Medicine & Science in Sports & Exercise:
Roundtable Consensus Statement
Physical activity and the progressive change in body composition with aging: current evidence and research issues
TOTH, MICHAEL J.; BECKETT, TRAVIS; POEHLMAN, ERIC T.
Division of Clinical Pharmacology and Metabolic Research, Department of Medicine, University of Vermont, Burlington, VT 05405
Address for correspondence: Eric T. Poehlman, Ph.D., Given Building C-247, University of Vermont, Burlington, VT 05405. E-mail: email@example.com.
Roundtable held February 4–7, 1999, Indianapolis, IN.
TOTH, M. J., T. BECKETT, and E. T. POEHLMAN. Physical activity and the progressive change in body composition with aging: current evidence and research issues. Med. Sci. Sports Exerc., Vol. 31, No. 11, Suppl., pp. S590–S596, 1999.
Purpose: The purpose was to review studies that have examined the effect of aerobic (AEX) or resistance exercise (REX) on body composition in older individuals (>55 yr). Our goal was to examine the effect of these two exercise paradigms on fat mass and fat-free mass and to consider those factors that may explain variability in findings among studies.
Methods: We conducted a literature search (Medline, 1984–1999) for intervention studies (at least 2 months in duration) that have examined the independent effect of either REX or AEX on body composition in older individuals.
Results: AEX decreased fat mass (range: −0.4 to −3.2 kg) but had little effect on fat-free mass. The change in fat mass with AEX was related to the duration of the exercise program (r = 0.51;P < 0.02) but not to body composition methodology. In contrast, REX reduced fat mass (range: −0.9 to −2.7 kg) and increased fat-free mass (range: 1.1 to 2.1 kg). Changes in body composition with REX were not related to body composition methodology or the duration of the exercise program.
Conclusion: Both AEX and REX appear to be beneficial in reducing body fat. REX appears to have the additional benefit of increasing fat-free mass.
In recent years, a significant number of studies have examined the effect of physical activity on body composition in older individuals. The high level of interest in this topic is partly mediated by the recognition of: 1) the reported age-related changes in physical activity, body composition, and their impact on health risk and 2) the potential role that increasing physical activity may have on improving cardiovascular and metabolic health in older individuals. This area of investigation, coupled with significant improvements in methods to measure energy expenditure (i.e., doubly labeled water) and body composition, have broadened our understanding of the relationship between physical activity and body composition.
Physical activity declines with age. The decline in physical activity and associated reduction in daily energy expenditure are thought to be important mediators of deleterious changes in body composition. Concomitant with the decline in physical activity, a loss of fat-free mass (specifically, skeletal muscle mass) and increase in fat mass is frequently observed. These age-related changes in body composition contribute to increased disease risk and reduced functional independence in the elderly. It is important to note, however, that these conclusions are derived primarily from cross-sectional observations. Thus, the “true” rate of age-related changes in body composition remains enigmatic. Moreover, given the paucity of longitudinal studies that have measured physical activity and body composition, it is currently unclear which of these events is primary and which is secondary.
Despite the absence of causal evidence that age-related changes in body composition are the result of a decline in physical activity, investigators have begun to examine the effects of physical activity on body composition using exercise training experiments. In this review we examine exercise intervention studies that have focused on older men and women. We considered the independent effects of aerobic (AEX) and resistance exercise (REX) training on body composition. The rationale for separating these two exercise paradigms is that their effects on body composition may differ: AEX primarily reduces body fat by promoting negative energy imbalance, whereas resistance exercise primarily increases fat-free mass by stimulating skeletal muscle growth. To review the current literature, a search was conducted using the Medline medical data base from 1984 to 1999 to locate studies (English language) that have examined the effect of either REX or AEX on total body composition. After locating articles through Medline, reference lists were searched for other studies not identified by the computer. Criteria for selection were: 1) articles published between 1984 and 1999; 2) subjects aged >55 yr; 3) an intervention design (i.e., pre- and postexercise measurements) of at least 2 months; 4) measurement of at least one component of body composition (i.e., either fat-free mass or fat mass) by either underwater weighing, dual energy x-ray absorptiometry, skinfolds, total body water, or in vivo neutron activation; and 5) no concomitant weight loss intervention (dietary restriction or pharmacological agent). Studies that examined the effect of combined AEX/REX on body composition were not included.
CURRENT STATUS OF KNOWLEDGE
The general conclusions drawn from this review of literature are that: 1) AEX is effective in reducing fat mass but has little effect on fat-free mass; 2) the magnitude of AEX-induced changes in fat mass are related to the total number of sessions in the exercise program; and 3) REX is effective in reducing fat mass and increasing fat-free mass.
Changes in Fat Mass with AEX
Evidence Statement: AEX is an effective intervention to decrease fat mass in older individuals. (Evidence Category C).
AEX was effective in reducing body fat stores in 20 out of 22 studies that did not instruct patients to maintain their body weight. The effect of AEX to reduce body fat is not unexpected, although the mechanism by which this change occurs is unclear. AEX-induced changes in body fat were not related to the method used to assess body composition. However, the change in fat mass was related to the total number of sessions in the AEX program (Fig. 1). That is, as the number of exercise sessions increased, the quantity of fat lost increased. Thus, the length of exposure to the exercise stimulus or the absolute caloric expenditure of the exercise program may be an important determinant of the amount of weight lost during AEX in older individuals.
The long-standing theory is that AEX reduces body fat stores by promoting negative energy imbalance (i.e., energy expenditure exceeds energy intake). Specifically, AEX increases daily energy expenditure in older individuals through the direct energetic cost of the exercise and possibly by increasing resting energy expenditure. Recent findings, however, showed that 8 wk of high-intensity AEX did not increase daily energy expenditure in older men and women (15). Thus, the effect of AEX on body fat stores may be mediated by changes in energy intake rather than changes in energy expenditure. Further studies are needed to delineate the mechanism by which AEX promotes a reduction in adiposity. Understanding the mechanism of AEX-induced changes in body composition will allow the refinement of exercise prescriptions (i.e., intensity and duration) to optimize reductions in body fat.
Changes in Fat-Free Mass with AEX
Evidence Statement: AEX is not an effective intervention to increase fat-free mass in older individuals. (Evidence Category C).
AEX does not appear to affect fat-free mass in older individuals. Only 8 out of 36 studies found an increase in fat-free mass, and this increase was less than 1 kg in most studies. Changes in the hydration of fat-free mass due to increased glycogen storage may account for these minimal changes in fat-free mass, although this has not been directly tested. The lack of effect of AEX on fat-free mass is not surprising, however, considering that this mode of exercise does not provide a significant anabolic stimulus to promote muscle growth. These results should not, however, be taken as evidence that AEX has no influence on fat-free mass. The possibility should be considered that AEX training may be effective in attenuating the age-related reduction in fat-free mass that results from inactivity and other hormonal and lifestyle factors. That is, AEX may provide an adequate stimulus to maintain fat-free mass with age. This hypothesis, however, has yet to be systematically tested.
Changes in Fat Mass with REX
Evidence Statement: REX is an effective intervention to decrease fat mass in older individuals. (Evidence Category C).
REX reduced fat mass in 15 out of 28 studies. On average, in the studies that found a reduction in fat mass with REX, the loss of fat mass was similar to those changes induced by AEX (REX: −1.7 ± 0.4 kg vs AEX: −1.9 ± 0.8 kg). This is somewhat surprising considering that the direct energetic cost of resistance exercise is smaller compared with that of AEX. Although REX has been shown to increase resting energy expenditure (7,43), similar changes have been found with AEX (39). Because no study has examined the effect of REX on free-living, daily energy expenditure, the effect of REX on energy balance remains unclear. Studies that examine changes in daily energy expenditure and its components with REX are needed to define the mechanism underlying REX-induced reductions in adiposity.
Changes in Fat-Free Mass with REX
Evidence Statement: REX is an effective intervention to increase fat-free mass in older individuals. (Evidence Category C).
In contrast to AEX, REX increased fat-free mass in 15 out of 28 studies (range: 1.1 to 2.1 kg). This finding is not surprising considering that REX is a potent anabolic stimulus to skeletal muscle growth. However, the specific component of fat-free mass that is increased with REX training has not been defined. Fat-free mass is a heterogenous compartment of body mass that is composed on a chemical level of minerals, water, protein and glycogen. Because the absolute (i.e., kilograms) contribution of minerals, protein, and glycogen to fat-free mass is quite small, changes in fat-free mass resulting from REX are likely caused by changes in body water. In support of this notion, data from Campbell et al. (5,6) showed that the increase in fat-free mass observed in older men and women following a 12-wk REX program was almost completely accounted for by an increase in total body water. Similar changes in total body water with REX training were found by Nelson et al. (35) in a 1-yr randomized study of older women. These changes in body water may be partially caused by increased skeletal muscle mass with REX. That is, REX-induced increases in skeletal muscle mass cause an increase in total body water because approximately 73% of skeletal muscle mass is water. Results from Nelson et al. (35) which showed that changes in total body water with REX primarily resulted from increased intracellular water support this conclusion. Thus, although REX appears to be effective in increasing fat-free mass in older men and women, a significant portion of this increase may be caused by changes in body water.
Body composition methodology and changes in fat mass and fat-free mass with exercise.
Recent developments in body composition methodology permit investigators to reliably assess multiple components of body mass. Despite these advances, however, most studies examining the effects of AEX and REX on body composition have employed the classic two-compartment model of body composition which divides body mass into fat and fat-free compartments. Because two-compartment models have been used, the specific tissue component of fat-free mass that changes with exercise has yet to be clearly defined. For example, as mentioned above, a significant portion of the REX-induced change in fat-free mass may be caused by changes in body water. Moreover, exercise-induced changes in body composition may be incorrect because of propagation of error. That is, in two-compartment models of body composition that measure one component of body composition and calculate the second component from the difference with body weight, error in the measured component of body composition is propagated to the calculated component. This may affect estimated changes in fat and fat-free mass with either AEX or REX. From these caveats, we can see that changes in body composition observed with AEX and REX may be dependent on the type of body composition methodology used. Thus, we recommend that future studies of the effects of AEX and REX on body composition in the elderly employ several body composition techniques to measure the various tissue components of fat-free mass, in particular body water, so as to clearly define the exact tissue components of body mass that are affected by AEX and REX.
Although our review of literature allows several tentative conclusions, many questions remain unanswered. We suggest the following questions and areas for future investigation:
• Only 10 of 36 AEX studies and 15 of 26 REX studies were randomized, controlled studies. Future studies should randomize subjects to exercise and control groups.
• What is the effect of gender in changes in body composition with AEX and REX? Most studies have not specifically compared the effect of gender on changes in body composition with AEX and REX despite a growing body of evidence that suggests a sex dimorphism in the response of certain hormonal and physiological systems to exercise.
• What is the effect of the intensity and duration (i.e., total number of exercise sessions) of the exercise intervention on body composition variables? Future studies should examine temporal changes in body composition with AEX and REX training regimens by conducting serial measurements of body composition throughout the exercise program and should examine AEX and REX programs of various intensities.
• What component or components of body composition are affected by AEX and REX training? Future studies should measure multiple components of body composition, including body water, using various techniques to determine the components of body composition affected by exercise.
• What is the mechanism underlying reductions in fat mass with AEX and REX training? Future studies should focus on measuring changes in energy expenditure and energy intake with AEX and REX training with doubly labeled water and multiple body composition methodologies.
This work was supported by a grant from the National Institutes of Health (AG-13978).
1. Ades, P. A., D. L. Ballor, T. Ashikaga, J. L. Utton, and K. S. Nair. Weight training improves walking endurance in healthy elderly persons. Ann. Intern. Med. 124: 568–572, 1996.
2. Binder, E. F., S. J. Birge, and W. M. Kohrt. Effects of endurance exercise and hormone replacement therapy on serum lipids in older women. J. Am. Geriatr. Soc. 44: 231–236, 1996.
3. Brown, M., S. J. Birge, and W. M. Kohrt. Hormone replacement therapy does not augment gains in muscle strength or fat-free mass in response to weight-bearing exercise. J. Gerontol. Ser. A, Biol. Sci. Med. Sci. 52: B166-B170, 1997.
4. Butterworth, D. E., D. C. Nieman, R. Perkins, B. J. Warren, and R. G. Dotson. Exercise training and nutrient intake in elderly women. J. Am. Diet. Assoc. 93: 653–657, 1993.
5. Campbell, W. W., J. O. Lyndon, S. L. Davey, D. C. Campbell, R. A. Anderson, and W. J. Evans. Effects of resistance training and chromium picolinate on body composition and skeletal muscle in older men. J. Appl. Physiol. 86: 29–39, 1999.
6. Campbell, W. W., M. C. Crim, V. R. Young, and W. J. Evans. Increased energy requirements and changes in body composition with resistance training in older adults. Am. J. Clin. Nutr. 60: 167–175, 1994.
7. Campbell, W. W., M. C. Crim, V. R. Young, L. J. Joseph, and W. J. Evans. Effects of resistance training and dietary protein intake on protein metabolism in older adults. Am. J. Physiol. 268: E1143-E1153, 1995.
8. Coggan, A. R., R. J. Spina, D. S. King, et al. Skeletal muscle adaptations to endurance training in 60- to 70-yr-old men and women. J. Appl. Physiol. 72: 1780–1786, 1992.
9. Coon, P. J., E. R. Bleecker, D. T. Drinkwater, D. A. Meyers, and A. P. Goldberg. Effects of body composition and exercise capacity on glucose tolerance, insulin, and lipoprotein lipids in healthy older men: a cross-sectional and longitudinal intervention study. Metabolism 38: 1201–1209, 1989.
10. Craig, B. W., J. Everhart, and R. Brown. The influence of high-resistance training on glucose tolerance in young and elderly subjects. Mech. Ageing Dev. 49: 147–157, 1989.
11. Cunningham, D. A., P. A. Rechnitzer, J. H. Howard, and A. P. Donner. Exercise training of men at retirement: a clinical trial. J. Gerontol. 42: 17–23, 1987.
12. Dupler, T. L. and C. Cortes. Effects of a whole-body resistive training regimen in the elderly. Gerontology 39: 314–319, 1993.
13. Ehsani, A. A., T. Ogawa, T. R. Miller, R. J. Spina, and S. M. Jilka. Exercise training improves left ventricular systolic function in older men. Circulation 83: 96–103, 1991.
14. Fiatarone, M. A., E. F. O’Neill, N. D. Ryan, et al. Exercise training and nutritional supplementation for physical frailty in very elderly people. N. Engl. J. Med. 330: 1769–1775, 1994.
15. Goran, M. I. and E. T. Poehlman. Endurance training does not enhance total energy expenditure in healthy elderly persons. Am. J. Physiol. 263: E950-E957, 1992.
16. Hagberg, J. M., J. E. Graves, M. Limacher, et al. Cardiovascular responses of 70- to 79-yr-old men and women to exercise training. J. Appl. Physiol. 66: 2589–2594, 1989.
17. Hersey, W. C., J. E. Graves, M. L. Pollock, et al. Endurance exercise training improves body composition and plasma insulin responses in 70- to 79-year-old men and women. Metabolism 43: 847–854, 1994.
18. Hurley, B. F., R. A. Redmond, R. E. Pratley, M. S. Treuth, M. A. Rogers, and A. P. Goldberg. Effects of strength training on muscle hypertrophy and muscle cell disruption in older men. Int. J. Sports Med. 16: 378–384, 1995.
19. Kahn, S. E., V. G. Larson, J. C. Beard, et al. Effect of exercise on insulin action, glucose tolerance, and insulin secretion in aging. Am. J. Physiol. 258: E937–E943, 1990.
20. Katzel, L. I., E. R. Bleecker, E. G. Colman, E. M. Rogus, J. D. Sorkin, and A. P. Goldberg. Effects of weight loss vs aerobic exercise training on risk factors for coronary disease in healthy, obese, middle-aged and older men: a randomized controlled trial. JAMA 274: 1915–1921, 1995.
21. Katzel, L. I., E. R. Bleecker, E. M. Rogus, and A. P. Goldberg. Sequential effects of aerobic exercise training and weight loss on risk factors for coronary disease in healthy, obese middle-aged and older men. Metabolism 46: 1441–1447, 1997.
22. King, A. C., W. L. Haskell, C. B. Taylor, H. C. Kraemer, and R. F. Debusk. Group- vs home-based exercise training in healthy older men and women: a community-based clinical trial. JAMA 266: 1535–1542, 1991.
23. Kirwan, J. P., W. M. Kohrt, D. M. Wojta, R. E. Bourey, and J. O. Holloszy. Endurance exercise training reduces glucose-stimulated insulin levels in 60- to 70-year-old men and women. J. Gerontol. 93: M84–90, 1993.
24. Koffler, K. H., A. Menkes, R. A. Redmond, W. E. Whitehead, R. E. Pratley, and B. F. Hurley. Strength training accelerates gastrointestinal transit in middle-aged and older men. Med. Sci. Sports. Exerc. 24: 415–419, 1992.
25. Kohrt, W. M., A. A. Ehsani, and S. J. Birge, JR. HRT preserves increases in bone mineral density (BMD) and reductions in body fat after a supervised exercise program. J. Appl. Physiol. 84: 1506–1512, 1998.
26. Kohrt, W. M., K. A. Obert, and J. O. Holloszy. Exercise training improves fat distribution patterns in 60- to 70-year-old men and women. J. Geronol. 47: M99-M105, 1992.
27. Kohrt, W. M., D. B. Snead, E. Slatopolsky, and S. J. Birge, Jr. Additive effects of weight-bearing exercise and estrogen on BMD in older women. J. Bone Miner. Res. 10: 1303–1311, 1995.
28. Kohrt, W. M., A. A. Ehsani, and S. J. Birge, Jr. Effects of exercise involving predominantly either joint-reaction or ground-reaction forces on BMD in older women. J. Bone Miner. Res. 12: 1253–1261, 1997.
29. Lan, C., J. S. Lai, S. Y. Chen, and M. K. Wong. 12-month Tai Chi training in the elderly: its effect on health fitness. Med. Sci. Sports. Exerc. 30: 345–351, 1998.
30. Menkes, A., S. Mazel, R. A. Redmond, et al. Strength training increases regional BMD and bone remodeling in middle-aged and older men. J. Appl. Physiol. 74: 2478–2484, 1993.
31. Meredith, C. N., W. R. Frontera, E. C. Fisher, et al. Peripheral effects of endurance training in young and old subjects. J. Appl. Physiol. 66: 2844–2849, 1989.
32. Meredith, C. N., W. R. Frontera, K. P. O’Reilly, and W. J. Evans. Body composition in elderly men: effect of dietary modification during strength training. J. Am. Ger. Soc. 40: 155–162, 1992.
33. Miller, J. P., R. E. Pratley, A. P. Goldberg, et al. Strength training increases insulin action in healthy 50- to 65-yr-old men. J. Appl. Physiol. 77: 1122–1127, 1994.
34. Nelson, M. E., E. C. Fisher, F. A. Dilmanian, G. E. Dallal, and W. J. Evans. A 1-yr walking program and increased dietary calcium in postmenopausal women: effects on bone. Am. J. Clin. Nutr. 53: 1304–1311, 1991.
35. Nelson, M. E., M. A. Fiatarone, J. E. Layne, et al. Analysis of body-composition techniques and models for detecting change in soft tissue with strength training. Am. J. Clin. Nutr. 63: 678–686, 1996.
36. Nichols, J. F., D. K. Omizo, K. K. Peterson, and K. P. Nelson. Efficacy of heavy-resistance training for active women over sixty: muscular strength, body composition, and program adherence. J. Am. Ger. Soc. 41: 205–210, 1993.
37. Nieman, D. C., B. J. Warren, K. A. O’Donnell, R. G. Dotson, D. E. Butterworth, and D. A. Henson. Physical activity and serum lipids and lipoproteins in elderly women. J. Am. Ger. Soc. 41: 1339–1344, 1993.
38. Pickering, G. P., N. Fellmann, B. Morio, et al. Effects of endurance training on the cardiovascular system and water compartments in elderly subjects. J. Appl. Physiol. 83: 1300–1306, 1997.
39. Poehlman, E. T. and E. Danforth, Jr. Endurance training increases metabolic rate and norepinephrine appearance rate in older individuals. Am. J. Physiol. 261: E233-E239, 1991.
40. Poehlman, E. T., A. W. Gardner, and M. I. Goran. Influence of endurance training on energy intake, norepinephrine kinetics, and metabolic rate in older individuals. Metabolism 41: 941–948, 1992.
41. Poehlman, E. T., A. W. Gardner, P. J. Arciero, M. I. Goran, and J. Calles-Escandon. Effects of endurance training on total fat oxidation in elderly persons. J. Appl. Physiol. 76: 2281–2287, 1994.
42. Posner, J. D., K. M. Gorman, L. Windsor-Landsberg, et al. Low to moderate intensity endurance training in healthy older adults: physiological responses after four months. J. Am. Ger. Soc. 40: 1–7, 1992.
43. Pratley, R., B. Nicklas, M. Rubin, et al. Strength training increases resting metabolic rate (RMR) and norepinephrine levels in healthy 50- to 65-yr-old men. J. Appl. Physiol. 94: 133–137, 1994.
44. Rall, L. C., S. N. Meydani, J. J. Kehayias, B. Dawson-Hughes, and R. Roubenoff. The effect of progressive resistance training in rheumatoid arthritis. Increased strength without changes in energy balance or body composition. Arthritis Rheum. 39: 415–426, 1996.
45. Ryan, A. S., R. E. Pratley, D. Elahi, and A. P. Goldberg. Resistive training increases fat-free mass and maintains RMR despite weight loss in postmenopausal women. J. Appl. Physiol. 79: 818–823, 1995.
46. Ryan, A. S., R. E. Pratley, A. P. Goldberg, and D. Elahi. Resistive training increases insulin action in postmenopausal women. J. Gerontol. 51: M199-M205, 1996.
47. Schwartz, R. S. Effects of exercise training on high density lipoprotein (HDL)s and apolipoprotein A-I in old and young men. Metabolism 88: 1128–1133, 1988.
48. Schwartz, R. S., K. C. Cain, W. P. Shuman, et al. Effect of intensive endurance training on lipoprotein profiles in young and older men. Metabolism 92: 649–654, 1992.
49. Seals, D. R., J. M. Hagberg, B. F. Hurley, A. A. Ehsani, and J. O. Holloszy. Effects of endurance training on glucose tolerance and plasma lipid levels in older men and women. JAMA 252: 645–649, 1984.
50. Sial, S., A. R. Coggan, R. C. Hickner, and S. Klein. Training-induced alterations in fat and carbohydrate metabolism during exercise in elderly subjects. Am. J. Physiol. 274: E785-E790, 1998.
51. Spina, R. J., T. Ogawa, W. M. Kohrt, W. H. Martin, J. O. Holloszy, and A. A. Ehsani. Differences in cardiovascular adaptations to endurance exercise training between older men and women. J. Appl. Physiol. 75: 849–855, 1993.
52. Spina, R. J., T. Ogawa, T. R. Miller, W. M. Kohrt, and A. A. Ehsani. Effect of exercise training on left ventricular performance in older women free of cardiopulmonary disease. Am. J. Cardiol. 71: 99–104, 1993.
53. Spina, R. J., M. J. Turner, and A. A. Ehsani. Exercise training enhances cardiac function in response to an afterload stress in older men. Am. J. Physiol. 272: H995-H1000, 1997.
54. Thomas, S. G., D. A. Cunningham, P. A. Rechnitzer, A. P. Donner, and J. H. Howard. Determinants of the training response in elderly men. Med. Sci. Sports. Exerc. 17: 667–672, 1985.
55. Treuth, M. S., A. S. Ryan, R. E. Pratley, et al. Effects of strength training on total and regional body composition in older men. J. Appl. Physiol. 77: 614–620, 1994.
56. Treuth, M. S., G. R. Hunter, T. Kekes-Szabo, R. L. Weinsier, M. I. Goran, and Reduction in intra-abdominal adipose tissue after strength training in older women. J. Appl. Physiol. 78: 1425–1431, 1995.
57. Tsutsumi, T., B. M. Don, L. D. Zaichkowsky, and L. L. Delizonna. Physical fitness and psychological benefits of strength training in community dwelling older adults. Appl. Hum. Sci. 16: 257–266, 1997.
58. Yarasheski, K. E., J. J. Zachwieja, J. A. Campbell, and D. M. Bier. Effect of growth hormone and resistance exercise on muscle growth and strength in older men. Am. J. Physiol. 268: E268-E276, 1995.
59. Yarasheski, K. E., J. A. Campbell, and W. M. Kohrt. Effect of resistance exercise and growth hormone on bone density in older men. Clin. Endocrinol. 47: 223–229, 1997.
RESISTANCE EXERCISE; AEROBIC EXERCISE; BODY COMPOSITION; ELDERLY
© 1999 Lippincott Williams & Wilkins, Inc.
Highlight selected keywords in the article text.