acute effects of ginger extract on biochemical and functional...

Original Articlehttp://mjiri.iums.ac.ir Medical Journal of the Islamic Republic of Iran (MJIRI)

Iran University of Medical Sciences

____________________________________________________________________________________________________________________1. (Corresponding author) MSc, Shiraz University, Shiraz, Iran. [email protected]. PhD, Faculty member, Shiraz University, Shiraz, Iran. [email protected]. PhD, Lab Medicine, Molavi Laboratory administrator, Shiraz, Iran. [email protected]. PhD student, Mazandaran University, Mazandaran, Iran. [email protected]

Acute effects of ginger extract on biochemical and functionalsymptoms of delayed onset muscle soreness

Khadijeh Hoseinzadeh*1, Farhad Daryanoosh2, Parvin Javad Baghdasar3

Hamid Alizadeh4

Received: 18 September 2014 Accepted: 5 June 2015 Published: 12 September 2015

AbstractBackground: Inflammation and pain induced by delayed onset muscle soreness (DOMS) as a re-

sult of eccentric exercise (EE) or unaccustomed activity cause some difficulties in exercise for ath-letes. The purpose of this study was to survey the effect of ginger extract on biochemical and func-tional symptom of delayed onset muscle soreness.

Methods: In a quasi-experimental study, 36 healthy female subjects, who were recruited by intradormitory calls, randomly divided into 3 groups, including: ginger intake 1 hour before exercise(GIBE), ginger intake immediately after exercise (GIAE) and placebo group (PL). Subjects con-sumed capsules contain 60 mg of ginger extract (equivalent of 2 g dried ginger powder) or placebobefore and after exercise. The exercise protocol consisted of a 20 minute step test using a 46cm stepat a rate of 15 steps per minute. The blood samples were taken before, 1, 24 and 48 hour after exer-cise to assay creatine kinase (CK) and interleukin-6 (IL-6). Muscle pain scores, isometric strengthand circumference of thigh muscle, and hip range of motion were recorded at mentioned times. Theanalysis of variance (ANOVA) with repeated measure was used to determine the differences betweengroups.

Results: The results showed a significant reduction of pain in GIBE compared to GIAE after 24 and48h of EE and GIAE compared to PL (p<0.05). IL-6 changed significantly in GIBE compared to PL(p<0.05) after 1, 24, and 48h after EE. The other factors didn’t change meaningfully.

Conclusion: The finding of this study suggests that 2 grams of ginger may have anti-inflammationand analgesic effect on DOMS.

Keywords: muscle soreness, exercise, Ginger, Interleukin-6, Creatine kinase (CK).

Cite this article as: Hoseinzadeh Kh, Daryanoosh F, Javad Baghdasar P, Alizadeh H. Acute effects of ginger extract on biochemical andfunctional symptoms of delayed onset muscle soreness. Med J Islam Repub Iran 2015 (12 September). Vol. 29:261.

IntroductionDelayed onset muscle soreness (DOMS)

is an unfavorable and unsightly feeling withpain and muscle stiffness consequence oftraining that can deter a beginner or even anathlete from continuing with the exercise. Itfrequently occurs as a result of strenuousunaccustomed physical activity chiefly ec-centric exercise in which force producingincrease s and lead to DOMS (1-6).

Five important signs of DOMS are acuteinflammation, pain, swelling, loss of func-

tion and range of motion (7,8) and increasein Thigh circumference (5). The mainmechanism of DOMS is not specified, butthere are some theories about it. Inflamma-tion theory is one of the most important ofthem (9). DOMS causes an increase in in-flammatory cytokines like IL-6, IL-8, andTNF-α, in the working muscle, plasma, andperhaps even the brain (10-13). Numeroustreatment strategies, both preventive andrehabilitative, have been suggested to helprelieve the severity of DOMS. Some of the

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http://mjiri.iums.ac.ir/article-1-3156-en.html

Temporal lobe epilepsy

2 Med J Islam Repub Iran 2015 (12 September). Vol. 29:261.http://mjiri.iums.ac.ir

presented treatments including herbal rem-edy (14-16) pharmacological treatmentsusing non-steroidal anti-inflammatorydrugs NSAIDs (17, 18) nutritional supple-ments (19-21) vibration (22,23), cryothera-py have been carried out (1, 24). However,little scientific evidence exists to supportthe full effectiveness of any of these thera-peutic interventions (12) .

One of the most used treatments is non-steroidal anti-inflammatory drugs(NSAIDs) such as ibuprofen, aspirin, keto-profen, naproxen, etc. (12,17,19). Thesedrugs control the generation of prostaglan-dins and provoke the neural terminals ofafferent neural fibers and ultimately thepain will be relieved (15, 18). But NSAID’suse is limited by the risk of adverse effects,particularly gastrointestinal and renal tox-icity (25).

Zingiber officinale, commonly known asginger, has been widely used in Ayurvedicand Chinese medicine for arthritis, rheuma-tism, sprains and muscular aches. It hasshown analgesic and anti-inflammatory ef-fects. Ginger inhibits the production ofimmune-system components called cyto-kines causing inflammation (26). Gingerolsand shogaols, which are constituents ofginger, have been shown to inhibit cy-clooxygenase (COX) 1 and 2. Ginger con-stituents inhibit arachadonic acid metabo-lism and thus prostaglandin synthesis. Oneconstituent specifically (6), Shogaol, (foundin semi-dry, but rarely fresh ginger), ap-pears to interfere with the arachadonic in-flammatory cascade (14,26). It is found toinhibit cyclooxygenases and prevents spe-cific prostaglandin release and hereby in-teracting with the vanilloid receptorTRPV1, which is known to play a role inprocessing nociceptive signals (27,28). Dai-ly consumption of raw and heat-treatedginger resulted in moderate-to-large reduc-tions in muscle pain following exercise-induced muscle injury in horses (14). Con-suming a 30-g dose of ginger has also beenshown to increases recovery of the fastphase of oxygen consumption after a max-imal exercise test and reduces cardiovascu-

lar recovery time but has no effect on in-flammatory factors (CK and IL-6 mRNA)(16). Ginger was as effective as mefenamicacid and ibuprofen in relieving pain inwomen with primary dysmenorrheal (29).

The purpose of current study was to de-termine if consumption of 2-g oral doses ofginger one hour before and immediatelyafter exercise would inhibit or decreasesigns of DOMS.

MethodsSubjectsForty untrained college students (women,

age between 21 and 24 year) volunteered toparticipate in the study. Risks and benefitswere explained to the subjects. Four ofthem were excluded from participation be-cause of the blood testing. The rest weregiven a written informed consent and healthquestionnaire. All participants werescreened for medical and orthopedic condi-tions that would preclude performance ofstrenuous step test. To control subject’s di-et, they were asked to feed from the dormi-tory dietary program, refrain from caffeinederivatives, medications and supplements,alcohol and didn’t train at least ten daysbefore and during testing days. Height andweight were taken for BMI assaying.

ProceduresA double-blind, randomized placebo-

controlled design was used for this study.Participants divided randomly into threegroups including: GIBE (Ginger IintakeBefore Eccentric exercise, n=12), GIAE(Ginger Intake After Eccentric exercise,n=12), and PL (placebo, n=12). Participantsmanaged to eat 60 mg ginger extract(equivalent 2 grams dried ginger) in theform of capsule. All subjects received aspecific code to show their groups and justthe physician of the project knew if it is aginger group or placebo. She revealed thecodes after the statistical analyze. Table 1shows time course of ginger using. Thesubjects were asked to keep their nosewhile eating capsule because the smellingof ginger didn’t make them to prejudge

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A.A. Asadi-Pooya, et al.

3Med J Islam Repub Iran 2015 (12 September). Vol. 29:261. http://mjiri.iums.ac.ir

about their feeling of pain when they reportit in the following steps of test.

Plant material and preparation of extractFresh rhizome of ginger (Zingiber offici-

nale Rosce) was purchased from a localmarket in India and authenticated by a bot-anist (Institute of Medicinal Plants, Jahad-e-Daneshgahi). The plant was dried in theshade. The dried rhizome was powderedmechanically and extracted by cold perco-lation with 95% ethanol for 24 hr. The ex-tract was recovered and 95% ethanol wasfurther added to the plant material and theextraction continued. The process was re-peated three times. The three extracts werepooled together and the combined extractwas concentrated under reduced pressure(22 – 26 mm Hg) at 45 – 60°C. Thirty gramof solvent-free extract was equivalent toone kilogram of the dried ginger (W/W)powder. The concentrate was weighed andcombined with the necessary excipients,and then filled into 500-mg capsules, eachcontaining 60 mg of the ginger extractequivalent 2 g ginger powder. The samecapsules were filled with lactose (70%),starch (20%) and talk (10%) as placebo.All of the above-mentioned procedureswere undertaken in the industrial pharmacydepartment of the Faculty of Pharmacy,Tehran University of Medical Sciences(TUMS).

Protocol designThe exercise consisted of a 20 minute

step test using a 46cm step at a rate of 15steps per minute. All subjects go up withright leg and go down with left leg and dothis with beep sounds of the metronome.Every 5 minutes they took a rest for 1 mi-nute in a standing position. This exerciseintensity has been demonstrated to stimu-late mild to moderate quadriceps muscle

pain(19,30).

Testing daysDuring the exercise, heart rate, respira-

tion, pulse and pain of subjects were con-trolled by a physician. None of the subjectspresented any problem. 5cc of blood wastaken from brachial vein before the test tomeasure plasma levels of creatine kinaseand interleukine-6. Then subjects con-sumed one capsule containing either 60 mgof ginger extract (equivalent 2 g dried gin-ger powder) or 2 g of lactose (placebo) with250 ml of water. The 2-g dose was chosenbecause 1- to 2-g doses have been shown toinduce central nervous system effects (15,32, 33). One hour later, subjects performedstep protocol in 25 minutes as describedbefore. Subjects ingested second capsulesimmediately after exercise. 1 hour after ex-ercise, 24 and 48 hour later blood sampleswere taken again.

MeasurementPain was measured using a self-reporting

visual analog scale (VAS) including a hori-zontal line, 100 mm in length, anchored byword descriptors at each end “no pain” and“severe pain” (2,31). Subjects were askedto perform one squat and then draw a lineon the scale corresponding to their level ofsoreness (9). Range of motion (ROM) ofhip was taken by a Jamar goniometer whilesubject was laying and the low back andsacrum was flat. Researcher placed the cen-ter of the goniometer on the greater tro-chanter of hip (32). The stationary arm wasparallel to the trunk and movable arm wasparallel to the femur. Subject flexed kneeand hip as she had felt no pain. Data wererecorded for an average of three times.Thigh muscle circumference was measuredusing a Gulick anthropometric tape (meas-ured 15 cm above the superior border of the

Table 1. Time course of ginger consumption.Group 1 hour before exercise Immediately after exerciseGIBE Ginger capsule PlaceboGIAE Placebo Ginger capsulePL Placebo Placebo

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patella). A mark was placed on each partic-ipant’s thigh for the next measurement(33). Subjects completed the assessments at1, 24 and 48 hour after the test again. Bloodsamples centrifuged at the test performanceplace to prevent changing in serum en-zymes. Human IL-6 kit (Canada, ID LabCompany) and creatine kinas kit CK-MMELISA Kit were used in the laboratory.

Statistical AnalysisANOVA was used for checking the dif-

ferences within groups in different timesand Repeated Measure and Bonferroni posthoc were used for checking the differencesbetween groups. Moreover, to compare theresults in different measurement betweengroups. The interaction effect of time andgroup was also measured. All statisticalanalysis were performed using SPSS 20.The significant level was considered atp≤0.05.

ResultsIn our quasi-experimental study, 36 sub-

jects were participated. IL-6, CPKthigh cir-cumference, hip range of motion and pain

rate of subjects were measured. The meanand standard deviation of participants areprovided in Table 2.

The descriptive indexes (Mean±SD) ofthigh circumference, hip range of motionand pain rate of subjects has been shown inTable 3.

The interaction effect of group and timewas just significant for thigh muscle pain.

According to Tables 3 and 4, the interac-tion effect of group and time is just signifi-cant for thigh muscle pain. Table 3 showsthat there is no significant difference be-tween groups in right thigh circumference.Nevertheless the result of ANOVA withrepeated measurements and Bonferroni posthoc for each group showed significant dif-ference between right thigh circumferencein pre-test and after 1h of EE with after 24hvalues in placebo group. About the leftthigh circumference values, there is no sig-nificant difference between groups. Withingroup analysis showed significant differ-ence between left thigh circumference inpre-test and after 1h of EE with 24h and48h after EE in GIBE. Within group analy-sis showed significant difference in range

Table 2. Characteristics of participants.Characteristic Mean ± SD Min. Max.Age (year) 22.0 ± 2.48 18 29Height (cm) 159.3 ± 5.67 147 171Weight (kg) 57.1 ± 8.00 41.6 74.6BMI (kg/m2) 22.5 ± 2.99 17.95 31.53

Table 3. Mean ± SD of thigh circumference, hip range of motion and pain.After 48hAfter 24hAfter 1hPre-testGroupVariable54.9±4.1554.7 ±4.5154.6±4.6254.5±4.52GIBERightthigh circumference57.7±5.0357.7±11.5357.5±5.0157.2±4.65GIAE54.7±3.6955±3.58*!54.9±3.4154.2±3.43PL

54.2±4.19*54.8±4.38*!54.2±4.4854.3±4.58GIBELeft thigh circumference57.4±4.7457.3±4.9556.8±4.6757±4.65GIAE54.2±3.3754.4±3.4753.7±3.1454.1±2.96PL97.7±10.398.5±8.44*101.7±9.64108±8.77GIBERight Hip Range Of Motion98.6±9.3497±11.78101.5±7.01*105.7±7.09GIAE

97.3±11.5299.3±11.91100.3±10.81105.8±6.81PL93±11.0893.5±7.44*101.1±11.58106.3±10.49GIBELeft Hip Range Of Motion

98.8±14.4691.3±19.65!108.8±12.02105.7±8.41GIAE93±11.19*93.6±8.05*99.7±7.53*110.9±9.73PL

53.7±9.32‡*57.9±10.76‡*!7.9±6.56*0GIBEThigh muscle pain33.3±9.85‡Ḡ*!40.0±11.28‡Ḡ*!3.0±3.06*0GIAE58.75±8.82*!65.0±14.30*!6.8±5.81*0PL

* (p≤0.05), (mean±SD)‡ Significant difference between GIBE and GIAEḟḟSignificant difference between GIAE and PL* Significant difference in comparison with pre-test! Significant difference in comparison with previous phase of measurement

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of motion (ROM) of right and left hip inpre-test and after 24h of EE in GIBE. Therewere significant differences in right hipROM in 1h after EE in GIAE and in 24h inGIBE in both right and left hip ROM com-pared to pre-test values. In PL, there wassignificant difference in left hip ROM inpre-test values compared to 1, 24 and 48hafter EE.

According to table 3, there is significantdifference between GIBE and PL with GI-AE in pain after 24 and 48h of EE. The re-sults of repeated measurements show thatin all of the groups, rate of the pain in-creased significantly after 1, 24 and 48h ofEE in comparison with pre-test. In all of the

three groups, in comparison with 1h afterEE, rate of the pain at 24h after EE, hadsignificant difference. Also, in GIAE andPL, rate of the pain at 48h after EE had sig-nificant difference compared with 24h, butnot in GIBE.

According to analysis of variances out-puts (ANOVA) it has been shown that thereis significant difference between GIBE andGIAE (p≤0. 001) and also between GIBEand PL (p=0.01) at 1h after EE (Fig. 1).This difference is significant at 24h afterEE (between GIBE and GIAE, p=0.001)and 48h after EE (between GIBE and GI-AE, p=0.001 and GIBE and PL, p=0.05).The result of ANOVA with repeated meas-

Table 4. The interaction effect of group and time on indexes of the study * (P≤0.05)pF+FactorVariable

0.3491.048Group × TimeIL-60.2631.325Group × TimeCPK

*0.000112.481Group × TimeThigh muscle pain0.3020.221Group × TimeRight thigh circumference0.2801.267Group × TimeLeft thigh circumference0.9330.252Group × TimeRight Hip Range of Motion0.1801.597Group × TimeLeft Hip Range of Motion0.7870.433Group × TimeIsometric strength of thigh

Fig. 1. The changes of IL-6

‡ Significant difference between GIBE and GIAE† Significant difference between GIBE and PLḟḟ Significant difference between GIAE and PL* Significant difference in comparison with pre-test! Significant difference in comparison with previous phase of measurement

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urements for each group didn’t show anysignificant difference between the phases ofmeasurement within groups.

As it is shown in Figure 2, there is nosignificant difference between groups inCPK levels (p>0.05). But ANOVA with

repeated measurements for within groupshowed significant difference in changes ofCPK in pre-test than to 24 and 48 h afterexercise in GIAE and PL (p≤0.05). In PL,there is significant difference in the chang-es of CPK at 1 and 24 h after EE. There is

Fig. 2. The changes of CPK‡ Significant difference between GIBE and GIAE

† Significant difference between GIBE and PLḟḟ Significant difference between GIAE and PL* Significant difference in comparison with pre-test! Significant difference in comparison with previous phase of measurement

Fig. 3. The isometric strength of thigh

‡ Significant difference between GIBE and GIAE† Significant difference between GIBE and PLḟḟ Significant difference between GIAE and PL* Significant difference in comparison with pre-test! Significant difference in comparison with previous phase of measurement

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no significant difference in all of the phasesof measurement in GIBE (p>0.05). As it isshown in Figure 3, there isn’t significantdifference in isometric strength of thighbetween and within groups after EE in noneof the phases of measurement.

DiscussionThe purpose of the current study was to

examine the acute effect of oral consump-tion of 2-g dose of ginger extract on somebiochemical and functional factors of de-layed onset muscle soreness after one ses-sion step test as an eccentric exercise. Rightand left thigh muscle circumference, ROMof right and left hip, isometric strength ofthigh and CPK after step test did not differbetween ginger and placebo conditions butthe ratio of pain and IL-6 were significantlydifferent between groups. Ginger exhibitedhypoalgesic effect on quadriceps pain in-tensity in GIBE and GIAE compared withPL.

The finding that ginger reduced musclepain as a result of delayed onset musclesoreness caused by eccentric exercise isconsisted with previous studies demonstrat-ing that 2-g use of raw or heated ginger canreduce arm pain in human after eccentricelbow action (14). One study showed thatadministration of 1500 mg ginger powderdaily for three days produce analgesia instudents with primary dysmenorrheal (34).Ginger act as a pain relief in patients withosteoarthritis of the knee (35) and havemore effect than ibuprofen (25). But ingest-ing 2-grams of ginger doesn’t have any ef-fect on quadriceps muscle pain during andafter moderate-intensity cycling exercise(15) and this may be because of the severityof the protocol was used. 6-Shogaol is oneof the major biologically active compoundsfound in the rhizome of Zingiber officinale/ginger that have analgesic effects (26). Toexplain the effects of ginger on pain relief,it has been reported that ginger inhibits cy-clooxygenase and lipooxygenase pathwaysin prostaglandin and leukotriene synthesisand the anti-inflammatory property of gin-ger has been attributed to inhibition of

prostaglandin synthesis (26, 36). Inflamma-tory response ends up in autacoid leukotri-ene synthesis. PGE2 directly causes pain bysensitizing types III and IV pain receptors.In the current study, perception of pain inGIBE was less than GIAE and PL and thismay be due to the inhibitory effect of gin-ger on prostaglandin’s release. It seems thatconsumption of ginger before exercisecould cease the cascade of inflammatoryfactors and thereby caused a lesser pain re-port. Ginger also showed an inhibitory ef-fect on IL-6 in GIBE compared with GIAEand PL; but within groups therewas no dif-ference. According to the results of some invitro studies, rhizome of ginger and itsmain components, gingerols and shogaols,can inhibit synthesis ofpro-inflammatorycytokines including IL-1, TNF-α and IL-8along with inhibiting prostaglandin andleukotriene synthesis enzymes (37). Thesystemic response to inflammation rapidlybecomes anti-inflammatory as plasma lev-els of IL-6, IL-10, IL-1ra and soluble TNF-α receptors rise in direct proportion to theintensity and duration of exercise (38, 39).The release of the pro-inflammatory cyto-kines into the circulation is inhibited by IL-6, which stimulates the production of theanti-inflammatory cytokines (40). Niemanet al. (2005) tested the relationship betweenplasma CPK, DOMS and various plasmacytokines. These researchers found thatmuscle damage, post-race DOMS and IL-6,IL-10 were positively correlated. The in-crease in the cytokines was greatest for IL-6 (125-fold), corresponding with a 112-foldincrease in CPK (13). In our study increasein IL-6 in GIBE in comparison with theother groups was less and this may be relat-ed to the anti-inflammatory effect of gin-ger. It seems that one hour, was enough forginger to affect on cytokine’s release. Aftermuscular damaged, the sarcolema disrup-tion allows muscle proteins such as CK tobe released from the fiber into the bloodstream (41, 42). The increased level ofCPK confirmed occurrence of DOMS. Af-ter eccentric exercise, CPK changed signif-icantly in GIAE and PL but not in GIBE

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that was similar to previous studies (43-45).The main symptoms of DOMS are pain,decrease in range of motion, decrease inmuscle strength and swelling (13,15).Swelling is often associated with acute in-flammation. Many studies using humans toinvestigate an association between DOMSand swelling. Loss of function and strengthis associated with loss of force generatingcapacity (12) . Our findings of increasedthigh muscle volume and decreases hipROM and isometric strength, clearlyshowed that the exercise protocol resultedin muscle damage, but ginger couldn’tameliorate these symptoms. Ginger andDHA (docosahexaenoic acid) (15, 46), andvitamin C (45) didn’t change arm volumeand elbow ROM after EE. The increase inisometric strength of thigh 1 hour after ex-ercise may be due to better use of dyna-mometer. Similar to Drager et al. study, thedecrease in ROM was associated with de-crease in isometric strength and this sug-gests that muscular tightness can impairmaximum isometric force production (46).Although the changes in these variablesweren’t statistically significance, but itshowed that ginger had a positive effect onGBE in comparison with GIAE and PL. Insummery the results of the present studysuggest that ginger extract could reducepain and inflammation caused by eccentricexerciseIt could be used as an effectiveherbal in healing DOMS.

AcknowledgementsWe would like to thank the students of

Shiraz University for their cooperation inthis work that wasa part of a Master of Sci-ence dissertation.

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