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Review Article
A Systematic Review on the Effects of Botanicals on Skeletal
Muscle Health in Order to Prevent Sarcopenia
M. Rondanelli,1A. Miccono,2G. Peroni,1F. Guerriero,3P. Morazzoni,4A. Riva,4
D. Guido,1,5,6 and S. Perna1
1Department of Public Health, Experimental and Forensic Medicine, Section of Human Nutrition, Endocrinology and Nutrition Unit,
Azienda di Servizi alla Persona, University of Pavia, 27100 Pavia, Italy
2Department of Clinical Sciences, Faculty of Medicine and Surgery, University of Milan, Milan, Italy
3Azienda di Servizi alla Persona, Pavia, Italy
4Research and Development Unit, Indena, 20139 Milan, Italy
5Department of Brain and Behavioral Sciences, Medical and Genomic Statistics Unit, University of Pavia, 27100 Pavia, Italy
6Department of Public Health, Experimental and Forensic Medicine, Biostatistics and Clinical Epidemiology Unit,
UniversityofPavia,27100Pavia,Italy
Correspondence should be addressed to S. Perna; simoneperna@hotmail.it
Received November ; Revised January ; Accepted January
Academic Editor: Hyunsu Bae
Copyright © M. Rondanelli et al. is is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
We performed a systematic review to evaluate the evidence-based medicine regarding the main botanical extracts and their
nutraceutical compounds correlated to skeletal muscle health in order to identify novel strategies that eectively attenuate skeletal
muscle loss and enhance muscle function and to improve the quality of life of older subjects. is review contains all eligible studies
from to and included publications. We focused our attention on eects of botanical extracts on growth and health of
muscle and divided these eects into ve categories: anti-inammation, muscle damage prevention, antifatigue, muscle atrophy
prevention, and muscle regeneration and dierentiation.
1. Introduction
Sarcopenia is the loss of muscle protein mass and of muscle
function and it occurs with increasing age, being a major
component in the development of frailty []. It is a syndrome
characterized by the progressive and generalized loss of skele-
tal muscle mass and strength with a risk of adverse outcomes
such as physical disability, poor quality of life, and death
[]. Preventative diet, exercise, or treatment interventions
particularly in middle-aged adults at the low end of the
spectrum of muscle function may help to preserve mobility
in later years and improve health span []. e therapeutic
options for sarcopenia are unclear and constantly evolving.
e most rational approach to delay the progression of
sarcopeniaisbasedonthecombinationofpropernutrition,
possibly associated with the use of dietary supplements, and
a regular exercise program []. Despite the major advantages
oered by natural therapies with their long traditional use and
poor physiological and psychological addiction as is com-
monly seen with conventional medicine [], few studies have
been performed on the topic of age-correlated pathologies of
skeletal muscle. e aim of this review was to investigate the
eectiveness of botanicals on skeletal muscle health focusing
on possible therapeutics approaches to prevent sarcopenia.
2. Materials and Methods
e present systematic review was performed according
to the steps by Egger et al. [] (Table ), as follows: (i)
conguration of a working group: three operators skilled
in clinical nutrition in the geriatric age, of whom one
was acting as a methodological operator and two were
participating as clinical operators; (ii) formulation of the
revision question on the basis of considerations made in
Hindawi Publishing Corporation
Evidence-Based Complementary and Alternative Medicine
Volume 2016, Article ID 5970367, 23 pages
http://dx.doi.org/10.1155/2016/5970367
Evidence-Based Complementary and Alternative Medicine
T : Summary of methodology.
Step General activities Specic activities
Step 1Conguration of a
working group
Selection of three operators skilled in clinical nutrition:
(i) One as methodological operator
(ii) Two as clinical operators
Step 2Formulation of the
revision question
Evaluation of the state of the art in metabolic and nutritional disorders of sarcopenia and their treatment
with botanicals
Step 3Identication of
relevant studies on
PubMed
(a) Identication of the key words (sarcopenia, nutrients, and dietary supplement), allowing the denition
of the interest eld of the documents to be searched, grouped in inverted commas (“...”), and used
separately or in combination
(b) Use of the Boolean (a data type with only two possible values: true and false) AND operator, which
allows the establishment of logical relations among concepts
(c) Research modalities: advanced search
(d) Limits: papers published in the last years; in vitro, animal, and humans studies; languages: English
(e) Manual search performed by the senior researchers experienced in clinical nutrition through the
revision of reviews and individual articles on sarcopenia in the elderly, published in journals qualied in
the Index Medicus
Step 4Analysis and
presentation of the
outcomes
e data extrapolated from the revised studies was investigated in the form of a narrative review of the
reports and was collocated in tables
the abstract: “sarcopenia and muscle mass, use of botanic
extracts during aging”; (iii) identication of relevant studies:
a research strategy was planned, on PubMed and Scopus, as
follows: (a) denition of the key words (sarcopenia, muscle
mass, inammation, antioxidants, botanical extracts, phy-
totherapy, muscle atrophy, muscle fatigue, Camellia sinensis,
Vitis v inifera,Zingiber ocinale,Citrus aurantium,andPanax
quinquefolius), allowing the denition of the interest eld of
the documents to be searched, grouped in inverted commas
(“...”), and used separately or in combination; (b) use of the
Boolean AND operator, which allows the establishment of
logical relationships among concepts; (c) research modalities:
advanced search; (d) limits: papers published until June
; humans, animals, in vivo, and in vitro studies; lan-
guages: English; (e) manual search performed by the senior
researchers, experienced in clinical nutrition, through the
revision of reviews and research articles on sarcopenia in the
elderly, published in qualied journals of the Index Medicus.
Analysisandpresentationoftheoutcomeshadbeendone
as follows: the data extrapolated from the revised studies were
summarized in Tables –; in particular, for each study, we
specied the author and year of publication, the plant and
theactiveprinciples,themodelsused,theposology,andthe
main results obtained. e analyses were carried out in the
form of a narrative review of the reports. e ow diagram
of narrative review of the literature has been reported in
Figure . As shown in Figure , we consider several eects
of botanical extracts on growth and health of muscle; we
divided these eects into ve categories: anti-inammatory
activity, muscle damage prevention, antifatigue, muscle atro-
phy prevention, and muscle regeneration and dierentiation.
Aer this, we examined the typology of the studies, that is,
in vitro, animals (mice, rats), or human, and we classied
the human data according to the dierent condition such
as postmenopausal women, athletes or others. Another key
point was to identify the dosage of the extracts for each trial
and the botanical compounds responsible for the activity.
e use of the databases as PubMed or Scopus was deter-
minant to enrich our review. At the end, we reported an
analysis of all plants and their extracts that have a benecial
role in preventing sarcopenia or improve muscle health
condition.
3. Results
3.1. Screening and Selection Process of Study. Of arti-
cles identied, studies met inclusion criteria (Figure ),
including focused on anti-inammation, focused on
muscle damage, based on antifatigue eects, based on
muscle athorpy, and based on muscle dierentiation and
regeneration (Figure ).
As reported in Table , there are dierent eects on
skeletal muscle for each botanical. At present, we eval-
uated in the literature over dierent mechanisms of
action.
3.2. Anti-Inammatory Activity. is research has been car-
ried out based on the keywords “skeletal muscle mass” and
“inammation” and “botanicals” or “plants” or “extracts”;
articles were sourced and studies are taken into account.
Among these papers, studies are in in vitro setting, in
animals, in humans, and two both in animals and in in vitro
setting (Table ).
Inammation and oxidative stress induce muscle damage
and muscle pain [] and several botanicals (Phlebodium
decamanum,Citrus aurantium,Coea arabica,Zingiber oc-
inale,Eugenia punicifolia,Panax ginseng,Go-sha-jinki-Gan,
Vitis v inifera,andCurcuma longa L.) have a signicant role in
the prevention of this phenomenon.
Evidence-Based Complementary and Alternative Medicine
Identication
Screening
Eligibility
Included
Records identied through databases
(Scopus, PubMed, and Google Scholar)
searching, n = 120
Record excluded, n = 34
Reasons
(i) Not pertinent, n = 20
(ii) Other manuscript type, n = 8
(iii) Duplicates, n = 6
Records screening
N = 86
Full text articles assessed for eligibility total, n = 86
(i) Muscle damage and anti-inammation, n = 21
(ii) Muscle damage, n = 11
(iii) Antifatigue, n = 20
(iv) Muscle atrophy, n = 15
(v) Dierentiation and regeneration, n = 19
Studies included in narrative review, n = 57
(iii) Antifatigue, n = 11
(iv) Muscle atrophy, n = 7
(v) Dierentiation and regeneration, n = 15
One article is in both categories.
∗
(i) Antin-ammation, n = 17∗
(ii) Muscle damage, n = 8∗
F : Flow diagram of narrative review of the literature.
Supplementation with Phlebodium decamanum ( cap-
sules of mg) reduces inammatory response and also
the degree of oxidative stress in human during high-
intensity exercise, through the decrease of -hydroxy--
deoxyguanosine and isoprostanes generation, the increase
of antioxidant enzyme activities in erythrocyte and total
antioxidant status in plasma, the decrease of tumor necrosis
factor (TNF-𝛼), and the increase of soluble receptor II of
TNF-𝛼(sTNF-RII), but kept the levels of interleukin- (IL-
) and interleukin- antagonist receptor (IL-ra) []. Other
studies examine the anti-inammatory eect of avonoids
isolated from Citrus aurantium,Coea arabica,andZingiber
ocinale on interleukins such as IL-𝛼and IL- and TNF-
𝛼on skeletal muscle cells. Specically, the avonoids (hes-
peridin, nobiletin, and naringin of Citrus aurantium,also
known as sour orange) inhibit the inammatory response
in lipopolysaccharide- (LPS-) induced L skeletal muscle
cells. In addition, the avonoids isolated from Korean Cit-
rus aurantium L. inhibit signicantly inducible nitric oxide
synthase (iNOS), cyclooxygenase- (COX-), IL-, and TNF-
𝛼by blocking the nuclear factor-kappa B (NF-𝜅b) and by
blocking mitogen-activated protein kinases (MAPKs) signal
pathways. Another study in the same muscle cells demon-
strates the anti-inammatory role of avonoids isolated from
Citrus aurantium through the modulation in protein related
to the immune response. Furthermore, the pretreatment with
avonoidsresultedinadecreasedlevelofcleavedcaspase-
, which is induced by muscle inammation and is involved
in muscle proteolysis and atrophy. Also, Zingiber oci-
nale, commonly known as ginger, showed interesting anti-
inammatory and analgesic eects in humans who ingested
grams of ginger or placebo aer exercise; however, this extract
Evidence-Based Complementary and Alternative Medicine
T : Eects on skeletal muscle for each botanical.
Eect Botanicals Physiology Study Authors
Downregulation of LPS-induced COX- and
iNOS expression Korean Citrus aurantium L. , , , and 𝜇g/mL Rat skeletal muscle cells Kim et al., []
Suppression or inhibition of NF-𝜅B
Korean Citrus aurantium L. , , , and 𝜇g/mL Rat skeletal muscle cells Kim et al., []
Eugenia punicifolia mg/mL Male mdx dystrophic mice Leite et al., []
Camellia sinensis .% or .% green tea extract, at
the age of days CBL/J and mdx mice Evans et al., []
Increase of NF-𝜅BPanax ginseng DS , , and mg/kg Rats Yu et al., []
Induction of the phosporylation of AMPK Glycine max 𝜇MCCmyotubes
Hirasaka et al.,
[]
Decrease of MURF- promoter activity Glycine max 𝜇MCCmyotubes
Hirasaka et al.,
[]
Suppression of LPS-induced phosphorylation of
the MAPKs (JNK, ERK, and p MAPK pERK)
Korean Citrus aurantium L. , , , and 𝜇g/mL Rat skeletal muscle cells Kim et al., []
Eugenia punicifolia 𝜇g/mL Mouse myoblastoma cells (CC) Leite et al., []
Increase of ERK/ ac tivity Hachimijiogan (HJG) HJG treatment (– 𝜇g/mL) Murine skeletal cells Takeda et al., []
Activation of p MAPK signaling Broussonetia kazinoki (pp) KP in % HS for h, – nM CC and T/ cells Hwang et al., []
Corydalis turtschaninovii (p-p) Various concentrations of THP CC myoblasts and broblast
T/ Lee et al., []
Increase of myogenin Eugenia punicifolia (.-kDa) mg/mL Male mdx dystrophic mice Leite et al., []
Increased expression of MHC, myogenin, and
Troponin-T
Broussonetia kazinoki KP in % HS for h, – nM CC and T/ cells Hwang et al., []
Corydalis turtschaninovii Various concentrations of THP CC myoblasts and broblast
T/ Lee et al., []
DecreaseoftheexpressionofTNF-𝛼
Korean Citrus aurantium L. , , , and 𝜇g/mL Rat skeletal muscle cells Kim et al., []
Vitis v inifera 𝜇M Mouse CC cells Wang et al., []
Panax notoginseng mgofRg Healthyyoungmen(𝑁=26)Houetal.,[]
Phlebodium decumanum
capsules of mg ( mg of leaf
extract and mg of rhizome
extract)
Amateurathletes(𝑁=40)D´
ıaz-Castro et al.,
[]
Eugenia punicifolia mg/mL Male mdx dystrophic mice Leite et al., []
Coee e same amount of drink in
control and coee group for weeks CBL/ mice Guo et al., []
Camellia sinensis .% w/w in diet for weeks aer
downhill running Mice Haramizu et al.,
[]
Rubus parvifolius L. (RPL) mg/kg and mg/kg Five-week-old male Chen et al., []
Glycine max 𝜇MCCmyotubes
Hirasaka et al.,
[]
Evidence-Based Complementary and Alternative Medicine
T : C o n t i n u e d.
Eect Botanicals Physiology Study Authors
Increase in sTNF-RII Phlebodium decumanum
capsules of mg ( mg of leaf
extract and mg of rhizome
extract)
Amateurathletes(𝑁=40)D´
ıaz-Castro et al.,
[]
Decrease of IL-𝛼Coee e same amount of drink in
control and coee group for weeks CBL/ mice Guo et al., []
Decrease of IL-
Korean Citrus aurantium L. , , , and 𝜇g/mL Rat skeletal muscle cells Kim et al., []
Curcumin (at h) . g twice daily Men (𝑁=17)Nicoletal.,[]
Coee e same amount of drink in
control and coee group for weeks CBL/ mice Guo et al., []
Rubus parvifolius L. (RPL) mg/kg and mg/kg Five-week-old male Chen et al., []
Increase of interleukin- (IL-) Curcumin (at h and h) . g twice daily Men (𝑁=17)Nicoletal.,[]
Decrease of IL- Curcumin g twice daily (corresponding to
mg curcumin twice a day)
Healthy, moderately active male
(𝑁=20)
Drobnic et al.,
[]
Decrease of IL-𝛽Eugenia punicifolia (.-kDa) mg/mL Male mdx dystrophic mice Leite et al., []
Panax ginseng DS Rats Yu et al., []
Camellia sinensis .% w/w in diet for weeks aer
downhill running Mice Haramizu et al.,
[]
Increase of IL- Panax notoginseng mgofRg Healthyyoungmen(𝑁=26)Houetal.,[]
Panax ginseng DS , , and mg/kg Rats Yu et al., []
Decrease of MCP- Camellia sinensis .% w/w in diet for weeks aer
downhill running Mice Haramizu et al.,
[]
Decreased MnSOD (only at high dose) Panax ginseng DS , , and mg/kg Rats Yu et al., []
Decreaseoftheexpressionofcleavedcaspase- Korean Citrus aurantium L. 𝜇g Rat skeletal muscle cells Kim et al., []
Eugenia punicifolia mg/mL Male mdx dystrophic mice Leite et al., []
Increased expression of antioxidant enzymes,
such as GPx (not at high dose) and GCS
Panax ginseng DS , , and mg/kg Rats Yu et al., []
Phlebodium decumanum (only GPx)
capsules of mg ( mg of leaf
extract and mg of rhizome
extract)
Amateurathletes(𝑁=40)D´
ıaz-Castro et al.,
[]
Increase of MMP- and MMP- Eugenia punicifolia 𝜇g/mL Mouse myoblastoma cells (CC) Leite et al., []
Reduced MMP- Eugenia punicifolia mg/mL CBL/ mice Leite et al., []
Reduced MMP- and MMP- Eugenia punicifolia mg/mL Male mdx dystrophic mice Leite et al., []
Increase of citrate synthase (CS) activity Panax notoginseng mgofRg Healthyyoungmen(𝑁=26)Houetal.,[]
Evidence-Based Complementary and Alternative Medicine
T : C o n t i n u e d.
Eect Botanicals Physiology Study Authors
Attenuation of the increases in mRNAs encoding
LyGandCDobservedathaerdownhill
running
Camellia sinensis .% w/w in diet for weeks aer
downhill running Mice Haramizu et al.,
[]
Increase of p and pAkt Eugenia punicifolia 𝜇g/mL Mouse myoblastoma cells (CC) Leite et al., []
Corydalis turtschaninovii (only
pAkt) Various concentrations of THP CC myoblasts and broblast
T/ Lee et al., []
ReductionofCyclinD Eugenia punicifolia 𝜇g/mL Mouse myoblastoma cells (CC) Leite et al., []
Increased expression of pAkt and pFoxOa Camellia sinensis – 𝜇M CCmyotubes Mirzaetal.,[]
Decrease in MPO activity Camellia sinensis .% w/w in diet for weeks aer
downhill running Mice Haramizu et al.,
[]
Decreased caspase- expression Vitis vinifera . mg per gram body mass per day Mice (male CBL/J mice) Ballak et al., []
Upregulation of phosphorylation of Akt, pSK,
mTO R , a nd E-B P
Vitis v inifera 𝜇M Mouse CC cells Wang et al., []
Coee Coee solution , , , and
𝜇g/mL Mousemyosatellitecells Guoetal.,[]
Prevention of HSPB phosphorylation Pinus pinaster . mg/mL Human muscle satellite cells Poussard et al.,
[]
Decrease in FoxO protein and promotion of
FoxO phosphorylation Vitis v inifera 𝜇M Mouse CC cells Wang et al., []
Decreased MURF- and MAFbx Camellia sinensis – 𝜇M CCmyotubes Mirzaetal.,[]
Increased MURF- Go-sha-jinki-Gan (GJG) (only
PGC-𝛼)% (w/w) Male SAMP, SAMR mice Kishida et al.,
[]
Increase of the expression of MAFbx/atrogin Chestnuts our Polyphenols ( nM) or
tocopherols ( nM) CC myotube cells Frati et al., []
Decreased expression of proteasomes S and S Camellia sinensis – 𝜇M CCmyotubes Mirzaetal.,[]
Decreased peak CK serum or activity
Curcumin mg before and h aer each
eccentric exercise Untrained young men Tan ab e e t a l. ,
[]
Curcumin . g twice daily Men (𝑁=17)Nicoletal.,[]
Curcumin mg/kg/day Male Wistar rats Boz et al., []
Decrease plasma-serum ammonia levels
Pumpkin (Cucurbita moschata)fruit , , , and mg/kg/day for
days MaleICRmice Wangetal.,[]
Angelica sinensis . g/kg/day (Ex-AS) and
. g/kg/day (Ex-AS), weeks Male ICR strain mice Yeh et al., []
Rubus parvifolius L. (RPL) mg/kg and mg/kg Five-week-old male Chen et al., []
Increase in blood creatine kinase Zingiber ocinale Roscoe g of ginger once a day for days non-weight trained participants Matsumura et al.,
[]
Eriobotrya japonica mg/kg/day Young (-month-old) and aged
(--month-old) rats Sung et al., []
Evidence-Based Complementary and Alternative Medicine
T : C o n t i n u e d.
Eect Botanicals Physiology Study Authors
Increase in serum creatinine Ashwagandha (Withania somnifera)
(WS)
mg/day × days; mg/day
× days; mg/day × days
Eighteen apparently healthy
volunteers Raut et al., []
Decrease of serum creatine kinase activity
Pumpkin (Cucurbita moschata)fruit , , , and mg/kg/day for
days MaleICRmice Wangetal.,[]
Salvia ocinalis , , and mg/kg BW rats JiPing, []
Angelica sinensis . g/kg/day (Ex-AS) and
. g/kg/day (Ex-AS), weeks Male ICR strain mice Yeh et al., []
Camellia sinensis .% or .% green tea extract at
the age of days CBL/J and mdx mice Evans et al., []
Withania somnifera mg of the whole root extract
twice daily; mg twice daily individuals Mishra and Trikamji,
[]
Decrease in plasma lactate or lactic acid
Korean mistletoe (Visc um a lb um
subsp. coloratum)
KME at or mg/(kg⋅d) for
week and , , , and
mg/kg
ICR mice Jung et al., []
Aegle marmelos (L.) Corr. , , and mg/kg BW for d BALB/c mice Nallamuthu et al.,
[]
Pumpkin (Cucurbita moschata)fruit , , , and mg/kg/day for
days MaleICRmice Wangetal.,[]
Tao-Hong-Si-Wu-Tang (THSWT) , , and mL/ kg body weight for
days male mice Li et al., []
Rubus parvifolius L. (RPL) mg/kg and mg/kg Five-week-old male Chen et al., []
Angelica sinensis . g/kg/day (Ex-AS) and
. g/kg/day (Ex-AS), weeks Male ICR strain mice Yeh et al., []
Increase in LDH and lactic acid
Panax ginseng mg/kg Rat Tan et a l., []
Acanthopanax senticosus (LDH)
mg/kg and mg/kg;
mg/kg or mg/kg; mg/kg or
mg/kg
Five-week-old male ICR mice Huang et al., []
Rubus parvifolius L. (RPL) mg/kg and mg/kg Five-week-old male Chen et al., []
Decreased myoglobin levels Curcumin mg/kg/day Male Wistar rats Boz et al., []
Decreased MDA levels in liver tissue
Curcumin mg/kg/day Male Wistar rats Boz et al., []
Aegle marmelos (L.) Corr. , , and mg/kg BW for
days BALB/c mice Nallamuthu et al.,
[]
Curcuma longa – 𝜇gkg
−1 of curcumin Wistar rats (𝑛 = 130)Vitadelloetal.,
[]
Increased MDA Panax ginseng mg/kg Rat Tan et al., []
Increased availability of serum free fatty acid Aegle marmelos (L.) Corr. mg/kg BW for days BALB/c mice Nallamuthu et al.,
[]
Evidence-Based Complementary and Alternative Medicine
T : C o n t i n u e d.
Eect Botanicals Physiology Study Authors
Decreased level of TG
Acanthopanax senticosus
mg/kg and mg/kg;
mg/kg or mg/kg; mg/kg or
mg/kg
Five-week-old male ICR mice Huang et al., []
Rubus parvifolius L. (RPL) mg/kg and mg/kg Five-week-old male Chen et al., []
Ashwagandha (Withania somnifera)
(WS)
mg/day × days; mg/day
× days; mg/day × days
Eighteen apparently healthy
volunteers Raut et al., []
Decrease in glucose and insulin Panax notoginseng mgofRg Healthyyoungmen(𝑁=26) Hou et al., []
Increase in blood glucose Pumpkin (Cucurbita moschata)fruit , , , and mg/kg/day for
days MaleICRmice Wangetal.,[]
Angelica sinensis . g/kg/day (Ex-AS) and
. g/kg/day (Ex-AS), weeks Male ICR strain mice Yeh et al., []
Increase in citrate synthase (CS) activity Panax notoginseng mgofRg Healthyyoungmen(𝑁=26)Houetal.,[]
Rate of glycogen accumulation Panax notoginseng mgofRg Healthyyoungmen(𝑁=26)Houetal.,[]
Increase in glycogen content of liver and muscle
Aegle marmelos (L.) Corr. , , and mg/kg BW for d BALB/c mice Nallamuthu et al.,
[]
Pumpkin (Cucurbita moschata)fruit , , , and mg/kg/day for
days MaleICRmice Wangetal.,[]
Panax ginseng mg/kg Rat Tan et a l., []
Tao-Hong-Si-Wu-Tang (THSWT) , , and mL/kg b ody weight for
days male mice Li et al., []
Angelica sinensis . g/kg/day (Ex-AS) and
. g/kg/day (Ex-AS), weeks Male ICR strain mice Yeh et al., []
Rubus parvifolius L. (RPL) mg/kg and mg/kg Five-week-old male Chen et al., []
Increase in cholinesterase (ChE) Salvia ocinalis , , and mg/kg BW rats JiPing, []
Upregulation of HSP mRNA levels or induction
of the expression of Hsp-
Rhodiola rosea 𝜇g/mL of Rhodiolife Murine skeletal muscle cells Hern´
andez-Santana
et al., []
Cichorium intybus (Cii) , , , and 𝜇g/mL CC myoblast Lee et al., []
Downregulation of Hsp- Aegle marmelos (L.) Corr. , , and mg/kg BW for
days BALB/c mice Nallamuthu et al.,
[]
Prevention of calpain upregulation Pinus pinaster Oligopin (. mg/mL) Cultured human skeletal muscle
satellite cells
Dargelos et al.,
[]
Inhibition of the level of ceramide Cichorium intybus (Cii) , , , and 𝜇g/mL CC myoblast Lee et al., []
Suppression or mitigation of the increases in
plasma CPK, AST, ALT, and MDA levels aer
downhill running
Camellia sinensis .% w/w in diet for weeks aer
downhill running Mice Haramizu et al.,
[]
Chlorella (only CPK) % Chlorella-supplemented diet
(CSD group) Transgenic mice Nakashima et al.,
[]
Reduction of the levels of carbonylated protein
Camellia sinensis .% w/w in diet for weeks aer
downhill running Mice Haramizu et al.,
[]
Curcuma longa – 𝜇gkg
−1 of curcumin Wistar rats (𝑛 = 130)Vitadelloetal.,
[]
Camellia sinensis GTE(mg/kgbodyweight) Sixtymalerats Alwayetal.,[]
Evidence-Based Complementary and Alternative Medicine
T : C o n t i n u e d.
Eect Botanicals Physiology Study Authors
Attenuation of hydrogen peroxide concentration Curcuma longa mg Male CBL/ mice Kawanishi et al.,
[]
Attenuation of NADPH-oxidase mRNA
expression Curcuma longa mg Male CBL/ mice Kawanishi et al.,
[]
Attenuation of F/ mRNA expression Curcuma longa mg Male CBL/ mice Kawanishi et al.,
[]
Counteraction of the increase of BiP, ATF,
XBPu, and XBPs mRNA Camellia sinensis Green tea extract (.% w/vol) Twelve-week-old female CBL/J
mice
Rodriguez et al.,
[]
Increase in the mitochondrial oxygen
consumption rate
Korean mistletoe (Visc um a lb um
subsp. coloratum)𝜇g/mL L cells and CC cells, mice Jung et al., []
Increaseoftheexpressionofperoxisome
proliferator-activated receptor coactivator-
(PGC-) 𝛼and SIRT-
Korean mistletoe (Visc um a lb um
subsp. coloratum)𝜇g/mL L cells and CC cells, mice Jung et al., []
Vitis v inifera .% trans-resveratrol for
months
Middle-aged ( months) C/BL
mice Jackson et al., []
Glycine max 𝜇MCCmyotubes
Hirasaka et al.,
[]
Vitis v inifera mg/kg/day irty-six male rats Bennettetal.,
[]
Decrease of PGC-𝛼expression Go-sha-jinki-Gan (GJG) (only
PGC-𝛼)% (w/w) Male SAMP, SAMR mice Kishida et al.,
[]
Decrease of BUN
Aegle marmelos (L.) Corr. mg/kg BW for days BALB/c mice Nallamuthu et al.,
[]
Pumpkin (Cucurbita moschata)fruit , , , and mg/kg/day for
days MaleICRmice Wangetal.,[]
Tao-Hong-Si-Wu-Tang (THSWT) , , and mL/kg b ody weight for
days male mice Li et al., []
Acanthopanax senticosus
mg/kg and mg/kg;
mg/kg or mg/kg; mg/kg or
mg/kg
Five-week-old male ICR mice Huang et al., []
Ashwagandha (Withania somnifera)
(WS)
mg/day × days; mg/day
× days; mg/day × days
Eighteen apparently healthy
volunteers Raut et al., []
Increase of SOD and catalase
Aegle marmelos (L.) Corr. , , and mg/kg BW for d BALB/c mice Nallamuthu et al.,
[]
Panax ginseng (only SOD) mg/kg Rat Tan et al., []
Salvia ocinalis (SOD and GSHPx) , , and mg/kg BW rats JiPing, []
Upregulation of GLUT- and AMPK-𝛼Aegle marmelos (L.) Corr. , , and mg/kg BW for d BALB/c mice Nallamuthu et al.,
[]
Decrease in SUN levels Rubus parvifolius L. (RPL) mg/kg and mg/kg Five-week-old male Chen et al., []
Increase of Grp protein Curcuma longa – 𝜇gkg
−1 of curcumin Wistar rats (𝑛 = 130)Vitadelloetal.,
[]
Decrease in myostatin and 𝛽-galactosidase Camellia sinensis mg/kg b.i.d. Young and old CBL/ male mice Gutierrez-Salmean et
al., []
Increase in the ratio of plasma
follistatin/myostatin Camellia sinensis mg of pure Epi (∼ mg/kg/day) Human subjects (𝑛=6)Gutierrez-Salmean et
al., []
Decrease in cross-sectional area (CSA) Eriobotrya japonica mg/kg/day Young (-month-old) and aged
(--month-old) rats Sung et al., []
Evidence-Based Complementary and Alternative Medicine
T : Botanicals with anti-inammatory eects on skeletal muscle.
Paper Botanical Compound Model Physiology Main results
In vitro
Kim et al.,
[]
Korean Citrus
aurantium L.
Flavonoids (hesperidin,
nobiletin, and naringin) Rat skeletal muscle cells Flavonoids , , ,
and 𝜇g/mL
Decrease in the production of inducible nitric oxide synthase,
cyclooxygenase-, TNF-𝛼, and IL-.
Kim et al.,
[]
Korean Citrus
aurantium L.
Flavonoids (naringin,
hesperidin, poncirin,
isosinnesetin, and
hexamethoxyavone)
Rat skeletal muscle cells 𝜇gProtection of cell-structure related proteins and decrease in level of
cleaved caspase-.
Leite et al.,
[]
Eugenia
punicifolia
Pentacyclic triterpenes
(barbinervic acid)
Mouse myoblastoma
cells (CC)
Ep-CM
𝜇g/mL
Reduction of CC cell density and proliferation. Increase of
metalloproteases activity: MMP- ( ±%, 𝑝 < 0.005)and
MMP- ( ±%, 𝑝 < 0.005).
Wang et al.,
[] Viti s vinifera Resveratrol
(,,-trihydroxystilbene) Mouse CC cells Resveratrol
𝜇M
Counteraction of TNF-𝛼induced muscle protein loss and reversion
of declining expression of Akt, mTOR, pSK, E-BP, and FoX.
Guo et al.,
[] Coee
Chlorogenic acid,
anhydrous caeine, and
polyphenols
Mouse myosatellite
cells
Coee solution
, , , and
𝜇g/mL
Increase in cell proliferation rate, enhancement of the DNA
synthesis of the proliferating satellite cells, and increase of the
activation level of Akt.
Animals
Yu et al., [] Panax ginseng Dammarane steroids (DS) Rats DS
, , and mg/kg
Anti-inammatory eects on skeletal muscle following
muscle-damaging exercise.
Kishida et al.,
[]
Go-sha-jinki-Gan
(GJG)
Paeoniorin, loganin, and
total alkaloids
Male SAMP, SAMR
mice
GJG
% (w/w)
Reduction of the loss of skeletal muscle mass and amelioration of
theincreaseinslowskeletalmusclebers.
Guo et al.,
[] Coee
Coee bean, chlorogenic
acid, anhydrous caeine,
and polyphenols
CBL/ mice
e same amount of
drink in control and
coee group for
weeks
Improvement in grip strength; faster regeneration of injured skeletal
muscles. Decrease in the levels of interleukins.
Leite et al.,
[]
Eugenia
punicifolia Dichloromethane fraction Male mdx dystrophic
mice
Ep-CM
mg/mL
Reduction of MMP- ( ±%, 𝑝 < 0.005) and MMP- ( ±%,
𝑝 < 0.005) activities. Reduction of TNF-𝛼production ( ±%,
𝑝 < 0.01)andNF-𝜅Bexpression(48 ± 7%, 𝑝<0.005).
Leite et al.,
[]
Eugenia
punicifolia
Pentacyclic triterpenes
(barbinervic acid) CBL/ mice Ep-CM
mg/mL
Reduction of MMP- activity (35 ± 7%, 𝑝 < 0.05) but dierence
concerning MMP- activity in the muscular lesion; reduction of the
inammatory lesion area.
Boz et al.,
[] Curcumin Curcumin Male Wistar rats mg/kg/day Decrease of CK activity (𝑝>0.05) and signicant decrease of
myoglobin levels (𝑝 < 0.05).
Evidence-Based Complementary and Alternative Medicine
T : C o n t i n u e d.
Paper Botanical Compound Model Physiology Main results
Humans
D´
ıaz-Castro et al.,
[]
Phlebodium
decumanum
Polyphenols, terpenoids,
and xavonoids
Amateur athletes
(𝑁=40)
capsulesofmg
( mg of leaf extract
and mg of rhizome
extract)
Reduction of oxidative stress (𝑝 < 0.0001). Reduction in the
inammatory response. Decrease of TNF-𝛼before and aer the
high-intensity exercise. Increase in sTNF-RII.
Hou et al.,
[]
Panax
notoginseng Ginsenosides Rg Healthy young men
(𝑁=26)mg ofRg
Increase in exercise time to exhaustion (Rg . ±. min versus
placebo . ±. min).
Improvement in meal tolerance during recovery (𝑝 < 0.05).
Blacketal.,
[]
Zingiber ocinale
Roscoe Gingerols and shogaols Individuals (𝑁=28) g of ginger aer
exercise
Postexercise reduction in arm pain the following day (%; −. ±
mm).
Blacketal.,
[]
Zingiber ocinale
Roscoe Gingerols and shogaols
participants in study
participants in study
gfor consecutive
days aer exercise
Decrease in pain-intensity ratings hours aer eccentric exercise
in both studies (𝑝 < 0.05).
Pumpa et al.,
[]
Panax
notoginseng Saponins (ginsenosides) Well - t r ai n e d ma le
volunteers (𝑁=20)gof P. notoginseng Decrease in IL- h aer the downhill run (placebo). Decrease in
TNF-𝛼 h aer the downhill run (placebo).
Drobnic et al.,
[] Curcumin Phytosome delivery system
(Meriva)
Healthy, moderately
active male (𝑁=20)
gtwicedaily
(corresponding to
mg curcumin twice
aday)
Signicant decrease in pain intensity for the right and le anterior
thigh (. ±. and . ±., 𝑝 < 0.05).
Lower increase in hsPCR levels at hours (.%). Lower increase
of IL- levels at hours (. ±. pg/mL, 𝑝 < 0.05).
Nicol et al.,
[] Curcumin Curcuminoids Men (𝑁=17).gtwicedaily
Moderate-to-large reduction in pain during single-leg squat (VAS
scale −. to −.; % CL: ±.), gluteal stretch (−. to −.; ±.),
and squat jump (−. to −.; ±.) and reduction in creatine kinase
activity (−–%; ±-%). Increase in IL- concentrations at h
(%; ±%) and h (%; ±%), but decrease in IL- at h
relative to postexercise period (−%; ±%).
Tanabe et al.,
[] Curcumin Curcuminoids
(eracurmin)
Untrained young men
(𝑁=14)
mg before and h
aer each eccentric
exercise
Faster recovery of maximum voluntary contraction torque (e.g.,
days aer exercise: − ±% versus − ±%), lower peak serum
CK activity (peak: ± IU/L versus ± IU/L,
𝑝 < 0.05). No signicant changes in IL- and TNF-𝛼aer exercise.
Evidence-Based Complementary and Alternative Medicine
T : Botanicals with counterbalancing muscle damage eects.
Paper Botanical Compound Model Physiology Main results
In vitro
Hern´
andez-
Santana et al.,
[]
Rhodiola rosea RR extracts: rosavins
and salidroside
Murine skeletal muscle
cells – 𝜇g/mL and others
Upregulation of HSP mRNA levels and enhancement of the
expression by exposure to H2O2(𝑝 < 0.05). Maintenance of HSP
protein levels in pretreated cell cultures compared to controls (−%).
Dargelos et al.,
[] Pinus pinaster Polyphenols
Cultured human
skeletal muscle satellite
cells
Oligopin (. mg/mL) Restorationofcellviability(.±.% versus . ±.% in H2O2
treated cells). Abolishment of H2O2induced apoptotic cell death.
Animals
Haramizu et al.,
[] Camellia sinensis
Catechins:
epigallocatechin
gallate,
epigallocatechin,
epicatechin gallate,
epicatechin,
gallocatechin, and
gallocatechin gallate
Mice
.% w/w in diet for
weeks aer downhill
running
Mitigation of the running-induced decrease in voluntary
wheel-running activity by %. Maintenance of endurance running
capacity ( ±versus± min, 𝑝<0.05).
Kawanishi et al.,
[] Curcuma longa Curcumin Male CBL/ mice mg Decrease of hydrogen peroxide concentration and NADPH-oxidase
mRNA expression (𝑝 < 0.05).
Rodriguez et al.,
[] Camellia sinensis Green tea extracts Twel v e-wee k - old
female CBL/J mice
Green tea extract (.%
w/vol)
Decrease of BiP, ATF, XBPu, and XBPs mRNA. No activity on
CHOP mRNA.
Humans
Shanely et al.,
[] Rhodiola rosea
Rosavin, salidroside,
syringin, triandrin, and
tyrosol
subjects (
completing all aspects
of the study)
mg/day for days
prior to, on the day of,
and aer days of the
marathon
No eects on DOMS increased (𝑝 = 0.700).
Pumpa et al.,
[]
Panax
notoginseng
Saponins
(ginsenosides)
Twe nty we l l -trai n e d
male volunteers
mg of P.
notoginseng capsules
Lower IL- concentrations h aer the downhill run in the placebo
group.
Matsumura et al.,
[]
Zingiber ocinale
Roscoe Gingerols and shogaols non-weight trained
participants
g of ginger once a day
for days
Acceleration in the recovery of muscle strength following intense
exercise.
Evidence-Based Complementary and Alternative Medicine
T : Botanicals with antifatigue activity on skeletal muscle.
Paper Botanical Compound Model Physiology Main results
In vitro
Jung et al.,
[]
Korean mistletoe
(Viscum albu m
subsp. coloratum)
KME (Korean
mistletoe extract)
L cells and CC
cells, mice 𝜇g/mL Acceleration of OCR (%). Signicant increase in PGC-𝛼mRNA
expression. .-fold increase in SIRT expression.
Nallamuthu et al.,
[]
Aegle marmelos
(L.) Corr. Polyphenols BALB/c mice , , and
mg/kg BW for d
Increase in the duration of swimming time to exhaustion by . and
.% for medium and higher doses, respectively.
Animals
Wang et al.,
[]
Pumpkin
(Cucurbita
moschata)fruit
C. moschata fruit
extract (CME) Male ICR mice
, , , and
mg/kg/day for
days
Dose-dependent increase in swimming time (𝑝 = 0.0006).
Tan e t al . ,
[] Panax ginseng Ginsenoside Rb
(GRb) Rat mg/kg Signicant decrease of maximum grip strength of the MG group and
the GG group (𝑝 < 0.05).
Li et al., []
Tao-Hong-Si-Wu-
Tan g
(THSWT)
male mice , , and mL/kg
body weight for days Signicant increase of exhaustive swimming times (𝑝 < 0.05).
JiPing, [] Salvia ocinalis rats , , and
mg/kg BW Reduction of lipid peroxidation, LDH, and CK.
Ye h e t a l . ,
[] Angelica sinensis Ferulic acid Male ICR strain mice
. g/kg/day (Ex-AS)
and . g/kg/day
(Ex-AS), weeks
Slight increase of grip strength (𝑝 = 0.0616), at the higher AS doses,
longer exercise performance (., 𝑝 = 0.0116).
Huang et al.,
[]
Acanthopanax
senticosus
Eleutheroside E,
eleutheroside E2
Five-week-old male
ICR mice
mg/kg and
mg/kg; mg/kg
or mg/kg; mg/kg
or mg/kg
Increase of swimming time to exhaustion at high dose (𝑝 < 0.01).
Chen et al.,
[]
Rubus parvifolius
L. (RPL)
ree saponins
(nigaichigoside,
suavissimoside, and
coreanoside)
Five-week-old male mg/kg and mg/kg
Delays of SUN and LA accumulation, decrease in TG level, and
increase in HG and LDH. Suppression of inammatory cytokine
production.
Jung et al.,
[]
Korean mistletoe
(Viscum albu m
subsp. coloratum)
ICR mice
KMEator
mg/(kg⋅d) for
week
and,,,and
mg/kg
Induction of mitochondrial activity and improvement in endurance.
Jackson et al.,
[] Vitis v inifera Resveratrol
Middle-aged (
months old) C/BL
mice
.% trans-resveratrol
for months
Protection against oxidative stress through the upregulation of
MnSOD. Increase in the muscles activity in animals that were
months of age by an additional ∼% (𝑝 ≤ 0.05).
Humans
Raut et al.,
[]
Ashwagandha
(With ania
somnifera)(WS)
Eighteen apparently
healthy volunteers
mg/day × days;
mg/day × days;
mg/day × days
Increase in serum creatinine and blood urea nitrogen. Signicant
decrease in total cholesterol.
Evidence-Based Complementary and Alternative Medicine
T:Botanicalswitheectsonmuscleatrophy.
Paper Botanical Compound Model Physiology Main results
In vitro
Lee et al.,
[]
Cichorium
intybus (Cii) CC myoblast , , , and 𝜇g/mL Prevention of cell viability loss.
Hirasaka et al.,
[] Glycine max Isoavone (genistein
and daidzein) CC myotubes 𝜇M Approximately -fold increase of SIRT mRNA expression.
Mirza et al.,
[] Camellia sinensis Epigallocatechin--
gallate CC myotubes – 𝜇MReduction of the expression of proteasome S and S subunits.
Reduction of the expression of MuRF- and MAFbx.
Frati et al.,
[] Chestnuts our
Chestnuts our extract
polyphenols or
tocopherols or SL-s
CC myotube cells
Polyphenols ( nM)
or tocopherols
( nM)
Counterbalance of cell atrophy. Γ-Tocopherol and sphingolipids
positivelyaectskeletalmusclecellatrophy.
Animals
Vitadello et al.,
[] Curcuma longa Curcumins Wistar rats (n=) – 𝜇gkg
−1 of
curcumin
About twofold increase of Grp in muscles of ambulatory rats
(𝑝 < 0.05).Counteractedlossofsoleusmassandmyober
cross-sectional area by % (𝑝 ≤ 0.02).
Nakashima et al.,
[] Chlorella Transgenic mice
% Chlorella-
supplemented diet
(CSD group)
Improvement of skeletal muscle atrophy and cytochrome C oxidase
activity. Recovery of body weight, enhancement of oxidative stress,
and increase of CPK.
Humans
Choquette et al.,
[] Glycine max
Isoavones (daidzein,
glycitein, and
genistein)
women Isoavones ( mg/day)
and exercise No eects.
Evidence-Based Complementary and Alternative Medicine
has no remarkable eect aer single administration. In fact,
only a moderate reduction in the progression of muscle pain
from h to h following eccentric exercise was observed
in participants who consumed ginger h aer exercise, and
this eect was not enhanced by heat-treated ginger. In mice,
Coea decreases the levels of interleukins IL-𝛼and IL-
and TNF-𝛼, which are correlated with muscle weight and
grip strength. Using mice cells in vitro, coee increases the
number of proliferating cells and augmented DNA synthesis
through the Akt signaling pathway. As a result, there is
a combination of augmented satellite cell activation and
decreased inammatory levels by coee treatment; it has
anti-inammatory eects both because it has antioxidant
properties and because it has compounds, such as kahweol,
with immunomodulatory properties [, , , , ]. Also,
Eugenia punicifolia showed anti-inammatory properties in
the gastrocnemius muscle of mdx dystrophic mice; in par-
ticular, the activity of dichloromethane fraction of Eugenia
punicifolia (Ep-CM), in mice, decreases metalloprotease-
and metalloprotease- activities (indicators of local inam-
mation and tissue remodeling, resp.) and levels of tumor
necrosis factor-𝛼and NF-𝜅B transcription factor []; iso-
lated pentacyclic triterpene from Eugenia punicifolia reduces
myoblast cells proliferation, has no eects on apoptosis, and
increases matrix metalloproteases and muscular area (MMP-
and MMP-) []. As shown in the study by Yu et al.
[], Dammarane steroids (DS) of Panax ginseng produce
anti-inammatory eects in rats, following muscle damage
exercise, because they potentiate inammation at baseline
but exerted anti-inammatory eects on skeletal muscle
following muscle-damaging exercise. Another study has also
highlighted the eect of steroid Rg (capsule with mg
of Rg), an ergogenic component of ginseng, in healthy
human against exercise challenge: the extract can minimize
unwanted lipid peroxidation and attenuate proinammatory
shi under exercise challenge and so it ameliorates the
postexercise recovery and mitochondria enzyme adaptation
probably because the incorporation of the bulky steroid
moiety of Rg into cellular membrane lipid may enhance
molecular complexity and mechanical stability of the cell
and mitochondrial membranes []. Panax notoginseng,as
shown by Pumpa et al., seems to have no particular eects
on interleukins, indicators of inammation and muscle
damage, in well-trained males aer a bout of eccentric
exercise designed to induce delayed-onset muscle soreness
(DOMS) (in the experiment, mg of Panax notoginseng
was used) []. Even Go-sha-jinki-Gan (GJG) maintains the
area of muscle bers in the soleus via normalizing signal
transduction through the insulin-growth factor (IGF-) Akt
axis, the suppression of inammation, and the maintenance
of mitochondrial-related transcription factors in mice [].
A positive eect on cell atrophy caused by TNF-𝛼was
shown with resveratrol (in Vitis vinifera) supplementation in
a muscle cell line (regulating the Akt/mTOR/FoxO signaling
pathways together with inhibition of the atrophy-related
ubiquitin ligase) [].
Finally, several studies have investigated the mechanisms
by which curcumin, a constituent of turmeric (Curcuma
longa L.), exerts its benecial eect on muscle []. Early
experimental study demonstrated that curcumin suppresses
the activation of NF-𝜅B, an eect of critical relevance in
DOMS relief, since NF-𝜅B appears to be involved in the
regulation of proteolysis and inammation in muscle [].
erefore, inhibition of NF-𝜅Bbycurcuminmayresultina
muscle-protective eect. Consistently, it has been suggested
that curcumin may prevent loss of muscle mass during sepsis
and endotoxaemia and may stimulate muscle regeneration
aer traumatic injury []. Other mechanisms potentially
responsible for the anti-inammatory and antioxidant prop-
erties of curcumin include induction of heat-shock response
[], reduction in the expression of the proinammatory
enzyme cyclooxygenase- (COX-), and promotion of the
antioxidant response by activation of the transcription factor
Nrf []. More recent studies conrm that curcumin can
reduce inammation and decrease some of the negative
eects associated with eccentric exercise-induced muscle
damage, including the release of proinammatory cytokines
and markers of muscle injury like creatine kinase (CK),
asshowninanimalmodels[]andininvitrosettings
[].
e three studies that have been conducted until now
in humans [, , ] have shown that curcumin, at the
dosages of g twice daily (as the Phytosomedelivery system,
Meriva) and . g twice daily, and mg of solid-lipid
nanoparticle curcumin (eracurmin), respectively, can
prevent DOMS with some evidence of enhanced recovery
of muscle performance, maximal voluntary contraction loss,
and serum creatine kinase activity increase.
In conclusion, the muscle that makes activities undergoes
an increase in inammation that can damage the mus-
cle itself. It is important to counteract the inammatory
activity in order to preserve the muscle from numerous
types of damage. Several animal and in vitro studies have
investigated the ecacy of botanicals with recognized anti-
inammatory activity (such as Phlebodium decamanum,Cit-
rus aurantium,Coea arabica,Zingiber ocinale,Eugenia
punicifolia,Panax ginseng,Go-sha-jinki-Gan,Vitis vinifera,
and Curcuma longa L.) on inammation secondary to muscle
activity (Table ). ese botanical extracts exerted their
eects through dierent biochemical pathways, specically
decreasing interleukins or aging on transcriptional factors.
Human studies were performed using four botanicals (Panax
ginseng,Zingiber ocinale,Phlebodium decumanum,and
Curcuma longa L.) showing that () the daily consumption
of raw and heat-treated Zingiber resulted in moderate-to-
largereductionsinmusclepainaerexercise-inducedmuscle
injury; () Phlebodium supplementation for both professional
and amateur athletes performing strenuous exercise resulted
in reducing the undesirable eects of the oxidative stress
and inammation signaling elicited during high-intensity
exercise; () Panax notoginseng did not convincingly have
an eect on performance, muscular pain, or assessed blood
markers in well-trained males aer an intense bout of eccen-
tric exercise that induced delayed-onset muscle soreness
(DOMS); () curcumin could prevent DOMS enhancing the
recovery of muscle performance and the maximal voluntary
contraction loss and modulating the serum creatine kinase
activity increase.
Evidence-Based Complementary and Alternative Medicine
All these clinical studies considered the reduction of
inammation and consequently muscle pain aer a strenuous
exercise and not in sarcopenic subjects, but this is a good
starting point for the future utilization of these plants in the
elderly.
3.3. Muscle Damage Prevention. is research has been
carried out based on the keywords “skeletal muscle mass”
and “damage” and “botanicals” or “plants” or “extracts”;
articles were sourced and studies have been taken into
consideration. Among these, studies are in in vitro setting,
inanimals,andinhumans(Table).
A recent study by Kawanishi et al. has claried properties
of curcumin aer downhill running-induced muscle damage
in mice. is study underlines how curcumin has an antiox-
idant eect in mice following downhill running-induced
muscle damage; however, no dierences in plasma creatine
kinase (CK) and plasma lactate dehydrogenase (LDH), as
markers of muscle damage, were observed. Curcumin admin-
istration immediately aer downhill running did not prevent
muscle damage but signicantly attenuates the concentration
of hydrogen peroxide and NADPH-oxidase gene expression;
therefore, curcumin may be benecial for the prevention of
oxidative stress in downhill running-induced skeletal muscle
damage []. Two recent studies in humans by Pumpa et
al. [] and Matsumura et al. [] investigated the eects of
Panax notoginseng ( mg) and Zingiber ocinale ( g for
days) on delayed-onset muscle soreness (DOMS); Zingiber
ocinale supplementation could have accelerated the recov-
eryofmaximalstrengthfollowingmuscledamagebutdidnot
prevent delayed muscle damage. e authors concluded that
there is no evidence to support the use of Panax as a pre-
ventive option for DOMS and its related inammation. Rho-
diola rosea ( mg/d) did not attenuate the postmarathon
decrease in muscle function, the increases in muscle damage,
the extracellular heatshock protein (eHSP), or the plasma
cytokines in human experienced runners []; however, the
same plant modulates in vitro the expression of molecular
factors (chaperone HSP) such as heatshock proteins (HSP)
in order to protect C C myotubes cells against peroxide-
induced oxidative stress, suggesting a potential antioxidant
role []. Finally, Haramizu et al. demonstrated that catechins
of Camellia sinensis attenuate downhill running-induced
muscle damage in mice, perhaps through their antioxi-
dant properties, hastening recovery of physical performance
[]. A typical example of muscle damage is the cellular
dysfunction caused by lipid excess. Lipid excess activates
endoplasmatic reticulum (ER) stress in skeletal muscle and,
as a consequence, accumulation of unfolded or misfolded
proteins in ER lumen. Rodriguez et al. demonstrated that
epigallocatechin--gallate (EGCG) from Camellia sinensis
could protect mice muscle against ER stress, especially thanks
to its antioxidant properties []. Dargelos et al. investigate
the role of a natural antioxidant extracted from pine bark
(Pinus pinaster)inculturedhumanskeletalmusclesatellite
cells. Results showed that this polyphenolic extract is able
to protect cells from oxidative stress (H2O2)damageand
prevent the apoptosis and the activation of calpains mediated
by H2O2[].
In conclusion (Table ), until today, important studies
were made on humans and animals for the prevention of
muscle damage. Most of the plants used (Curcuma longa,
Panax notoginseng,Zingiber ocinale,Rhodiola rosea,Camel-
lia sinensis,andPinus pinaster)actonDOMS,thankstotheir
antioxidant properties. In human, Panax notoginseng seems
to have no eect as a preventive option for DOMS, and Rhodi-
ola rosea does not attenuate muscle damage. Further studies
are needed but we can say that botanical supplementation,
thanks to its antioxidant properties, could be useful to prevent
sarcopeniaduetothefactthatthelossofmusclemassinaging
is driven also by oxidative stress, as it happens aer strenuous
exercise.
3.4. Antifatigue. is research has been carried out based
on the keywords “skeletal muscle mass” and “fatigue” and
“botanicals” or “plants” or “extracts”; articles were sourced
and studies are taken into account. Among these, only one
study is made in humans, one in in vitro settings, and one
both in in vitro settings and in animals and the others are
made in animals (Table ).
Tan et al. in investigated for the rst time the
role of ginsenoside Rb (Grb) in Panax quinquefolius,as
antifatigue agent, on postoperative fatigue syndrome (POFS)
in a rat model induced by major small intestinal resection,
through its antioxidant properties and the improvement of
energy metabolism. Grb enhances maximum grip strength
and increases the activity of lactate dehydrogenase and
other biochemical parameters. e results suggested that
GRb improves the maintenance of normal pH range in
muscle tissue by reducing the accumulation of lactic acid
(LA) and attenuates LA induced side eects of various bio-
chemical and physiological processes, which impair bodily
performance []. In accordance, the study by Nallamuthu
et al. demonstrated the antifatigue properties in mice of
A.marmelos fruit, most probably manifested by delaying
the accumulation of serum lactic acid, increasing the fat
utilization, and upregulating the skeletal muscle metabolic
regulators []. Likewise, Salvia sativa,Angelica sinensis,
Cucurbita moschata,Withania somnifera,andAcanthopanax
senticosus extracts exhibit dierent antifatigue eects. All
of these studies, with the exception of Withania somnifera,
are performed in animals (rats or mice). ese studies
demonstrate that the antioxidant properties of plants play an
important role in reducing fatigue. Salvia reduces lipid per-
oxidation, lactate dehydrogenase, creatine kinase activities,
enhanced antioxidant enzymes, and cholinesterase (ChE)
activities in the skeletal muscle of endurance exercise rats;
similar eects have been observed for other extracts, with
some dierences between each other, in which, additionally,
antifatigue is measured also by forelimb grip strength and
exhaustive swimming time as well as serum levels of lactate,
ammonia, glucose, and creatine kinase aer a min swim-
ming exercise. Specically, the mechanisms of Acanthopanax
(also called Eleutherococcus senticosus or Siberian ginseng)
are the reduction of the level of triglycerides by increasing fat
utilization, the delay of the accumulation of blood urea nitro-
gen (BUN), and the increase of the lactate dehydrogenase
(LDH) to reduce the accumulation of lactic acid in muscle
Evidence-Based Complementary and Alternative Medicine
andthenprotectthemuscletissue[,,,,].Strange
but active is Tao-Hong-Si-Wu-Tang that shows antifatigue
activity in mice due to extended exhaustive swimming time,
theincreaseofliverandmuscleglycogencontents,andthe
decrease of the lactic acid (BLA) and urea nitrogen (BUN)
plasmaticcontents[].Also,Chenetal.denetheantifa-
tigue property of Rubus parvifolius L. (RPL) in experiment
with mice, nding that total saponins from RPL possess
potent capabilities to alleviate fatigue induced by forced
swimming and that nigaichigoside F was responsible for the
pharmacological eect. e underlying mechanisms include
delays in the accumulation of serum urea nitrogen (SUN)
andlacticacid(LA),adecreaseinTGlevelbyincreasingfat
consumption, increases in hepatic glycogen (HG) and LDH
so that lactic acid accumulation was decreased, the reduction
of ammonia in the muscle, and the suppression of increased
immune activation and inammatory cytokine production
[]. Viscum album subsp. coloratum increase mitochondrial
oxygen consumption rate (OCR) in L cells and increase
the expression of peroxisome proliferator-activated receptor
c coactivator- (PGC-) a and silent mating type information
regulation homolog (SIRT), two major regulators of
mitochondria function, in CC cells, suggesting that this
extracthasgreatpotentialasanovelmitochondria-activating
agent and could exert the antifatigue eect []. Jackson et
al. try to understand how Vitis vinifera and its compound
resveratrol could prevent muscle fatigue. Resveratrol has a
protective eect against aging-induced oxidative stress in
skeletal muscle, likely through the upregulation of manganese
superoxide dismutase (MnSOD) activity, reducing hydrogen
peroxide, and lipid peroxidation levels in muscle samples, but
sarcopenia was not attenuated by resveratrol [].
Withania somnifera (gradual escalating doses from to
mg/day) in humans has demonstrated muscle strength-
ening and lipid lowering [].
In conclusion, there are several preclinical lines of evi-
dence that botanical extracts, such as Panax quinquefolius,A.
marmelos fruit, Salvia sativa,Angelica sinensis,Phalaenopsis
cornu-cervi,Cucurbita moschata,Withania somnifera ,Acan-
thopanax senticosus, deer antler extract, Tao-Hong-Si-Wu-
Ta ng , Rubus parvifolius L.,velvetantlerextract,Vi scum album
subsp. coloratum,andVitis vinifera,canreducethemuscle’s
fatigue, aer intense exercise or simply in a condition of loss
of muscle mass, as in sarcopenia (Table ). Commonly, these
properties are due to their antioxidant eects: in general,
these plants reduce lipid peroxidation, lactic acid, and serum
levels of ammonia and creatine kinase and increase liver
andmuscleglycogen.eonlystudyfoundinhuman
wasthatofRautetal.,inwhichsupplementationwith
Withania somnifera (with gradual escalating doses from
to mg/day) seems to have good eects on antifatigue,
but this is a preliminary study. Until today, the role of
plants in antifatigue in clinical studies has been not deeply
documented and so it is dicult to recommend particular
supplementation.
3.5. Muscle Atrophy Prevention. is research has been car-
ried out based on the keywords “skeletal muscle mass” and
“atrophy” and “botanicals” or “plants” or “extracts”; articles
were sourced and studies are taken into account. Among
these, are in in vitro settings and are in animals and only
one is in human (Table ).
Curcuma longa can prevent muscle atrophy. It stimu-
lates glucose-regulated protein kDa (Grp) expression
in myogenic cells, whose levels decrease signicantly in
unloaded muscle, and it is involved in attenuation of myober
atrophy in rats []. Also, Camellia sinensis extracts in
rats appear to counteract the increased protein degradation
(linked with its ability to downregulate key components of
the ubiquitin proteasome proteolytic pathway) []. Instead,
Cichorium intybus extract prevents skeletal muscle atrophy
in vitro, probably increasing heat-shock protein- (Hsp-)
production and inhibiting the level of ceramide: Hsp-, in
fact, has a positive eect on reducing oxidative stress of cells
and ceramide is involved in the regulation of cell death [].
Also, chestnut sweet our (rich in 𝛾-tocopherol) protects
from skeletal muscle cell atrophy, but this protection appears
not to be due to a general antioxidant action, but maintaining
cellular redox homeostasis through the regulation of NADPH
oxidase, mitochondrial integrity []. Isoavones are the
most important phytochemicals in Glycine max for prevent-
ing muscle atrophy. ese products could induce in vitro
the expression of SIRT-, a sirtuin that normally deacetylates
p, in order to reduce the activity of MuRF- related to
muscle atrophy. Overall, they suppress MuRF- promoter
activity and myotube atrophy induced by TNF-𝛼in CC
myotubes []. However, a study performed by Choquette
et al. demonstrated that, in postmenopausal women, only
exercise, but not soy isoavones ( mg/day), could improve
muscle strength and reduce risks of mobility impairments
[]. In addition, consumption of Chlorella,aunicellular
green alga, could prevent age-related muscle atrophy in mice,
because it contains various antioxidant substances, including
carotenoids and vitamins and plastoquinone that has been
showntoholdgreaterantioxidantproperties.Chlorella con-
tains also amino acids such as the brain chain amino acids
(BCAA) valine, leucine, and isoleucine, which are important
components of actin and myosin, the fundamental muscle
proteins, and may be important in prevention of sarcopenia.
Finally, Chlorella also prevents mitochondrial dysfunction
[].
In conclusion, it is clear that botanical extracts can
preventtheatrophyofmuscle,aerintenseexerciseorsimply
in a condition of loss of muscle mass, as in sarcopenia.
We considered several botanicals (Curcuma longa,Camellia
sinensis,Cichorium intybus, chestnut sweet our, Glycine
max,andChlorella): most of them have important antiox-
idant properties, which prevent muscle’s atrophy. However,
the only study made on human, using Glycine max,didnot
show positive results and so other researches are needed to
substantiate the use of botanicals supplementation to prevent
muscle atrophy.
3.6. Muscle Regeneration and Dierentiation. is research
has been carried out based on the keywords “skeletal muscle
mass” and “regeneration” and “botanicals” or “plants” or
“extracts”; articles were sourced and studies are taken
into account. Among these, are in in vitro settings, in
Evidence-Based Complementary and Alternative Medicine
animals,andinhumanandoneisbothinanimalsandin
humans (Table ). Nutraceutical compounds by C. sinensis
in mice decrease myostatin and 𝛽-galactosidase and increase
levels of markers of muscle; instead, in humans, they (-day
treatment with epicatechin at mg/kg/day) increase hand grip
strength and the ratio of plasma follistatin/myostatin []
and regulate NF-𝜅B activity in regenerating muscle bers [].
Camellia also induces changes in satellite cell number and it
improves muscle recovery following a period of atrophy in
old rats and decreases oxidative stress, but this is insucient
to improve muscle recovery following a period of atrophy
[]. Also, an increase in myogenin (due to a supplement
of Vitis v inife ra resveratrol extracts) served to stimulate
dierentiation to compensate for an impaired function of
satellitecells(SCs)intheoldmuscles[].Anarticleby
Ballak et al., about resveratrol, says that this compound does
not rescue the hypertrophic response and even reduces the
numberofsatellitecellsinhypertrophiedmuscleofmice[].
Also, Ferula hermonis Boiss. and Vitis vinifera signicantly
increase muscle weight and enhance the growth of skeletal
muscle bers or ber size (increase the ber cross-sectional
area of type IIA and IIB bers) and nuclear number in
order to enhance the growth of skeletal muscle [, ]. It is
noteworthy that proanthocyanidins of Vitis have been used in
aclinicaltrial.Anincreaseofmusclemassandtheimprove-
ment of several physical conditions have been observed in
middle-aged women (with at least one menopausal symp-
tom) treated with doses from to mg/d []. Brous-
sonetia kazinoki (B.kazinoki), Corydalis turtschaninovii,and
Hachimijiogan, in vitro, promote myogenic dierentiation
through activation of key promyogenic kinase (p MAPK)
or ERK/ and MyoD transcription activities (MyoD family
transcription factors play a key role in promoting myoblast
dierentiation) without aecting the Akt signaling pathway
[–]. Another in vitro study, performed by Poussard et al.,
indicated Oligopin, a pine bark extract, as natural antioxidant;
in fact, with aging, oxidative stress produces disruption of
cytoskeleton and phosphorylated heat-shock protein beta-
(HSPB) may help to repair injured structures. Furthermore,
Oligopin prevents the stress-induced phosphorylation of
HSPB- in human cells []. Curcumin (Curcuma longa)may
modulate the entry into apoptosis during immobilization
and stimulate initial steps of muscle regeneration, aging on
proteins and enzyme such as proteasome chymotrypsin-like
activity and proapoptotic smac/DIABLO protein levels, and
apoptosome-linked caspase- activities []. Another study
was performed in humans with Withania somnifera:itseems
to improve muscle strength and endurance for the aged
subjects and so it could be used in preventing sarcopenia
(– mg twice daily for three months) []. Finally, Kim
et al. demonstrate that physical exercise combined with tea
catechin supplementation ( mL of a tea beverage fortied
with mg of catechins) had a benecial eect on physical
function measured by walking ability and muscle mass in
women with sarcopenia [].
Lastly, a very recent study [] demonstrated in ani-
mal models that loquat (Eriobotrya japonica) leaf extract
(LE) diminished the age-associated loss of grip strength
and enhanced muscle mass and muscle creatine kinase
(CK) activity. Histochemical analysis revealed that loquat
(Eriobotrya japonica) leaf extract (LE) abrogated the age-
associated decrease in cross-sectional area (CSA) and
decreased the amount of connective tissue in the muscle
of aged rats. Moreover, in order to investigate the mode
of action, CC murine myoblasts were used to evaluate
the myogenic potential of LE. e expression levels of
myogenic proteins (MyoD and myogenin) and functional
myosin heavy chain (MyHC) were measured by western
blot analysis. LE enhanced MyoD, myogenin, and MyHC
expression. e changes in the expression of myogenic genes
corresponded to an increase in the activity of CK, a myogenic
dierentiation marker. Finally, loquat (Eriobotrya japonica)
leaf extract (LE) activated the Akt/mammalian target of
rapamycin (mTOR) signaling pathway, which is involved in
muscle protein synthesis during myogenesis. ese ndings
suggest that loquat (Eriobotrya japonica) leaf extract (LE)
attenuates sarcopenia by promoting myogenic dierentiation
and subsequently promoting muscle protein synthesis.
In conclusion, there are several preclinical lines of evi-
dence for a variety of plants (Camellia sinensis,Vitis vinifera,
Ferula hermonis Boiss., grape seed,Broussonetia kazinoki,
Corydalis turtschaninovii, Hachimijiogan, pine bark,Cur-
cuma longa,Withania somnifera,andEriobotrya japonica),
but only four studies are available in humans: two of these
were conducted with supplementation of Camellia sinensis
products, one with Withania somnifera and one with grape
seed.Inparticular,theuseofWithania somnifera (– mg
twice a day) resulted in improving muscle strength in human
andalsothesupplementationwithmgofcatechinfrom
Camellia sinensis induced positive physical improvement.
e second study demonstrated an improvement in grip
strength, but it was only an experimental study with mg
of pure EGCG. Finally, the clinical trial with grape seed
(– mg/d) seemed to increase muscle mass and improve
other physical conditions during menopause. For muscle
regeneration, the main studies to take into account were
thoseperformedbyKimetal.andbyMishraetal.,in
which sarcopenic subjects have been enrolled. However, it
is clear that the supplementation with EGCG should be
complementary to appropriate physical exercise in order to
reach the benecial eects on muscle mass and that further
studies are needed also for Withania supplementation.
4. Discussion
Currently, only diet and exercise are recognized as an eective
means to counteract loss of muscle []. Regarding exercise,
it is important to note that exercise-induced muscle damage
(EIMD)canbecausedbyeccentrictypeorunaccustomed
(novel) exercise and results in decrements in muscle force
production, development of delayed-onset muscle soreness
(DOMS) and swelling, rise in passive tension, and an increase
in blood intramuscular proteins [].
Delayed-onset muscle soreness is generally considered a
hallmark sign of EIMD [], and it is thought that DOMS
is partially related to direct muscle ber damage, and its
magnitude appears to vary with the type, duration, and
intensity of exercise [].
Evidence-Based Complementary and Alternative Medicine
T : Botanicals with eects on muscle regeneration.
Paper Botanical Compound Model Physiology Results
In vitro
Hwang et al.,
[]
Broussonetia
kazinoki Kazinol-P (KP) CC and T/ cells KP in % HS for h,
– nM
Increase of expression of MHC, myogenin, and Troponin-T. Increase
in the level of an actively phosphorylated form of p MAPK (pp)
in a dose-dependent manner.
Lee et al.,
[]
Corydalis
turtschaninovii
Tetrahydropalmatine
(THP)
CC myoblasts and
broblast T/
Various concentrations
of THP
Enhancement of the expression of muscle-specic proteins, including
MHC, MyoD, and myogenin. Increase in the levels of phosphorylated
p MAPK.
Takeda e t a l . ,
[]
Hachimijiogan
(HJG) Murine skeletal cells HJG treatment
(– 𝜇g/mL) .-fold increase in the cell number.
Poussard et al.,
[] Pinus pinaster
Natural antioxidant:
short oligomers of
catechin and
epicatechin
Human muscle satellite
cells . mg/mL Block of the apoptosis and the protein oxidation. Recovery of HSPB.
Animals
Allouh, [] Ferula hermonis Ferutinin, teferdin,
teferin, and epoxy-benz Adult male rats mg/kg/rat Signicant increase in muscle weight, ber size, and nuclear number.
Bennett et al.,
[] Vitis vinifera Resveratrol (,,-
trihydroxystilbene) irty-six male rats mg/kg/day Favorable changes to type IIA and type IIB muscle ber CSA and
reduction of apoptotic signaling in muscles of old animal.
Alway et al.,
[] Camellia sinensis
Epicatechin,
gallocatechin,
epigallocatechin,
epicatechin--gallate,
and epigallocatechin--
gallate
Sixty male rats GTE ( mg/kg body
weight)
Counterbalance of the loss of hind limb plantaris muscle mass
(𝑝 < 0.05) and tetanic force (𝑝 < 0.05) during HLS. Improvement of
muscle ber cross-sectional area in both plantaris (𝑝 < 0.05)and
soleus aer HLS.
Evans et al.,
[] Camellia sinensis
Gallocatechin,
epigallocatechin,
epicatechin, and
epigallocatechin gallate
CBL/J and mdx
mice
.% or .% green
tea extract
Increase in the area of normal ber morphology (𝑝≤0.05). Decrease
in the area of regenerating bers (𝑝≤0.05).
Ballak et al.,
[] Vitis v inifera Resveratrol Mice (male CBL/J
mice)
. mg per gram body
mass per day
No modication of the age-related decrease in muscle force, specic
tension, or mass.
Gutierrez-
Salmean et al.,
[]
Camellia sinensis Epicatechin Young and old
CBL/ male mice mg/kgb.i.d. Signicant decrease of myostatin levels in young and old mice (%
and %, resp.). Signicant decrease of SA-𝛽-Gal in old SkM (%).
Vazeille et al.,
[] Curcuma longa Curcumin Male Wistar rats mg/kg body weight Improvement of recovery during reloading.
Sung et al.,
[]
Eriobotrya
japonica Leaf extract
Young (-month-old)
and aged
(--month-old) rats
mg/kg/day
Enhancement in MyoD, myogenin, and MyHC expression. Activation
of mTOR signaling pathway, which is involved in muscle protein
synthesis during myogenesis.
Evidence-Based Complementary and Alternative Medicine
T : C o n t i n u e d.
Paper Botanical Compound Model Physiology Results
Humans
Terauchi et al.,
[] Grape seeds Proanthocyanidin of
grape seeds women or mg/d
proanthocyanidin
Changes in lean mass and muscle mass from baseline to weeks
signicantly higher in treated groups.
Gutierrez-
Salmean et al.,
[]
Camellia sinensis Epicatechin Human subjects
(𝑛=6)
mg of pure Epi
(∼mg/kg/day)
Increaseinbilateralhandstrengthof∼%. Signicant increase (. ±
.%) in the ratio of plasma follistatin/myostatin levels.
Kim et al.,
[] Camellia sinensis Catechins women mg of catechins
daily
Signicant group ×time interactions in TUG (𝑝 = 0.005), usual
walking speed (𝑝 = 0.007), and maximum walking speed (𝑝<0.001).
Mishra and
Trikam j i , [ ]
With ania
somnifera
Alkaloids and steroidal
lactones individuals
mg of the whole
root extract twice daily;
mg twice dai ly
Improvement of the strength and functioning of the muscle.
Evidence-Based Complementary and Alternative Medicine
e inammatory response to EIMD results in the release
into blood of reactive species from both neutrophils and
macrophages and an array of cytokines from the injured mus-
cle including tumor necrosis factor- (TNF-) 𝛼, interleukin-
(IL-) 𝛽, and IL-, which contribute to low-grade systemic
inammation and oxidative stress []. e proinammatory
and prooxidant response can provoke secondary tissue dam-
age [], thus prolonging the regenerative process, which is
generally characterized by restoration of muscle strength and
resolution of inammation []. All these phenomena must
be avoided in elderly sarcopenic subjects and so it is critical in
this population to better preserve skeletal muscle and muscle
function.
In this review, we focused our attention on eects of
several botanicals on growth and health of muscle and we
divided these eects into ve categories: anti-inammation,
muscle damage prevention, antifatigue, muscle atrophy pre-
vention, and muscle regeneration and dierentiation.
To date, although the animal studies and in vitro studies
are numerous and promising, studies in humans evaluating
the eectiveness of anti-inammatory and antioxidant activ-
ities of botanicals on welfare of skeletal muscle are still very
few.
Although only relatively few human studies have been
published on the potential use of botanicals for the prevention
and treatment of muscle function, the present review is
important because it highlights the need of continued eorts
to nd eective treatment of this debilitating condition. e
available results, in particular considering human studies,
suggest that the botanicals that may be potentially useful
dietary supplements to prevent loss of muscle mass and
function are curcumin from Curcuma longa,alkaloidsand
steroidal lactones from Withania somnifera (Solanaceae),
catechins from Camellia sinensis,proanthocyanidinofgrape
seeds, and gingerols and shogaols from Zingiber ocinale.
It should be noted that this review is not claiming that the
use of these botanicals has been proven to prevent and treat
loss of muscle mass and muscle function, but we believe that
early and preliminary observations are promising. Further
researcheswillsupporttheuseofthesebotanicalsinthe
management of age-related muscle dysfunction and this may
openthepossibilityoftreatingage-relatedlossofmusclemass
and function with supplements.
Conflict of Interests
e authors declare no conict of interests regarding the
publication of this paper.
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