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Authors Accepted Manuscript

Ethnobotanical survey of medicinal plants used in


the traditional treatment of diabetes in Chtouka Ait
Baha and Tiznit (Western Anti-Atlas), Morocco

M. Barkaoui, A. Katiri, H. Boubaker, F. Msanda

www.elsevier.com/locate/jep

PII: S0378-8741(17)30196-4
DOI: http://dx.doi.org/10.1016/j.jep.2017.01.023
Reference: JEP10670
To appear in: Journal of Ethnopharmacology
Received date: 19 June 2016
Revised date: 10 January 2017
Accepted date: 14 January 2017
Cite this article as: M. Barkaoui, A. Katiri, H. Boubaker and F. Msanda,
Ethnobotanical survey of medicinal plants used in the traditional treatment of
diabetes in Chtouka Ait Baha and Tiznit (Western Anti-Atlas), Morocco, Journal
of Ethnopharmacology, http://dx.doi.org/10.1016/j.jep.2017.01.023
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Ethnobotanical survey of medicinal plants used in the traditional treatment of
diabetes in Chtouka Ait Baha and Tiznit (Western Anti-Atlas), Morocco
M.Barkaoui, A.Katiri, H.Boubaker, F.Msanda*
Laboratoire de Biotechnologies et Valorisation des Ressources Naturelles, Facult des
Sciences, Universit Ibn Zohr, Agadir, Morocco.
*
Corresponding author. Laboratoire de Biotechnologies et Valorisation des Ressources
Naturelles, Facult des Sciences, B.P. 8106, Cit Dakhla, Agadir, Morocco. Tel.: 212 0528
220957; fax: 212 0528 220100 f.msanda@uiz.ac.ma (F. Msanda)

Abstract
Ethnopharmacological relevance:
In Morocco, diabetes mellitus is a major public health problem with more than 1.5
million cases in 2014. Medicinal plants are widely used by the Moroccan population to
treat the illness.

Aim of the study:


The aim of this work is to make an inventory of plant species used in folk medicine for
the management of diabetes in Chtouka Ait Baha and Tiznit provinces.

Materials and methods:


The survey was carried out by means of semi-structured questionnaires. A total of 380
interviews were conducted with traditional health practitioners and knowledgeable
villagers. The data were analysed through use value (UV), fidelity level (FL) and
relative frequency of citation (RFC).

Results:
In total, 48 plant species belonging to 25 families were reported. Lamiaceae, Asteraceae
and Apiaceae were reported as the most represented families. Six plants are reported for
the first time as used in traditional treatment of diabetes and one plant species was
previously unknown for its medicinal use to treat diabetes in Morocco. The most
frequently cited plant species are Allium sativum L., Salvia officinalis L., Marrubium
vulgare L. and Lavandula dentata L. Leaves were the most cited plant part used,
decoction is the preferred mode of preparation.

1
Conclusion:
This study showed the importance of folk medicine in the healthcare system for the
local people living in the study area. The current study represents a useful
documentation, which can contribute to preserving knowledge on the use of medicinal
plants in this region and to explore the phytochemical and pharmacological potential of
medicinal plants.

Keywords: Ethnobotanical survey, Diabetes, Chtouka Ait Baha, Tiznit, Morocco.

1. Introduction
Diabetes mellitus is a metabolic disease characterized by chronic hyperglycemia resulting
from defects in insulin secretion, insulin action or both (WHO, 1999). The majority of cases
of diabetes fall into two types (i) type 1, known as juvenile diabetes mellitus or insulin
dependent diabetes mellitus which is hereditary and is treated by insulin (ii) type 2, known as
adult type or non-insulin dependent diabetes mellitus which is treated by controlling the diet
and oral hypoglycemic drug (Singh, 2011). Diabetes is a major public health problem which
affects millions of people and its associated with serious complication, such as
hyperlipidemia, hyperinsulinemia, hypertension and atherosclerosis (Luo et al., 2004; Sepici
et al., 2004). According to the International Diabetes Federation (IDF) there were 415 million
people in the world with diabetes and this is projected to increase to 642 million by 2040
(IDF, 2015). In Morocco, diabetes mellitus is one of the most common metabolic diseases,
there were over 1.4 million cases of diabetes in 2013 (IDF, 2013). Diabetes affects both rural
and urban population, its prevalence ranges between 4.4 % in rural areas and 9 % in urban
areas (Moroccan Ministry of Health, 2012). Several factors were involved as causes of
diabetes mellitus including lifestyle changes, eating of fatty foods, sugary foods and
beverages, obesity, unhealthy diet and physical inactivity (Karoui, 2006; Keter and Mutiso,
2012). The management of diabetes mellitus consists of the use of numerous anti-
hyperglycemic agents including plant species.
Morocco is known for its rich vegetation and plant biodiversity with 5200 species and
subspecies of vascular plants including 900 endemic plants (Fennane and Ibn Tattou, 2012)
and the Moroccan medicinal flora is estimated to 600 species (Rejdali, 1996). In Morocco, the
use of plants for medical care has been practiced since immemorial time and patients are more
dependent on folk medicine (Abouri et al., 2012; Bellakhdar et al., 1991; El Amri et al., 2015;

2
Jouad et al., 2001). The local folk medicine continues to be an important source of remedies
for primary healthcare (Abouri et al., 2012; Saadi et al., 2013). Previous studies revealed the
importance given by the diabetics to traditional plants medicine and that medicinal plants play
an important role in the treatment of diabetes mellitus (Eddouks et al., 2002; Jouad et al.,
2001; Tahraoui et al., 2007; Ziyyat et al., 2009). Herbal medicines have been traditionally
used because of several advantages; they are affordable, easily accessible, and there is no
evidence of resistance to whole-plant extracts and also effectiveness (Abouri et al., 2012; Al-
Adhroey et al., 2010; Nasri and Shirzad, 2013; Venkatesh et al., 2003). However, very little
information is available on medicinal plants in central Morocco (Abouri et al., 2012; Saadi et
al., 2013) and there is no documentation on the use of plants for the treatment of diabetes. In
addition, the sector is one of the most remarkable regions of North Africa as a region of great
biodiversity (Msanda et al., 2005). The aim of this study was to identify the medicinal plant
species commonly used to treat diabetes by the population of Chtouka Ait Baha and Tiznit
regions where there is no such investigation.
2. MATERIALS AND METHODS
2.1. Study area
The study was conducted in Chtouka Ait Baha and Tiznit Provinces, situated in central
Morocco (Figure 1). Geographically, the area corresponds to the western side of the
mountains of the Anti-Atlas and constitutes a part of the Arganeary Reserve Biosphere
approved by the UNESCO in 1998. The elevation ranges from 400 m to approximately 2250
m. The climate is Mediterranean type, precipitation levels vary between 200 and 500 mm
according the location and the altitude. The plant formations are constituted by Argania
spinosa (L.) Skeels and shrublands dominated by Cistus creticus L., Lavandula dentata,
Artemisia herba-alba Asso and Thymus saturejoides Coss. The sector is one of the most
remarkable regions of North Africa as a region of great biodiversity (Msanda et al., 2005).
2.2. Ethnobotanical survey
An ethnobotanical survey was conducted from January 2013 to June 2014. The data were
collected through semi structured interviews. Interviews were conducted in Tashelhit (local
Berber language) and plant names were mostly given in Tashelhit, but names in Moroccan
Arabic were recorded when mentioned. A total of 380 people were interviewed for this
purpose. Interviews were designed in to record information about the plants used to treat
diabetes mellitus and their local names, methods of preparation, parts of the plant used,
administration of medicines and the demographic characteristics of the participants in the
study.

3
The collected plants were identifying by using Flora of Morocco (Fennane et al., 1999,
2007, 2014). Scientific names of plant species were determined according to the Plant List
(http://www.theplantlist.org) and voucher specimens of each plant were deposited in
herbarium of the laboratory of Biotechnology and Valorization of the Natural Resources,
Faculty of Sciences, Ibn Zohr University, Agadir, Morocco.

Figure 1: Study area


2.3. Data analysis
2.3.1. Use value (UV)
The use value (UV) gives the relative importance of plant species known locally in the
traditional medicine. It was calculated using the following formula (Phillips et al., 1994):
UV = U/N where U is the number of use reports for a given plant species mentioned by each
informant and N is the total number of informants interviewed for a given plant.
2.3.2. Fidelity level (FL)
Fidelity level (FL) indicates the percentage of informants claiming the use of a certain plant
species for the same major purpose. Fidelity level is calculated by the following formula:

4
FL (%) = NP \N x 100, where Np is the number of informants that claimed a use of a plant
species to treat a particular disease and N is the number of informants that used plants as a
medicine to treat any given disease (Friedman et al.,1986).
2.3.3. Relative frequency of citation
The relative frequency of citation shows the local importance of each species and its obtained
by dividing the number of informants, who mention the use of the species, also known as the
Frequency Citation (FC), by the number of informants participating in the survey (N) (Tardo
and Pardo-de-Santayana, 2008).
RFC = FC\N (0< RFC<1)
3. Results and discussion
3.1. Demographic features
A total of 380 informants including traditional healers, herbalists and knowledgeable villagers
participated in this study. One hundred and ninety five of respondents are women and 185 are
men. The age of respondents varies between 20 and 75 years and the mean age is 54.6 years.
The age group [50 70] was the most represented by 46.3%. This age group is the most
relevant in terms of ethnomedicinal knowledge. Indeed, in study area, interviews show that
elderly people were particularly competent and possess a much greater knowledge of native
plants than younger people. On another hand, in Morocco, younger people usually move to
urban area to look for paid employment and are poorly implicated in traditional medicine. Our
observation is in agreement with previous reports in other regions of Morocco where
indigenous knowledge on use of medicinal plants is still strong with elderly people (Abouri et
al., 2012; Mehdioui and Kahouadji, 2007). Similar findings were observed in Togo where
ethno-medicinal knowledge in the treatment of diabetes is mainly held by the elderly (Kpodar
et al., 2015).
The knowledge of medicinal plants was inversely related to the level of education of the
interviewed respondents; illiterate (58.4%), primary education (23.1%), secondary education
(16.5%) and university education (1.8%). This agrees with other ethnobotanical studies
carried out in Morocco (Eddouks et al., 2002; Ziyyat et al., 1997) in which knowledge on the
use of medicinal plants in the treatment of diabetes mellitus is owned by illiterate. Similarly,
Kadir et al. (2012) in Bangladesh; Kpodar et al. (2015) in Togo and Tag et al. (2012) in India
indicated that illiterate people have greater competence in using plants in the treatment of
diabetes mellitus. Traditional knowledge on medicinal plants has largely been passed by
orally from generation to generation. Majority of interviewers acquired the traditional medical
knowledge from members of their families mainly grandparents and parents and this

5
knowledge has not been documented. The traditional healers claimed to diagnosis diabetes
mellitus in their patients by observing symptoms such as excessive urination and presence of
sugar in urine revealed by its sweet taste. The taste of urine was also used to diagnose patients
with diabetes in Bangladesh (Rahmatullah et al., 2012) and in Cameroon (Tsabang et al.,
2016).
3.2. Medicinal plants and floristic analysis
In this ethnobotanical survey we recorded information on a total of 48 medicinal plant
species, belonging to 25 families and 44 genera. The plants were listed in alphabetical order
by families, genera and species (Table 1). Information such as local name of plants species,
used parts, mode of preparation, ethnobotanical indices are provided for each species.
Families with the most reported plant species were Lamiaceae (8 species), Asteraceae,
Apiaceae (5 species each) and Fabaceae (4 species) (Figure 2). This finding is in agreement
with previous reports where these families were the most represented families in diabetes
mellitus treatment in Morocco (Ghourri et al., 2013; Orch et al., 2015, Tahraoui et al., 2007),
in Algeria (Benarba et al., 2015; Telli et al., 2016), in Italy (Savo et al., 2011), in Spain
(Benitez et al., 2010) and in Iran (Nowbandegani et al., 2015). The importance of Asteraceae
and Lamiaceae are also documented to treat diabetes mellitus respectively in Limpopo
Province in South Africa (Semenya et al., 2012) and in Northwest Iran (Bahmani et al., 2014).
Dominance of these families could be attributed to their abundance in the flora of the study
area and in the flora of Morocco (Fennane and Ibn Tattou, 2012).

Figure 2: Number of species per family (Lam: Lamiaceae, Api: Apiaceae, Ast: Asteraceae,
Fab: Fabaceae, Apo: Apocynaceae, Cis: Cistaceae, Cuc: Cucurbitaceae, Eup: Euphorbiaceae,
All: Alliaceae, Ama: Amaranthaceae, Ana: Anacardiaceae, Bra: Brassicaceae, Cac:

6
Cactaceae, Dra: Dracaenaceae, Eph: Ephedraceae, Mor: Moraceae, Ole: Oleaceae, Myr:
Myristicaceae, Pap: Papaveraceae, Pun: Punicaceae, Rha: Rhamnaceae, Ros: Rosaceae, Sap:
Sapotaceae, The: Theaceae, Urt: Urticaceae)

The analysis of the growth forms of the medicinal plants used in the study area revealed the
predominance of nanophanerophytes (shrubs) (33.3%) followed by annual herbs (20.8%),
macrophanerophytes (trees) (18.8%), chamaephytes (small shrubs) (14.6%), geophytes
(perennial plants where the resting bud is below ground) (8.3%) and hemi cryptophytes
(herbaceous perennial plants with the resting bud at near the soil line) (4.2%).
A total of 48 plant species belonging to 25 families were reported, this number is found to be
far higher than that of other areas, in Morocco, investigated for traditional treatment of
diabetes (Errajraji et al., 2010; Orch et al., 2015; Ziyyat et al., 1997). The majority of
medicinal plants (32 plant species) recorded in this survey were growing in the wild reflecting
the social importance of the local floristic resources (e;g; Argania spinosa, Artemisia herba-
alba, Thymus saturejoides, Lavandula dentata, Cistus creticus) thirteen were cultivated (e;g;
Allium sativum , Opuntia ficus-indica (L.) Mill., Prunus dulcis (Mill.) D. A. Webb, Punica
granatum L.) and three were imported from the outside of Morocco (e.g. Camellia sinensis
(L.) Kuntze and Glycine max (L.) Merr.). Plants growing in wild are also most commonly
used for medicinal purposes in other regions of Morocco (Abouri et al., 2012; Saadi et al.,
2013) and in Algeria (Telli et al., 2016).
Our survey showed that wild population of Thymus saturejoides and Artemisia herba-alba are
threatened due to their overexploitation. Indeed, these plants are popular medicinal herbs in
Morocco and are widely exported as herbs or essential oils. Our observation is in accordance
with previous reports of overexploitation of medicinal plants in Morocco (Abbad et al., 2011;
Fennane and Ibn Tattou, 1998). Therefore conservation of these medicinal plants is a
promising alternative for their sustainable use.
3.3. Ethnobotanical indices
The data obtained were analyzed and ranked on the basis of fidelity level (FL), use value
(UV) and relative frequency of citation (RFC), values of collected plants species ranged from
3.33 to 78.95%, 1 to 1.83 and 0.04 to 0.64, respectively (Table 1).
Of the 48 inventoried species eight plant species were identified with FL greater than 0.50;
Apteranthes europaea (Guss.) Murb., Dracaena draco (L.) L., Warionia saharae Benthem ex
Benth. & Coss., Lavandula stoechas L., Hammada scoparia (Pomel) Iljin, Lupinus
angustifolius L., Periploca angustifolia Labill., Raphanus sativus L., Scorzonera undulata

7
Vahl. Four species showed high values (>50%) of UV; Allium sativum, Salvia officinalis,
Marrubium vulgare, Lavandula dentata. Of all medicinal plants reported in this study
Lavandula dentata, Thymus saturejoides, Artemisia herba-alba, Apteranthes europaea, Salvia
officinalis, Trigonella foenum-graecum L., Allium sativum, Argania spinosa, Marrubium
vulgare and Carum carvi L. were the most frequently used plants to treat diabetes based on
RFC values. In the obtained results, Lavandula dentata, Salvia officinalis, Allium sativum and
Marrubium vulgare shows significant values of UV (1.42 1.83) and RFC (0.29 0.64).
Our results are similar to those reported in Morocco in other studies (Bnouham et al., 2008;
Eddouks et al., 2002; Jouad et al., 2001; Moukal, 2004; Tahraoui et al., 2007; Ziyyat et al.,
1997) where Lavandula dentata, Artemisia herba-alba, Salvia officinalis, Trigonella foenum-
graecum, Allium sativum, Argania spinosa and Marrubium vulgare are the plant species most
used to treat diabetes mellitus. Trigonella foenum-graecum is also the most recommended
plant for treat diabetes in Fars region of Iran (Nowbandegani et al., 2015) and in west Algeria
(Allali et al., 2008). Recently, Artemisia herba-alba and Trigonella foenum-graecum are also
documented as the most frequently used species to treat diabetes in Southeastern Algeria
(Telli et al., 2016). Eighty nine percent of the plant species cited in this study have been
reported in other scientific studies to be used traditionally to treat diabetes (Table 1), this
supports the use of these plants in the management of diabetes mellitus. Several studies
revealed through in vivo research the hypoglycemiant effect of these plants and support their
traditional use in diabetes mellitus control. These species include Trigonella foenum-graecum
(Ali et al., 1995; Hamza et al., 2015; Renuka et al., 2009), Artemisia herba-alba (Al-Khazraji
et al., 1993; Hamza et al., 2015), Allium sativum (Chang and Johnson, 1980; Eidi et al., 2006),
Ajuga iva (L.) Schreb. (El Hilaly and Lyoussi, 2002), Marrubium vulgare (Boudjelal et al.,
2012; Elberry et al., 2015), Salvia officinalis (Eidi et al., 2005, Eidi and Eidi, 2009).
Indeed, the hypoglycemic effect of Trigonella foenum-graceum has been reported in animals
(Khatir et al., 1999; Raju et al., 2001; Ribes et al., 1984; Vats et al., 2002) and in human
patients (Kassaian et al., 2009; Raghuram et al., 1994; Sharma et al., 1990) and has been
attributed to its high fiber content (Ali et al., 1995; Gomez and Bhaskar, 1998; Sharma et al.,
1986). Fibers of fenugreek interfere with the digestion and absorption of carbohydrates and
thus reduce blood glucose (Sharma et al., 1986; Madar et al., 1984; 1988; Srinivasan, 2005).
The seeds of this herb contain other bioactive compounds with hypoglycemic activity such as
4-hydroxyisoleucine (Broca et al., 2004; Moorthy et al., 1989; Ribes et al., 1986) and
trigonelline (Hannan et al., 2007; Raju et al., 2001). The 4-hydroxyisoleucine is reported as an
insulin-stimulating substance (Hillaire-Buys et al., 1993; Jette et al., 2009; Sauvaire et al.,

8
1998). Effect of trigonelline is due to enhanced pancreatic regeneration and restoring its
insulin content (Shah et al. 2006, Zhou et al., 2012).
Several studies have investigated the antidiabetic effect of Allium sativum in diabetic rats
(Belemkar, 2013; Chandra et al., 2007; Eidi et al., 2006) and the hypoglycaemic action has
been attributed to sulphur compounds (Belemkar, 2013; Chandra et al., 2007; Chang and
Johnson, 1980; Eidi et al., 2006; Marles and Farnsworth, 1995; Otunola et al., 2010). Allium
sativum improves glycemic control through increased insulin secretion and increased insulin
sensivity (Belemkar et al., 2013; Carson, 1987; Liu et al., 2005).
Also of interest, a phytochemical investigation of aqueous extract of Marrubium vulgare has
shown the presence of flavonoids and verbascoside derivates with known antidiabetic activity
(Boudjelal, 2012). Furthermore, Rodrigues et al. (1998) have reported that Marrubiin is the
main active compound isolated from Marrubium vulgare. The mechanism of hypoglycaemic
action of Marrubium vulgare involves stimulation of secretion of insulin (El Berry, 2013).
Additionally, the antidiabetic activity of Artemisia herba-alba (Djeridane et al., 2006; Hamza
et al., 2015; Khlifi et al., 2013), Ajuga iva (Boudjelal, 2016; El Hilaly and Lyoussi, 2002;
Khaled-Khodja et al., 2014) and Salvia officinalis (Durling et al., 2007) may be associated to
the presence of phenolics and flavonoids compounds.

Table 1: Plants use to treat diabetes in Chtouka Ait Baha and Tiznit areas.
Families Vernacular Used Prepar Mode of U FL R Literature references in
and plant name parts ation administ V F relationship of
species ration C medicinal use of plants
in diabetes

In Morocco Out of
Morocco
Amarylli
daceae Tiskert / Bulb Raw Oral 1. 27. 0. (Benkhnigu (Ahmad
Allium Touma 83 66 29 e et al., et al.,
sativum 2014 ; 2009 ;
L. Eddouks et Ezuruike
CABT00 al., 2002 ; and
4 El Amrani Prieto,
et al., 2014 ;
2010 ; Gho Keter
urri et al., and
2013 ; Mutiso,
Saadi et al., 2012 ;
2013 ; Mukherj
Ziyyat et ee et al.,
al., 1997) 2006 ;

9
Nowban
degani et
al.,
2015 ;
Telli et
al.,
2016)
Amarant
haceae Assay Seed Decoct Oral 1. 60. 0. (Abouri et (Allali,
Hammad ion 00 00 07 al., 2012 ; et al.,
a El Rhaffari 2008 ;
scoparia and Zaid, Telli et
(Pomel) 2000) al.,
Iljin 2016)
CABT07
8
Anacardi
aceae Btem/Igg/ Fruit Decoct Oral 1. 21. 0. No data (Telli et
Pistacia Drou ion 08 05 18 al.,
atlantica 2016)
Desf.
CABT13
7
Apiaceae
Carum Lkarwya Seed Decoct Oral 1. 11. 0. (Benkhnigu (Eidi et
carvi L. ion, 00 65 27 e et al., al.,
CABT02 macera 2014 ; 2010 ;
7 tion, Eddouks et Telli et
infusio al., al.,
n and 2002 ; El 2016)
powde Amrani et
r al.,
2010 ; Gho
urri et al.,
2013 ;
Jamila and
Mostafa,
2014 ;
Saadi et al.,
2013 ;
Tahraoui et
al., 2007)

Eryngiu Tasnant Stem Decoct Oral 1. 37. 0. No data No data


m /Iglifin and ion 26 04 22
ilicifoliu leaf and
m Lam. powde
CABT06 r
4

10
Foenicul Nafaa Seed Decoct Oral 1. 19. 0. (Abouri et (Telli et
um ion 26 35 13 al., 2012 ; al.,
vulgare Benkhnigue 2016)
Mill. et al.,
CABT07 2014 ;
3 Eddouks et
al., 2002 ;
El Amrani
et al.,
2010 ;
Ghourri et
al., 2013 ;
Jamila and
Mostafa,
2014 ;
Tahraoui et
al., 2007)

Pastinac Left Root Raw Oral 1. 28. 0. No data No data


a sativa lmahfour 14 57 09
L.
CABT12
7

Pimpinell Habbat Seed Decoct Oral 1. 37. 0. (Abouri et No data


a anisum hlawa ion 13 50 07 al., 2012 ;
L. Benkhnigue
CABT13 et al.,
5 2014 ;
Ghourri et
al., 2013)
Apocyna
ceae Oukan Stem Decoct Oral 1. 78. 0. (Benkhnigu No data
Apterant iddan ion, 00 95 33 e et al.,
hes infusio 2014)
europaea n, and
(Guss.) raw
Murb.
CABT01
0
.
Nerium Defla/Alili Leaf Fumig Inhalatio 1. 31. 0. (Abouri et No data
oleander ation n 25 25 11 al., 2012 ;
L. Benkhnigue
CABT11 et al.,
8 2014 ;
Bouayyadi
et al.,
2015 ;
Eddouks et

11
al., 2002 ;
El Amrani
et al.,
2010 ;
Ghourri et
al., 2013 ;
Jamila and
Mostafa,
2014 ; Orch
et al.,
2015 ;
Tahraoui et
al., 2007 ;
Ziyyat et
al., 1997)

Periploc Asllif Fruit Decoct Oral 1. 60. 0. (El Rhaffari No data


a ion 00 00 07 and Zaid,
angustifo 2000)
lia
Labill.
CABT13
1
Asterace
ae Izri/Chih Stea Decoct Oral 1. 6.9 0. (Bellakhdar (Allali et
Artemisia m, ion 11 7 31 et al., al.,
herba- leaf and 1991 ; 2008 ;
alba and infusio Benkhnigue Telli et
Asso root n et al., al.,
CABT01 2014 ; 2016 ;
5 Eddouks et Twaij
al., 2002 ; and Al-
El Amrani Badr,
et al., 1988)
2010 ; Fadil
et al.,
2015 ;
Ghourri et
al., 2013 ;
Jamila and
Mostafa,
2014 ; Orch
et al.,
2015 ;
Tahraoui et
al., 2007 ;
Ziyyat et
al., 1997)

12
Echinops Taskra Flow Decoct Oral 1. 50. 0. (Saadi et No data
spinosissi er ion 00 00 07 al., 2013)
mus
Turra
CABT06
0

Launaea Iferskel/Mo Stem Decoct Oral 1. 25. 0. (Benkhnigu No data


arboresc ulbina , leaf ion 17 00 13 e et al.,
ens and and 2014 ;
(Batt.) flow infusio Eddouks et
Murb. er n al., 2002 ;
CABT09 Ghourri et
1 al., 2013 ;
Jamila and
Mostafa,
2014 ;
Saadi et al.,
2013)

Scorzone Tamtla Flow Raw Oral 1. 57. 0. No data No data


ra er 00 14 09
undulata
Vahl
CABT15
9

Warionia Afssas Leaf Infusio Oral 1. 64. 0. (Ghourri et No data


saharae n 00 29 20 al., 2013)
Benthem
ex Benth.
& Coss.
CABT17
6
Brassicac
eae Lfjel Root Raw Oral 1. 60. 0. (Benkhnigu (Yaseen
Raphanu 00 00 07 e et al., et al.,
s sativus 2014 ; 2015)
L. Ghourri et
CABT14 al., 2013)
5
Cactacea
e Lhndia/Akn Stem Decoct Oral 1. 6.4 0. (Allali et (Semeny
Opuntia ari , ion 19 5 09 al., 2008 ; a et al.,
ficus- flow and Benkhnigue 2012)
indica er powde et al.,
(L.) Mill. r 2014 ;
CABT12 Bouayyadi
4 et al.,

13
2015 ;
Ghourri et
al., 2013 ;
Tahraoui et
al., 2007)
Cistaceae
Cistus Irgel Leaf Decoct Oral 1. 3.3 0. (Saadi et No data
creticus ion 28 3 11 al., 2013)
L.
CABT03
6

Cistus Tirgelt Leaf Decoct Oral 1. 33. 0. (Saadi et No data


salviifoli ion 11 33 07 al., 2013)
us L.
CABT03
7
Cucurbit
aceae Aferziz Seed Decoct External 1. 16. 0. (Abouri et (Allali et
Citrullus ion use 25 67 13 al., 2012 ; al., 2008 ;
colocynth and Bellakhdar Bahmani
is (L.) powde et al., 1991 ; et al.,
Benkhnigue 2014 ;
Schrad. r et al., 2014 ; Boukef,
CABT03 Eddouks et 1986 ;
8 al., 2002 ; El Ezuruike
Amrani et and
al., 2010 ; El Prieto,
Rhaffari and 2014 ; Le
Zaid, 2000 ; Floch,
Ghourri et 1983 ;
al., 2013 ; Lev and
Jamila and Amar,
Mostafa, 2002 ;
2014 ; Saadi Mukherje
et al., 2013 ; e et al.,
Tahraoui et 2006 ;
al., Nowband
2007 ; Ziyya egani et
t et al., 1997) al., 2015 ;
Telli et
al., 2016 ;
Yaseen et
al., 2015)

Cucumis Lkhiar Fruit Raw Oral 1. 38. 0. (Benkhnigu (Yaseen


sativus L. 08 46 11 e et al., et al.,
CABT04 2014 ; 2015)
8 Ghourri et
al., 2013)
Dracaena
ceae Ajgal Stem Decoct Oral 1. 75. 0. No data No data

14
Dracaen and ion 00 00 13
a draco leaf
subsp.
ajgal
Benabid
& Cuzin
CABT05
7
Ephedrac
eae Tougel Stem Decoct Oral 1. 36. 0. No data No data
Ephedra argan , leaf ion 00 84 16
altissima and
Desf. whol
CABT06 e
2 plant
Euphorbi
aceae Tikiout/Dag Stem Powde Oral 1. 16. 0. (Abouri et No data
Euphorbi hmouss and r 09 67 24 al., 2012 ;
a leaf Benkhnigue
officinar et al.,
um 2014 ;
subsp. Ghourri et
echinus al., 2013)
(Hook. f.
& Coss.)
Vindt
CABT06
8

Euphorbi Tikiout/Dag Stem Powde Oral 1. 33. 0. No data No data


a hmouss and r 22 33 13
officinar leaf
um L.
subsp.
officinar
um
CABT06
9
Fabaceae
Ceratoni Tikida/Lkh Leaf Decoct Oral 1. 8.7 0. (Ghourri et No data
a siliqua aroub and ion 12 0 13 al., 2013 ;
L. seed and Benkhnigue
CABT03 powde et al., 2014)
0 r

Glycine Soja Seed Macer Oral 1. 37. 0. (Abouri et No data


max (L.) ation 00 50 07 al., 2012 ;
Merr. and Jouad et al.,
CABT07 raw 2001 ;
6 Tahraoui et

15
al., 2007)

Lupinus Ibawn Seed Powde Oral 1. 60. 0. (Benkhnigu No data


angustifo dekouk r 00 00 07 e et al.,
lius L. 2014)
CABT10
4

Trigonell Lhelba/Tifi Seed Decoct Oral 1. 20. 0. (Abouri et (Ahmad


a das ion 37 00 31 al., 2012 ; et al.,
foenum- and Bellakhdar 2009 ;
graecum powde et al., Allali et
L. r 1991 ; al.,
CABT17 Benkhnigue 2008 ;
0 et al., Bahmani
2014 ; et al.,
Bouayyadi 2014 ;
et al., Miara et
2015 ; al.,
Eddouks et 2013 ;
al., 2002 ; Mukherj
El Amrani ee et al.,
et al., 2006 ;
2010 ; El Nowban
Hafian et degani et
al., 2014 ; al.,
Fadil et al., 2015 ;
2015 ; Telli et
Ghourri et al.,
al., 2013 ; 2016 ;
Hachi et al., Yaseen
2015 ; et al.,
Jamila and, 2015)
Mostafa,
2014 ; Orch
et al.,
2015 ;
Saadi et al.,
2013 ;
Tahraoui et
al., 2007 ;
Ziyyat et
al., 1997)
Lamiacea
e Timerna Stem Powde Oral 1. 11. 0. (Abouri et (Allali et
Ajuga iva nzenkhad/ and r 40 90 11 al., 2012 ; al. 2008 ;
(L.) Chndkoura leaf Benkhnigue Miara et
Schreb. et al., al.,
CABT00 2014 ; El 2013 ;
2 Amrani et Rebbas

16
al., 2010 ; et al.,
El Rhaffari 2012 ;
and Zaid, Telli et
2000 ; al.,
Ghourri et 2016)
al., 2013 ;
Orch et al.,
2015 ;
Tahraoui et
al.,
2007 ; Ziyy
at et al.,
1997)

Lavandul Timzeria Stem Decoct Oral 1. 15. 0. (Benkhnigu No data


a dentata and ion, 42 26 64 e et al.,
L. leaf infusio 2014 ;
CABT09 n and Eddouks et
4 raw al., 2002 ;
Orch et al.,
2015 ;
Ziyyat et
al., 1997)

Lavandul Igazioen Stem Decoct Oral 1. 38. 0. (Abouri et No data


a and ion 00 89 16 al., 2012 ;
marocca leaf Saadi et al.,
na Murb. 2013)
CABT09
5

Lavandul Imzeria/Tik Leaf Decoct Oral 1. 61. 0. (Benkhnigu (Allali et


a enkert ion 00 11 24 e et al., al.,
stoechas 2014 ; 2008)
L. Bouayyadi
CABT09 et al.,
8 2015 ;
Ghourri et
al., 2013 ;
Jamila and
Mostafa,
2014 ;
Tahraoui et
al., 2007)

Marrubiu Mriwt/Ifzi Leaf Decoct Oral 1. 6.6 0. (Bellakhdar (Allali et


m ion 43 7 29 et al., al.,
vulgare 1991 ; 2008 ;
L. Benkhnigue Telli et
CABT10 et al., al.,

17
8 2014 ; 2016)
Eddouks et
al., 2002 ;
El Amrani
et al.,
2010 ; El
Hafian et
al., 2014 ;
El Rhaffari
and Zaid,
2000 ;
Ghourri et
al., 2013 ;
Orch et al.,
2015 ;
Saadi et al.,
2013 ;
Tahraoui et
al., 2007 ;
Ziyyat et
al., 1997)

Salvia Salmia Leaf Decoct Oral 1. 46. 0. (Abouri et (Telli et


officinali ion 43 67 31 al., 2012 ; al., 2016
s L. and Benkhnigue
CABT15 infusio et al.,
7 n 2014 ;
Bouayyadi
et al.,
2015 ; El
Amrani et
al., 2010 ;
El Hafian et
al., 2014 ;
Ghourri et
al., 2013 ;
Hachi et al.,
2015 ;
Jamila and
Mostafa,
2014 ; Orch
et al.,
2015 ;
Saadi et al.,
2013 ;
Tahraoui et
al., 2007 ;
Ziyyat et
al., 1997)

18
Teucrium Tawerart/Fl Leaf Decoct Oral 1. 47. 0. (Bahmani (Altunda
polium L. you lbour ion 00 83 24 et al., g and
CABT16 and 2014 ; El Ozturk
4 powde Amrani et 2011 ;
r al., 2010 ; zdemir
Saadi et al., and
2013) Alpnar,
2015 ;
Telli et
al.,
2016)

Thymus Asserkna Leaf Infusio Oral 1. 10. 0. (Abouri et No data


saturejoi n, 17 85 51 al., 2012 ;
des Coss. powde Benkhnigue
CABT16 r, and et al.,
9 macera 2014 ;
tion Saadi et al.,
2013 ;
Tahraoui et
al., 2007)
Lythrace
ae Rman Peric Decoct Oral 1. 24. 0. (Abouri et (Allali et
Punica arp ion, 22 39 22 al., 2012 ; al.,
granatum infusio Benkhnigue 2008 ;
L. n, and et al., Mukherj
CABT14 powde 2014 ; Edd ee et al.,
3 r ouks et al., 2006 ;
2002 ; El Semenya
Amrani et et al.,
al., 2010 ; 2012 ;
Ghourri et Telli et
al., 2013 ; al.,
Tahraoui et 2016)
al., 2007)
Moracea
e Tazart/Lkar Fruit Decoct Oral 1. 40. 0. (Abouri et (Yaseen
Ficus mous ion 30 00 09 al., 2012 ; et al.,
carica L. Benkhnigue 2015)
CABT07 et al.,
2 2014 ;
Tahraoui et
al., 2007 ;
Ziyyat et
al., 1997)
Myristica
cea Lgouza Seed Powde Oral 1. 20. 0. (El Hafian No data
Myristica r 13 00 07 et al., 2014)
fragrans
Houtt.

19
CABT11
6
Oleaceae
Olea Jbouj/Azmo Leaf Decoct Oral 1. 40. 0. (Abouri et (Allali et
europaea ur/ Zitoun ion, 18 91 20 al., 2012 ; al.,
L. macera Benkhnigue 2008 ;
CABT12 tion et al., Keter
2 and 2014 ; and
powde Bouayyadi Mutiso,
r et al., 2012 ;
2015 ; Nowban
Eddouks et degani et
al., 2002 ; al.,
El Amrani 2015 ;
et al., Sargin,
2010 ; 2015 ;
Ghourri et Telli et
al., 2013 ; al.,
Hachi et al., 2016)
2015 ;
Jamila and
Mostafa,
2014 ; Orch
et al.,
2015 ;
Saadi et al.,
2013 ;
Tahraoui et
al., 2007 ;
Ziyyat et
al., 1997)

Papavera
ceae Belaaman Seed Powde Oral 1. 37. 0. (Bahmani (Allali et
Papaver r 13 5 07 et al., 2014) al.,
rhoeas L. 2008)
CABT12
6
Rhamnac
eae Nbeg/Azou Leaf Decoct Oral 1. 22. 0. (Abouri et (Allali et
Ziziphus ggar ion 19 58 16 al., al.,
lotus (L.) and 2012 ; Ben 2008 ;
Lam. powde khnigue et Telli et
CABT18 r al., 2014 ; al.,
0 El Amrani 2016)
et al.,
2010 ;
Ghourri et
al., 2013 ;
Tahraoui et

20
al., 2007)
Rosaceae
Prunus Louz imrzig Seed Raw Oral 1. 42. 0. (Eddouks et (Sargin,
dulcis 14 86 13 al., 2002 ; 2015 ;
(Mill.) D. Ghourri et Yaseen
A. Webb al., 2013 ; et al.,
CABT14 Orch et al., 2015)
2 2015 ;
Tahraoui et
al., 2007)
Sapotace
ae Argan Seed Raw Oral 1. 9.8 0. (Abouri et No data
Argania 33 5 29 al., 2012 ;
spinosa Benkhnigue
(L.) et al.,
Skeels 2014 ;
CABT01 Ghourri et
1 al., 2013 ;
Saadi et al.,
2013)
Theaceae
Camellia Attay Leaf Infusio Oral 1. 33. 0. (Benkhnigu No data
sinensis n 17 33 04 e et al.,
(L.) 2014 ;
Kuntze Ghourri et
CABT02 al., 2013)
3
Urticacea
e Taznagt/Tig Stem Decoct Oral 1. 22. 0. (Bahmani (Altunda
Urtica zenin/ and ion 36 73 11 et al., g and
dioica L. Lhriga leaf 2014 ; Ozturk
CABT17 Benkhnigue 2011)
1 et al.,
2014 ;
Jamila and
Mostafa,
2014 ; Orch
et al., 2015)

The medicinal uses of plants collected in our study were compared with other ethnobotanical
surveys of plants used traditionally in treating diabetes mellitus in Morocco and in other parts
of the world (Table 1). The frequency of citation of medicinal plants in literature constitutes a
probable evidence of their activity. The review of the available literature showed that in
Morocco, among the 48 collected species, 41 were described as antidiabetic plants and 7 were

21
reported here for the first time as antidiabetic plants (Table 1). The ethnobotanical studies
conducted out of Morocco showed that among these 41 medicinal plant species only 23
species were reported as antidiabetic plants (Table 1). Also of interest, the present
investigation has revealed that 25 plant species were used only in Morocco and four of which
are endemic (Argania spinosa, Lavandula maroccana Murb., Dracaena draco subsp. ajgal
Benabid & Cuzin and Euphorbia officinarum L. subsp. officinarum). The medicinal plants
reported in this work and in previous research; Allium sativum, Ajuga iva, Artemisia herba-
alba, Carum carvi, Citrullus colocynthis (L.) Schrad., Marrubium vulgare, Olea europaea L.,
Salvia officinalis and Trigonella foenum-graecum have been frequently reported as being
used for the management of the diabetes (Table 1).
However, despite their wide use as antidiabetic some of the inventoried plant species are
toxic. The main toxic plants are Nerium oleander L. (Al-Yahya et al., 2000; Bousliman et al.,
2012; Eddouks et al., 2007), Citrullus colocynthis (Al-Yahya et al., 2000; Marzouk et al.,
2010), Euphorbia officinarum L. (Daoubi et al., 2007), Myristica fragrans Houtt. (Bousliman
et al., 2012). The toxicity of Myristica fragrans has been validated experimentally in vitro in
several studies (El Malti et al., 2008; El-Alfy et al., 2009). Known in Morocco as Lgouza,
Myristica fragrans possess psychoactive properties and at high doses is considered a cheap
substitute to several drugs (El-Alfy et al., 2009). Myristica fragrans is traditionally largely
used for spice and medicinal purposes (Merzouki et al., 2000; Mollik et al., 2010; Morita et
al., 2003; Ram et al., 1996).
Fortunately, most of the healers are aware of the toxicity of these plants which are used in the
treatment of the diabetes in Morocco. Furthermore, despite their toxicity, these plant species
are used in traditional medicine to treat various diseases as reported in several studies; Nerium
oleander (Eddouks et al., 2002, Merzouki et al., 2000), Citrullus colocynthis (Merzouki et al.,
2000; Eddouks et al., 2002), Euphorbia officinarum (Abouri et al., 2012).
3.4. New reports and new uses
Comparative literature analysis suggests that two endemic subspecies (Dracaena draco subsp.
ajgal and Euphorbia officinarum subsp. officinarum) and four plant species (Eryngium
ilicifolium Lam., Pastinaca sativa L., Scorzonera undulata, Ephedra altissima Desf.) are
described for the first time for treating diabetes. This finding is an important contribution to
the indigenous knowledge of the medicinal plants. The majority of these plants have been
reported as medicinal plants in the treatment of other diseases. Eryngium ilicifolium has been
reported for pharyngitis disease (Warda et al., 2009). Pastinaca sativa was used to improve
milk production and appetite and has also digestive and diuretic properties (Jari et al., 2007).

22
Ephedra altissima has been used to treat respiratory diseases and vascular hypertension
(Hammiche and Maiza 2006). Scorzonera undulata used, in Algeria, as diuretic, emollient,
sudorific and depurative (Rebbas et al., 2012). Euphorbia officinarum subsp. officinarum,
endemic subspecies of Morocco, has been used for respiratory, circulatory and skeleton
ailments in Agadir Ida Ou Tanane Province in Morocco (Ouhaddou et al., 2014). Dracaena
draco subsp. ajgal was described here for the first time as medicinal plant. This subspecies
was discovered in Morocco in 1996 by Benabid and Cuzin (1996) and is very close to
Dracaena draco subsp. draco of the Canary islands which is a rich source of phenolic
compounds (Santos et al., 2011). Other species of Dracaena genus were known for the
treatment of diabetes, this is the case of Dracaena arborea (Willd.) Link in Togo, Kpodar
(2015) and Dracaena cochinchinensis S. C. Chen in China (Li and al., 2014). However, the
exact mechanism of hypoglycemic effect needs further analysis for the discovery of potential
new antidiabetic drugs. Finally, in this work, Pistacia atlantica Desf. is mentioned for the first
time in Morocco as a remedy against diabetes; this plant has been recently reported in the
treatment of diabetes in Algeria (Telli et al., 2016)
3.5. Plant parts used, mode of preparation and administration
Leaves were the most used plant part with a percentage of 38%, followed by seeds (23%),
stems (14%), flowers and fruits (7% each) and roots (5%). Pericarps, bulbs and whole plants
were rarely used (Figure 3). Previous studies have reported leaves as the mainly used plant
parts in the treatment of diabetes Orch et al. (2015) and Hachi et al. (2015) in Morocco, Keter
and Mutiso (2012) in Kenya, Kpodar et al.( 2015) in Togo, Yaseen et al. (2015) in Pakistan.
The use of leaves to treat diseases is based on the fact that leaves are the main photosynthetic
organs and constitute the parts relatively most easily accessible and available throughout the
year (Fzan et al., 2008). The results showed that aerial plant parts play an important role in
herbal medicine preparation in the study area, agreeing with the results of Abouri et al.
(2012), Jamila and Mostafa (2014), Saadi et al. (2013), in Morocco and in other countries
(Benarba et al., 2015; Boughrara and Belgacem, 2016, Kadir et al., 2012; Katemo et al., 2012;
Kpodar, et al., 2015; Nowbandegani et al., 2015; Telli et al., 2016; Yetein et al., 2013).

23
Figure 3 : Plant parts used (%)
The decoction was the main mode of preparation of herbal medicines accounting for 41%
followed by powder preparation (23%), infusion (15%), raw form (13%), maceration (6%)
and inhalation (3%) (Figure 4). This finding is in agreement with other ethnobotanical studies
where decoction was the most frequently mode of preparation (Afolayan et al., 2014;
Bahmani et al., 2014; El-Hilaly et al., 2003; Kadir et al., 2012; Nowbandegani et al., 2015;
Tahraoui et al., 2007; Urso et al., 2016; Ziyyat et al., 1997). The great majority of the
remedies were taken orally (96 %) usually drunk as teas. Similar types of results were
obtained in other studies (Benarba et al., 2015; Semenya et al., 2012).

Figure 4 : Percentage of types of administration

24
4. Conclusion
This study is the first to focus on ethnopharmacologgical knowledge of plants used in the
treatment of diabetes in Central Morocco. The investigation revealed that folk medicine
continues to play an important role in the healthcare system for the local people. Forty-eight
medicinal plants belonging to 44 genera and 25 families are used for treating diabetes in the
study area. Six plants are reported for the first time as used in traditional treatment of diabetes
and 1 plant was new medicinal plant to treat diabetes in Morocco. The current study
represents a useful documentation, which can contribute to preserving knowledge on the use
of medicinal plants in this region.

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