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A methodology to evaluate short term changes in energy metabolism at the whole animal level in pigs

A methodology to evaluate short term changes in energy metabolism at the whole animal level in pigs
Combined use of respiration chambers to quantify the dynamics of heat production and measurement of 13CO2 production in pigs. This methodology, allow to observe daily variations in energy metabolism, oxidation and deposition of nutrients.

Indirect calorimetry with quantification of 13CO2 production

Rapid modifications of energy metabolism at the whole animal level induced by dietary or sanitary factors are difficult to assess because of inertia of metabolism and because of the inability of classical methodologies to quantify these rapid variations. The development of on-line measurements of 13C-enrichment in expired air after infusion or intake of labelled nutrients offers the opportunity to detect these changes. Additionally, mathematical modelling of heat production and energy metabolism can give further insights in the evaluation of changes in energy metabolism, nutrient oxidation and nutrient deposition on a short term basis.
Our objectives were to combine indirect calorimetry with quantification of 13CO2 production following the intake of [U-13C]-glucose to determine the effects of a sanitary challenge on energy metabolism of piglets that originated from two genetic lines selected for a low or a high residual feed intake (RFI; Gilbert et al, 2007). The RFI of a growing animal is calculated as the difference between its actual feed intake and predicted feed intake required for maintenance and growth, but not for other non-productive functions such as inflammatory and immune response.

A low invasive method

The experiment was conducted during two periods of three days each, with one day between the two periods. During this day, the animals were submitted to an inflammatory challenge using an intravenous injection of complete Freund’s adjuvant (CFA). During each period, heat production, nitrogen and energy balances were measured in castrated male piglets from each line individually housed in a respiration chamber. Additionally, total heat production was partitioned between its components related to physical activity, thermic effect of feeding and resting metabolism from a mathematical approach on O2 consumption and CO2 production (van Milgen et al, 1997). On the last day of each period, we estimated the dynamics of dietary [U-13C]-glucose oxidation from measurements of 13CO2 production in expired air through sampling of the air that goes out the respiration chamber, on-line measurement of CO2 concentration and IRMS determination of isotope ratio of CO2. The recovery of 13C from labelled glucose as 13CO2 was used as an estimate of oxidation of carbohydrates to calculate lipogenesis. Then, the model that partitions heat production was adapted to determine the kinetics of expired 13CO2. It was assumed that 13C from labelled glucose contributed to a common pool of carbon (12C plus 13C) available for metabolic processes involved in thermic effect of feeding. This was modeled by adding to the original two-compartment model a third compartment for modeling the mixing between C isotopes. Identical fractional outflow rates for each compartment were used to calculate the time required to recover 50% of 13C as expired 13CO2.
Because of genetic selection, the most efficient piglets had a lower resting heat production and tended to increase their energy retention due to 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. The CFA injection also decreased the rate of dietary glucose oxidation in the less efficient piglets to the level of the most efficient piglets (50% of intake on average). Contrary to the most efficient piglets, less efficient piglets tended to oxidize less dietary glucose after the CFA injection than before, whereas the time required to recover 50% of 13CO2 after intake of labelled glucose was not affected and averaged 3.8 h. In the most efficient piglets, this time increased after CFA injection up to 4.8 h. Finally, the respiratory quotient calculated as the ratio between expired CO2 and inspired O2 was transiently modified on the day following CFA injection in the most efficient piglets and indicated a decrease in the rate of lipogenesis.

Toward precision feeding in pig production

The combined utilization of respiration chamber and 13C stable isotopes gives opportunity to study the short term changes in energy metabolism of farm animals in the context of precision feeding. Understanding how and when the animals switch between anabolic and catabolic states at a time span lower than the day of measurement will help in explaining inter-individual variations in productive performance and robustness.


  • Labussière, E., Merlot, E., Thibault, J.-N., Noblet, J., Le Floc'h, N., van Milgen, J. (2013). Nutrient utilization during inflammation differs between pigs selected for differences in feed efficiency. In: Energy and protein metabolism and nutrition in sustainable animal production (p. 401-402). EAAP Publication, 134. Presented at 4th International symposium on energy and protein metabolism and nutrition (ISEP), Sacramento, USA (2013-09-09 - 2013-09-12). Wageningen, NLD : Wageningen Academic Publishers. [link]
  • Labussière, E., Dubois, S., Gilbert, H., Thibault, J.-N., Le Floc'h, N., Noblet, J., Van Milgen, J. (2015). Effect of inflammation stimulation on energy and nutrient utilization in piglets selected for low and high residual feed intake. Animal, 9 (10), 1653-1661. [DOI]


  • Gilbert, H., Bidanel, J. P., Gruand, J., Caritez, J.-C., Billon, Y., Guillouet, P., Lagant, H., Noblet, J., Sellier, P. (2007). Genetic parameters for residual feed intake in growing pigs, with emphasis on genetic relationships with carcass and meat quality traits. Journal of Animal Science, 85 (3), 3182-3188. [DOI]
  • van Milgen, J., Noblet, J., Dubois, S., Bernier, J.F. (1997). Dynamic aspects of oxygen consumption and carbon dioxide production in swine. British Journal of Nutrition, 78, 397-410. [Full text]