Ethnopharmacobotanical study on the medicinal plants used by herbalists in Sulaymaniyah Province, Kurdistan, Iraq

Background Medicinal plants still play an important role in the Kurdish community. Sulaymaniyah Province in South Kurdistan (Iraq) has a great diversity of plants, including medicinal plants, yet very few scattered ethnobotanical studies conducted in Kurdistan are available in the scientific literature. Thus the study of Kurdish ethnobotany may be crucial for understanding local medicinal plant uses and their relationships to surrounding areas. Therefore, the objective of this investigation was to document traditional medicinal plant uses among healers of southern Kurdistan. Methods An ethnobotanical survey was conducted to document traditional knowledge on medicinal plants uses among traditional healers in the Province of Sulaymaniyah during 2014 and 2015. The data were collected by interviewing 45 traditional healers (36 males and 9 females between the ages of 25 and 80 years) who retain traditional knowledge on medicinal plants. Furthermore, the use value (UV) of taxa was determined and informant consensus factor (ICF) was calculated for the medicinal plants included in the study. Further analysis was carried out to compare the field data with the Kurdish ethnobotanical literature. Results The present study found a total of sixty-six plant species, belonging to sixty-three genera within thirty-four plant families, used to treat ninghty-nine different types of ailments and diseases. The most important family was Lamiaceae (7 species), followed by Apiaceae, Asteraceae, and Fabaceae (6 species each). The most frequently used parts were leaves (46 %), followed by flowers (15 %), and seeds (10 %). The most common preparation method was decoction (68 %), whereas few taxa were consumed as a vegetable (13 %) or ingested in powder form (10 %). The respiratory issues category had the highest ICF value (0.68), followed by inflammations and women’s diseases (0.58 and 0.54, respectively). The highest UVs were recorded for the species Zingiber officinale (0.48), Matricaria chamomilla (0.37), Adiantum capillus-veneris (0.31), Thymus vulgaris (0.31) and Pimpinella anisum (0.31). A comparison with previous ethnobotanical studies conducted in Kurdistan (especially within the territory of present-day Turkey) and surrounding areas showed that several medicinal plant reports recorded in the current investigation are new to Kurdish ethnomedicine, and that they have possibly been influenced by other scholarly medical traditions. Conclusions The present study demonstrates that the area is rich in medicinal plant knowledge. The information reported by the traditional healers of this region is invaluable for further research in the field of cross-cultural ethnobotany and ethnopharmacology.


Background
Medicinal plants have been prescribed and used widely for thousands of years to treat various disorders and ailments in traditional herbal medicine systems all over the world [1] and have considerable importance in international trade today [2]. There is an increasing demand for the utilization of medicinal plants for providing primary health care to populations, as they are extensively available and inexpensive [3]. In developing countries, approximately 80 % of the native inhabitants still rely on traditional medicine, mainly based on phytotherapy, for their primary health care [4]. The use of plants as medicine is as old as the history of mankind [5,6]. Many countries throughout the world, including Iraq [5][6][7], have their own traditional systems of healing and depend on local folk remedies and Traditional Medicine to meet their needs and treat different diseases. The WHO Traditional Medicine (TM) Strategy 2014-2023 stated that traditional treatments, traditional practitioners and herbal medicines are the main source of health care, if not the only source, for many millions of people [3]. The evaluation of these products and ensuring their safety and efficacy via registration and regulation are major challenges. Recognition of their clinical, pharmaceutical and economic value is still growing, although this varies widely between countries [2]. Nowadays, medicinal plants are not only used as regional and traditional treatments but also registered as official medicines that are verified with pharmacopoeias [8]. Medicinal plants play a major role in pharmacological research and drug development, not only when plant constituents are exploited directly as therapeutic agents, but also as starting materials for the synthesis of drugs or as models for pharmacologically active compounds [2,9,10]. In many developing countries traditional medicinal knowledge and practices have not been adequately studied, exploited or documented [11]. These traditional knowledge systems, either lost or transmitted orally from one generation to the next among traditional health practitioners, are in danger due to poor relations between older and younger generations [4,5,12]. It has been estimated that about 35,000 to 70,000 plant species are utilized for medicinal purposes globally, of which 6,500 species belong to Asia [13]. Iraq is well known for its great variation in wild plants due to the countries geographical diversity and variable climatic conditions, especially Kurdistan in which Sulaymaniyah Province is located. Traditional medicine in Iraq can be traced back to the Sumerian period (3000-1970 B.C.), and then to the Babylonian and Assyrian periods (1970-589 B.C.) [14]. Hopper and Field (1973) also reported on the useful plants and drugs of Iran and Iraq [15]. Sulaymaniyah boasts a great diversity of plant species given the regions climatic variation and diverse ecological habitats, such as mountains, hills, plains, valleys, and lakes. The different ways of life and rich culture in districts of Sulaymaniyah Province have led to a diverse local health care system. This traditional medicine system depends on the knowledge and practical experience of each individual healer with regard to diagnosing and treating ailments using natural materials. As far as the author is aware, this is the first ethnobotanical study of medicinal plants conducted in Sulaymaniyah Province, Kurdistan, Iraq. The primary objective of this study, therefore, is to identify and document the medicinal plants and associated ethnobotanical knowledge of the local people. It is hoped that these plants will be further studied in order to investigate their phytochemistry and pharmacology.

Study area
Sulaymaniyah Province (Silêmanî in Kurdish), which is located in southern Kurdistan (northeastern Iraq), is the largest Governorate in Iraqi Kurdistan (Kurdistan Regional Government). The Governorate consists of ten districts, including Rania, Pshdar, Dukan, Sharbazher, Sulaymaniyah, Penjwin, Chamchamal, Halabja, Darbandikhan, Kalar, and borders the country of Iran to the east, and the Iraqi provinces of Erbil, Kirkuk, Salah Al-Din, and Diyala to the North, West, and South respectively. The geographic coordinates (latitude and longitude) of Sulaymaniyah city, the capital of Sulaymaniyah Governorate, are 35°33′40″N and 45°26′14″E, and elevation is about 830 m above sea level. The total area of Sulaymaniyah Province is 17,023 km 2 [16,17]. Figure 1 shows the location of the study area including the districts of Sulaymaniyah Province. Sulaymaniyah's economy today relies on tourism, agriculture, the oil industry and a number of small factories, most of which are involved in the building trade [16,18]. The province features the fertile plains of Sharazur (Halabja) and Bitwen (Rania), which give way to hills and the Zagros mountain range in the northeast. The climate of Sulaymaniyah is typical for the region as the summer months (June-August) are dry and hot with an average temperature of 31.5 (°C). The winter (December-February) is much colder, wetter and windier, with occasional snowfall and an average temperature of 7.6 (°C). Rainfall, which averages about 400-600 mm per annum [16], starts in October with light storms and intensifies during the month of November and then continues until May.
conflicts, as well as 30,000 Syrian refugees, for whom the Governorate represents a safe haven. The majority of inhabitants in Sulaymaniyah Province are ethnic Sunni Muslim Kurds, but the Governorate is also home to Shiite Kurds and a number of Chaldean Christian communities. The inhabitants mostly speak Sorani Kurdish dialects with a minority of people who speak Hawrami (sub-dialect of Gorani) in some villages of Halabja District [16,18]. Although the modern health care system is easily accessible everywhere, many people still believe in alternative and complementary medicines including traditional medicine. Therefore, traditional healers continue to play a significant role in local communities.

Data collection
An ethnobotanical survey was conducted to collect data and document traditional knowledge on the medicinal plants in the province of Sulaymaniyah during 2014-2015. The survey was carried out via semi-structured interviews of traditional healers who have traditional knowledge concerning medicinal plants, adapted from the methods of [4,6,19]. The information recorded during the survey included the names and ages of the informants, local names of utilized plants, plant parts used, preparation procedures, method of administration, ailments treated, and duration of treatments (Appendix 1). The healers were chosen randomly among those living in the different districts of the Sulaymaniyah Province. In total, 45 informants, including 36 males and 9 females, between the ages of 25 and 80 years were interviewed in their local language (Kurdish Sorani). For ethical considerations connected to fieldwork, prior to conduct the interviews, permission and ethical approval were obtained from the Department of Agricultural Extension, Bakrajo Agricultural Technical Institute and Sulaimani Polytechnic University. Prior Informed Consent was always verbally obtained before each interview.

Demographic characteristics of participants
Details of the informants were ascertained and recorded via face-to-face interviews. The majority of informants were healers who practice herbal medicine; a few (five) were farmers or sellers of local products. Demographic details of the informants are provided in Table 1. The majority of informants interviewed were above 40 years of age (~62 %), and males (80 %) greatly outnumbered females (20 %). Although all traditional healers claimed to be experts in traditional medicine [14,20], only 5 % of them were licensed to dispense herbal medicine. Just over 30 % of informants lacked even primary school education, which may be related to the fact that traditional healing not only uses plants, but also involves rituals and spiritual aspects as part of the therapy [21].

Botanical identification
The collected plant specimens were prepared and processed according to the plant taxonomic method [22]. All reported medicinal species were identified with the help of the available literature and Flora of Iraq. The medicinal plant reports of a single plant were accepted as valid only if it was mentioned by at least three independent informants. Voucher specimens, collected from the wild, dried, and assigned a code, were deposited at the Herbarium at Bakrajo Agricultural Technical Institute, Sulaimani Polytechnic University. In this study, scientific names of plant species were checked for accuracy according to The Plant List database (www.plantlist.org).

Statistical analysis
The information obtained during the interviews was statistically analyzed using Microsoft Office Excel software (2010). On the basis of the data given by the informants in the study area, all the reported ailments were classified into 17 categories and the use value (UV) of taxa was determined. In addition, the informant consensus factor (ICF) was calculated for all medicinal plants included in the study. Further analysis was carried out to compare the current results with previous studies [5,8,11,12,14,19,[23][24][25][26][27][28][29][30][31][32][33][34][35][36][37] conducted in the Kurdish lands of Iraq, Iran, and Turkey in order to identify new medicinal properties of plant species which have not been reported before.

Informant consensus factor (ICF)
Informant consensus factor (ICF), which was performed for each category of disease to establish the homogeneity of the information obtained from informants, was calculated according to the formula [38]: where, Nur indicates the number of use citations from informants for a particular plant-use category, and Nt refers to the number of taxa or species utilized by all informants for that specific plant use category. ICF values range between 0 and 1, where 1 indicates the highest level of informant consent and 0 the lowest.

Use value (UV)
Use value, a quantitative method that demonstrates the relative importance of plant species known locally, was also evaluated according to the following formula [38]: where, UVi refers to the use value of a species, Ui to the number of citations per specific plant species, and Ni to the number of informants. A high use value indicates the potential importance of the plant species reported.

Medicinal plant diversity, growth habit and plant parts used
The present study found 66 plant species, belonging to 63 genera within 34 plant families, used to treat 99 different types of ailments and diseases in Sulaymaniyah Province. Table 2 lists the utilized medicinal plant species arranged in alphabetical order by scientific name, family name, English name, Kurdish name, parts used, mode of administration, preparation, medicinal uses and Use Value. The results revealed that the taxonomic family with the greatest number of utilized plants was Lamiaceae (7 species), followed closely by Apiaceae, Asteraceae and Fabaceae (6 species each), and then Rosaceae (4 species) and Malvaceae (3 species). The remaining plant families were represented by only one or two species. This     indicates the widespread importance of the abovementioned families in the study area. These results are in general agreement with previous investigations which indicated that the most prominent family was Fabaceae [20,39,40]. Figure 2 indicates that herbs (75 %) were the most abundant plants utilized by traditional healers to treat various disorders and ailments in local areas of Sulaymaniyah Province, followed by trees (13 %) and shrub species (12 %). The leaves of medicinal plants (Fig. 3) were the most frequently used parts (46 %) in herbal drugs to cure diseases; however, many other less important plant parts were also employed: flowers (15 %), seeds (10 %), roots (7 %), fruits (7 %), stems (6 %), whole plants (2 %), bulbs (2 %) and barks (2 %), as well as stalks, rhizomes, and stigmas (1 % each). These results are in accordance with what found in studies conducted in other parts of the world [1,12,41,42], which reported the predominant use of plant leaves followed by flowers, fruits and stems. On the other hand, a study conducted in India [20] indicated that roots were the most commonly utilized parts followed by leaves. This discrepancy is probably due to the diversity of plants, weather conditions, and chemical compounds present in the plant parts between the various study areas. As indicated in Table 2, in which we reported the most common preparation methods for various treatments, with instructions on how to administer them, as well as the recommended doses, the most popular preparation was the decoction (nearly 68 %), followed by the use of the plant as a vegetable (13 %), or ingested as a powder (10 %) or hydrodistillation (5 %). Similarly [13] reported that in Iran the most common mode of preparation was decoction (44 %), followed by infusion (21 %), poultice (15 %), oral applications (13 %) and hydrodistillation (7 %).

Ailments treated by plants
The traditional knowledge of phytotherapy of this province provides excellent results in the treatment of 99 different types of ailments and diseases in humans (  [43,44]. There are no prior investigations that have estimated ICF in the study area, but compared to other regions differences have been reported. In a survey conducted in Nigde/Aladaglar [37], cardiovascular diseases had the highest ICF value (0.86), whereas respiratory diseases were ranked fifth (0.61) on the list. In the study by [36] in Malatya, constipation had the highest ICF score (0.72). In contrast, in the investigation by [35] in Solhan (Bingöl, Turkey) diabetes had the highest ICF value (0.65). The high ICF value (0.68) for the respiratory issues category in traditional Kurdish medicine may be due to the fact that the region and in particular big cities have not met sufficient ecological standards. Air quality of the region may also poor due in part to a chemical weapons attacks occurring in the past decades; in addition, in recent years dust storms that have lasted for several days and even a week have hit Kurdistan. These dust storms,   [36]. As calculated by [35], in Solhan (Bingöl, Turkey), Urtica dioica (0.59), Malva neglecta (0.52), and Rosa canina (0.50) were reported to be the most important medical plants.
The high use value we recorded for Zingiber officinale (0.48) in the study area may be due in part to the fact that Kurdish ethnomedicinal knowledge has likely been influenced by Islamic traditional medicine, as mentioned in the Holy Quran [45] or addressed by Arabic scholarly medical traditions of the Middle East.
In our study we recorded in fact also some species mentioned in the Holy Quran, such as olives, ginger, garlic, basil, and castor oil plant, as well as by Muhammad, the Prophet of Islam (i.e. black cumin, chicory, fenugreek, watercress, celery, colocynth, dill, and hawthorn).
The present study shows that not all the mentioned plants are cultivated locally and most of them grow naturally in the wild. Furthermore, many plant materials pass the borders from neighboring countries without proper inspection and verification by quality control. Although pharmaceuticals are available in local areas, herbal medicine has remained popular in Kurdistan for various historical and cultural reasons. Interestingly, traditional healers mentioned that in cases in which a chemical medicine has no effect on their health, patients sometimes attempt to use herbal medicines as an alternative to chemical drugs with the hope of curing certain disorders and ailments. Therefore, documentation of local folk knowledge through ethnobotanical studies is essential for the conservation and utilization of these medical traditions [41,46]. Plants as medicine play a significant role in the public health sector worldwide, as many cultures share a strong belief in their ability to cure certain diseases [14].

Comparison with the Kurdish medical ethnobotany
Previous studies conducted in Kurdistan (Kurdish lands in current Iraq, Iran, and Turkey) reported the exploitation of some medicinal plants, which were also documented in the present study. However, this is the first ethnobotanical study in Sulaymaniyah, and thus 17 plant species and 49 new properties of plant species were found in the present investigation that have never been reported before in Kurdistan and surrounding areas (Table 4), including the use of the following: Allium roseum to alleviate abdominal and duodenal pains, and headaches; Aloe vera to relieve headaches, toothaches, and indigestion; Borago officinalis to treat cough, hoarseness, asthma, bronchitis, and abdominal pain; Curcuma longa to alleviate arthritis pain, to burn fat, and as a spice, as well as antiviral and anticancer agents; Cirsium vulgare to treat inflammations as well as urinary and digestive tract problems; Cucumis melo var. flexuosus to treat stomach pain, colon problems, diabetes, diarrhea, and intestinal inflammation; Ceratonia siliqua to alleviate abdominal pain and diarrhea; Lavandula angustifolia to cure intestinal worms and as an antispasmodic; Mentha piperita to treat flatulence, thoracic pain, indigestion, skin sensitivity, colon problems, and stomach pain, as well as an appetizing and carminative; Pelargonium roseum to treat headaches, hemorrhoids, and burns; Ranunculus ficaria to relieve haemorrhoids and arthritis; Rosa canina to treat blood cell disorders, and as a diuretic and sedative; Raphanus sativus to cure kidney stones and gallstones, for increasing breast milk, and as a diuretic; Spinacia oleracea to treat phlegm, rickets, bad breath, and tuberculosis, as well as for weight loss; Trifolium alexandrinum to cure colic; and Ziziphus jujuba to alleviate sore throat and asthma.
Of the abovementioned species a few ones, and most notably Eremurus spectabilis and Rheum ribes are prototypical plant species native to Kurdistan.
Interestingly, there are certain mixtures of different medicinal plants that are often used for a variety of purposes, for instance a mixture of Pimpinella anisum with Nigella sativa is used not only to treat menopause (menstruation), diarrhea (particularly in children), ascaris worms, sleeplessness, and colon problems, but also as an appetizing and stomachic, and for increasing breast milk. Similarly, a combination of Adiantum capillus-veneris and Crataegus azarolus with Tribulus terrestris is used to cure kidney and urinary system problems. Moreover, the current study showed that the folk remedies used by healers in Sulaymaniyah are sometimes mixtures of diverse plants, thus suggesting the influence that scholar medical systems (notably the Arabic and the Persian) may have had in shaping the ethnobotanical traditions we recorded.
For example, a combination of air-dried flowers of Althaea officinalis are ground and mixed with a little milk, then applied to burns twice daily. Also, the flowers of this plant are boiled and the decoction is then filtered and drunk after having a meal to treat cough and chest inflammation. In addition, Zingiber officinale mixed with Table 4 New folk medicinal reports for Kurdistan found in the current study powdered corn and oil is used to alleviate back pain. A number of different plants seem to be reported for the first time in this study; these uses need to be investigated pharmacologically to confirm the biological activities that have been claimed for them.
The study area is considered the most famous and important area of Kurdistan, and possibly even all of Iraq, with lofty mountains and scattered flora, many of which are still unexplored from taxonomic and medicinal points of view. Many herb species have been scientifically studied and their pharmacological properties discovered. For example, Nigella sativa has been found to possess antidiabetic, anticancer, antimicrobial, anti-inflammatory, and antioxidant properties, as well as act as an immunomodulatory, analgesic, bronchodilator, hepato-protective, renal protective, and gastro-protective, among others [47]. Salvia officinalis is another well-known herb which has demonstrated interesting pharmacological properties, such as antioxidant, anti-microbial, anti-inflammatory, analgesic, antipyretic, hemostatic, hypoglycemic and antitumor [48]. Herbalists should be aware of the side effects of the prolonged use of herbal medicines, otherwise it could possibly lead to toxic levels. For instance, as commonly known, the use of Salvia officinalis may lead to epileptic seizures, if taken in large quantities [49]. Also, not much is known about the interactions that may occur with either other medicines or food taken at the same time during the treatment period. In recent years, the use of herbal medicine has expanded dramatically in the search of new medical entities or novel lead nuclei with the prospect of managing diverse diseases [9,10].

Conclusions
The current study conducted in the Sulaymaniyah Province recorded sixty-six plant species belonging to sixty-three genera distributed across thirty-four families that have been indicated by the interviewed healers to be able to treat nighty-nine human ailments. The current study reported seventeen new medicinal species that had not been previously reported in the Kurdish ethnomedicine. The present study also demonstrates that southern Kurdistan, due to its geographical and cultural diversity, is rich in medicinal plant knowledge that can be important for being considered for treating a wide range of human ailments.
Sulaymaniyah Governorate, as part of the Kurdistan region of Iraq, has a quite well-developed health care system across the region and many people have access to modern medicine even in rural areas. In addition, many people living in villages are strongly linked to cities as their family is often divided into two parts, one part living in the city and the other one in the village. The residents of both rural areas and cities still trust traditional medicine as a path to well-being. Therefore, the patients in Kurdistan could continue to take advantage of these traditional medicines by encouraging scientific research aimed at the bio-evaluation of these invaluable species, leading to the development of local plants-based phytomedicines. Moreover, today medicinal plants face extinction or severe genetic loss due to over-harvesting and exploitation. As a result of this, special attention is urgently required to gather and systematically document this empirical knowledge and to protect and conserve wild medicinal plants, and their habitats, as well as traditional knowledge concerning their use. It is important for all herbalists and those dealing with medicinal plants to save them from extinction as they play an essential role in the public health sector.
These findings suggest that medicinal plants and folk medicines used by healers in Southern Kurdistan may represent a starting point for further comparative crosscultural ethnobiological research, which may contribute to increase the current knowledge of folk medicinal plants and could lead to the conservation strategies aimed at protecting possible rare plant species. The current research contributed to the existing ethnobotanical literature by identifying a number of new plant uses and their perceived health benefits to humans. Perhaps, more importantly, the results of this study could assist small-scale companies to utilize local plant resources for medicine, as natural products meet the demand of patients, who also in Kurdistan desire less pharmaceuticals; moreover, medicinal plants may provide economic benefits to local communities as well, in an area of the Middle East, which have gone through hard times in the last decades.

Appendix 1
Date Village/town Given name and surname of informant Age and gender Level of education Which kinds of plants do you use to treat different ailments? What is the vernacular name of these plants? Do you know any other names for these plants? How have you learned to recognize them? Which plant parts do you use and for what diseases? Can you describe the preparation of the remedy in detail? Is the remedy internally or externally administered? When should the medicine be taken and for how long? Where and when did you acquire this knowledge?