Similar Regional Hypertrophy of the Elbow Flexor Muscles in Response to Low-Load Training With Vascular Occlusion at Short Versus Long Muscle Lengths

Abstract

Background:

The regional hypertrophy response of elbow flexor muscles was compared after unilateral elbow flexion training in extended versus flexed shoulder position under vascular occlusion, which can induce muscle hypertrophy in the absence of muscle damage-induced edema/swelling.

Hypothesis:

Hypertrophy of elbow flexor muscles would be greater in extended compared with flexed shoulder position.

Study Design:

Randomized within-subject trial.

Level of Evidence:

Level 2.

Methods:

A total of 21 resistance-trained men (age, 25 ± 5 years; height, 1.78 ± 0.07 m; weight, 79.3 ± 13.1 kg) performed unilateral elbow flexions with one shoulder extended/elbow flexor muscles lengthened/long muscle length (LONG) and the other flexed/elbow flexor muscles shortened/short muscle length (SHORT) under a low-load (30% 1-repetition maximum) vascular occlusion training regimen (15 repetitions per set, 4 sets per session, 4 sessions per week for 3 weeks, using 80% of vascular occlusion pressure). Magnetic resonance imaging measured elbow flexor muscles cross-sectional area (EFCSA) pre- and post-training at 45%, 65%, and 85% of humerus length.

Results:

EFCSA significantly increased in both SHORT (P = 0.04) and LONG (P = 0.05) at 45% and 85% lengths (P < 0.01 for both). Changes in EFCSA between SHORT and LONG were statistically similar at the 45% (+6.20% vs +5.08%; Cohen d = 0.006; P = 0.98), 65% (+5.91% vs +3.83%, Cohen d = 0.28, P = 0.30), and 85% lengths (+8.51% vs +7.38%, Cohen d = 0.18,P = 0.56).

Conclusion:

Muscle hypertrophy of the elbow flexor muscles displayed a similar behavior after low-load elbow flexion training with vascular occlusion performed in the extended versus flexed shoulder position.

Clinical Relevance:

Therapists, clinicians, and coaches may choose elbow flexion exercises expecting to achieve similar results for hypertrophy in this muscle group, such that exercise selection may rely on availability of equipment in the training room or personal preference.

Muscle hypertrophy is a hallmark adaptation of resistance training (RT) targeted for sports and clinical purposes. ⁵ Despite the established international guidelines to support RT-induced muscle hypertrophy through the manipulation of variables such as intensity, volume, and interset resting interval,^7,18 the body of evidence investigating the influence of muscle length/joint angle on muscle hypertrophy during dynamic exercises is incipient and its findings are controversial.^{2,16,17,20,29} Nevertheless, most studies indicate that muscle hypertrophy is optimized when RT is conducted at long versus short muscle lengths. ²¹ This might be attributed to the greater overall mechanical tension that occurs when a muscle is tensioned as it is lengthened, presumably due to active and passive tension overlapping,^22,30 although others speculate that muscle hypertrophy is likely attributable to greater metabolic stress and insulin-like growth factor-1 expression associated with exercise at long muscle lengths.^11,30

The vast majority of studies comparing muscle hypertrophy response with RT at long versus short muscle lengths adopted a lower-body exercise protocol, or a partial versus full range of motion training at different joint angles about the same joint (eg, knee extensors trained at knee 0°-60° vs 0°-100°).^22,23 However, RT guidelines generally recommend dynamic exercises for both lower- and upper-body as well as with a full range of motion when possible.^7,18 Moreover, measures of muscle edema were not performed in most of the aforementioned chronic studies,^{2,16,17,20,29} which is concerning due to the potential interference of this factor on muscle hypertrophy analysis. ²⁶ In addition, the lack of regional hypertrophy analysis is also a hallmark in the previous studies, which may have impaired the interpretation of hypertrophy responses across muscles differently lengthened. ³¹ Thus, it is of undisputable practical relevance to understand whether upper-body exercises trained at full range of motion and placing the same muscle(s) under long versus short conditions affect regional hypertrophy response while employing muscle edema measures or RT methods known to induce muscle hypertrophy in the absence of muscle damage-induced edema/swelling.

The 3 primary flexor muscles of the elbow are the biceps brachii, the brachioradialis, and the brachialis. They provide important functions for daily living activities and sports, such as eating food, pulling, lifting, ²⁵ climbing, ⁶ and wheelchair movement. ¹ Of its 3 constituent muscles, the biarticular biceps brachii crosses not only the elbow but also the shoulder joint and is lengthened more in the backward (shoulder-extended) than in the forward (shoulder-flexed) arm position. ¹³ Both backward and forward arm positions during elbow flexions are commonly implemented in the literature and RT routines (often called “incline dumbbell curl” and “preacher curl,” respectively), but their difference has never been discussed, particularly for their hypertrophic effects.

Therefore, we investigated the effects of low-load RT with vascular occlusion performed in the backward versus forward arm position on muscle hypertrophy of the elbow flexor muscles. The vascular occlusion protocol was employed in the present study due to its recognized capacity to significantly enhance muscle hypertrophy over a short period of time (ie, 3 weeks) without associated muscle damage-induced muscle edema/swelling. ²⁶ Using a straightforward methodology, we hypothesized based on recent reviews that hypertrophy of the elbow flexor muscles would be greater in the backward compared with forward arm position.^22,23

Methods

Participants

A sample size of 21 (ie, n = 21 arms per condition) was deemed well sufficient based on recent studies of similar nature.^16,17 Therefore, 21 subjects were recruited between June and July 2023 from our university to participate in the study. According to the physical activity readiness questionnaire during the preliminary screening, participants were all healthy men (age, 25 ± 5 years; height, 1.78 ± 0.07 m; bodyweight, 79.3 ± 13.1 kg; body mass index, 25.0 ± 3.1 kg m²) and recreationally engaged in strength training programs for at least 1 year by the time the study was conducted (training experience, 2 ± 1 years; training frequency, 3 ± 1 days per week).

Participants self-reported neither cardiovascular and neuromuscular disorders nor health problems that could affect the outcomes of the present study. Exclusion criteria considered the self-reported use of medicines, any kind of dietary supplements or ergogenic aids within the last 2 months before the study, or a history of anabolic steroids usage. Participants were oriented to maintain their physical training program and food habits until the study completion, and these recommendations were checked verbally regarding their accomplishment. They were informed about the risks and benefits of the study before providing a written consent letter. This study was approved by the Institutional Ethics Committee (approval No. 28798720.0.0000.5512) and was conducted according to the 2013 version of the Declaration of Helsinki.

Experimental Design

The experimental design is illustrated in Figure 1. Approximately 72 hours before beginning the training program, participants were evaluated for upper-body arterial occlusion pressure (determined with a portable vascular Doppler probe) in both arms. Thereafter, all participants performed a familiarization session for the unilateral elbow flexion 1-repetition maximum (1-RM) test, where one arm was tested in a backward position (ie, incline dumbbell curl exercise) and the other in a forward position (ie, preacher dumbbell curl exercise). At 72 hours after this session, participants repeated the 1-RM test and were considered familiarized with the test procedures when the interday strength value variation was ≤5%, having the highest value determined as 1-RM (0 hours). The 1-RM values for all participants were obtained within ≤3 visits. The 1-RM loads were used to individualize training loads. Participants were instructed to abstain from alcohol and unaccustomed exercise for the elbow flexor muscles in the 48 hours before the testing sessions, as well as caffeine in the 24 hours preceding the tests. Participants arrived at the laboratory at least 2 hours after their last meal, and water consumption was allowed ad libitum during the training and testing sessions.

Figure 1.

Experimental design. 1-RM, 1-repetition maximum; EFCSA, elbow flexor muscles cross-sectional area; LL-BFR, low-load blood flow restriction; W0, week zero; W3, week 3.

At least 72 hours after the last 1-RM test, the cross-sectional area of the elbow flexor muscles (EFCSA) was obtained through magnetic resonance imaging (MRI). After the MRI scan, each subject’s arm was allocated in a randomized and balanced way, according to 1-RM and EFCSA values, to 1 of 2 training groups: backward arm position—shoulder extended/elbow flexor muscles lengthened/long muscle length (LONG); and forward arm position—shoulder flexed/elbow flexor muscles shortened/short muscle length (SHORT). The arms were also counterbalanced according to dominance, such that the LONG and SHORT groups included 11 dominants and 10 nondominant arms. RT protocol for both arms consisted of a low-load exercise with vascular occlusion (LL-VO) and was performed 4 times per week (Tuesday, Wednesday, Thursday, and Friday) for 3 weeks (totaling 12 sessions). After the third week of training (W3), EFCSA was reassessed 48 hours after the last training session. The training load was kept the same throughout the training period, and food intake was assessed by three 24-hour food diaries before and after the intervention.

EFCSA Assessment

EFCSA was obtained via MRI (Signa LX 9.1; GE Healthcare). Participants were positioned on the device in a supine position with elbows extended and arms straight. A bandage was used to restrain arm movements during the test. An initial reference image was obtained to determine the perpendicular distance from the superior border of the greater tubercule of the humerus to the inferior border of the lateral epicondyle of the humerus, which was defined as the segment length. EFCSA was measured in both arms at 45%, 65%, and 85% of the segment length with 0.8-cm slices for 3 seconds (Appendix Figure A1, available in the online version of this article). The pulse sequence was performed with a field of view between 400 and 420 mm, time of repetition of 350 ms, eco time from 9 to 11 ms, 2 signal acquisitions, and a matrix of reconstruction of 256 × 256 mm. The images were then transferred to a computer (Mac OS X, Version 10.5.4; Apple) and analyzed using open-source software (OsiriX, Version 3.2.1; OsiriX Imaging Software). Elbow flexor muscles images were traced in triplicate by a specialized researcher, and their mean values were used for further analysis. The segment slice was divided into skeletal muscle, subcutaneous fat tissue, bone, and residual tissue. EFCSA was determined by subtracting the bone and subcutaneous fat area. The mean absolute and relative typical errors calculated for EFCSA between 2 measures at the baseline were 0.55 cm² and 2.23%, respectively.

Determination of Blood Flow Restriction Pressure

Arterial occlusion of both arms was taken to determine the pressure used for the LL-VO protocol. After 10 minutes of rest in a seated position, a vascular Doppler probe (DV-600; Marted, Ribeirão Preto) was placed on the brachial artery to capture its auscultatory pulse. A nylon wide cuff (12 × 22 cm; JPJ) was placed at the top of the arm and inflated to the lowest point at which an auscultatory pulse was no longer detected. This value was defined as the arterial occlusion pressure. A pressure equivalent to 80% of the resting arterial occlusion pressure was used during the training sessions, which has been shown previously to induce favorable increases in muscle size and strength.^27,28

Maximum Strength Testing Procedures

Maximum dynamic strength (1-RM) was determined at baseline as the maximum possible weight lifted in a single and complete repetition during the unilateral elbow flexion exercises (Figure 2) for both SHORT (ie, preacher dumbbell curl exercise) and LONG (ie, incline dumbbell curl exercise) groups. Elbow joint amplitude was set at 100° using a goniometer (the lateral epicondyle of the humerus was used as the point of intersection, while the radial styloid process and the acromion process were fixed as the extremities) for both arms. The second arm was tested immediately at the end of the first arm testing, and the testing order was alternated at each familiarization session. The 1-RM load in both exercises was used to individualize the training loads.

Figure 2.

Examples of how unilateral incline dumbbell curl (left squares) and preacher dumbbell curl (right squares) exercises were performed, with starting (upper line) and ending positions (bottom line) depicted.

The procedures followed the American Society of Exercise Physiologists guidelines. ³ Before testing, participants ran for 5 minutes on a treadmill at 9 km h^-1 for a general warm-up. Afterward, participants performed a specific warm-up set of 8 repetitions at approximately 50% of the estimated 1-RM followed by another set of 3 repetitions at 70% of the estimated 1-RM. Warm-up sets were separated by a 2-minute rest interval. After completion of the second specific warm-up set, participants rested for 3 minutes. Subsequent lifts were single repetitions of progressively heavier loads, until failure. Maximum dynamic strength was determined as the maximum weight that could be lifted once with proper technique. A rest interval of 3 minutes was given between sets, and a maximum of 5 attempts was allowed. All the tests were supervised by 2 experienced researchers. Increments in weight were determined according to the researchers’ perception. Strong verbal encouragement was provided during all lifts. The coefficient of variation across the familiarization sessions was 4.4% and 5.0% for the LONG and SHORT groups, respectively.

Resistance Training Protocol

Both SHORT and LONG performed a unilateral elbow flexion LL-VO on the same position employed during the 1-RM tests. Training was performed 4 days per week for 3 weeks (total of 12 sessions). The initial arm performing the session was alternated each subsequent session. At the beginning of each training session, participants performed a general warm-up at 9 km h^-1 on a treadmill for 5 minutes followed by a specific warm up composed of 1 set of 5 repetitions at 50% 1-RM. After a 1-minute rest interval, the training protocol started. A pressure cuff was positioned near the axillary region for 1 arm and inflated to the targeted training pressure. The training protocol consisted of 4 sets of 15 repetitions at 30% 1-RM with a 1-minute rest period afforded between sets. This protocol has been demonstrated previously to induce favorable increases in muscle size over short training periods without associated muscle damage-induced muscle edema/swelling.^26,28 Vascular occlusion was maintained throughout the training session (including rest periods) and was removed immediately after the end of the final set.

Food Intake Analysis

Food intake was assessed before and after training 3 times by 24-hour food diaries undertaken on separate days (2 weekdays and 1 weekend day). Energy and macronutrient intakes were analyzed with a computer software containing nutritional information about local food and ingredients (WebDiet Health Manager). All participants were instructed on how to complete food diaries by a trained nutritionist; they received a booklet containing instructions and real-sized photos of real food to help them record portion sizes.

Statistical Analysis

Data are presented as means and standard deviations, relative changes and absolute changes, and effect sizes. Gaussian distribution was previously confirmed through the Shapiro-Wilk test, thus EFCSA and food intake at baseline were compared between groups using unpaired t tests. The intervention effects on EFCSA and food intake were investigated through a mixed-model analysis of variance having “group” (SHORT and LONG) and “time” (pre- and post-training) as fixed factors and participants as a random factor. A Tukey post hoc test was used for multiple comparisons correction. Unpaired t tests were also used to compare the absolute variation (ie, post-pre delta) in EFCSA between groups. Furthermore, we calculated the effect sizes as the Cohen d (d) and classified d < 0.2 as negligible effect, d between 0.2 and 0.49 as small effect, d between 0.50 and 0.79 as moderate effect, and d ≥ 0.80 as large effect. Analyses were conducted using the SAS software Version 9.3 (SAS Institute Inc). The significance level was set a priori at P ≤ 0.05.

Results

EFCSA at 45% of Humerus Length

No between-group differences for EFCSA at 45% of humerus length were detected at baseline (P = 0.93). The mixed model analysis revealed that both SHORT and LONG groups experienced a small (+0.86 ± 1.63 cm², +6.20 ± 10.97%; and +0.78 ± 1.20 cm², +5.08 ± 8.30%, respectively) but significant (P = 0.04 and P = 0.05, respectively) muscle hypertrophy response at 45% of humerus length (Figure 3a). However, the absolute change analysis did not show any between-group difference for the increases in EFCSA at this length (Figure 4a).

Figure 3.

CSA of elbow flexor muscles at (a) 45%, (b) 65%, and (c) 85% of humerus length before and after low-load vascular occlusion training at a shortened (SHORT) or lengthened (LONG) muscle length. *Significant difference (at P < 0.05) compared with PRE. CSA, cross-sectional area.

Figure 4.

Absolute change in CSA of the elbow flexor muscles at (a) 45%, (b) 65%, and (c) 85% of humerus length in response to LL-VO training at a shortened (SHORT) or lengthened (LONG) muscle length. CSA, cross-sectional area; LL-VO, low-load vascular occlusion.

EFCSA at 65% of Humerus Length

No between-group differences for EFCSA at 65% of humerus length were detected at baseline (P = 0.96). Both SHORT and LONG groups experienced a small (+1.37 ± 1.84 cm², +5.91 ± 7.52%; and +0.83 ± 1.40 cm², +3.83 ± 5.89%, respectively) muscle hypertrophy response at 65% of humerus length (Figure 3b), with SHORT but not LONG exhibiting a significant within-group difference (P < 0.01 and P = 0.11, respectively). On the other hand, the absolute change analysis did not show any between-group difference for the increases in EFCSA at this length (Figure 4b).

EFCSA at 85% of Humerus Length

No between-group differences for EFCSA at 85% of humerus length were detected at baseline (P = 0.90). The analysis showed that both SHORT and LONG groups experienced a small (respectively, +2.19 ± 2.27 cm², +8.51 ± 7.78%; and +1.81 ± 1.73 cm², +7.38 ± 7.09%) but significant (P < 0.01 and P < 0.01) muscle hypertrophy response at 85% of humerus length (Figure 3c). The absolute change analysis did not show any between-group difference for the increases in EFCSA at this length (Figure 4c).

Food Intake

No significant differences were detected for daily energy (2707 ± 650 vs 2617 ± 542 kcal; P = 0.54), carbohydrate (338 ± 90 vs 311 ± 72 grams; P = 0.39), fat (85 ± 37 vs 83 ± 34 grams; P = 0.42) or protein intake (145 ± 20 vs 156 ± 48 grams; P = 0.21) between pre- and post-training periods.

Discussion

The primary finding of this investigation was that muscle hypertrophy of the elbow flexor muscles occurred in a similar magnitude after 3 weeks of unilateral low-load vascular occlusion training performed in the backward versus forward arm position (ie, long vs short muscle length).

There have been consecutive reports demonstrating that training in a lengthened muscle position elicits more favorable muscle hypertrophy compared with training at shorter muscle lengths.^22,23 Although such results have been confirmed in some muscles (ie, quadriceps), there is a paucity of studies examining this hypothesis in upper-body muscles operating under full range of motion in a dynamic manner, as recommended by international guidelines.^7,18 To the authors knowledge, there is 1 study that was designed to compare muscle hypertrophy response with 2 preacher curl exercises performed under full range of motion. ²⁰ Specifically, exercises were performed either on a cable-pulley system, in which a greater torque was applied during the exercise when elbows were flexed and the biceps brachii muscle was shortened; or with a barbell, in which greater torque was applied when the elbows were extended and the biceps brachii muscle was elongated. Curiously, no difference in muscle hypertrophy was detected between the exercises, ²⁰ but caution should be exercised when interpreting these results. First, both men and women were included in the same experimental groups, and there are concerns about the possible influence of menstrual cycle on RT-induced muscle hypertrophy. ¹⁰ Second, the between-subject design employed may have exacerbated the potential confounding effects of variations in biology and nutritional status on the study results. Third, muscle thickness was assessed only at the midportion of the biceps brachii muscle; considering that RT-induced hypertrophy may be inhomogeneous, ³¹ the assessment of more muscle sites could have provided greater insights regarding the hypertrophy responses.

Overcoming these issues, our study demonstrated that the LONG and SHORT groups increased EFCSA in a similar extent across the different humerus lengths, which corroborates previous studies but contradicts our initial hypothesis. ²⁰ Since equivalent neuromuscular activity of the biceps brachii may be expected from the chosen exercises in the current study, ²¹ the rationale for our hypothesis was based on the additional mechanical tension that the biarticular biceps brachii muscle may suffer from passive elements when reaching elongated muscle lengths, ¹² which was not confirmed herein. A number of methodological precautions were adopted to surpass potential sources of bias in the study conduction and interpretation. First, only trained male subjects were recruited. Second, participants were fully acquainted with strength performance tests before the intervention, minimizing the risk of learning effects and excluding the chance of an inadequate training intensity prescription. Third, the adopted within-subject design conceivably reduced diet and genetics-associated variations in results, ¹⁵ and our food consumption analysis showed that this variable is unlikely to have had any influence on the results throughout the study. Fourth, muscle hypertrophy response to the LL-VO protocol employed in this study was shown previously to occur in the absence of edema-induced muscle swelling, ²⁶ meaning that the observed EFCSA increases were due to muscle protein accretion as opposed to accumulation of fluid. Finally, muscle hypertrophy was assessed in multiple lengths and still no significant differences were detected in the EFCSA increases between LONG and SHORT groups. We are confident this straightforward methodology sorted out potential biases, thereby allowing us to conclude that elbow flexion training in a backward or forward arm position lead to the same hypertrophy response of the elbow flexor muscles.

The current findings might be explained, at least in part, by muscle mechanical properties (eg, length-tension relationship). Some evidence indicates that the elbow flexor muscles work mainly in the ascending limb and plateau region of the length-tension curve, ¹⁹ suggesting their sarcomeres reach near maximal active force generation at longer muscle lengths. Since the passive elements contribute more to force generation in the descending limb of the length-tension curve and less in the ascending and plateau portion,^4,8 it is possible that most fibers of the elbow flexor muscles do not experience additional mechanical tension induced by passive elements upon reaching longer muscle lengths. Conversely, other studies indicate that the sarcomeres of the biceps brachii and brachialis reside primarily on the descending limb, ⁴ which seemingly would refute this hypothesis and raise the possibility that heightened passive force production might in fact be involved. Further research is needed to draw stronger inferences on this issue. It is noteworthy that both exercises were performed in the present study with free weights and with the forearm supinated. It becomes important to determine in the future whether the same results would be detected if cables or machines had been used, which may affect the moment arm length, and, hence, the exercise strength curve, or with the forearm pronated, which may also lengthen the biceps brachii and brachioradialis muscles. Elucidating this topic may contribute to refining effective and safe exercise prescription.

Finally, our investigation reinforced that LL-VO training is an efficient model to promote muscle hypertrophy (3.8%-8.5%), even over very short periods (in this case, 3 weeks). ¹⁴ Such an effect is in agreement with a previous meta-analysis, which indicated a mean gain in muscle hypertrophy of 7.2% with this training procedure. ¹⁴ The exact mechanisms responsible for such changes are beyond the scope of the current study but are likely attributable to an increase in fast-twitch fiber recruitment and reduced expression of genes related to muscle protein breakdown, the activation and proliferation of myogenic stem cells and expression and activation of satellite cells, and an increased muscle protein synthetic response. ²⁴

Limitations

Our study has limitations that should be noted. First, our results are specific to young, trained men, and it is uncertain whether the observed changes would be similar for other populations, such as women, elderly, and untrained persons. Second, we cannot rule out the possibility of a cross-education effect confounding changes given the within-subject design. However, differently from neuromuscular responses, biochemical responses to exercise (eg, protein and/or mRNA abundance) such as hypertrophy show no measurable signs of transfer between limbs. ⁹

Conclusion

Similar muscle hypertrophy response to unilateral elbow flexion LL-VO training may be obtained with the arm in a backward and forward position. These results indicate that therapists, coaches, athletes, and practitioners may choose elbow flexion exercises expecting to achieve similar results for hypertrophy in this muscle group, implying that exercise selection may rely on the availability of equipment in the training room or personal preference. The combination of both exercises may also be a valid strategy to increase total training volume for the elbow flexor muscles.