Photobiomodulation in human muscle tissue: an advantage in sports performance?

A. Acute photobiomodulation (PBM) response to exercise using upper limb muscles

To our best of knowledge, the first randomized clinical trial (RCT) was conducted by Craig et al. [10] (level 1b). The authors investigated the efficacy of three different frequencies (2.5 Hz, 5 Hz, 20 Hz) of pulsed PBM using low-level laser therapy (LLLT) at 660 nm and 950 nm to mitigate DOMS induced by repeated eccentric contractions of the elbow flexor muscles with free weights until exhaustion in a randomized, placebo-controlled trial. The subjects received LLLT on the biceps brachii exercised for 3 days. However, DOMS increased for all groups treated with different LLLT pulse frequencies, as well as for the control and placebo groups. Range of motion was impaired and pain increased for all groups. The authors reported no effect of PBM in DOMS assessed by visual analogue scale (VAS) and mechanical pain threshold/tenderness (MPT).

Years later, the same research group [11] (level 1b) conducted a very similar study to investigate the effectiveness of LLLT on DOMS during a treatment period of 7 days in a randomized, placebo-controlled trial. DOMS induction, as well as LLLT device used were similar to previous study [10], consisting of elbow flexion exercises with free weights and laser diodes at (660 nm and 950 nm, 73 Hz), respectively. After complete DOMS induction, subjects were treated com placebo, or LLLT, or control (rest in supine position) on 1 point over the biceps brachii for 5 consecutive days, plus 2 days in the following week. The authors reported no effect of LLLT to mitigate DOMS assessed by VAS and MPT.

Vinck et al. [9] (level 1b) investigated the effects of LEDT (cluster of 32 LEDs, 950 nm) on DOMS after induction of fatigue in the biceps brachii muscle using an isokinetic dynamometer. The authors reported no significant difference between the LEDT group and the placebo group regarding elbow flexor peak torque exerted and pain in this randomized, single-blind, placebo-controlled trial. However, using similar methodology, Douris et al. [8] (level 1b) in a randomized, double-blind placebo-controlled trial applied LEDT (cluster of 36 LEDs, 880 nm and 660 nm) on the biceps brachii muscles after elbow flexion/extension bearing free weights, and found a significant reduction in DOMS after 48 h when comparing LEDT to the control and placebo groups.

Using a muscular pre-conditioning protocol, Leal Junior et al. [13] (level 1b) applied LLLT (655 nm) on the biceps brachii muscle before elbow flexion/extension until exhaustion on a Scott bench in a randomized, double-blind, placebo-controlled trial. The PBM was applied on 4 points located on the muscle, and then maximum voluntary contractions (MVC) were applied with a load of 75%. The number of repetitions and total time to accomplish the exercise increased significantly in all the volunteers that received muscular pre-conditioning PBM compared to the placebo group. However the results of blood lactate were not significantly different. Moreover, similar studies have been conducted by the same research group, investigating a muscular pre-conditioning regimen with LLLT (830 nm) applied on 4 points of the biceps brachii [21] (8/10, level 1b). They also compared red (660 nm) and near-infrared (830 nm) wavelengths applied on the biceps brachii muscle before MVC on a Scott bench [22] (level 1b). These authors found significant differences between the placebo group and both groups irradiated with LLLT, but without significant difference between the two different wavelengths regarding the mean and peak force developed by each group irradiated.

Applying a muscular pre-conditioning protocol on 2 sites on the biceps brachii during 30 sec, Leal Junior et al. [23] (level 1b) in a randomized, double-blind, crossover, placebo-controlled trial reported an increased number of repetitions could be achieved, and found decreased lactate levels in blood as well as lower CK and C-reactive protein. The PBM used in this study was delivered by a cluster of 5 laser diodes (810 nm). Similar results were reported by the same research group [24] (level 1b) using a cluster of 69 LEDs (850 nm and 660 nm) applied on 1 site of the biceps brachii muscle in a muscular pre-conditioning protocol using elbow flexion/extension with a load of 75% of MVC on a Scott bench. The LEDT group increased the number of repetitions and the duration of exercise compared to placebo group in this randomized, double-blind, crossover, placebo-controlled trial. LEDT also decreased blood levels of lactate, CK and C-reactive protein compared to placebo group.

Investigating the effects of PBM by LEDT (630 nm) applied after an exercise protocol to induce muscle damage by eccentric elbow flexion/extension, Borges et al. [25] (level 1b) reported a reduction in DOMS, and a slower decay in the isometric force able to be exerted by the LEDT group when compared to the placebo group in a randomized, double-blind, placebo-controlled trial. The authors also reported less restriction or a smaller decrease in the range of motion possible in the LEDT group 24 h, 48 h, 72 h and 96 h after induction of muscle damage. In a similar study Felismino et al. [26] (level 1b) applied LLLT (808 nm) on the biceps brachii muscle between 10 sets of 10 repetitions with a load corresponding to 50% of the 1-repetition maximum test (1-RM) during exercise consisting of elbow flexion/extension on a Scott bench. The results of this randomized, double-blind, placebo-controlled trial pointed to a significant reduction in muscle damage (measured by CK) only at 72 h after the exercise test compared to the placebo group. However, there was no significant difference in muscle performance (load) between groups.

Rossato et al. [27] (level 1b) compared the effects of large cluster probe (33 diodes; 30.2 cm²) versus small cluster probe (9 diodes; 7.5 cm²) on elbow flexor muscle fatigue in a randomized, crossover, double-blind, placebo-controlled trial. The authors reported an increased time to exhaustion when active PBM by LEDT with large and small cluster probes were used as muscular pre-conditioning to increase fatigue resistance assessed in an isokinetic dynamometer through maximum voluntary isometric contraction (MVIC). Both cluster probes induced an increase in time to exhaustion compared with respective placebo therapies, but there was no difference between both active cluster probes. Moreover, there were no significant differences among placebo, large and small cluster probes groups regarding maximum peak torque and electromyography analysis in the biceps brachii.

Some other studies did not report significant benefits of PBM on the biceps brachii, such as that by Higashi et al. [28] (level 1b) who used an exercise protocol on a Scott bench. These authors used a muscular pre-conditioning protocol with LLLT (808 nm) on 8 sites of irradiation on the biceps brachii. There was no significant increase in the number of repetitions and reduction in lactate levels in the blood, or reduction in fatigue assessed by surface electromyography in this randomized, triple-blind, crossover, placebo-controlled trial. Finally Larkin-Kaiser et al. [29] (level 1b) in a randomized, double-blind, crossover, placebo-controlled trial enrolling both men and women, applied a muscular pre-conditioning protocol with LLLT (800 nm and 970 nm) on the biceps brachii muscle at 15 points of irradiation. Although only a very small difference was found compared with placebo group, the LLLT group had an improvement in MVIC assessed by isokinetic dynamometer, and no significant effect on muscle point tenderness.

Figure 2 shows an example of the sites of irradiation on the muscles and exercise test for upper arms. Table 2 presents all parameters of photobiomodulation used for testing acute response in exercises with upper arm muscles.

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Figure 2

A) Example of muscular pre-conditioning irradiating multiple sites or points on the biceps brachii. B) Exercise test on a Scott bench.

B. Acute photobiomodulation (PBM) responses in exercise using lower limb muscles

One of the first studies published in this area was conducted by Gorgey et al. [12] (6/10, level 1b). The authors performed a muscular pre-conditioning protocol applying photobiomodulation (PBM) by LLLT (808 nm) for 5 minutes (scanning mode) comparing low energy (3 J) with high energy (7 J) on the quadriceps femoris muscles before induction of fatigue by neuromuscular electrical stimulation. Although apparently less fatigue in the LLLT groups compared to control, there was no significant difference among all groups.

Leal Junior et al. [30] (level 1b) in randomized, double-blind, crossover, placebo-controlled trial irradiated the rectus femoris muscle before Wingate tests with a muscular pre-conditioning protocol. These authors reported no significant effects of the LLLT (830 nm) on muscle performance, but the levels of CK and lactate in bloodstream were decreased when compared to the placebo group. Leal Junior et al. [31] (level 1b) conducted another randomized, double-blind, crossover, placebo-controlled trial using the Wingate test and compared the effects of LLLT (single diode, 810 nm) to LEDT (cluster of 69 LEDs, 850 nm and 660 nm) on the muscle performance of athletes. LLLT or LEDT was applied on 2 sites on the rectus femoris muscle in a muscular pre-conditioning protocol. LEDT decreased CK levels in blood compared to placebo and LLLT groups. However, there was no improvement in muscle performance or reduction in lactate levels in the bloodstream of the LEDT group compared to placebo and/or LLLT groups. Similar results were reported by Denis et al. [32] (level 1b) who also did not find positive results when LEDT (cluster of 69 LEDs, 950 nm and 660 nm) was applied during the rest intervals of the Wingate tests. These authors reported no significant differences in muscle peak power, fatigue index and blood lactate levels when compared to the placebo group in this randomized, single-blind, crossover, placebo-controlled trial.

In another randomized, double-blind, crossover, placebo-controlled trial using Wingate test, Leal Junior et al. [33] (level 1b) also compared the effects of photobiomodulation by LEDT (cluster of 69 LEDs, 850 nm and 660 nm) to the use of cold-water immersion (cryotherapy) in order to promote muscle recovery. Six athletes performed 3 Wingate tests on non-consecutive days and received either LEDT or cold-water immersion of the lower limbs (5°C for 5 minutes) as a therapy. LEDT was applied on 2 sites on the quadriceps femoris muscles, 2 sites on the hamstrings and 1 site on the triceps surae. Comparing both groups, LEDT significantly decreased levels of CK and lactate in the blood but was not able to increase muscle work in the Wingate test and did not reduce C-reactive protein.

In a similar study, de Paiva et al. [34] (level 1b) investigated the effects of cryotherapy on DOMS and muscle damage (CK) as a single treatment, or combined with PBM by a cluster with 1 infrared laser diode (905 nm), 4 red LEDs (640 nm) and 4 infrared LEDs (875 nm) in a randomized, double-blinded, placebo-controlled trial. The authors induced muscle damage in subjects with eccentric contractions of knee extensor muscles in an isokinetic dynamometer. Three minutes after, the subjects received either placebo, or PBM, or cryotherapy, or PBM + cryotherapy, or cryotherapy + PBM. Post-exercise assessments consisted of measuring CK in blood, visual analogue scale for pain (VAS) and maximum voluntary isometric contraction (MVIC) at 1 h, 24 h, 48 h, 72 h and 96 h. Treatments were repeated at 24 h, 48 h and 72 h. PBM improved MVIC, decreased DOMS and CK from 24 h to 9 h when compared to placebo, cryotherapy and cryotherapy + PBM. The combination of PBM + cryotherapy reduced the efficacy of PBM. Finally, cryotherapy as a single treatment, and cryotherapy + PBM were similar to placebo, showing the superiority of PBM as a single treatment.

Assessing muscle performance by an exercise protocol using eccentric exercise in an isokinetic dynamometer, Baroni et al. [35] (level 1b) used a muscular pre-conditioning protocol with LLLT (cluster of 5 laser diodes, 810 nm) applied on 6 sites of the quadriceps femoris muscles in a randomized, double-blind, placebo-controlled trial. The authors reported an improved MVIC immediately and 24 h after the exercise protocol, and increased lactate dehydrogenase (LDH) activity at 48 h after exercise, and the CK levels in blood decreased after 24 h and 48 h when compared to the placebo group. However, the DOMS was not improved by LLLT. In addition, this same research group [36] (level 1b) also investigated the effects of the same LEDT cluster (69 LEDs, 850 nm and 660 nm) applied on 3 sites of the quadriceps femoris muscles before a fatigue protocol performed in an isokinetic dynamometer for knee flexion/extension. The authors reported that LEDT was able to decrease the decay of the knee extensor peak torque exerted compared to placebo group in this randomized, double-blind, crossover, placebo-controlled trial.

With a similar protocol of exercise in isokinetic dynamometer of previous study [36],Antonialli et al. [37] (level 1b) used laser diodes (905 nm) and LEDs (640 nm and 875 nm) assembled in the same device to stimulate muscle recovery when applied as a muscular pre-conditioning protocol on the quadriceps femoris muscles before a fatigue protocol with eccentric contractions and MVIC in an isokinetic dynamometer. Muscular pre-conditioning using lasers and LEDs was performed 3 minutes before the exercise protocol in a randomized, double-blind, placebo-controlled trial. The authors reported that light energies of 10 J, 30 J and 50 J per site of irradiation increased the percentage of knee extensor peak torque of maximum voluntary isometric contraction (MVIC) immediately and the effect lasted until 96 h after the muscular pre-conditioning. DOMS was reduced significantly using light energies of 30 J and 50 J when compared with the placebo group. Finally, this study reported a significant reduction of CK with light energies (doses) of 10 J, 30 J and 50 J.

On the other hand, the same aforementioned research group conducted another randomized, double-blind, placebo-controlled trial with soccer athletes and assessed also the effects of PBM using LLLT on the knee extensor peak torque of MVIC, DOMS, CK and interleukin-6 expression [38] (level 1b). This study applied LLLT on 6 sites of irradiation on the quadriceps femoris muscles similar to Antonialli et al. [37], but interestingly found different effects for light energies (doses) of 10 J, 30 J and 50 J. Light energies (doses) of 10 J and 50 J per site of irradiation were more effective to decrease CK levels in blood and interleukin 6 (IL-6), with better results in favor of 50 J. Moreover, MVIC was improved immediately after exercise up to 24 h after exercise with 50 J, and from 24 h to 96 h with 10 J. However, 30 J per site of radiation had no effect on MVIC, CK, IL-6 and DOMS. The main difference from this study [38] and the previous study [37] was the device used for photobiomodulation. While Antonialli et al. [37] used a cluster of lasers and LEDs, this study [38] used a cluster of 5 lasers diodes (810 nm) similar to used in previous study [35] that found positive effects with 30 J per site of irradiation.

In another study looking at dose-response, Hemmings et al. [39] (level 1b) developed a randomized, double-blind, crossover, placebo-controlled trial with 34 subjects to investigate the effects of PBM with LEDT on quadriceps femoris muscle performance in an isokinetic dynamometer. LEDT was applied as muscular pre-conditioning with light energies of 41.7 J, 83.4 J, 166.8 J, or placebo. Compared to placebo therapy, the authors reported a higher number of repetitions when LEDT was applied 83.4 J and 166.8 J per site of irradiation. However, there was no effect on blood lactate levels or torque exerted by knee extensor muscles in MVIC.

Toma et al. [40] (level 1b) in a randomized, triple-blind, crossover, placebo-controlled trial used a muscular pre-conditioning protocol with LLLT (808 nm) on the quadriceps femoris muscles and assessed muscle fatigue by surface electromyography during 60 seconds of leg extension exercise, also measuring the maximum number of repetitions. The authors reported an increased number of repetitions in the LLLT group compared to the placebo, but surface electromyography showed no statistical difference. In a similar study, Dos Santos Maciel et al. [41] (level 1b) used a muscular pre-conditioning protocol with LLLT (780 nm) applied on the tiabialis anterior muscle and investigated fatigue in an isokinetic dynamometer combined with surface electromyography analysis. This double-blind controlled trial reported an increased torque exerted by the tiabialis anterior muscle after muscular pre-conditioning, but muscle fatigue analyzed by surface electromyography was not reduced, and lactate levels in blood were not significantly different between groups.

On the other hand, de Brito Vieira et al. [42] (level 1b) in a randomized, double-blind, crossover, placebo-controlled trial applied a photobiomodulation by LLLT (808 nm) on 5 sites of the quadriceps femoris muscles between 3 sets of 20 maximum voluntary repetitions in an isokinetic dynamometer at a single training session. Two days after the training session, all volunteers were evalutated through the number of maximum repetitions of knee flexion/extension in the isokinetic dynamometer in conjunction with surface electromyography to measure muscle fatigue. The authors reported increased number of repetitions in the LLLT group and less muscle fatigue compared to the placebo group. Similarly, aiming to investigate the responsivess of elderly woman to photobiomodulation, Vassao et al. [43] (level 1b) applied LLLT (808 nm) on 8 sites of the rectus femoris before a fatigue protocol in an isokinetic dynamometer in conjunction with surface electromyography and blood lactate analysis in a randomized, double-blind, crossover, placebo-controlled trial. The LLLT group had decreased blood levels of lactate, and reduced muscle fatigue assessed by surface electromyography, but were not able to improve their muscle performance in an isokinetic dynamometer.

da Silva Alves et al. [44] (level 1b) investigated the effects of PBM on cardiopulmonary exercise testing in conjunction with electromyography analysis performed on a cycle ergometer in a randomized, double-blind, crossover, placebo-controlled trial. The authors applied a muscular pre-conditioning protocol with a cluster of 7 laser diodes (850 nm) on three sites of the quadriceps femoris muscles (1 vastus lateralis, 1 vastus medialis, 1 rectus femoris) and 1 site on the gastrocnemius muscles. Compared to placebo, LLLT increased the peak O₂ uptake, cardiovascular efficiency, but had no effect on time of running, and fatigue in electromyography analysis.

Zagatto et al. [45] recently developed a randomized, double-blind, placebo controlled-trial to investigated the effects of PBM by LLLT on performance, muscle damage and inflammatory markers in water polo players. LLLT (810 nm) was applied on 8 points of the adductor muscle region immediately after each one of the 5 training days. The authors reported a moderate improvement in the 30-s crossbar jump test (performance) in the group treated with LLLT compared to placebo, but without further improvements in performance (200 m maximal swim). In addition, there was no significant differences between groups regarding muscle damage measuring lactate dehydrogenase (LDH) and CK, or inflammatory markers measuring interleukin 1 beta (IL-1β), interleukin 10 (IL-10) and tumor necrosis factor alpha (TNF-α).

In an attempt to find the best time point to apply PBM on muscles, Dos Reis et al. [46] (level 1b) compared the effectiveness of LLLT (830 nm) applied on the quadriceps femoris muscles as muscular pre-conditioning, or after an exercise protocol using leg extension with 75% of 1-RM until muscle fatigue in a randomized, double-blind, placebo-controlled trial. The authors reported that there was no significant difference regarding the number of maximum repetitions performed by all groups. However, lactate and CK levels in blood were lower in the group that was treated with LLLT after the exercise protocol when compared to placebo and LLLT delivered before the exercise.

Fritsch et al. [47] (level 1b) investigated the effects of photobiomodulation by LLLT (810 nm) on plyometric exercises, muscle damage (ultrasonography), soreness (visual analogue scale - VAS), torque in maximum voluntary contraction (MVC), as well as the best moment of irradiation: muscular pre-conditioning versus irradiation after a bout of exercise. This randomized, double-blind, placebo-controlled trial reported that both irradiation time points (muscular pre-conditioning and after exercise) promoted significant reduction in muscle damage compared to placebo (contralateral limb), but did not produce positive effects on VAS and MVC.

Recently Pinto et al. [48] (level 1b) investigated the effects of photobiomodulation using laser diodes and LEDs on muscle performance of rugby athletes in a randomized, crossover, double-blinded, placebo-controlled trial. These athletes received a muscular pre-conditioning protocol with laser diodes (905 nm) and LEDs (640 nm and 875 nm) assembled in the same device, or placebo therapy, before assessment in the Bangsbo Sprint Test at the training field, and blood lactate collection at 3, 10, 30 and 60 minutes after the Bangsbo Sprint Test. Compared to placebo therapy, the authors reported an improved average time for the sprints, lower fatigue index and lower percentage of blood lactate when athletes received the muscular pre-conditioning. However, PBM was not able to improve the best time for all the seven sprints performed in the Bangsbo Sprint Test.

Regarding the use of photobiomodulation in the sports field in real life competition, and trying to translate laboratory findings to clinical practice, Ferraresi et al. [49] (level 1b) used an array of 200 LEDs (100 LEDs at 850 nm and 100 LEDs at 630 nm) to test the effectiveness of PBM by LEDT for prevention of muscle damage in a randomized, double-blind placebo- controlled trial. The authors applied muscular pre-conditioning with LEDT on the quadriceps femoris, hamstrings and triceps surae muscles of professional volleyball players before each official match during a national championship to prevent muscle damage measured by CK. In addition, this study tested 4 light energies (doses): 105 J, 210 J and 315 J and placebo. The authors reported that the effective light energies (210 J and 315 J) could prevent a statistically significant rise in CK while 105 J and placebo allowed significant increases in CK to occur in the blood 24 h after each official match.

Table 3 presents all parameters of PBM used in acute response to exercises with lower limbs. Figure 3 shows an example of the sites of irradiation on the quadriceps femoris muscles and an exercise test for lower limbs in isokinetic dynamometer in conjunction with surface electromyography analysis.

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Figure 3

A) Muscular pre-conditioning irradiating multiple sites or points of the quadriceps femoris muscles in order to cover the whole muscle group. B) Exercise testing in an isokinetic dynamometer in conjunction with surface electromyography analysis.

C. Acute photobiomodulation (PBM) responses in exercise on a treadmill

There have been several studies in the literature looking at the acute effects of PBM on muscles when used in muscular pre-conditioning regimens, and testing exercise performed on a treadmill. De Marchi et al. [50] (level 1b) in a randomized, double-blind, crossover, placebo-controlled trial used a cluster of 5 laser diodes (810 nm) applied on the quadriceps femoris muscles, hamstrings and triceps surae before a protocol of progressive and maximum effort on a treadmill. This study showed that LLLT increased both the relative and absolute oxygen uptake as well as the maximum time of running on the treadmill when compared with the placebo group. In addition, LDH, CK and lipid peroxidation (TBARS - thiobarbituric acid reactive substances) were significantly higher in the placebo group showing the PBM had protected against muscle damage. Finally, superoxide dismutase enzyme activity was lower in the placebo group after the exercise compared to the PBM group sugesting that PBM can protect aginst oxidative stress.

Analyzing the kinetics of oxygen uptake, Ferraresi et al. [51] (level 3b) conducted a randomized, double-blind, crossover, placebo-controlled trial with a single elite runner athlete. The authors applied a muscular pre-conditioning protocol on the lower and upper limbs and the trunk muscles using an array of 50 LEDs (850 nm) before high-intensity constant workload running exercise on a treadmill. Compared to placebo therapy, LEDT improved the speed of muscular VO₂ adaptation, decreased O₂ deficit, increased the VO₂ from the slow component phase, and increased the time limit of exercise. LEDT also decreased CK in blood (muscle damage) and reduced other markers of muscle damage and fatigue, which were alanine and lactate levels in the urine analyzed by proton nuclear magnetic resonance spectroscopy (¹H NMR).

Miranda et al. [52] (level 1b) also conducted a randomized, double-blind, crossover, placebo-controlled trial to investigate the effects of PBM using a cluster probe with laser diodes (905 nm) and LEDs (640 nm and 875 nm) on cardiopulmonary exercise tests. The authors reported increases in the distance covered, time to exhaustion, ventilatory rate and less dyspnea when active PBM was applied on 9 sites of the quadricesps femoris muscles, 2 sites of the hamstrings and 2 sites on gastrocnemius muscles immediately before (muscular pre-conditioning) the cardiopulmonary exercise test.

However, recently a double-blind, crossover, placebo-controlled trial conducted by Malta et al. [53] (level 1b) investigated the effects of LEDT applied as muscular pre-conditioning to improve high-intensity running effort in health subjects. This study used a cluster with 56 red (660 nm) and 48 infrared (850 nm) LEDs applied on the quadriceps femoris and biceps femoris muscles and between soleus and gastrocnemius region. The authors reported no effect of LEDT on maximal accumulated oxygen deficit, or contributions of the three different types of muscle metabolism (aerobic or glycolytic or phosphagen), time to exhaustion, peak lactate concentration, exhaustion perceived and heart rate at exhaustion. Moreover, the authors reported a possible negative effect of LEDT on maximal accumulated oxygen deficit and lactate based on the magnitude inference of effect size.

Table 4 presents all parameters of PBM used in acute response to exercises performed on treadmill. Figure 4 shows an example of the sites of irradiation on the quadriceps femoris muscles and a cardiopulmonary exercise testing on treadmill.

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Figure 4

A) Muscular pre-conditioning irradiating multiple sites or points of the quadriceps femoris muscles in order to cover all muscle group. B) Cardiopulmonary exercise testing on a treadmill.

MRH was funded by US NIH grant AI050875. CF was supported by CNPq, Conselho Nacional de Desenvolvimento Científico e Tecnológico (Scholarship 202313/2014-0).