Background: Physical exercise plays an important role in metabolic health, especially in the insulin-like growth factor-1 (IGF-1) system. The objective of this study was to perform a systematic review and meta-analysis to evaluate the effects of a single endurance and resistance exercise session on IGF-1 serum. Methods: The systematic review was performed in SPORTDiscus, MEDLINE, PubMed, and Google Scholar databases. All analyses are based on random-effect models. The study identified 249 records of which 21 were included. Results: There was an effect of endurance exercise on total IGF-1 (P = .01), but not for free IGF-1 (P = .36). Resistance exercise similarly only affected total IGF-1 (P = .003) and not free IGF-1 (P = .37). The effect size indicated that total IGF-1 is more affected (ES = 0.81) by endurance than by resistance exercise (ES = 0.46). The present study showed that IGF-1 serum concentrations are altered by exercise type, but in conditions which are not well-defined. Conclusions: The systematic review and meta-analysis suggest that there is no determinant in serum IGF-1 changes for the exercise load characteristic. Therefore, physical exercise may be an alternative treatment to control changes in IGF-1 metabolism and blood concentration.

It is possible to notice that physical exercise plays an important role in endocrinal systems linked to muscle function. The muscle response to exercise results in acute hormone changes such as an increase in growth hormone (GH) and also perhaps on insulin-like growth factor-1 (IGF-1) levels.1

The IGF-1 is a polypeptide primarily produced in the liver, but it can be produced by the muscle. IGF-1 production is mainly controlled by the GH through the hypothalamic-pituitary axis.2 IGF-1 is found freely in the blood, linked to the binding protein carriers (IGBP1 to IGFBP6 proteins) and total IGF-1 form.

IGF-1 is important for the normal function of the organism and health maintenance. IGF-1 participates in several metabolic functions (eg, glycemic control), cellular proliferation, tissue growth, skeletal muscles, increased protein synthesis, and fat burning.1 In addition, epidemiological studies have associated serum IGF-1 levels with the risk of cardiovascular disease, cancer, and death.3 Thus, subjects with reduced IGF-1 concentration or change in function of this polypeptide (ie, GH axis abnormalities, diabetes, obesity, older people) can present a lack in some of these functions.3,4 Therefore, these subjects could benefit from regular practice of physical exercise as an alternative way to regulate levels and effects of IGF-1.

Physical exercise is a potential stimulus for GH release, and muscle contraction is an important stimulus for local production of IGF-1.5 It appears that both the central (GH–IGF-1 axis) and the local (muscle IGF-1) mechanisms are sensitive to the intensity and duration of muscle contraction. Previous studies have shown that serum GH concentration was higher after high-intensity and high-volume protocol,6 and muscle expression of IGF-1 is increased after endurance and resistance exercise.7

However, exercise has resulted in inconsistent effects on IGF-1 serum levels. Studies in the literature have pointed out increases, reductions, and no changes in the IGF-1 component group postexercise.813 In addition, the literature does not compare the effects of endurance and resistance exercise on IGF-1 serum.8,10,14 Endurance and resistance exercise at the same intensity have presented different metabolic, hormonal, and contraction rates. Thus, it is possible that blood IGF-1 concentrations may differ between these 2 types of physical exercise. Our knowledge on the dose–response relationship between different exercise protocols and the magnitude of their impact on free and total IGF-1 remain uncertain. Furthermore, no comparisons of the impacts of different exercise types have been presented using a meta-analysis.

Therefore, the objective of this study was to evaluate the effects of a physical exercise session and compare endurance and resistance exercise session on the level of IGF-1 serum through a meta-analysis of the scientific literature in an attempt to answer the question about the sensitivity of serum IGF-1 to different muscle contraction intensities and durations.

Methods

Literature Search

The review methodology adopted the Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines and was prospectively registered in the PROSPERO (register number: 176716) database for systematic reviews. Two authors (D.D.A.B. and E.D.S.A.) completed the selection process, data extraction, and quality appraisal. The SPORTDiscus, MEDLINE, PubMed, and Google Scholar databases were searched up until June 2019 for all studies, which investigated IGF-1 responses to exercise. The search was performed using the following keyword combinations in the English language: “IGF-1,” “exercise,” “resistance,” “endurance,” and its “mesh terms.” The present review includes studies which (1) present original research data on healthy human participants and (2) are published in peer-reviewed journals. No age, training status, or gender restrictions were imposed during the search stage.

Eligibility Criteria and Selection Process

Research studies investigating the effects of resistance and endurance exercise on IGF-1 were the primary focus of the literature search. A total of 249 studies were identified. The next step was to select studies according to the next home page filter: (1) human effects, (2) randomized controlled trial, (3) English language, and (4) age 19–44 years. A total of 98 studies were found in this stage. Then, each study was read to select the following inclusion criteria: (1) healthy subjects, (2) IGF-1 serum, and (3) acute effects. The IGF-1 analysis method was not considered as inclusion or exclusion criteria. After critically analyzing the initial studies collected with the previously mentioned criteria, 21 records were identified for complete reading (Figure 1).

Figure 1
Figure 1

—Study selection for systematic reviews and meta-analyses flow diagram.

Citation: Journal of Physical Activity and Health 17, 5; 10.1123/jpah.2019-0453

Meta-Analysis

The meta-analysis was conducted based on the number of free or total IGF-1 preexercise and postexercise. Then, 2 authors (E.D.S.A. and J.P.P.R.) were asked to review the selected articles for inclusion in the meta-analysis. The IGF-1 forms were required to be measured at baseline and postintervention with the aim of verifying the exercise effects on IGF-1 concentration in order to meet the inclusion criteria for the meta-analysis.

Quality Assessment

The quality of all studies was assessed by 2 authors (D.D.A.B. and E.D.S.A.) according to criteria of a study by Saw et al15 (Table 1). The scores were allocated based on how well each criterion was met, assuming that a maximum possible score of 8 (low risk of bias) and a risk of bias of 4 or less were considered to be bad and if necessary were therefore excluded.15 Kappa agreement (κ) was used by 2 reviewers (D.D.A.B. and L.A.F.) to describe the intensity of agreement. Publication bias was determined for the meta-analysis using an approach in which differences in baseline assessments were checked for all intervention groups. Next, the interventions were divided into nonsignificant (P > .05) or significant (P < .05) results to determine the percentage of interventions with nonsignificant differences. (These procedures were followed as per other meta-analyses.)16 All data were analyzed using the CMAv3 trial (version 3; Biostat, NJ) program and an Excel worksheet (version 2013; Microsoft, Redmond, WA).

Table 1

Risk of Bias Assessment Criteria

Scoring
CriteriaDefinition012
APeer reviewedStudy published in peer-reviewed journalNoYes
BNumber of participantsNumber of participants included in study findings<56–30>30
CPopulation definedAge, genderNoPartlyYes
DExperimental designStudy experimental design was described and replicableNoPartlyYes
EIGF-1 parametersThe IGF-1 parameters were describedNoYes

Statistical Analysis

Heterogeneity of the included studies was evaluated by examining forest plots, confidence intervals (CIs), and I2. The I2 values of 25, 50, and 75 indicate low, moderate, and high heterogeneity, respectively.17 Random effects were analyzed using the DerSimonian and Laird18 approach. Mean, SD, and statistics for all outcomes were selected for the meta-analysis, and SDs were calculated when the standard of error was reported using the formula SD=SE×n. If pertinent data were absent, the authors were contacted, and the necessary information was requested via e-mail. If the original data were not provided by the authors, the mean and SD were extracted from graphical representation using the Ycasd tool19 or estimated from the median, range, and sample size.20 Statistical significance was set at a level of P ≤ .05, and the magnitude of differences were calculated using effect size (ES) module with 95% CI. The sensitivity of the exercise protocol on IGF-1 serum was quantified using ES (large effect > 0.80, moderate effect 0.20–0.80, small effect < 0.20).21 The coefficient of variation (ie, [SD ÷ mean] × 100, with 95% CI) of each exercise protocol was calculated to interpret its respective level of instability.16 Variables with a large coefficient of variation are less likely (odds ratio) to detect statistically significant differences during repetitive measurements.18

Results

Systematic Review Findings

From the 21 studies analyzed, 12 were classified as resistance exercise, 8 as endurance exercise, and just 1 compared resistance and endurance exercise. The included studies involved a total of 299 participants. Age range based on mean and SD values presented by studies were 17–41 years. The participants were healthy, and physical activity levels ranged from sedentary to trained athletes. Endurance exercise mostly consisted of running or cycling, while one study used ski training. Resistance exercise used workout equipment, while 2 used a step exercise protocol with extra body mass load (Table 1). The exercise load components and more characteristics of studies included in the systematic review are presented in Tables 2 and 3.

Table 2

Characteristics of Endurance Studies Include in the Systematic Review

Endurance exercise
StudySampleExercise protocolIGF-1 serum changeComments
Brahm et al512 healthy individuals (6 men and 6 women; age 21–36 y)30 min of one leg with progressive load until exhaustion in bicycle ergometer→ arterial total IGF-1

↑ venous total IGF-1
 
Nguyen et al2225 healthy athletes; age 25 (1) yIncremental ergometer cycling exercise until exhaustion;

60-km international Nordic ski race

2 periods of 45 min separated by 15-min rest (soccer demand) (TSG)
↑ total IGF-1 after

↓ total IGF-1 after NSR

→ total IGF-1 after each half time
 
Wallace et al1217 trained men 26.9 (1.5) y30 min on a cycle ergometer; (80% VO2max)↑ total IGF-1 after

→ free IGF-1 after
Declining to baseline values 30 min after exercise
Wideman et al139 men (25 [1.5] y)

9 women (25 [1.0] y)
30 min on cycle ergometer (∼72% power output)→ total IGF-1 afterIGF-1 concentrations were similar in men and women
Eliakim et al1410 healthy adult male (27.8 [1.4] y)10-min unilateral wrist flexion↑ total IGF-1 10 min afterTotal IGF-1 levels increased in the resting arm too
Dall et al816 athletes both sex (8 women 23 [0.1] y, men 26 [0.9] y)30-min progressive load exercise (55%, 65%, 75%, and 85% of VO2max)↓ free IGF-1 after

↑ total IGF-1 during

→ total IGF-1 after
IGF-1 concentrations were similar in men and women after exercise
De Palo et al2320 male professional cyclists (19 [2] y)(1) 25-min cycling exercise (10-min warm-up+ 15 min at exhaustion)

(2) 40-min cycling exercise (10-min warm-up+ 15 min 70%–80% VO2max+15 min increasing workload until exhaustion)
↑ total IGF-1 after

↓ free IGF-1 after

↑ total IGF-1 after

→ free IGF-1 after
 
Rakover et al1112 women (27.3 [1.1] y)10-min treadmill run at 85% peak VO2→ total IGF-1 after 
Consitt et al2416 women (33 [8] y)40-min cycling at 75% HRmax→ free IGF-1 after 

Abbreviations: ICE, incremental ergometer cycling exercise; IGF, insulin-like growth factor-I; NSR, Nordic ski race; TSG, training soccer group.

Table 3

Characteristics of Resistance Studies Include in the Systematic Review

Resistance exercise
StudySampleExercise protocolIGF-1 serum changeComments
Nindl et al2510 young, healthy men (22 [1] y)50 resistance exercises (1 set of 5 or 10 RM (75% 1RM and 5RM (85% 1RM, respectively)→ total IGF-1 after

→ free IGF-1 after
 
Goekint et al2615 men (20.1 [0.4] y)6 resistance exercise (3 set × 10RM; 80% 1RM)→ total IGF-1 after 
Hasani-Ranjbar et al2710 healthy trained men (22.40 [1.84] y)

8 healthy untrained men (21.75 [0.89] y)
4 resistance exercise (3 set × 10RM; 70%–80% 1RM)→ total IGF-1 after both groups 
Taylor et al2812 men (20.2 [3.12] y)Single-legged resistance exercise

 (1) 8–10 reps; 80%–85% 1RM

 (2) 18–20 reps; 60%–65% 1RM
→ free IGF-1 after both exercises 
Forbes et al914 resistance trained males (25 [4] y)8 resistance exercises (3 sets × 10 reps; ∼75% 1RM)→ total IGF-1 after 
Rubin et al2910 men (23.3 [2.4] y)6 sets × 10 reps per leg of stepping on an elevated platform

(loading 50% of total body lean mass)
→ total IGF-1 after 
Rubin et al3010 men trained (24.6 [3.7] y)6 sets × 10 reps per leg of stepping onto an elevated platform (loading 50% of total body lean mass)→free IGF-1 after 
Gonzalez-Badillo et al319 men (23.3 [3.9] y)Bench press + squat (80% 1RM)

 (1) 3 sets × 8 reps until failure

 (2)3 sets × 4 reps no failure
↑ total IGF-1 after both protocolsIGF-1 was higher in 3 × 8 vs 3 × 4 reps
Fink et al3214 young athletes (20.0 [0.6] y)Squat + bench press

4 sets until at failure (40% 1RM)

Rest of 30 s

Rest of 150 s
↑ total IGF-1 after both protocolsThere was no difference between 2 protocols
Sheikholeslami-Vatani et al3315 men (21.73 [1.58] y)9 resistance exercise with different exercise order (A, large to small muscle; B, small to large muscle 3 sets until fail Load = 10RM)↑ total IGF-1 after both exercise orderIGF-1 was higher in A vs B

IGF-1 returned to baseline levels after 30 min of recovery
Pareja-Blanco et al3410 men (23.6 [3.7] y)Bench press + squat (70%1RM)

 (1) 3 sets × 12 reps until failure

 (2) 3 × 6 reps no failure
→ total IGF-1 afterIGF-1 after was higher in 3×6 compared with 3 × 12 protocol
Nindl et al1016 men (∼27–29 y)6 sets × 10 reps in the squat (∼75% 1RM)↑ total IGF-1 during and after

↓ free IGF-1 during and after
 
Consitt et al2416 women (33 [8] y)8 resistance exercise (4 set × 10–12 reps; 70%–80% 1RM)→ free IGF-1 after 

Abbreviations: 1RM, 1-repetition maximum; IGF, insulin-like growth factor-1.

Meta-Analysis Results

Included studies had a low risk of bias, with a score >4. The average bias score for the studies was 6 (range, 5–7). The studies of Consitt et al,24 Sheikholeslami-Vatani et al,33 and Taylor et al28 were excluded from the meta-analysis due to impossibility for data extraction. The meta-analysis results are summarized in Figures 25.

Figure 2
Figure 2

—The total IGF-1 meta-analysis for endurance exercise. ES indicates effect size; LCL, lower confidence limit; n, study population; UCL, upper confidence limit; WGHT, weight of study.

Citation: Journal of Physical Activity and Health 17, 5; 10.1123/jpah.2019-0453

Figure 3
Figure 3

—The free IGF-1 meta-analysis for endurance exercise. ES indicates effect size; LCL, lower confidence limit; n, study population; UCL, upper confidence limit; WGHT, weight of study.

Citation: Journal of Physical Activity and Health 17, 5; 10.1123/jpah.2019-0453

Figure 4
Figure 4

—The total IGF-1 meta-analysis for resistance exercise. ES indicates effect size; LCL, lower confidence limit; n, study population; UCL, upper confidence limit; WGHT, weight of study.

Citation: Journal of Physical Activity and Health 17, 5; 10.1123/jpah.2019-0453

Figure 5
Figure 5

—The free IGF-1 meta-analysis for resistance exercise. ES indicates effect size; LCL, lower confidence limit; n, study population; UCL, upper confidence limit; WGHT, weight of study.

Citation: Journal of Physical Activity and Health 17, 5; 10.1123/jpah.2019-0453

Endurance Exercise and IGF-1

A total of 4 data points (48 participants) reported positive effects of endurance exercise on total IGF-1 serum. Only one study (18 participants) reported negative effect (95% CI, −1.72 to −0.33; ES = −1.03; Figure 2). There was an effect of endurance exercise on total IGF-1 (95% CI, 0.19 to 1.43; P = .01; ES = 0.81; Figure 2), but not for free IGF-1 (95% CI, −0.73 to 0.23; ES = −023; P = .36; Figure 3).

Resistance Exercise and IGF-1

In total, 3 data points (33 participants) reported positive effects of endurance exercise on total IGF-1 serum. Similarly, the resistance exercise only affected total IGF1 (95% CI, 0.16 to −0.76; ES = 0.46; P = .003; Figure 4) and not free IGF-1 (95% CI, −0.38 to 0.41; ES = −1.2; P = .37; Figure 5). The ES indicated that total IGF-1 is more affected (ES = 0.81) by endurance exercise than by resistance exercise (ES = 0.46).

Discussion

The aim of this study was to evaluate the effects of an endurance and resistance exercise session on the IGF-1 serum level. A total of 21 studies were included for systematic review and 18 studies for meta-analysis. The overall results indicated that endurance or resistance exercise increase the total IGF-1, but not free IGF-1. In addition, endurance exercise showed higher ES on total IGF-1 than resistance exercise. Thus, it appears that increases in total IGF-1 concentration are more sensitive to the characteristics of endurance exercise.

The total IGF-1 represents all its forms in plasma, that is, in its free form or binding to carrier proteins (IGFBP1 to IGFB6.) However, free IGF-1 represents a small percentage of blood IGF-1, while IGFBP3 (for example) represents 80% of IGF-1 in the blood. This low concentration of free IGF-1 is the result of its rapid interaction with the carrier proteins after their release into the bloodstream. In addition, their half-life in free form is around 10 to 20 minutes,24 suggesting that their changes can be masked in long-term exercise. Thus, it is expected that free IGF-1 form has already been distributed among its blood carrier in exercise with duration above this time, which leads to its not changing by the end of the exercise. Accordingly, no change in free IGF-1 was found.10 The authors evaluated the effects of squatting exercises (6 sets × 10 repetitions − 75% 1-repetition maximum [RM]) in 16 untrained men. The results showed a reduction in free IGF-1 and increases in total IGF-1. The authors explained that the free IGF-1 reduction may be due to its greater capture by the carrier proteins (IGFBs), which had high concentrations at the end of the exercise and increased exercise-induced musculature withdrawal. Goekint et al26 found no changes in free IGF-1 concentrations after 6 resistance exercises (3 sets × 10RM − 80% 1RM) in 15 young adults. The authors suggest that the nonchange in IGF-1 concentration is the result of a possible delay in its production. The GH synthesis and secretion is first necessary so that it reaches the liver and then IGF-1 synthesis and release occur.

Therefore, it is possible to speculate greater difficulty in detecting changes in free IGF-1 compared with total IGF-1 concentration by immunoreactive assays. However, a smaller amount and short time of the free IGF-1 serum does not totally prevent detecting its alterations from physical exercise. De Palo et al23 found increases in free and total IGF-1 after 20 and 40 minutes of progressive-intensity exercise in 20 professional cyclists. As expected, the authors suggest that these increases were the result of increased hepatic and muscular production/release of this polypeptide.

The highest total IGF-1 level found in this study is in accordance with literature studies. For example, in a study involving 15 untrained men, Sheikholeslami-Vatani et al33 found increases in total IGF-1 after 9 resistance exercises performed with 3 set × 10RM. Nguyen et al22 found an increase of total IGF-1 after an incremental ergometer cycling exercise until exhaustion (∼21 min). Wallace et al12 found an increase of total IGF-1 after 30 minutes ergometer cycling exercise (80% VO2max) in trained subjects. The literature points out that changes in IGF-1 concentration in the blood after exercise are the result of the greater release of GH and the increase of its production by the muscle.7,35 In addition, Wallace et al12 suggest that changes in IGF-1 are due to tissue repair processes which increase after exercise. Thus, it is concluded that IGF-1 concentration is sensitive to different exercise protocols, as different exercise intensity and duration can change the serum IGF-1 concentration.

However, the question of why the endurance exercise presented a major ES on IGF-1 serum concentration remains open. So far, it is not possible to do a direct comparison between endurance exercise and resistance protocols, since there is difficulty in equalizing the intensity and duration in these 2 types of exercise. In this meta-analysis review, exercises such as running, cycling, or other activities with long continuous effort performed with large muscular groups were considered as endurance exercise. On the other hand, the resistance exercise was compared with studies presenting protocols with short-duration interval effort performed on specific devices (eg, workout machines and dumbbells) to generate external resistance of movement for specific muscle groups. One of the most obvious differences between endurance and resistance exercises is the time and intensity of muscle contraction. Most of the endurance exercise protocols used in this meta-analysis were performed continuously, characterizing a longer time of muscle contraction. On the other hand, the resistance exercises presented a rest interval between the stimuli, which certainly represents a shorter time by which the muscle remains in contraction. Thus, the greatest effect of endurance exercise on IGF-1 concentration may be related to the longer duration of muscle contraction in this type of exercise. However, the total IGF-1 serum concentration would be more sensitive to time for which the muscle remains in contraction rather than the intensity or the total volume of exercise session. Nevertheless, an exacerbated exercise duration (>3 h) may reduce the blood concentration of IGF-1, since prolonged exercise time allows greater distribution of IGF-1 among its carriers.22

The regulation of IGF-1 blood concentration is dynamic and complex. It depends on a complex system between its production and action mechanisms, in which these 2 are modulated by factors other than exercise such as age, body composition, physical fitness level, diet, other hormones, and plasma volume. This number of intervening factors may explain the large variations between individuals and why there was no effect of exercise on the IGF-1 presented in some studies.

Regarding the IGF-1 regulation, although its production by the hepatic cells is controlled by GH, it seems that IGF-1 concentration in the blood is not. Previous studies have shown that IGF-1 changes are not accompanied by alterations in serum GH.11,22 Therefore, even if both endurance or resistance exercises increase GH values, it probably would not lead to a greater IGF-1 serum.

Some studies did not show effects on the elevated IGF-1 after exercise. In addition, some results point to its reduction in blood.8 Hasani-Ranjbar et al27 did not find alterations in total IGF-1 after exercise (4 exercises, 3 series × 10RM: 70%–80% 1RM) in trained or untrained subjects. The authors suggest that no change in IGF-1 concentration is a result of an increase in the IGF-1 removal rate due to increased glomerular filtration permeability, and proximal tubular protein reabsorption saturation could have contributed to nonelevation of total serum IGF-1 after exercise in this study. Taylor et al28 found no change in free IGF-1 at 20 minutes after 2 protocols with different intensities in a unilateral lower limb exercise in 12 untrained men. The authors explain that IGF-1 is not temporally related to GH release in response to exercise and that increased IGF-1 muscle consumption reduces its concentration in the blood, thus maintaining its serum concentration throughout and at the end of the exercise.

Plasma volume may also interfere in interpreting the exercise effects on IGF-1 blood concentration. Dall et al8 found divergent results regarding the IGF-1 values after 30 minutes of progressive exercise (55%, 65%, 75%, and 85% of VO2max) in athletes. These concentrations were corrected by a decrease in blood volume. Total IGF-1 increased during exercise when its values were not corrected for blood volume. When the results were corrected for blood volume, there was no change in total IGF-1 concentration. Free IGF-1 decreases after exercise both with and without blood volume correction. Thus, it appears that IGF-1 changes may be due to reduced blood volume caused by exercise. However, in a study by Eliakim et al,14 the reduction in plasma volume after 10 minutes of unilateral wrist flexion was 2% to 4%, while IGF-1 increases were 7% to 8%. Thus, it seems reasonable to speculate that increased IGF-1 concentration is also attributed to its muscular or hepatic release.

Regarding the effects of exercise on IGF-1 metabolism, no increase in this polypeptide indicates that exercise does not necessarily affect the total concentration, but the exercise-induced IGF-1 is distributed among its carriers. IGF-1 has the IGF-binding protein IGBP1 to IGFBP6 proteins just like its carriers in plasma. However, IGFBP3 (IGF-1 binding protein type 3) represents 80% of the total, being the main blood transporter of IGF-1 in the blood.24

Increases in arterial concentration of IGFBP1 were found after 21 minutes of progressive effort to exhaustion, and IGFBP3 values were increased after 21 minutes22 and 30 minutes5 of progressive exercise to exhaustion without alteration of total IGF-1. In addition, increases in IGFBP3 were found after a strength-training session with 2-hours duration, but free and total IGF-1 was not altered. Decreased free IGF-1 and high IGFBP-2 and IGFBP-3 concentrations were found after 6 sets of 10 repetitions (75% 1RM) of squatting in 16 untrained males.10 Perhaps the reduction of free IGF-1 may be due to its greater capture by the carrier proteins (IGFBs).

Metabolism regulation such as maintaining blood glucose22 is necessary for IGF-1 carriers. IGFBP-1 has a hyperglycemic function while free IGF-1 has hypoglycemic insulin-like functions. IGF-1 binds to insulin receptors, favoring glucose uptake. Thus, it makes sense that your concentration does not change during or immediately after exercise in order to prevent hypoglycemia.25 However, during prolonged exercise when insulin concentrations decline, IGF-1 insulin-like action has been suggested to increase gradually to meet the demand for glucose in working muscle as muscle glycogen stores deplete. The result of the IGF-1 action would then be to induce the organism into hypoglycemic state during exercise.36 To equilibrium these effects, there is an increase in IGFBP-1 concentration to preserve adequate glycemic levels.36

Regarding physical fitness, Eliakim et al37 found a positive correlation between physical fitness level (VO2max) and total IGF-1 in female adolescents. However, the levels of this polypeptide decreased after 5 weeks of endurance training. The authors suggest that the reduction of muscle mass and a possible catabolic state induced by training are responsible for the IGF-1 blood loss. Regarding the training effects, increases in free IGF-1 were found after 8 weeks of resistance exercises performed 5 days by week in adults.1 Gregory et al38 also found increases in total IGF-1 after 8 weeks of resistance training in women. In contrast, the endurance training group did not present blood alteration for this polypeptide.

In total, 2 studies support that diet (especially protein calories) affects the IGF-1 circulatory system. Smith et al39 found a decrease in IGF-1 serum in adults after 6 days of protein calorie restriction. Rarick et al40 evaluated the impact of 11 days of physical exercise with isocaloric, hypocaloric, and hypercaloric diets with increased protein consumption. IGF-1 decreased after all interventions. Thus, it appears that physical exercise may overlap the effects of energy balance and macronutrient consumption on IGF-1 concentration.

Regarding body composition, Rubin et al30 showed that both lean and obese men increased IGF-1 values in response to exercise. However, the obese group showed lower elevation after exercise compared with the lean group. According to Rubin et al,30 these differences may be due to a decrease in available GH in these subjects or greater liver resistance to GH action. Regarding muscle mass, Eliakim et al37 found a positive correlation between muscle volume and blood IGF-1 in 23 female adolescents.

Age also interferes in IGF-1 response to exercise. Le Roith41 showed that IGF-1blood concentration increases until 12–15 years of age, and then reduces after that period. Lukanova et al42 showed an inverse correlation between age and IGF-1 in premenopausal and postmenopausal women, thus reinforcing the previous findings. Tissue responsiveness to IGF-1 is altered with age, therefore being associated with a decreased number and phosphorylation of IGF-1 muscle receptors.43

The increase in GH release by the pituitary gland and its hepatic action and muscle production are the causes most frequently mentioned as being responsible for the increase in serum IGF-1 during and after exercise. Some explanations related to exercise duration, plasma volume change, insulin effects, and distribution of free IGF-1 among their blood carriers are indicated as modulators and do not change the concentration of this polypeptide in the bloodstream.

Finally, the meta-analysis results point to a difference in exercise load capable of affecting IGF-1 concentration. Total IGF-1 is more affected by exercise compared with its free concentration. Considering the ES found, total IGF-1 concentrations appear to be more affected by endurance compared with resistance exercise. However, these results should be interpreted with caution, since the evaluated studies presented moderate to high values of heterogeneity, indicating that the studies presented medium and high inconsistency (endurance total IGF-1 I2 = 87.3, endurance free IGF-1 I2 = 51.6, resistance total IGF-1 I2 = 40.5, resistance free IGF-1 I2 = 95.7).

The standard errors of the mean differences had to be estimated in some studies, leading to less precision in the statistical analyses. Also, the low number of studies with free IGF-1 analysis limited understanding of the exercise effect on this IGF-1 form. In addition, the studies used in the present meta-analysis showed large differences in exercise load. The vast differences in intensity and duration of exercise can have very different effects on the GH–IGF axis and muscle IGF-1 release. Thus, the variability of the responses between the studies could hinder interpreting the effects of exercise on IGF-1 concentrations.

Conclusions

This study showed that IGF-1 serum concentrations are altered by endurance and resistance exercise, but in conditions which are not well-defined. Endurance exercise had a major effect on systemic IGF-1 concentrations compared with resistance exercise. Although IGF-1 is one of the main mechanisms involved in increasing muscle mass, this does not mean that endurance training is more adequate for muscle mass gain than resistance training.

According to the findings presented by the systematic review and meta-analysis, the selected studies suggest that there is no exercise load configuration determinant for serum IGF-1 changes. Exercise from low to high intensity, from short to long duration, or involved with small or large muscle masses, are able to affect IGF-1 serum concentrations.

However, the biological effect of the endurance exercise was superior to resistance exercise. Thus, if physical exercise is considered as an alternative way to regulate blood levels of IGF-1 and that increasing the concentration of this polypeptide is the goal, the individual should spend more time in their training program performing endurance exercises.

Finally, endurance and resistance exercise coaches should acknowledge that systemic and muscle IGF-1 actions are affected by training type. They must be attentive to the mechanisms involved in this muscle morphological adaptation to clarify their training goals. It is important to keep in mind that IGF-1 actions are extremely important within a complex system of exercise adaptation.

Acknowledgments

The authors express their gratitude to the Centro de Estudos em Psicobiologia e Exercício (CEPE) of the Universidade Federal de Minas Gerais, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), CAPES, Fundação Mapfre, and Fundação de Amparo a Pesquisa de Minas Gerais (FAPEMIG).

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    Brabant G, Wallaschofski H. Normal levels of serum IGF-I: determinants and validity of current reference ranges. Pituitary. 2007;10:129133. PubMed ID: 17487588 doi:10.1007/s11102-007-0035-9

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Schneider HJ, Saller B, Klotsche J, et al. Opposite associations of age-dependent insulin-like growth factor-I standard deviation scores with nutritional state in normal weight and obese subjects. Eur J Endocrinol. 2006;154:699706. PubMed ID: 16645017 doi:10.1530/eje.1.02131

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Brahm H, Piehl-Aulin K, Saltin B, Ljunghall S. Net fluxes over working thigh of hormones, growth factors and biomarkers of bone metabolism during short lasting dynamic exercise. Calcif Tissue Int. 1997;60:175180. PubMed ID: 9056167 doi:10.1007/s002239900210

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Kraemer WJ, Ratamess NA. Hormonal responses and adaptations to resistance exercise and training. Sports Med. 2003;35(4):339361. doi:10.2165/00007256-200535040-00004

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Velloso CP. Regulation of muscle mass by growth hormone and IGF-I. Br J Pharmacol. 2008;154:557568. PubMed ID: 18500379 doi:10.1038/bjp.2008.153

  • 8.

    Dall R, Lange KH, Kjaer M, et al. No evidence of insulin-like growth factor-binding protein 3 proteolysis during a maximal exercise test in elite athletes. J Clin Endocrinol Metab. 2001;86:669674. PubMed ID: 11158029

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Forbes SC, Harber V, Bell GJ. Oral L-arginine before resistance exercise blunts growth hormone in strength trained males. Int J Sport Nutr Exerc Metab. 2014;24:236244. PubMed ID: 24225560 doi:10.1123/ijsnem.2013-0106

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Nindl BC, Alemany JA, Rarick KR, et al. Differential basal and exercise-induced IGF-I system responses to resistance vs calisthenic-based military readiness training programs. Growth Horm IGF Res. 2017;32:3340. PubMed ID: 27979730 doi:10.1016/j.ghir.2016.12.001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Rakover N, Nemet D, Meckel Y, Pantanowitz M, Zaken BZ, Eliakim A. The effect of vigorous aerobic and standard anaerobic exercise testing on GH-IGF-1 secretion in adult females. Trends Sport Sci. 2013;3(20):141146.

    • Search Google Scholar
    • Export Citation
  • 12.

    Wallace JD, Cuneo RC, Baxter R, et al. Responses of the Growth Hormone (GH) and insulin-like growth factor axis to exercise, GH administration, GH withdrawal in trained adult males: a potential test for GH abuse in sport. J Clin Endocrinol Metab. 1999;84:35913601. PubMed ID: 10523001

    • Search Google Scholar
    • Export Citation
  • 13.

    Wideman L, Weltman JY, Shah N, Story S, Veldhuis JD, Weltman A. Effects of gender on exercise-induced growth hormone release. J Appl Physiol. 1999;87:11541162. PubMed ID: 10484590 doi:10.1152/jappl.1999.87.3.1154

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Eliakim A, Oh Y, Cooper DM. Effect of single wrist exercise on fibroblast growth factor-2, insulin-like growth factor, growth hormone. Am J Physiol Regul Integr Comp Physiol. 2000;279:548553. doi:10.1152/ajpregu.2000.279.2.R548

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Saw AE, Main LC, Gastin PB. Monitoring the athlete training response: subjective self-reported measures trump commonly used objective measures: a systematic review. Br J Sports Med. 2016;50:281291. PubMed ID: 26423706 doi:10.1136/bjsports-2015-094758

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Sokal RR, Braumann CA. Significance tests for coefficients of variation and variability profiles. Syst Zool. 1980;29:5066. doi:10.2307/2412626

  • 17.

    Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557560. PubMed ID: 12958120 doi:10.1136/bmj.327.7414.557

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177188. PubMed ID: 3802833 doi:10.1016/0197-2456(86)90046-2

  • 19.

    Gross A, Schirm S, Scholz M. Ycasd—a tool for capturing and scaling data from graphical representations. BMC Bioinformatics. 2014;15:219. PubMed ID: 24965054 doi:10.1186/1471-2105-15-219

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, the size of a sample. BMC Med Res Methodol. 2005;5(13):110.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Lande R. On comparing coefficients of variation. Syst Biol. 1977;26:214217. doi:10.1093/sysbio/26.2.214

  • 22.

    Nguyen UN, Mougin F, Simon-Rigaud ML, Rouillon JD, Marguet P, Regnard J. Influence of exercise duration on serum insulin-like growth factor and its binding proteins in athletes. Eur J Appl Physiol. 1998;78:533537. doi:10.1007/s004210050456

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    De Palo EF, Antonelli G, Gatti R, Chiappin S, Spinella P, Cappellin E. Effects of two different types of exercise on GH/IGF axis in athletes. Is the free/total IGF-I ratio a new investigative approach? Clin Chim Acta. 2008;387:7174. PubMed ID: 17916342 doi:10.1016/j.cca.2007.09.005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Consitt LA, Copeland JL, Tremblay MS. Endogenous anabolic hormone responses to endurance versus resistance exercise and training in women. Sports Med. 2002;32:122. PubMed ID: 11772159 doi:10.2165/00007256-200232010-00001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Nindl BC, Kraemer WJ, Marx JO, et al. Overnight responses of the circulating IGF-I system after acute, heavy-resistance exercise. J Appl Physiol. 2001;90:13191326. PubMed ID: 11247930 doi:10.1152/jappl.2001.90.4.1319

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Goekint M, De Pauw K, Roelands B, et al. Strength training does not influence serum brain-derived neurotrophic factor. Eur J Appl Physiol. 2010;110:285293. PubMed ID: 20467874 doi:10.1007/s00421-010-1461-3

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Hasani-Ranjbar S, Soleymani Far E, Heshmat R, Rajabi H, Kosari H. Time course responses of serum GH, insulin, IGF-1, IGFBP1, IGFBP3 concentrations after heavy resistance exercise in trained and untrained men. Endocrine. 2012;41:144151. PubMed ID: 21983797 doi:10.1007/s12020-011-9537-3

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Taylor LW, Wilborn CD, Kreider RB, Willoughby DS. Effects of resistance exercise intensity on extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase activation in men. J Strength Cond Res. 2012;26:599607. PubMed ID: 22343976 doi:10.1519/JSC.0b013e318242f92d

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Rubin DA, Castner DM, Pham H, Ng J, Adams E, Judelson DA. Hormonal and metabolic responses to a resistance exercise protocol in lean children, obese children and lean adults. Pediatr Exerc Sci. 2014;26:444454. PubMed ID: 25372379 doi:10.1123/pes.2014-0073

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Rubin DA, Pham HN, Adams ES, et al. Endocrine response to acute resistance exercise in obese versus lean physically active men. Eur J Appl Physiol. 2015;115:13591366. PubMed ID: 25633069 doi:10.1007/s00421-015-3105-0

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Gonzalez-Badillo JJ, Rodriguez-Rosell D, Sanchez-Medina L, et al. Short-term recovery following resistance exercise leading or not to failure. Int J Sports Med. 2016;37:295304. PubMed ID: 26667923

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Fink JE, Schoenfeld BJ, Kikuchi N, Nakazato K. Acute and long-term responses to 359 different rest intervals in low-load resistance training. Int J Sports Med. 2017;38:118360. PubMed ID: 27984843

    • Search Google Scholar
    • Export Citation
  • 33.

    Sheikholeslami-Vatani D, Ahmadi S, Salavati R. Comparison of the effects of resistance exercise orders on number of repetitions, serum IGF-1, testosterone and cortisol levels in normal-weight and obese men. Asian J Sports Med. 2016;7(1):16. doi:10.5812/asjsm.30503

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Pareja-Blanco F, Rodriguez-Rosell D, Sanchez-Medina L, et al. Acute and delayed response to resistance exercise leading or not 406 leading to muscle failure. Clin Physiol Funct Imaging. 2017;37:630639. PubMed ID: 26970332 doi:10.1111/cpf.12348

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Berg U, Gustafsson T, Sundberg CJ, Kaijser L, Carlsson-Skwirut C, Bang P. Interstitial IGF-I in exercising skeletal muscle in women. Eur J Endocrinol. 2007;157:427435. PubMed ID: 17893256 doi:10.1530/EJE-07-0141

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    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Frystyk J. Free insulin-like growth factors—measurements and relationships to growth hormone secretion and glucose homeostasis. Growth Horm IGF Res. 2004;14:337375. PubMed ID: 15336229 doi:10.1016/j.ghir.2004.06.001

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    • Search Google Scholar
    • Export Citation
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    Eliakim A, Brasel JA, Mohan S, Barstow TJ, Berman N, Cooper DM. Physical fitness, endurance training, the growth hormone-insulin-like growth factor I system in adolescent females. J Clin Endocrinol Metab. 1996;81:39863992. PubMed ID: 8923848

    • PubMed
    • Search Google Scholar
    • Export Citation
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    Gregory SM, Spiering BA, Alemany JA, et al. Exercise-induced insulin-like growth factor I system concentrations after training in women. Med Sci Sports Exerc. 2013;45:420428. PubMed ID: 23034644 doi:10.1249/MSS.0b013e3182750bd4

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    Smith WJ, Underwood LE, Clemmons DR. Effects of caloric or protein restriction on insulin-like growth factor-I (IGF-I) and IGF-binding proteins in children and adults. J Clin Endocrinol Metab. 1995;80:443449. PubMed ID: 7531712

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If the inline PDF is not rendering correctly, you can download the PDF file here.

de Alcantara Borba is with the Department of Human Movement Sciences, Faculty of Physical Education, University of Minas Gerais State, Ibirité, Minas Gerais, Brazil. da Silva Alves is with the Health Science Department, State University of Santa Cruz, Santa Cruz, Bahia, Brazil. Rosa, Facundo, A.C. Silva, Narciso, A. Silva, and de Mello are with the Department of Sports, Physical Education School, Physiotherapy and Occupational Therapy, Federal University of Minas Gerais, Belo Horizonte, Minas Gerais, Brazil. Costa is with the Southeast Federal Institute of Minas Gerais, Campus Rio Pomba, Minas Gerais, Brazil.

de Alcantara Borba (diegoalcantara1@gmail.com) is corresponding author.
  • View in gallery

    —Study selection for systematic reviews and meta-analyses flow diagram.

  • View in gallery

    —The total IGF-1 meta-analysis for endurance exercise. ES indicates effect size; LCL, lower confidence limit; n, study population; UCL, upper confidence limit; WGHT, weight of study.

  • View in gallery

    —The free IGF-1 meta-analysis for endurance exercise. ES indicates effect size; LCL, lower confidence limit; n, study population; UCL, upper confidence limit; WGHT, weight of study.

  • View in gallery

    —The total IGF-1 meta-analysis for resistance exercise. ES indicates effect size; LCL, lower confidence limit; n, study population; UCL, upper confidence limit; WGHT, weight of study.

  • View in gallery

    —The free IGF-1 meta-analysis for resistance exercise. ES indicates effect size; LCL, lower confidence limit; n, study population; UCL, upper confidence limit; WGHT, weight of study.

  • 1.

    Kraemer WJ, Ratamess NA, Nindl BC. Recovery responses of testosterone, growth hormone, IGF-1 after resistance exercise. J Appl Physiol. 2017;122:549558. PubMed ID: 27856715 doi:10.1152/japplphysiol.00599.2016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Frystyk J. Exercise and the growth hormone-insulin-like growth factor axis. Med Sci Sports Exerc. 2010;42:5866. PubMed ID: 20010129 doi:10.1249/MSS.0b013e3181b07d2d

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Brabant G, Wallaschofski H. Normal levels of serum IGF-I: determinants and validity of current reference ranges. Pituitary. 2007;10:129133. PubMed ID: 17487588 doi:10.1007/s11102-007-0035-9

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Schneider HJ, Saller B, Klotsche J, et al. Opposite associations of age-dependent insulin-like growth factor-I standard deviation scores with nutritional state in normal weight and obese subjects. Eur J Endocrinol. 2006;154:699706. PubMed ID: 16645017 doi:10.1530/eje.1.02131

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Brahm H, Piehl-Aulin K, Saltin B, Ljunghall S. Net fluxes over working thigh of hormones, growth factors and biomarkers of bone metabolism during short lasting dynamic exercise. Calcif Tissue Int. 1997;60:175180. PubMed ID: 9056167 doi:10.1007/s002239900210

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Kraemer WJ, Ratamess NA. Hormonal responses and adaptations to resistance exercise and training. Sports Med. 2003;35(4):339361. doi:10.2165/00007256-200535040-00004

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Velloso CP. Regulation of muscle mass by growth hormone and IGF-I. Br J Pharmacol. 2008;154:557568. PubMed ID: 18500379 doi:10.1038/bjp.2008.153

  • 8.

    Dall R, Lange KH, Kjaer M, et al. No evidence of insulin-like growth factor-binding protein 3 proteolysis during a maximal exercise test in elite athletes. J Clin Endocrinol Metab. 2001;86:669674. PubMed ID: 11158029

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Forbes SC, Harber V, Bell GJ. Oral L-arginine before resistance exercise blunts growth hormone in strength trained males. Int J Sport Nutr Exerc Metab. 2014;24:236244. PubMed ID: 24225560 doi:10.1123/ijsnem.2013-0106

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Nindl BC, Alemany JA, Rarick KR, et al. Differential basal and exercise-induced IGF-I system responses to resistance vs calisthenic-based military readiness training programs. Growth Horm IGF Res. 2017;32:3340. PubMed ID: 27979730 doi:10.1016/j.ghir.2016.12.001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Rakover N, Nemet D, Meckel Y, Pantanowitz M, Zaken BZ, Eliakim A. The effect of vigorous aerobic and standard anaerobic exercise testing on GH-IGF-1 secretion in adult females. Trends Sport Sci. 2013;3(20):141146.

    • Search Google Scholar
    • Export Citation
  • 12.

    Wallace JD, Cuneo RC, Baxter R, et al. Responses of the Growth Hormone (GH) and insulin-like growth factor axis to exercise, GH administration, GH withdrawal in trained adult males: a potential test for GH abuse in sport. J Clin Endocrinol Metab. 1999;84:35913601. PubMed ID: 10523001

    • Search Google Scholar
    • Export Citation
  • 13.

    Wideman L, Weltman JY, Shah N, Story S, Veldhuis JD, Weltman A. Effects of gender on exercise-induced growth hormone release. J Appl Physiol. 1999;87:11541162. PubMed ID: 10484590 doi:10.1152/jappl.1999.87.3.1154

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Eliakim A, Oh Y, Cooper DM. Effect of single wrist exercise on fibroblast growth factor-2, insulin-like growth factor, growth hormone. Am J Physiol Regul Integr Comp Physiol. 2000;279:548553. doi:10.1152/ajpregu.2000.279.2.R548

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Saw AE, Main LC, Gastin PB. Monitoring the athlete training response: subjective self-reported measures trump commonly used objective measures: a systematic review. Br J Sports Med. 2016;50:281291. PubMed ID: 26423706 doi:10.1136/bjsports-2015-094758

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Sokal RR, Braumann CA. Significance tests for coefficients of variation and variability profiles. Syst Zool. 1980;29:5066. doi:10.2307/2412626

  • 17.

    Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327:557560. PubMed ID: 12958120 doi:10.1136/bmj.327.7414.557

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7:177188. PubMed ID: 3802833 doi:10.1016/0197-2456(86)90046-2

  • 19.

    Gross A, Schirm S, Scholz M. Ycasd—a tool for capturing and scaling data from graphical representations. BMC Bioinformatics. 2014;15:219. PubMed ID: 24965054 doi:10.1186/1471-2105-15-219

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, the size of a sample. BMC Med Res Methodol. 2005;5(13):110.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Lande R. On comparing coefficients of variation. Syst Biol. 1977;26:214217. doi:10.1093/sysbio/26.2.214

  • 22.

    Nguyen UN, Mougin F, Simon-Rigaud ML, Rouillon JD, Marguet P, Regnard J. Influence of exercise duration on serum insulin-like growth factor and its binding proteins in athletes. Eur J Appl Physiol. 1998;78:533537. doi:10.1007/s004210050456

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23.

    De Palo EF, Antonelli G, Gatti R, Chiappin S, Spinella P, Cappellin E. Effects of two different types of exercise on GH/IGF axis in athletes. Is the free/total IGF-I ratio a new investigative approach? Clin Chim Acta. 2008;387:7174. PubMed ID: 17916342 doi:10.1016/j.cca.2007.09.005

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Consitt LA, Copeland JL, Tremblay MS. Endogenous anabolic hormone responses to endurance versus resistance exercise and training in women. Sports Med. 2002;32:122. PubMed ID: 11772159 doi:10.2165/00007256-200232010-00001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Nindl BC, Kraemer WJ, Marx JO, et al. Overnight responses of the circulating IGF-I system after acute, heavy-resistance exercise. J Appl Physiol. 2001;90:13191326. PubMed ID: 11247930 doi:10.1152/jappl.2001.90.4.1319

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Goekint M, De Pauw K, Roelands B, et al. Strength training does not influence serum brain-derived neurotrophic factor. Eur J Appl Physiol. 2010;110:285293. PubMed ID: 20467874 doi:10.1007/s00421-010-1461-3

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Hasani-Ranjbar S, Soleymani Far E, Heshmat R, Rajabi H, Kosari H. Time course responses of serum GH, insulin, IGF-1, IGFBP1, IGFBP3 concentrations after heavy resistance exercise in trained and untrained men. Endocrine. 2012;41:144151. PubMed ID: 21983797 doi:10.1007/s12020-011-9537-3

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Taylor LW, Wilborn CD, Kreider RB, Willoughby DS. Effects of resistance exercise intensity on extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase activation in men. J Strength Cond Res. 2012;26:599607. PubMed ID: 22343976 doi:10.1519/JSC.0b013e318242f92d

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Rubin DA, Castner DM, Pham H, Ng J, Adams E, Judelson DA. Hormonal and metabolic responses to a resistance exercise protocol in lean children, obese children and lean adults. Pediatr Exerc Sci. 2014;26:444454. PubMed ID: 25372379 doi:10.1123/pes.2014-0073

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Rubin DA, Pham HN, Adams ES, et al. Endocrine response to acute resistance exercise in obese versus lean physically active men. Eur J Appl Physiol. 2015;115:13591366. PubMed ID: 25633069 doi:10.1007/s00421-015-3105-0

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Gonzalez-Badillo JJ, Rodriguez-Rosell D, Sanchez-Medina L, et al. Short-term recovery following resistance exercise leading or not to failure. Int J Sports Med. 2016;37:295304. PubMed ID: 26667923

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Fink JE, Schoenfeld BJ, Kikuchi N, Nakazato K. Acute and long-term responses to 359 different rest intervals in low-load resistance training. Int J Sports Med. 2017;38:118360. PubMed ID: 27984843

    • Search Google Scholar
    • Export Citation
  • 33.

    Sheikholeslami-Vatani D, Ahmadi S, Salavati R. Comparison of the effects of resistance exercise orders on number of repetitions, serum IGF-1, testosterone and cortisol levels in normal-weight and obese men. Asian J Sports Med. 2016;7(1):16. doi:10.5812/asjsm.30503

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Pareja-Blanco F, Rodriguez-Rosell D, Sanchez-Medina L, et al. Acute and delayed response to resistance exercise leading or not 406 leading to muscle failure. Clin Physiol Funct Imaging. 2017;37:630639. PubMed ID: 26970332 doi:10.1111/cpf.12348

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Berg U, Gustafsson T, Sundberg CJ, Kaijser L, Carlsson-Skwirut C, Bang P. Interstitial IGF-I in exercising skeletal muscle in women. Eur J Endocrinol. 2007;157:427435. PubMed ID: 17893256 doi:10.1530/EJE-07-0141

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Frystyk J. Free insulin-like growth factors—measurements and relationships to growth hormone secretion and glucose homeostasis. Growth Horm IGF Res. 2004;14:337375. PubMed ID: 15336229 doi:10.1016/j.ghir.2004.06.001

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 37.

    Eliakim A, Brasel JA, Mohan S, Barstow TJ, Berman N, Cooper DM. Physical fitness, endurance training, the growth hormone-insulin-like growth factor I system in adolescent females. J Clin Endocrinol Metab. 1996;81:39863992. PubMed ID: 8923848

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38.

    Gregory SM, Spiering BA, Alemany JA, et al. Exercise-induced insulin-like growth factor I system concentrations after training in women. Med Sci Sports Exerc. 2013;45:420428. PubMed ID: 23034644 doi:10.1249/MSS.0b013e3182750bd4

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Smith WJ, Underwood LE, Clemmons DR. Effects of caloric or protein restriction on insulin-like growth factor-I (IGF-I) and IGF-binding proteins in children and adults. J Clin Endocrinol Metab. 1995;80:443449. PubMed ID: 7531712

    • PubMed
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