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Table of Contents
ORIGINAL ARTICLE
Year : 2019  |  Volume : 62  |  Issue : 6  |  Page : 273-278

The impact of high-intensity laser therapy on oxidative stress, lysosomal enzymes, and protease inhibitor in athletes


1 Department of Pathophysiology of Hearing and Balance, Ludwik Rydygier Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University, Torun; Rehabilitation Center Multidisciplinary City Hospital, Bydgoszcz, Poland
2 Department of Medical Biology and Biochemistry, Ludwik Rydygier Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University, Torun, Poland
3 Department of Pathophysiology of Hearing and Balance, Ludwik Rydygier Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University, Torun, Poland
4 Rehabilitation Center Multidisciplinary City Hospital, Bydgoszcz; Department of Laser Therapy and Physiotherapy, Ludwik Rydygier Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University, Torun, Poland
5 Department of Neurosurgery, Stanislaw Staszic Specialist Hospital, Pila, Poland
6 Department of Psychiatry, Ludwik Rydygier Collegium Medicum of Nicolaus Copernicus University, Bydgoszcz, Poland

Date of Submission10-May-2019
Date of Acceptance16-Oct-2019
Date of Web Publication29-Nov-2019

Correspondence Address:
Dr. Jolanta Czuczejko
Department of Psychiatry, Ludwik Rydygier Collegium Medicum of Nicolaus Copernicus University, M. Curie Sklodowskiej 9 Street, 85-094 Bydgoszcz
Poland
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/CJP.CJP_40_19

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  Abstract 

The aim of the study was to assess the effect of one session of high-intensity laser therapy (HILT) on the levels of selected oxidative stress parameters, lysosomal hydrolases, and anti-inflammatory serine protease inhibitor in the peripheral blood of amateur athletes with torn or pulled tendons of the ankle or the knee joint. The group of injured athletes comprised 16 males and females aged 16.3 ± 1.3 years, while the control group of 14 healthy, noninjured amateur athletes of both sexes (controls; age 17.4 ± 4.6 years). Material for the study was peripheral blood taken at three study time points: Immediately before, 30 min after, and 24 h after HILT intervention. In plasma and erythrocytes, thiobarbituric acid reactive substances (TBARSpl and TBARSer, respectively) were determined. In erythrocytes, the activities of superoxide dismutase (SOD), glutathione peroxidase (GPx), and catalase (CAT) were measured. In serum, the activity of acid phosphatase (AcP), arylsulfatase (ASA), cathepsin D (CTS D), and α1-antitrypsin (AAT) were determined. Among oxidative stress parameters, only the CAT activity significantly decreased 24 h after HILT compared to measurement 30 min after the treatment in the injured individuals (P < 0.01), while the GPx activity in that group was meaningfully higher 30 min after HILT compared to controls (P < 0.05). Thirty min after the intervention, the activities of AcP and ASA were lower in the injured participants compared to the uninjured ones (P < 0.01 and P < 0.05, respectively). The CTS D activity was lower 30 min and 24 h after HILT in both groups (P < 0.001) and did not differ significantly between them (P > 0.05). Moreover, the study showed statistically significant linear relationships between the TBARSer concentration and the SOD activity before HILT in the healthy participants (r = -0.6, P = 0.021) and 24 h after HILT in the injured ones (r = 0.6, P = 0.025). In the noninjured athletes before HILT, the CTS D activity linearly correlated with the AAT activity (r = -0.70, P = 0.005), and 30 min after the treatment, with the AcP activity (r = 0.5, P = 0.041). 24 h after the HILT intervention, the CTS D and AcP activities were also correlated in the injured athletes (r = 0.8, P = 0.002). The study suggests that one HILT intervention does not significantly influence the redox equilibrium but stabilizes lysosomal membranes.

Keywords: High-intensity laser therapy, lysosomal hydrolases, oxidative stress, α1-antitrypsin


How to cite this article:
Sielski &, Sutkowy P, Katarzyna PO, Woźniak A, Skopkowska A, Woźniak B, Czuczejko J. The impact of high-intensity laser therapy on oxidative stress, lysosomal enzymes, and protease inhibitor in athletes. Chin J Physiol 2019;62:273-8

How to cite this URL:
Sielski &, Sutkowy P, Katarzyna PO, Woźniak A, Skopkowska A, Woźniak B, Czuczejko J. The impact of high-intensity laser therapy on oxidative stress, lysosomal enzymes, and protease inhibitor in athletes. Chin J Physiol [serial online] 2019 [cited 2019 Dec 8];62:273-8. Available from: http://www.cjphysiology.org/text.asp?2019/62/6/273/272023

Łukasz Sielski and Paweł Sutkowy contributed equally to this work.



  Introduction Top


There are many methods of physiotherapy successfully used in the rehabilitation of the locomotor system. Among the most recent methods is the use of laser light with a wavelength of approximately 1000 nm (mostly 1064 nm) (high-intensity laser therapy [HILT], or high-power laser therapy, HPLT) in extremely short pulses (the BTL HIL technique), which yields a completely new therapeutic quality by generating a photomechanical wave in a tissue (with a typical energy of 0.51–120 J/cm2 and a laser power output of up to 12 W). This leads to the generation of heat in the diseased tissue (an increase of approx. 2°C–3°C) and mechanical stimulation of nociceptors and other nerve terminals. As a result, pain pathways in the nervous system are blocked, which brings an instant pain relief. HILT also significantly reduces inflammation and improves metabolism in the injured tissue, since it locally stimulates blood and lymph circulation leading to reduced edema and increased blood supply. Consequently, healing of the damaged tissue occurs, and a potent yet nonaddictive pain therapy is provided.[1],[2]

HILT appears to be a more interesting branch of specialized physiotherapy compared to, e.g., low-level laser therapy (LLLT), a better known and longer used method with similar properties but lower levels of treatment parameters (energy dose in the range of 0.01–100 J/cm2 with a laser power output of 0.001–0.1 W; wavelength usually near to 500–600 nm).[3] In HILT, thanks to the higher laser energy, the range of the effect on the diseased tissue is much greater (depth up to 10 cm), hence the therapeutic effect is probably much more pronounced. However, the impact of HILT on the human body is still poorly known, particularly as regards biochemical phenomena[4] which have already been partially studied with LLLT (increased ATP production and expression of genes related to cell migration and proliferation, anti-inflammatory signaling, antiapoptotic proteins, and antioxidant enzymes).[5]

Injuries in sports are largely caused by mechanical damage resulting from excessive load to tissues involved in physical effort or from impacts and abrasion. A considerable role in the onset of an injury is played by physiological processes, such as the oxidant–antioxidant equilibrium associated with the capacity of the body for effort and regeneration. Therefore, damage to the locomotor system is not only a result of mechanical damage but also of metabolic dysfunctions. The oxidant–antioxidant equilibrium can be severely disrupted as a result of excessively intense physical effort and/or incorrect diet (oxidative stress) or as a result of oversupply of antioxidants (“reductive stress”). Inflammation plays an essential role in this phenomenon, as inflammatory processes are strictly associated with the production of oxidants (reactive oxygen species [ROS] and reactive nitrogen species [RNS]).[6] To assess the degree of ROS and RNS generation in the organism, the activity or concentration of low molecular weight antioxidants (e.g., Vitamins A, E, and C) and high molecular weight antioxidants (e.g., superoxide dismutase [SOD]; glutathione peroxidase [GPx]; catalase [CAT]) can be determined, together with the concentration of free radical oxidation products (e.g., thiobarbituric acid reactive substances [TBARS]; malondialdehyde [MDA]; 4-hydroxynonenal; F2-isoprostanes; protein carbonyls; 8-hydroxydeoxyguanosine).[6],[7],[8] In turn, inflammation is linked to the increased activity of not only inflammation mediators but also lysosomal hydrolases (e.g., cathepsin D [CTS D]) and anti-inflammatory proteins (e.g., α1-antitrypsin [AAT]).[6],[9]

The aim of the study was to assess the effect of one HILT intervention on redox parameters (TBARS, SOD, GPx, and CAT), selected lysosomal hydrolases (acid phosphatase [AcP]; arylsulfatase [ASA]; CTS D), and the activity of the anti-inflammatory serine protease inhibitor AAT in peripheral blood of injured amateur athletes.


  Materials and Methods Top


Participants

The study participants were a group of 30 amateur athletes randomly selected from 120 male and female members of volleyball and Kayak clubs in Bydgoszcz, Poland. The group of injured athletes comprised 16 male and female participants with a locomotor system injury involving pain resulting from tearing or pulling of tendons in the ankle or knee joint. Fourteen amateur athletes of both sexes and without any injury constituted the control group. The characteristics of the study participants are shown in [Table 1].
Table 1: Characteristics of the study participants (mean±standard deviation)

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The participants were examined at the beginning of the sports season when they trained for a maximum of 5 times/week. Exclusion criteria included recent surgical procedures, chronic diseases (asthma), ongoing viral or bacterial infections with fever, or other systemic inflammation. Moreover, the injured participants did not take any analgesics and/or anti-inflammatory drugs. HILT was the only method of treating the injury and was performed up to 12 h after the injury.

Parents/legal guardians of the study participants had signed their consent for participation in the study. The study was approved by the Bioethics Committee of Ludwik Rydygier Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Torun, Poland (no. KB 395/2013) and registered in a clinical trial database (no. CTRI/2018/01/011344).

All participants were subjected to one session of HILT using a BTL-6000 HIL 12 W device with settings for an analgesic effect: wavelength 1064 nm, laser power 8 W, surface energy density 6 J/cm2, frequency 25 Hz, and exposure time of a treatment point 10 s. In every participant, laser emitted from the diode of the device acted on six treatment points on the skin of the ankle or knee joint (25 cm2, total energy 150 J).

The experimental material was peripheral blood taken from the basilic vein into vacuum tubes with potassium versenate (full blood, plasma; Vol. 4 mL) and vacuum tubes with coagulation activator and separation gel (blood serum; Vol. 5 mL). The blood from each participant was taken three times (total volume 27 mL): immediately before the intervention (baseline) (9 mL), 30 min after the end of the intervention (9 mL), and 24 h thereafter (9 mL). The TBARS, SOD, CAT, and GPx levels were assayed in fresh blood samples (up to 2–3 h from collection, transport at 4°C) in plasma and/or erythrocyte suspension that were prepared according to the method described by Beuge and Aust.[10] The activities of lysosomal enzymes (AcP, ASA, and CTS D) and that of the inhibitor of serine proteases (AAT) were assayed in serum stored at −20°C with no additions (cryoprotectants, protease inhibitors, etc.) up to 1 month prior to conducting the assays.

Methods

Blood was examined using spectrophotometric methods. In blood plasma and red blood cells, TBARS were determined (TBARSpl and TBARSer, respectively). The following reagents were added to blood plasma and erythrocyte suspension (50% v/v in PBS solution): 0.375% thiobarbituric acid (TBA), 15% trichloroacetic acid (TCA), and 0.25 mol/L HCl, and subsequently incubated on a water bath for 20 min at 100°C. The samples were then cooled down (to 4°C) and centrifuged for 15 min (at 2000×g). After centrifugation, supernatants were collected, and absorbance at λ = 532 nm was measured.[11],[12] Moreover, in red blood cells, the activities of (SOD; E. C. 1.15.1.1), (GPx; E. C. 1.11.1.9), and (CAT; E. C. 1.11.1.6) were measured. The SOD activity was determined based on the inhibition of adrenaline autoxidation to adrenochrome in alkaline conditions.[13] The GPx activity was estimated using a method based on the decomposition of hydrogen peroxide with the concurrent oxidation of reduced glutathione, a cofactor in this reaction.[14] The CAT activity was determined by measuring the decrease in the absorbance of a solution of hydrogen peroxide due to decomposition of H2O2 by the enzyme.[15]

In blood serum, the activity of (AcP; E. C. 3.1.3.2) was determined using the Bessey–Lowry–Brock method, as modified by Krawczyński;[16] that of (ASA; E. C. 3.1.6.1) – using the Roy method, as modified by Błeszyński;[17] that of (CTS D; E. C. 3.4.23.5) – using a method by Anson described by Sielski et al.;[17] and that of AAT – using a method by Eriksson.[18] To determine the AcP activity, disodium p-nitrophenylphosphate (substrate) in 0.5 mol/L citrate-tartrate-formaldehyde buffer at pH 4.9 was used. The measure of enzyme activity was the quantity of p-nitrophenol released during the enzymatic hydrolysis of the substrate.[15] To determine the ASA activity, 0.01 mol/L 4-nitrocatechol sulfate (substrate) in 0.5 mol/L acetate buffer at pH 5.6 was used. The measure of enzyme activity was the quantity of 4-nitrocatechol released during the enzymatic hydrolysis of the substrate.[16] To determine the CTS D activity, 2% denatured bovine hemoglobin was subjected to hydrolysis with the enzyme at 37°C. The reaction was subsequently stopped with a 0.1 mol/L NaOH solution, a phenolic reagent was added (to obtain blue coloration), and absorbance of the resulting solution was measured at λ = 660 nm.[17] To determine the AAT activity, measurement of the decreasing enzymatic activity of trypsin after short incubation with blood serum was conducted.[18]

Statistical analysis

The results were analyzed using parametric tests. The Kolmogorov–Smirnov test for the normality of distribution and Levene's test of the homogeneity of variances were performed. The main analysis was based on an ANOVA test with a posteriori multiple comparison test, Tukey's HSD test. Moreover, Pearson's product–moment correlation coefficient (r) was calculated in the study between parameters. The results were expressed as an arithmetic mean ± standard deviation. Differences between the means with P < 0.05 were considered to be statistically significant.


  Results Top


All study results are presented in [Table 2]. The study did not demonstrate statistically significant changes in the concentration of TBARS. A tendency of these substances to reach their highest levels in healthy athletes 24 h after the HILT intervention was observed in both plasma end erythrocytes (P > 0.05). A similar tendency was noted in the injured athletes, but only regarding the TBARSpl concentration, since the TBARSer concentration was slightly decreased at that study time point (P > 0.05). The GPx activity 24 h after HILT was the highest in the controls (P > 0.5), but not in the other group of participants. In the injured athletes, the GPx activity slightly decreased 24 h after the treatment, while the highest activity of the enzyme was revealed 30 min after HILT, and it was higher in a statistically significant manner compared with the activity measured in healthy athletes at that time point (P < 0.05).
Table 2: The levels of oxidant stress parameters and lysosomal enzymes, as well as the activity of anti-inflammatory protein in healthy and injured amateur athletes (arithmetic mean±standard deviation)

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As for the other antioxidant enzymes, SOD and CAT, their activities were higher 30 min after HILT compared to baseline in both study groups, and 24 h after HILT were insignificantly lower than before the intervention (P > 0.05). The CAT activity in the injured athletes was significantly lower 24 h after the intervention compared with that measured at the 30-min time point (P < 0.01). In general, differences in activities of antioxidant enzymes between the healthy and the injured athletes were statistically insignificant, except for the aforementioned difference in the GPx activity.

The activities of the investigated lysosomal enzymes changed to a greater extent. In both groups of participants, a tendency for a decrease in the AcP activity after the intervention was observed, which was more pronounced in the group of injured athletes (P > 0.05). The AcP activity measured in that group was slightly lower than in the noninjured athletes, and in measurement II performed 30 min after HILT, the activity was statistically significantly lower (P < 0.01). Similarly, the AcP activity measured 24 h after the intervention was lower than before the intervention, but only in the injured athletes the difference was meaningful (P < 0.05). The change in the ASA activity in both groups resembled those observed for the antioxidant enzymes (P > 0.05). Comparing the two groups, the ASA activity 30 min after the intervention, as in the case of AcP, was higher in the healthy athletes than in the injured ones (P < 0.05). The CTS D activity was similar in both groups (P > 0.05) and changed in a similar way –30 min and 24 h after completing the HILT procedure, it was lower in a statistically significant manner compared with the baseline activity. However, also in this case, the changes in the CTS D activity were more pronounced in the injured participants, since the enzyme activity 24 h after the HILT session was significantly lower compared with a measurement performed 30 min after the intervention (P < 0.05). The AAT activity practically did not change in the study (P > 0.05).

Moreover, the study showed statistically significant linear relationships between the determined parameters. At study timepoint I, in the noninjured persons, the TBARSer concentration was strongly inversely correlated with the SOD activity [r = −0.6, P = 0.021; [Figure 1], similarly to the activities of AAT and CTS D [r = −0.7, P = 0.005; [Figure 2]. In measurement II, in the same study participants, a strong and direct linear relationship was revealed between the CTS D and AcP activities [r = 0.5, P = 0.041; [Figure 3], whereas 24 h after HILT, strong and very strong positive linear correlations between the TBARSer concentration and the SOD activity [r = 0.6, P = 0.025; [Figure 1] and between the AcP and CTS D activities [r = 0.8, P = 0.002; [Figure 3], respectively, were found in the injured athletes.
Figure 1: Linear regression between the TBARSer concentration and the SOD activity in measurement I (before HILT) in healthy participants (r = −0.6, P = 0.021) and in measurement III (24 h after HILT) in injured participants (r = 0.6, P = 0.025). HILT: high-intensity laser therapy, TBARSer: Thiobarbituric acid reactive substances in erythrocytes, SOD: Superoxide dismutase.

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Figure 2: Pearson's r coefficient between the CTS D and AAT activities in noninjured participants before HILT application (r = −0.70, P = 0.005). HILT: High-intensity laser therapy, CTS D: Cathepsin D, AAT: a1-antitrypsin.

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Figure 3: Linear correlations between the CTS D and AcP activities 30 min after HILT procedure in uninjured participants (r = 0.5, P = 0.041) and 24 h thereafter in injured participants (r = 0.8, P = 0.002). HILT: High-intensity laser therapy, CTS D: Cathepsin D, AcP: Acid phosphatase.

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  Discussion Top


No relevant impact of HILT on the oxidant–antioxidant balance was revealed in the study participants, since most changes in the levels of oxidoreduction parameters were out of the statistical significance range, also comparing both groups (P > 0.05). However, the obtained results suggest a slightly greater influence of one HILT treatment on the redox equilibrium in red blood cells in the injured individuals compared to the uninjured ones. In the former, the GPx activity was higher 30 min after the intervention, and the CAT activity 24 h thereafter decreased to a greater extent than in the latter (comparison to 30-min time point; P < 0.01). The increased activity of GPx proves an increased concentration of hydrogen peroxide (H2O2), whereas the decreased activity of CAT proves a decreased concentration of this ROS, since both enzymes react with it and reduce it to oxygen and/or water.[7] Moreover, negative linear correlations were found in the study between the TBARS concentration and the SOD activity [Figure 1]. SOD removes superoxide anion radical (O2˙–); therefore, the higher radical concentration, the higher the SOD activity. However, when the production of O2˙– exceeds antioxidant capacity (the SOD activity), the portion of the radical which has not been neutralized by SOD initiates oxidative damage to cellular structures including lipids. As a result, MDA, a secondary lipid peroxidation product which dominates among TBARS, appears.[8] Thus, the negative correlation between the SOD activities and the TBARS concentration may be evidence of a disturbance in the oxidant–antioxidant equilibrium. The relationship was observed in the healthy participants before the HILT procedure (r = −0.6, P = 0.021). These participants practiced sports and physical exercise disrupts redox balance.[7] In the injured participants, a positive correlation was revealed 24 h after HILT, with the same strength and almost identical statistical significance (r = 0.6, P = 0.025). Thus, one HILT treatment modified the relationship between these elements in redox reactions in erythrocytes. It seems unlikely that the change was caused by the injury, since no other correlations between oxidoreduction parameters were found, and in particular, there were no statistically significant differences between baseline measurements in both groups.

Greater differences were observed in the case of the lysosomal enzymes whose values differed between the groups despite the usually similar changes after HILT. An unambiguous interpretation of the results is not straightforward, although the study appears to confirm the beneficial effect of the HILT intervention on the regeneration of damaged tissue.[2] AcP is an enzyme that dephosphorylates phosphate monoesters. For example, it has been shown that serum AcP concentration increases in the course of cancer in humans.[19] There is a close relationship between neoplasia and oxidative stress and inflammation: a continuous oxidative stress promotes chronic inflammation which can lead to carcinogenesis and other chronic diseases.[6],[20] In turn, ASA is an enzyme that hydrolyzes sulfuric acid esters, participating in the metabolism of the neuronal myelin sheath (metabolism of glycosphingolipids). Mutations in the ASA gene (leading to reduced or abolished enzyme activity) cause neurodegenerative diseases.[21] In the present study, the AcP and ASA serum activities 30 min after the HILT intervention were lower in the injured athletes than in the healthy ones (P < 0.01 and P < 0.05, respectively). The AcP activity in the injured group was also lower 24 h after the intervention compared to baseline (P < 0.05). A similar change in the noninjured athletes was statistically insignificant (P > 0.05). The CTS D activity also significantly decreased in both study groups after HILT, both 30 min, and 24 h after treatment (P < 0.01). CTS D is the main lysosomal hydrolase, endowed with a high proteolytic activity and involved in the metabolism of proteins. Increased activity of CTS D and its release into the intercellular space has been found in severe local inflammations (e.g., during tumor progression), which can also be the source of increase in its activity in peripheral blood.[22] Thus, the results indicate a reduction of proteolytic activity in serum as a result of HILT intervention; however, no such impact of the injury was observed. The CTS D activity did not differ compared with controls (P > 0.05). Similarly, the activity of AAT, an acute-phase protein with anti-inflammatory properties,[9] was practically the same throughout the study (P > 0.05). The negative correlation between the CTS D and AAT activities in the noninjured athletes at the start timepoint of the study indicates a correct cooperation between them [Figure 2]. A similar phenomenon can be proposed based on the positive correlation between the CTS D and AcP activities [Figure 3]. Lysosomes are cell organelles that liberate their hydrolases into the cytoplasm and intercellular spaces. During inflammation, this process increases and manifests as elevated activities of lysosomal enzymes in blood.[23] However, lysosomal enzyme leakage is also strictly associated with oxidative stress. ROS at excessive concentrations initiate oxidation of lysosomal protein–lipid membrane (free-radical lipoperoxidation). This results in membrane fragmentation and increased permeability, interalia to enzymes. Naturally, similar effects appear during oxidation of other biological membranes, e.g., cell membrane.[7],[24] Thus, HILT apparently improved the lysosomal membrane stability, perhaps as a result of improved blood flow in the injured tissue, since the impact on the redox balance was rather insignificant, as it is discussed here.

The biochemical effects of HILT in humans can be similar to those of LLLT, a type of laser therapy which uses lower-energy laser. The authors suppose that the laser light used in the LLLT technique (400–700 nm or 780–1100 nm, 0.005–5 W/cm2, 0.04–50 J/cm2) is absorbed by cytochrome c oxidase. It results in an increased electron transport in mitochondria and elevated ATP production. Other hypothesis concerns activation of numerous signaling pathways via absorption of laser light by light-sensitive ion channels resulting in, e.g., increased ROS and calcium concentrations inside the cell. The induced pathways promote transcription of genes associated with cell migration and proliferation, as well as anti-inflammatory, antiapoptotic, and anti-oxidant signaling.[5] Fillipin et al. suggested that LLLT protects against oxidative stress and fibrosis of torn Achilles tendons in rats. The authors demonstrated that the concentration of TBARS, the chemiluminescence induced by hydroperoxides, and the concentration of collagen in the damaged tendons during 14- and 21-day periods of irradiation with laser light (904 nm, 0.045 W, 5 J/cm2, duration 35 s, continuously) were significantly lower, with a concurrent higher activity of SOD, than in injured tendons not treated with LLLT. They also demonstrated a reduction of inflammation and fibrosis in the damaged tissue as a result of LLLT.[25]


  Conclusions Top


An intervention using HILT does not have a significant impact on the oxidant–antioxidant equilibrium in young amateur athletes, only slightly disturbing this equilibrium, but appears to enhance the stability of lysosomal membranes.

Acknowledgments

The study did not receive specific funding but was performed as part of the employment of the authors in Ludwik Rydygier Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University, Toruń, Poland.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Alayat MS, Mohamed AA, Helal OF, Khaled OA. Efficacy of high-intensity laser therapy in the treatment of chronic neck pain: A randomized double-blind placebo-control trial. Lasers Med Sci 2016;31:687-94.  Back to cited text no. 1
    
2.
Wyszyńska J, Bal-Bocheńska M. Efficacy of high-intensity laser therapy in treating knee osteoarthritis: A first systematic review. Photomed Laser Surg 2018;36:343-53.  Back to cited text no. 2
    
3.
Farivar S, Malekshahabi T, Shiari R. Biological effects of low level laser therapy. J Lasers Med Sci 2014;5:58-62.  Back to cited text no. 3
    
4.
Santamato A, Solfrizzi V, Panza F, Tondi G, Frisardi V, Leggin BG, et al. Short-term effects of high-intensity laser therapy versus ultrasound therapy in the treatment of people with subacromial impingement syndrome: A randomized clinical trial. Phys Ther 2009;89:643-52.  Back to cited text no. 4
    
5.
de Freitas LF, Hamblin MR. Proposed mechanisms of photobiomodulation or low-level light therapy. IEEE J Sel Top Quantum Electron 2016;22. pii: 7000417.  Back to cited text no. 5
    
6.
Reuter S, Gupta SC, Chaturvedi MM, Aggarwal BB. Oxidative stress, inflammation, and cancer: How are they linked? Free Radic Biol Med 2010;49:1603-16.  Back to cited text no. 6
    
7.
Peternelj TT, Coombes JS. Antioxidant supplementation during exercise training: Beneficial or detrimental? Sports Med 2011;41:1043-69.  Back to cited text no. 7
    
8.
Grotto D, Santa Maria L, Valentini J. Importance of the lipid peroxidation biomarkers and methodological aspects for malondialdehyde quantification. Quim Nova 2009;32:169-74.  Back to cited text no. 8
    
9.
Mila-Kierzenkowska C, Woźniak A, Szpinda M, Boraczyński T, Woźniak B, Rajewski P, et al. Effects of thermal stress on the activity of selected lysosomal enzymes in blood of experienced and novice winter swimmers. Scand J Clin Lab Invest 2012;72:635-41.  Back to cited text no. 9
    
10.
Buege JA, Aust SD. Microsomal lipid peroxidation. Methods Enzymol 1978;52:302-10.  Back to cited text no. 10
    
11.
Esterbauer H, Cheeseman KH. Determination of aldehydic lipid peroxidation products: Malonaldehyde and 4-hydroxynonenal. Methods Enzymol 1990;186:407-21.  Back to cited text no. 11
    
12.
Misra HP, Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem 1972;247:3170-5.  Back to cited text no. 12
    
13.
Paglia DE, Valentine WN. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 1967;70:158-69.  Back to cited text no. 13
    
14.
Beers RF Jr. Sizer IW. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 1952;195:133-40.  Back to cited text no. 14
    
15.
Krawczyński J. Enzymatic diagnostics in practical medicine. In: Methods of Investigation. Warszawa: Wydawnictwo lekarskie PZWL; 1972.  Back to cited text no. 15
    
16.
Błeszyński W, Działoszyński LM. Purification of soluble arylsulphatases from ox brain. Biochem J 1965;97:360-4.  Back to cited text no. 16
    
17.
Sielski Ł, Sutkowy P, Skopowska A, Pawlak-Osińska K, Augustyńska Z, Hewelt K, et al. The oxidant-antioxidant equilibrium and inflammatory process indicators after an exercise test on the AlterG antigravity treadmill in young amateur female athletes. Oxid Med Cell Longev 2018;2018:1-8.  Back to cited text no. 17
    
18.
Eriksson S. Studies in alpha 1-antitrypsin deficiency. Acta Med Scand Suppl 1965;432:1-85.  Back to cited text no. 18
    
19.
Muniyan S, Chaturvedi NK, Dwyer JG, Lagrange CA, Chaney WG, Lin MF. Human prostatic acid phosphatase: Structure, function and regulation. Int J Mol Sci 2013;14:10438-64.  Back to cited text no. 19
    
20.
Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007;39:44-84.  Back to cited text no. 20
    
21.
Almeciga-Diaz CJ, Echeverri OY, Salazar-Barreto D, Barrera LA. Understanding the metabolic consequences of human arylsulfatase A deficiency through a computational systems biology study. Cent Nerv Syst Agents Med Chem 2017;17:72-7.  Back to cited text no. 21
    
22.
Tsukuba T, Okamoto K, Yasuda Y, Morikawa W, Nakanishi H, Yamamoto K. New functional aspects of cathepsin D and cathepsin E. Mol Cells 2000;10:601-11.  Back to cited text no. 22
    
23.
Johansson AC, Appelqvist H, Nilsson C, Kågedal K, Roberg K, Ollinger K. Regulation of apoptosis-associated lysosomal membrane permeabilization. Apoptosis 2010;15:527-40.  Back to cited text no. 23
    
24.
Sutkowy P, Woźniak A, Boraczyński T, Boraczyński M, Mila-Kierzenkowska C. The oxidant-antioxidant equilibrium, activities of selected lysosomal enzymes and activity of acute phase protein in peripheral blood of 18-year-old football players after aerobic cycle ergometer test combined with ice-water immersion or recovery at room temperature. Cryobiology 2017;74:126-31.  Back to cited text no. 24
    
25.
Fillipin LI, Mauriz JL, Vedovelli K, Moreira AJ, Zettler CG, Lech O, et al. Low-level laser therapy (LLLT) prevents oxidative stress and reduces fibrosis in rat traumatized achilles tendon. Lasers Surg Med 2005;37:293-300.  Back to cited text no. 25
    


    Figures

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