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Relation between feeding behaviour and energy metabolism in pigs fed diets enriched in dietary fibre and wheat aleurone
- K. Quemeneur, L. Montagne, M. Le Gall, Y. Lechevestrier, E. Labussiere
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Feed intake and its daily pattern are regulated both at a short and a long term by several control pathways, including energy balance regulation. This trial aimed to determine the effect of dietary fibre (DB) (mix of wheat, soy and sugar beet pulp fibres) and aleurone supplementation and their interaction on energy and nitrogen balances in growing pigs with ad libitum access to feed. Forty pigs (BW: 35 kg) were fed diets differing by fibre concentration (NDF concentration: 10% or 14% DM) and aleurone supplementation (0, 2 or 4 g/kg) during 3 weeks. Pigs were housed individually in a respiration chamber during the last week to record feeding behaviour and measure energy and nitrogen balances (n = 36). Glucose oxidation was studied on the 6th day with an injection of [U-13C] glucose and measurement of 13CO2 production. There was no significant interaction between DB inclusion and aleurone supplementation on any variables characterizing feeding behaviour. Pigs had less but longer meals with high level of DB, with an increased interval between two meals without effect on daily feed intake. The meal frequency significantly decreased when aleurone supplementation increased. Total tract apparent digestibility coefficient of DM, organic matter, ash, nitrogen and gross energy decreased when pigs received high DB level. Dietary fibre level increased significantly faecal excreted nitrogen. Aleurone supplementation decreased nitrogen retention. Free access to the feed induced a great individual variability not only in feed intake level (from 784 to 2290 g/day) but also in feeding behaviour (from 5.5 to 21.5 meals per day). This variability can be linked with the importance of underlying feed intake regulation pathways and difference in energy balance and metabolism efficiency. Several profiles of metabolism efficiency can be discriminate, thanks to a clustering based on feeding behaviour and pre-prandial concentrations of metabolites and hormones. In conclusion, DB inclusion decreased meal frequency, increased average meal size, decreased total tract apparent faecal digestibility coefficient of nitrogen and gross energy. Supplementation of aleurone decreased average daily feed intake with a reduction of the meal number per day, without modification of average meal size. Aleurone supplementation decreased nitrogen retention and nutrient deposition. Independently of experimental diets, the high individual variability permitted discriminating different profiles with different metabolic strategies. Efficient pigs with a high energy retention as protein and lipid seem to be able to adapt their metabolism according to energy sources.
Effects of oral supplementation with Spirulina and Chlorella on growth and digestive health in piglets around weaning
- H. Furbeyre, J. van Milgen, T. Mener, M. Gloaguen, E. Labussière
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Weaning of piglets is associated with important changes in gut structure and function resulting from stressful events such as separation from the sow, moving to a new facility and dietary transition from a liquid to a solid feed. This may result in post-weaning diarrhoea and a decrease in feed intake and growth. In humans, the cyanobacterium Spirulina platensis (SP) and the freshwater microalga Chlorella vulgaris (CV) are known for their beneficial health effects. This study aimed to determine the effects of early oral administration of Spirulina and Chlorella in piglets on mucosal architecture and cytokine expression in the intestine around weaning, and consequences on growth performance and diarrhoea incidence. The experiment was conducted on 108 suckling piglets of 14 days of age (initial BW=4.9±0.7 kg) and weaned at 28 days of age (day 0). Animals received orally 385 mg/kg BW per day of SP or CV, or water (negative control (NC)) during 4 weeks from day −14 to day 14 and their growth performance was measured daily. After weaning, growth, feed intake and diarrhoea incidence were measured daily. Intestinal morphology and functionality were assessed at day −1, day 2, and day 14. During the suckling period, average daily gain (ADG) in SP piglets was higher, resulting in a higher weaning BW compared to NC and CV piglets (P<0.05). No significant difference between treatments was observed for ADG, average daily feed intake, and gain to feed (G : F) ratio after weaning, but the extent of growth retardation after weaning was the lowest in piglets supplemented with Chlorella (P<0.01). Supplementation with Spirulina reduced diarrhoea incidence by 50% from day 0 to day 14 (P<0.05). Mucosal architecture at the jejunum was unaffected by Spirulina or Chlorella administration (P>0.10). Shorter ileal villi were measured in SP and CV piglets than in NC piglets (P<0.05). Cytokine expression did not differ between treatments in response to weaning. At day 14, IL-8 expression in the ileum was higher in SP piglets, while IL-1β expression in the jejunum was higher in CV piglets (P<0.05). This study shows that Spirulina administration around weaning alleviates diarrhoea in weaned piglets, without marked modulation of local inflammation.
Effects of rapeseed meal fiber content on phosphorus and calcium digestibility in growing pigs fed diets without or with microbial phytase
- M. Bournazel, M. Lessire, M. J. Duclos, M. Magnin, N. Même, C. Peyronnet, E. Recoules, A. Quinsac, E. Labussière, A. Narcy
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The optimization of dietary phosphorus (P) and calcium (Ca) supply requires a better understanding of the effect of dietary fiber content of co-products on the digestive utilization of minerals. This study was designed to evaluate the effects of dietary fiber content from 00-rapeseed meal (RSM) on P and Ca digestibility throughout the gastrointestinal tract in growing pigs fed diets without or with microbial phytase. In total, 48 castrated male pigs (initial BW=36.1±0.4 kg) were housed in metabolic crates for 29 days. After an 8-day adaptation period, pigs were allocated to one of the eight treatments. The impact of dietary fiber was modulated by adding whole RSM (wRSM), dehulled RSM (dRSM) or dRSM supplemented with 4.5% or 9.0% rapeseed hulls (dRSMh1 and dRSMh2). Diets contained 0 or 500 phytase unit of microbial phytase per kg. From day 14 to day 23, feces and urine were collected separately to determine apparent total tract digestibility (ATTD) and apparent retention (AR) of P and Ca. At the end of the experiment, femurs and digestive contents were sampled. No effect of variables of interest was observed on growth performance. Microbial phytase increased ATTD and AR of P (P<0.001) but the P equivalency with the wRSM diet was lower than expected. Moreover, stomach inorganic P (iP) solubility was improved by microbial phytase (P<0.001). The ATTD of Ca was not affected by microbial phytase which increased AR of Ca and femur characteristics (P<0.05). Ileal recovery of P was not affected by microbial phytase but cecal recovery was considerably reduced by microbial phytase (P<0.001). The decrease in digesta pH between the distal ileum and cecum (7.6 v. 5.9) enhanced the solubility of iP and may have improved its absorption, as supported by the negative relationship between soluble iP and pH (R2=0.40, P<0.001 without microbial phytase and R2=0.24, P=0.026 with microbial phytase). The inclusion of hulls improved the solubility of iP (P<0.05). In conclusion, dehulling does not largely increase nutrient digestibility although dRSM seems to improve the efficacy of microbial phytase in releasing phosphate in the stomach. Moreover, dietary fiber may affect solubilization process in the cecum which potentiates the effect of microbial phytase on P digestibility.
Review: divergent selection for residual feed intake in the growing pig
- H. Gilbert, Y. Billon, L. Brossard, J. Faure, P. Gatellier, F. Gondret, E. Labussière, B. Lebret, L. Lefaucheur, N. Le Floch, I. Louveau, E. Merlot, M.-C. Meunier-Salaün, L. Montagne, P. Mormede, D. Renaudeau, J. Riquet, C. Rogel-Gaillard, J. van Milgen, A. Vincent, J. Noblet
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This review summarizes the results from the INRA (Institut National de la Recherche Agronomique) divergent selection experiment on residual feed intake (RFI) in growing Large White pigs during nine generations of selection. It discusses the remaining challenges and perspectives for the improvement of feed efficiency in growing pigs. The impacts on growing pigs raised under standard conditions and in alternative situations such as heat stress, inflammatory challenges or lactation have been studied. After nine generations of selection, the divergent selection for RFI led to highly significant (P<0.001) line differences for RFI (−165 g/day in the low RFI (LRFI) line compared with high RFI line) and daily feed intake (−270 g/day). Low responses were observed on growth rate (−12.8 g/day, P<0.05) and body composition (+0.9 mm backfat thickness, P=0.57; −2.64% lean meat content, P<0.001) with a marked response on feed conversion ratio (−0.32 kg feed/kg gain, P<0.001). Reduced ultimate pH and increased lightness of the meat (P<0.001) were observed in LRFI pigs with minor impact on the sensory quality of the meat. These changes in meat quality were associated with changes of the muscular energy metabolism. Reduced maintenance energy requirements (−10% after five generations of selection) and activity (−21% of time standing after six generations of selection) of LRFI pigs greatly contributed to the gain in energy efficiency. However, the impact of selection for RFI on the protein metabolism of the pig remains unclear. Digestibility of energy and nutrients was not affected by selection, neither for pigs fed conventional diets nor for pigs fed high-fibre diets. A significant improvement of digestive efficiency could likely be achieved by selecting pigs on fibre diets. No convincing genetic or blood biomarker has been identified for explaining the differences in RFI, suggesting that pigs have various ways to achieve an efficient use of feed. No deleterious impact of the selection on the sow reproduction performance was observed. The resource allocation theory states that low RFI may reduce the ability to cope with stressors, via the reduction of a buffer compartment dedicated to responses to stress. None of the experiments focussed on the response of pigs to stress or challenges could confirm this theory. Understanding the relationships between RFI and responses to stress and energy demanding processes, as such immunity and lactation, remains a major challenge for a better understanding of the underlying biological mechanisms of the trait and to reconcile the experimental results with the resource allocation theory.
Effects of dietary supplementation with freshwater microalgae on growth performance, nutrient digestibility and gut health in weaned piglets
- H. Furbeyre, J. van Milgen, T. Mener, M. Gloaguen, E. Labussière
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In pigs, digestive disorders associated with weaning lead to antibiotic use to maintain intestinal health. Microalgae have been studied in humans and rodents for their beneficial effects on health. The nutritional value of microalgae in animal diets has been assessed, but results were not conclusive. Dietary supplementation with microalgae as an alternative to antibiotic use was studied in two trials (72 piglets with initial BW=9.1±1.1 kg in trial 1 and 24 piglets with initial BW=9.1±0.9 kg in trial 2). All piglets were weaned at 28 days of age and then housed in individual cages. Piglets were randomly allocated to one of the four diets during 2 weeks after weaning: a standard diet with no supplementation (NC) or the standard diet supplemented with 1% Spirulina (SP), with 1% Chlorella (CV), or with 0.2% of colistin as positive control (PC). Trial 1 was performed to determine the effect of microalgae supplementation from 28 to 42 days on performance and incidence of diarrhoea. Animals received then a standard diet from 42 to 56 days of age. Trial 2 was performed from 28 to 42 days of age to assess nutrient digestibility of the experimental diets and to determine inflammatory status and intestinal morphology at 42 days of age. In trial 1, 94% of the pigs had diarrhoea in the 1st week after weaning with no beneficial effect of colistin on diarrhoea incidence, average daily feed intake (ADFI), average daily gain (ADG), and gain : feed (G : F) ratio. This suggests that the diarrhoea was due to digestive disorders that did not result from enterotoxigenic Escherichia coli infection. Supplementation with either Spirulina or Chlorella did not affect ADFI, ADG and G : F in trials 1 and 2 (P>0.10). Diarrhoea incidence was reduced in CV pigs compared with NC, SP and PC pigs (P<0.05). Total tract digestibility in pig receiving microalgae was greater for gross energy (P<0.05), and tended to be greater for dry matter, organic matter and NDF (P<0.10) compared with NC and PC pigs. Villus height at the jejunum was greater in SP and CV pigs compared with NC and PC pigs (P<0.05). This study shows a potential effect of both Spirulina and Chlorella supplementation on intestinal development and a potential of Chlorella supplementation to manage mild digestive disorders. Further investigation is necessary to determine the mechanism action of Spirulina and Chlorella on gut health and physiology.
Effect of α-linolenic acid and DHA intake on lipogenesis and gene expression involved in fatty acid metabolism in growing-finishing pigs
- A. De Tonnac, E. Labussière, A. Vincent, J. Mourot
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- British Journal of Nutrition / Volume 116 / Issue 1 / 14 July 2016
- Published online by Cambridge University Press:
- 16 May 2016, pp. 7-18
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- 14 July 2016
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The regulation of lipogenesis mechanisms related to consumption of n-3 PUFA is poorly understood. The aim of the present study was to find out whether α-linolenic acid (ALA) or DHA uptake can have an effect on activities and gene expressions of enzymes involved in lipid metabolism in the liver, subcutaneous adipose tissue and longissimus dorsi (LD) muscle of growing–finishing pigs. Six groups of ten pigs received one of six experimental diets supplemented with rapeseed oil in the control diet, extruded linseed, microalgae or a mixture of both to implement different levels of ALA and DHA with the same content in total n-3. Results were analysed for linear and quadratic effects of DHA intake. The results showed that activities of malic enzyme (ME) and fatty acid synthase (FAS) decreased linearly in the liver with dietary DHA. Although the expression of the genes of these enzymes and their activities were poorly correlated, ME and FAS expressions also decreased linearly with DHA intake. The intake of DHA down-regulates the expressions of other genes involved in fatty acid (FA) metabolism in some tissues of pigs, such as fatty acid desaturase 2 and sterol-regulatory element binding transcription factor 1 in the liver and 2,4-dienoyl CoA reductase 2 in the LD muscle. FA oxidation in the LD muscle and FA synthesis decreased in the liver with increasing amount of dietary DHA, whereas a retroconversion of DHA into EPA seems to be set up in this last tissue.
Effect of high dietary fat content on heat production and lipid and protein deposition in growing immunocastrated male pigs1
- N. Batorek-Lukač, S. Dubois, J. Noblet, M. Čandek-Potokar, E. Labussière
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In immunocastrated (IC) pigs, revaccination (V2) increases lipid deposition (LD) because of increased voluntary feed intake; but little is known on associated effect of diet composition on partitioning of nutrients in IC pigs. Digestibility measurements, N and energy balances in respiration chambers were performed in two subsequent stages in four replicates of two male littermates to determine the changes between 85 (stage 1) and 135 (stage 2) kg live weight due to combined effect of IC, growth and increased feed intake (IC/growth). During stage 1, pigs received a standard low-fat diet (LF diet; 2.5% dry matter (DM) of fat fed at 2.27 MJ metabolizable energy (ME)/kg BW0.60 per day), whereas during stage 2, feed intake was increased to 2.47 MJ ME/kg BW0.60 per day and one littermate was fed LF diet whereas the second received a fat-enriched diet (HF diet; 8.9% DM of fat) to determine the effect of increased dietary fat content on energy utilization in IC pigs. Results from N balance and measurements of gas exchanges were used to calculate respiratory quotient (RQ), heat production (HP), nutrient contribution to fat retention, components of HP, protein deposition (PD) and LD. Nutrients and energy apparent digestibility coefficients, methane losses and N retention (P<0.05) increased with IC/growth. Despite higher ME intake, total HP remained similar (1365 kJ/kg of BW0.60 per day; P=0.47) with IC/growth. Consequently, total retained energy (RE) increased with IC/growth (from 916 to 1078 kJ/kg of BW0.60 per day; P<0.01) with a higher fat retention (625 to 807 kJ/kg BW0.60 per day; P<0.01), originating mainly from carbohydrates associated with a higher lipogenesis (536 to 746 kJ/kg BW0.60 per day; P<0.01) and RQ (1.095 to 1.145; P<0.01). Both PD (from 178 to 217 g/day; P=0.02) and LD (from 227 to 384 g/day; P<0.01) increased due to IC/growth. Feeding HF diet after IC was associated with increased crude fat digestibility (P<0.01) and increased RE as fat (807 to 914 kJ/kg BW0.60 per day; P=0.03), originating mainly from dietary fat (P<0.01) and resulting in increased LD (384 to 435 g/day; P<0.01) and lower RQ (from 1.145 to 1.073; P<0.01). Altogether, present results indicate that increased fatness of IC pigs is a result of increased daily LD caused by higher energy intake and lower basal metabolic rate. In addition, LD is further enhanced by dietary energy enrichment with fat after V2.
Effect of inflammation stimulation on energy and nutrient utilization in piglets selected for low and high residual feed intake
- E. Labussière, S. Dubois, H. Gilbert, J. N. Thibault, N. Le Floc’h, J. Noblet, J. van Milgen
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Selection of animals for improved feed efficiency can affect sustainability of animal production because the most efficient animals may face difficulties coping with challenges. The objective of this study was to determine the effects of an inflammatory challenge (using an intravenous injection of complete Freund’s adjuvant – CFA) in piglets from two lines of pigs divergently selected during the fattening period for a low (RFI−) or a high (RFI+) residual feed intake (RFI; difference between actual feed intake and theoretical feed requirements). Nitrogen and energy balances (including heat production – HP – and its components: activity-related HP – AHP, thermic effect of feeding, and resting HP) were measured individually in thirteen 20-kg BW castrated male piglets (six and seven from RFI+ and RFI− line, respectively) fed at the same level (1.72 MJ ME/kg BW0.60 per day) from 3 days before to 3 days after CFA injection. Dynamics of dietary U-13C-glucose oxidation were estimated from measurements of 13CO2 production on the day before and 3 days after the CFA injection. Oxidation of dietary nutrients and lipogenesis were calculated based on HP and O2 consumption and CO2 production. The data were analyzed as repeated measurements within piglets in a mixed model. Before CFA injection, RFI− piglets had a lower resting energy expenditure than RFI+ piglets, which tended to increase energy retention because of a higher energy retention as fat. The CFA injection did not affect feed intake from the day following CFA injection onwards but it increased energy retention (P=0.04). Time to recover 50% of 13C from dietary glucose as expired 13CO2 was higher in RFI+ piglets before inducing inflammation but decreased after to the level of RFI− piglets (P<0.01). Oxidation of U-13C-glucose tended to slightly increased in RFI− piglets and to decreased in RFI+ piglets (P=0.10) because of CFA. Additionally, RFI− piglets had a lower respiratory quotient during the 1st day following the CFA injection whereas RFI+ piglets tended to have a higher respiratory quotient. In conclusion, selection for RFI during the fattening period also affected the energy metabolism of pigs during earlier stages of growth. The effects of CFA injection were moderated in both lines but the most efficient animals (RFI−) exhibited a marked re-orientation of nutrients only during the 1st day after CFA, and seemed to recover thereafter, whereas the less efficient piglets expressed a more prolonged alteration of their metabolism.
Fasting heat production and metabolic BW in group-housed broilers
- J. Noblet, S. Dubois, J. Lasnier, M. Warpechowski, P. Dimon, B. Carré, J. van Milgen, E. Labussière
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Fasting heat production (FHP) is used for characterizing the basal metabolic rate of animals and the corresponding maintenance energy requirements and in the calculation of net energy value of feeds. In broilers, the most recent FHP estimates were obtained in the 1980s in slow-growing and fatter birds than nowadays. The FHP values (n=73; six experiments) measured in 3 to 6-week-old modern lines of broilers weighing 0.6 to 2.8 kg and growing at 80 to 100 g/day were used to update these literature values. Each measurement was obtained in a group of fasting broilers (5 to 14 birds) kept in a respiration chamber for at least 24 h. The FHP estimate corresponds to the asymptotic heat production corrected for zero physical activity obtained by modeling the decrease in heat production during the fasting day. The compilation of these data indicates that FHP was linearly related to the BW0.70 (in kg), which can be considered as the metabolic BW of modern broilers. The 0.70 exponent differs from the conventional value of 0.75 used for mature animals. The FHP per kg of BW0.70 ranged between 410 and 460 kJ/day according to the experiment (P<0.01). An experiment conducted with a shorter duration of fasting (16 h) indicated that FHP values are higher than those obtained over at least 24 h of fasting. Our values are similar to those obtained previously on fatter and slow-growing birds, even though the comparison is difficult since measurement conditions and methodologies have changed during the last 30 years. The FHP values obtained in our trials represent a basis for energy nutrition of modern broilers.
Estimation of milk leakage into the rumen of milk-fed calves through an indirect and repeatable method
- E. Labussière, H. Berends, M. S. Gilbert, J. J. G. C. van den Borne, W. J .J. Gerrits
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In milk-fed calves, quantification of the milk that enters the rumen (ruminal milk volume, RMV) because of malfunction of the esophageal groove reflex may explain part of the variability observed between animals in their growth performance. The RMV can directly be quantified by adding an indigestible marker to the diet and measuring its recovery in the rumen at slaughter, but this technique cannot be repeated in time in the same animal. The objective of the study was to evaluate three indirect methods for estimating RMV. The first method was based on the assumption that ruminal drinking delays and limits acetaminophen appearance in blood after ingestion of milk supplemented with acetaminophen. The second method was based on a negative linear relationship between RMV and urinary recovery of non-metabolizable monosaccharides (3-O-methylglucose, l-rhamnose and d-xylose) added to the milk, owing to rumen fermentation. In the third method, RMV was calculated as the difference between total milk intake and the increase in abomasal milk volume (AMV) at feeding, measured through ultrasonography shortly after feeding, or estimated from the mathematical extrapolation of AMV to feeding time, based on consecutive measurements. These methods were tested in three experiments where calves (n=22, 10 and 13) were bucket fed or partly tube fed (i.e. by inserting milk replacer into the rumen via a tube to mimic ruminal drinking). In addition, Co-EDTA and Cr-EDTA were used as an indigestible marker in one experiment to trace bucket-fed or tube-fed milk replacer, respectively, to measure RMV. The relationship between AMV measured by ultrasonography and AMV measured at slaughter improved when kinetics of AMV were extrapolated to the time of slaughter by mathematical modeling (error between predicted and measured AMV equaled 0.49 l). With this technique, RMV during feeding averaged 17% and 24% of intake in Experiments 2 and 3, respectively. Plasma acetaminophen kinetics and recovery of non-metabolizable monosaccharides in urine were partly associated with ruminal drinking, but these techniques are not considered quantitatively accurate without further information of rumen degradation and absorption. The recovery of indigestible marker measured at slaughter gave a quantitative estimate of RMV (2% in Experiment 3), but improper measurement of emptying rate of fluid from the rumen may lead to underestimation. In conclusion, measuring changes in AMV by ultrasonography, in response to milk feeding, was the most promising indirect method to quantify RMV in veal calves.
Effect of feed intake on heat production and protein and fat deposition in milk-fed veal calves
- E. Labussiere, G. Maxin, S. Dubois, J. van Milgen, G. Bertrand, J. Noblet
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Energy requirements for veal calves have not been updated recently despite the increased age at slaughter and the predominance of the Prim’Holstein breed in Europe. The objectives of this study were to determine the effects of four feeding levels (FLs) on protein and fat deposition and heat production in milk-fed calves at three stages of fattening and to determine energy requirements of calves. At each stage, 16 Prim’Holstein male calves (mean body weight (BW): 73.4, 151.6 and 237.4 kg) were fed a milk replacer at 79%, 87%, 95% or 103% of a reference FL. Measurements for one stage were conducted over 4 successive weeks in two open-circuit respiration chambers and consisted of a 6-day nitrogen and energy balance followed by a fasting day for estimating fasting heat production (FHP) of the calves. Heat production (HP) measurements were analyzed using a modeling approach to partition it between HP due to physical activity (AHP), feed intake (thermic effect of feeding (TEF)) and FHP. There was no effect of FL and stage on apparent digestibility coefficients, except for a tendency for increased digestibility coefficient of fat as animals got older. The metabolizable energy (ME)/digestible energy (DE) ratio did not depend on FL but decreased (P < 0.01) as animals got older in connection with marked increases in urinary glucose and urea excretion. The AHP and TEF components of HP were not affected by stage or FL and averaged 8.4% and 7.8% of ME intake, respectively. The FHP, expressed per kg BW0.85, increased with increasing FL, suggesting that also ME requirement for maintenance (MEm) may depend on FL. For an average intake of 625 kJ ME/kg BW0.85 per day (95% of the reference FL), FHP was 298 kJ/kg BW0.85 per day. Energy retention as protein and fat increased with increasing FL resulted in higher BW gain. But the rate of increase depended on stage of growth. The slope relating protein deposition to FL was lower in the finishing phase than in the growing phase, while the slope for lipid deposition was greater. Protein and fat contents of BW gain were not affected by FL but increased as animals got older. From these results, the energy requirements of veal calves are proposed according to a new approach, which considers that MEm (expressed per kg BW0.85) depends on ME intake (kJ/kg BW0.85) according to the following relationship: MEm = 197 + 0.25 × ME intake. The corresponding marginal efficiencies of ME utilization for protein and fat deposition are then 82% and 87%, respectively.