Evidence-Based Complementary and Alternative Medicine
Volume 2021 (2021), Article ID 5515634, 16 pages
https://doi.org/10.1155/2021/5515634

Research Article

Ethnobotanical Survey of Medicinal Plants Used by Traditional Healers to Treat Diabetes in the Taza Region of Morocco

Hanae Naceiri Mrabti,¹ Abdelhakim Bouyahya,² Nidal Naceiri Mrabti,³ Nidal Jaradat,⁴ Latifa Doudach,⁵ and My El Abbes Faouzi¹

¹Laboratory of Pharmacology and Toxicology, Bio Pharmaceutical and Toxicological Analysis Research Team, Faculty of Medicine and Pharmacy, Mohammed V University in Rabat, BP 6203, Rabat, Morocco
²Laboratory of Human Pathologies Biology, Department of Biology, Faculty of Sciences, and Genomic Center of Human Pathologies, Mohammed V University in Rabat, Rabat, Morocco
³Computer Chemistry and Modeling Team, Laboratory of Materials, Modeling and Environmental Engineering, LIMME, Faculty of Sciences Dhar El Mehraz, Sidi Mohammed Ben Abdellah University, USMBA, BP.1796, 30000, Atlas, Fez, Morocco
⁴Department of Pharmacy, Faculty of Medicine and Health Sciences, An-Najah National University, P.O. Box 7, Nablus, State of Palestine
⁵Department of Biomedical Engineering Medical, National School of Arts and Crafts Rabat (ENSAM), Mohammed V University, BP 6203, Rabat, Morocco

Correspondence should be addressed to Hanae Naceiri Mrabti; naceiri.mrabti.hanae@gmail.com and Abdelhakim Bouyahya; boyahyaa-90@hotmail.fr

Received 5 February 2021; Revised 4 April 2021; Accepted 13 April 2021; Published 26 April 2021

Academic Editor: Ahmed Mediani

Copyright © 2021 Hanae Naceiri Mrabti et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

Type 2 diabetes is one of the noncommunicable diseases that is becoming a pandemic in Africa. In Morocco, traditional healers have started to use herbal medicines for the treatment of diabetes either individually or in combination with food. The current study aimed to perform an ethnobiological survey of antidiabetic plants use in the Taza region of Morocco. A total of 193 traditional healers were interviewed using a semistructured questionnaire. Data collected were analyzed utilizing the use value (UV), fidelity level (FL), and relative frequency citation (RFC) indices. Forty-six plant species belonging to 28 families were recorded for the treatment of diabetes in the Taza region of Morocco. The most frequently cited plant species are Salvia officinalis, Marrubium vulgare, and Ajuga iva. Lamiaceae, Asteraceae, and Fabaceae were the most reported families. Leaves are the most used part of plants to prepare drugs, the decoction is the preferred mode of preparation, and remedies are often administered orally. Interestingly, Cytisus battandieri, Urginea maritima, Plantago ovata, and Ziziphus jujuba were reported as new medicinal plants used to treat diabetes in the Taza region of Morocco. People in the Taza region still rely on indigenous plants for their basic healthcare needs. Further research should be carried out to validate the antidiabetic effect of the newly reported plant species. This validation can be investigated by the determination of bioactive compounds and evaluation of their in vitro and in vivo antidiabetic effects.

1. Introduction

Herbal medicine is an alternative or a parallel treatment in many acute and chronic diseases. It is generating renewed interest in many countries around the world, particularly in North Africa. Indeed, a large number of plants are used in traditional medicine in Morocco, including some for the treatment of diabetes [1]. Despite the presence of antidiabetic drugs known on the pharmaceutical market, herbal remedies are importantly used to treat this disease [2]. Indeed, good knowledge and authentication of medicinal species in particularly by their vernacular names can avoid the problems of their side effects and toxicities [3]. However, for millennia, herbal medicines have been a valuable source of therapeutic agents, and many of today's drugs are inspired from natural herbal plants or their derivatives [4].

Scientific research on traditional herbal remedies for diabetes can provide valuable leads for the development of alternative medicines and strategies [5, 6]. Despite numerous studies carried out in Morocco to bring up rational science about the use of plants by the local populations [1, 7–9], there is still a need to pursue investigation in order to have a comprehensive database on medicinal plants used for diabetes management. The available literature showed several Moroccan medicinal species with antidiabetic properties [6]. Although some of these plants have a great reputation in traditional medicine, many remain to be scientifically demonstrated [10].

In Morocco, as in developing countries, the use of traditional medicine is widespread, and several herbal remedies used individually or in combination with conventional medicines are recommended to treat diabetes [8]. Indeed, recently an ethnobotanical survey was carried out in the Beni Mellal region of Morocco [11] to collect the data about the traditional herbal medicine used for diabetes treatment in this region. So far, no scientific investigation has been carried out in the Taza region. Therefore, the current study aims to perform an ethnopharmacological survey on traditional knowledge of medicinal plants used to treat diabetes in the Taza region.

2. Materials and Methods

2.1. Study Area

This study was conducted in the province of Taza, situated in the northeast of Morocco. It is bounded by the Rif in the North, the Middle Atlas in the South, the Rharb plain in the West, and the Guercif plain in the East (Figure 1); it constitutes the northern termination of the Middle Atlas and extends over a length of 50 km and a width of 15 km. The altitudes are between 500 and 1980 m. The temperature varies between 3.2 and 44.5°C. Although annual rainfall in this region has ranged between 84 and 120 mm over the last 8 years [12], the climate is subtropical to tropical, very dry on the coast, and wetter at altitude.

Figure 1: Map of the study area.

2.2. Ethnobotanical Survey

An ethnobotanical survey was conducted from March 2019 to February 2020, and before starting the collection of ethnobotanical data, a brief explanation to the informants on the objectives of the study and the importance of the information they would provide was provided in order to obtain their consent to participate in the study. A total of 193 healers were interviewed for this purpose. The data were collected through semistructured interviews using Moroccan language (Darija). These interviews were designed to record information about the plants used to treat diabetes mellitus and their local names, the used parts of the plant, the methods of preparation, the administration of drugs, and the demographic characteristics of the study participants.

2.3. Preservation of Plant Specimens

The standard method was followed with a record to collect the plant materials, drying, mounting, preparation, and preservation in special glass frames; they were later identified by Pr. Latifa Doudach. These samples of plant material were given herbarium specimen codes, and the voucher plant samples were kept in the Herbarium of the Botany Department of the Scientific Institute of Rabat, Morocco. The complete floristic list was established after the identification and verification of the samples; the identification process included the Traditional Moroccan Pharmacopeia [13], Practical Flora of Morocco [14], Moroccan Medicinal and Aromatic Plants [15], and Vascular Flora of Morocco [14] as references. The taxonomy was confirmed based on data available on the International Plant Names Index website: http://www.ipni.org/.

2.4. Data Analysis

Medicinal plants inventoried in this study were organized in alphabetical order by family. The data reported concerned family, scientific name, local name, part used the utilized preparations, main therapeutic use, and identification code. The obtained results were analyzed using specific quantitative parameters.

2.4.1. Use Value (UV)

The use value (UV) demonstrates the relative importance of plants known locally in traditional medicine [16]. Use value (UV) was calculated using the following formula:

where UV is the use value of species, U is the number of respondents who mentioned the use of the species, and n is the total number of respondents interviewed for a given species (herbalists and local population). The highest use recorded in inquiry reports for a given plant gives a rise to the highest UV value.

2.4.2. Fidelity Level (FL)

Fidelity level (FL) indicates the percentage of informants claiming the use of a certain plant species for the same major purpose [17]. The fidelity level is calculated by the following formula:

where Np is the number of informants who independently indicated the use of a species for the same major ailment and N is the total number of informants who mentioned the plant for any major ailment.

2.4.3. Relative Frequency Citation (RFC)

The collected ethnomedicinal information was quantitatively analyzed using an index of relative frequency citation (RFC) (0 < RFC < 1):

This index shows the local importance of each species, and it is given by the frequency of citation (FC, the number of informants mentioning the use of the species) divided by the total number of informants participating in the survey (N), without considering the use categories [16].

3. Results and Discussion

3.1. Demographic Features

This study enrolled 193 informants, including traditional healers, herbalists, and knowledgeable villagers represented by 169 women (87.56%) and 24 men (12.44%), and they were interviewed (Table 1). The results showed that women were more involved in the use of medicinal plants than men, and this could be explained by the activities of women at home. Indeed, they were responsible for drying, storing, and the preparation of the herbal remedy for maintaining the healthcare of their family. Their average age was 59.5 years with a minimum of 32 years and a maximum of 87 years. The age group [18–38] was the most represented with 46.11%. The majority of the respondents belong to the rural area (92%); and 84.45% are illiterate, 12.95% primary education, 2.07% secondary education, and 0.51% university education. Regarding the origin of their knowledge, the majority of them (96.89%) who participated in this survey acquired the traditional medical knowledge of their family members, mainly grandparents and parents, and this knowledge has not been documented.

Table 1: Sociodemographic characteristics and experience of herbalists.

Characteristics
Number of informants (n)
Frequency (%)

Ages (years)

    30–50
56
29.01

    50–70
89
46.11

    70–90
48
24.87

Total
193
100

Gender

    Male
24
12.44

    Female
169
87.56

Total
193
100

Education

    Illiterate
163
84.45

    Primary
25
12.95

    Secondary
4
2.07

    University
1
0.51

Total
193
100

Origin of knowledge

    Family heritage
187
96.89

    Traditional initiation
6
3.11

Total
193
100

3.2. Medicinal Plants and Floristic Analysis

This ethnobotanical survey revealed the presence of 46 plant species, belonging to 28 families used for the treatment of diabetes by participants from the Taza region, and these species were reported along with their medicinal uses and their methods of use (Table 2). The most common medicinal plant family is Lamiaceae (6 species), Asteraceae and Fabaceae (5 species each), and Apiaceae and Myrtaceae (3 species each), respectively, whereas the other families were represented with a variable number of fewer than 2 species.

Table 2: Medicinal plants used to treat diabetes in the Taza region (Morocco).

Family name
Plant species
Voucher codes
Vernacular name
Parts used
Preparation
Administration
UV
FL
RFC
Recorded literature for antidiabetic uses in Morocco
Recorded literature for antidiabetic uses out Morocco

Amaranthaceae
Chenopodium ambrosioides L.
RAB13518
Mkhinza
Leaves
Infusion
Oral
0.20
28.57
0.07
[11, 39–42]
Nd

Anacardiaceae
Pistacia atlantica Desf.
RAB 1372
Drou
Fruits
Decoction
Oral
0.11
30.00
0.05
[8, 43]
Nd

Apiaceae
Carum carvi L.
RAB7119
Lkarwya
Seeds
Decoction
Maceration
Infusion
Powder
Oral
0.16
41.67
0.06
[8, 11, 42, 44–46]
Nd

Apiaceae
Foeniculum vulgare Mill.
RAB9217
Nafaa
Seeds
Decoction
Oral
0.30
47.83
0.12
[8, 11, 40, 44–46]
Nd

Apiaceae
Ammi visnaga (L.) Lam
RAB12423
Bachnikha
Fruits
Decoction
Oral
0.35
35.29
0.09
[11, 13, 41, 45, 47–50]
Nd

Apocynaceae
Nerium oleander L.
RAB18820
Defla
Leaves
Fumigation
Inhalation
0.18
14.29
0.07
[11, 43–47, 51, 52]
nd

Asteraceae
Artemisia herba-alba Asso.
RAB43124
Chih
Stems
Leaves
Roots
Decoction
Infusion
Oral
0.90
69.35
0.32
[8, 11, 13, 41, 42, 44, 45, 47–49, 52, 53]
nd

Asteraceae
Matricaria chamomilla L.
RAB12321
Babounj
Flowers
Decoction
Infusion
Oral
0.38
29.03
0.16
[8, 11, 13, 41, 42, 44, 45, 47–49, 52, 53]
[54]

Asteraceae
Dittrichia viscosa (L.) Greuter
RAB14422
Magramane
Leaves
Roots
Decoction
Oral
1.45
32.20
0.61
[50]
nd

Asteraceae
Taraxacum officinale L.
RAB14324
Garnina
Leaves
Roots
Decoction
Powder
Oral
0.14
57.14
0.11
[55]
[56, 57]

Asteraceae
Calendula arvensis L.
RAB14312
Zwiwl
Stems
Flowers
Decoction
Oral
0.07
9.09
0.06
[58]

Brassicaceae
Lepidium sativum L.
RAB14317
Habbrchad
Seeds
Infusion
Oral
0.62
38.33
0.31
[11, 44, 59]
[60]

Cactaceae
Opuntia ficus-indica (L.) Mill.
RAB12411
Lhndia
Stems
Flowers
Decoction
Powder
Oral
0.41
20.51
0.20
[8, 11, 44]
nd

Capparaceae
Capparis spinosa L.,
RAB97161
Lekbar
Fruits
Decoction
Oral
0.32
43.48
0.12
[11, 45, 49, 53]
[61]

Cupressaceae
Tetraclinis articulata Benth.
RAB18717
Al’Araâr
Leaves
Decoction
Oral
0.19
38.10
0.11
[7, 11, 41, 45, 49, 50, 55]
nd

Ericaceae
Arbutus unedo L.,
RAB 101549
Sasnou
Leaves
Decoction
Oral
0.43
59,52
0.22
[7, 11, 41, 45, 49, 50, 55, 62, 63]
nd

Euphorbiaceae
Euphorbia resinifera Berg.
RAB14822
Ssekoum
Leaves
Decoction
Oral
0.35
57.58
0.17
[11, 18, 50]
nd

Fabaceae
Ceratonia siliqua L.,
RAB38628
Lkharoub
Leaves
Seeds
Decoction
Powder
Oral
0.26
52.63
0.10
[11, 19, 47, 50]
nd

Fabaceae
Glycine max (L.) Merr.
RAB07616
Soja
Seeds
Decoction
Powder
Oral
0.70
45.65
0.24
[8, 11]
nd

Fabaceae
Trigonella foenum-graecum L.
RAB24117
Lhelba
Seeds
Decoction
Powder
Oral
1.01
72.73
0.40
[7, 11, 13, 19, 40–42, 44, 46, 49, 53, 59]
[2, 20–23]

Fabaceae
Lupinus albus L.
RAB21118
Termes
Seeds
Powder
Oral
0.28
41.67
0.06
[11, 18, 45, 47, 55]
nd

Fabaceae
Cytisus battandieri Maire
RAB23246
Akhamelel
Leaves
Decoction
Oral
0.04
33.33
0.02
Nd
nd

Gentianaceae
Centaurium erythraea Rafn
RAB22415
Kassatlahya
Flowers
Decoction
Oral
0.44
21.21
0.17
[13, 45, 48–50, 55]
nd

Lamiaceae
Ajuga iva (L.) Schreb.
RAB04
Chndkoura
Stems
Leaves
Powder
Oral
1.16
65.78
0.94
[8, 11, 13, 41, 43, 46]
[60]

Lamiaceae
Marrubium vulgare L.
RAB47249
Mriwt
Leaves
Decoction
Oral
1.35
81.28
0.97
[8, 11, 19, 43, 44, 59]
[24, 60]

Lamiaceae
Salvia officinalis L.
RAB61862
Salmia
Leaves
Decoction
Infusion
Oral
1.63
95.34
1.00
[8, 11, 18, 19, 42, 43, 49, 53, 64]
[25–27]

Lamiaceae
Calamintha officinalis Moench
RAB6922
Manta
Leaves
Stems
Flowers
Decoction
Infusion
Oral
0.37
40.00
0.05
[11, 49, 64]
nd

Lamiaceae
Thymus broussonetii Boiss.
RAB40441
Zaitra
Leaves
Decoction
Oral
0.63
33.33
0.08
[8, 19]
nd

Lamiaceae
Rosmarinus officinalis L.
RAB8088
Azir
Leaves
Decoction
Oral
0.21
25.00
0.06
[11, 19, 44, 45, 49–51, 55]
nd

Liliaceae
Urginea maritima (L.) Baker
RAB23142
Bssallansal
Leaves
Decoction
Oral
0.01
16.67

Nd
nd

Moraceae
Ficus carica L.
RAB8217
Lkarmous/Chriha
Leaves
Decoction
Oral
0.34
16.67
0.03
[7, 8, 11, 18, 41, 44, 58]
[23]

Myristicaceae
Myristica fragrans Houtt.
RAB1161
Lgouza
Seeds
Powder
Oral
0.33
30.00
0.05
[8, 11]
[60]

Myrtaceae
Eucalyptus globulus Labill (sp.)
RAB9318
Al’Kalitouss
Leaves fruits
Decoction
Oral
0.45
33.33
0.06
[7, 11, 18, 43, 45, 49, 51, 59]
[6, 28]

Myrtaceae
Eugenia caryophyllata Thunb.
RAB41219
Qronfel
Leaves
Flowers
Decoction
Powder
Maceration
Oral
0,28
20,00
0,01
[7, 11, 45, 49, 59, 64]
nd

Myrtaceae
Myrtus communis L.
RAB49621
Arraihan
Leaves
Fruits
Decoction
Infusion
Oral
0.18
12.50
0.04
[7, 11, 41, 43–45, 49, 51, 59]
[25]

Oleaceae
Olea europea L.
RAB51119
Zaytoun
Leaves
Decoction
Oral
1.53
77.60
0.65
[8, 11, 19, 41, 43–47, 49]
[29, 60]

Papaveraceae
Papaver rhoeas L.
RAB51218
Belaaman
Seeds
Powder
Oral
0.66
23.53
0.09
[8, 11]
[25]

Plantaginaceae
Plantago ovata Forssk.
RAB003
Katouna
Seeds
Infusion
Oral
0.06
20.83
0.12
Nd
[30]

Ranunculaceae
Nigella sativa L.
RAB35821
Sanûj
Seeds
Powder
Oral
1.08
37.10
0.32
[11, 19, 43, 44, 49, 59, 64]
[2, 23, 60]

Rhamnaceae
Ziziphus lotus (L.)
RAB62218
Nbeg
Leaves
Decoction
Powder
Oral
0.50
25.00
0.02
[7, 8, 11, 41, 44, 46, 47]
[60]

Rhamnaceae
Ziziphus jujuba Mill

Zafzouf
Leaves
Decoction
Oral
0.61
22.22
0.28
Nd
[31]

Rosaceae
Prunus amygdalus Batsch
RAB55417
Louzmarr
Seeds
Raw
Oral
0.88
23.08
0.03
[7, 13, 41, 45, 47, 49, 53, 59]
[23]

Rutaceae
Citrus aurantium L.
RAB62131
Larnaj
Fruits
Raw
Oral
0.90
33,33
0,01
[44, 53]
[32]

Salicaceae
Salix alba L

Aouad lma
Leaves
Decoction
Oral
0.09
28.57
0.04
[51, 52]
nd

Urticaceae
Urtica dioica L.
AB56517
Lhriga
Stems
Leaves
Decoction
Oral
0.25
12.50
0.04
[7, 8, 11, 41, 49, 59]
[25]

Zygophyllaceae
Peganum harmala L.
RAB41116
Lharmel
Seeds
Maceration
Oral
0.01
16.67
0.03
[7, 41, 45, 49, 59]
[25, 60]

3.3. Ethnobotanical Indices

In this study, the analysis of data collected in the field allowed us to determine forty-six (46) most commonly cited plants known to most medical informants about the treatment of diabetes disease (Table 2). The obtained data were analyzed and ordered based on the value of use (UV), level of accuracy (FL), and relative citation frequency (RFC). The values of the collected plant species ranged from 0.01 to 1.63 for UV; 8.33 to 95.34% for FL, and 0.01 to 1 for RFC, respectively. Among 46 inventoried species, ten plants species identified had high FL values (FL of ˃50%), which are Salvia officinalis, Marrubium vulgare, Trigonella foenum-graecum, Olea europaea, Artemisia herba-alba, Ajuga iva, Arbutus unedo, Euphorbia resinifera, Taraxacum officinale, and Ceratonia siliqua. Likewise, while Salvia officinalis (1.00) has the highest value of RFC followed by Marrubium vulgare (0.97) and Ajuga iva (0.94), respectively. These positions correspond to the fact that these plants were reported by the highest number of informants and RFC directly depends on the number of informants mentioning the use of this plant (FC). As shown in Table 2, S. officinalis has the highest use value (1.63) followed by M. vulgare (1.53) and A. iva (1.46).

3.4. Comparative Analysis with the Ethnobotanical Literature

Four medicinal plants have been mentioned for the first time to treat diabetes. Indeed, the literature reviewed showed that these plants have not been reported by other Moroccan studies. These species include Cytisus battandieri, Urginea maritima, Plantago ovata, and Ziziphus jujuba (Table 2).

3.5. Plant Parts Used, Mode of Preparation, and Administration

The data showed that the leaves were the most used part (44%) of the medicinal plants followed by seeds (22%), flowers and fruits (10% each), stems (8%), and roots (5%) (Figure 2).

Figure 2: Medicinal use of medicinal plants of the Taza area against diabetes according to plant parts used.

The decoction was the primary mode of preparation of herbal medicines accounting for 55% followed by powder (19%), infusion (15%), raw form (5%), maceration (5%), and inhalation (2%) (Figure 3).

Figure 3: Medicinal use of medicinal plants of the Taza area against diabetes according to the preparation methods.

3.6. Antidiabetic Effects of Medicinal Plants Cited in This Survey

In vitro and in vivo antidiabetic effects of some of the cited plants in this survey were investigated. Indeed, four medicinal plants (A. iva, Arbutus unedo, Calendula arvensis, and Ziziphus lotus) were tested in vitro. Twelve plants (A. iva, Calamintha officinalis, Carum carvi, Ammi visnaga, Lepidium sativum, Chamaerops humilis, Capparis spinosa, Arbutus unedo, Eucalyptus globulus, Nigella sativa, and Urtica dioica) were tested in vivo (Table 3).

Table 3: In vitro and in vivo antidiabetic cited medicinal plants in this survey.

Species
Part used
Extracts
Dose/rate of administration
Experimental model
Key results
References

Ajuga iva
Whole plant
Aqueous extract
10 mg/kg orally
Normal and STZ-induced diabetic rats
Strong hypoglycemic effect in diabetic rats significantly decreased in plasma glucose level
[46]

Whole plant
Aqueous extract
10 mg/kg orally
Normal and STZ-induced diabetic rats
Hypolipidemic and hypoglycemic activity in diabetic rats
[65]

Aerial parts
Aqueous extract
—
α-Amylase inhibition
IC₅₀ = 0.210 ± 0.003 µg/mL
[35]

—
α-Glucosidase inhibition
IC₅₀ = 0.180 ± 0.005 µg/mL

Methanolic extract
—
α-Amylase inhibition
IC₅₀ = 0.172 ± 0.012 µg/mL

—
α-Glucosidase
IC₅₀ = 0.130 ± 0.008 µg/mL

Calamintha officinalis
Aerial part
Aqueous extract
100 mg/kg, during 3 weeks orally
Diabetes mellitus model of the mouse (high-fat diet orally)
Antidiabetic activity, a loss of weight as well as a decrease in the free fatty acid plasmatic concentrations
[66]

Aerial part
Aqueous extract
20 mg/kg, single or daily oral
Normal and STZ-induced diabetic rats
Significant hypoglycemic effect without affecting basal plasma insulin concentrations.
[67]

Carum carvi
Fruits
Aqueous extract
Single oral dose (20 mg/kg) or 14 daily doses orally
Normal and STZ-diabetic rats
Significant decreases in blood glucose levels in STZ diabetic rats without affecting basal plasma insulin concentrations but not high changes in blood glucose were observed in normal rats.
[68]

Ammi visnaga
Aerial part
Aqueous extract
Single and repeated dose of 20 mg/kg orally
Normal and STZ-induced diabetic rats
The extract possesses a significant hypoglycemic effect in both normal and STZ diabetic rats.
[69]

Lepidium sativum
Aerial part
Aqueous extract
Single dose (20 mg/kg) or chronic 15 daily repeat administration orally
Normal and STZ-induced diabetic rats
Aqueous extract of LS exhibits a potent hypoglycemic activity in rats without affecting basal plasma insulin concentrations.
[70]

Aerial part
Aqueous extract
10 mg/kg/h intravenously and orally
Normal and STZ-induced diabetic rats
Extract reduced blood glucose levels both in normal and diabetic rats. Oral administration of LS for 15 days normalized glycemia enhanced glycosuria and decreased the amount of urinary TGF-β 1 in diabetic rats. The extract caused a potent inhibition of renal glucose reabsorption, which in turn reduced blood sugar.
[71]

Chamaerops humilis
Leaves
Aqueous extract
Single and chronic dose (10 mg/kg)
Normal and obese-hyperglycemic-hyperlipidemic (OHH) Meriones shawi rats
Plant extract decreased plasma glucose levels
[72]

Capparis spinosa
Fruits
Aqueous extract
20 mg/kg orally
Normal and STZ-induced diabetic rats)
Significant antihyperglycemic activity in STZ rats without affecting basal plasma insulin concentrations
[1]

Aerial part
Aqueous extract
100 mg/kg, during 3 weeks orally
Diabetes mellitus model of the mouse (high-fat diet orally)
Antidiabetic activity, a loss of weight as well as a decrease in the free fatty acid plasmatic concentrations
[73]

Arbutus unedo
Roots
Aqueous extract
400 mg/L in the chronic treatment of streptozotocin-induced diabetic rats (intraperitoneally) 150 mg/kg in oral glucose tolerance test (orally)
Oral glucose tolerance test normal and STZ-induced diabetic rats
Decreasing in plasma glucose levels at 31.6 %.
[62, 63]

Roots
Aqueous extract

α-Amylase inhibition
IC₅₀ = 730.15 ± 0.25 µg/mL
[63]

α-Glucosidase inhibition
IC₅₀ = 94.81 ± 5.99 µg/mL

Eucalyptus globulus
Leaves
Aqueous extract
150 and 300 mg/kg body weight intraperitoneally
Single and repeated oral STZ-induced diabetic rats
Exhibited a significant, dose-dependent hypoglycemic effect in streptozotocin-induced diabetic rats. The extract significantly increased the basal plasma insulin concentrations
[74]

Nigella sativa
Seeds
Aqueous extract
2 g/kg/day orally
Short-circuit current technique oral glucose tolerance test
Inhibited the electrogenic intestinal absorption of glucose in vitro chronic treatment improved glucose tolerance in rats also reduced body weight without any toxic effect.
[75]

Seeds
Petroleum ether extract
2 g/kg/day during four-week intragastric gavage
STZ-induced diabetic rats
The petroleum ether extract exerts an insulin-sensitizing action by enhancing the activity of the two major intracellular signal transduction pathways of the hormone’s receptor.
[76]

Seeds
Ethanol extract
2 g/kg/day during four-week intragastric gavage
Oral glucose tolerance test on Meriones shawi rats
Hypoglycemic and hypolipidemic activity
[77]

Calendula arvensis
Flowers
Aqueous extract

α-Amylase
1368.27 ± 9.14 µg/mL
[78]

α-glucosidase
1121.10 ± 6.42 µg/mL

β-Galactosidase
2116.82 ± 17.57 µg/mL

Methanol extract

α-Amylase
573.37 ± 36.85 µg/mL

α-Glucosidase
848.83 ± 49.93 µg/mL

Hexane extract

β-Galactosidase
1422.66 ± 260.87 µg/mL

α-Amylase
1955 ± 28.13 µg/mL

α-Glucosidase
1722.59 ± 22.42 µg/mL

β-Galactosidase
3156.98 ± 58.17 µg/mL

Ziziphus Lotus
Roots
Catechin

α-Glucosidase inhibition
IC₅₀ = 87.55 ± 2.23 µg/mL
[79]

Fruits
Methanolic extract

α-Amylase inhibition
IC₅₀ = 31.91 ± 1.53 µg/mL

Leaves
Methanolic extract

α-Glucosidase inhibition
IC₅₀ = 27.95 ± 2.45 µg/mL

Α-Amylase inhibition
IC₅₀ = 20.40 ± 1.30 µg/mL

α-Glucosidase inhibition
IC₅₀ = 8.66 ± 0.62 µg/mL

Urtica dioica
Aerial part
Aqueous extract
250 mg/kg
Oral glucose tolerance test (OGTT) at dose 250 mg/kg in normal and alloxan-induced diabetic rats.
Strong glucose-lowering effect in normal rats and no effect in alloxan-induced diabetic rats
[80]

Urtica dioica
Aerial part
Aqueous extract
Intraperitoneally 400 mg/L in the chronic treatment of streptozotocin-induced diabetic rats. 150 mg/kg in oral glucose tolerance test
Oral glucose tolerance test STZ-induced diabetic rats
Decrease in plasma glucose levels at 31.6. Significant reduction of hyperglycemia in oral glucose tolerance.
[62]

4. Discussion

This study reports the medicinal plants used in the Taza region to treat diabetes. The demographic features showed that women were often at home during survey hours. Some previous studies have also shown this trend [7, 8, 11]. Moreover, the interviews showed that the elderly were particularly competent and had better knowledge of plants than the young; similar results have been observed in other studies where indigenous knowledge on the use of medicinal plants is still strong with the elderly [81–83]. On the other hand, results revealed that the majority of the respondents belong to rural areas and are illiterate. These results are corroborated by other studies, which have shown that illiterate people have more expertise in the uses of traditional medicine [5].

Medicinal plants diversity showed a floristic diversity. Indeed, the findings were in agreement with previous studies, where these families were the most represented in diabetes mellitus treatment in Morocco [8, 44, 47, 64], Turkey [84], and Togo [85]. The reasons for the high degree of ethnomedicinal plants of families Lamiaceae, Asteraceae, Fabaceae, Apiaceae, and Myrtaceae in the region is their wide occurrence with several traditional uses known by the local informants [8].

The survey revealed that S. officinalis, M. vulgare, and A. iva are the most used in traditional medicine to treat diabetes in this region. Literature reports showed that several of these plants have been reported in other ethnomedical surveys for the treatment of diabetes [7, 44, 45, 47]. The antidiabetic activity of certain plants has also been experimentally proven by in vivo or in vitro studies. These species include A. herba-alba [21, 33, 34], S. officinalis [27], O. europaea [29], A. iva [35], A. unedo [63], and M. vulgare [24]. Actually, certain mentioned plants open up interesting perspectives in the search for new therapeutic means, which can thus provide credible solutions by the production of low-cost and effective drugs for the treatment of diabetes.

However, the use of C. battandieri, U. maritime, P. ovate, and Z. jujube for managing diabetes has not been reported. International literature has shown P. ovate and Z. jujube have been used for diabetes in other countries like Iran [30, 31, 36]. The majority of these plants have been reported as medicinal plants in the treatment of other diseases. C. arvensis has been used as a disinfectant, antispasmodic, antipyretic, anti-inflammatory, antiepileptic, antimicrobial, and diuretic [37, 38]. Urginea maritima was used for the treatment of cardiac failure, chronic bronchitis, asthma, and diuretic [86]. Salix alba has been used for the treatment of various ailments due to its potent antipyretic, analgesic, and anti-inflammatory properties [87].

In addition, the part of the plant most frequently used in this study was the leaves, which corresponds to previous studies that declared that the leaves are part of the plant mainly used in the treatment of diabetes in Morocco [8, 11], Kenya [88], Togo [81], and Pakistan [23]. The reason for the high use of leaves can be explained by their availability and their ease of collection compared with other parts like roots, flowers, and fruits [89].

Concerning the mode of preparation, similar types of results were obtained in other studies, where decoction was the most frequent mode of preparation [11, 17, 25, 41]. The most frequently used mode of herbal remedy administration is oral ingestion (98.30 %). Today, most of the medicines were given orally, which is in agreement with other studies [11, 90, 91].

A bibliometric study was carried out to identify which cited medicinal plants were already tested in vitro and in vivo for their antidiabetic effects. In vitro investigations showed that some plants were studied in vitro. Indeed, Abudunia et al. [78] have tested the in vitro antidiabetic effects of methanolic, hexane, and aqueous extracts of C. arvensis collected from the region of Khemisset. All tested extracts exhibited enzymatic inhibitory effects on α-amylase, α-glucosidase, and β-glucosidase with some variability. Indeed, methanolic extract seems to be the most effective product, in particular, against α-amylase (IC₅₀ = 573.37 ± 36.85 µg/mL) and α-glucosidase (IC₅₀ = 848.83 ± 49.93 µg/mL). Saad et al. [35] showed that aqueous and methanolic extracts of Ajuga iva exhibited remarkable inhibition of α-amylase (IC₅₀ = 0.210 ± 0.003 and IC₅₀ = 0.180 ± 0.005 µg/mL, respectively) and α-glycosidase (IC₅₀ = 0.172 ± 0.012 and IC₅₀ = 0.130 ± 0.008 µg/mL, respectively). The authors suggested that these effects are related to the phenolic compounds present in plant extracts. Moreover, the acute toxicity evaluation on rats showed that these extracts are not toxic [35].

The root aqueous extract of A. unedo has revealed significant enzyme inhibition of α-amylase and α-glucosidase [63]. The inhibitory effect was significantly important against α-glucosidase (IC₅₀ = 94.81 ± 5.99 mg/mL). This remarkable result led Naceiri Mrabti and collaborators to fractionate the root aqueous extract of A. unedo and to isolate the major compounds. The results revealed the presence of catechin as the main compound, which was isolated and tested for its inhibitory effect against α-glucosidase [92]. Indeed, the inhibitory activity of α-glucosidase was increased (IC₅₀ = 87.55 ± 2.23 mg/mL), compared with the inhibitory activity of aqueous extract [92]. Marmouzi et al. [79] tested the methanolic extracts of leaves and fruits of Z. lotus (Rhamnaceae) showed significant inhibition of α-amylase and anti-α-glucosidase at lower concentrations with some differences between fruit and leaf extracts. Indeed, the leaf extract revealed higher inhibitory potency as anti-α-amylase and anti-α-glucosidase compared with the fruit extract for which IC₅₀ = 20.40 ± 1.30 and IC₅₀ = 8.66 ± 0.62 mg/mL, respectively [79].

However, several medicinal plants cited in this survey have shown important in vivo antidiabetic effects. U. dioica aqueous extracts were tested using the oral glucose tolerance test and intravenous glucose tolerance test and showed that the administration of extract orally at 250 mg/kg decreased glycemia significantly, which indicates a significant inhibition of glucose absorption. Moreover, using oral glucose tolerance on normal and streptozotocin-induced diabetic rats has shown that the same extract decreases plasma glucose levels at 27.4% [62]. Moreover, at the same concentration, another study revealed that the antidiabetic effect was also accompanied by hypolipidemic action [65]. Calamintha officinalis is another Moroccan antidiabetic medicinal plant that belongs to Lamiaceae family. On the other hand, Eddouks et al. [70] reported that the L. sativum aerial part aqueous extract (Brassicaceae) administered orally at 20 mg/kg exhibits a potent hypoglycemic effect without affecting basal plasma insulin. However, oral and intravenous administration of the same extract at 10 mg/kg/h in normal and STZ-induced diabetic rats caused a significant reduction of blood glucose levels in both normal and diabetic rats. Therefore, this extract normalized glycemia, enhanced glycosuria, and decreased the amount of urinary TGF-β 1 in diabetic rats. These suggest that the plant extract has a potent inhibition of renal glucose reabsorption, which reduces blood sugar [70]. Eddouks et al. [70] showed that the oral administration of C. humilis leaf aqueous extract at 10 mg/kg decreased plasma glucose levels in normal and obese-hyperglycemic-hyperlipidemic (OHH) Meriones shawi rats. Moreover, another study showed that, at the dose of 20 mg/kg, the hypoglycemia effect was also accompanied by the potent inhibition of renal glucose reabsorption [71]. However, in vitro study using short-circuit current technique revealed that the aqueous extract caused significant inhibition of the electrogenic intestinal absorption of glucose [75]. Bnouham et al. [80] studied the hypoglycemic effect of aerial part aqueous extracts of U. dioica (Urticaceae) using oral glucose tolerance test (OGTT) at a dose of 250 mg/kg in normal and alloxan-induced diabetic rats. The results showed a strong glucose-lowering effect in normal rats and no effect in alloxan-induced diabetic rats. In another work, intraperitoneal administration of aerial part aqueous extracts of this plant at a dose of 400 mg/L in the chronic treatment of streptozotocin-induced diabetic rats and 150 mg/kg in the oral glucose tolerance test caused a significant reduction of glycemia in oral glucose tolerance and plasma glucose levels [62].

The study highlighted results about antidiabetic medicinal plants as a source of antidiabetic drugs for further investigations, in particular for medicinal plants that have not been yet investigated. However, some limitations were found during this study. The first concerns the limits in the samples of traditional healers consulted because the majority of people with significant traditional knowledge refuse to provide information through the interviews. Indeed, some participants refuse to give the names of certain plants because they consider that it is a secret in itself and quickly it limits the transmission of this ancestral knowledge. The second limitation concerns the intellectual level of these traditional healers who risk passing information that is not clear enough. The number of traditional healers interviewed is also an important limitation of this study. This limit is indeed due to the low participation of traditional healers in this survey. Moreover, other difficulties related to reaching certain areas of this region because of a bad infrastructure, which justifies the reduced number of questionnaires. In addition, despite the efforts to reach some of these regions, the questionnaire has not been completed because these areas speak the Tamazight language, which we do not speak. In this sense, future work with a well-equipped research team full of linguistic skills could yield other interesting information about traditional knowledge.

5. Conclusion

This work has enabled us to inventory forty-six medicinal species used in traditional medicine in the treatment of diabetes, in the Province of Taza. The frequency of the use of medicinal plants is very linked to the profile of the interviewees; younger people generally ignore this know-how. Women and men have shared medicinal knowledge, with a slight difference in favor of the former in terms of the use of medicinal plants. The most widely used medicinal plants in the studied region belong to 28 families, the most popular of which are Lamiaceae, Asteraceae, and Fabaceae. In traditional medicine, the leaves mainly represent the parts of the plant used. The decoction is the galenic form most practiced by the local population whose oral route constitutes the most used route of administration. This study allowed us to appreciate and know the practices of traditional medicine in the treatment of diabetes, transmitted by the population in this region.

Data Availability

The data used to support the findings of this study are included within the article.

Additional Points

Highlights. Medicinal plants used by traditional healers to treat diabetes in the Taza region of Morocco were reported. Lamiaceae, Asteraceae, and Fabaceae were the most represented familiesSalvia officinalis L., Marrubium vulgare, and Ajuga iva are the most frequently used medicinal plants against diabetes.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Authors’ Contributions

Hanae Naceiri Mrabti and Latifa Doudach contributed equally in the supervision of this work.

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