Dietary Patterns for the Reduction of Obesity Using Medicinal Plants in Northern Pakistan

Objective: Different types of studies have indicated an increased risk of obesity and other related diseases in Pakistan. This study examines the rich availability of anti-obesity plants among the local communities. This is the first ethnobotanical study to document folk remedies for the treatment of obesity and overweight disorders in Northern Pakistan. Methods: Field trips and interviews were carried out for documentation of ethnomedicinal data from local communities of the study area. Information on age, gender, education, anti-obesity medicinal plants, their common name, other diseases and psychosomatic behavior related to obesity was collected. The data was quantitatively analyzed using descriptive statistics and Family Importance Value (FIV) and Relative Frequency of Citation (RFC). Results: A total of 77 medicinal plants from 38 families were reported against obesity and overweight. Fruits were commonly used plant part and extract was the common mode for herbal preparations while oral intake was the common route of administration. The significant species based on the values of RFC was Trachyspermum ammi (0.291) while the significant family regarding FIV was Fabaceae (5.20). Conclusion: The current knowledge is novel and could be further exploited by carrying phytochemical investigations which may lead to the isolation and characterization of novel agents for the obesity treatment which could improve healthcare systems.


Introduction
Obesity is the excessive fat accumulation in the body, chronic and nutritional disorder and insulin resistance metabolic syndrome [1] which indirectly reduced life quality and cause mortality and morbidity [2]. According to WHO, obesity is the weight of a particular individual taken in kilograms divided by the height taken in the square [3]. The causes include excessive intake of calories, physical inactivity, sedentary lifestyles, urbanization, endocrine disorders, irregular metabolism, lack of sleeping time, medications, eating patterns, inheritance and environmental [4][5][6][7]. About 53 diseases are directly or indirectly associated with obesity [4,8]. According to the estimate of WHO (2008), more than 1/10th adults of the world's population are obese [6] while in children about 8 million and 35 million in developed and developing countries are overweight respectively [9]. based natural products are used worldwide [28][29][30][31]. In developed countries, the option of weight loss runs out and the people shift towards the use of synthetic drugs but synthetic drugs and surgical procedures involve high cost and high toxicity. In developing rural areas, unavailability of orthodox drugs and clinical limitations are the major risk reported in various case studies. Therefore, people rely on natural remedies for weight loss [32]. Pakistan is a developing country which is blessed with a varied climatic and ecological zones-ranging from tropical, subtropical to temperate conditions, with vast floral diversity [33]. A number of medicinal plants have also been listed from Northern Pakistan [34,35] but no study has been conducted on antiobesity plants and the associated folk remedies present in the area. The aim of the present work is, therefore, the documentation of such plants and preservation of related indigenous knowledge.

Study area
Northern Pakistan (South Asia) covers Khyber Pakhtunkhwa (KPK), Azad Kashmir, Federally administered Northern areas (FANA) and central Punjab ( Figure 1). The northern-Pakistan includes the world's three great mountain ranges i.e. Himalaya, Hindukush, and the Karakoram. The confluence of these ranges form a unique geographical pattern on earth [36] which support diverse flora. Climatically, three seasons are present in these high and sub-mountain regions include hot weather (April-June), rainy season (July-September) and cooler season (October-March). In KPK, the climate varies immensely with a region like from 0 -30°C in North Region (Chitral District), 5-38°C in South Region (Dir, Swat and Hazara) and 20-45°C in Southern North-West areas.
In FANA, the maximum temperature ranges from 30-40°C and the minimum 1-19°C. In Azad Kashmir, it ranges from 20-30°C in summers and 0-4°C in winters. In Central Punjab, it ranges from 2-45°C. The average rainfall ranges from 152-203 cm in lower Himalayan valleys during July-August [37,38]. Various ethnic groups are living in northern Pakistan including Kashmiri, Balti, Chitrali, Kalashi and Shina in Kashmir and FANA, Pakhtuns in Khyber Pakhtunkhwa (KPK) while Punjabi in central Punjab. All these ethnic groups have a diverse culture and the predominant majority are Muslims. Agriculture is the major source of income which roughly accounts 50% for their income ( Figure 1).

Data collection
Ethnobotanical field trips were conducted at different seasons of the year at different localities. The data collection methods included semistructures interviews, group discussions, and field observations. The sample size was 192, of native informants, which were purposively selected. The recorded data included demographic characters of the informants i.e. age, gender, education, experience (Table 1) and antiobesity plants, their local name, part(s) used, mode of utilization, route of administration, and detail recipe for the reduction of obesity and overweight. The consent was taken from informant before the interview and the aims and procedure of the study were explained to them. The interviews were mostly conducted near the homes of the informants and each interview lasted for 1-2 hours. The national and international laws, especially the ethical guidelines adopted by the Society of Ethnobiology (2006) were strictly followed.

Collection and identification of plant specimens
The specimens were collected in triplicate and processes following slandered procedure. The identification was made using several sources, i.e. through the taxonomist in the Department of Plant Sciences, Quai-i-Azam University Islamabad, by comparing with the already identified specimen in the herbarium and through the matching of specimens' characters with the flora of Pakistan [39,40]. The species names were assigned in accordance to "Medicinal Plant Names Services" while the families names in accordance to the "Angiosperm Phylogeny Group, 2009". The dried specimens were mounted on herbarium sheets and deposited in the Herbarium of Pakistan (ISL) for future reference.

Frequency of Citation
The collected data were arranged in excel spreadsheets (MS office 2013). The Frequency of citation (FC) was determined using formula; where 'ni' is the number of informants mentioning the use of the species and 'N' is the total number of informants participated in the study.
The Relative frequency of citation (RFC) was determined using the formula; Whereas FC is the number of informants mentioned the species as useful and N is the total number of informants enquired in the study. The index of relative frequency will be zero if nobody reports the use of plant and unlikely could be 1 when all the informants mention the plant as useful [41,42].

Family importance value
Family importance value (FIV) was calculated [43] using formula; FIV=(No. of informants who cite the family/Total no of informants) × 100.

Study Population
A total of 192 informants were interviewed. Among them, 15 informants (7.81%) were traditional healers and the rest of the informants include Punjabis, Pathans, Potoharis, Kashmiris, Chitralis, Kalash and Hindkowans people. Majority of the informants were females 102 (53.12%) followed by males 90 (46.87%). The high percentage of informants was about 50-60 years old while the lowest percentage of informants was about more than 60 years (8.3%). The experimental periods of traditional healers were also mentioned in study and in (Table 1) and the preponderance of traditional healers had at least 2-5 years of practice (33.33%).

Documentation of anti-obesity plants diversity and habit
In this scrupulous survey, 77 medicinal plant species from 38 families were documented for the treatment and prevention of obesity ( Table 2). The dominant families regarding number of species were Fabaceae (10 spp. having FIV 5.20) followed by Apiaceae (6 spp. having FIV 3.12; Figure 2). The reported species were found to be of different habits where 48% spp. were herbs followed by trees (36%), shrubs (11%) and climbers (5%) (Figure 3). In current study, the value of RFC ranges from 0.036 to 0.291 where the highest RFC were reported for the species Trachyspermum ammi (0.291), followed by Mentha arvensis and Coriandrum sativum (0.265 each; Figure 4).

Plant part used and modes of utilization
Fruits (35%) were the major plant part used among nine different parts of plants followed by leaves (26%) ( Figure 5). Also, 29% species were used in fresh forms while 71% were used in dried or semi-dried form. The people were found to use a total of 9 different modes of preparations where the most common were plant extract and raw form (16% each) followed by decoction and juice (14% each; Figure 6). All the species (except Chamaemelum nobile and Cedrus deodara) were taken orally while 57% species recipes were based on the combination of different species.  Among the reported species 62% were cultivated and 14% were wild while 23% were available in both i.e. cultivated and in wild too. 77% species were marketable while 23% were non-marketable. Regarding general use of the reported species, 22% were used as fruits/nuts, 12% as vegetables/salad and 23% as spice/condiments/flavoring agent while the remaining 31% were either of no special use or were miscellaneously used. Fresh parts were preferred to use by the local people (Table 2) as possibly some phytochemical constituents may be changed on drying. The predominantly oral route of administration like in present study (Table 2) has been reported from different regions [44][45][46].

Variations in traditional knowledge among informants
Age wise variation in traditional knowledge is a common ethnobotanical phenomenon reported in different studies [47][48][49]. Regarding gender, older women were more familiar with the nutritional preparation of different recipes while older men knew a longer list of species used. The herbalists were having some special expertise in identifying some wild species with their detailed recipes including number and amount of doses to be used. The knowledge of urban people about anti-obesity plants was not only indigenous, as the role of print and electronic media about nutritional diet for maintaining body weight was not negligible.

Other diseases related to obesity
Obesity and overweight cause many disturbances in body and results in many other diseases. Seven different types of diseases/ syndromes were related to obesity and overweight in the study area. In the study area, obese and overweight people were found to have many other diseases as hypertension, cardiovascular and cerebrovascular diseases, diabetes, arthritis, sleep apnea, cancer and psychological disorders (Figure 7). The psychological disorders like social phobia, avoidant personality disorder, major depressive disorder and obsessivecompulsive disorder were also observed in obese and overweight people.

Comparison with previous studies and novelty index
Extensive literature search including ethnobotanical work and biological screening were performed which demonstrate that a 86% anti-obesity plant species are already reported from different parts of the world but 11 species (14%) are new reports in the study ( Table 2). The relative frequency of citation (RFC) describes the local importance of plant species with reference to informants in the study area. Based on the RFC values, the most commonly used species includes Trachyspermum ammi and Coriandrum sativum which are also reported by Chandrasekaran [50] and by George and Nimmi [51] respectively. But Mentha arvensis (RFC 0.26) and Elettaria cardamomum (RFC 0.25) are reported for the first time. Other frequently used species are Citrus limon, Melia azedarach, Cinnamomum verum (0.234), Foeniculum vulgare (0.239) and Trigonella foenum-graecum (Table 2) are also reported from different parts of the world [6,50,[52][53][54]. The highest FIV was reported for family Fabaceae (5.20) followed by Apiaceae (3.1), Brassicaceae (2.60), Solanaceae (2.08) and Cucurbitaceae (2.08) according to the present results. The calculations taken from literature review shows that approximately 354 species from 137 families are reported against obesity in which the Fabaceae (30 spp.) has the highest number of species followed by Asteraceae (28 spp.) and Lamiaceae (17 spp.) while the reported number of species from family Apiaceae, Brassicaceae, Solanaceae, and Cucurbitaceae are 15, 3, 6 and 8 respectively.

Discussion
The results indicated that 77 anti-obesity medicinal plants of high nutritional value from 38 families were documented. In villages people were found to be more rely on nutritional herbal medicines as compared to large cities where people preferred to use pharmaceuticals. But in Pakistan, ethnomedicines were found to be a part of culture as the nutritional herbal remedies was found to be recommended by old people present in each home as a blessing.
The reported anti-obesity medicinal plant species of high nutritional value were dominantly herbs followed by trees and shrubs. The dominance of herbs in the area was probably due to easy collection and preparation as compared to other life forms. Herbs as dominant life form have been reported in other studies for reducing weight by acting on metabolism and digestion [51] and for antilipase activity [55]. Fruits followed by leaves were the major parts used because of its effortless plucking, market availability, usage without processing and its less effects plant life. The major use of same plant parts have been reported by the Chandrasekaran [50]. Similarly, the extract and raw form as dominant mode of utilization in present study have been shown in other studies [52,55]. Above half of the recipes (i.e. 57%) were prepared by the combination of multiple plant species of nutritional value which is considered as good by having high therapeutic power [56] but according to Kazemipoor [53] single plant preparations have higher degree of safety and efficacy. The combinations of some medicinal plants may result either in lowering efficacy or cause unexpected side effects.
To overcome excess weight gain, the uses of allopathic and pharmacological drugs are popular ways in developed countries but adverse toxicities limit their overall usefulness [6]. Also, the high cost and adverse side effects in long term usage are other limiting factors. The uses of natural products for treating obesity are under exploration, which is an alternative way for developing safe anti-obesity drugs [57][58][59]. The present study includes mostly the edible species which are safe and could be the best an inexpensive alternative in weight loss and management [6]. A variety of natural products, like crude extracts and isolated compounds from plants, can cause a reduction in body weight and could prevent diet-induced obesity. Therefore, for treating obesity they have been widely used [60]. The majority of the species in the present study were vegetables and fruits ( Table 2) which are low in calories and fats but contain good amounts of minerals and vitamins.
Researchers consider botanical sources as more safe, reliable and cheaper than synthetic chemical drugs and surgical procedures having an adverse effect [53]. Recent preliminary reports suggested that herbs with natural substances and with a long history of use produce less toxicity which is effective in reducing appetite and also aid in weight loss [6]. The anti-obesity plant preparations exhibit their effects in many ways, including stimulating thermogenesis, enhancing lipolysis, lowering lipogenesis, suppressing appetite and decreasing absorption of lipids [53].
The understanding of heterogeneity in knowledge and practices within a given area is important for sustaining knowledge transmission in relation to resource management [61]. Medicinal plants knowledge was passing mostly in vertical form from generation to generation but also horizontally within the community. Such transmission of knowledge has been reported by Monigatti [62] while dealing with medicinal plant use in Andean communities of Peru. The people having stronger link with the ancestors (age, living in rural area and economic dependency on natural resources) were more knowledgeable and it was vice versa in case of higher income and education and living in urban areas. There was considerable age wise difference in knowledge of individuals and its vertical transfer was getting slow.
The majority of the people in the study area were found to be affected by obesity due to their lifestyle, medications, and dietary patterns. Other studies conducted in different countries [4,8,51,63,64] linked obesity with several other diseases. The psychological disorders were also observed in obese people due to poor mobility which reduce their social interaction results in depression, also reported in other [65,66]. Obesity, being a prominent syndrome in Pakistani society but up till there is no existing ethnobotanical surveys on medicinal plants used for this purpose so the present work in the first step towards this direction. This survey would facilitate the investigation of health status of people and will provide robust data for future evaluation and preparation of herbal drugs for obesity and overweight.

Conclusion
The use of traditional medicines for the treatment of various ailments and their importance are well recognized in Pakistan. This study shows that indigenous knowledge about medicinal plants is still practiced in many parts of Northern Pakistan. Obesity is the major and growing problem in the country and also associates with many other diseases, therefore there is a dire need to emphasize on weight management for the prevention of obesity and many other related diseases. This study provides us the recognition and documentation of anti-obesity plants knowledge which could further be exploited by phytochemical investigations that may lead to isolation and characterization of new possible novel agents.