Artículo Original | Original Article Antimicrobial, antioxidant and phytochemical assessment of wild medicinal plants from Cordillera Blanca (Ancash, Peru) [Evaluación antimicrobiana, antioxidante y fitoquímico de plantas medicinales silvestres de la Cordillera Blanca (Ancash, Perú)]

Abstract

Twenty-eight native plants mainly used to cure diseases related to microbial infection and stress oxidative disorders were selected to test the antimicrobial activity against E. coli, P. aeruginosa, S. aureus, B. subtilis, and C. albicans using diffusion and microdilution methods. The antioxidant activity was determined by scavenging DPPH free-radical and phytochemical evaluation was performed for plants with promising activities. Twenty-seven plants showed antibacterial activity, four had anti-Candida activity, and four showed antioxidant activity. It was found that Oreocallis grandiflora, Gentianella weberbaueri, Gamochaeta americana, Hypericum laricifolium, Loricaria ferruginea, Muehlenbeckia volcanica, and Oenothera multicaulis, showed promising biological activity and contained alkaloids, phenolic compounds, flavonoids, catecholic or gallic tannins. This study leaves evidence about the medicinal potential of wild high-Andean plants; thus, further pharmacological, phytochemical, ecological and biotechnological studies will contribute to promote their conservation and sustainable use; especially since they are highly vulnerable and risk extinction.

Full text

BOLETÍN LATINOAMERICANO Y DEL CARIBE
DE PLANTAS MEDICINALES Y AROMÁTICAS
17 (3): 270 - 285 (2018)
© / ISSN 0717 7917 / www.blacpma.usach.cl
Artículo Original | Original Article
270
Antimicrobial, antioxidant and phytochemical assessment of wild
medicinal plants from Cordillera Blanca (Ancash, Peru)
[Evaluación antimicrobiana, antioxidante y fitoquímico de plantas medicinales silvestres de la
Cordillera Blanca (Ancash, Perú)]
Carmen Tamariz-Angeles1, Percy Olivera-Gonzales1 & Miguelina Santillán-Torres2
1Laboratorio de Biología, Facultad de Ciencias, Universidad Nacional Santiago Antúnez de Mayolo, Huaraz, Ancash, Perú
2Laboratorio de Química, Facultad de Ciencias, Universidad Nacional Santiago Antúnez de Mayolo, Huaraz, Ancash, Perú
Contactos | Contacts: Carmen TAMARIZ-ANGELES - E-mail address: ctamariz@unasam.edu.pe
Abstract: Twenty-eight native plants mainly used to cure diseases related to microbial infection and stress oxidative disorders were selected
to test the antimicrobial activity against E. coli, P. aeruginosa, S. aureus, B. subtilis, and C. albicans using diffusion and microdilution
methods. The antioxidant activity was determined by scavenging DPPH free-radical and phytochemical evaluation was performed for plants
with promising activities. Twenty-seven plants showed antibacterial activity, four had anti-Candida activity, and four showed antioxidant
activity. It was found that Oreocallis grandiflora, Gentianella weberbaueri, Gamochaeta americana, Hypericum laricifolium, Loricaria
ferruginea, Muehlenbeckia volcanica, and Oenothera multicaulis, showed promising biological activity and contained alkaloids, phenolic
compounds, flavonoids, catecholic or gallic tannins. This study leaves evidence about the medicinal potential of wild high-Andean plants;
thus, further pharmacological, phytochemical, ecological and biotechnological studies will contribute to promote their conservation and
sustainable use; especially since they are highly vulnerable and risk extinction.
Keywords: Cordillera Blanca; Andean plant; antibacterial; anti-Candida; antioxidant; phytochemical assay.
Resumen: Se seleccionó veintiocho plantas nativas usadas principalmente para tratarcurar enfermedades relacionadas principalmente con
infecciones microbianas y desordenes oxidativos. A estas plantas se para ser evaluóados en su actividad antimicrobiana sobre E. coli, P.
auriginosa, S. aureus, B. subtilis, y C. albicans usando métodos de difusión y microdilución. Se determinó la actividad antioxidante
mediante el ensayo del libre radical DPPH y se realizó la evaluación fitoquímica de las plantas con actividades promisorias. Veinte siete
plantas mostraron actividad antibacteriana, cuatro mostraron actividad anti-Candida, y cuatro actividad antioxidante. Oreocallis grandiflora,
Gentianella weberbaueri, Gamochaeta americana, Hypericum laricifolium, Loricaria ferruginea, Muehlenbeckia volcanica, y Oenothera
multicaulis mostraron actividad biológica promisoria, y se encontró que contienen alcaloides, compuestos fenólicos, flavonoides, taninos
gálicos y catecólicos. Este estudio deja evidencia del potencial medicinal de las plantas silvestres alto andinas; por lo tanto, los estudios
farmacológicos, fitoquímicos, ecológicos y biotecnológicos contribuirían en la promoción de su conservación y uso sustentable debido a su
alta vulnerabilidad y riesgo de extinción.
Palabras clave: Cordillera Blanca; planta Andina; antibacteriano; anti-Candida; antioxidante; ensayo fitoquímico.
Recibido | Received: August 6, 2017
Aceptado | Accepted: January 14, 2018
Aceptado en versión corregida | Accepted in revised form: April 12, 2018
Publicado en línea | Published online: May 31, 2018
Declaración de intereses | Declaration of interests: this research was financially supported by the Dirección General de Investigación (DGI) of the Universidad Nacional Santiago
Antúnez de Mayolo (UNASAM-Perú) as a component of the project “Caracterización biológica, fitoquímica y molecular de plantas Peruanas altoandinas con potencial en la industria
farmacológica”
Este artículo puede ser citado como / This article must be cited as: C Tamariz-Angeles, P Olivera-Gonzales, M Santillán-Torres2. 2018. Antimicrobial, antioxidant and
phytochemical assessment of wild medicinal plants from Cordillera Blanca (Ancash, Peru). Bol Latinoam Caribe Plant Med Aromat 17 (3): 270 – 285.

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/271
INTRODUCTION
Facing an increased demand for new bioactive
principles to cure new and emergent diseases
secondary metabolites from plants are being explored
continuously. Nowadays pathogen microorganisms
have the ability to develop resistance to conventional
antibiotics (Abedini et al., 2014; Guil-Guerrero et al.,
2016), therefore, new antimicrobial compounds
become necessary to fight the prominent microbial
infections (Aumeeruddy-Elalfi et al., 2016); which can
be achieved by focusing in plants used in traditional
medicine (Aumeeruddy-Elalfi et al., 2016; Gupta et al.,
2016; Chander et al., 2016). It seems that plants have
different mechanisms for microbial growth inhibition
compared to microbial or synthetic origin antibiotics,
furthermore it seems that pathogen microorganisms
do not develop resistance to antimicrobial compounds
from plants (Abedini et al., 2014).
Likewise, within the cells oxidative stress
generates free radicals (ROS) that degrade proteins,
lipids and DNA (Jayathilake et al. 2016); this damage
is associated with neurodegenerative and coronary
diseases, diabetes, atherosclerosis, inflammation,
digestive system disorders, viral infections, and
cancer (Tauchen et al., 2016; Al-Jaber et al., 2011;
Jayathilake et al., 2016). Cells produce antioxidant
substances for its self-protection, but when this
activity is low or the oxidative stress increases, it is
recommended the consumption of antioxidant
substances commonly provided by food and
medicinal plants (Jayathilake et al., 2016); usually
these plant antioxidant metabolites are polyphenols
(Al-Jaber et al., 2011).
Therefore, the knowledge of medicinal plants
as a source of bioactive principles provides great
opportunities for the development of new medicines
(Barboza et al., 2009; Rehecho et al., 2011; Chander
et al., 2016). Ethnopharmacology studies in Andean
zones report a wide diversity of plants used to treat
different ailments (Rojas et al., 2003; De-la-Cruz et al.,
2007; Bussmann et. al., 2010; Rehecho et al., 2011;
Gonzales De La Cruz et al., 2014), including some
diseases related to microbial infections and oxidative
stress. The Cordillera Blanca in Ancash has a
representative biodiversity of high-Andean Peruvian
ecosystems from which wild medicinal plants are
extracted and marketed. Most of them are herbaceous
and are collected with roots and flowers generating
risks of extinction by over exploitation such as
Muehlenbeckia volcanica, Perezia coerulescens,
Perezia multiflora, Perezia pinnatifida, Senecio
canescens, Senecio rhizomatus, Stangea sp. (De-la-
Cruz et al., 2007; Gonzales De La Cruz et al., 2014).
In addition, the climate change is making the high-
Andean biodiversity conservation problem bigger,
because it increases the vulnerability and
irreplaceability of the biodiversity of the high-
Andean ecosystem represented by small populations
of endemic species (Ramirez-Villegas et al., 2014);
therefore conservation effort should take place urgently
in order to protect most vulnerable species (Gonzales De
la Cruz et al., 2014). Some studies to perform in vitro
culture techniques to protect these genetic resources
were described only to Perezia coerulescens (Olivera et
al., 2010), O. grandiflora (Olivera-Gonzales et al.,
2017a), and P. pinnatifida (Olivera-Gonzales et al.,
2017b); but in this panorama, studies of their
pharmacological activities, phytochemical composition,
and even less genetic authentification are not considered
as a urgent topic to study.
Hence, this research is focused in medicinal
wild plants from the Ancash high Andean zone. The
antimicrobial activity was evaluated against four
bacteria and one yeast involved in common infections
illnesses such as respiratory, skin, urinary, stomach,
etc.. Their antioxidant activity was also screened, and
phytochemical studies began. The results support
other studies, which aim to promote biotechnological
applications for the conservation and sustainable use
of these threatened plants.
MATERIALS AND METHODS
Plant material
Some wild plants mostly used to treat diseases related
to microbial infections were selected. Most were
collected from or around the Huascaran National
Park located in Cordillera Blanca (Ancash-Peru); and
a few were bought at popular market from Huaraz.
Other criteria of selection were vulnerability, risk of
extinction and/or endemism. The taxonomic
identification and storage of herbarium specimens
(samples with flowers) were made at the David Smith
Herbarium of the Universidad Nacional Santiago
Antúnez de Mayolo
Http://grbio.org/institution/uiversidad-nacional-
santiago-antunez-de-mayolo) In addition, little
piece of dried leaves were stored at -70° C for future
DNA barcoding preparation.
Plant extracts preparation
Plant extract preparation was performed according

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/272
Martin et al. (1965) and Cáceres (1996). The plants
were washed with tap water and dried under fresh air
and shade. The dried samples were milled and sieved
up to 2 mm. After that, they were macerated with
ethanol 50º (10:90 w/v) under darkness and room
temperature (18-22° C) for 12 days to attain
maximum extraction. The samples were filtered on
filter paper followed by sterilization using 0.2 μm
millipore filter, and the extracts were concentrated
using rotavapor (Buchi, Switzerland) up to 40° C, and
left at 4° C for 10 days to achieve complete dryness.
Dry extracts were dissolved at 100 mg·mL-1
using DMSO and water in the relation 1:24. These
stock extract dilution were used in antimicrobial and
antioxidant assays immediately or were stored at 4 °C
for 14 days as a maximum. These stocks were diluted
in culture medium (antimicrobial microdilution
assay) or methanol (antioxidant assay). For the
antimicrobial diffusion method, in order to
standardize amount (mg) of extract by filter paper
disk and considering that they are crude extract. Filter
paper disks impregnated with 2 mg of plant extract
were prepared in the following way: 20 µL (4 µL x 5
times) of extracts were soaked in sterile filter paper
disks of 5 mm and dried in a sterile chamber for 1
hour. The amount of tetracycline, streptomycin or
nystatin by each filter paper disk was 0.2 or 1.6 mg
respectively, since they showed good inhibition halos
between 10 - 25 mm against the strains tested.
Antibacterial activity
E. coli ATTC25922, S. aureus ATCC25923, B.
subtilis ATCC11774, and P. aeruginosa ATCC27853
were tested by diffusion and microdilution methods
according to M02-A7 and M07-A8 protocols of the
Clinical and Laboratory Standards Institute (CLSI).
In both methods, the initial inoculum (IIB)
was made with two colonies from a 14 hours grown
plate diluted in NaCl 0.8% until 0.08 - 0.1 OD620.
Streptomycin (Sigma) and tetracycline (Sigma) were
used as standard antibiotics. Three replicates per test
were performed, and the reproducibility was
evaluated two times.
Antibacterial diffusion assay
The IIB was done by swabbing it twice onto 12 x 12
cm Petri dishes (Sigma) containing 40 mL of Müller
and Hinton Agar (MHA, Merck), and immediately
filter paper disks soaked with a sample or standard
antimicrobial solutions were placed on the inoculated
Petri dishes. The sample disk contained 2 mg of
sample or 0.2 mg of standard antibiotic. Plates were
incubated for 24 hours at 35° C. The inhibition halos
were measured subtracting the disk diameter; then
values ≥ 2 were considered as inhibition.
Antibacterial minimum inhibitory concentration
(MIC) using tetrazolium salt
Extracts were serial diluted in Müller and Hinton
Broth II (MHBII, Difco) at 0.10, 0.25, 0.50, 0.75,
1.00 to 10.00 mg·mL-1 (increasing 0.50). The serial
dilutions were dispensed into 96-well plates (100 µL
per well) and were inoculated with 10µL of IIBd (IIB
diluted in MHBII 1:20). Controls of growth (MHBII
with inoculum) and contamination (MHBII or
extracts without inoculum) were prepared. Plates
were incubated for 24 hours at 35° C. Tetrazolium
salt was used as growth indicator (Ncube et al., 2008;
Klančnik et al., 2010); adding 10 μL of tetrazolium
violet 0.1% (TV, Sigma T0138) to each well and
incubated for 4 hours at 35° C under dark. TV is
reduced to violet precipitated, in presence of
respiratory activity. MICs were considered like the
lowest concentrations of extracts that inhibited the
bacterial growth that was noticed by the absence of
violet precipitated.
Anti-Candida activity
The susceptibility of C. albicans ATCC90028 was
evaluated by diffusion and microdilution methods
according to M44-A and M27-2A (CLSI) protocols
with few modifications. Nystatin (commercial
suspension) was used as an antifungal standard.
Three replicates per test were performed and the
reproducibility was evaluated two times. Preparation
of initial inoculum (IIY) was similar to antibacterial
assay.
Anti-Candida diffusion assay
IIY was done by swabbing it twice onto 12 x 12 cm
Petri dishes with TSA and continued as described
previously for the Antibacterial diffusion assay.
Incubation was for 48 hours. The sample disk
contained 2.0 mg, and the nystatin disk had 1.6 mg.
Anti-Candida MIC using tetrazolium salt
Extracts were serial diluted in TSB at 0.2, 0.5, 1.0,
1.5, 2.0 to 20.0 mg·mL-1 (increasing 1.0). The serial
dilutions were dispensed into 96-well plates (100 μL
per well) and inoculated with 100 μL of IIYd (IIY
diluted in TSB 1:5). Controls of growth and
contamination were prepared. Plates were incubated

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/273
at 35° C for 48 hours, and MICs were obtained as
described in Antibacterial minimum inhibitory
concentration (MIC) assay.
Antioxidant activity tested by DPPH scavenging
method
Microdilution method described by Guaratini et al.
(2012) was used, and ascorbic acid was used as a
standard. Extracts (100 mg·L-1) were serially diluted
with methanol at 25 to 2000 μg·mL-1. 100 µl of each
dilution was dispensed into six wells; immediately 10
μL of fresh DPPH (10 mg·L-1 dissolved in MeOH)
was added into three well, and 10 μL of MeOH into
the other three. Plates were incubated at 25° C in
darkness for 30 min. After, the absorbance at 517 nm
was measured twice in a microplate
spectrophotometer (BioTek, USA). The percentage of
radical inhibition per sample was calculated as % I =
[DPPHA - (MA-BMA)/DPPHA] x 100. Where
DPPHA is the DPPH absorbance, MA is the
absorbance of the sample plus DPPH, BMA is the
absorbance of the sample without DPPH.
The antioxidant activity was expressed as
IC50, which represent the extract concentration to
inhibit 50% of DPPH radical (Lee et al., 2003), and it
is calculated from the regression curve I% versus
extract concentration.
Phytochemical evaluation
Thin layer chromatography (TLC) and method
proposed by Lock (1994) were used for
phytochemical evaluation of samples leaf extracts
that gave the best results. The evaluation was
repeated twice and 250 mL of ethanol extracts
prepared as previously described, were used.
In the first method, 20 mL of ethanol extract
were separated (fraction A), and 230 mL were dried
and fractionated in 4 fractions (B, C, D, E)
considering pH, solubility, and polarity (Lock, 1994).
The presence of phenols, alkaloids, amino acids,
tannins, triterpenes and/or steroids,
leucoanthocyanidins, and quinones was evaluated
with color reactions.
TLC was developed on silica gel 60 F254,
Aluminum sheets (Merck), with BAW (n-butanol-
acetic acid-water) at ratios (3:1:3), (4:1:1), (4:1:3)
and (4:1:5). For the phenolic groups, the chromate
plates were evaluated without or with FeCl3 (1%) or
H2SO4 (1%) and were observed using white light,
UV254, and UV365; the retention factor (Rf) of the
separated compounds were calculated, color and
fluorescence were observed and compared with
literature (Wagner & Bladt, 1966; Harborne, 1984;
Lock, 1994; Galand et al., 2002). Similarly, alkaloids
were studied using Dragendorff reagent.
Statistical analysis
The antimicrobial and antioxidant assays were
performed using 6 replicates, and phytochemical
screening had 2 replicates. The results were
expressed as values, and standard deviations were
calculated. ANOVA and Duncan’s test were used to
compare the values of antimicrobial diffusion assay
and antioxidant DPPH scavenging method.
Table No. 1
Taxonomic, ethnopharmacology, market and endemism information of selected plants
N°
Scientific name, family, common
names*/used part in popular medicine*
Traditional medicinal use*
CS**
E
*
M
P
1
Alonsoa linearis (Jacq.) Ruiz & Pav.
Scrophulariacea
rirkacock, shoqumpa wëta, aturash, flor
de muerto, pillwi pillwi, rinriqora,
chanllillí ᶲ/whole plant
To cure stomach pain. It is used with other plants to
take baths against cold. (5, 6)
x
a
2
Baccharis genistelloides Pers.
Asteraceae
carqueja, kima esquina, cuchu-
cuchu/stem
To cure urinary, liver, and kidney problems; to treat
malaria, rheumatism, diabetes, and cholesterol.
Diuretic, antidiarrheal, and blood purification.(5, 6, 7)
x
a
3
Berberis lutea Ruiz & Pavon
Berberidaceae
chekci, qarwash casha, qontsi, qarwa
quinche, carhuascasa/fruit, root, leaf,
stems
As anti-inflammatory during respiratory tract, and
muscle pains. It is used as dye: the fruit (color blue)
and roots (color yellow). (4,6)
4
Buddleja incana Ruiz & Pav.
Scrophulariacea
To treat the Carrion disease (an endemic disease
caused by Bartonella bacilliformis), it is an astringent
x
a

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/274
quisuar, quishuar/leaf
to treat wart and to wash open sore. Leaf and barks
are rubbed on genitals in order to prevent postpartum
infections. It is used to take baths against cold. (4,5,6)
5
Gamochaeta americana (Mill) Wedd.
Asteraceae
alkupa allung, lengua de perro/leaf,
stem, flowers
Against cold, conjunctivitis, and diarrhea. (5, 10)
x
w
6
Gentianella weberbaueri (Gild) Fabris
Gentianacea
puca makashqa, puca shaqwa, puca
shaqapa, antenaria /whole plant
To prevent cavities. The flowers are collected to
decorate religious statues and the boiled extract is
used as red coloring. (6)
fᴪ
y
7
Hypericum laricifolium Juss.
Hypericaceae
chinchango, cypres, romero de la
altura/stem, leaf, flower
To cure warts, cold, chills, tiredness of all the body.
Antidepressant. (5,6)
x
a
8
Jungia paniculata (DC.) A. Gray
Asteraceae
matico, qaramati, caramate/leaf
For wound healing, injuries, stomach ulcers,
nephritis, hemorrhoids, vaginitis, urinary tract illness
and hurts. Antiseptic or antibiotic, and anti-
inflammatory. (4, 6, 8, 9)
x
a
9
Loricaria ferruginea (Ruiz & Pav.)
Wedd.
Asteraceae
wallpapa chaquin, pata de gallo/stem
To alleviate menstrual delay, and for blood
circulation. Steam mixed up with other plants is used
for bath to cold.
(2, 5, 6)
x
a
10
Lupinus weberbaueri Lubr.
Fabacea
taulli macho, tararwa /leaf
For stomach problems or ulcers, diabetes. The
flowers are collected to decorate religious statues. (5)
fᴪ
11
Muehlenbeckia volcanica (Benth) Endl.
Polygonaceae
mullaca , mullak´a, viruta,
mullaka/whole plant, fruit
For diarrhea, flu, asthma, other bronchia disorders,
stomach pain and “internal wounds” with
hemorrhage. Antipyretic, antitussive, analgesic and
antiseptic to treat throat infections. (4,5, 8)
x
w
12
Notrotice obtusa A. W. Hill
Malvacea
raíz de alte, qori waqaq, shiric-yalckoy,
tupucpa-ashuan/leaves, stem and flower
Leaves and flowers of Notrotiche sp. are used to
make a tea to treat colic. (6)
To kidney problemsᶲ.
x
w
y
13
Oenothera multicaulis Ruiz & Pavon
Onagraceae
chupasangre,tullpishᶲ/leaf
Wound healing, and antiseptic. (9)
x
w
14
Oreocallis grandiflora (Lam.) R. Br.
Proteacea
tzaq'pa, chacpá, cucharillo/flowers, leaf,
stem
To alleviate flu and strong sensation of cold, cough,
pain after hard work in the sun, headache, diabetes,
and fever. To cure liver and kidney problems. (5,10)
x
f
15
Peperomia hartwegiana Miq.
Piperacea
congona redonda ᶲ, congona,
winayquilla, congona /stem, leaf
To cure gingivitis and otitis; lung, liver and kidney
diseases, stomach ulcers, bruises. (5, 6)
x
a
16
Perezia coerulescens Wedd.
Asteraceae
valeriana, patza maki/root, rhizome
To alleviate heart pain. Sedative, diuretic, and
diaphoretic.
(4, 5)
x
w
17
Perezia multiflora (Bonpl.) Less
Asteraceae
escorzunera, chancoruma/leaf
Diuretic, febrifuge, sudorific, expectorant,
antitussive, analgesic, anti-inflammatory. To treat
back ache, stomach ache, flu, cough, bronchitis,
tuberculosis, and diarrhea. To cicatrize teeth and
throat injuries. (1, 4, 5, 6, 7)
x
w
18
Perezia pinnatifida (Bonpl.) Wedd.
Asteraceae
valeriana, contrahierba, valeriana
fina/leaf, root, rhizome
To treat asthmatic cough, headache, and heart
disorders. Central nervous system stimulant,
antitussive, sedative, tonic, tranquilizer. (4, 6)
x
w
19
Senecio calvus Cuatrec.
Asteraceae
Huamamrripa, vira vira/leaf
For cough, respiratory sickness, and it is used in bath
against cold. (4, 5)
x
w
y
20
Senecio canescens (Bonpl.) Cuatr.
Sudorific, expectorant, antipyretic. To treat bronchia
x
w

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/275
Asteraceae
ancosh, anqush, wila-wila, oreja de
venado, utco, oreja de conejo/leaf
disorders, flu, asthma, cough and cold. (2, 4, 6, 7, 8)
21
Senecio leucophorbius Cuatr.
Asteraceae
Used as S. canescens because it have similar
morphology. (1)
y
22
Senecio rhizomatus Rusby
Asteraceae
llancahuasᶲ, llancahuasa/leaf
For liver colic, and kidney infection. (4)
x
w
23
Senecio serratifolius (Meyen & Wapl.)
Cuatrec.
Asteraceae
wamanripa /leaf, flowers
For pneumonia. (6)
24
Valeriana henrici (Graebn.) B. Eriksen
Caprifoliaceae
corehuajay, qallu-qallu, llingli-llingli,
rosetón/whole plant
To alleviate heart pain, “mal aire”, and nauseas. (5,6)
x
w
25
Valeriana aff. pycnantha A. Gray.
Caprifoliaceae
Siete sabiosᶲ/whole plant
To alleviate heart pain ᶲ
x
w
26
Valeriana globularis A. Gray.
Caprifoliaceae
Siete sabios/whole plant
Its roots are eaten. (6)
To alleviate heart painᶲ.
x
w
27
Werneria nubigena Kunth.
Asteraceae
yekishkoda, patzamaki/leaf, root
For cold, and diarrhea. (5)
28
Xenophyllum dactylophyllum (Sch. Bip.)
V.A. Funk
Asteraceae
cuncush, peqa-peqa, botón-botón/stem
For head ache. It is used with other plants. (6)
x
a
*, it was done with literature references: (1) Beltrán et al. (2006), (2) Bussman et al. (2010), (3) Ccana-
Ccapatinta et al. (2014), (4) De-la-Cruz et al. (2007), (5) Gonzales De La Cruz et al. (2014), (6) Kolff & Kolff
(2005), (7) Monigatti et al. (2013), (8) Rehecho et al. (2011), (9) Rojas et al. (2003), (10) Tene et al. (2007).
ᶲAuthor observation from Huaraz traditional markets.
**, commercial status (CS) observed in traditional markets from Huaraz. M, observed in traditional markets
from Huaraz: x, presence in traditional markets. P, part of the plant collected and marketed to diverse use:
a, aerial part containing stem, leaves and flowers; f, only flower; w, whole plant; ᴪ, collected but not
marketed. E, endemic from Peru: y, positive answer.
Table No. 2
Collection data of specimen plants selected
N°
Species
Sample ID
Collection
Date
Collection place
Sector
Latitude
Longitude
Elevation
1
Alonsoa linearis
UNASAM
-HDS-127
14/06/14
Qda. Quillcayhuanca
-9.50447
-77.44772
3850m
2
Baccharis
genistelloides
UNASAM
-HDS-104
10/06/13
Qda. Huaripampa
-8.95068
-77.56283
3751 m
3
Berberis lutea
UNASAM
-HDS-118
29/09/13
Qda. Llanganuco
-9.04832
-77.60837
3953 m
4
Buddleja incana
UNASAM
-HDS-128
22/09/13
Qda. Shallap
-9.50106
-77.36886
4137 m
5
Gamochaeta
americana
UNASAM
-HDS-105
14/05/15
Marketed
6
Gentianella
weberbaueri
UNASAM
-HDS-121
23/01/13
Qda. Churup
-9.47707
-77.42478
4570 m
7
Hypericum laricifolium
UNASAM
-HDS-119
15/06/14
Qda. Quillcayhuanca
-9.50604
-77.44159
3861m
8
Jungia paniculata
UNASAM
-HDS-106
24/06/13
Road to Pitec, Huascaran
National Park
-9.51771
-77.48164
3392m

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/276
9
Loricaria ferruginea
UNASAM
-HDS-107
29/09/13
Portachuelo from
Llanganuco
-9.04041
-77.57577
4403 m
10
Lupinus weberbaueri
UNASAM
-HDS-120
22/09/13
Qda. Shallap
-9.49495
-77.36011
4246 m
11
Muehlenbeckia
volcanica
UNASAM
-HDS-125
29/09/13
Portachuelo from
Llanganuco
-9.04492
-77.59792
4443 m
12
Nototriche obtusa
UNASAM
-HDS-122
10/06/13
Punta Unión, between Qda.
Huaripampa-Santa Cruz
-8.91228
-77.58159
4735 m
13
Oenothera multicaulis
UNASAM
-HDS-123
12/01/15
Aquia
-10.0759
-77.14399
3409m
14
Oreocallis grandiflora
UNASAM
-HDS-126
30/09/13
Qda. Llanganuco
-9.10854
-77.68562
3420m
15
Peperomia
hartwegiana
UNASAM
-HDS-124
22/09/13
Qda. Shallap
-9.50209
-77.37635
4128 m
16
Perezia coerulescens
UNASAM
-HDS-108
13/12/13
Qda. Churup
-9.47619
-77.42422
4695 m
17
Perezia multiflora
UNASAM
-HDS-109
11/06/13
Path to Alpamayo, Qda.
Santa Cruz
-8.90928
-77.62427
4201 m
18
Perezia pinnatifida
UNASAM
-HDS-110
24/04/14
Marketed
19
Senecio calvus
UNASAM
-HDS-111
29/09/13
Portachuelo from
Llanganuco
-9.04641
-77.59298
4597 m
20
Senecio canescens
UNASAM
-HDS-112
10/06/13
Punta Unión, between Qda.
Huaripampa-Santa Cruz
-8.91228
-77.58159
4735 m
21
Senecio leucophorbius
UNASAM
-HDS-113
11/06/13
Path to Alpamayo, Qda.
Santa Cruz
-8.89591
-77.63219
4293 m
22
Senecio rhizomatus
UNASAM
-HDS-114
29/09/13
Portachuelo from
Llanganuco
-9.04041
-77.57577
4403 m
23
Senecio serratifolius
UNASAM
-HDS-115
05/01/13
Qda. Ulta
-9.12989
-77.51445
4864 m
24
Valeriana aff.
pycnantha
UNASAM
-HDS-130
13/12/13
Qda. Churup
-9.47650
-77.42436
4680 m
25
Valeriana globularis
UNASAM
-HDS-131
27/05/16
Marketed
26
Valeriana henrici
UNASAM
-HDS-129
27/01/16
Marketed
27
Werneria nubigena
UNASAM
-HDS-117
10/06/13
Qda. Huaripampa
-8.95067
-77.56283
3751 m
28
Xenophyllum
dactylophyllum
UNASAM
-HDS-116
10/06/13
Punta Unión, between Qda.
Huaripampa-Santa Cruz
-8.91228
-77.58159
4735 m
Qda. quebrada. Collectors were C.Tamariz & P. Olivera
RESULTS
Plant material
According to the ethnopharmacology information
twenty-eight plants of twelve families were selected.
Then, twenty four were collected and four were
bought at Challhua, a popular market from Huaraz
(Tables No. 1 & 2 and Figure No. 1). Most species
are used for flu, some for urinary diseases, dental
cleaning, wounds or stomach pain. A few are used for
diseases related to oxidative stress such as diabetes,
heart pain or nerves. From observation in traditional
markets from Huaraz, thirteen species are marketed
as whole plant, from which P. coerulescens, P.
pinnatifida, N. obtusa, V. henrici, V. aff. pycnantha
are considered highly vulnerable because they are
collected with lots of flowers and sailwomen refer
that they are collected from places near the glaciers.
About endemisms, four plants are endemic (Table
No. 1). Additional, the flowers of G. weberbaueri, L.
weberbaueri, and O. grandiflora are used as
ornamental. This last one is marketed, and other two
are used to decorate statues in Holy week.

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/277
Figure No. 1
Map of the collection area. Numbers are the samples are in the Table No. 2
Antibacterial activity
The size of the clear zone of growth inhibition (halo)
and MICs are shown in Table No. 3. Two plants (M.
volcanica and O. grandiflora) showed activity
against the four bacteria tested, three against three
bacteria (H. laricifolium, L. ferruginea, and O.
multicaulis), 17 plants against two bacteria, three
against one bacterium tested, and only one plant did
not show activity.
In the diffusion test against S. aureus, the
statistic test showed that 2 mg·L-1 ethanolic extracts
activity of B. incana, G. americana, A. linearis, O.
multicaulis, O. grandiflora did not have a significant
difference with 0.2 mg·L-1 streptomycin, it means that
these extracts have the same activity that streptomicin
at the condition descripted. In this way, the activity of
P. hartweguiana (2 mg·L-1) against B. subtilis did not
show a statistic difference with tetracycline (0.2
mg·L-1), this activity was followed by S. rhizomatus,
O. multicaulis, L. ferruginea, and others.
It was found that positive results in the
diffusion test were also positive in the dilution
method with exception of a few extracts (7, 11, 14),
and this could be related to the bioactive metabolite
solubility involved in the antibacterial effect. Then,
considering the two methods, three (9, 11, 14) and
four (7, 11, 13, 14) plants had antibacterial activities
against E. coli, and P. aeruginosa respectively. In the
disk diffusion assay against E. coli only two (9, 14)
extracts were positive, but their activities was low
compared to standard antibiotics used. Interestingly,
2 mg·L-1 of O. grandiflora extract showed better
inhibition halo than 0.2 mg·L-1 tetracycline against P.
aeruginosa.

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/278
Finally, according to diffusion assay, low
MICs and/or a broad spectrum of antibacterial
activity were found for H. laricifolium, L. ferruginea,
O. grandiflora, M. volcanica, and O. multicaulis.
Anti-Candida activity
The antifungal activity against C. albicans was
uncommon in the plants tested; only G. weberbaueri,
L. ferruginea, and O. multicaulis showed anti-
Candida activities using the dilution and diffusion
methods, while X. dactylophyllum had a slightly
positive activity with the diffusion method (Table No.
3).
Antioxidant activity
Table No. 3 shows the IC50 of antioxidant activity
using DPPH scavenging assay, values and the
statistic test was made only to samples which showed
IC50 less than 300 µg·L-1; values ≥ 300 µg·L-1 are not
reported. The lowest IC50 values were found in leaves
and stems of H. laricifolium (55.6 ± 2.4 and 62.3 ±
2.0 µg·L-1), and leaves of G. americana (65.4 ± 12.1
µg·L-1); followed for M. volcanica (98.7 ± 3.1 µg·L-1)
and leaves of O. grandiflora (113.5 ± 4.4 µg·L-1).
These plants are considered promissory to continue
research.
Phytochemical evaluation
In concordance to the antimicrobial and antioxidant
results, O. grandiflora, H. laricifolium, G.
weberbaueri, G. americana, L. ferruginea, M.
volcanica, and O. multicaulis were selected for
phytochemical evaluation. Following Lock (1994)
method, the tannins were present in the majority of
plants, flavonoids and leucoanthocyanidins were also
abundant. Alkaloids were found in five plants,
triterpenes and/or steroids in four, amino acids in
three, and quinones only in one (Table No. 4). In the
TLC method, BAW (4:1:5) was the best mobile
phase and was selected to all assays. According to the
different retention factor (Rf), color and fluorescence
of the different TLC treatments with or without
FeCl3 or H2SO4 for phenolic compounds and
Dragendorf for alkaloids; it was possible to
differentiate some types of tannins, flavonoids,
alkaloids and other phenolic compounds for each
sample (Table No. 5). Both methods assayed were
complementary, and did not show contradictory
results.
DISCUSION
Most of plants selected (96%) showed antibacterial
activity at least against one bacterial strain tested
supporting the importance and usefulness of the
ethnobotanical information about plants that cure
infection during research of new antimicrobial
compounds. The anti-Candida activity is consider as
an urgent need to explore in active constituents of
traditional medicine, because candidiasis of the skin,
nails, oral cavity, esophagus and vagina is the most
prevalent fungal infection; (Tangarife-Castaño et al.,
2011; Zida et al., 2017) and four plants (14%)
showed this activity; correlation with their traditional
uses are discussed below. On the other hand, four
species (5, 7, 11, 14) showed promising antioxidant
activity; this activity could be helpful in the case of
diseases caused by oxidative stress such as cancer,
diabetes, and neurodegenerative problems (Tauchen
et al., 2016) but other assays to confirm this activity
could be necessary. Although most of the plants
showed antimicrobial activities, the discussion is
focusing mainly in the plants with promising results.
Table No. 3
Antimicrobial and antioxidant activities of ethanolic extracts of medicinal plants
N°
Species
PE
Antimicrobial activity
Diameter inhibition halo* mm, (MIC mg·mL-1)
DPPH activity
IC50
µg·L-1
Sa
Bs
Ec
Pa
Ca
1
A. linearis
l
15.5 ± 2.1bcd
(2.5)
5.5±0.7ef
(2.5)
274.2 ± 17.0g
s
8.5±0.7gh
(3.0)
4.5±2.1efgh
(3.0)
2
B. genistelloides
s
4.5±0.7ijkl
(4.0)
3.5±0.7efgh
(4.0)
3
B. lutea
l
7.0±1.4hi
(7.5)
3.5±0.7efgh
(5.0)
202.2 ± 8.5d
4
B. incana
l
16.5±0.7bc
(3.0)

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/279
5
G. americana
l
15.5±0.7bcd
(2.5)
2.5±0.7gh
(3.5)
65.4 ± 12.1b
6
G. weberbaueri
l
6.0±1.4hijk
(3.0)
4.0±1.4efgh
(3.0)
3.0±0.0d
(8.0)
236.4 ± 1.9fg
r
6.5±0.7hij
(2,5)
4.5±2.1efgh
(3.0)
8.0±0.0bc
(5.0)
282.6 ± 15.9e
7
H. laricifolium
l
8.5±0.7gh
(0.5)
4.0±1.4efgh
(0.5)
0.0
(8.0)
55.6 ± 2.4b
s
7.0±1.4hi
(0.4)
5.0±1.4efg
(1.0)
0.0
(8.0)
62.3 ± 2.0b
8
J. paniculata
l
6.0±2.8hijk
(3.0)
2.5±0.7gh
(9.0)
9
L. ferruginea
l+s
13.5±0.7cdef
(2.5)
6.0±1.4e
(3.0)
3.5±0.7d
(>10)
8.0±0.0bc
(8.0)
10
L. weberbaueri
l
11
M. volcanica
l+s
3.0±0.0ijkl
(2.0)
0.0
(3.0)
0.0(8.0)
7.0±0.0d
(8.0)
98.7 ± 3.1c
12
N. obtusa
l
3.5±0.7ijkl
(7.5)
4.5±2.1efgh
(3.0)
s
1.5±0.7l
(>10.0)
3.5±0.7efgh
(5.0)
13
O. multicaulis
l
15.0±2.8bcde
(2.0)
9.5±0.7d
(1.5)
0.0
(8.50)
8.0±1bc
(1.0)
r
4.0±1.4ijkl
(2.0)
9.5±0.7d
(5.5)
4.0±0.7d
(9.0)
7.0±1c (1.5)
14
O. grandiflora
l
15.0±1.4bcde
(1.5)
2.5±0.7gh
(2.5)
5.0±0.0c
(8.0)
15.0±1.4b
(1.5)
113.5 ± 4.4c
15
P. hartwegiana
l+s
7.0±0.0hi
(2.0)
16.5±0.7bc
(3.0)
16
P. coerulescens
l
2.5±0.7kl
(>10)
4.5±0.7efjh
(5.5)
rh+
r
6.5±0.7hij
(>10)
4.5±0.7efgh
(3.0)
17
P. multiflora
l
2.5±0.7gh
(7.0)
18
P. pinnatifida
rh+
r
2.5±0.7kl
(>10)
4.5±0.7efgh
(3.0)
19
S. calvus
l
12.0±2.8ef
(5.0)
2.0±0.0h
(>10)
20
S. canescens
l
5.5±2.1hijk
(5.0)
0.0
(8.0)
21
S. leucophorbius
l
11.0±2.8fg
(>10)
22
S. rhizomatus
l
4.5±0.7ijkl
(>5.0)
14.5±0.7c
(3.0)
23
S. serratifolius
l
4.5±2.1ijkl
(8.5)
0.0
(8.0)
24
V. henrici
l+r
0.0
(8.0)
25
V. aff. pycnantha
l+r
6.5±2.1hij
(3.0)
3.0±0.0fgh
(1.5)
26
V. globularis
l
6.0±1.4hijk
(5.5)
0.0
(3.0)
27
W. nubigena
l+r
3.0±0.0jkl
(4.0)
3.0±0.0fgh
(6.0)
28
X. dactylophyllum
l+s
12.5±2.1def
(2.0)
4.5±0.7efgh
(2.0)
9.0±1.0b
(>10)
Tetracycline
20,0±1,4ab
18.5±2.1b
15.5±0.7b
13.0±0.0c

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/280
(<0.02)
(<0.02)
(<0.02)
(<0.02)
Streptomycin
17,5±0,7a
(<0.02)
25.5±0.7a
(<0.02)
20.0±0.0a
(<0.02)
17.5±0.7a
(<0.02)
Nystatin
11.0±1.4a
(>1.0)
Ascorbic acid
22.6 ± 0.3a
PE, part of plant used to prepare the extract; l, leaf; s, stem; r, root; rh, rhizome; f, flower; w, whole plant.
Sa, S. aureus; Bs, B. subtilis; Ec, E. coli; Pa, P. aueriginosa; Ca, C. albicans.
*, inhibition halo was calculated minus 5 mm (filter paper disk).
Values ± standard deviation, and letters as super index correspond to statistic group according to Duncan’s
test (p<0.05).
Table No. 4
Phytochemical composition using Lock (1994) method
Type of secondary
metabolite
Color reagent
Plants
Ogl
Hll
Gwl
Gal
Lfa
Mva
Oml
Alkaloid
Dragendorff Mayer
x
x
x
x
x
Tannin
Gelatin
x
x
x
x
x
x
Phenolic compound
FeCl3
x
x
x
x
x
x
x
Flavonoid
Shinoda
x
x
x
x
x
Leucoanthocyanin
Rosenheim
x
x
x
Triterpen and/or steroid
Lieberman-Buchard
x
x
x
x
Quinone
Bortranger
x
Og, O. grandiflora; Hl, H. laricifolium; Gw, G. weberbaueri; Ga, G. americana; Lf, L. ferruginea; Mv, M.
volcanica; and Om, O. multicaulis. l, leaves; a, whole aerial part.“x” represent the presence of the secondary
metabolite
H. laricifolium is a shrub that grows in the
high Andean areas from Venezuela, Ecuador, and
Peru (Crockett et al., 2010). Some Hypericum species
are well known for their medicinal properties (Cirak
et al., 2017), and H. laricifolium is used mainly to
treat cold, wart, and as an antidepressant (Table No.
1). Their leaves and stems showed activities against
P. aeruginosa, B. subtilis, and S. aureus. The latter
activity was also reported for ethanolic, methanolic
and chloroformic extracts of samples from other
regions (Bussmann et. al., 2010; Jerves-Andrade et
al., 2014). Antibacterial compounds of H.
laricifolium have not still been determined; but
tetraketone and hyperforin were isolated from H.
perfolatum had antibacterial and antidepressant
activities (Saddiqe et al., 2010). Some Hypericum
species are known for their antioxidant property
(Kızıl et al., 2008; Boga et al., 2016), and H.
laricifolium showed antioxidant activity with DPPH
assay. In their phytochemistry, Hypericum species
contain phenolic, flavonoids and tannins compounds,
which would be responsible for their cytotoxic,
antitumor, and anti-inflammatory properties (Boga et
al., 2016); in concordance, H. laricifolium has
phenolic compounds especially flavonoids and gallic
tannins. Likewise, its leaves contain caffeic acid (El-
Seedi et al., 2003) which is a potent antioxidant
(Gülçin, 2006); acylphloroglucinol derivatives
(Ccana-Ccapatinta & von Poser, 2015) which are
associated with antitumor, antibacterial, and anti-HIV
activities of H. sampsonii (Zhu et al., 2015). Also, H.
laricifolium inhibited a proliferative growth of Hep3
cells (Carraz et al., 2015), but the compounds
involved in this effect are not described yet.
O. grandiflora is a tree that grows in the
Peruvian inter-Andean valleys between 1500-4000
m.a.s.l. (Reynel & Marcelo, 2009), and some areas
from Ecuador (Alejandro-Espinosa et al., 2013). It is
used to treat cold and fever (Tene et al., 2007;
Gonzales De La Cruz et al., 2014); and it has shown
a broad spectrum of antibacterial activity, where the
halos size against S. aureus and P. aeruginosa were
similar to reference antibiotic halos. Likewise, O.
grandiflora has shown antioxidant activity, possibly
by the presence of phenolic compounds such as
catecholic tannins and flavonoids found in its

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/281
phytochemical evaluation. It is used to treat diabetes
(Gonzales De La Cruz et al., 2014), which could be
related to its antioxidant activity; however,
Alejandro-Espinosa et al. (2013) have found that O.
grandiflora leaves inhibited α-amylase and β-
glucosidase as a hypoglycemic activity mechanisms,
and showed antioxidant activity using DPPH assay.
About its conservation status, Pretell et al. (1985)
consider that O. grandiflora is an endangered species
in Peru due to its irrational use; besides it is being
displaced from its habit by exotic and agricultural
forest species; thus, Olivera-Gonzales et al. (2017a)
have performed a methodology for O. grandiflora in
vitro propagation such as an alternative for its
conservation.
Table No. 5
Phytochemical evaluation using TLC with reagent and detection method
Plant
Alkaloid
Type of tannins
Type of flavonoid (number)
Other phenolic
compound
Ogl
2
catechol (1)
flavanonol, flavone, flavonone or isoflavone
(3); anthocyanin (1)
2
Hll
3
catechol (3)
flavone, isoflavone or flavonol (6)
4
Gwl
2
-
flavone, isoflavone or flavonol (5)
2
Gal
2
catechol (2)
flavanone or flavone (2)
4
Lfa
3
catechol (1)
flavanone or flavone (2)
6
Mva
3
catechol (1)
flavone, flavonol or flavanone (3)
4
Oml
1
gallic acid (1)
flavonol, flavone or chalcone (2)
1
Og, O. grandiflora; Hl, H. laricifolium; Gw, G. weberbaueri; Ga, G. americana; Lf, L. ferruginea; Mv, M.
volcanica, and Om, O. multicaulis. l, leaves; a, whole aerial part.
G. weberbaueri is a herb that is an endemic
plant from Ancash (Peru) that grows between 3900 to
5100 m a. s. l., and it is in vulnerable status (Castillo
et al., 2006). It is used to avoid cavities (Kolff &
Kolff, 2005), and we observed antimicrobial activity
against S. aureus, B. subtilis, and C. albicans,
remarking that C. albicans is a yeast involved in
dental infections (de Oliveira et al., 2013). No other
medicinal uses have been reported, interestingly G.
weberbaueri has shown antioxidant activity. Other
Gentianella species are used to treat diabetic, liver
and depurative disorders (Li et al., 2010; Gonzales de
la Cruz et al., 2014); and according to the
phytochemical and ethnopharmacology review of
Gentianella this genus is considered as a great source
of medicinal plants characterized by the presence of
xanthones, C-glucoflavonoids, and terpenoids, which
are probably responsible for their biological activity
(Li et al., 2010). The phytochemical evaluation has
found alkaloids, phenolic compounds, flavonoids,
and triterpenes and/or steroids in its leaves, but
studies about this plant are scarce.
G. americana is a herb with a wide
distribution in Central and South America; in Peru, it
grows in different habitats (Dillon & Sagástegui,
1991) mainly as weed. In traditional medicine, it is
used as an antiseptic and for this reason is named
commonly "alkupa allung", which means "dog's
tongue"; it is also used to alleviate diarrhea (Gonzales
De La Cruz et al., 2014). In agreement with previous
ethnopharmacology studies, G. americana showed
good antibacterial activity against B. subtilis and S.
aureus, being the last a common pathogen of purulent
infections (Lima et al., 2016). Both bacteria could be
involved in diarrheal processes. Although G.
americana is not used for chronic diseases, it showed
good antioxidant activity (IC50 65.4 ± 12.1 µg·L-1).
The phytochemical evaluation revealed the presence
of alkaloids, tannins, catechol, flavonoids and
phenolic compounds.
M. volcanica grows between 1500 - 4500
m.a.s.l. from Mexico to Bolivia (Heim, 2014). It
showed broad activity against gram positive and
negative bacteria, which could be in agreement with
its traditional use as antiseptic and anti-diarrheal
(Rehecho et al., 2011). It also showed good
antioxidant activity and could be due to the presence
of phenolic compounds such as catechol. Despite its
wide distribution, it has been categorized as
endangered species in Canta - a Peruvian Andean

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/282
province - because it is highly collected without agro-
ecological study for its conservation and sustainable
use (De-la-Cruz et al., 2007).
O. multicualis inhibited the growth of B.
subtilis, S. aureus, P. aeruginosa, and C. albicans,
such as reported Rojas et al. (2003). Furthermore, the
last three bacteria are related to skin infections (Lima
et al., 2016), which could explain its usefulness as an
antiseptic (Table No 1). O. multicaulis has shown the
presence of tannins, phenolic compounds, flavonoids,
triterpenes and/or steroids, quinones and amino acids;
with exception of the two last compounds all were
described in other Oenothera species (Festa et al.,
2015). Likewise Srivastava et al. (2007) isolated
oenosyticin - a potent metabolite against S. aureus
and S. epidermidis - from O. biennis; but no more
phytochemical research was found for the family. O.
multicualis is widely distributed from Ecuador to
Bolivia; however, the whole plant is collected
identifying it as a probably threatened species.
L. ferruginea is a shrub that grows from
Central Ecuador - Central Peru between 3300-4800
masl, and is sold as a medicinal plant in popular
markets (Dillon & Sagastegui, 1991). It is used
together to others plants for bathing (Gonzales de la
Cruz et al., 2014). It showed antibacterial activity
against S. aureus, B. subtilis, and E. coli; as well as
anti-Candida activity. Concerning its phytochemical
composition, phenolic compounds and catechol-type
tannins were found. Malca et al. (2016), reported the
presence of 5,7-dimethoxycoumarin that inhibit
cancer cells and 5,7,8-trimethoxycoumarin with anti-
HIV activity, being the only other publication
describing the phytochemical content of this plant
In addition, ethanolic extracts from others
species such as A. linearis, B. incana, J. paniculata,
P. hartwegiana, V. aff. pycnantha, and X.
dactylophyllum showed MICs up to 3.0 mg·mL-1
against S. aureus; this activity could be important
because S. aureus is one of the main opportunistic
pathogens with high capacity to acquire resistance to
chemotherapy (Mendem et al., 2016); likewise, other
plants are still important because it is possible that
they have other medicinal properties, e.i. P.
coerulescens and P. muliflora have shown an
antiproliferative activity of Hep3B hepatocarcinoma
cells (Carraz et al., 2015).
CONCLUSION
This is the first study that focuses on completely wild
native plants from the Peruvian high Andes, a fragile
ecosystem facing global warming; and according to
these results the most promising species are G.
americana, G. weberbaueri, H. laricifolium, L.
ferruginea, M. volcanica, O. multicaulis and O.
grandiflora. There is enough evidence about their
pharmacological potential as an important source for
new drugs. Most of the plants do not have
phytochemical and bioactive activity information and
in many cases, the whole plants are collected without
management plans and are over exploited. For this
reason, their promising biological activities studies
and biotechnological applications could contribute to
improve their conservation and sustainable use.
ACKNOWLEDGEMENTS
The authors want to thank Cecilia Vásquez-Robinet
and Nikolai Hidalgo who revised and corrected the
English grammar in the draft manuscript. Too, thank
Alberto Castañeda who prepared the map. Likewise,
this research was financially supported by the
Dirección General de Investigación (DGI) of the
Universidad Nacional Santiago Antúnez de Mayolo
(UNASAM-Perú) as a component of the project
“Caracterización biológica, fitoquímica y molecular
de plantas Peruanas altoandinas con potencial en la
industria farmacológica”.
REFERENCES
Abedini A, Roumy V, Mahieux S, Gohari A,
Farimani MM, Rivie C, Samaillie J, Sahpaz
S, Bailleul F, Neut C, Hennebelle T. 2014.
Antimicrobial activity of selected Iranian
medicinal plants against a broad spectrum of
pathogenic and drug multiresistant micro-
organisms. Lett Appl Microbiol 59: 412 -
421.
Al-Jaber NA, Awaad AS, Moses JE. 2011. Review
on some antioxidant plants growing in Arab
world. J Saudi Chem Soc 15: 293 - 307.
Alejandro-Espinosa M, Jaramillo-Fierro X, Ojeda-
Riascos S, Malagón-Aviles O, Ramírez-
Robles J. 2013. Actividad antioxidante y
antihiperglucemiante de la especie medicinal
Oreocallis grandiflora (Lam.) R. Br., al sur
del Ecuador. Bol Latinoam Caribe Plant
Med Aromat 12: 59 - 68.
Aumeeruddy-Elalfi Z, Gurib-Fakim A,
Mahomoodally MF. 2016. Chemical
composition, antimicrobial and antibiotic
potentiating activity of essential oils from 10
tropical medicinal plants from Mauritius. J

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/283
Herb Med 6: 88 - 95.
Barboza G, Cantero J, Núñez C, Pacciaroni A, Ariza
EL. 2009. Medicinal plants: A general review
and a phytochemical and
ethnopharmacological screening of the native
Argentine Flora. Kurtziana 34: 7 - 365.
Beltrán H, Granda A, León B, Sagástegui A, Sánchez
I, Zapata M. 2006. Asteraceae endémicas del
Perú. Rev Peru Biol 13:64 -164.
Boga M, Ertas A, Eroglu-Ozkan E, Kizil M, Ceken
B, Topcu G. 2016. Phytochemical analysis,
antioxidant, antimicrobial, anticholinesterase
and DNA protective effects of Hypericum
capitatum var. capitatum extracts. South
African J Bot 104: 249 - 257.
Bussmann RW, Malca G, Glenn A, Sharon D, Chait
G, Díaz D, Pourmand K, Jonat B, Somogy S,
Guardado G, Aguirre C, Chan R, Meyer K,
Kuhlman A, Townesmith A, Effio-Carbajal J,
Frías-Fernandez F, Benito M. 2010.
Minimum inhibitory concentrations of
medicinal plants used in Northern Peru as
antibacterial remedies. J Ethnopharmacol
132: 101 - 108.
Cáceres A. 1996. Plantas de uso medicinal en
Guatemala. Ed. Universitaria, Guatemala.
Carraz M, Lavergne C, Jullian V, Wright M, Gairin
JE, Gonzales de la Cruz M, Bourdy G. 2015.
Antiproliferative activity and phenotypic
modification induced by selected Peruvian
medicinal plants on human hepatocellular
carcinoma Hep3B cells. J Ethnopharmacol
166: 185 - 199.
Castillo S, Salinas N, León B, Sánchez I. 2006.
Gentianaceae endémicas del Perú. Rev Peru
Biol 13: 339 - 355.
Ccana-Ccapatinta GV, Serrano-Flores C, Urrunaga-
Soria EJ, Choquenaira-Pari J, Galiano-
Sánchez W, Crockett SL, von Poser GL, del
Carpio-Jimenez C. 2014. Assessing the
phytochemical profiles and antidepressant-
like activity of four Peruvian Hypericum
species using the murine forced swimming
test. Phytochem. Lett. 10: 107 - 112.
Ccena-Ccapatinta GV, von Poser GL. 2015.
Acylphloroglucinol derivatives from
Hypericum laricifolium Juss. Phytochem
Lett 12: 63 - 68.
Chander MP, Pillai CR, Sunish IP, Vijayachari P.
2016. Antimicrobial and antimalarial
properties of medicinal plants used by the
indigenous tribes of Andaman and Nicobar
Islands, India. Microbiol Pathog 96: 85 - 88.
Cirak C, Radusiene J, Jakstas V, Ivanauskas L, Seyis
F, Yayla F. 2017. Altitudinal changes in
secondary metabolite contents of Hypericum
androsaemum and Hypericum polyphyllum.
Biochem Syst Ecol 70: 108 - 115.
Crockett S, Eberhardt M, Kunert O, Schühly W.
2010. Hypericum species in the Páramos of
Central and South America: A special focus
upon H. irazuense Kuntze ex N. Robson.
Phytochem Rev 9: 255 - 269
De-la-Cruz H, Vilcapoma G, Zevallos PA. 2007.
Ethnobotanical study of medicinal plants
used by the Andean people of Canta, Lima,
Peru. J Ethnopharmacol 111: 284 - 294.
de Oliveira JR, de Castro VC, Vilela PGF, Camargo
SCA, Carvalho CAT, Jorge AOC, de Oliveira
LD. 2013. Cytotoxicity of Brazilian plant
extracts against oral microorganisms of
interest to dentistry. BMC Complement.
Altern Med 13: 208.
Dillon MO, Sagastegui A. 1991. Gamochaeta pp. In
Macbride JF et al. (Eds.). Flora of Peru,
Family Asteraceae: Part V, Fieldiana Botany,
USA.
El-Seedi HR, Ringbom T, Torssell K, Bohlin L.
2003. Constituents of Hypericum laricifolium
and their cyclooxygenase (COX) enzyme
activities. Chem Pharm Bull 51: 1439 -
1440.
Festa C, D’Auria MV, Sepe V, Ilaš J, Leick A,
N’Gom S, de Marino S. 2015. Triterpenoid
profile and bioactivity study of Oenothera
maritima. Phytochem Lett 13: 324 - 329.
Galand N, Pothier J, Viel C. 2002. Plant drug
analysis by planar chromatography. J
Chromatograph Sci 40: 1 - 13
Gonzales De La Cruz M, Balden MS, Beltran SH,
Jullian V, Bourdy G. 2014. Hot and cold:
Medicinal plant uses in Quechua speaking
communities in the high Andes (Callejon de
Huaylas, Ancash, Peru). J Ethnopharmacol
155: 1093 - 1117.
Guaratini T, Lopes NP, Marinho-Soriano E,
Colepicolo P, Pinto E. 2012. Antioxidant
activity and chemical composition of the non
polar fraction of Gracilaria domingensis
(Kitzing) Sonder ex Dickie and Gracilaria
birdiae (Plastino & Oliveira). Braz J
Pharmacogn 22: 724 - 729.

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/284
Guil-Guerrero JL, Ramos L, Moreno C, Zúñiga-
Paredes JC, Carlosama-Yepez M, Ruales P.
2016. Antimicrobial activity of plant-food
by-products: A review focusing on the
tropics. Livest Sci 189: 32 - 49.
Gülçin İ. 2006. Antioxidant activity of caffeic acid
(3,4-dihydroxycinnamic acid). Toxicology
217: 213 - 220.
Gupta D, Dubey J, Kumar M. 2016. Phytochemical
analysis and antimicrobial activity of some
medicinal plants against selected common
human pathogenic microorganisms. Asian
Pacific J Trop Dis 6: 15 - 20.
Jayathilake C, Rizliya V, Liyanage R. 2016.
Antioxidant and free radical scavenging
capacity of extensively used medicinal plants
in Sri Lanka. Proc Food Sci 6: 123 - 126.
Jerves-Andrade L, León-Tamariz F, Peñaherrera E,
Cuzco N. 2014. Medicinal plants used in
South Ecuador for gastrointestinal problems:
An evaluation of their antibacterial potential.
J Med Plant Res 8: 1310 - 1320.
Harborne JB. 1984. Phytochemical method- A
guide to modern technique of plant
analysis. Chapman and Hall Ltd. New York,
USA.
Heim E. 2014. Flora of Arequipa, Peru: an
illustratedfield guide for nature lovers.
Books on Demand, USA.
Kızıl G, Kızıl M, Yavuz M, Emen S, Hakimoğlu F.
2008. Antioxidant activities of ethanol
extracts of Hypericum triquetrifolium and
Hypericum scabroides. Pharm Biol 46: 231 -
242.
Klančnik A, Piskernik S, Jeršek B, Možina SS. 2010.
Evaluation of diffusion and dilution methods
to determine the antibacterial activity of plant
extracts. J Microbiol Methods 81: 121 -
126.
Kolff K, Kolff A. 2005. Flores silvestres de la
Cordillera Blanca, Instituto de Montaña,
Huaraz, Perú.
Lee SE, Hwang HJ, Ha JS, Jeong HS, Kim JH. 2003.
Screening of medicinal plant extracts for
antioxidant activity. Life Sci 73: 167 - 179.
Li MH, Li L, Yang YM, Zhang N, Song XL, Xiao
PG. 2010. Genus Gentianella Moench: a
phytochemical and ethnopharmacological
review. Chin Herb Med 2: 262 - 271.
Lima VN, Oliveira-Tintino CD, Santos ES, Morais
LP, Tintino SR, Freitas TS, Geraldo YS,
Pereira RL, Cruz RP, Menezes IR, Coutinho
HD. 2016. Antimicrobial and enhancement
of the antibiotic activity by phenolic
compounds: Gallic acid, caffeic acid and
pyrogallol. Microbiol Pathog 99: 56 - 61.
Lock O. 1994. Investigacion Fitoquímica. Métodos
en el estudio de productos naturales.
PUCP-Fondo Editorial, Lima, Perú.
Malca GGR, Hennig L, Rodríguez REF, Bussmann
RW. 2016. Coumarins of Loricaria
ferruginea. Rev Bras Farmacogn 26: 471 -
473.
Martin EW, Fullerton CE, Levallen EE, Osol A, Tice
LF, Van MC. 1965. Farmacia práctica de
Remington. Ed. UTEHA, México DF,
México.
Mendem SK, Alasthimannahalli GT, Shivannavar
CT, Gaddad SM. 2016. Antibiotic resistance
patterns of Staphylococcus aureus: A
multicenter study from India. Microb Pathog
98: 167 - 170.
Monigatti M, Bussmann RW, Weckerle CS. 2013.
Medicinal plant use in two Andean
communities located at different altitudes in
the Bolivar Province, Peru. J
Ethnopharmacol 145: 450 - 464.
Ncube NS, Afolayan AJ, Okoh AI. 2008. Assessment
techniques of antimicrobial properties of
natural compounds of plant origin: current
methods and future trends. Afr J Biotechnol
7: 1797 - 1806.
Olivera P, Tamariz C, Gutiérrez–Correa M. 2010.
Desinfección e influencia del bencil
aminopurina (BAP) y ácido naftalén acético
(ANA) en la multiplicación in vitro de
Perezia coerulescens Wedd, planta medicinal
altoandina. Rev Aporte Santiaguino 3: 117 -
124.
Olivera-Gonzales P, Yldefonzo EM, Mestanza EM,
Tamariz-Angeles C. 2017a. In vitro
propagation of Oreocallis grandiflora (Lam.)
R. Br., a medicinal threatened plant. Annu
Res Rev Biol 14: 1 - 9.
Olivera-Gonzales P, Espinoza R, Tamariz-Angeles C.
2017b. In vitro multiplication and somatic
embryogenesis of Perezia pinnatifida
(Asteraceae) medicinal plant. Rev Per Biol
24: 323 - 328.
Pretell J, Ocaña D, Jon R, Barahona E. 1985.
Apuntes sobre algunas especies forestales
de la sierra peruana. FAO/Holanda/INFOR,

Tamariz-Angeles et al.
Pharmacological potential of high-Andean medicinal plants
Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas/285
Lima, Perú.
Ramirez-Villegas J, Cuesta F, Devenish C, Peralvo
M, Jarvis A, Arnillas CA. 2014. Using
species distributions models for designing
conservation strategies of Tropical Andean
biodiversity under climate change. J Nat
Conserv 22: 391 - 404.
Rehecho S, Uriarte-Pueyo I, Calvo J, Vivas LA,
Calvo MI. 2011. Ethnopharmacological
survey of medicinal plants in Nor-Yauyos, a
part of the Landscape Reserve Nor-Yauyos-
Cochas, Peru. J Ethnopharmacol 133: 75 -
85.
Reynel C, Marcelo J. 2009. Arboles de los
ecosistemas forestales andinos, Manual de
Identificacion de Especies. First Ed. Perú,
Programa ECOBONA, Lima, Perú.
Rojas R, Bustamante B, Bauer J, Fernandez I, Alban
J, Lock O. 2003. Antimicrobial activity of
selected Peruvian medicinal plants. J
Ethnopharmacol 88: 199 - 204.
Saddiqe Z, Naeem I, Maimoona A. 2010. A review of
the antibacterial activity of Hypericum
perforatum L. J Ethnopharmacol 131: 511 -
521.
Srivastava V, Darokar MP, Fatima A, Kumar JK,
Chowdhury C, Saxena HO, Dwivedi GR,
Shrivastava K, Gupta V, Chattopadhyay SK,
Luqman S, Gupta MM, Negi AS, Khanuja
SP. 2007. Synthesis of diverse analogues of
oenostacin and their antibacterial activities.
Bioorg Med Chem 15: 518 - 525.
Tauchen J, Bortl L, Huml L, Miksatkova P, Doskocilf
I, Marsika P, Villegas PPP, Flores YB, Van
Damme P, Lojka B, Havlik J, Lapcik O,
Kokoska L. 2016. Phenolic composition,
antioxidant and anti-proliferative activities of
edible and medicinal plants from the
Peruvian Amazon. Rev Bras Farmacogn 26:
728 - 237.
Tangarife-Castaño V, Correa-Royero J, Zapata-
Londoño B, Durán C, Stanshenko E., Mesa-
Arango CA. 2011. Anti-Candida albicans
activity, cytotoxicity and interaction with
antifungal drugs of essential oils and extracts
from aromatic and medicinal plants. Infectio
15: 160 - 167.
Tene V, Malagón O, Finzi PV, Vidari G, Armijos C,
Zaragoza T. 2007. An ethnobotanical survey
of medicinal plants used in Loja and Zamora-
Chinchipe, Ecuador. J Ethnopharmacol
111: 63 - 81.
Wagner H, Bladt S. 1966. Plant drug analysis - A
thin layer cromathography atlas. Second
Edition. Springer. Berlin, Alemania.
Zida A, Bamba S, Yacouba A, Ouedraogo-Traore R,
Guiguemdé RT. 2017. Anti-Candida albicans
natural products, sources of new antifungal
drugs: A review. J Med Mycol 27: 1 - 19.
Zhu H, Chen C, Tong Q, Chen X, Yang J, Liu J, Sun
B, Wang J, Yao G, Luo Z, Xue Y, Zhang Y.
2015. Hyperisampsins H-M, cytotoxic
polycyclic polyprenylated acylphloro-
glucinols from Hypericum sampsonii. Sci
Rep 5: 14772.