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.

3. Results and Discussion

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).

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).

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.

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.