J Gen Physiol. 2016 Sep;148(3):183-93.

Claims of Several-Fold Improvements of Cardiac Efficiency by Dietary Supplementation with Fish-Oils are Inconsistent with Thermodynamic Considerations

Denis S Loiselle, PhDa,c, Eden Goo, PhDb, June-Chiew Han, PhDc, Brian Chapman, PhDd, Christopher J Barclay, PhD e, Anthony JR Hickey, PhD f and Andrew J Taberner, PhDc,g

 

aDepartment of Physiology, The University of Auckland, Auckland, New Zealand

bMedical Student, University of Western Australia, Crawley, WA 6009, Australia

cAuckland Bioengineering Institute, The University of Auckland, Auckland, New Zealand

dSchool of Applied and Biomedical Science, Faculty of Science and Technology, Federation University Australia, Churchill, Vic 3842, Australia

eSchool of Physiotherapy & Exercise Science, Griffith University, Gold Coast, Queensland 4222, Australia

fSchool of Biological Sciences, The University of Auckland, New Zealand

gDepartment of Engineering Science, The University of Auckland, Auckland, New Zealand

 

Short Title: Fishing for Improved Cardiac Efficiency

doi: 10.1085/jgp.201611620

 

Supplement:

A seductive theme that occurs particularly in the popular press, but also occasionally in the scientific literature, is that particular foods achieve improved performance by the heart. Our cardiac mechano-energetics group is generally sceptical of such claims. This scepticism motivated us to test a particular published claim1  – namely, that a diet supplemented with Omega-3 fish oils had demonstrably improved the contractile efficiency of the heart.

 

Using the hearts of rats that had been raised, post-weaning, on one of three diets, we tested this claim at two widely-differing scales in vitro: isolated, perfused whole-hearts and superfused trabeculae isolated from their left ventricles.2 The enthalpy output, H (the sum of work, W, and heat Q) of the whole heart was quantified as the sum of its pressure-volume work and its rate of oxygen consumption. The enthalpy output of trabeculae was quantified as the sum of the force-length work and heat production. In both scenarios, efficiency was calculated as the ratio of work to enthalpy: ε = W/H.

 

Rats were fed on one of three diets: (i) a reference (REF) diet consisting of standard laboratory rat chow pellets, (ii) a diet in which the food pellets were mixed with commercial fish-oil (FO) and (iii) a diet in which the pellets were mixed with saturated animal fat (SAT). The three diets were equicaloric.

 

Figure 1 shows the results from the series of whole-heart experiments, conducted at two different temperatures of the coronary perfusate : 37°C (i. e., body temperature) and 32°C. As the figure shows, there was no discernible effect of diet on peak efficiency (Panel A) at either temperature. The same result obtained for the afterload at which peak efficiency occurred (Panel B). There was an effect of temperature, however, reflecting the well-known fact that the twitch force of cardiac muscle varies inversely with temperature.3

 

 

Figure 1. Mean ± SEM values of peak total efficiency (A) and the afterload at which it occurred (B) (at a preload of 10 mmHg), for each diet group at 37°C (filled bars) and at 32°C (open bars).

 

Despite revealing no evidence of efficiency at the scale of the whole-heart, we nevertheless undertook comparable experiments using left-ventricular trabeculae – measuring heat output in lieu of oxygen consumption2. This set of experiments was performed at body temperature (37°C). Prior to commencing experimentation, each trabecula was stretched to its optimal length – i.e., the length at which active force production was maximised. The resulting force, divided by the cross-sectional area of the trabecula, provided an index of active stress development, where ‘active’ stress differs from ‘total’ or ‘systolic’ stress by the contribution of ‘passive’ stress. Each trabecula underwent a series of isometric contractions at different muscle lengths, with the results shown in Figure 2.

 

 

Figure 2. Average steady-state peak stress (S: systolic, A: active and P: passive) of trabeculae at their optimal lengths for each Diet group: reference (REF), fish-Oil supplemented (FO), and supplementation with saturated animal fat (SAT).

 

Upon completion of the ‘isometric contraction series’, detailed in Figure 2, the same muscles were required to undergo isotonic contractions at various afterloads, with the results shown in Figure 3. Panel A plots the average dependence of mechanical efficiency on the relative afterload, while the muscles contracted isotonically. The curved lines arose from cubic polynomials fitted to the raw data (not shown) and constrained to converge at coordinates (0,0) and (1,0). The location of the peak of each relation is indicated by the symbol and its associated standard error bar. For all three diets, the peak mechanical efficiency occurred at an afterload of approximately 40% of peak isometric stress development.

 

As shown in Panel B, there was no significant difference of absolute values of peak mechanical efficiencies among the three diets. The result is a diet-independent mean mechanical efficiency of approximately 12%. This value is lower than the average value that can be estimated from the data shown in Figure 1B (approximately 9%). The difference arises because of the distinction between ‘total efficiency’ and ‘mechanical efficiency’. The former includes the cost of activation of contraction – i.e., the energy required to return intracellular Ca2+ concentration to its diastolic value following release from its internal stores and triggering of mechanical contraction. Inclusion of this metabolic cost necessarily reduces the calculated value of efficiency.
The difference of efficiency estimates between these two efficiency indices (‘total’ and ‘mechanical’) allows estimation of the metabolic cost of activating contraction –of the order of 25% of the total metabolic cost of contraction. This value is in remarkable agreement with data recently published by Pham et al4. using a very different and much more direct approach.

 

 

Figure 3. A: mean (± SEM) mechanical efficiencies, as functions of relative afterload (S/So), for trabeculae from each of the diet groups. B: mean ± SEM peak mechanical efficiencies, which are also superimposed on the curved lines-of-best-fit to the raw data; REF (n = 12, black), FO (n = 9, blue) and SAT (n = 12, red).

 

Summary

Whether measuring the pressure-volume work of the isolated hearts and calculating their efficiency from their rates of oxygen consumption, or the force-length work of isolated left-ventricular trabeculae and calculating their efficiency from their rates of heat production, we see no diet-dependence of efficiency. These results bolster our conviction that Claims of Several-Fold Improvements of Cardiac Efficiency by Dietary Supplementation with Fish-Oils are Inconsistent with Thermodynamic Considerations.

 

References

  1. Pepe S, McLennan PL: Cardiac membrane fatty acid composition modulates myocardial oxygen consumption and postischemic recovery of contractile function. Circulation, 105: 2303-2308, 2002.
  1. Goo S, Han J-C, Nisbet LA, LeGrice IJ, Taberner AJ, Loiselle DS: Dietary pre-exposure of rats to fish oil does not enhance myocardial efficiency of isolated working-hearts or their left ventricular trabeculae. Journal of Physiology, 592: 1795-1808, 2014.
  1. Bers DM, Excitation-Contraction Coupling and Cardiac Contractile Force, Second Edition. edited by Kluwer Academic Publishers, 2001.
  1. Pham T, Tran K, Mellor KM, Hickey A, Power A, Ward M-L, Taberner A, Han J-C, Loiselle D. Does the intercept of the heat–stress relation provide an accurate estimate of cardiac activation heat? Journal of Physiology  595.14 (2017) pp 4725–4733.