to 6 d to 13 d to 13 d Gain:feed, mg gain:g feed 0 to 6 d to 13 d to 13 d Total of 120 poults was used with five birds per cage, 12 cages for each line; the cage was the experimental unit. and RBC2 lines at 14 d of age (Table 3). The dry matter content of jejunal serosa in the F line was lower (P < 0.001) than that of the RBC2 line. There were no differences between the two lines in protein and DNA contents or in the protein:dna ratio of jejunal mucosa. Selection for rapid growth in turkey poults had no effect on any of the jejunal histomorphometric variables measured (Table 4). The F line poults did not consume more O 2 per minute per gram wet jejunum than the RBC2 line (Table 5). The F line had a 58% greater (P < 0.013) cycloheximide-sensitive O 2 consumption rate than the TABLE 2. Weight and length of poult small intestinal segments at 14 d of age, Trials 1 and 2 1 Feed-deprived body weight, 3 g Weight, g Small intestine Duodenum Jejunum Ileum Length, cm Small intestine Duodenum Jejunum Ileum Tissue density, mg/cm Small intestine Duodenum Jejunum Ileum Adjusted weight, mg/g FBW 3 Small intestine Duodenum Jejunum Ileum Adjusted length, mm/g FBW 3 Small intestine Duodenum Jejunum Ileum Total of 72 poults were used with 3 birds per cage; the experimental unit was a bird. 3Eighteen-hour feed-deprived body weight (FBW).

5 1742 FAN ET AL. TABLE 3. Jejunal dry matter content and jejunal mucosa protein and DNA contents in poults at 14 d of age, Trials 1 and 2 1 Component, % Serosa Mucosa Dry matter content, % Intact tissue Mucosa Serosa Mucosa characteristics Protein, 5 mg/g DNA, 5 mg/g Protein:DNA, mg protein:mg DNA Total of 72 poults was used with 3 birds per cage, 12 cages for each line. Experimental unit was a poult. 3Jejunal serosa percentage was estimated as the weight of intact tissue scraped free of mucosa divided by weight of intact tissue and multiplied by Estimated by subtraction of percentage serosa from Wet basis. RBC2 line. There were no differences in O 2 consumption rate and proportions of ouabain- and cycloheximidesensitive O 2 consumption of jejunal serosa between the two lines. Compared to the RBC2 line, the F line had a greater (P < 0.013) proportion of cycloheximide-sensitive O 2 consumption. There was no difference between the two lines in the proportion of jejunal mucosal ouabainsensitive O 2 consumption. The F line inspired 59% more O 2 /min over the entire jejunum after adjustment for FBW (P < 0.001). There were no significant differences between F line and RBC2 line in glucose active uptake rates per gram of jejunum, or per the entire jejunum, although the F line had 23% heavier (P < 0.001) FBW and 36% greater (P < 0.001) jejunal weight (Table 6). The jejunal active glucose transport rates adjusted by FBW were similar in F line and RBC2 line. TABLE 4. Histomorphometric analysis of jejunal tissue in poults at 14 d of age, Trial 2 1 Item F RBC2 P Villus, mm Height 635 ± ± Width ± ± Perimeter 1,336 ± 56 1,233 ± Crypt depth, mm 161 ± ± Muscle thickness, 4 mm 222 ± ± Villus height:crypt depth ratio 4.15 ± ± Enterocyte height, mm 29.4 ± ± Values were means ± SEM of 11 F poults and 8 RBC2 poults. 3Width at villus base. 4Total thickness of muscularis externa. Whole-body O 2 consumption measured between 7 and 10 d was 16% higher (P < 0.007) in the F line due to a 21% greater (P < 0.001) BW (Table 7). After adjustment for BW, no difference in whole-body O 2 consumption was exhibited between F and RBC2 lines. In Trial 1, significant within-line positive correlations existed between BW gain and density of duodenum (r = 0.71, P < 0.01), jejunum (r = 0.65, P < 0.001), and ileum (r = 0.63, P < 0.001), respectively. In contrast, BW gain of poults was negatively correlated with jejunal O 2 consumption (r = 0.27, P < 0.05). No significant correlations existed between feed intake and variables associated with jejunal O 2 consumption. In Trial 2, no significant partial correlations were exhibited between histomorphometric variables and glucose active transport. DISCUSSION The heavier BW at hatch and faster growth during the first 2 wk of age in the F line compared to the RBC2 line confirmed that the two samples of turkey poults used in the present study came from two different populations whose growth characteristics have previously been described (McCartney, 1964; Nestor et al., 1967; McCartney et al., 1968; Anthony et al., 1991). Previous studies have shown that the response to selection for rapid growth causes an increase in absolute length and mass of the small intestine, but a decrease in these values relative to BW (Mitchell and Smith 1991; O Sullivan et al., 1992). Further, selection for growth increase has led to positive correlated responses in mass of the small intestinal mucosa (Smith et al., 1990) and in the amount and turnover rate of transporters in the enterocyte membrane (Ferraris et al., 1989). Of these, the increases in small intestinal length and weight are the most common adaptive processes. The rapid growth of the

6 GROWTH AND INTESTINAL FUNCTION 1743 TABLE 5. Jejunal respiration in poults at 14 d of age, Trial 1 1 Jejunal component F RBC2 SE P Intact tissue mmol O 2 /(min g) OS, 4 % CS, 5 % Serosa mmol O 2 /(min g) OS, 4 % CS, 5 % Mucosa mmol O 2 /(min g) OS, 4 % CS, 5 % Entire jejunum 6 mmol O 2 /min mmol O 2 (min g FBW) Total of 72 poults was measured with 3 birds per cage and 12 cages for each line. Experimental unit was bird. 3Wet weight basis. 4OS = ouabain-sensitive. 5CS = cycloheximide-sensitive. 6Estimated as product of intact tissue O 2 consumption and jejunal weight. 7FBW = 18 h feed-deprived body weight. small intestine in early life ensures that the neonate has adequate absorptive capacity to meet postnatal nutritional demands and adequate length of the small intestine provides a reserve absorptive template permitting an immediate response to pathophysiological changes (Weaver et al., 1991). In the present study, the small intestinal weight and length (Table 2), both on an absolute basis and relative to BW, increased and decreased, respectively, with selection for rapid growth, whereas histomorphometric characteristics such as villus, crypt, and enterocyte structure exhibited no changes (Table 4). Our findings and those of earlier studies (Mitchell and Smith 1991; O Sullivan et al., 1992) support the conclusion of Fan et al. (1996) that the small intestine adapts readily to meet demands for increases in nutrient needs in response to selection for increased body growth. Rapid growth resulting from selection may be achieved through altering efficiencies of nutrient absorption or postabsorptive nutrient partitioning and utilization. Fast growth with similar whole-body O 2 consumption per gram of BW in F line poults implies more body mass accretion at the same energy cost. However, in the present study neither feed:gain (Table 1) nor glucose transport (Table 6) was altered in the F line poults. We have no explanation for this discrepancy. It is possible that a longer interval of feed intake and growth measurements would have detected differences in the efficiency of growth. The Na+/K+-adenosine triphosphatase located on the basolateral membrane in enterocytes generates the electrochemical gradient needed for Na+-dependent nutrient transport (Okada et al., 1977). Ouabain-sensitive TABLE 6. Jejunal glucose transport in poults at 14 d of age, in Trial 2 1 Feed-deprived body weight, 3 g Jejunum weight, g Glucose transport nmol/(min g) mmol/(min per jejunum) nmol per jejunum (min g FBW) Total of 32 poults was measured with 16 birds for each line. 2F line was selected for rapid growth at 16 wk. 3Eighteen-hour feed-deprived body weight (FBW).

7 1744 FAN ET AL. TABLE 7. Whole-poult oxygen consumption at 7 to 10 d of age, Trial 3 1 Body weight, g Respiration, mmol O 2 /min mmol O 2 /(min g body weight) Total of 40 poults was measured with 20 birds for each line. 2F line selected for rapid growth at 16 wk. respiration provides a very useful estimation of energy utilization by this sodium pump (Park, 1993). On a per gram of jejunum basis, F line poults did not have a greater ouabain-sensitive respiration rate but did have a higher cycloheximide-sensitive respiration rate associated with increased protein synthesis in intact jejunal tissue or mucosa (Table 5). The increase of O 2 consumption rate in intact jejunal tissue or jejunal mucosa in F line poults is likely attributable to higher rates of jejunal protein synthesis rather than a more active sodium pump. The magnitude of respiratory inhibition by cycloheximide, however, was much higher in jejunal serosa than in intact jejunal tissue in both lines. Nevertheless, comparison of line effect on the jejunal protein synthesis should be valid because there is no evidence for an interaction between genotype and cycloheximide-sensitive O 2 consumption of intestinal tissue components. This result suggests that a higher proportion of jejunal O 2 consumption in the F line is partitioned towards protein synthesis rather than active nutrient transport powered by sodium pumps. Mitchell and Smith (1991) investigated the effect of selection for rapid growth rates in chickens on small intestinal mucosal weight and stated (page 257) that It may thus be postulated that the net efficiency of digestion and absorption per unit of mucosa may be increased concomitant with the increased growth rate and this may at least in part contribute to the observed increase in feed conversion efficiencies. The results of the present study, however, do not support their hypothesis because the rapidly growing poults had heavier jejuna (jejunal weight/fbw, Table 2) and greater jejunal mucosa percentage (Table 3) plus similar jejunal O 2 consumption, when adjusted to FBW (Table 5), while transporting similar amounts of glucose (Table 6) as compared to the RBC2 line. These results suggest there is no improvement in the energetic efficiency of glucose transport as a result of genetic selection for rapid growth in poults. We were unable to make direct estimates of the energetic efficiency of glucose transport in the present study because intestinal O 2 consumption rates and glucose transport rates were not simultaneously measured in the same animals. Further studies are needed to verify that selection for rapid growth does not concomitantly result in alterations in energetic efficiency of other intestinal Na+-dependent nutrient transport in poults. REFERENCES Anthony, N. B., D. A. 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