Journal of Applied Physiology
Vol. 81, No. 4, pp. 1584-1588, October 1996
EXERCISE AND MUSCLE

Mechanical overload and skeletal muscle fiber hyperplasia: a meta-analysis

George Kelley

Department of Physical Education, Northern Illinois University, DeKalb, Illinois 60115-2854

ABSTRACT

INTRODUCTION

METHODS

RESULTS

DISCUSSION

ACKNOWLEDGEMENTS

FOOTNOTES

REFERENCES

ABSTRACT

Kelley, George. Mechanical overload and skeletal muscle fiber hyperplasia: a meta-analysis. J. Appl. Physiol. 81(4): 1584-1588, 1996.With use of the meta-analytic approach, the purpose of this study was to examine the effects of mechanical overload on skeletal muscle fiber number in animals. A total of 17 studies yielding 37 data points and 360 subjects met the initial inclusion criteria: 1) "basic" research studies published in journals, 2) animals (no humans) as subjects, 3) control group included, 4) some type of mechanical overload (stretch, exercise, or compensatory hypertrophy) used to induce changes in muscle fiber number, and 5) sufficient data to accurately calculate percent changes in muscle fiber number. Across all designs and categories, statistically significant increases were found for muscle fiber number [15.00 ± 19.60% (SD), 95% confidence interval = 8.65-21.53], muscle fiber area (31.60 ± 44.30%, 95% confidence interval = 16.83-46.37), and muscle mass (90.50 ± 86.50%, 95% confidence interval = 61.59-119.34). When partitioned according to the fiber-counting technique, larger increases in muscle fiber number were found by using the histological vs. nitric acid digestion method (histological = 20.70%, nitric acid digestion = 11.10%; P = 0.14). Increases in fiber number partitioned according to species were greatest among those groups that used an avian vs. mammalian model (avian = 20.95%, mammalian = 7.97%; P = 0.07). Stretch overload yielded larger increases in muscle fiber number than did exercise and compensatory hypertrophy (stretch = 20.95%, exercise = 11.59%, compensatory hypertrophy = 5.44%; P = 0.06). No significant differences between changes in fiber number were found when data were partitioned according to type of control (intra-animal = 15.20%, between animal = 13.90%; P = 0.82) or fiber arrangement of muscle (parallel = 15.80%, pennate = 11.60%; P = 0.61). The results of this study suggest that in several animal species certain forms of mechanical overload increase muscle fiber number.

muscle mass; enlargement; hypertrophy

INTRODUCTION

RECENTLY, A NARRATIVE REVIEW has suggested that increases in muscle fiber number (hyperplasia) in animals occur as a result of stretch overload, whereas compensatory hypertrophy (ablation, tenotomy) does not generally change fiber number (8). In addition, it was also reported that exercise models in animals have led to mixed results with regard to increases in muscle fiber number (8). Although the above-mentioned review provided valuable information, it relied on the traditional narrative approach, that is, chronologically arranging and then describing studies. A need exists for the quantification of the magnitude and direction of changes in skeletal muscle fiber number as a result of different types of mechanical overload in animals. Thus the purpose of this study was to use the meta-analytic approach (12, 14, 20, 26) to examine the effect of different types of mechanical overload (stretch, exercise, and compensatory hypertrophy) on skeletal muscle fiber number in animals.

METHODS

RESULTS

Table 1. Study characteristics Reference Overload Subject Muscle Technique Alway (1) Chronic stretch Quail ALD NAD Alway (2) Chronic stretch Quail ALD Histo Alway (3) Chronic stretch Quail ALD Histo Alway et al. (4) Chronic stretch Quail ALD NAD Alway et al. (5) Chronic stretch Quail ALD NAD and Hist Antonio and Gonyea (6) Intermittent stretch Quail ALD Histo Antonio and Gonyea (7) Intermittent stretch Quail ALD Histo Antonio and Goynea (9) Intermittent stretch Quail ALD Histo Gollnick et al. (15) Chronic stretch Chicken ALD NAD Gollnick et al. (16) Ablation Rat Soleus, plantaris, and EDL NAD Gonyea (17) Weights Cat FCR Histo Gonyea (18) Weights Cat FCR Histo Gonyea et al. (19) Weights Cat FCR NAD Ho et al. (21) Weights Rat AL Histo Tamaki et al. (28) Sprints/weights Rat Plantaris NAD Timson et al. (30) Ablation Mice Soleus NAD Vaughan and Goldspink (31) Tenotomy Mice Soleus Histo ALD, anterior latissimus dorsi; EDL, extensor digitorum longus; FCR, flexor carpi radialis; AL, adductor longus; Histo, histological cross sections; NAD, nitric acid digestion.

Table 2. Changes in muscle fiber number for individual studies Reference No. of Subjects Treatment Control Difference Change, %  Alway (1) 5 1,653 ± 239  1,278 ± 145  375 29 Alway (2) 15 1,764 ± 221  1,208 ± 128  556 46 Alway (3) 12 1,766 ± 343  1,189 ± 270  577 48 Alway et al. (4) 10 1,251 ± 328  1,200 ± 367  51 4 9 1,247 ± 315  1,143 ± 304  104 9 8 1,240 ± 253  1,154 ± 148  86 7 8 1,247 ± 335  1,084 ± 202  162 15 8 1,283 ± 228  1,024 ± 176  258 25 9 1,305 ± 304  999 ± 167  306 31 9 1,462 ± 136  1,174 ± 102  287 24 Alway et al. (5) 12 1,945 ± 419  1,281 ± 287  664 52 Antonio and Gonyea (6) 7 1,626 ± 188  1,652 ± 251   26  1 Antonio and Gonyea (7) 5  10 5 0 6 2 5 31 5 82 Antonio and Gonyea (9) 6 1,500 ± 148  1,631 ± 286   131  8 6 1,803 ± 279  1,398 ± 210  405 29 Gollnick et al. (15) 12 4,216 ± 575  4,116 ± 821  100 24 Gollnick et al. (16) 11 2,914 ± 192  2,942 ± 192   28  1 15 10,526 ± 1,359  10,564 ± 1,139   38  0.4 5 5,224 ± 273  5,192 ± 74  32 0.6 11 2,914 ± 282  2,910 ± 268  4 0.1 10 11,521 ± 715  11,481 ± 721  40 0.3 4 5,232 ± 58  5,254 ± 102   22  0.4 Gonyea (17) 5 9,081 ± 1,027  7,609 ± 918  1,472 19 Gonyea (18) 6 39,759 ± NR 36,550 ± NR 3,209 9 Gonyea et al. (19) 6 9,055 ± 1,029  7,522 ± 570  1,533 20 4 7,817 ± 810  7,556 ± 854  261 3 Ho et al. (21) 15 2,477 ± 424  2,204 ± 530  273 12 Tamaki et al. (28) 8 12,559 ± 269  11,030 ± 304  1,529 14 8 11,349 ± 327  11,030 ± 304  319 3 Timson et al. (30) 18 958 ± 92  953 ± 85  5 0.5 Vaughan and Goldspink (31) 24 24  784 ± 220 933 ± 188  798 ± 82 752 ± 92   14 1,881  2 24  24 990 ± 144  749 ± 193  241 32 Values for treatment and control are means ± SD. NR, not recorded.

DISCUSSION

This meta-analysis attempted to quantify the magnitude of change in muscle (particularly muscle fiber number) as a result of mechanical overload. Across all designs and categories, mechanical overload resulted in increases in muscle mass, muscle fiber area (hypertrophy), and muscle fiber number (hyperplasia). Not surprisingly, increases in fiber area were approximately twice as great as increases in fiber number. It appears that hyperplasia in animals is greatest when certain types of mechanical overload, particularly stretch, are applied. The results of this investigation are similar to a recent narrative review that concluded that muscle fiber hyperplasia 1) consistently occurs as a result of chronic stretch, 2) rarely occurs with overload in the form of compensatory hypertrophy, and 3) has produced mixed results when overload in the form of exercise is employed (8). Although it is well established that mechanical-overload training results in increased fiber area (hypertrophy), and thus increases in muscle mass, the contribution of increased fiber number (hyperplasia) to increases in muscle mass has been more controversial. However, there now exists quantitative evidence to support the fact that certain types of overload, particularly stretch, result in increases in muscle fiber number. Unfortunately, it is beyond the scope of this investigation to examine the processes (satellite cell proliferation and longitudinal fiber splitting) responsible for such changes. The greater changes in muscle fiber number found in avian vs. mammalian species may not be the result of the species used so much as the fact that stretch was the mechanical overload employed on all avian species included in this meta-analysis. The fact that increases in fiber number were approximately twice as great when histological vs. nitric acid digestion methods were used is consistent with previous investigations (5, 6). Because of the ability to directly count each fiber, the nitric acid digestion method is generally considered to be the more accurate method of assessing changes in fiber number. However, small fibers may be missed when this method is used (8).

Despite the knowledge that studies can be more objectively evaluated by using the meta-analytic vs. traditional narrative approach, potential limitations still exist. In general, the very nature of meta-analysis dictates that the meta-analysis itself inherits those limitations that exist in the literature. For example, a review article by Timson (29) led him to conclude that none of the animal models (stretch, exercise, or compensatory hypertrophy) currently used to examine exercise-induced muscle enlargement truly represents the human strength-training situation under all conditions. In addition, the fact that 11 of the 17 studies involved essentially the same authors could have resulted in biased results. In summary, the results of this study suggest that in several animal species certain forms of mechanical overload increase muscle fiber number.

ACKNOWLEDGEMENTS

The author thanks Dr. Russ Moore (Dept. of Kinesiology, University of Colorado, Boulder, CO), Dr. Ben Timson (Dept. of Biomedical Science, Southwest Missouri State University, Springfield, MO), and Dr. Zung Vu Tran (College of Health and Human Sciences, University of Northern Colorado, Greeley, CO) for their assistance in the preparation of this manuscript.

FOOTNOTES

Address for reprint requests: G. Kelley, Exercise Science, Dept. of Physical Education, Northern Illinois Univ., Anderson Hall, Rm. 233, DeKalb, IL 60115-2854.

Received 26 February 1996; accepted in final form 15 February 1996.

REFERENCES