Effects of dietary triiodothyronine or dopamine on small intestinal oxygen consumption in chicks

Shen-Chang Chang; Yang-Kwang Fan; Shao-Yu Peng; Min-Jung Lin

doi:10.4103/0304-4920.359798

ORIGINAL ARTICLE

Year : 2022 | Volume : 65 | Issue : 5 | Page : 250-257

Effects of dietary triiodothyronine or dopamine on small intestinal oxygen consumption in chicks

Shen-Chang Chang¹, Yang-Kwang Fan², Shao-Yu Peng³, Min-Jung Lin⁴
¹ Kaohsiung Animal Propagation Station, Livestock Research Institute, Council of Agriculture, Pingtung City, Taiwan
² Department of Animal Science, National Chung Hsing University, Taichung City, Taiwan
³ Department of Animal Science, National Pingtung University of Science and Technology, Pingtung City, Taiwan
⁴ Changhua Animal Propagation Station, Livestock Research Institute, Council of Agriculture, Changhua City, Taiwan

Date of Submission	25-May-2022
Date of Decision	04-Aug-2022
Date of Acceptance	25-Aug-2022
Date of Web Publication	27-Oct-2022

Correspondence Address:
Dr. Min-Jung Lin
Changhua Animal Propagation Station, Livestock Research Institute, Council of Agriculture, Changhua City
Taiwan

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0304-4920.359798

Abstract

This study aimed to investigate the effects of triiodothyronine (T₃)- or dopamine (Dp)-supplemented diets on oxygen consumption by Na⁺, K⁺-ATPase activity in broiler chicks. Five groups, each with twenty-four 6-day-old chicks, randomly received one of the five dietary treatments: (1) Basal diet (commercial broiler rations with 23.0% crude protein and 3,133 kcal metabolizable energy/kg) or CON, (2) basal diet plus 0.7 μmol Dp/kg diet or Dp0.7, (3) basal diet plus 2.4 μmol Dp/kg diet or Dp2.4, (4) basal diet plus 1.9 μmol T₃/kg diet or T1.9, and (5) basal diet plus 3.8 μmol T₃/kg diet or T3.8 from 6 to 14 days of age. There were four replicates per treatment and 120 birds in total. At 14 days of age, three chicks from each replicate of each treatment were pooled into a flock and fed commercial broiler diets until 7 weeks of age. Compared to CON group, birds fed with T3-supplemented diets had lower thyroid, abdominal fat pad, gizzard and pancreas weight, and heavier heart weight adjusted for fasted body weight. Chicks with T1.9 had lower ileal densities at 14 day old compared with those in Dp groups or CON. Chicks with T3.8 exhibited greater duodenal and jejunal O₂ consumptions as well as ouabain-sensitive O₂ consumptions of jejunum and small intestine (duodenum, jejunum, and ileum) by 46.5%, 58.3%, 40.6%, and 26.4% increases, than those in CON. Partial correlation analysis revealed that the weight and length of the small intestine were negatively correlated with body weight gain. Oxygen consumption in the various small intestinal segments was negatively correlated with their respective densities (mg/mm²). In conclusion, a greater oxygen requirement for maintaining ouabain-sensitive respiration (Na⁺-K⁺-ATPase) in the intestine limits energy availability to support gastrointestinal tract growth and, thereby, may result in lower body weight gain.

Keywords: Broiler, dopamine, oxygen consumption, small intestine, triiodothyronine

How to cite this article:
Chang SC, Fan YK, Peng SY, Lin MJ. Effects of dietary triiodothyronine or dopamine on small intestinal oxygen consumption in chicks. Chin J Physiol 2022;65:250-7

How to cite this URL:
Chang SC, Fan YK, Peng SY, Lin MJ. Effects of dietary triiodothyronine or dopamine on small intestinal oxygen consumption in chicks. Chin J Physiol [serial online] 2022 [cited 2023 Sep 28];65:250-7. Available from: https://www.cjphysiology.org/text.asp?2022/65/5/250/359798

Introduction

Intestinal Na⁺-K⁺-ATPase, localized on the basolateral membranes of enterocytes, transports three Na⁺ out and two K⁺ into the cell per Adenosine triphosphate (ATP) expended. ATP expended in the intestinal enterocytes is used to sustain the exchange of these ions to maintain a favorable electrochemical gradient for the functioning of luminal Na⁺-dependent glucose^{[1],[2],[3],[4]} and Na⁺-dependent amino acid transporters.^[5] For each molecule of D-glucose or D-galactose transported into enterocytes, two sodium ions are simultaneously imported.^[1] The energy expenditure for Na⁺-K⁺-ATPase in the enterocytes accounts for 19%–50% of total energy consumption in the small intestine of chickens.^[6],[7] Similarly, the energy consumption by sodium pumps accounts for 8.3%–20.0% in mice^[8],[9] and 14.4%–55.0% in dairy cows.^[10],[11]

A previous study showed that peritoneal injection of thyroxine (T₄) or triiodothyronine (T₃) increases whole-body oxygen consumption in single comb white leghorns at 40 days of age^[12] and rats.^[13] Another study showed that the administration of T₄ to hypothyroxinemia rats increased oxygen consumption in the jejunal mucosa and energy consumption by sodium pumps by 26% and 57%, respectively.^[14]

Dopamine (Dp) is a neurotransmitter under physiological conditions. It is one of the most widely used vasoactive agents in the treatment of acute circulatory failure. Dp acts directly to constrict intestinal vessels and reduce blood flow and oxygen uptake by approximately 56% and 45% at the end of the infusion.^[15] In response to 5 and 10 μg min⁻¹ kg⁻¹ infusion rates, a significant increase in VO₂ corresponding to 6% and 15%, respectively, was observed.^[16]

A Dp-supplemented diet fed to posthatch broiler chicks from 6 to 12 days of age exerted no effect on their growth and weights of visceral organs. A quadratic and cubic linear regression of heart weight as a percentage of fasted body weight on dietary Dp supplementation was reported.^[17] In contrast, a T₃-supplemented diet fed to broiler chicks from 6 to 15 days of age increased the feed conversion ratio and liver weight. In addition, the weights and lengths of the various small intestinal segments showed a linear response to T₃ levels_. It is unclear whether these changes in growth and visceral organ morphologies are associated with physiological changes in small intestinal energy metabolism.

This study aimed to determine if the administration of T₃, an agent that increases overall energy metabolism within the body, or Dp, an agent that inhibits intestinal oxygen uptake, to broiler chicks affects whole-body growth and the weights of intestinal and other visceral organs. Moreover, we aimed, in particular, to determine if any effects of T₃ or Dp administration during the early life of chicks persisted into the growth thereafter.

Materials and Methods

Experimental design

The study was conducted in a randomized complete block design. Chicks were subjected to one of the following five experimental treatments: (1) basal diet or CON, (2) basal diet plus 0.7 μmol Dp/kg diet or Dp0.7, (3) basal diet plus 2.4 μmol Dp/kg diet or Dp2.4, (4) basal diet plus 1.9 μmol T₃/kg diet or 3.8 T1.9, and (5) basal diet plus 3.8 μmol T₃/kg diet or T3.8. The basal diets comprised commercial broiler ration with 23.0% crude protein (CP) and 3,133 kcal metabolizable energy (ME)/kg. The Dp and T₃ used were 3,4-dihydroxyphenethylamine (Sigma Chemical Co., St. Louis, MO, USA) and 3,3',5-triiodo-L-thyronine (Sigma Chemical Co., St. Louis, MO, USA), respectively. All the treatments were replicated four times. For each replicate, four cages each with six 6 days of age posthatch chicks were randomly allotted into the five treatments. A total of 120 birds were used. The chicks were fed the experimental diets from 6 to 14 days of age. Feed and drinking water were provided ad libitum.

Animal care and diet

The care and use of all chicks were in accordance with the Regulations of Laboratory Animals, National Chung Hsing University, Taiwan. Hubbard broiler chicks of undetermined sex were wing-banded immediately after being hatched. Except for during the T₃ and Dp administration period from 6 to 14 days of age, all the chicks were fed ad libitum with commercial rations of 23% CP and 3,133 kcal ME/kg and 19.6% CP and 3215 kcal ME/kg from 0–3 to 4–7 weeks of age, respectively. Drinking water supplemented with vitamins was freely accessible from 0 to 6 days of age and drinking water only was freely accessible thereafter till 7 weeks of age. The chicks were raised in 45 cm × 90 cm wire-floored cages. Light and heat were supplied 24 h a day from an incandescent 40-Watt bulb at a height that maintained the ambient temperature at 32°C during 0 and 6 days of age, at 29°C during 7 and 14 days of age, and at 27°C during 15 and 21 days of age, and with no artificial heat source thereafter.

Tissue preparation and analysis

The birds were sacrificed by cervical dislocation at 14 days or 7 weeks of age postfeed deprivation for 18 h. Whole-body weight, feed-deprived body weight (FDBW) and the weight of the thyroid gland, heart, spleen, breast muscle, abdominal fat pad, gizzard, liver, pancreas, duodenum, jejunum, ileum, and ceca of each bird were determined, and the length of the duodenum, jejunum, ileum, and cecum was measured. Duodenal, jejunum, and ileum were identified and sampled as previously defined.^[18] The duodenum begins at its attachment with the gizzard and ends at the conjunction of the bile and pancreatic ducts. The jejunum is defined as the proximal four-fifths of the jejunoileum, and the ileum as the distal one-fifth.^[19] Pieces of tissue 2–3 cm in length were sliced from the middle proportions of the duodenum, jejunum, and ileum samples for measuring the oxygen consumption by these tissues.

Small intestinal oxygen consumption

The rate of O₂ consumption (μmol O₂ min⁻¹ g⁻¹) by intact tissue of the duodenum, jejunum, and ileum was measured using an O₂ monitor (Model No 5331, Yellow Springs Instruments) as described.^[20] Tissues from the middle portions of duodenal, jejunal, and ileal segments were prepared by culturing them in cold medium 199 (11 g M199, 5.96 g HEPES and 0.36 g NaHCO₃ in 1 L H₂O, pH 7.4; Sigma Chemical Co., St. Louis, MO, USA) to remove digest and then four tissue pieces (20 mg) were excised using a hole puncher 4.0 mm in diameter. The rate of O₂ consumption by the tissues constantly stirred in 4 mL of media at 37°C was electronically recorded using a dual-channel chart recorder.

The rate of O₂ consumption by intact tissue of each small intestine segment (μmol O₂ min⁻¹ g⁻¹) was estimated by dividing O₂ consumption by the segment weight. Duodenal, jejunal, ileal, and small intestinal O₂ consumption adjusted by FDBW (μmol O₂ min⁻¹ kg FDBW⁻¹) was calculated by dividing the O₂ consumption by the duodenum, jejunum, ileum, and small intestine with FDBW, respectively. Oxygen consumption by the duodenal, jejunal, and ileal segments (μmol O₂ min⁻¹ segment⁻¹) was estimated by multiplying the O₂ consumption rate per gram of duodenum, jejunum, and ileum by their respective weights. Oxygen consumption by the small intestine (μmol O₂ min⁻¹) was calculated by the O₂ consumption of the duodenal, jejunal, and ileal segments. Oxygen consumption attributable to Na⁺-K⁺-ATPase was determined by calculating the difference in O₂ consumption in the presence and absence of ouabain (10⁻⁴ M Sigma Chemical Co., St. Louis, MO, USA).

Statistics

Data were analyzed using the general linear models procedure of the SAS software (SAS Institute Inc, Cary, NC, USA).^[21] For each variable measured, each cage and replicate was regarded as an experimental unit and block, respectively. The differences between the means of any two of the five treatments were tested using LSMEANS. The partial correlation between two variables was determined using multivariate analysis of variance.

Results

In comparison to CON, Dp0.7, and Dp2.4 group chicks, T1.9 and T3.8 group chicks had lighter thyroid (P < 0.001), abdominal fat pad (P < 0.001), and heart (P < 0.01) [Table 1] but lighter pancreas at 14 days of age. At 50 days of age, these differences were no longer significant (P > 0.10). T3.8 but not T1.9 group chicks had lighter (P < 0.05) gizzard weights at 14 days of age compared to those in the other groups. Chicks in Dp0.7, however, had heavier gizzards at 7 weeks of age than the birds in Dp2.4 or CON group chicks. Except for gizzard weight, other variables measured at 7 weeks of age were not different among the five treatments [Table 1].

Table 1: Effect of dietary supplementation of triiodothyronine or dopamine at 14 days and 7 weeks of age on organs weights adjusted by eighteen-hour feed-deprived body weight in broilers

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Chicks fed diets supplemented with various levels of T₃ or Dp from 6 to 14 days of age did not exhibit significant differences in the weights of the duodenum, small intestine, and ceca adjusted to FDBW at 14 days of age [Table 2]. Dp2.4 group chicks had a significantly heavier jejunum compared to those in T3.8 at 14 days of age. The chicks in Dp2.4 had significantly heavier ileum compared to those in T1.9 at 14 days of age. These differences, however, did not persist by 7 weeks of age. There were no differences in the lengths of various small intestinal segments, the whole small intestine, and the cecum in chicks subjected to the five treatments at 14 days or 7 weeks of age [Table 3]. T1.9 group chicks had less dense ileum (mg/cm) at 14 days of age than the CON, Dp0.7, and Dp2.4 group chicks (P < 0.05) [Table 4]. Other variables pertaining to the densities of small intestinal segments, shown in [Table 4], were not significantly different among the five treatments at either 14 days or 7 weeks of age.

Table 2: Effect of dietary supplementation of triiodothyronine or dopamine at 14 days and 7 weeks of age on intestinal weight adjusted by Eighteen-hour feed-deprived body weight in broilers

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Table 3: Effect of dietary supplementation of triiodothyronine or dopamine at 14 days and 7 weeks of age on intestinal length adjusted by eighteen-hour feed-deprived body weight in broilers

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Table 4: Effect of dietary supplementation of triiodothyronine or dopamine at 14 days and 7 weeks of age on small intestinal density in broilers

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The chicks in T3.8 had higher (P < 0.05) duodenal and jejunal O₂ consumption at 14 days of age than those in CON [Table 5]. Duodenal and small intestinal segments consumed more oxygen (P < 0.05) in chicks fed a diet supplemented with 3.8 μmol T₃/kg than those in CON at 14 days of age. These differences were, however, no longer apparent at 7 weeks of age [Table 5]. Compared to CON chicks, Dp0.7, Dp2.4, or T1.9 group chicks did not show a significant difference in duodenal, jejunal, and ileal O₂ consumption.

Table 5: Effect of dietary supplementation of triiodothyronine or dopamine at 14 days and 7 weeks of age on small intestinal oxygen consumption in broilers

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Chicks in T3.8 had 40.6% higher (P < 0.05) O₂ consumption than those subjected to other treatments due to Na⁺-K⁺-ATPase function in the jejunum at 14 days of age [Table 6]. Chicks in T3.8 also showed a 26.4% increase (P < 0.10) in Na⁺-K⁺-ATPase O₂ consumption at 14 days of age compared to those subjected to other treatments. Chicks in Dp 0.7 had higher O₂ consumption by Na⁺-K⁺-ATPase than CON chicks at 14 days of age [Table 6].

Table 6: Effect of dietary supplementation of triiodothyronine or dopamine at 14 days of age and 7 weeks of age on the percentage of small intestinal O₂ consumption by Na⁺ -K⁺ ATPase in broilers

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The partial correlation coefficients among the variables measured and the significant ones between growth performance-relating variables and digestive tract-related variables associated with intestinal function are presented in [Table 7]. The weight of the small intestine at 14 days of age was negatively correlated with body weight gain between 6 and 14 days of age (P < 0.05) [Table 7]. Duodenal consumption at 14 days of age was negatively correlated with the percentage of O₂ consumption by Na⁺-K⁺-ATPase (P < 0.05) [Table 8]. However, jejunal and ileal O₂ consumption was positively correlated with the percentage of O₂ consumption by Na⁺-K⁺-ATPase (P < 0.05) at 14 days of age.

Table 7: Correlation between growth performances, weights and/or lengths of visceral organs, abdominal fat pad weight, and breast muscle weight of 14-day-old chicks

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Table 8: Correlation between oxygen consumption, the percentage of oxygen consumption by Na⁺ -K⁺ -ATPase, and the density of the small intestinal segments in 14-day-old chicks

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Discussion

A previous study showed that chickens fed a diet supplemented with various levels of CP plus 1 mg T₃/kg diet between 7 and 28 days of age showed less body weight compared to controls.^[22] T₃ supplementation can increase the T₃ concentration in the blood and concomitantly reduce the abdominal fat pad weight.^[23] Moreover, the effect of T₃ in increasing basal metabolic rate^[24] and lipolysis has been well documented.^[25] The findings of this study [Table 1] support previous observations that T₃ supplementation during 6 and 14 days of age decreases abdominal fat pad weight.^[17] Thyroid gland weight decreased with dietary supplementation of T₃. This may be because the feedback inhibition in response to increased blood concentrations of T₃ due to dietary supplementation resulted in reduced releases of thyrotropin-releasing hormone and thyroid-stimulating hormone from the hypothalamus and pituitary gland, respectively, resulting in thyroid atrophy. Because of the short half-life of T₃, the differences in thyroid weights caused by dietary supplementation from 6 to 14 days of age were not present by 7 weeks of age.

Although breast weights adjusted for FDBW were not different among chicks subjected to different treatments at 14 days of age, the absolute weights of breasts were substantially lower in the chicks fed T₃-supplemented diets. This lack of difference in breast weight adjusted for FDBW is likely due to the effect of T₃ supplementation on absolute weights of breast and body in similar proportions.

T₃ (10 μg/kg BW/day) supplementation in water has previously been shown to have a significant increase in oxygen consumption in rats.^[13] Injection of T₄ or T₃ in the abdominal area of 40-day-old single comb white leghorns increased whole-body oxygen consumption.^[12] Thyroxine administration resulted in a 26% increase in jejunal mucosal O₂ as well as a 57% increase in mucosal Na⁺-K⁺-ATPase O₂ consumption.^[26] Artificially manipulated blood T₃ and T₄ concentrations in sheep resulted in a 33% increase in energy expenditures associated with Na⁺-K⁺-ATPase activity in hepatocytes.^[27]

In a recent experiment, chicks fed a diet supplemented with 3.8 μmol T₃/kg from 6 to 14 days of age showed 46.5%, 58.3%, and 51.2% greater duodenal, jejunal, and small intestinal O₂ consumptions (μmol O₂ min⁻¹ g⁻¹), respectively, than in CON. Similarly, we found that O₂ consumption by Na⁺-K⁺-ATPase in the jejunum and the small intestine increased with the dietary supplementation of T₃ [Table 6]. These results suggest that treatment with T₃ resulted in increased energy requirements to maintain Na⁺-K⁺-ATPase activity, which resulted in less energy available to support body weight gain as reflected by the decrease in body weight at 14 days of age.

Dp has been reported to increase active sodium transport and lung edema clearance by stimulating Na⁺-K⁺-ATPase function in the alveolar epithelium of normal rats.^[28] Dp is used as a vasodilator^[29] and, therefore, may counteract hemorrhage-induced intestinal mucosal hypoxia. Dp decreases blood flow in the mucosal villus after endotoxin-induced mucosal vasoconstriction^[30] and increases mucosal tissue partial pressure of O₂.^[31] Chicks fed 0.7 μmol Dp/kg showed higher O₂ consumption by Na⁺-K⁺-ATPase at 14 days of age than CON chicks [Table 6]. However, Dp administration did not significantly affect intestinal O₂ consumption at 14 days of age [Table 5] and led to only a 28.7% higher O₂ consumption due to Na⁺-K⁺-ATPase function within the jejunum compared to CON. Dp infusion increased resting energy expenditure from 1839 kcal/day to 2071 kcal/day after cessation of infusion.^[32]

The weights of the duodenum, jejunum, ceca, and small intestine, adjusted for FDBW, at 14 days of age were positively correlated with the feed conversion ratio from 6 to 14 days of age [Table 7]. Our data suggest that the heavier is the intestinal tract, the lower is the feed conversion ratio, that is, chicks might consume more energy to sustain a heavier and longer intestinal tract. If the amount of nutrients absorbed does not increase in parallel with the increased energy consumption by the intestinal tract, body weight gain may decrease owing to the extra energy required for maintenance by the intestine and subsequently less energy available for muscle growth.

O₂ consumption by each segment of the small intestine was negatively correlated with its tissue density (mg tissue/cm tissue length) [Table 8] at 14 days of age. This increased small intestinal O₂ consumption and subsequent increase in energy requirement for sustaining intestinal function might indicate a simultaneous decrease in small intestinal nutrient absorption by the sign of decreased small intestinal density [Table 8]. Ultimately, this may have resulted in the reduced overall growth of chicks.

Conclusion

Chicks fed the T₃-supplemented diets had heavier hearts adjusted for fasted body weight compared to CON group chicks. At 14 days of age, duodenal and jejunal O₂ consumptions were greater in T3.8 group chicks than in CON group chicks. Ouabain-sensitive O₂ consumption by the jejunum and whole small intestine (duodenum, jejunum, and ileum) was 40.6% and 26.4% greater, respectively, than in CON group chicks.

A greater O₂ requirement to maintain ouabain-sensitive respiration (Na⁺-K⁺-ATPase) in the intestine leads to less available net energy to support growth, which causes lower body weight gain.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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