Ethnobotanical investigation on medicinal plants in Algoz area (South Kordofan), Sudan

Background The inhabitants of western Sudan use traditional medicine for the treatment of various ailments due to lack of medical doctors and unaffordable prices of pharmaceutical products. The present study is the first documentation of the traditional plant knowledge on medicinal uses of plants by healers in Algoz (South Kordofan), Sudan. Method Ethnobotanical data were collected over a period from March to November 2015 using semi-structured interviews with 30 healers (24 male and 6 female) living in the investigated area. Quantitative indices such as use categories, use value (UV) and informant consensus factor (ICF) were intended to evaluate the importance of medicinal plant species. Results A total of 94 medicinal plants, which belong to 45 families and 81 genera, were recorded in the study area. The most represented families are Leguminosae with 20 species followed by Combretaceae (6 species), Rubiaceae (5 species) and Asteraceae (4 species). The reported species were belonging to herbs (43%), trees (28%), shrubs (22%), climbers (4%) and parasites (3%). Root and stem (21% each) were the most plant parts used. A majority of remedies are administered orally (67%) where infusion (36%) and maceration (32%) are the most used methods. The highest ICF (0.87) was reported for poisonous animal bites followed by urinary system diseases (0.89), blood system disorders (0.88) and gynaecological diseases (0.87). Anastatica hierochuntica, Ctenolepis cerasiformis, Echinops longifolius, Cleome gynandra, Maerua pseudopetalosa, Martynia annua, Oldenlandia uniflora, Opuntia ficus-indica, Solanum dubium, Sonchus cornutus, Tribulus terrestris and Drimia maritima were reported for the first time in this study. Conclusion The number of medicinal plants reported in this paper reflects evidence that Algoz area had a high diversity of medicinal plants which will continue to play an important role in the healthcare system in the study area.


Background
In 2011, Sudan split into two countries with one third of the country being proclaimed a new state named "Republic of South Sudan" leaving behind the remaining area retaining the older name "the Republic of Sudan" [1]. In its former integral state, Sudan was the largest country in Africa and the tenth in the world, boasting an area of 2.5 million square kilometers which spanned diverse terrains and climatic zones [1]. This did bear directly on the wide diversity of vegetation, from those in the desert and semi-desert in the north through the equatorial in the central part to the extreme of the humid equatorial in the south. Such prevailing conditions favoured diverse vegetation consisting of 3137 documented species of flowering plants belonging to 170 families and 1280 genera, 15% of which are endemic [2]. A large number of these plants have a vital contribution to human health care needs throughout the country. Medicinal and aromatic plants and their derivatives represent an integral part of life in Sudan. Communities in different regions of Sudan use traditional medicine for the treatment of various ailments due to lack of medical doctors and unaffordable prices of pharmaceutical products beside their faith on the medicinal values of traditional medicine [3]. It has been estimated that only 11% of the population has access to formal health care [1].
The geographical position of Sudan represents a multicultural melting pot of diverse traditional knowledge over large distances and facilitated the exchange of knowledge about medicinal plants with other countries from Africa to Middle East and Asia [4].
Despite the varied flora and socio-cultural diversity in Sudan, there is a far-reaching lack of written information on the traditional use of medicinal plants [4]. So, documentation of plants used as traditional medicines in Sudan is warranted. The aim of this study was to investigate the traditional plant knowledge on medicinal uses of plants by local healers in Algoz area (South Kordofan), Sudan.

Study area
Algoz area is situated in the northern part of South Kordofan state, and its borders are Northern Kordofan state from the north and northeast, West Kordofan state from the northwest, Dellang locality from the south and Habella locality from the southeast direction (Fig. 1). It is located between latitudes 12°-12°30 N and longitudes 29°48-300 E and 622 m above sea level, with a total area of 35,000 km 2 . Short grass and short scattered trees prevail. The area is associated with exposed rocks crossing the central Sudan forming a surface water divide. The White Nile which is the main tributary of the River Nile bounds the hydrologic system to the east, while the highlands of Kordofan Plateau and the Nuba Mountains bound it to the west and the south respectively. Khor Abu Habil is a major seasonal wadi that crosses the study area and flows from the west to the east. The wadi disappears into the sand dunes a few kilometers before reaching the White Nile. The climate in the area is semiarid with long hot summers (March-September) and short mild winters (December-February). Seasonal rainfall occurs only during summer (June-September) and varies between 200 mm/year in the north and 450 mm/year in the south [5].
Algoz area has a multi-population with tribes as Dar Shungool, Gaboosh, Dar Bati, Albargo, Albarno, Flata and some Arabic nomads. They are working mainly in agriculture, animal grazing and trade [6].

Data collection and plant identification
Ethnobotanical data were collected from March to November 2015. Information about the medicinal use of plants was collected by carrying out semi-structured interviews with 30 healers (24 male and 6 female) living in the investigated area. The questionnaire was designed to collect data on (i) local names of the plants, (ii) ailments treated by the plant, (iii) plant parts used, (iv) condition of the plant material (dried or fresh) and (v) modes of preparation and administration. Some social factors like the name, age, occupation and education level of the interviewed person were also recorded. Also, the geographic locality and date of the interview were recorded. Plant specimens were collected for taxonomic identification using keys of written floras such as Broun and Massey [7], Andrews [8][9][10][11], Ross [12], Hutchinson and Dalziel [13], Maydell [14] and Elamin [15]. Voucher specimens were deposited at the Herbarium of Institute of Medicinal and Aromatic Plants, National Centre for Research, Sudan (MAPTMR-H). The botanical names and plant families are given according to the standards of the plant list (www.ipni.org/).

Ethnobotanical data analysis
Data analysis was carried out by using both the classical ethnobotanical systematic investigation and a numerical quantitative approach in order to evaluate the importance of the mentioned plant species in the investigated area. The quantitative study was carried out by calculating the following ethnobotanical indices: Use categories The medicinal plant uses were classified into categories following the standard developed by Cook [16]. Each time a plant was mentioned as "used" was considered as one "use report". If one informant used a plant to treat more than one disease in the same category, it was considered as a single use report [17].
Use value (UV) The relative importance was calculated employing the use value [18], a quantitative measure for the relative importance of species known locally: where U i is the number of use reports cited by each informant for a given species and n refers to the total number of informants. Use values are high when there are many use reports for a plant, implying that the plant is important, and approach zero (0) when there are few reports related to its use. The use value, however, does not distinguish whether a plant is used for single or multiple purposes.
Informant consensus factor To test homogeneity of knowledge, the informant consensus factor was used [19]: where N ur refers to the number of use reports for a particular use category and N t refers to the number of taxa used for a particular use category by all informants. Informant consensus factor (ICF) values are low (near 0) if plants are chosen randomly or if there is no exchange of information about their use among informants and approach one (1) when there is a well-defined selection criterion in the community and/or if information is exchanged between informants [20].

Medicinal plant diversity
A total of 94 medicinal plants, which belong to 45 families and 81 genera, were recorded in the study area. Results provide the following information for each species: scientific name, botanical family, local common name, plant habitat, plant part used, disease treated, route of administration and use value (

Habitat of the plants
Analysis of data based on their habitat showed that the reported species belong to herbs (43%), trees (28%), shrubs (22%), climbers (4%) and parasites (3%) (Fig. 2). The majority of medicinal plants are collected from the wild, and only 11% are cultivated or purchased (0.01%) from the market ( Table 1).

Parts of medicinal plants used
Data on different plant parts used in traditional medicine are indicated in Fig. 3. Those that are used the most were the root and stem (21% each) followed by the fruit (15%), whole plant (14%), seed (12%), leaf (11%), gum/latex, bulb/corm and heartwood (0.02%) and flower (0.01%) respectively. There are cases where different parts of the same plant are being used for the treatment of different diseases.

Method of preparation
A majority of remedies are administered orally (67%) where infusion (36%) and maceration (32%) are the most used methods. Some prescriptions can be prepared by both methods: infusion or maceration represented 13%, while decoction represented 11% of preparations. Dried powder or freshly collected plant parts are also used. Other prescriptions are used externally (33%)

Medicinal plants used in combination
For the treatment of particular ailment, sometimes herbalists used more than one plant. For example, Allium sativum bulb is mixed with Zingiber officinale rhizome and applied to the anus for the treatment of haemorrhoids. A potion is prepared from the seed of Trigonella foenum-graecum, curcuma, Negilla sativa and bee honey for the treatment of uterus inflammation. Root of Tinospora bakis is mixed with Syzygium aromaticum (clove) for the treatment of malaria. Atroon is added to some preparations like those of Ziziphus spina-christi and Acacia oerfota for the treatment of dysentery and toothache respectively.

Quantitative analyses of ethnomedicinal data Informant consensus factor
Fifteen ailment categories were identified. The ICF was calculated for each ailment category, and the range was from 0.50 to 0.91 (Table 3). The highest ICF (0.91) was reported for poisonous animal bites with 8 species and 77 use reports, followed by urinary system diseases (0.89) with 17 species and 156 use reports, blood system disorders (0.88) with 14 species and 116 use reports and gynaecological diseases (0.87) with 12 species and 86 use reports. The highest ICF for poisonous animal bites can be probably related to the hard and dangerous environmental conditions. The category of plants used for treatment of eye diseases has the lowest degree of consensus (0.50) where only three informants mentioned ailments in this category.

Most frequently cited plant species and medicinal uses
In this study, the most cited plants, those that had at least 20 or more citations for specific ailment, were Guiera senegalensis (57 citations) mainly used for the treatment of malaria (22 citations) and kidney disorders (20 citations). This is followed by Hydnora abyssinica (55 citations) used in the treatment of gastrointestinal system diseases (mainly for diarrhoea and dysentery (40 citations), Geigeria alata (50 citations) used mainly for the treatment of diabetes (20 citations) and hypertension (17 citations), Kigelia africana (32 citations) with 28 citations for the treatment of breast swellings and Carissa spinarum (28 citations) for envy eye.

Medicinal plants and the associated knowledge
Thirty healers (24 male and 6 female) were interviewed and divided into five different age groups (20-30, 31-40, 41-50, 51-60 and > 60). Analysis of the result on ages of healers revealed that the most dominant age of men is 41-50 while for women which were few in number is > 60 (Figs. 3 and 4).

Discussion
In this study, the most cited plants, Guiera senegalensis, Hydnora abyssinica, Geigeria alata, Kigelia africana and Carissa spinarum, were previously reported with the same traditional uses in ethnobotanical studies from other regions of Sudan. For example, Guiera senegalensis was reported by EL-Kamali [3] and Suleiman [21] for the treatment of malaria. Hydnora abyssinica (H. johannis) for the treatment of diarrhoea and dysentery and Kigelia africana for the treatment of breast swellings were also reported by Musa et al. [22]. Geigeria alata for the treatment of diabetes was reported by EL-Kamali [3] and Suleiman [21]. Carissa spinarum (C. edulis) was reported by EL-Kamali [3] for charm and the treatment of madness. Kigelia africana was reported by Doka and Yagi [23] for swollen mastitis. The high frequency of citations of medicinal plants can be explained by the fact that these plants are the best known and have long been used by the majority of informants, representing a source of reliability. In fact, many biological activity and phytochemical evaluation were carried out for these plants. For example, Traore-Keita et al. [24] reported that the chloroform extract of roots of Guiera senegalensis exhibited a pronounced antimalarial activity. They isolated two alkaloids, namely, harman and tetrahydroharman, that displayed high antimalarial activity (IC 50 (50% inhibition) lower than 4 μg/mL) and low toxicity against human leukemia monocytic cell line (THP1). Yagi et al. [25] found that Hydnora johannis roots have no activity against bacteria spp. that are mainly responsible of diarrhoea but are rich in phenols. They suggested that the curing potency of the roots of H. johannis was not mainly associated with the presence of antibacterial activity agent(s) against bacterial species responsible of dysentery or diarrhoea but might be attributed to the role of tannins in reducing the effect through denaturing the proteins by the formation of protein tannate, thereby causing the intestinal mucosa to become more resistant, reducing the intestinal transit and by acting as a barrier against toxin exerted by bacteria. The antidiabetic potential of Geigeria alata root was evaluated, and diabetic rats dosed with 250 mg/kg of aqueous methanolic extract were found to have significantly (p < 0.05) decreased blood glucose level closer to that of nondiabetic rats and improved β-cell function and antioxidant status [26]. Kigelia africana was found to suppress the breast MCF7 [27], human colon adenocarcinoma (Caco-2), human embryonic kidney (HEK-293) [28] and HeLa cervical cancer cell proliferation [29].

Comparative review of traditional usages of reported species with previous studies from Sudan
A comparative review with previous reports [3,[21][22][23][30][31][32][33] from different parts of Sudan was performed to identify the new medicinal plants and new uses reported in this study ( Table 4). The plants reported by Suleiman [21] for traditional plants used by communities of Northern Kordofan region included a total of 44 plant species with 22 species with same traditional uses which

Setaria acromelaena Evil eye
Solanum dubium Jaundice treat diabetes, but in this study, it is used also for menstrual cramps. The fruit of Senna occidentalis is reported to treat eczema beside its common use as a laxative. Plicosepalus acaciae is commonly used to enhance wound healing and as a lactagogue, but in this study, the smoke fumigant of the seeds is reported to repel insect from ear. New species and new uses for species are reported for the first time in this study. For example, Urine retention Gonorrhoea 4 Anastatica hierochuntica, Ctenolepis cerasiformis, Echinops longifolius, Cleome gynandra, Maerua pseudopetalosa, Martynia annua, Oldenlandia uniflora, Opuntia ficus-indica, Solanum dubium, Sonchus cornutus, Tribulus terrestris and Drimia maritima were not being mentioned in any previous study for the traditional Sudanese medicine. Acanthorrhinum ramosissimum, Cleome viscosa and Setaria acromelaena which were used for evil eye were also reported for the first time.
The majorities of the healers declared that they had learned about medicinal plants from their parents or grandparents. The lack of systematic documentation for medicinal plant knowledge which appears to occur in many parts of the world may contribute to the loss of this knowledge, particularly for plants that are neglected or non-preferred [34][35][36].

Conclusion
The number of medicinal plants reported in this paper reflects evidence that the Algoz area harbours a high diversity of medicinal plants that will continue to play an important role in the healthcare system in the study area. Evaluation of their claimed pharmacological potential efficacy and toxicity profile is essential. Moreover, the present study could contribute in conserving such rich heritage and providing precious information as a contribution through writing the Sudanese pharmacopeia.
Conservation of this traditional knowledge is very important. The progressing mass destruction of wild vegetation for various purposes may accelerate the disappearance of medicinal plants. This in turn may have profound consequences on the roles of traditional medicine on human health. Furthermore, the drop in the availability of raw materials due to the depletion of natural resources affects the discovery of potential drugs [37]. Thus, raising community awareness about conservation and sustainable utilization of the traditional medicinal plants is a vital part for the entire plant biodiversity [22]. Modern biotechnical approaches like genetic engineering, micropropagation via tissue encapsulation of propagules, tissue culture and fermentation should be applied to improve yield and modify the potency of medicinal plants [38].
Abbreviations ICF: Informant consensus factor; UV: Use value