VOLKSMED Database: A Source for Forgotten Wound Healing Plants in Austrian Folk Medicine^{[ # ]}

Abstract

The global increase in the incidence of wounds is concerning and fuels the search for new treatment options. The use of traditional medicinal plants in wound healing represents an appreciated available therapeutic possibility. This work introduces the VOLKSMED database, which contains plants and other materials used in Austrian folk medicine, either as monographs or mixtures. This work focuses on the monographs of the database. Concerning wound healing, Hypericum sp., Arnica montana, Calendula officinalis, Plantago sp., and Malva sp. are the most commonly used plants. The focus of this paper is set on selected lesser-known plants (Abies alba, Anthyllis vulneraria, Brassica sp., Gentiana sp., Larix decidua, Picea abies, Sambucus sp., Sanicula europaea) and their status quo in literature concerning wound healing. A systematic search using the databases SciFinder, SCOPUS, and PubMed yielded substantial evidence for the wound healing potential of Brassica sp., Gentiana sp., the Pinaceae A. abies, L. decidua, and P. abies, as well as Sambucus nigra. In vivo and clinical studies substantiate their use in Austrian folk medicine. According to the literature, especially A. vulneraria, Sambucus racemosa, and S. europaea would be worth investigating in-depth since data concerning their wound healing effects – even though scarce – are convincing. In conclusion, the VOLKSMED database contains promising opportunities for further treatment options in the field of wound healing. Future research should consider the listed plants to support their traditional use in Austrian folk medicine and possibly promote the implementation of old knowledge in modern medicine.

Key words

Austrian folk medicine - wound healing - medicinal plants - VOLKSMED database

Introduction

The skin is the largest organ, covering the body entirely to protect the system from the intrusion of chemicals and pathogens from outside and the loss of water and electrolytes [1]. Whenever there is a disruption in the integrity of the skin, which means a wound occurs, a strictly regulated and incredibly complex mechanism of wound healing starts to repair the barrier function. During this mechanism, several growth factors, cytokines, and cell types are involved in four phases: hemostasis, inflammation, proliferation, and tissue remodeling. Different factors and comorbidities may impair the wound healing mechanism and lead to chronicity of the wound [2], [3]. A chronic wound is defined as a wound that does not heal within an anticipated time frame. There is no generally available definition of this time frame since the etiology, size, location, morbidity, and other variables of chronic wounds are fairly heterogeneous [3], [4], [5].

However, acute and chronic wounds occur with a prevalence of 3 – 4/1000 people, which equates to up to 2 million people only in the EU 27 [6]. The incidence of chronic wounds is often referred to as a silent epidemic since there is a global increase in chronic diseases and comorbidities leading to impaired wound healing such as diabetes, obesity, and vascular diseases, as well as antimicrobial resistance of microbes colonizing wounds, accompanied by an aging population [7], [8], [9]. Chronic wounds are associated with several individual and economic consequences. Patients generally suffer from a decreased quality of life due to pain and limitations in social contact and mobility as well as depression, and an enormous financial burden [10]. The latter also concerns the public healthcare systems. Approximately 2 – 4% of the European health expenditure has to be spent on the treatment of wounds. The treatment of a chronic wound in Europe accounts for up to €10 000 per year [8], [11]. Only in Germany, the treatment of chronic wounds in 2023 was estimated to cost, overall, €10 billion per year [12].

Unfortunately, data on the situation in Austria is scarce. In 2015, a survey was conducted and resulted in the first realistic assessment of chronic wounds in the Austrian population. At that time point, 250 000 people were suffering from at least one chronic wound, indicating a prevalence of up to 50 per 1000 citizens [13], [14].

Since the management of chronic wounds represents an increasing and significant problem worldwide, the necessity of alternative treatment options and research in this field is urgent [8]. One approach to heal wounds and prevent the chronicity of a wound is to use traditional medicinal plants. Plants and plant-derived substances have been used for centuries all over the world to treat and prevent various diseases [15]. Still, natural sources play an important role in the development of new drugs; either natural products derived directly from these sources, semisynthetic analogs, or synthetic compounds inspired by nature [16]. Medicinal plants can produce different secondary metabolites of various substance classes, and therefore, may possess numerous bioactivities. This feature is very beneficial in complex mechanisms such as wound healing. The power of plant extracts is given by their nature as multicomponent mixtures. In the case of skin lesions, they might hold antioxidant, anti-inflammatory, and antimicrobial activities as well as platelet aggregation inhibitory and immunomodulatory effects, which all contribute to wound healing [2], [16], [17], [18], [19]. Therefore, using medicinal plants to treat wounds is reasonable and might hold some new, or forgotten, therapy options.

This review aims to give an overview of plants that are used in wound healing in Austrian folk medicine. Furthermore, chosen examples, which intentionally do not cover the most commonly used wound healing plants, are discussed in detail concerning their status quo in the literature about their wound healing effects. Hence, future research can concentrate on promising candidates to provide a treatment alternative to decrease the probability of chronicity of a wound.

The VOLKSMED Database

Traditional knowledge is often passed and preserved only by word of mouth without being laid down on paper. Therefore, important information about plants and their traditional use might be lost over the decades of transfer. To unite and preserve valuable knowledge about the traditional use of plants and other materials in Austrian folk medicine, the VOLKSMED database was compiled [20], [21], [22]. Between 1983 and 2004, diploma students studying pharmacy at the University of Vienna conducted their diploma thesis intending to gather information about Austrian folk medicine. For that purpose, the students interviewed people with traditional knowledge in their area of origin. These interviewed people were, on the one hand, pharmacists or physicians, but, on the other hand, people known to be well-educated in folk medicine, such as farmers or foresters. All the information gathered during the diploma theses was entered in the VOLKSMED database, either as monographs of single plants or other materials or as mixtures. This work focuses on the monographs of the database.

For the establishment of the monographs, so far, 46 diploma theses have been used, covering all parts of Austria, with some areas in South Tyrol as well as some regions in southeastern Bavaria/Germany (information on the respective diploma theses can be found as Table 1S, Supporting Information). In the monograph part of the database, overall, 2114 people were interviewed, resulting in 73 681 “entries”. The number of entries corresponds to the number of persons mentioning one particular piece of information. Similar information within one diploma work was combined to a “record”, which resulted in 43 348 records using these 46 diploma theses. The establishment of individual records depended on various parameters: (i) A new record was generated within every single diploma work that reflects the folk medicinal knowledge within one unique region; and (ii) A new record was generated in case slight differences in the extracting method, about preparation or application, were given. One record can be mentioned by more than one person interviewed within one diploma work. These records were composed as follows: identity number, number of the respective diploma thesis, genus (plants, animal, and mineral origin), plant genus (all other origins labeled “diverse”), family, Latin plant name (with genus and, if available, species, subspecies, or variety), part used, internal or external use, indication, preparation form, use of fresh or dry material, number of entries, and further information about preparation and application as well as the extracting agent ([Fig. 1]). However, when comparing the use of plants within all studied Austrian regions, the number of entries was chosen as a suitable criterion.

Fig. 1 Registered information and structure of records in the VOLKSMED database.

The database contains valuable information but also reveals some drawbacks. For data compilation, no uniform questionnaire was used during the interviews, which may be regarded as a strength as well as a weakness. On the one hand, the biography or qualifications of the interviewed people were not recorded, only their identity and address. Therefore, it is not known, if a record was stated by a pharmacist or physician, which might indicate scientific evidence, or by a person without higher education. In any case, all interview partners were locally acknowledged as persons with profound folk medicinal knowledge. On the other hand, the records do not always contain all of the information as depicted in [Fig. 1], especially about the use of fresh or dry material or further information about the application. Furthermore, in some records, only the plant genus is available without any further declaration of species, subspecies, or variety, since not all of the interviewed persons were botanically trained.

Nevertheless, the VOLKSMED database contains a huge amount of incredibly valuable information and knowledge about Austrian folk medicine. The collected data is unique and can be used to gain insights into the traditional use of plants and other materials in Austria.

Wound Healing Plants in Austrian Folk Medicine

This paper aimed to review the VOLKSMED database concerning all kinds of wound healing. To simplify the enormous amounts of records, it was searched for all indications, including the key words “wounds” and “wound healing” (abrasions, burns, cuts, decubitus, ulcerous legs/feet, infected/nonhealing/purulent/slow-healing wounds). It has to be kept in mind that these key words are sub-indications of the indication “skin”. While introducing the records into the database, some wound healing records might not have been linked to one of these sub-indications but were referred to the overall indication “skin”, which was not considered for this review. Therefore, the listed records and entries in this work might not be complete.

However, in the field of “wounds” and “wound healing”, the database contains 1037 records with 1945 entries, whereof 93 records with 119 entries are materials other than plants (fungi, animal, or mineral origin); however, plants cover 944 records with 1826 entries. The list contains 111 genera from 53 different families, with the following being most abundant: Asteraceae (16), Rosaceae (7), Apiaceae (6), Brassicaceae (5), Lamiaceae (5), and Pinaceae (4). All mentioned families and the respective count of genera are depicted in [Table 1].

Table 1 Families and respective number of genera found in the VOLKSMED database in wound healing indications.

Families	Genera per family
Asteraceae	16
Rosaceae	7
Apiaceae	6
Brassicaceae, Lamiaceae	5
Pinaceae	4
Boraginaceae, Fabaceae, Malvaceae, Poaceae, Polygonaceae	3
Amaranthaceae, Betulaceae, Crassulaceae, Gentianaceae, Iridaceae, Plantaginaceae, Primulaceae, Ranunculaceae, Solanaceae	2
Acoraceae, Amaryllidaceae, Araliaceae, Aristolochiaceae, Asphodelaceae, Cannabaceae, Cucurbitaceae, Cupressaceae, Cyperaceae, Equisetaceae, Ericaceae, Fagaceae, Geraniaceae, Hypericaceae, Juglandaceae, Liliaceae, Linaceae, Lycopodiaceae, Melanthiaceae, Papaveraceae, Polypodiaceae, Rubiaceae, Salicaceae, Sapindaceae, Scrophulariaceae, Taxaceae, Tropaeolaceae, Urticaceae, Verbenaceae, Viburnaceae, Violaceae, Vitaceae	1

[Fig. 2] depicts plants with more than 10 entries; the blue-colored examples were chosen arbitrarily and analyzed in-depth in this work. All plants with less than 10 entries can be found in Table 2S, Supporting Information.

Fig. 2 Traditional wound healing plants with more than 10 entries in the VOLKSMED database. Blue-marked plants are further discussed in this work.

[Table 2] contains information about plants with more than 10 entries in the abovementioned indications in decreasing number of frequency of entries. It covers genera, species, and families, which were updated to the currently accepted names according to Plant of the Worlds online [23]. If older synonyms were used in the database, the respective plant name is marked by a superscript, which covers the particular synonym in the footnote. Furthermore, the table contains information about the used plant part and the application form, as well as the usage of dry (d) or fresh (f) plant material, or both (df), if this information was available. The used part and the application form are listed according to their frequencies; in case of the same frequency, they are organized in alphabetic order.

Table 2 Traditional wound healing plants with more than 10 entries in the VOLKSMED database. The table contains currently accepted species. If the database contains synonyms, they are marked by superscripts and explained in the footnote. The application form indicates the usage of dry (d), fresh (f) plant material, or both (df), or the information is not available (−).

Genus	Species	Family	Part used	Application form	Entries
1 Matricaria recutita L; 2 Chamomilla suaveolens (Pursh) Rydb; 3 Sedum maximum (L.) Hoffm; 4 Sedum telephium L; 5 Ornithogalum caudatum Aiton
Hypericum	sp. maculatum Crantz perforatum L.	Hypericaceae	Herb	In oil (df), ointment (df), alcoholic extract (df), tea (d), herb directly on wounds (f)	267
			Flower	In oil (df), alcoholic extract (d), flower directly on wounds (d), ointment (df), tea (−)
Arnica	montana L.	Asteraceae	Flower	Alcoholic extract (df), in oil (df), ointment (df), tea (as a bath) (d)	243
			Root	Alcoholic extract (−), ointment (df), tea (−)
			Herb	Alcoholic extract (−)
			Leaves	Leaves directly on wounds (df)
Calendula	officinalis L.	Asteraceae	Flower	Ointment (df), alcoholic extract (as an embrocation) (df), in oil (df), tea (for rinsing, as a bath) (d), flower directly on wounds (as a compress) (−)	239
			Herb	Ointment (df), herb directly on wounds (as a compress) (−)
Plantago	lanceolata L. major L. media L.	Plantaginaceae	Leaves	Juice from leaves or leaves directly on wounds (f), tea (as a bath) (df), ointment (f)	122
Malva	sp. neglecta Wallr. pusilla Sm. sylvestris L.	Malvaceae	Leaves	Tea (for rinsing, as a bath or compress) (df), leaves directly on wounds (f), ointment (df)	83
Brassica	oleracea var. capitata L. oleracea var. sabauda L. oleracea var. sabellica L.	Brassicaceae	Leaves	Leaves directly on wounds (f)	54
	rapa L.	Brassicaceae	Turnip	Turnip directly on wounds (f)
Matricaria	chamomilla 1 L. discoidea 2 DC.	Asteraceae	Flower	Tea (for rinsing, as a bath or compress) (df), ointment (df), flower directly on wounds (as a compress) (df), in oil (−)	53
Symphytum	officinale L.	Boraginaceae	Root	Ointment (df), root directly on wounds (f), alcoholic extract (df)	47
			Leaves	Leaves directly on wounds (f), ointment (−)
Tussilago	farfara L.	Asteraceae	Leaves	Leaves directly on wounds (f), tea (for rinsing) (−)	46
Achillea	millefolium L.	Asteraceae	Herb	Herb directly on wounds (as a compress) (df), tea (for rinsing, as a compress) (df), in oil (f), ointment (−)	42
			Leaves	Leaves directly on wounds (f)
			Flower	Tea (d)
Anthyllis	vulneraria L.	Fabaceae	Flower	Alcoholic extract (d), tea (for rinsing, as a bath) (d), ointment (d)	42
			Herb	Tea (for rinsing, as a bath or compress) (df), juice from leaves or leaves directly on wounds (f)
			Leaves	Ointment (d), tea (d)
Larix	decidua Mill.	Pinaceae	Resin/balm	Resin/balm directly on wounds (df), ointment (df), alcoholic extract (df)	41
Peucedanum	ostruthium (L.) W. D. J.Koch	Apiaceae	Root	Fumigation (d), root directly on wounds (d), tea (as a bath) (d), alcoholic extract (as an inunction) (−), ointment (d)	31
			Leaves	Leaves directly on wounds (as a compress) (f), ointment (−)
Sempervivum	sp. tectorum L.	Crassulaceae	Leaves	Juice from leaves or leaves directly on wounds (f), ointment (d)	29
			Herb	Juice from herb directly on wounds (f)
Equisetum	sp. arvense L. telmateia Ehrh.	Equisetaceae	Herb	Tea (for rinsing, as a bath or compress) (df), cold maceration in water (as a compress) (df), herb directly on wounds (as a compress) (df)	28
Alchemilla	sp. alpina L. vulgaris L.	Rosaceae	Herb	Tea (for rinsing, as a bath) (d), herb directly on wounds (as a compress) (f), ointment (−)	26
			Leaves	Leaves directly on wounds (df), tea (for rinsing, as a bath) (d)
Sambucus	nigra L.	Viburnaceae	Leaves	Leaves directly on wounds (f)	24
			Bark	Bark directly on wounds (df)
			Flower	Ointment (−)
	racemosa L.	Viburnaceae	Fruits	Oil gained by boiling fruits in water applied on wounds (df), in oil (df)
Sedum	acre L.	Crassulaceae	Leaves	Juice from leaves or leaves directly on wounds (f), alcoholic extract (−)	24
Hylotelephium	maximum 3 (L.) Holub
telephium 4 (L.) H.Ohba
Lycopodium	sp. annotinum L. clavatum L.	Lycopodiaceae	Spores	Spores directly on wounds as a powder (df)	20
Albuca	bracteata 5 (Thunb.) J. C.Manning & Goldblatt	Asparagaceae	Leaves	Juice from leaves or leaves directly on wounds (df), ointment (d)	18
Picea	abies (L.) H.Karst.	Pinaceae	Resin/balm	Resin/balm directly on wounds (df), ointment (df)	18
			Shoot tips	Tea (−)
Althaea	officinalis L.	Malvaceae	Herb	Cold maceration in water (d), tea (for rinsing) (d)	17
			Root	Cold maceration in water (d), tea (for rinsing, as a bath or compress) (d)
			Flower	Cold maceration in water (−), tea (as a bath or compress) (−)
			Stem	Tea (as a bath) (−)
Salvia	glutinosa L. officinalis L. pratensis L.	Lamiaceae	Leaves	Tea (for rinsing, as a bath or compress) (df), leaves directly on wounds (f), in oil (−), ointment (df)	16
			Herb	Tea (for rinsing, as a bath or compress) (−)
Verbascum	sp. densiflorum Bertol. phlomoides L.	Scrophulariaceae	Flower	In oil (−), ointment (−), tea (for rinsing, as a bath) (df), alcoholic extract (df)	16
Gentiana	lutea L. punctata L.	Gentianaceae	Root	Tea (for rinsing, as a compress) (d), alcoholic extract (d)	14
			Leaves	Leaves directly on wounds (f)
Sanicula	europaea L.	Apiaceae	Root	Ointment (d)	14
			Herb	Tea (for rinsing, as a bath) (−), herb directly on wounds (as a compress) (−)
			Leaves	Leaves directly on wounds (d), ointment (−)
Geranium	sp. pratense L. robertianum L.	Geraniaceae	Herb	Tea (for rinsing, as a bath or compress) (d), herb directly on wounds (f)	13
Allium	cepa L.	Amaryllidaceae	Bulb	Bulb directly on wounds (f), fried in olive oil and applied on wounds (f), ointment (−), tea (for rinsing) (f)	11
	sativum L.	Amaryllidaceae	Bulb	Alcoholic extract (f), bulb directly on wounds (f)
	ursinum L.	Amaryllidaceae	Leaves	Juice from leaves or leaves directly on wounds (f), alcoholic extract (−)
Abies	alba Mill.	Pinaceae	Resin	Bark with resin or resin directly on wounds (f), ointment (f)	10
			Needles	Tea (for rinsing) (df)
Capsella	bursa-pastoris (L.) Medik.	Brassicaceae	Herb	Herb directly on wounds (df), tea (for rinsing, as a compress) (d), alcoholic extract (d), ointment (d)	10

Almost every part of plants is used in the treatment of wounds: flowers (37.2%), leaves (25.0%), the whole herb (21.7%), roots (6.9%), resin/balm (3.3%), fruits (1.3%), buds (1.2%), spores (1.0%), bark (0.66%), seeds (0.60%), bulb (0.49%), shoot tips (0.33%), cones (0.11%), rhizome (0.05%), stem (0.05%), stylus (0.05%), tuber (0.05%), and turnip (0.05%). The preparation methods are simple and reflect the possibilities people have commonly at home. The most frequent form of preparation is apolar formulations (33.8%), with slightly more entries for ointments (17.4%) than for oily preparations (16.4%). For ointments, plant parts are processed with fat, whereas for oily preparations, the plant parts are inserted into oil. In both cases, people are using oils and fats they have at home at the moment, mostly olive oil, linseed oil, lard, and butter, but also goose or rabbit fat. The use of plant parts without any extraction is the second most abundant form of preparation (31.5%). Parts of the plant are either directly applied (21.4%), or processed before application (10.1%), for example, squeezed and the juice applied, crushed, burnt, cut, or powdered. Of the entries, 18.4% belong to aqueous extracts, either as an infusion (17.7%) or cold maceration (0.7%). These extracts are used as a bath, for rinsing, or as a compress. Alcoholic extracts (15.9%) are made using schnapps (ethanol 40%) or spirits of wine (ethanol 96%). Furthermore, boiling plant parts in milk (0.16%) as well as extraction with vinegar (0.11%) are mentioned in the entries.

The most frequently used plants in Austrian folk medicine (Hypericum sp., Arnica montana, Calendula officinalis, Plantago sp., and Malva sp.) are well-known wound healing agents. They have already been intensively investigated in this field and discussed in numerous publications [1], [19], [24], [25], [26], [27], [28], [29]. The next section focuses on lesser-known plants.

Known Wound Healing Properties of Selected Plants

Selected plants were analyzed in-depth with a focus on the current state of knowledge concerning their wound healing properties. English plant names were obtained from Plants of the World online [23], Wikispecies, [30], Medicinal Plant Name Services [31], or the Encyclopedia of Life [32]; German names were acquired from the Excursion Flora of Austria, Liechtenstein, and Switzerland [33]. The status quo in the literature about their wound healing effects was collected by a literature search using the databases SCOPUS, SciFinder, and PubMed. No time frame was set in the search and as key words, the Latin plant name and “wound healing” were used.

Anthyllis vulneraria

Anthyllis vulneraria L. (Engl. common kidney vetch; Ger. Echter Wundklee) belongs to the family Fabaceae. It is a perennial herb native throughout Europe and Northern Africa and is nowadays mostly used in cosmetics [34], [35]. In the VOLKSMED database, this plant has 42 entries. All aerial parts are mentioned as being used, mostly the flower, followed by the whole herb and the leaves. All of the plant parts are prepared as tea for rinsing or bathing the wound, but also used as a compress. Furthermore, an ethanolic extract is made of the flower and used mostly for cleansing the wound and as a compress. The preparation of an ointment is mentioned for the flower and leaves. Moreover, the fresh herb is either squeezed and the resulting juice is applied to the wound, or the herb is put directly on the wound as a compress.

The Latin name A. vulneraria already suggests the use of this plant in wound healing since the Latin word “vulnerare” means to wound. Already in medieval times, kidney vetch was used to treat wounds [36], however, this plant is meagerly investigated in the field of wound healing. The aerial parts of A. vulneraria contain different substance classes, such as saponins, flavonoids, phenolic acids, and tannins. Extracts of flowers and leaves exhibited significant antioxidant properties, whereby the total polyphenol and flavonoid content was higher in the flowers than in the leaves [37]. Csepregi et al. tested ethanolic and aqueous extracts of kidney vetch concerning several bioactivities that are beneficial in wound healing: antimicrobial, antioxidant, and pro-migratory effects. The 50% ethanolic extract showed moderate minimum inhibitory concentrations (MIC₈₀) against Streptococcus pyogenes and Bacillus subtilis, a weak antimicrobial activity on Staphylococcus aureus, as well as no effect at all on Escherichia coli and Pseudomonas aeruginosa. To determine the antioxidant properties of the extracts, different assays were conducted, leading to the lowest antioxidant capacity of all plants that were tested in this work, but still a good antioxidant effect. Furthermore, the pro-migratory activity of the extracts was tested on 3 T3 fibroblasts and HaCaT keratinocytes. A weak pro-migratory stimulation of the A. vulneraria extracts was detected on HaCaT keratinocytes, whereas no effect could be seen on fibroblasts [38]. These first findings emphasize the potential of A. vulneraria as a wound healing agent. Further research has to be conducted to gain more insights into the bioactivities of this plant.

Brassica sp.

Different species and varieties of the genus Brassica (Brassicaceae) are mentioned in the VOLKSMED database: Brassica oleracea var. capitata L. (Engl. cabbage; Ger. Weiß-Kraut/Rot-Kraut), Brassica oleracea var. sabauda L. (Engl. savoy cabbage; Ger. Kohl, Wirsing-Kohl), and Brassica oleracea var. sabellica L. (Engl. curly kale; Ger. Kraus-Kohl), as well as Brassica rapa L. (Engl. field mustard, turnip mustard; Ger. Rüben-Kohl, Rübsen). The database contains 54 entries of Brassica sp. All of the B. oleracea varieties are used the same way: the fresh leaves are used, either squeezed (often with a rolling pin) and applied to the wound or cooked to a soft consistency prior to application. For B. rapa, the turnip is mashed and applied as a wound healing agent.

Species from the Brassicaceae family are economically very valuable as edible plants, spice sources, or as feed plants all over the world. Due to their nutritional value, Brassica sp. are very well investigated, especially concerning their chemical composition, and are known to possess antitumor, antioxidant, antimicrobial, and anti-inflammatory effects [39], [40], [41], [42], [43], [44]. But also, their potential and value as wound healing agents have already been analyzed.

Lysophosphatidic acid (LPA) is known to mediate cell proliferation and migration and, therefore, is used as a positive control in wound healing assays. Cabbage has a high activity of phospholipase D (PLD), an enzyme forming phosphatidic acid (PA) after tissue disruption like homogenization, cutting, or chewing. Therefore, cabbage leaves represent a rich source of PA, which is further hydrolyzed by phospholipase A₂ to LPA after ingestion in the gastrointestinal tract [45]. Tanaka et al. not only detected PA in homogenized cabbage leaves but also LPA [46]. Since phospholipase A₂ is also present in human skin [47], this enzyme might increase the content of LPA in topical applied squeezed cabbage leaves, which might be part of the wound healing activity of B. oleracea plants. In addition, pectin-type polysaccharides might be involved; different pectin fractions were extracted from white cabbage, kale, and red kale. All of the fractions showed complement-fixing activity and, therefore, may promote wound healing by stimulation of innate immunity [48], [49]. Moreover, bandages containing anthocyanin extracts gained from red cabbage are an easy-to-use, quick, and eco-friendly colorimetric indicator for pH changes in wound fluids, which is a helpful tool for monitoring the healing process. Additionally, an increasing concentration of anthocyanins in the bandage correlates with a higher antimicrobial activity [50], [51], [52], [53], [54].

Even in vivo studies are available: Hassanzadeh et al. reported the promoting effect of an aqueous B. oleracea extract applied as a cream on reepithelialization and contraction of burn wounds in Sprague-Dawley rats [55]. Rebolla et al. investigated the bioactivity of a B. oleracea var. capitata 10% glycolic extract on surgical skin wounds in Wistar rats. The results of this study revealed a predominance of mature type I collagen fibers in the treated group compared to the control group, and therefore an improved wound healing process [56]. These findings were confirmed by Sarandy et al., who also tested a B. oleracea var. capitata 10% glycolic extract balsam as well as an ointment on wounds in Wistar rats over 20 days. Both preparations led to a boost in cell proliferation and differentiation, and an initial increase in type III collagen fibers. The fast formation of granulation tissue as well as a higher content of type I collagen than type III at the end of the treatment suggests the reconstruction of mature tissue [57]. Moreover, in another study, an ointment containing 10% glycolic extract of B. oleracea var. capitata was tested on wounds in Wistar rats. It resulted in an enhanced remodeling phase by faster substitution of type III collagen fibers for type I [58].

Nanoparticles (NPs) of silver, gold, or iron are known to promote wound healing and reveal antimicrobial activity. Different studies describe the use of B. oleracea var. capitata extracts for the successful synthesis of such NPs and demonstrate the antibacterial, antioxidant, anti-cancer, and in vivo wound healing potential of these NPs [59], [60], [61], [62].

Broccoli (B. oleracea var. italica Plenck) is another variety not mentioned in the VOLKSMED database. Nevertheless, bioactive proteins and peptides isolated from the stems of broccoli were found to promote the proliferation of keratinocytes in vitro and, therefore, promote wound healing [63].

Taken together, different Brassica species repeatedly proved their traditional use as wound healing agents. Further research on these plants could lead to easily accessible, cheap, and commercially available preparations for wound healing.

Gentiana sp.

Gentiana lutea L. (Engl. yellow gentian; Ger. Gelb-Enzian) and Gentiana punctata L. (Engl. spotted gentian; Ger. Tüpfel-Enzian) are a class among the family of Gentianaceae. These perennial herbs are native throughout Europe and Western Asia [64], [65]. In Austrian folk medicine, gentian root is used as a tea for bathing and rinsing the wound or as an alcoholic extract. Only one entry contains the application of fresh leaves of G. punctata directly on cuts and wounds. Most publications considered for this review deal with G. lutea. G. punctata is only discussed by Pasdaran et al. [65]. However, since the chemical composition appears to be similar, the results found for G. lutea may be transferred to G. punctata.

The root of G. lutea is an authorized drug in the European Pharmacopeia (“Gentianae Radix”) used to treat various digestive disorders but has also been used traditionally to treat wounds in several countries. Gentian is known to reveal antimicrobial, anti-inflammatory, and antioxidant effects, which are caused by different substance classes. The main constituents are secoiridoids, but also flavonoids, terpenoids, iridoids, and xanthones can be detected. The secoiridoid sweroside contributes to wound healing by an antioxidant effect and by increasing the formation of a procollagen complex. The terpenoid lupeol promotes reepithelialization, and the flavonoid isoorientin leads to an upregulation of the skin regenerative protein involucrin. Furthermore, the xanthone mangiferin has an impact on several inflammatory pathways as well as on immunohistochemical angiogenesis markers in wound healing [64], [65], [66]. The overall wound healing effect of gentian has also been investigated in vivo in mice and rats. After oral administration of alcohol and petrol ether extracts of G. lutea rhizomes, an increase in wound closure and breaking strength of the remodeled tissue, as well as a higher rate of granulation tissue with increment in fibroblasts and collagen fibers were reported [67]. The latter was also reported by Öztürk et al., who tested an ethanolic extract as well as three pure secoiridoids in vitro in cultured chicken embryonic fibroblasts. They indicate swertiamarine as the main bioactive secoiridoid [68]. Moreover, gentiopicroside alone was administered to rats with diabetic wounds, again resulting in an improvement in wound healing by the acceleration of collagen fiber synthesis [69].

Gentiana macrophylla Pall. is a Gentiana species native to Asia, mostly Mongolia, China, and Siberia, and is another species well investigated in the field of wound healing. The chemical composition seems to be similar to the European species [70], [71]. Yin et al. investigated a methanolic root extract and described an antioxidant activity as well as antibacterial effects against bacterial strains isolated from burn wounds [71]. Furthermore, Buyantogtokh et al. prepared a gel containing ethanolic extracts of Calvatia gigantea and G. macrophylla for the treatment of burn wounds. This gel increased the wound healing process significantly by promoting the migration of myofibroblasts, fibroblasts, and macrophages as well as reepithelialization [72].

Taken together, Gentiana species are well investigated in the field of wound healing, especially G. lutea. Since G. macrophylla appears to be an effective treatment alternative for burn wounds, it would be interesting to investigate if G. lutea reveals the same potential. Further in vitro and in vivo experiments concerning the wound healing mechanism of Gentiana species as well as clinical studies should be launched to push for the development of a pharmaceutical wound healing product.

Pinaceae members

Different plants belonging to the family Pinaceae are mentioned in the database: Abies alba Mill. (Engl. European silver fir; Ger. Edel-Tanne), Larix decidua Mill. (Engl. European larch; Ger. Europa-Lärche), as well as Picea abies (L.) H.Karst. (Engl. Norway spruce; Ger. Gewöhnlich-Fichte). Only the needles of A. alba, and the shoot tips of P. abies, which are prepared as tea for rinsing wounds, are different plant parts appearing in the VOLKSMED database. The other entries treat the resin or balm of these trees, and since their composition is expected to be resembling [73], they are discussed together in this section. These exudates are directly used on wounds as a compress or band-aid, or processed with lard to make an ointment.

The chemical composition of different parts of A. alba, L. decidua, and P. abies is well investigated [74], [75], [76], [77], [78], [79], [80]. The database contains the usage of needles and shoot tips of European silver fir and Norway spruce. Geana et al. investigated the phytochemical composition and bioactivities of 50% ethanolic extracts gained from the barks and needles of these two plants. Flavonoids, phenolic acids, and derivatives, as well as stilbenes, terpenes, lignans, and carboxylic acids, were detected in these extracts. The extract gained from P. abies needles exhibited a significant antibacterial effect against P. aeruginosa, E. coli, Enterococcus faecalis, and methicillin-resistant S. aureus, whereas the needle extract of A. abies only showed activity against S. aureus and E. faecalis, but with the lowest IC₅₀ concentrations. Furthermore, in silico molecular docking experiments suggested the possible effect of selected phenolic compounds found in the extracts on the PI3K/AKT signaling pathway, which is linked to wound healing [75]. Moreover, a 40% ethanolic extract of European larch bark led to similar results. The extract revealed antimicrobial activity against S. aureus, Klebsiella pneumoniae, and P. aeruginosa [77]. Häsler Gunnarsdottir et al. summarized the wound healing potential of different bark extracts from common European trees. Here, the main active compounds in larch bark were specified as flavonoids, lignans, and stilbenoids with antioxidant and antimicrobial activity, but no wound healing assays were available. Spruce bark revealed stilbenes, flavonoids, phenolic acids, tannins, and lignin as the main active substance classes, also with antioxidative and antimicrobial activity as well as results from an in vivo scratch assay using a human melanoma cell line [79]. Interestingly, the essential oils of four different Abies species, Cedrus libani, and Picea orientalis were found to hold wound healing potential in vivo on wounds in rats. Significant results were detected only for the essential oils from C. libani and Abies cilicica subsp. cilicica [81]. Moreover, a standardized extract of Pinus pinaster bark, another Pinaceae member, significantly promoted wound healing and reduced the development of scars in an in vivo study on female Sprague-Dawley rats, as well as showed antimicrobial activity [82]. Polycaprolactone/gelatin nanofibers containing extracts of Pinus radiata bark were developed for the application on wounds. These extracts revealed antibacterial activity against S. aureus and E. coli and a pro-migratory effect on HaCaT keratinocytes [83]. In addition, the essential oil gained from the cones and needles of different Pinus species showed in vivo wound healing potential in mice and rats [84], [85], [86].

According to the VOLKSMED database, Pinaceae exudates such as resins and balms are the main plant parts used in Austrian folk medicine. No publications on the exudates of A. alba concerning wound healing have been published. As mentioned above, the chemical composition of Pinaceae resins and balms appears to be very comparable. Therefore, the results found for other coniferous exudates might also apply to A. alba and would be an interesting research target for the future. Even though the Committee for Veterinary Medicinal Products from the European Medicines Agency approved the use of the resin of L. decidua for wound healing in animals due to its long history of safe topical application [87], only scarce data about its in vitro and in vivo activities is available. Substances contained in the resin of European larch contribute to an overall wound healing effect through anti-inflammatory and antimicrobial activity [74]. In vitro, the balm exhibits a pro-migratory effect on keratinocytes in a wound healing assay [73]. No in vivo studies concerning the wound healing effect of larch exudates have been conducted so far.

On the contrary, P. abies balm is a well-known wound healing agent. Different diterpenoid resin acids showed an in vivo pro-migratory effect on keratinocytes [76]. However, comparing the balms and resins of European larch, Norway spruce, and black pine in the respective wound healing assay on keratinocytes, only the balm of L. decidua revealed significant reepithelialization boosting effects [73]. The resin of Norway spruce is known to hold antimicrobial effects against different bacteria such as methicillin-resistant S. aureus, B. subtilis, or vancomycin-resistant Enterococcus, but also against fungi such as Candida albicans, Trichophyton rubrum or Trichophyton mentagrophytes [88], [89], [90], [91], [92]. Using ointments containing spruce balm or resin, different in vivo studies and clinical trials have already been conducted. Ointments of P. abies exudates were tested on castration wounds in piglets and showed higher rates of completely healed wounds and lower contamination of the wounds with fungi compared to the untreated group [93]. In 2005, the treatment of pressure ulcers in 37 patients with a 10% spruce resin salve resulted in significantly higher complete healing rates in the resin group compared to the control group (94 vs. 36%). Another study involving 23 patients with surgical wounds also showed the great wound healing potential of spruce resin salve, with a healing rate of 100% within a mean healing time of 43 days. However, it has to be kept in mind that an allergic reaction in the form of contact dermatitis is possible while using such natural resins [88], [94], [95]. This clinical evidence supported the admission of monographs on the balm and an ointment consisting of 20% balm in lard in the Austrian Pharmacopeia. Furthermore, a medicinal product with the same composition is available on the Austrian market. First experiments using other ointment bases than lard were conducted to develop a more stable, standardized, and animal-friendly formulation [96].

In summary, wound healing bioactivities of different Pinaceae members are well investigated. The balm of P. abies has proven its traditional use and is on a good way to be an alternative in the treatment of various wounds in everyday wound management. Since the composition of different balms and resins of Pinaceae trees is supposed to be similar, further research on other coniferous exudates would be promising.

Sambucus sp.

The VOLKSMED database contains Sambucus nigra L. (Engl. elder, black elder; Ger. Schwarz-Holunder) and Sambucus racemosa L. (Engl. red-berried elder; Ger. Rot-Holunder, Trauben-Holunder). In the literature, the genus Sambucus is attributed inconsistently to the families Viburnaceae, Adoxaceae, or Caprifoliaceae. However, according to Plants of the World online [23], Sambucus sp. belongs to the family Viburnaceae. The two species are used very differently. Leaves and bark, more precisely the green liber below the outermost bark of S. nigra, are applied directly on wounds, or the flowers are mixed with lard and applied as an ointment. Regarding S. racemosa, only the ripe red fruits are used traditionally. The fruits are either inserted in oil, or the fruits are boiled in water. During the boiling procedure, the oil contained in fruits separates and accumulates on the water surface due to the difference in density. After skimming this oil, it can be applied to wounds.

Black elder can be found all over the world, in Europe, North Africa, Asia, and America [97]. S. nigra is known to be used traditionally in different folk medicines as a wound healing agent. In the Balkan region, the bark of S. nigra is either extracted with olive oil for sunburns or boiled with buttermilk for thermal burns. Furthermore, the balm is mixed with fresh flowers for the treatment of all wounds [24]. The use of S. nigra flowers for wound healing is also reported in the folk medicine of the Maratea area, Italy, but there it is prepared as a decoction instead of an ointment [98]. In 2018, Jarić et al. already summarized the ethnobotanical and pharmacological characteristics of S. nigra. Anthocyanins, flavonoids, tannins, and triterpenes are active compounds found in different parts of the plant and bring forth antibacterial, antioxidant, astringent as well as anti-inflammatory activities. A soft extract from the leaves of S. nigra was tested in vivo on thermal skin burns in Wistar rats and led to a promotion in wound healing due to flavonoids and tannins. Furthermore, extracts of S. nigra berries and flowers revealed antimicrobial effects against C. albicans, P. aeruginosa, Salmonella typhi, E. coli, and B. subtilis as well as S. aureus [24]. More recent publications confirmed this antimicrobial activity, especially against methicillin-resistant S. aureus, and suggested inhibition of bacterial efflux pumps as the mode of action [99]. Peptides found in the flowers of S. nigra are known to exhibit antimicrobial activity against gram-negative bacteria found in aquaculture [100], and therefore, might be responsible for these antibacterial properties. Popova et al. analyzed the effects of a cream containing extracts of Pelargonium sidoides, S. nigra, and Hypericum perforatum on different microbes, resulting in a high antimicrobial effect against C. albicans, E. coli, and S. aureus [101]. Concerning the positive effect of S. nigra on inflammation, aqueous and ethanolic black elder leaf extracts showed a high anti-inflammatory potential by inhibition of TNF-α and reactive oxygen species [102]. Furthermore, an aqueous black elder fruit extract and its ferment were investigated concerning their anti-inflammatory and antioxidant activity as well as their impact on fibroblasts and keratinocytes. Both extracts stimulated proliferation and metabolism in the two cell types, inhibited elastase and collagenase, and revealed a high antioxidant effect. Interestingly, the fermented extract exhibited a higher anti-inflammatory activity than the non-fermented extract, which could be explained by the increase in simple phenolics such as chlorogenic acid and protocatechuic acid during the fermentation process [103].

On the contrary, only very few publications about S. racemosa are available, and none of them concern the wound healing effects of its fatty oil. This species is native to North America and Europe and can be found in higher elevations [104], [105], [106]. The few publications available are about the chemical composition. The oldest literature (1902 – 1977) deals with the composition of the fatty oil of S. racemosa fruits [107], [108], [109]. Newer studies cover other substance classes such as glycoprotein lectins [110] and a neolignane glycoside [111] gained from the bark, as well as hydroxycinnamic acids and flavonoids in fruit extracts [112]. In 2020, Miljković et al. conducted the first assessment of the free radical scavenging activity of different S. racemosa fruit extracts using different solvents. All extracts were active in the DPPH assay, and the different activities were linked to the respective concentrations of phenolic compounds in each extract [113].

Moreover, a third Sambucus species, Sambucus ebulus L., has been investigated concerning its wound healing properties. An ointment containing 5% S. ebulus fruit extract led to an acceleration of wound healing in rats by reepithelialization, wound contraction, formation of granulation tissue and collagen, as well as revascularization. The authors only mentioned flavonoid glycosides as components found in S. ebulus fruits [114]. Therefore, a comparison of the composition of fruits of S. ebulus and S. racemosa could shed light on possible analogies in wound healing effects.

In summary, S. nigra is already well investigated concerning its antimicrobial effects, and the first in vivo study has already been conducted. The results suggest further investigations of this plant concerning its wound healing effects. For S. racemosa, first investigations in the direction of wound healing would be interesting to find evidence for its traditional use.

Sanicula europaea

Sanicula europaea L. (Engl. wood sanicle; Ger. Sanikel) belongs to the family Apiaceae and is a perennial plant found all over Europe [115]. In Austrian folk medicine, the roots of sanicle as well as the herb and leaves are used traditionally. The roots are traditionally processed into an ointment, and the herb is mostly prepared as tea and used for rinsing and bathing the wound. Furthermore, the fresh herb is applied as a compress after a bath. Leaves of sanicle are either prepared as an ointment, or dry leaves are applied directly onto the wound.

In Austria, only the herb of sanicle (“Herba Saniculae”) is commercially available and also used in homeopathic preparations against rhinitis and sinusitis [116]. Interestingly, “Radix Saniculae” might also be linked to other plants (e.g., Cardamine enneaphyllos, Polygonatum odoratum) [33], [117], [118], [119], [120] since they are all associated with the same Austrian vernacular names “Sanigl” or “Saunigl”. Therefore, the use of “Radix Saniculae” has to be mentioned with caution in Austria, since the correct botanical source first must be identified. The entries discussed in this work refer to sanicle, S. europaea.

The Latin word “sanare” means “to heal”, which is comprised in the Latin name Sanicula europaea, already indicating its use as a wound healing plant. The aerial parts of sanicle contain hydroxycinnamic acids, tannins, coumarins, and flavonoids [121] as well as triterpene saponins [122], [123], [124]. Interestingly, even though the use of sanicle in the field of wound healing has been reported several times [24], [115], [121], [122], [124], [125], [126], [127], only a few publications are available concerning its detailed bioactivities in the treatment of wounds. S. europaea is known to possess antimicrobial as well as anti-inflammatory effects [22], [122], [128], which may contribute to an overall wound healing activity. Beggs et al. tested aqueous and methanolic extracts in an in vitro scratch assay on 3 T3 fibroblasts to investigate their potential to close this model wound over 20 h. In this assay, sanicle extracts did not lead to an increased wound closure but rather caused cytotoxic effects in the first hours of the experiments. The authors suggest that this cytotoxic activity may contribute positively to the wound healing process as an antibiotic to decrease wound infections [115]. Further in vitro tests on other cell lines than fibroblasts as well as investigations on the antibacterial potential of sanicle on wound-colonizing bacteria might lead to a better understanding of the wound healing activities of this plant.

Conclusion and Future Perspectives

This review presents the high value and application possibilities of the VOLKSMED database, a database containing monographs and mixtures of plants and other materials used in Austrian folk medicine. Concerning wound healing, the most abundant plants are well-known wound healing agents such as Calendula officinalis or Hypericum sp. However, the focus of this work was laid upon lesser-known or, in the meantime, forgotten plants. Eight genera were chosen at random for detailed discussion, keeping in mind that the VOLKSMED database holds many other possible candidates for future investigations. A. vulneraria, S. racemosa, and S. europaea appear to belong to the forgotten medicinal plants for wound healing. None or only very few publications about their wound healing potential are available. Thus, these plants represent interesting opportunities for researchers to investigate their wound healing activities and support their traditional use in folk medicine. On the contrary, Brassica sp., Gentiana sp., Pinaceae members as well as S. nigra have already been well investigated concerning their wound healing effects, even with evidence from in vivo studies. Therefore, future research is instrumental for a better understanding of the underlying mechanisms as well as the development of new therapeutic products in the treatment of wounds, which definitely could have a place in modern medicine.

Contributorsʼ Statement

Design of the study: J. Saukel, S. Glasl; analysis and interpretation of the data: E. Eichenauer, J. Saukel; drafting the manuscript: E. Eichenauer, S. Glasl; critical revision of the manuscript: E. Eichenauer, S. Glasl, J. Saukel

Conflict of Interest

The authors declare that they have no conflict of interest.

Acknowledgements

We are grateful to Wolfgang Kubelka for the possibility of realizing this project during his time as Head of the Division of Pharmacognosy. Further, we want to thank all diploma students for their work and Siegrun Gerlach for her contribution to summarizing parts of the VOLKSMED database.

^# This work is dedicated to Professors Rudolf Bauer, Chlodwig Franz, Brigitte Kopp, and Hermann Stuppner for their invaluable contributions and commitment to Austrian Pharmacognosy.

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Publication History

Received: 29 September 2023

Accepted after revision: 28 November 2023

Article published online:
06 June 2024