Ethnobotanical uses of wild taxa as galactagogues in Sicily (Italy)

Breastfeeding furnishes optimal nutrition, immune support, and a multitude of health benefits to mothers and newborns. Since ancient times plants have been employed as galactagogues in the folk medicine of many human cultures. In Sicily, a region with great floristic diversity in the Mediterranean area, where a conspicuous pool of species is traditionally used for food and aromatic, cosmetic, handicraft, agricultural, forestry, and medicinal purposes, some people recognize the galactagogue properties of some spontaneous plants. The goal of this study was to identify wild plants with galactagogue properties and vegetable-food remedies traditionally used by women during breastfeeding to increase milk production. It was conducted in the Madonie territory (province of Palermo) by interviewing a sample of 105 people that was divided into three age groups. Ethnobotanical investigations revealed a total of 34 species, belonging to 11 families and 25 genera, used as galactagogues. For each taxon, the parts used, the methods of preparation, and the phytochemical profiles according to the literature were reported. The most represented family was Asteraceae, with 12 genera and 17 species, the majority of which contained latex. The most frequently used parts of the galactagogue plants were leaves (69%) that were mainly eaten as cooked vegetables, raw in salads, or utilized as an infusion tea. The species cited in this study are mainly wild traditional vegetables with high nutritional profiles that could improve the quality and the quantity of the milk produced. The study found that older people represent a precious source of information to help younger people preserve the cultural identity of the territory.

The goal of this study was to: (i) identify the wild galactagogue plants and vegetable-food remedies traditionally used by women living in the Madonie area during breastfeeding to increase milk production, and (ii) determine the used parts and their mode of preparation.

Material and methods
The area of study The Madonie mountains are located in the northern part of Sicily. The territory is located between Pollina River to the east and Imera River to the west. The central part of the area is characterized by carbonatic substrates, which give rise to variation in relief that at higher altitudes constitutes the second group of mountains of Sicily (Pizzo Carbonara, 1,979 m). In the Madonie mountains, there are various geological formations dating from the Upper Triassic to the Lower Miocene age [60,61]. The landscape is characterized by calcarenitic and dolomitic rocks with peaks and cliffs, whereas some areas consist of quarzarenitic and silico-clastic rocks (Flysch Numidico). The climate is characterized by cold winters with snowfall and xerothermic summers. The various orographic areas exhibit complex ecological characteristics that result in a wide variety of environments, with numerous habitats giving rise to singular biological and biocenotic expressions. The territory is considered a biodiversity hotspot because of the numerous species and the high level of endemism. In a surface area equal to 1.55% of the entire island, there are 1,700 vascular plant taxa (approximately 55% of the Sicilian flora), among which 170 are endemic. From a biogeographical point of view, the flora is expressed in several groups, including the eastern and southern ones, as well as the Mediterranean element in the Steno and Eurimediterranean expressions [60,61]. The main population centers, which have played an important role in the anthropization and exploitation of the area, are Petralia Sottana, Polizzi Generosa, Geraci Siculo, Isnello, Castelbuono, Collesano, and Petralia Soprana. Other very close centers are Gratteri, Campofelice di Roccella, Cefalù, and Pollina in the north and San Mauro Castelverde, Scillato, Caltavuturo, Sclafani Bagni, Gangi, Blufi, and Castellana Sicula in the south (Fig. 1). The first traces of human presence in the Madonie go back to the Greek expansion in Sicily, whereas the main economic activities started in the Middle Ages. The urban structures and the subdivision of the territories (latifundium) are typical of the feudal age [60,61]. The economy has always been based on agriculture, forest exploitation, and grazing, but because of the ever-increasing anthropization, excessive grazing, deforestation, and summer residence buildings, many ecosystems have been destroyed. To protect these territories, in 1989 the natural regional "Park of Madonie" was established, which covers more than 40,000 hectares of the area [60,61].

Field study methods
The field work was carried out in the years 2010-2015 by gathering ethnobotanical information from the inhabitants of 18 rural Sicilian communities, belonging to the Madonie mountain territory in the province of Palermo. Data were obtained by means of a structured questionnaire, which included general questions (name, surname, sex, age, level of education, work experience) and specific ones on wild taxa and some plants that have been cultivated for a long time in Sicily and are traditionally utilized as galactagogues. The questions were concerned with the vernacular names of the vegetables, the parts used, and methods of use. The interviews, frequently conducted in both the Italian and Sicilian dialect, were performed (after prior informed consent) with a stratified, randomly selected sample of 105 local people, divided into three age groups: 60-80, 40-59, and 20-39 years. For each age-group consisting of 35 people, we selected 25 women (18 housewives, five farmers, two teachers) and 10 men (four shepherds, four farmers, two specialists in ethnic traditions) because the topic concerns women, although men are usually the experts concerning folk plants. The identification of the most common taxa was carried out in the field. Plant samples were usually collected together with the interviewees, during or after the interview, and we confirmed the correct identification of the plants. Alternatively, specimens were collected and identified in the laboratory according to Flora d'Italia and more recent taxonomic revisions [62]. Voucher specimens of the plants were collected and deposited in the Herbarium of Francesco Minà Palumbo Museum (Castelbuono-Palermo, Sicily). Nomenclature follows the Sicilian checklists [63,64] and the standards set by The Plant List database [65]. The biological forms and chorological data of the investigated taxa were also reported [64]. The study was carried out following The Code of Ethics of the International Society of Ethnobiology [66].

Data analysis
We compared the data gathered during the field study to other ethnobotanical investigations dealing with this subject, and to national and international ethnobotanical literature sources and popular references that considered the traditional uses of wild plants in local cuisines for galactagogue purposes [1,12,23,[28][29][30][31][32]39,[49][50][51][52]. The data obtained (frequency of mention, usage of the parts of the plants, and methods of preparation) were evaluated using the cross-table analysis tool in Microsoft Excel software.

Results
Ethnobotanical investigation revealed a total of 34 species, belonging to 11 families and 25 genera, used by local people for galactagogue purposes. The reported taxa are listed in Tab. 1 including their scientific and Sicilian vernacular names, information concerning their life forms, their geographical distribution areas (chorotype), their parts used, their methods of preparation, and their relative phytochemical profiles according to the literature. The most represented family was Asteraceae, with 12 genera and 17 species, whereas the Urticaceae family included only one genus with four species (i.e., U. dioica, U. membranacea, U. urens, and U. pilulifera), which are sometimes collected indifferently. Most of the listed species are spontaneous, but some traditionally cultivated species were also reported, including Cichorium endivia, Lactuca sativa, Avena sativa, Medicago sativa, Trifolium pratense, and Trigonella foenum-graecum. Concerning the biological spectrum (Fig. 2), the majority of galactagogue species belonged to the hemicryptophytes (53%), followed by terophytes (44%). The analysis of the chorological spectrum ( Fig. 3) showed that the Eurimediterranean and Stenomediterranean elements were the most represented (18% and 15%, respectively).

Rosaceae
Rubus idaeus L.  [4,6]; stinging hairs: histamine, formic acid, acetylcholine, acetic acid, butyric acid, leukotrienes, 5-hydroxytryptamine [6] groups with a frequency ranging between 49% and 77%. Nigella damascena, Tragopogon porrifolius, and Crepis vesicaria were rarely cited, especially by the 20-39 age group, whereas Urospermum dalechampii was not mentioned by the youngest interviewed people (Tab. 1). Low frequency of mention was also found for Althaea hirsuta, A. officinalis, and Medicago sativa because they do not occur very frequently; in particular, Medicago sativa is uncommonly cultivated in Sicily because of inadequate water resources.
The most used parts of galactagogue plants were the leaves (69%), mainly eaten as cooked vegetables or raw in salads. The seeds of Trigonella foenum-graecum, Nigella damascena, Foeniculum vulgare. subsp. vulgare, and Avena sativa were employed as a decoction or infusion, as well as the dried roots of Althaea officinalis, A. hirsuta, Cichorium intybus, and Taraxacum officinale. The fresh fruits of Vitex agnus-castus and Rubus idaeus were utilized. For some species, more than one part or the entire plant was used, i.e., Foeniculum vulgare. subsp. vulgare, Cichorium intybus, Silybum marianum, Taraxacum officinale, Borago officinalis, Nasturtium officinale, Rubus idaeus, and Vitex agnus-castus ( Fig. 5A and Tab. 1).

Discussion
As reported by numerous studies [1,23,49-51, 56,59], several wild spontaneous plants contain a wide variety of phytochemical substances with potential galactogenic properties (Tab. 1). These plants, consequently, can be used as food remedies to augment milk production in breastfeeding women.
The prevalent mention of the taxa belonging to the Asteraceae family ( Fig. 4 and Tab. 1) as being utilized to increase milk production during breastfeeding, as well as for food and a source of vegetable remedies, was because the taxa of this family are rich in secondary metabolites and are the most abundant in the Mediterranean flora, and therefore are easily available to local people. These plants have been gathered and employed for many generations in Sicily for their diversified phytochemical profiles, which enrich the human diet with biologically active molecules [54,67,68]. According to the Checklist of the vascular flora of The age-group columns include the data of Urtica dioica L., U. membranacea Poir., U. pilulifera L., and U. urens L.
Sicily, the Asteraceae family occurs in Sicilian flora with 103 genera and 371 specific and infraspecific taxa [64]. Many galactagogues are obtained from plants containing latex, the majority of which belong to the Asteraceae family, such as Lactuca sativa, Cichorium intybus, Reichardia picroides, Sonchus spp., Crepis vesicaria, Hypochaeris radicata, Taraxacum officinale, and Hyoseris radiata (Tab. 1). This fact recalls the medieval "doctrine of signatures" by Paracelsus, according to which plants possess signs indicating their usage. Though this doctrine cannot be scientifically validated, there are indeed several latex-producing plant species that are stated to be quite efficient in promoting lactation [12].
Some taxa, such as Lactuca sativa, Cichorium endivia, Cichorium intybus, and Hypochaeris achyrophorus, are eaten after being boiled, or consumed raw in salads seasoned with oil, salt, and lemon or vinegar or in mixed vegetable soups [54,56]. The leaves of Fig. 2 Biological spectrum of the investigated taxa. Fig. 3 Chorological spectrum of the investigated taxa. Urtica spp. and Foeniculum vulgare subsp. vulgare are also employed to prepare sauces to flavor local dishes [56]. Alternatively, fresh or dry leaves can be utilized for infusions to increase milk production (Tab. 1 and Fig. 5B).
The seeds are generally employed to prepare tea infusions. The seeds of Foeniculum vulgare subsp. vulgare, containing anethole and estragole phytoestrogens, are also an ingredient for seasoning many traditional Sicilian dishes [47]. Moreover, these seeds, beyond their galactagogue properties, are used in Sicily to prepare infusions for soothing colic in infants through breastfeeding [49].
Traditionally in Sicily, Silybum marianum is utilized as food and a galactagogue remedy (Tab. 1 and Fig. 5): leaves, young shoots, inflorescences, and stems are eaten raw in salads or boiled, or powdered dried leaves are consumed as an infusion [54,68]. Previous studies conducted on humans and animals suggested that this species has positive effects on milk secretion because it contains a mixture of flavonolignans. Silybin, the major constituent of silymarin, binds to cytosolic estrogen receptors determining phytoestrogenic activity [48,69,70].
Rubus idaeus and Vitex agnus-castus are the only two species cited by local people regarding the consumption of fresh fruits to increase milk production (Fig. 5). The active principles of làganu (Vitex agnus-castus) consist in a combination of iridoids (aucubin and agnusid), flavonoids (casticin, kampferol, quercetagetin, vitexin), and volatile oils (Tab. 1). Rubus idaeus (amureddu di San Franciscu) produces sweet and flavorful red fruits, which contain high levels of bioactive compounds (Tab. 1), such as anthocyanins, vitamins, carotenoids, phenols, and minerals. However, in both cases, there are not scientific studies confirming their direct effects on breastfeeding [12], but their use may have positive implications for women's and newborns' overall health.
Nasturtium officinale (crisciuni) is a perennial leafy plant that grows in rivulets, ditches, and pond margins. Its leaves have a spicy but pleasing taste and they can be eaten as a fresh salad vegetable [54,56], but it is recommended that women during breastfeeding consume them boiled to avoid the risk of Fasciola hepatica infection. The nutraceutical use of their leaves is caused by the significant content of glucosinolates and breakdown products (isothiocyanates, nitriles, and thiocyanates), pigments (carotenoids and chlorophylls), phenolics compounds (coumaric acid, caftaric acid, and quercetin, among others), vitamins (A, B1, niacin, and C), and mineral salts (Fe, Ca, P, Na, and K). The presence of various phytochemicals and their nutritional benefits give Nasturtium officinale the capacity of maintaining and improving immunity and health of the body [71]. Despite the lack of scientific evidence confirming its galactogenic characteristics, the consumption of watercress by women during breastfeeding can be an alternative source of nutrients (in particular mineral salts and vitamins) useful to the improvement of milk secretion.
Elderly men and women (age group 60-80) resulted the best connoisseurs of traditional plant uses. Among men, in particular, shepherds possessed the widest knowledge of galactagogue plants because of their indirect experience through animals; moreover, young shepherds maintain the oral knowledge handed down by family members. It is noteworthy that men in Sicily usually pay particular attention to their wives during the breastfeeding period, and they know and collect the useful plants to help them provide a good source of milk for their newborns.
Among women, housewives and farmers knew the plants used to increase milk production during breastfeeding either directly or on the basis of the tradition. Nevertheless, this information declines as generations pass (as appreciable in Tab. 1). Women having the highest education level often indirectly knew the uses of plants through the experience of their mothers and grandmothers.

Conclusions
This work represents a first contribution to the knowledge of the plants traditionally used in the Madonie area to increase milk production in women and to improve their and their newborns' wellbeing. A balanced diet, rich in nutritional benefits, together with a healthy lifestyle is the main factor for good production of breast milk. The galactagogue plants can provide valuable support, although it is crucial to know that some of their active constituents may cause side effects in both mothers and their infants. This fact argues for increased public awareness and for available information on the safety implications of using herbal medicines to be provided at least among breastfeeding women [38]. The species cited in this study are mainly vegetables commonly utilized by local populations with high nutritional profiles, which can improve the quality and quantity of milk produced by mothers. Their use has been supported by centuries of experience, but it is not confirmed by scientific evidence that would definitely show their action and effectiveness. Lactation represents a particularly delicate phase in women's lives, because it rests on hormonal, neural, and psychological factors. According to Jelliffe and Jelliffe [72], differences in benefits suggest that in some cases, the effectiveness of the employment of wild vegetable galactagogues may derive from the consolidate belief that they will work well. This enables the mother to relax and facilitates the stimulation of the milk-let-down reflex [72].
The interviews carried out in this study in the Madonie area showed that older people are a precious source of information for the younger generations. Therefore, they represent a significant resource to enhance the cultural identity of the territory with the valorization and rediscovery of the wild-vegetable heritage before the traditions disappear permanently. It would be desirable to perform new research on characterization, quantification, and the mechanism of action of the active principles contained in these galactagogue wild plants to link their traditional uses to future applications.