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O RIGINAL R ESEARCH

Preventive Effects of 10-Day Supplementation With Saffron and Indomethacin on the Delayed-Onset Muscle Soreness

Abbas Meamarbashi, PhD and Ali Rajabi, MSc

Objective: Delayed-onset muscle soreness (DOMS) often occurs after unaccustomed eccentric exercise and reduces exercise perfor- mance. We aimed to study the preventive effects of saffron and indomethacin on the biochemical and functional indicators of DOMS after 1-session eccentric exercise.

Design: A 10-day, randomized, double-blind, placebo-controlled, pretest posttest design.

Setting: Controlled research laboratory.

Participants: Thirty-nine nonactive male university students randomly divided into saffron (n = 12), indomethacin (n = 12), and control (n = 15) groups.

Interventions: Saffron group received 1 capsule containing dried saffron powder (n = 12, 300 mg/d), indomethacin group received 75 mg indomethacin (n = 12, 25 mg thrice a day), and control group (n = 15) received placebo capsules, 1 week before and 3 days after eccentric exercise. Ten days before and 24, 48, and 72 hours after muscle soreness protocol, the maximum isometric and isotonic forces, plasma creatine kinase (CK), plasma lactate dehydrogenase (LDH), perceived pain, knee range of movement, and thigh circum- ference were measured. Muscle soreness protocol was performed with a weight load equal to 80% of the maximum isotonic force in 4 sessions with 20 repetitions and 3-minute rest in between.

Main Outcome Measures: This study shows that 10-day supplementation with 300 mg saffron signicantly decreased the CK and LDH concentrations ( P , 0.0001). In the saffron group, there was no decline in maximum isometric and isotonic forces after eccentric exercise, but a signi cant decline in the isometric force was observed in the control group ( P , 0.0001). No pain was reported in the saffron group, whereas the indomethacin group experienced pain before 72 hours ( P , 0.001).

Conclusions: Results obtained from the current novel research indicate a strong preventive effect of 10-day supplementation with saffron on the DOMS.

Submitted for publication August 7, 2013; accepted March 5, 2014. From the Department of Physical Education and Sports Sciences, University of Mohaghegh Ardabili, Ardabil, Iran. Supported by the university postgraduate thesis grant M416. A. Meamarbashi was an employee of University of Mohaghegh Ardabili at the time of this study, and A. Rajabi was an MSc student during this study in the University of Mohaghegh Ardabili. Corresponding Author: Abbas Meamarbashi, PhD, Department of Physical Education and Sports Sciences, University of Mohaghegh Ardabili, Ardabil 56199-11367, Iran (a_meamarbashi@yahoo.com). Copyright © 2014 Wolters Kluwer Health, Inc. All rights reserved.

Clin J Sport Med Volume 25, Number 2, March 2015

Clinical Relevance: The saffron can be used to prevent DOMS and alleviate the DOMS symptoms.

Key Words: saffron, indomethacin, delayed-onset muscle soreness, creatine kinase, lactate dehydrogenase, isometric and isotonic forces

( Clin J Sport Med 2015;25:105112)

INTRODUCTION

Delayed-onset muscle soreness (DOMS) is associated with pain and discomfort in the rst few days after a strenuous exercise session. Eccentric muscular contractions in downhill running, hopping, plyometric exercise, squatting, and during the lowering phase of lifting weights can produce DOMS. 1 Athletes are concerned about muscular discomfort and pain phenomena because it can limit their exercise and training activity. 2 The main symptoms in DOMS are muscular stiff- ness, tenderness, and pain during active movements. 3,4 There are many symptoms related to the muscle in ammation and damage such as muscle bre swelling, 5 elevated serum activ- ities of muscle speci c enzymes such as the creatine kinase (CK) and lactate dehydrogenase (LDH), 6,7 reduced muscle strength, 1 and knee joint range of movement (ROM). 8 Eccentric exercise has series of effects in the cell membrane, causing an inammatory response that leads to production of prostaglandin E 2 and leukotrienes. The muscle microscopic injury is instigated by a mechanical disruption to sarcomeres, 9 T-tubules, myobrils, cytoskeletal protein, and the sarcoplasmic reticulum, 10 12 which leads to an inamma- tory response. 13 After muscle injury, enzymatic reactions and inammatory mediators such as thromboxanes, prostaglandins, and leukotrienes from the cyclooxygenase and lipoxygenase pathways correspond to increases in vascular permeability and pain perception by sensitizing the types III and IV afferent nerve bres to both chemical and mechanical stimuli. 1 The magnitude of force loss after eccentric exercise has been claimed to be the best indirect marker of muscle soreness. 14 Mechanism of maximal force reduction in DOMS is thought to be secondary to sarcomere popping and disorganization, 15 as well as damage to components of the excitation contraction coupling process. 16,17 Prevention and treatment strategies to alleviate the symptoms and signs of DOMS are numerous and varied, including pharmacological (eg, nonsteroidal anti-inammatory medications), 18 20 exercise, 19,21 24 stretching, 19,21,22 whey pro- tein, 25 sh oil, isoavones, 26 caffeine, 27 L-carnitine, 28 herbs, 29 antioxidant vitamins, 30 cryotherapy, 19,31 34 transcutaneous elec- trical nerve stimulation, 32 and ultrasound. 24,35 However, these

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methods had small or no effect on DOMS or were not consis- tent in attenuating DOMS pain and other symptoms. 1 Administration of aspirin and acetaminophen did not reduce the DOMS and the CK response to eccentric exercise. 36 Previous studies found that ibuprofen 37 has no effect on muscle soreness. In addition, several dietary supplements have been tested in the treatment of DOMS, including whey protein, vitamin C, protease enzymes, phosphatidylserine, chondroitin sulfate, vitamin E, and sh oil, all with small effect or not effective on DOMS. 1,26,38 45 There is no clear consensus in the existing literature on an intervention that can effectively relieve pain after eccentric exercise. Conclusively, it is difcult to recommend with condence the use of these methods for minimizing the signs and symptoms of muscle soreness. 45 Some herbs and spices such as saffron are widely used in the human diet. Saffron is a spice derived from the ower of the Crocus sativus. Saffron has been traditionally used in ancient medicine against various human diseases. Saffron stigma contains more than 150 volatile and aroma-yielding compounds. It also has many nonvolatile active components, 46 many of which are carotenoids, including zeaxanthin, lyco- pene, and various a- and b-carotenes. 47 Recent experimental ndings indicate that saffrons major compounds, crocin and crocetin, which are derivatives of carotenoids, are powerful antioxidants, 48 with anti-inammatory 49 and antinocicep- tive 50,51 activities. Nonsteroidal anti-in ammatory drugs (NSAIDs) such as ibuprofen, indomethacin, and diclofenac are the most commonly investigated treatment for DOMS. The risk of overuse and its potential side effects such as stomach ulcers, hepatic, and renal toxicity should be considered. NSAIDs blocking cyclooxygenase enzyme thus inhibit the synthesis of prostaglandins from arachidonic acid and therefore neutrophil and macrophage functions are inhibiting. 52 Previously, pre- ventive effect of indomethacin (75 mg per day) for 5 days on the cytokine responses to strenuous exercise in humans has been studied. 53 The results demonstrate that indomethacin blunted serum intelukin-6 and augmented tumor necrosis factor-alpha (TNF- a ) and intelukin-10 during and after stren- uous physical exercise. It is worthy to note that in ammation itself is an essential natural process of muscle remodeling and regeneration after muscle injury, and these medicines can cause harm to the muscle. Based on the anti-in ammatory and antinociceptive effects of saffron and to compare any preventive effect of saffron with indomethacin, therefore, this study aimed to investigate the effects of 10-day supplementation with saffron in DOMS in young male university students.

METHODS

The Physical Activity Readiness Questionnaire (PAR-Q) was used for tness and health screening of volunteers. Subjects were excluded if they regularly participated in vigorous exercise in the previous 3 months. Thirty-nine young healthy male nonactive university students (age: 18.2 6 0.4 years) were selected among 50 volunteers. This study used a 10-day, ran- domized, double-blind, placebo-controlled, xed-dose, parallel- group, pretestposttest design. The university ethics committee

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approved the study (M416). The purpose and procedures of the study were fully explained, and they signed the con- sent form. The weight of the subjects, wearing minimal clothing and standing height without shoes were measured with a Seca digital scale (Seca model 707; Vogel & Halke GmbH & Co, Hamburg, Germany) to the nearest 0.1 kg and 0.5 cm. A dietary recommendation sheet was given to the subjects and requested to refrain from any nutritional supple- ments or medicines, including anti-inammatory medicines, 1 week before and during the study. Crocus sativus L. stigma was powdered, and soft capsules were lled with 300 mg saffron

powder. Contents of indomethacin capsules (25 mg) were transferred to a similar 500 mg capacity capsule, and identical placebo capsules containing 300 mg lactose were provided. The saffron group received 1 capsule containing dried saffron stigma powder (n = 12, 300 mg/d), indomethacin group received 75 mg indomethacin (n = 12, 25 mg thrice

a day), and the control group (n = 15) received placebo cap-

sules containing 300 mg lactose powder. Participants were asked to take the saffron and placebo capsules daily at 6 PM with a cup of water and indomethacin every 8 hours imme- diately after a meal. A leg press apparatus equipped with 2 force isometric sensors connected to a computerized dynamometer was used to determine the maximum isometric force. Participants were familiarized with the leg press machine and protocols before testing. First, all the participants underwent a 10-minute warm- up. Then, each participant was tested for maximum isometric force in a leg press machine. The maximum isometric force was measured while the weight is locked and subject was seated on the leg press bench, placed feet on the plantar plate with knee angle at 90 8. Two computerized dynamometer sen- sors measured the forces applied by the feet to the plantar

plates. Force data were recorded on a laptop computer and software calculated the maximum isometric force during 3 to 5 seconds trial. After 10-minute rest, maximum isotonic force was measured when the weight bar was unlocked, and the subject was seated on the bench with knee angle at 90 8 and pushed-up the weights by feet. Verbal encouragement was given to achieve a maximal effort isometric and isotonic strength tests. After a 10-minute rest, participants were instructed to perform 4 sets of eccentric exercise on a leg press machine. The weight load was set to 80% maximum isotonic force in 4 sets. Each set consisted of 20 repetitions with 3-minute rest between the sets. Participants were instructed to push the weights up by extending legs and let it slowly swing back after

a short pause. Movements were harmonized by a metronome

sound. The participants performed the protocol with a maximal effort until they were unable to continue a repetition with proper technique. The force applied to the plantar plate was recorded by a computerized dynamometer during the eccentric exercise. All participants completed the protocol. One day before the supplementation and 3 days after eccentric exercise, the blood sample was taken after overnight fasting from the control and experimental groups and before other tests. Five milliliters of venous blood was sampled from

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Preventive Effects of Saffron and Indomethacin on DOMS

an antecubital vein and collected into a tube containing tri- potassium EDTA. Samples were centrifuged at 3000 rates per minute for 10 minutes to separate the plasma. Plasma LDH and CK concentration were determined by an automatic biochemistry analyser (Hitachi Model 902; Hitachi Ltd, Tokyo, Japan) using commercial kits (Pars Azmoon, Tehran,

Iran). Muscle swelling/in ammation was determined by mea- suring the right thigh circumference. It was measured while

the subject was standing relaxed with the right leg slightly apart to facilitate easy measurement. Mid-thigh circumference was determined midway between the greater trochanter and the lateral epicondyle of the femur using a plastic measure- ment tape. The skin was marked with a semi-permanent marker for consistency on subsequent days. The thigh circumference of the right leg was measured 3 times to the nearest 1 mm, and the averages were reported.

To measure the knee joint ROM, subjects laid prone on

an examination table with both knees fully extended. The right knee joint angle was determined by using a goniometer and universal landmarks (lateral epicondyle of the femur, lateral malleous, and greater trochanter) to ensure alignment. Landmarks were marked with a semi-permanent pen to ensure consistency of subsequent measures. The axis of the goni- ometer placed at the intersection of the right thigh and shank

at the knee joint. The goniometer stationary arm was along

the line from the knee joint to the greater trochanter. The movable arm was along the lateral aspect of the bula. Knee exion range was determined when the subject maximally

and voluntarily exed his right knee.

A general rating of muscle pain was assessed using

a 0 to 6 point scale modi ed from that described by Talag. 7,54

A score of 0 corresponded to a rating of no pain, whereas

a score of 6 corresponded to a rating of unbearably pain-

ful. Subjects were requested to rate the discomfort in only

the quadriceps and calf regions of the right leg, before, 24, 48, and 72 hours after eccentric exercise. The pretest and posttest data were obtained before the supplementation and repeated 24, 48, and 72 hours after eccentric exercise at 11 to 12 AM Normal distribution of all the data was assessed using the Shapiro Wilk test. For each dependent variable, Lev- enes test was used to determine homogeneity of variance, with P , 0.05 indicating that the variance was not homo- geneous. Changes in the measures in each group over time were analyzed separately using a 2-way (group by time) repeated-measures analysis of variance (ANOVA) with Bonferroni pairwise comparisons. Measurements at before the supplementation were used as baseline measurement for the statistical analysis. The independent t test was used for further comparison be tween 2 groups at each time measurement. Data were expressed as mean 6 SD. Values of P , 0.05 were considered signi cant. The magnitude of the dif- ference between pretest and posttest was assessed by using Cohen s d as the effect size. Cohen s d of 0.20 is considered

a minor, 0.50 a medium, and 0.80 a major difference. Statis-

tical analysis was performed using SPSS 16.0 software (SPSS

Inc, Chicago, Illinois).

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RESULTS

The Shapiro Wilk test shows normality of all the data distribution except for the pain perception in the pretest due to pain-free status. Interpretation of data was performed using a 2-way repeated-measure ANOVA with Bonferroni pairwise comparison. Results obtained from the repeated-measure ANOVA with Bonferroni pairwise comparison were used for interpretation. The maximum isotonic force showed equality in the maximum force between all groups in the pretest session. Conspicuously, in the control group, there was a signi cant decline in the maximum isotonic force: after 24 hours (15.3%), 48 hours (23.8%), and 72 hours (24.3%) after the eccentric protocol. The maximum isotonic force between saffron and control groups showed signi cant differences after 24 ( P , 0.05), 48 ( P , 0.0001), and 72 hours ( P , 0.0001). The indomethacin and control groups comparison had a signi cant difference after 48 ( P , 0.05) and 72 hours ( P , 0.05). Comparison between saffron and indomethacin showed the only signi cant difference after 24 hours ( P , 0.05). The effect size between saffron and control group after 24, 48, and 72 hours was 0.99, 1.7, and 2.1, respectively. The effect size between indomethacin and control group after 24, 48, and 72 hours was 0.02, 0.19, and 0.23, respectively. The saffron group had the highest effect size after 72 hours of muscle soreness (Cohen s d = 2.149) (Figure 1). At baseline, there were no signicant differences in maximum isometric force between groups. The saffron group exhibited signicant increase in the isometric force after 24

(P , 0.05), 48 (P , 0.05), and 72 (P , 0.0001) hours (63.6%

increase) compared with baseline. The maximum isometric force between saffron and control groups showed signicant

differences after 24 (P , 0.05), 48 (P , 0.0001), and 72 hours

(P , 0.0001). Unlike saffron group, the control group showed

a signicant decrease in the isometric and isotonic forces. Comparison between saffron and indomethacin showed a sig- nicant difference only after 72 hours (P , 0.05), whereas the indomethacin and control groups comparison had a signicant difference after 48 and 72 hours (P , 0.05). The effect size between saffron and control groups after 24, 48, and 72 hours was 2.6, 2.9, and 2.6, respectively. The effect size between indomethacin and control groups after 24, 48, and 72 hours was 1.3, 0.28, and 0.29, respectively. The highest effect size belonged to the saffron group compared with control after 72 hours of muscle soreness (Cohens d = 2.9) (Figure 2). Plasma CK values were not signi cantly different between the groups at baseline. However, Figure 3 demon- strates that after 24 hours, CK concentration in the saffron and indomethacin groups decreased as compared with the control group. Plasma CK in the control group peaked at 48 hours after exercise (125.8%). Plasma CK level in the saffron group compared with baseline (100%) increased after 24 hours of exercise but it was not signi cant (3.7%) after 24 hours of exercise and then returned to a normal level. Plasma CK in saffron and control groups was signi cantly different after 24, 48, and 72 hours ( P , 0.0001). However, a difference between indomethacin and control groups was signi cant only after 48 and 72 hours (P , 0.0001). Saffron and

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FIGURE 1. Maximum isotonic force changes between the saffron ( ), indomethacin ( n), and control ( :) groups (mean 6 SD). *Indicates a significant difference ( P , 0.05) compared with the control group. †Indicates a significant difference ( P , 0.0001) compared with the control group.

difference ( P , 0.0001) compared with the control group. indomethacin groups exhibited a signi fi

indomethacin groups exhibited a signi cant difference only after 24 hours ( P , 0.005). The effect size between saffron and control groups after 24, 48, and 72 hours was 2.6, 2.9, and 2.6, respectively. The effect size between indometh- acin and control groups after 24, 48, and 72 hours was 1.3, 0.28, and 0.29, respectively. The maximum effect size has seen between saffron and control groups after 24 hours (Cohen s d = 3.397).

There was no signi cant difference between groups in the plasma LDH concentration at baseline. Plasma LDH concentrations presented in F igure 4 indicate that the saf- fron group exhibits a signi cant decrease after 24, 48, and 72 hours ( P , 0.0001). The indomethacin group has a sig- ni cant difference with control group after 48 and 72 hours ( P , 0.0001). The saffron and indomethacin compa- rison had a signi cant difference only after 24 hours

FIGURE 2. Comparison between maximum isometric force in the saffron ( ), indomethacin ( n ), and control ( :) groups (mean 6 SD). *Indicates a significant difference ( P , 0.05) compared with the con- trol group. †Indicates a significant difference ( P , 0.0001) compared with the control group.

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Preventive Effects of Saffron and Indomethacin on DOMS

FIGURE 3. Comparison between plasma CK concentration in the saf- fron ( ), indomethacin ( n), and control ( :) groups (mean 6 SD). *Indicates a significant difference ( P , 0.0001) compared with the control group.

difference ( P , 0.0001) compared with the control group. ( P , 0.0001). The effect

( P , 0.0001). The effect size bet ween saffron and control groups after 24, 48, and 72 hours was 2.6, 3.8, and 2.7, respectively. The effect size between indomethacin and control group after 24, 48, and 72 hours was 2.2, 0.61, and 0.63, respectively. Highest level of effect size was observed in the comparison between saffron and control groups after 48 hours (Chohen s d = 3.772).

Right leg pain perception had a signi cant difference between saffron and control groups after 24, 48, and 72 hours ( P , 0.0001) (Figure 5). Pain perception in the saffron group after 24 hours was 11.2 times lower than the control group, and all the subjects in the saffron group experiences no pain after 48 and 72 hours, whereas in the indomethacin group pain alleviated after 72 hours.

FIGURE 4. Comparison between plasma LDH concentration in the saffron ( ), indomethacin ( n), and control ( :) groups (mean 6 SD). *Indicates a significant difference ( P , 0.0001) compared with the control group.

difference ( P , 0.0001) compared with the control group. Copyright 2014 Wolters Kluwer Health, Inc.

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FIGURE 5. Comparison between Talag scale perceived pain (left) in the saffron ( ), indomethacin ( n ), and control ( :) groups (mean 6 SD). * Indicates a significant differ- ence ( P , 0.05) compared with the control group. †Indicates a signifi- cant difference ( P , 0.0001) com- pared with the control group.

( P , 0.0001) com- pared with the control group. The right thigh circumference did not

The right thigh circumference did not show any signif- icant differences at baseline. In the control group, the thigh circumferences after 24, 48, and 72 hours of eccentric exercise showed a signicant increase as compared with the pretest. Thigh circumference in the saffron group did not increase after eccentric exercise. There was no signicant difference between the indomethacin and control groups (Table). Control group exhibited a signi cant decrease in the right knee joint ROM 24, 48, and 72 hours after exercise compared with the pretest. The right knee joint ROM in saffron and control groups had no signi cant differences after 24, 48, and 72 hours. However, comparison between indomethacin and control groups showed a signi cant differ- ence after 24 hours ( P , 0.0001).

DISCUSSION

The present investigation demonstrated that saffron and indomethacin markedly prevented the laboratory and clinical

indices of exercise-induced DOMS in the nonactive young university students. The saffron was also more effective compared with indomethacin in the prevention of DOMS. The results of this study are encouraging because they serve to highlight the potential importance of saffron as a natural product in aiding the performance of athletes. The best indicator of muscle damage is the force loss. 14 In our experiment, the control group had a signi cant decrease in the maximum isometric and isotonic forces through the study. Noticeably, isometric force in the control group signi cantly decreased (19.6%), whereas saffron group experienced a signi cant increase after eccentric exercise (63.6%). However, there were nonsignicant changes of max- imum isometric force in the indomethacin group. This ten- dency might provide a clue that saffron has double positive effects on muscle, the preventive effect on DOMS, and mus- cle force enhancement. It has been proposed by Proske and Morgan 55 that mus- cle damage due to eccentric exercise leads to a release of Ca 2+

TABLE. Participants’ Range of Motion of the Knee and Thigh Circumference Measurements Between the 3 Groups During the Tests (Mean 6 SD)

Group

Before

24 Hours

48 Hours

72 Hours

Thigh circumference

Saffron

53.0 6 4.91

53.0 6 4.87

53.0 6 4.91

53.0 6 4.91

Indomethacin

54.1 6 4.70

54.7 6 4.72

54.0 6 4.70

54.0 6 4.70

Control

53.8 6 4.83

56.2 6 5.15*

57.1 6 4.81*

55.9 6 4.75

Knee ROM

Saffron

41.1 6 3.39

41.0 6 3.39

40.8 6 3.35

40.7 6 3.4

Indomethacin

35.2 6 2.5

36.1 6 2.51

35.2 6 2.52

35.2 6 2.5

Control

36.7 6 2.0

39.0 6 2.07*

41.0 6 2.18*

39.5 6 2.1*

*Signi cant difference , 0.001. Signi cant difference , 0.0001.

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Preventive Effects of Saffron and Indomethacin on DOMS

in the sarcoplasm. The increased Ca 2+ levels can trigger proteolysis and assist in the break down of the damaged mus- cle bers. Moreover, damage due to increased myoplasmatic Ca 2+ levels can lead to inammation, resulting in edema and muscle swelling. 55,56 The inammation is assumed to sensitize the nociceptors and leads to pain in the affected area. 57,58 Our previous report about the novel protective effect of saffron on the erythrocyte osmotic hemolysis (76.0%) 59 might support this notion that saffron might protect the muscle bers by enhancing the muscle cell membrane integrity. An increase in the maximum isometric force in the saffron group is a novel nding of this study. In a very recent and unpublished research, we found signi cant ergogenic effect of saffron after 10-day saffron supplementation. We postulated that this ergogenic effect of saffron might be related to (1) enhance muscle metabolism, (2) increased neuronal excitability, increased motor unit recruitment, (3) combination of these mechanism with or without anti- in amatory and antinociceptive effects of saffron. Antioxi- dant effects and the facilitation in tissue oxygenation properties of saffron components (eg crocin, crocetin, and safranal) were previously reported. 60 Increases in plasma CK and LDH levels are established indicators of in ammation and pathological consequences of DOMS. Saffron showed better prevention of CK and LDH elevation after eccentric exercise compared with indometha- cin. Anti-in ammatory and antioxidant effects of saffron are the most likely responsible. These effects may also be responsible for the perceived pain tolerance in this study. This study was limited to the inactive and healthy university male students, and similar research on the athletes is necessary to nd out the effectiveness of saffron on the athletes.

CONCLUSIONS

We conclude that 10-day supplementation with saffron has potent preventive effects on DOMS as compared with indomethacin and control groups. The ancient spice saffron has shown eminent preventive effect on DOMS as compared with indomethacin. Considering NSADs medicine side effects, saffron with its health-promoting properties will be preferred in the prevention of DOMS. Further research is necessary to unravel the mechanisms involved and dose- dependent effect of saffron on DOMS.

ACKNOWLEDGMENTS The authors are most grateful to the participants in this research study.

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