In the pursuit of excellence, many athletes take dietary supplements to help improve performance. These supplements may provide a variety of benefits such as increasing strength, power, speed, or endurance or alternatively, by altering body weight or body composition . Fish oil (containing the omega-3 fatty acids, EPA and DHA) may be considered one of these performance-enhancing supplements. In fact, the use of these important fatty acids has increased among various populations to enhance sport, including elite athletes and children alike [2, 3].
Doesn’t our diet provide enough omega-3 fatty acids?
Major dietary changes have taken place over the past 10,000 to 15,000 years but the human being’s genetic profile has changed very little (if any) throughout that time period (reviewed in ). Human beings evolved consuming a diet that contained roughly equal amounts of omega-6 and omega-3 fatty acids. Today’s Western diet, on the other hand, provides a ratio of omega-6 to omega-3 fatty acids in the range of 10:1 to 20:1 instead of the traditional range of 1:1 to 2:1 (reviewed in [5, 6]). Excess consumption of omega-6 fatty acids relative to omega-3 fatty acids can promote inflammation so the Western diet’s nutritional adequacy has been called into question (reviewed in ). The consumption of omega-3 fatty acids (specifically EPA and DHA) or supplementation with these fatty acids can help to counteract this inflammatory state.
Why is fish oil recommended for athletes?
Omega–3 fatty acids are considered essential fatty acids because humans cannot make them; therefore, they must be obtained through the diet or supplementation. Fish oils are an excellent source of omega-3 fatty acids that offer numerous health benefits for everyone, as well as a variety of performance-enhancing effects, such as increasing muscle growth, improving strength and physical performance, reducing exercise-induced muscle damage and delayed-onset muscle soreness, combating negative immune effects of intensive training, strengthening bones, improving heart and lung functioning, and enhancing cognitive functioning. Below is a summary of the research to support fish oil’s performance-enhancing benefits.
Benefits of Fish Oil
1. Fish oil increases protein synthesis
The correct balance of exercise and nutritional building blocks is necessary within the body for muscle growth to occur. Nutritional status is important to optimize this important process. Protein is an essential raw material that supplies the body with amino acids used to repair and build muscle (reviewed in ) and protein powders are popular supplements within the sports industry . Fish oil is not as well recognized but it may play an important role in muscle growth.
It has been hypothesized that fish oils may improve the anabolic effect of exercise (reviewed in ). In fact, a review of the scientific literature has concluded that omega-3 fatty acids combined with an anabolic stimulus (e.g., physical activity, protein, insulin) can improve protein metabolism . Another scientific review made similar conclusions saying that compelling evidence exists for the combination of omega-3 fatty acids with an anabolic stimulus to improve lean body mass function and quality .
How could fish oil confer an anabolic effect? Omega-3 fatty acids may enhance insulin-sensitive aspects of protein metabolism . Supplementation with fish oil (1,860 mg EPA + 1,500 mg DHA) in nine healthy subjects for eight weeks increased muscle protein synthesis in response to an insulin and amino acid infusion. Additionally, the fish oil increased muscle protein concentration as well as the protein/DNA ratio (i.e., muscle cell size) . The effects of fish oil supplementation (1,860 mg EPA + 1,500 mg DHA) on muscle protein synthesis were also assessed in 16 healthy older adults for eight weeks. Similar to the previous study, the fish oil increased muscle protein synthesis in response to an insulin and amino acid infusion . Based on these results, omega-3 fatty acids from fish oil seem to have anabolic properties in both healthy young adults and middle-aged adults.
Therefore, fish oil supplementation could be a simple intervention to improve the muscle gains associated with strength or resistance training and this may occur via an insulin-sensitizing effect on protein metabolism.
2. Fish oil increases muscle strength and physical performance
Does this increased muscle protein synthesis attributed to fish oils translate into muscular strength gains? It appears that it does. First off, a cross-sectional and retrospective cohort study of almost 3,000 adults (aged 59 to 73 years) revealed that consumption of fatty fish (rich in EPA and DHA) was strongly associated with grip strength measured by a handheld device. An increase in grip strength of 0.43 kg in men and 0.48 kg in women was observed for each additional portion of fatty fish consumed per week .
Similar results have been demonstrated in fish oil supplementation trials. A six-month randomized, double blind pilot study involving 126 postmenopausal women reported that daily fish oil supplementation (1,200 mg EPA + DHA) significantly improved physical performance (measured by a change in walking speed) . Furthermore, in a 90-day randomized trial, 45 women were randomly assigned to 3 groups: strength training only; strength training + fish oil supplementation (~400 mg EPA + 300 mg DHA); or fish oil supplementation for 60 days prior to training and then strength training + fish oil supplementation. While strength training alone increased muscle strength in all muscles assessed, this effect was greater in both groups supplemented with fish oil. Additionally, muscle activation and functional capacity were also significantly improved in the fish oil groups compared to the strength training only group .
These results suggest that omega-3 fatty acids may exert an important influence on muscle function, helping to improve muscular strength, physical performance, and functional capacity.
3. Fish oil reduces exercise-induced muscle damage and delayed-onset muscle soreness
Exercise-induced muscle damage, which is caused by vigorous exercise, can result in delayed-onset muscle soreness and loss of physical function, which can have a profound effect on adaptations to exercise training programs. Athletes are commonly prescribed nonsteroidal anti-inflammatory drugs (NSAIDs; e.g., aspirin and ibuprofen) post-exercise to help alleviate these symptoms. NSAIDs are believed to exert their pain-reducing effects by inhibiting the conversion of arachidonic acid (an omega-6 fatty acid) to proinflammatory molecules (reviewed in ). Omega-3 fatty acid supplementation decreases the arachidonic acid content of cell membranes and reduces the production of pro-inflammatory molecules (reviewed in ). Furthermore, extensive evidence suggests that fish oil is effective in the prevention and treatment of inflammatory conditions (reviewed in ). Therefore, fish oil may represent an alternative strategy to NSAIDs in the prevention or minimization of exercise-induced muscle damage, which may positively impact recovery time between exercise sessions and thereby improve performance and enhance training adaptations.
Fish oil has been shown to be effective in ameliorating exercise-induced inflammation in a number of studies. A one-month randomized, double-blinded, repeated measures study revealed that fish oil (324 mg EPA + 216 mg DHA daily) attenuated eccentric exercise-induced inflammatory markers in 45 untrained men. Even a lower dose of fish oil (300 mg daily) has been shown to have a synergistic effect with aerobic exercise in attenuating inflammation in 79 healthy sedentary post-menopausal women.
In addition to reducing exercise-induced inflammation, fish oil supplementation has also been shown to reduce exercise-induced muscle soreness and thus aid the recovery process. For example, in a crossover trial involving 11 healthy men and women, two weeks of fish oil supplementation (2,000 mg EPA + 1,000 mg DHA daily) reduced arm soreness from bicep curls by 15% . Similarly, a one-month randomized, double-blinded, repeated measures study revealed that 1,800 mg daily of omega-3 fatty acids (324 mg EPA + 216 mg DHA) ameliorated delayed-onset muscle soreness in the lower limbs in 27 healthy men following eccentric exercise whereby subjects repeatedly stepped up on a bench. In this same trial, fish oil supplementation reduced knee range of motion limitations 48 hours following exercise, which is an indirect indication of muscle stiffness and soreness .
These results suggest that fish oil supplementation may represent a possible nutritional strategy for facilitating exercise recovery and enhancing exercise training adaptations.
4. Fish oil helps to combat negative effects of intensive training on the immune system
Regular exercise helps to boost the immune system (reviewed in ), however, athletes can be exposed to exercise-induced stress when they consume inadequate diets and when they train too intensely; this exercise-induced stress can lead to the generation of free radicals (reviewed in [26, 27]). Omega-3 fatty acids may offer a solution to help modify blood antioxidant status after exercise and therefore protect against exercise-induced free radical damage. For example, in a six-week study, two groups of healthy, fit males performed one hour of exercise at 60% of their maximal oxygen consumption before and after a low dose of omega-3 fatty acids (390 mg EPA + 260 mg DHA). The endurance exercise markedly decreased activity of the powerful antioxidant enzyme, superoxide dismutase, but this effect was partially mitigated by the omega-3 fatty acids. Supplementation with the omega-3 fatty acids also tended to increase catalase antioxidant enzyme activity in response to exercise and this activity was significantly higher after one hour of recovery . Additionally, a six-week double-blind, randomized, placebo-controlled supplementation trial revealed that fish oil supplementation reduced selected markers of oxidative stress after a single bout of eccentric knee contractions .
Ultimately, exercise-induced stress is problematic because it can lead to suppression of the immune system (reviewed in ).Omega-3 fatty acids may help to attenuate some of these adverse immune responses to intensive training. For example, supplementation with fish oil (950 mg EPA + 500 mg DHA daily) improved exercise-associated immune responses in competitive swimmers over a six week period . Supplementation with 3,000 mg daily of fish oil in a 60-day controlled trial was also shown to prevent some of the negative changes in immunity induced by running a marathon in 21 runners .
Overall, these results suggest that omega-3 fatty acids may help to improve the body’s reaction to exercise-induced stress, with potential benefits for the immune system.
5. Fish oil may strengthen bones
Physical activity is widely known to exert positive effects on bone health (reviewed in ). While nutritional supplements, including calcium and magnesium have received a lot of attention for their bone benefits, omega-3 fatty acids are generally overlooked despite the fact that dietary fats may play a role in bone health through the inflammatory pathway (reviewed in ). Research reveals that higher red blood cell omega-3 levels may reduce the risk of hip fractures and promote higher bone mineral density [34-36]. Supplementation trials have also provided some encouraging preliminary results. For example, a 16-week trial involving 56 healthy postmenopausal women reported that aerobic exercise (walking and jogging up to 65% of maximum heart rate three times a week) and omega-3 fatty acids (180 mg EPA + 120 mg DHA) positively affect calcium regulating hormones both alone and in combination . In fact, omega-3 fatty acids and exercise may work synergistically to improve bone health according to a 24-week study involving 79 healthy postmenopausal women; long-term aerobic exercise training (walking and jogging up to 65% of maximum heart rate three times a week) plus omega-3 fatty acid supplementation (180 mg EPA + 120 mg DHA) had a synergistic effect in augmenting bone mineral density. Results from this trial revealed that this bone benefit may be achieved through anti-inflammatory activity .
These preliminary studies suggest that omega-3 fatty acids may play an important bone-strengthening role and this effect has been noted at a relatively low dose of only 300 mg of EPA+DHA daily.
6. Fish oil improves cardio-respiratory functioning
Omega-3 fatty acids have beneficial effects on exercise parameters in people with heart disease, including heart rate at rest, heart rate recovery, heart rate variability, exercise capacity, exercise time, and blood vessel dilation [38-41]. Since omega-3 fatty acids seem to positively impact the cardio-respiratory system in people with heart disease, interest has been expressed regarding fish oil’s potential to benefit exercise parameters in healthy individuals and athletes.
Exercise helps to improve cardiovascular functioning by improving the heart’s ability to pump blood and consequently deliver oxygen to working muscles. Dietary fat also impacts cardiovascular performance . This has been shown in two small supplementation studies involving healthy subjects whereby omega-3 fatty acids (3 grams EPA + 2 grams DHA) improved blood flow [43, 44]. Omega-3 fatty acid supplementation has also proven effective at improving heart parameters in athletes. For example, a five-week randomized, double-blind study in elite Australian Rules football players revealed that 1.92 grams of EPA + DHA daily decreased diastolic blood pressure and heart rate during submaximal exercise . An eight-week double-blind, parallel design trial involving 16 well-trained male cyclists reported similar results as 3.2 grams of EPA + DHA lowered heart rate, whole-body oxygen consumption, and the heart’s oxygen consumption .
Exercise also strengthens and tones the lungs, which enables the pulmonary system to increase the maximum amount of oxygen that the lungs can handle. Preliminary research reveals that fish oil may actually improve lung function during exercise. For example, a 12-week placebo-controlled trial involving 40 healthy young male wrestlers performing incremental training (up to 95% of exercise maximum heart rate) revealed that a low daily dose of omega-3 fatty acids (180 mg EPA + 120 mg DHA) improved scores on numerous lung function tests . Fish oil supplementation may also improve pulmonary functioning in athletes who suffer from wheezing, coughing, and shortness of breath. In a three-week randomized, double-blind crossover study involving elite athletes with exercise-induced airway constriction, fish oil (3.2 g EPA + 2.2 g DHA) improved lung function following exercise . Another three-week randomized, double-blind crossover study involving 16 asthmatic patients revealed that fish oil (3.2 g EPA + 2.0 g DHA) improved lung function and reduced the usage of asthma medication . Both of these studies reported that fish oil supplementation significantly reduced various inflammatory mediators [48, 49].
While this research is in its infancy, it provides an indication that fish oil supplementation may help to improve both heart and lung functioning in athletes with and without exercise-induced airway constriction.
7. Fish oil improves cognitive function
Improving complex cognitive ability during exercise may boost performance in sports that have strong cognitive demands. Omega-3 fatty acid supplementation may serve to enhance decision making and reaction time efficiency in athletes by increasing communication between the brain and body. Fish oil (1.6 grams EPA + 0.8 grams DHA) has been shown to be associated with improved attention, reduced reaction times, and increased vigour in healthy subjects. Furthermore, exercise and omega-3 fatty acids may work synergistically to improve brain function and cognition (reviewed in ). For example, omega-3 fatty acids (1.2 grams EPA + 0.6 grams DHA) plus policosanol improved mood state, reduced reaction time, and increased vigour in a 21-day placebo-controlled trial involving 18 healthy practitioners of karate; the positive effects on mood persisted even 21 days after discontinuation of supplementation . Another 4-week double-blind placebo-controlled study revealed that omega-3 fatty acids (3.5 grams DHA) improved complex reaction time and efficiency .
Based on the available research, fish oil supplementation may serve as an exciting strategy to improve athletic performance by enhancing concentration and cognitive functioning.
The North American population consumes inadequate amounts of omega-3 fatty acids but this can easily be remedied with fish oil supplementation. While omega-3 fatty acids boost overall health, reduce inflammation, and offer prevention and treatment strategies for various health conditions, they also offer performance-enhancing benefits that can help athletes of all levels.
1. Gomez, J., M. American Academy of Pediatrics Committee on Sports, and Fitness, Use of performance-enhancing substances. Pediatrics, 2005. 115(4): p. 1103-6.
2. Heikkinen, A., et al., Dietary supplementation habits and perceptions of supplement use among elite Finnish athletes. Int J Sport Nutr Exerc Metab, 2011. 21(4): p. 271-9.
3. Sanchez-Benito, J.L., E. Sanchez-Soriano, and J.G. Suarez, Unbalanced intake of fats and minerals associated with hypertension risk in young cyclists. Nutr Hosp, 2007. 22(5): p. 552-9.
4. Simopoulos, A.P., Evolutionary aspects of the dietary omega-6:omega-3 fatty acid ratio: medical implications. World Rev Nutr Diet, 2009. 100: p. 1-21.
5. Eaton, S.B. and M. Konner, Paleolithic nutrition. A consideration of its nature and current implications. N Engl J Med, 1985. 312(5): p. 283-9.
6. Eaton, S.B., S.B. Eaton, 3rd, and M.J. Konner, Paleolithic nutrition revisited: a twelve-year retrospective on its nature and implications. Eur J Clin Nutr, 1997. 51(4): p. 207-16.
7. Dideriksen, K., S. Reitelseder, and L. Holm, Influence of amino acids, dietary protein, and physical activity on muscle mass development in humans. Nutrients, 2013. 5(3): p. 852-76.
8. Wiens, K., et al., Dietary Supplement Usage, Motivation, and Education in Young, Canadian Athletes. Int J Sport Nutr Exerc Metab, 2014.
9. Macaluso, F., et al., Do fat supplements increase physical performance? Nutrients, 2013. 5(2): p. 509-24.
10. Di Girolamo, F.G., et al., Omega-3 fatty acids and protein metabolism: enhancement of anabolic interventions for sarcopenia. Curr Opin Clin Nutr Metab Care, 2014. 17(2): p. 145-50.
11. McDonald, C., J. Bauer, and S. Capra, Omega-3 fatty acids and changes in LBM: alone or in synergy for better muscle health? Can J Physiol Pharmacol, 2013. 91(6): p. 459-68.
12. Gingras, A.A., et al., Long-chain omega-3 fatty acids regulate bovine whole-body protein metabolism by promoting muscle insulin signalling to the Akt-mTOR-S6K1 pathway and insulin sensitivity. J Physiol, 2007. 579(Pt 1): p. 269-84.
13. Smith, G.I., et al., Omega-3 polyunsaturated fatty acids augment the muscle protein anabolic response to hyperinsulinaemia-hyperaminoacidaemia in healthy young and middle-aged men and women. Clin Sci (Lond), 2011. 121(6): p. 267-78.
14. Smith, G.I., et al., Dietary omega-3 fatty acid supplementation increases the rate of muscle protein synthesis in older adults: a randomized controlled trial. Am J Clin Nutr, 2011. 93(2): p. 402-12.
15. Robinson, S.M., et al., Diet and its relationship with grip strength in community-dwelling older men and women: the Hertfordshire cohort study. J Am Geriatr Soc, 2008. 56(1): p. 84-90.
16. Hutchins-Wiese, H.L., et al., The impact of supplemental n-3 long chain polyunsaturated fatty acids and dietary antioxidants on physical performance in postmenopausal women. J Nutr Health Aging, 2013. 17(1): p. 76-80.
17. Rodacki, C.L., et al., Fish-oil supplementation enhances the effects of strength training in elderly women. Am J Clin Nutr, 2012. 95(2): p. 428-36.
18. Schoenfeld, B.J., The use of nonsteroidal anti-inflammatory drugs for exercise-induced muscle damage: implications for skeletal muscle development. Sports Med, 2012. 42(12): p. 1017-28.
19. Calder, P.C., n-3 fatty acids, inflammation and immunity: new mechanisms to explain old actions. Proc Nutr Soc, 2013. 72(3): p. 326-36.
20. Fetterman, J.W., Jr. and M.M. Zdanowicz, Therapeutic potential of n-3 polyunsaturated fatty acids in disease. Am J Health Syst Pharm, 2009. 66(13): p. 1169-79.
21. Tartibian, B., B.H. Maleki, and A. Abbasi, Omega-3 fatty acids supplementation attenuates inflammatory markers after eccentric exercise in untrained men. Clin J Sport Med, 2011. 21(2): p. 131-7.
22. Tartibian, B., et al., Long-term aerobic exercise and omega-3 supplementation modulate osteoporosis through inflammatory mechanisms in post-menopausal women: a randomized, repeated measures study. Nutr Metab (Lond), 2011. 8: p. 71.
23. Jouris, K.B., J.L. McDaniel, and E.P. Weis, The effect of omega-3 fatty acid supplementation on the inflammatory response to eccentric strength exercise. JSSM, 2011. 10: p. 432-438.
24. Tartibian, B., B.H. Maleki, and A. Abbasi, The effects of ingestion of omega-3 fatty acids on perceived pain and external symptoms of delayed onset muscle soreness in untrained men. Clin J Sport Med, 2009. 19(2): p. 115-9.
25. Karacabey, K., Effect of regular exercise on health and disease. Neuro Endocrinol Lett, 2005. 26(5): p. 617-23.
26. Venkatraman, J.T. and D.R. Pendergast, Effect of dietary intake on immune function in athletes. Sports Med, 2002. 32(5): p. 323-37.
27. Powers, S.K. and M.J. Jackson, Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev, 2008. 88(4): p. 1243-76.
28. Poprzecki, S., et al., Modification of blood antioxidant status and lipid profile in response to high-intensity endurance exercise after low doses of omega-3 polyunsaturated fatty acids supplementation in healthy volunteers. Int J Food Sci Nutr, 2009. 60 Suppl 2: p. 67-79.
29. Gray, P., et al., Fish Oil Supplementation Reduces Markers of Oxidative Stress But Not Muscle Soreness After Eccentric Exercise. Int J Sport Nutr Exerc Metab, 2013.
30. Andrade, P.M., et al., Effects of the fish-oil supplementation on the immune and inflammatory responses in elite swimmers. Prostaglandins Leukot Essent Fatty Acids, 2007. 77(3-4): p. 139-45.
31. Santos, V.C., et al., Effects of DHA-Rich Fish Oil Supplementation on Lymphocyte Function Before and After a Marathon Race. Int J Sport Nutr Exerc Metab, 2013. 23(2): p. 161-9.
32. Pigozzi, F., et al., Bone mineral density and sport: effect of physical activity. J Sports Med Phys Fitness, 2009. 49(2): p. 177-83.
33. Kelly, O.J., et al., Long-chain polyunsaturated fatty acids may mutually benefit both obesity and osteoporosis. Nutr Res, 2013. 33(7): p. 521-33.
34. Orchard, T.S., et al., The association of red blood cell n-3 and n-6 fatty acids with bone mineral density and hip fracture risk in the women’s health initiative. J Bone Miner Res, 2013. 28(3): p. 505-15.
35. Moon, H.J., et al., Positive correlation between erythrocyte levels of n-3 polyunsaturated fatty acids and bone mass in postmenopausal Korean women with osteoporosis. Ann Nutr Metab, 2012. 60(2): p. 146-53.
36. Jarvinen, R., et al., Associations of dietary polyunsaturated fatty acids with bone mineral density in elderly women. Eur J Clin Nutr, 2012. 66(4): p. 496-503.
37. Tartibian, B., B.H. Maleki, and A. Asghar, The calciotropic hormone response to omega-3 supplementation during long-term weight-bearing exercise training in post menopausal women. JSSM, 2010. 9: p. 245-252.
38. Moyers, B., et al., Relation of whole blood n-3 fatty acid levels to exercise parameters in patients with stable coronary artery disease (from the heart and soul study). Am J Cardiol, 2011. 107(8): p. 1149-54.
39. O’Keefe, J.H., Jr., et al., Effects of omega-3 fatty acids on resting heart rate, heart rate recovery after exercise, and heart rate variability in men with healed myocardial infarctions and depressed ejection fractions. Am J Cardiol, 2006. 97(8): p. 1127-30.
40. Ninio, D.M., et al., Docosahexaenoic acid-rich fish oil improves heart rate variability and heart rate responses to exercise in overweight adults. Br J Nutr, 2008. 100(5): p. 1097-103.
41. Tagawa, T., et al., Long-term treatment with eicosapentaenoic acid improves exercise-induced vasodilation in patients with coronary artery disease. Hypertens Res, 2002. 25(6): p. 823-9.
42. Rontoyanni, V.G., et al., A comparison of the changes in cardiac output and systemic vascular resistance during exercise following high-fat meals containing DHA or EPA. Br J Nutr, 2012. 108(3): p. 492-9.
43. Walser, B., R.M. Giordano, and C.L. Stebbins, Supplementation with omega-3 polyunsaturated fatty acids augments brachial artery dilation and blood flow during forearm contraction. Eur J Appl Physiol, 2006. 97(3): p. 347-54.
44. Walser, B. and C.L. Stebbins, Omega-3 fatty acid supplementation enhances stroke volume and cardiac output during dynamic exercise. Eur J Appl Physiol, 2008. 104(3): p. 455-61.
45. Buckley, J.D., et al., DHA-rich fish oil lowers heart rate during submaximal exercise in elite Australian Rules footballers. J Sci Med Sport, 2009. 12(4): p. 503-7.
46. Peoples, G.E., et al., Fish oil reduces heart rate and oxygen consumption during exercise. J Cardiovasc Pharmacol, 2008. 52(6): p. 540-7.
47. Tartibian, B., B.H. Maleki, and A. Abbasi, The effects of omega-3 supplementation on pulmonary function of young wrestlers during intensive training. J Sci Med Sport, 2010. 13(2): p. 281-6.
48. Mickleborough, T.D., et al., Fish oil supplementation reduces severity of exercise-induced bronchoconstriction in elite athletes. Am J Respir Crit Care Med, 2003. 168(10): p. 1181-9.
49. Mickleborough, T.D., et al., Protective effect of fish oil supplementation on exercise-induced bronchoconstriction in asthma. Chest, 2006. 129(1): p. 39-49.
50. Fontani, G., et al., Cognitive and physiological effects of Omega-3 polyunsaturated fatty acid supplementation in healthy subjects. Eur J Clin Invest, 2005. 35(11): p. 691-9.
51. Gomez-Pinilla, F., Collaborative effects of diet and exercise on cognitive enhancement. Nutr Health, 2011. 20(3-4): p. 165-9.
52. Fontani, G., et al., Effect of omega-3 and policosanol supplementation on attention and reactivity in athletes. J Am Coll Nutr, 2009. 28 Suppl: p. 473S-481S.
53. Guzmán, J.F., et al., DHA- rich fish oil improves complex reaction time in female elite soccer players. JSSM, 2011. 10: p. 301-305.