Plants with Hair Growth Activity for Alopecia: A Scoping Review on Methodological Aspects

Abstract

Alopecia is a common dermatological disorder of patchy hair loss with substantial patient burden. Phytotherapeutic compounds are increasingly used as a source of new therapeutic options. This review aimed to synthesize the evidence on plant species in hair growth and the methodological aspects of in vivo experimental models. The systematic scoping review was conducted following the PRISMA checklist, the Joanna Briggs Institute, and in accordance with Cochrane. A systematic search was carried out in the Pubmed, Scopus, Web of Science, and SciELO databases. In vivo experiments that evaluated hair growth activity using natural substances of plant origin were included. Data collection and analysis: a total of 1250 studies were identified, of which 175 were included for qualitative synthesis. Of these, 128 used mice, 37 rats, 10 rabbits, 1 guinea pig, and 1 sheep as animal models. The methodologies mapped were as follows: hair growth analysis, histological analysis, immunohistochemistry, gene expression analysis, Western blot, enzyme-linked immunosorbent assay, and biochemical analysis. Minoxidil and finasteride were the most commonly used positive controls. The studies evaluated plant species (166), algae (11), or isolated substances (31). Overall, 152 plant species and 37 isolated substances were identified. This is the first systematic scoping review on the methodological aspects of in vivo hair growth activity. We created a checklist to be completed by authors to allow data comparison and reproducibility, facilitate data interpretation by readers, and ensure better quality of evidence. This work may become a valuable tool for future research and contribute to significant advances in hair growth studies.

Keywords

hair regrowth - baldness - herbal medicine - biological products - methodology

Introduction

Hair loss or alopecia is a common multi-etiological dermatological disease. Alopecia is classified as scarring and nonscarring, with nonscarring being more frequent [1]. The main types of nonscarring alopecia are androgenetic alopecia, alopecia areata, trichotillomania, and telogen effluvium, with androgenetic alopecia being the most frequent [2].

Although hair loss is not life-threatening, it greatly impacts self-image and mental and emotional health, reducing social interactions and patientsʼ quality of life [3]. Several studies show that alopecia is associated with psychiatric comorbidities such as anxiety, depression [4], [5], [6], [7], and suicide risk [8], [9], as well as chemotherapy treatment due to cancer and stress for various reasons. In Australia, there were four deaths of young people aged 14 to 17 years old affected by alopecia areata, which the coroner recorded as suicide [10].

Clinical treatments for alopecia include surgical and medical therapies that are constantly expanding, reaching billions of dollars worldwide [11]. Although hair transplant surgery has reliable effects, there are still some limitations, including invasive surgical processes, high prices, and limited sources of donor follicles, and the risk of infection after surgery cannot be ignored [12], [13].

Minoxidil and finasteride are drugs approved by the United States Food and Drug Administration (US-FDA) [14]. However, the application of these drugs is limited due to their adverse effects, toxicity, high recurrence rate, non-adherence to treatment, and limited and transient effects [15], [16]. In June 2022, the US-FDA approved the use of baricitinib for the systemic treatment of severe alopecia areata in adult patients [17], [18]. In this context, the search for herbal products with greater efficacy and safety, less toxicity, and fewer adverse effects has been widely promoted in developing new substances against hair loss [19]. Thus, this study aimed to synthesize the available evidence of the methodological aspects to assess the hair growth activity of natural products of plant origin through a systematic scoping review of in vivo studies.

Methods

This research was designed according to the recommendations from the Preferred Reporting Items for Systematic Reviews and Meta-Analyses Extension for Scoping Reviews (PRISMA-ScR) [20] (Table 1S, Supporting Information), Cochrane Handbook for Systematic Reviews of Interventions, [21] and the Joanna Briggs Institute, [22] with Open Science Framework (OSF) register DOI: doi:10.17605/OSF.IO/Z5VQG.

Search strategy

A systematic search was performed in the electronic databases PubMed, Scopus, Web of Science, and SciELO with no restriction for publication, date, or language (updated in December 2023). The main descriptors used were ʼhair follicleʼ, ‘hair growthʼ, ‘animal modelʼ, ‘herbal medicineʼ, and ʼnatural productsʼ. The full search strategy can be found in Supporting Information. Grey literature and manual search in the reference list of the included studies was also conducted.

Inclusion and exclusion criteria

We have included in vivo experimental studies that used animal models (of any type) to evaluate hair growth activity using extracts, fractions, or isolated compounds of plant origin.

In vitro studies, clinical trials, reviews of any kind, letters to the editor, abstracts, cohort studies, editorials, and book chapters were excluded. Studies that analyzed allopathic medicines, phytotherapics, formulations, and substances of mineral or animal origin and articles written in non-Roman characters were also excluded.

Eligibility and data extraction

The selection process of the studies involved two steps: reading the titles and abstracts to exclude irrelevant records and reading the full text to select eligible studies for data extraction. A standardized form was then used to collect data on the characteristics of the animal model, natural substance, and methodological aspects. All the results were described qualitatively. Two reviewers conducted all steps independently, and a third reviewer was consulted in case of disagreements.

Data synthesis

Data were extracted using structured tables containing the general characteristics of the studies such as authors, year of publication, and country, the characteristics related to the animal model such as lineage, sex, age, and weight, the characteristics related to plant species, and the methods used to evaluate hair growth in each study. Based on the extracted data, we created a checklist to guide future authors.

Results

A total of 1218 records were retrieved from the databases after removing duplicates. Of these, 970 were excluded during screening (title and abstract reading). Of the remaining 248 studies, 93 were excluded after full-text evaluation (Table 2S, Supporting Information). Twenty articles were added by manual search. Finally, 175 studies that met the eligibility criteria had their data extracted and analyzed as shown in [Fig. 1] [23], [24], [25], [26], [27], [28], [29], [30], [31], [32], [33], [34], [35], [36], [37], [38], [39], [40], [41], [42], [43], [44], [45], [46], [47], [48], [49], [50], [51], [52], [53], [54], [55], [56], [57], [58], [59], [60], [61], [62], [63], [64], [65], [66], [67], [68], [69], [70], [71], [72], [73], [74], [75], [76], [77], [78], [79], [80], [81], [82], [83], [84], [85], [86], [87], [88], [89], [90], [91], [92], [93], [94], [95], [96], [97], [98], [99], [100], [101], [102], [103], [104], [105], [106], [107], [108], [109], [110], [111], [112], [113], [114], [115], [116], [117], [118], [119], [120], [121], [122], [123], [124], [125], [126], [127], [128], [129], [130], [131], [132], [133], [134], [135], [136], [137], [138], [139], [140], [141], [142], [143], [144], [145], [146], [147], [148], [149], [150], [151], [152], [153], [154], [155], [156], [157], [158], [159], [160], [161], [162], [163], [164], [165], [166], [167], [168], [169], [170], [171], [172], [173], [174], [175], [176], [177], [178], [179], [180], [181], [182], [183], [184], [185], [186], [187], [188], [189], [190], [191], [192], [193], [194], [195], [196], [197].

Fig. 1 Flow diagram of the systematic scoping review. Adapted from Page et al. [198].

The main characteristics of the included studies are presented in [Table 1]. The studies were published between 1980 and 2022. These studies were conducted in the following countries: South Korea (n = 67; 38.29%), India (n = 35; 20%), China and Japan (n = 19; 10.86%), Indonesia (n = 12; 6.86%), Thailand (n = 4; 2.29%), and Pakistan and Iran (n = 3; 1.71%), as well as in the following countries: the United States of America, Nigeria, Malaysia, and Taiwan (n = 2; 1.14%) and Bangladesh, Brazil, Jordan, the Philippines, and South Africa (n = 1; 0.57%).

Table 1 Main characteristics of all the studies included in the systematic scoping review.

Methodology	Number of studies	Country	Animal Model	Treatment	Reference
1- Hair growth analysis	170	South Korea (n = 67) India (n = 35) China (n = 18) Japan (n = 17) Indonesia (n = 11)’ Thailand (n = 4) Pakistan (n = 3) Iran (n = 2) Nigeria (n = 2) Taiwan (n = 2) USA (n = 2) Malaysia (n = 2) Bangladesh (n = 1) Brazil (n = 1) Jordan (n = 1) Philippines (n = 1) Southern Africa (n = 1)	Mice, Rat, Rabbit, Guinea pig, Sheep	Plant species, Algae, Isolated substance	[23], [24], [25], [26], [27], [28], [29], [30], [31], [32], [33], [34], [35], [36], [37], [38], [39], [40], [41], [42], [43], [44], [45], [46], [47], [49], [50], [51], [52], [53], [54], [55], [56], [57], [58], [59], [60], [61], [62], [63], [64], [65], [66], [67], [68], [69], [70], [71], [72], [73], [74], [75], [76], [77], [78], [79], [80], [81], [82], [83], [84], [85], [86], [87], [88], [89], [90], [91], [92], [93], [94], [95], [96], [97], [98], [99], [100], [101], [102], [103], [104], [105], [106], [107], [108], [109], [110], [111], [112], [113], [114], [115], [116], [117], [118], [120], [121], [122], [123], [124], [125], [126], [127], [128], [130], [131], [132], [133], [134], [135], [136], [137], [138], [139], [140], [141], [142], [143], [144], [145], [146], [147], [148], [149], [150], [151], [152], [153], [155], [156], [157], [158], [159], [160], [161], [162], [163], [164], [165], [166], [167], [168], [169], [170], [171], [172], [174], [175], [176], [177], [178], [179], [180], [181], [182], [183], [184], [185], [186], [187], [188], [189], [190], [191], [192], [193], [194], [195], [196], [197]
2- Histological analysis	107	South Korea (n = 50) India (n = 22) China (n = 18) Japan (n = 4) Thailand (n = 3) Iran (n = 2) USA (n = 2) Brazil (n = 1) Indonesia (n = 1) Malaysia (n = 1) Nigeria (n = 1) Philippines (n = 1) Southern Africa (n = 1)	Mice, Rat, Rabbit	Plant species, Algae, Isolated substance	[23], [24], [27], [28], [29], [30], [31], [32], [33], [35], [36], [37], [38], [39], [40], [41], [42], [43], [44], [46], [47], [50], [52], [53], [55], [56], [59], [60], [64], [65], [66], [69], [75], [77], [78], [79], [80], [81], [84], [87], [89], [90], [93], [94], [95], [97], [98], [99], [104], [105], [106], [110], [115], [116], [117], [119], [122], [123], [124], [125], [126], [127], [129], [130], [131], [133], [134], [135], [136], [137], [138], [140], [141], [142], [144], [145], [146], [149], [150], [153], [154], [156], [158], [161], [162], [164], [165], [166], [168], [169], [171], [172], [174], [175], [176], [180], [181], [183], [184], [186], [187], [188], [192], [194], [195], [196], [197]
3- Immunohistochemistry	34	South Korea (n = 24) China (n = 5) Japan (n = 2) India (n = 1) Taiwan (n = 1) Indonesia (n = 1)	Mice, Rat	Plant species, Isolated substance	[36], [43], [55], [56], [59], [60], [74], [80], [87], [90], [92], [98], [99], [104], [105], [106], [116], [119], [122], [123], [125], [130], [131], [145], [150], [155], [166], [169], [172], [173], [177], [178], [192], [196]
4- Gene expression analysis	24	South Korea (n = 16) China (n = 5) Indonesia (n = 1) Japan (n = 1) Iran (n = 1)	Mice	Plant species, Algae, Isolated substance	[24], [41], [47], [48], [53], [56], [60], [84], [87], [104], [115], [124], [126], [131], [132], [140], [145], [153], [168], [169], [175], [187], [188], [195]
5- Western blot assay	19	South Korea (n = 12) China (n = 6) Indonesia (n = 1)	Mice	Plant species, Isolated substance	[24], [27], [31], [47], [56], [69], [78], [80], [84], [87], [104], [106], [115], [116], [126], [131], [140], [150], [166]
6- Enzyme-linked immunosorbent assay	8	South Korea (n = 3) China (n = 4) Indonesia (n = 1)	Mice	Plant species, Isolated substance	[24], [32], [80], [104], [116], [149], [186], [197]
7- Biochemical analysis	2	South Korea (n = 2)	Mice	Plant species, Algae	[27], [149]

Methodological aspects

Most studies used more than one methodology to assess hair growth in animal models. The methodologies mapped in this systematic scoping review were hair growth analysis, histological analysis, immunohistochemistry, gene expression analysis, Western blot, ELISA, and biochemical analysis.

Hair growth analysis

One hundred and seventy studies (97.14%) performed this analysis to assess hair growth. The references of studies that carried out this analysis are presented in [Table 1]. The following [Table 2] describes the evaluations using this methodology.

Table 2 Hair growth activity measured in studies.

Hair growth analysis	Studies (n)	%
Visual observation (skin color)	120	70.59
Hair length	68	40.00
Hair growth score	43	25.29
Hair growth % area	19	11.18
Hair growth initiation time and completion time	17	10.00
Hair weight	16	9.41
Hair density	15	8.82
Hair thickness	13	7.65
Percentage of anagen induction	4	2.35
Diameter of shaved area	2	1.18
Anagen/Telogen ratio	2	1.18
Growth activity	2	1.18
Reverse side skin evaluation of anagen induction	1	0.59
Hair tensile strength	1	0.59
Percentage growth	1	0.59

Histological analysis

Overall, 107 studies (61.14%) performed histological analysis ([Table 1]). All criteria evaluated in the studies are described in [Table 3].

Table 3 Histological analysis performed in studies.

Histological analysis	Studies (n)	%
Number of hair follicle	61	57.01
Anagen/Telogen ratio	46	42.99
Length of hair follicle	39	36.45
Observation of follicular phases	43	40.19
Skin thickness	16	14.95
Depth of hair follicle	10	9.34
Thickness of hair follicle	7	6.54
Bulb hair size	5	4.67
Number of master cells	3	2.80
Melanogenesis	3	2.80
Shape of hair follicle	2	1.87
Thickness of hair shaft	2	1.87
Number of basal cells	2	1.87
Roots of hair follicle	2	1.87
Number of hair shaft	1	0.93
Length of hair shaft	1	0.93
Shafts differentiation	1	0.93
Thickness of hair roots	1	0.93
Number of bulb hair	1	0.93
Number of blood vessels	1	0.93
Distance between hair follicle and dermis	1	0.93
Distance between hair germ and subcutaneous layer	1	0.93

Immunohistochemistry

Thirty-four studies (19.43%) performed immunohistochemical analyses ([Table 1]). The studiesʼ analyses evaluated the expression of fibroblast growth factors (FGF-5 and FGF-7), epidermal growth factor (EGF), vascular endothelial growth factor (VEGF), insulin-like growth factor-1 (IGF-1), transforming growth factor-β2 (TGF-β2), tumor necrosis factor (TNF-α), β-catenin, caspase-3, caspase-8, pro-caspase-9, protein (p53, p63), Bcl-2-associated X protein (Bax), B-cell lymphoma-2 (Bcl-2), Bcl-xL, cleavage-activating protein (SCAP), dickkopf-1 (DKK-1), telomerase reverse transcriptase (TERT), interleukin (IL) IL-1β, IL-4, IL-13, bone morphogenetic protein 4 (BMP4), sonic hedgehog (Shh), Ki-67 keratinocytes, keratin 19 (K19), K15, cluster of differentiation (CD34), p-JNK, p-IKB, SPTLC, cytokeratin 19 (CK19), substance P (SP⁺), calcitonin gene-related peptide (CGRP⁺), high-mobility group box 1 (HMGB1), stem cell factor (SCF), wingless-related integration site (Wnt) 3, Wnt3a, Wnt10b, alkaline phosphatase (ALP), and 5α-reductase.

The studies evaluated the detection of apoptotic cells by the terminal deoxynucleotidyl transferase dUTP nick end labeling (TUNEL) method and the proliferation of keratinocytes by bromodeoxyuridine labeling.

Gene expression analysis

Twenty-four studies (13.71%) analyzed gene expression ([Table 1]). The markers evaluated by the real-time polymerase chain reaction (PCR) technique were keratinocyte growth factor (KGF), VEGF, hepatocyte growth factor (HGF), transforming growth factor β (TGF-β), TGF-β1, IGF-1, DKK-1, FGF-5, FGF-7, bax, Wnt10b, Wnt10a, Wnt3, Wnt3a, Wnt5a, low-density lipoprotein receptor-related protein 5 (LRP5), frizzled receptor 1 (FZDR1), frizzled 7, lymphoid enhancer factor 1 (LEF1), cyclin D1 (Cyc-D1), fas cell surface death receptor (fas), p53, matrix metallopeptidase 2 (MMP2), MMP9, disheveled 2, glycogen synthase kinase 3β (GSK-3β), β-catenin, and ALP.

Western blot

Nineteen studies (10.86%) performed Western blot analysis ([Table 1]). The markers evaluated in this methodology were β-catenin, cleaved caspase 3, caspase-3, -8 e − 9, active caspase-3, procaspase-9, extracellular signal-regulated kinase (ERK), phosfo (p)-ERK, stress-activated protein kinase (SAPK)/c-Jun N-terminal kinase (SAPK/JNK), p- SAPK/JNK, p38, p-p38, p53, bcl-2, bcl-xL, bax, NF-kB, IkB-α, p-IkB-α, IGF-1, TGF-β, TGF-β1, TGF-β2, MMP2, MMP9, phospho-Akt (Akt phospholylation), jun proto-oncogene, AP-1 transcription factor subunit (c-Jun), FGF-5, FGF-7, LEF-1, Shh, smoothened (Smo), GLI family zinc finger 1 (Gli-1), Cyclin D1, Cyclin E, Wnt3a, Wnt5a, Wnt 10 b, frizzled 7, disheveled 2, GSK-3β, and ALP.

Enzyme-linked immunosorbent assay

The expression levels of KGF, VEGF, HGF, transforming growth factor α (TGF-α), TGF-β, TNF-α, IL-1β, IGF-1, FGF-7, EGF, p21, β-catenin, and Shh were measured by ELISA (n = 8; 4.57%).

Biochemical analysis

Only two studies (1.14%) measured the enzymatic activity of γ-glutamyl transpeptidase and ALP.

Animal models

Studies retrieved from the databases reported strain, sex, age, and use of guidelines.

Mice

Of the 175 studies selected in our systematic search, 128 (73.14%) used mice as an experimental model to assess hair growth. The strains identified in studies were C57BL/6 (n = 96; 75%), C3H/He (n = 12; 9.38%), Swiss (n = 7; 5.47%), Balb/c (nu/nu) (n = 4; 3.13%), Balb/c (n = 4; 3.13%), Kunming (n = 2; 1.96%), B6CBAF1/j (n = 1; 0.78%), Balb/Black (n = 1; 0.98%), dd-K (n = 1; 0.78%), and ICR (n = 1; 0.78%). Four studies (3.13%) did not report the strain used, and five studies used two different strains.

Seventy-three studies (57.03%) used male mice, 37 (28.91%) used females, 8 (6.25%) used both sexes, and 11 (8.59%) did not report the sex. Among the studies that reported the age of the animals, the age ranged from 5 to 36 weeks, with 7-week-olds being the most used (n = 54; 42.19%). One hundred and two studies (79.69%) used guidelines and/or institutional protocols on animal management. The other studies did not report this information (n = 26; 20.31%).

Rats

Thirty-seven studies (21.14%) analyzed rats. The strains were Wistar (n = 24; 64.86%), Sprague–Dawley (n = 5; 13.51%), and Swiss (n = 3; 8.11%), and five studies (13.51%) did not report the strain used. Sixteen studies (43.24%) used male rats, six studies (16.22%) used female rats, five studies (13.51%) used both sexes, and ten studies (27.03%) did not provide data on the sex of the animals. The age of the animals ranged from 5 to 36 weeks, with the most-used mean age being 12 weeks (n = 7; 18.92%). However, most studies did not report this information (n = 21; 56.76%). Thirty studies (81.08%) used guidelines and/or institutional protocols on animal management.

Rabbits

Ten studies (5.71%) used rabbits in experiments to evaluate hair growth. The strains were Angora (n = 3; 30%) and New Zealand (n = 1; 10%); however, most studies (n = 6, 60%) did not report the strain. In nine studies (90%), the animals were males, and only one study (10%) used females. The age of the animals ranged from 3 to 5 weeks (n = 6; 60%). Four studies (40%) did not report this information. Eight studies (80%) use guidelines and/or institutional protocols on animal management.

Other models

Only one study (0.57%) used guinea pigs, and another (0.57%) used sheep as animal models. The study with guinea pigs did not provide any information about the lineage, sex, and age of the animals used in the experiments, and the sheep study reported using 1- to 2-year-old female animals of Lohi lineage. Neither study reported the use of guidelines.

Induction of alopecia

Thirty-four studies (19.43%) induced alopecia in animals by administering the following hormones: testosterone (n = 25; 14.29%), dihydrotestosterone (n = 4; 2.29%), or hydrocortisone (n = 1; 0.57%), or the antineoplastics cyclophosphamide (n = 3; 1.71%) and bleomycin (n = 1; 0.57%). Hormones were administered subcutaneously, topically, or intramuscularly, and antineoplastics intraperitoneally.

The remaining studies performed mechanical depilation of animals with electric hair clippers (n = 82; 46.86%), depilatory cream (n = 23; 13.14%), shaved+cream (n = 21; 12%), and wax (n = 10; 5.71%).

Four studies (2.29%) used nude mice, and one study (0.57%) used old animals (spontaneous hair loss). Two studies (1.14%) did not report the method used. One study carried out two methods for depilation (cream and shaved+cream), and one carried out three methods (shaved, cream, and wax).

Treatments

The plants and algae analyzed in the studies were prepared as crude extracts (n = 128; 73.14%), fractions (n = 16; 9.14%), or oils (n = 16; 9, 14%). Two studies (1.14%) did not report this data. Forty-nine studies (28%) did not report the part of the plant used, and 53 (30.29%) did not report the extraction method and solvent used (n = 22; 12.57%).

Plant species

From the 175 studies selected in our systematic scoping review, 166 (94.86%) evaluated plant species. We identified 152 different plant species, corresponding to 64 families. We report the complete list of plant species and families in [Table 4]. However, 20 studies (11.43%) did not report or make clear the plant species used. The most frequent plant species in the studies were Phyllanthus emblica L. Hibiscus rosa-sinensis L., Panax ginseng C. A.Mey., and Polygonum multiflorum Thunb. Four plants were not completely identified: Espinosilla, Aconiti Ciliare Tuber, Longanae Arillus, and Polygonati Rhizoma. They are suggested to be Loeselia mexicana Brand, Aconitum carmicarnichaelii Debeaux, Dimocarpus longan Lour, and Polygonati rhizome, respectively.

Table 4 Plant species, respective family, organ, extraction method, and solvent used in studies.

Plant species	Family	Organ	Extraction Method	Solvent
NE = not evaluated; NR = not related
Abrus precatorius L.	Leguminosae	Seed, Leaf	Maceration, Soxhlet	CHCl3: H2O, H2O, Petroleum ether: EtOH
Acorus calamus L.	Acoraceae	Root, NR	NR, Reflux	EtOH 30%, EtOH : H2O
Adiantum capillus-veneris L.	Pteridaceae	Aerial part	Maceration	EtOH 95%
Albizia julibrissin Durazz.	Fabaceae	NR	Reflux	EtOH 75%
Allium tuberosum Rottler ex Spreng	Amaryllidaceae	NR	NR	EtOH : Hex : DCM
Aloe vera (L.) Burm.f.	Asphodelaceae	Leaf	Blended	NR
Anemarrhena asphodeloides Bunge	Asparagaceae	Rhizome	NR	NR
Angelica dahurica (Hoffm.) Benth&Hook.f. ex Franch&Sav.	Apiaceae	NR	Reflux	EtOH 75%
Angelica gigas Nakai	Apiaceae	NR, Root, Root, NR	Reflux, NR, NR, Reflux, Reflux	EtOH : H2O, EtOH 30%, EtOH 98%, Hot water : EtOH
Angelica sinensis (Oliv.) Diels	Apiaceae	Root	Maceration	EtOH 70%
Angiopteris evecta (G.Forst) Hoffm.	Marattiaceae	Root	Maceration, Soxhlet	EtOH, EtOH : H2O
Apium graveolens L.	Apiaceae	Root, Leaf	Reflux, Maceration	EtOH
Asiasarum heterotropoides (F. Schmidt) F. Maek.	Aristolochiaceae	Root	NR	EtOH
Asiasarum sieboldii (Miq.) F. Maek	Aristolochiaceae	Root	NR	MeOH 95%
Astragalus spp	Fabaceae	NE	NE	NE
Bacopa monnieri (L.) Wettst.	Plantaginaceae	Whole plant, Leaf, Leaf, Entire herb	NR, Direct boiling, Boiling, NR	NR, Olive oil, NR, NR
Bergera koenigii L.	Rutaceae	NR	NR	NR
Biota orientalis (L.) Endl. (Platycladus orientalis)	Cupressaceae	NR	Reflux	EtOH 75%
Bletilla striata (Thunb.) Rchb.f.	Orchidaceae	Tuber	Reflux	MeOH
Blumea eriantha DC.	Asteraceae	NR	NR	EtOH
Boswellia carteri Birdw.	Burseraceae	NR	Reflux	EtOH 75%
Brassica hirta Moench	Brassicaceae	Seed	Reflux	MeOH
Brassica juncea (L.) Czern.	Brassicaceae	Seed	NR	EtOH
Brassica rapa L.	Brassicaceae	Seed	NR	NR
Buxus wallichiana Baill.	Buxaceae	Bark	Soxhlet	Petroleum ether, CHCl3, MeOH, H2O
Calotropis gigantea (L.) W. T.Aiton	Apocynaceae	Leaf	Maceration	NR
Camellia oleifera C.Abel	Theaceae	Seed cake	NR	EtOH 60%, CaO
Camellia sinensis (L.) Kuntze	Theaceae	Leaf, Leaf	NR, 50 °C/3 h	EtOH 30%, MeOH 50%
Carthamus tinctorius L.	Asteraceae	Flower	Maceration (2×), Decoction, NR	EtOH 50, 95%, H2O, EtOH 30%
Centella asiatica (L.) Urb.	Apiaceae	Leaf	Soxhlet	EtOH
Chamaecyparis obtusa (Siebold & Zucc.) Endl.	Cupressaceae	NR	Vapor	H2O
Chrysanthemum indicum L.	Asteraceae	NR	Reflux	EtOH 75%
Chrysanthemum zawadskii Herbich	Asteraceae	Whole plant	Reflux	EtOH 95%
Chrysanthemum zawadskii var. latilobum (Maxim.) Kitam.	Asteraceae	Whole plant	Ultrasonic	EtOH 70%
Chrysanthemum zawadskii var. latilobum (Maxim.) Kitam.	Asteraceae	Aerial parts	NR	MeOH 95%
Cinchona succirubra Pav. ex Klotzsch	Rubiaceae	Bark	NR	EtOH
Cinnamomum osmophloeum Kaneh.	Lauraceae	Leaf	Gasheating cryogenic distillation	H2O
Cistanche tubulosa (Schenk) Wight ex Hook.f.	Orobanchaceae	NR (2×)	NR (2×)	H2O, EtOH 80%
Citrullus colocynthis (L.) Schrad.	Cucurbitaceae	Fruit	Soxhlet	Petroleum ether after EtOH 95%
Clitoria ternatea L.	Fabaceae	Flower	Flowers crushed and filtered	NA
Cnidium officinale Makino	Apiaceae	Root	NR	EtOH 30%
Cocos nucifera L.	Arecaceae	Fruit	NR	NR
Coix lacryma-jobi L.	Poaceae	NR	Maceration	EtOH 70%
Commiphora molmol (Engl.) Engl. ex Tschirch	Burseraceae	NR	Reflux	EtOH 75%
Corydalis ternata Nakai	Papaveraceae	NR	Reflux	EtOH 75%
Crataegus cuneata Siebold & Zucc.	Rosaceae	Fruit	Reflux	MeOH
Crataegus pinnatifida Bunge	Rosaceae	Fruit	NR	H2O
Crinum asiaticum var. japonicum Backer	Amaryllidaceae	NR	NR	EtOH 95%
Cucumis melo var. makuwa Makino	Cucurbitaceae	Leaf	Reflux	H2O
Cucurbita pepo L.	Cucurbitaceae	Seed	NE	NE
Cuscuta reflexa Roxb.	Convolvulaceae	Stem	Soxhlet	Petroleum ether
Cynanchum wilfordii (Maxim.) Hemsl.	Apocynaceae	NR	Decoction, Boiling, Fermented by Bacillus subtilis	H2O
Cyperus rotundus L.	Cyperaceae	Rhizome	Soxhlet, NR	EtOH, NR
Dicerocaryum senecioides (Klotzsch) Abels	Pedaliaceae	Leaf	Shaker	EtOH
Dictamnus dasycarpus Turcz.	Rutaceae	Root bark	NR	EtOH
Eclipta alba (L.) Hassk	Asteraceae	Leaf, Stems, and Flower, Aerial parts, Whole plant	NR, Reflux, Soxhlet	MeOH 95%, Petroleum ether MeOH, MeOH 95%
Eclipta prostrata L.	Asteraceae	NR, NR	Sonication, Boiling	MeOH, H2O
Equisetum hyemale L.	Equisetaceae	Stem	Maceration	Hexane, Ethyl acetate, MeOH, H2O
Erica multiflora L.	Ericaceae	NR	Maceration	EtOH 70%
Eriobotrya japonica (Thunb.) Lindl.	Rosaceae	Leaf	NR	NR
Erythrina variegata L.	Fabaceae	Leaf	Maceration	EtOH 96%
Geranium sibiricum L.	Geraniaceae	NR	NR	MeOH
Ginkgo biloba L.	Ginkgoaceae	Leaf	Maceration, Decoction	H2O, EtOH
Glycine max (L.) Merr.	Fabaceae	Bean	NR	NR
Glycine max subsp. soja (Siebold & Zucc.) H.Ohashi	Fabaceae	Bean	Shaker incubator	EtOH 20%
Glycyrrhiza glabra L.	Fabaceae	Root (4×)	Soxhlet (3×), Maceration	H2O : EtOH, Petroleum ether (2×), EtOH
Glycyrrhiza uralensis Fisch.	Fabaceae	Root, NR	NR, Reflux	EtOH 30%, Hot water : EtOH
Vitis vinifera L.	Vitaceae	Fruit	NR	NR
Hibiscus rosa-sinensis L.	Malvaceae	Leaf (4×), Leaf Flower (3×)	Soxhlet (3×), Percolation, Maceration	EtOH (3×), Petroleum ether (2×)
Hordeum vulgare L. var. distichon Alefeld	Poaceae	Seed	Maceration	H2O 75%:Acetone
Houttuynia cordata Thunb.	Saururaceae	NR	Boiling at 96 – 100 °C/4 h	H2O
Hura crepitans L.	Euphorbiaceae	Bark	NR	EtOH 70%
Hydrangea macrophylla (Thunb.) Ser.	Hydrangeaceae	NR	NR	NR
Indigofera suffruticosa Mill.	Fabaceae	NR	NR	Coconut oil
Lawsonia alba Lam.	Lythraceae	NR	NR	Coconut oil
Leea indica (Burm.f.) Merr.	Vitaceae	Leaf	Maceration	MeOH
Leonurus sibiricus L.	Lamiaceae
Lespedeza bicolor Turcz.	Fabaceae	Leaf	Maceration	MeOH 80%
Ligusticum striatum DC.	Apiaceae	NR	Boiling/Reflux	H2O/EtOH
Ligustrum lucidum W. T.Aiton	Oleaceae	NR	Reflux	MeOH
Liriope muscari (Decne.) L. H.Bailey	Asparagaceae	NR	Under pressure at at 100 °C/3 h	H2O
Loranthus parasiticus (L.) Merr.	Loranthaceae	NR	Boiling at 100 °C/2 h	H2O
Lycium chinense Mill.	Solanaceae	NR	Maceration	EtOH 70%
Solanum lycopersicum L.	Solanaceae	Fruit	NR	NR
Lygodium japonicum (Thunb.) Sw.	Lygodiaceae	Spore	Maceration	EtOH 50%
Malvaviscus arboreus Dill. ex Cav.	Malvaceae	Leaf	Maceration	EtOH 70%
Mangifera indica L.	Anacardiaceae	Leaf	Reflux	H2O
Martynia annua L.	Martyniaceae	Fruit, Leaf	Decoction, Fine paste	H2O
Melandrium firmum Rohrb.	Caryophyllaceae	Whole plant	NR	H2O
Miscanthus sinensis Andersson	Poaceae	Flower	NR	MeOH
Morus alba L.	Moraceae	NR	Reflux	EtOH 75%
Murraya koenigii (L.) Spreng.	Rutaceae	Leaf	Cloth pouch boiling	NR
Musa paradisiaca L.	Musaceae	Fruit	Soxhlet	MeOH, H2O
Myrica rubra (Lour.) Siebold & Zucc.	Myricaceae	NR	Maceration	EtOH 50%
Nardostachys jatamansi DC.	Caprifoliaceae	Rhizome	Soxhlet	Hexane
Naringi crenulata (Roxb.) Nicolson	Rutaceae	Leaf	Maceration	H2O, CHCl3, Acetone
Nigella sativa L.	Ranunculaceae	Seed	Boiling	Coconut oil 60%
Nothopanax scutellarius (Burm.f.) Merr.	Araliaceae	Leaf	Maceration	EtOH 96%
Ocimum gratissimum L.	Lamiaceae	Leaf	Hydrodistillation	H2O
Oryza sativa L.	Poaceae	Bran	Supercritical	CO2
Paeonia lactiflora Pall.	Paeoniaceae	Root	Boiling	H2O
Panax ginseng C. A.Mey.	Araliaceae	Dried root, Root	NR, NR	MeOH 95%, EtOH 30%
Perilla frutescens (L.) Britton	Lamiaceae	NR	Boiling at 96 – 100 °C/4 h	H2O
Perilla L.	Lamiaceae	NR	NR	NR
Phyllanthus emblica L.	Phyllanthaceae	Dried fruit	Fried	Sesame oil
Phyllanthus niruri L.	Phyllanthaceae	NR	Maceration	EtOH 70%
Phyllanthus urinaria L.	Phyllanthaceae	Whole plant	Reflux	EtOH 50%
Pinus densiflora Siebold & Zucc.	Pinaceae	NR	Reflux	H2O : EtOH
Pinus thunbergii Parl.	Pinaceae	Bark	Reflux	H2O
Piper nigrum L.	Piperaceae	Leaf	Reflux	MeOH 50%
Platycarya strobilacea Siebold & Zucc.	Juglandaceae	NR	NE	NE
Platycladus orientalis (L.) Franco	Cupressaceae	Leaf	Reflux	EtOH 70%
Polygara senega var. latifolia Torr. et Gray	Polygalaceae	Root	NR	MeOH
Polygonum multiflorum Thunb.	Polygonaceae	Root	NR	MeOH 95%
Prunus mira Koehne	Rosaceae	Seed	Pressing seeds	NA
Prunus persica Batsch	Rosaceae	Seed	NR	EtOH 30%
Psoralea corylifolia L.	Fabaceae	NR	Boiling at 100 °C/2 h	H2O
Pueraria thomsonii Benth.	Fabaceae	NR	Reflux	EtOH 50%
Punica granatum L.	Lythraceae	Leaf	Soxhlet	EtOH: H2O
Rehmannia glutinosa (Gaertn.) DC.	Orobanchaceae	NR	Boiling	H2O
Ribes nigrum L.	Grossulariaceae	NR	NR	NR
Rosa multiflora Benth.	Rosaceae	Fruit	NR	NR
Rosa rugosa Thumb. var. plena Regl.	Rosaceae	Flower	Maceration	EtOH 50%
Rosmarinus officinalis L.	Lamiaceae	Leaf	Reflux	EtOH 50%
Rubus coreanus Miquel	Rosaceae	NR	Boiling at 100 °C/2 h	H2O
Rumex japonicus Houtt.	Polygonaceae	Root	NR	EtOH 95%
Russelia equisetiformis Schltdl. & Cham.	Plantaginaceae	Whole plant	Cold extraction	MeOH
Salvia miltiorrhiza Bunge	Lamiaceae	Root	NR	EtOH 30%
Salvia plebeia R.Brown	Lamiaceae	Whole plant	Maceration	MeOH
Sanguisorba officinalis L.	Rosaceae	Root	NR	NR
Schisandra nigra Maxim.	Schisandraceae	Fruit	Maceration	EtOH 85%
Schisandra Michx.	Schisandraceae	Fruit	Decoction	H2O
Schizandra chinensis (Turcz.) Baill.	Schisandraceae	NR	Boiling at 100 °C/2 h	H2O
Scrophularia buergeriana Miq.	Scrophulariaceae	Root	NR	EtOH 30%
Serenoa repens (W.Bartram) Small	Arecaceae	NE	NE	NE
Sesamum indicum L.	Pedaliaceae	NR	Reflux	EtOH 75%
Sophora angustifolia Siebold & Zucc.	Fabaceae	NR	Reflux	H2O : EtOH
Sophora flavescens Aiton	Fabaceae	Root	NR	EtOH
Stemona japonica (Bl.) Miq.	Stemonaceae	NR	Under pressure at at 100 °C/3 h	H2O
Sterculia urceolata Sm.	Malvaceae	Leaf	Maceration	EtOH
Theobroma cacao L.	Malvaceae	Fruit peel	Maceration	EtOH 96%
Thuja orientalis L.	Cupressaceae	Leaf	NR	Hot water
Thuja occidentalis L.	Cupressaceae	NR	Reflux	EtOH 95%:Ethyl acetate
Trichosanthes cucumerina L.	Cucurbitaceae	Leaf	NR	H2O
Tridax procumbens L.	Asteraceae	Entire aerial part	NR	NR
Trigonella foenum-graecum L.	Fabaceae	Seed, Seed	Direct boiling, Paste cloth method (boiling)	Olive oil, NR
Vernonia anthelmintica (L.) Willd.	Asteraceae	Seed	NR	EtOH 60%
Vitex rotundifolia L.f	Lamiaceae	Fruit	Reflux	MeOH
Wikstroemia retusa A.Grey	Thymelaeaceae	Bark	NR	EtOH 70%
Wrightia tinctoria R.Br.	Apocynaceae	Leaf and bark	Maceration	Coconut oil
Zanthoxylum schinifolium Siebold & Zucc.	Rutaceae	Bark	NR	EtOH 30%
Ziziphus mauritiana Lam.	Rhamnaceae	Root	Maceration	EtOH
Zizyphus jujuba Mill.	Rhamnaceae	Seed	Hydrodistillation	H2O

Isolated substances

Thirty-one articles (17.71%) used isolated substances. A total of 37 different substances were identified and are depicted in [Table 5].

Table 5 Isolated substances found in all evaluated articles.

Number of isolated substances	Chemical class	References
(1) Oleuropein	Iridoid	[104]
(2) Cedrol	Sesquiterpenoid	[66], [183]
(3) Baicalin	Flavonoid	[114], [115]
(4) Lycopene	Carotenoid	[153]
(5) Ginsenoside Rb1	Saponin	[173]
(6) Ginsenoside Rd	Saponin	[173]
(7) Ginsenoside F2	Saponin	[99], [172]
(8) Procyanidin B-3	Proanthocyanidin	[68]
(9) (+)-Catechin	Flavonoid	[68]
(10) Stigmast-5-en-3-O-glucopyranosidetriacetate-51-ol	Steroid	[110]
(11) Shikimic acid	Carboxylic acid	[79]
(12) 2,3,5,4′-Tetrahydroxystilbene-2-O-β-D-glucoside	Polyphenol	[87]
(13) 6-Gingerol	Ketone	[24]
(14) Astragaloside IV	Saponin	[116]
(15) Ginsenoside Ro	Saponin	[151]
(16) Formononetin	Isoflavone	[106]
(17) Linoleic acid	Fatty acid	[31], [41]
(18) Policosanol	Alcohol	[41]
(19) γ-Oryzanol	Sterol Ferulate	[41]
(20) γ-Tocotrienol	Tocotrienol	[41]
(21) β-Sitosterol	Phytosterol	[31]
(22) Bicyclo(10.1.0)tridec-1-ene	Cyclic olefin	[31]
(23) 6,7-Epoxy-5-hydroxyresiniferonol-14-(2,4-tetradecadienoate)	Diterpenoid	[31]
(24) Capsaicin	Alkaloid	[121]
(25) Nardin	Terpenoid	[57]
(26) Jatamansic acid	Terpenoid	[57]
(27) α-Terpineol	Monoterpene alcohol	[178]
(28) L-Menthol	Monoterpene alcohol	[132]
(29) Stevioside	Diterpene glycoside	[132]
(30) Cyanidin 3-O-arabinoside	Anthocyanin	[125]
(31) Apocynin	Acetophenone	[125]
(32) WGBP-A2b	Polysaccharides	[32]
(33) Fisetin	Flavonoid	[169]
(34) Resveratrol	Polyphenol	[169], [196]
(35) Physcion	Anthraquinone	[56]
(36) Decursin	Coumarin	[150]
(37) Timosaponin BII	Saponin	[55]

Algae

Eleven studies (6.29%) analyzed algae to verify hair growth activity. The algae were Ecklonia cava Kjellman, Ishige sinicola (Setchell & N. L.Gardner) Chihara, Undariopsis peterseniana (Kjellmann) Miyabe & Okamura, Sargassum kjellmanianum f. muticum Yendo, Sargassum glaucescens J.Agardh, Fucus vesiculosus, Laminaria japonica Areschoug, Eucheuma cottonii Weber Bosse, and Undaria pinnatifida (Harvey) Suringar.

Safety assessment

Less than 20% of the studies (n = 34) performed a primary skin irritation test on the animals. Only nine studies (5.14%) investigated the presence of acute or chronic inflammatory processes, six studies performed toxicity tests (3.43%) of the investigated substances, and only one study (0.57%) evaluated clinical manifestations and animal behavior.

Reproducibility is a fundamental pillar of scientific research, being essential to validate and consolidate discoveries. During data extraction, we identified that many studies lack clarity and completeness in data presentation. The omission of essential information compromises not only the robustness of the results obtained, but also the ability of other researchers to replicate and expand knowledge.

Discussion

This is the first systematic scoping review to synthesize the evidence of over 170 experimental in vivo studies on the effects of plants on hair growth activity. Our study mapped the methods, the animal models, and alopecia induction and reported the plant species, algae, and isolated substances investigated.

Although we were able to gather the evidence mentioned above, we observed that several studies had “flaws” because they were unclear or did not report all the necessary information about the models, methods, and study results, such as lineage, sex, weight, age of animals, name of the plant species used or the correct and accepted scientific name of the plant species, part of the plant material used, extraction and partition method, the solvent used, and others. This information is paramount to allow data comparison and scientific reproducibility [199], [200]. In addition, due to the heterogeneity between the studies (different animal models, methods of inducing alopecia, methods of evaluating hair growth, and markers used), it was not possible to compare them. Therefore, based on the information reported in the studies included in our review, we created a checklist that researchers should complete when evaluating natural compounds with hair growth activity ([Table 6]). This checklist aims to standardize the conduct and reporting of studies in this area, thus allowing the comparison of studies and the establishment of firm conclusions. Furthermore, it will direct the investigation of the mechanisms of action of the compounds.

Table 6 Checklist for conduct and reporting experimental in vivo studies.

Checklist Item	Reported on page nº
Animal model
Strain
Sex
Age
Weight
Guidelines – Committee approved
Induction of alopecia
Hormonal
Antineoplastics
Other type
Plant specie
Complete, correct, and accepted scientific name of the specimen
Date of plant collection (day, month, year)
Place of plant collection (city, state, country)
Coordinates of plant collection (latitude and longitude)
Voucher specimen number
Name of the Herbarium code (Index Herbarium)
Name of the person responsible for the collection and identification of the species
Isolated Substance
Complete, correct, accepted scientific name of the compound and chemical structure
If purchased, mention the name of the industry/ laboratory
Crude extract production
Part of the plant used, ground, and fresh or dried
Solvent and volume used
Plant and solvent proportion (w/v)
Method of extraction
Time and temperature of extraction
Yield of crude extract
Fraction production
Solvent and volume used
Method of extraction
Time and temperature of extraction
Yield of fraction
Safety evaluation
Primary skin irritation test
Toxicity tests
Investigation of inflammatory infiltrates
Observation of animal behavior
Duration of treatment
Methodology
Hair growth analysis
Qualitative
Visual observation/photography (skin color)
Hair growth initiation time and completion time
Quantitative
Hair length
Hair growth score
Hair density
Hair weight
Hair growth % area
Hair thickness
Others Yes ( ) No ( )
Which
Histological analysis
Number of hair follicle
Anagen/Telogen ratio
Length of hair follicle
Observation of follicular phases
Depth of hair follicle
Thickness of hair follicle
Others Yes ( ) No ( )
Which
Immunohistochemistry
Yes ( ) No ( )
Which
Real-time polymerase chain reaction
Yes ( ) No ( )
Which
Western blot assay
Yes ( ) No ( )
Which
ELISA
Yes ( ) No ( )
Which
Biochemical analyses
Yes ( ) No ( )
Which

Previous studies have shown that several plant metabolites, such as polyphenolic compounds, fatty acids, phytoestrogens, capsaicin, procyanidin B2, and epigallocatechin-3-O-gallate, have hair growth activity [201], [202], [203], [204]. Plants and their active compounds can induce hair growth via stimulation or inhibition of growth factors, cytokines, hormones, and enzymes or through modulation of signaling pathways [205]. In our review, a survey of 152 different plant species and 37 isolated substances evaluated in in vivo models of hair growth are depicted in [Tables 4] and [5], respectively. We also present the chemical structures of the isolated substances identified in the studies (Figure 1S, Supporting Information).

This review identified that 73.14% of the studies used mice as an experimental model, especially the C57BL/6 strain. This strain is the most used in in vivo models [174], [206] because it allows the visual assessment of hair growth since the animalsʼ skin color changes from pink to black as the hair cycle progresses from telogen to anagen [207]. This is because truncal pigmentation in animals is dependent on their follicular melanocytes. Melanin production in hair follicles is associated with the anagen phase of the hair growth cycle [208].

Hair growth and histological analyses were the most frequently performed methods in the included studies. However, these techniques lack information about the probable mechanism of action of the substances. Furthermore, we identified that only one-third of the included studies conducted molecular biology analyses. These methodologies contribute to investigating the probable mechanism of action of the substances in hair growth, as they allow the identification of levels and expression of cytokines, growth factors and signaling pathways involved in the hair cycle [209], [210], [211], [212]. Understanding and clarifying the mechanisms of action of plant species in promoting hair growth is important and should be further investigated in future research so that new herbal products that are effective against hair loss are available on the market [19].

Our review also found that very few studies conducted tests to assess the safety and irritation potential of the extracts or tested substances, such as primary skin irritation tests, toxicity tests, investigation of inflammatory infiltrates, and/or observation of animal behavior. These tests are important and must be performed to have reliable and safe herbal products for patients, minimizing risks and ensuring the protection of human health [213], [214].

This study has some limitations. It was not possible to find 12 of the studies, although we contacted the authors and requested information from colleagues from other countries and institutions. Another limitation was the heterogeneity between the studies, making it impossible to compare them. Thus, filling out the checklist that we developed should be considered.

However, it can be stated that the most widely used animal model was the mouse. Histological analyses accompanied by immunohistochemistry, gene expression analysis, and Western blot assay were the most commonly used.

Finding a product of natural origin for the treatment of alopecia will improve patientsʼ quality of life and help prevent people from taking their lives due to this situation, which we understand is not merely about esthetics but is a public health problem.

Conclusion

The treatment of alopecia remains a challenge for modern medicine. Although many natural drugs have been studied and discovered, it is still necessary to search for new hair-promoting agents. Furthermore, the underlying mechanisms of many compounds have not been studied or explained in detail.

The data synthesized in this review and the checklist can support and guide the development and execution of more robust future research that will contribute to an effective and safe natural product being approved and included for the treatment of alopecia. In addition, it will allow the comparison, reproducibility, and standardized reporting of results.

Contributorsʼ Statement

Conceptualization: JCPM; Methodology: SBG, MNP, MMF, DCMA, DC; Formal analysis and investigation and Writing – original draft preparation: SBG, MMF; Writing – review and editing, Funding acquisition, and Supervision: JCPM.

Conflict of Interest

The authors declare that they have no conflict of interest.

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Publication History

Received: 12 August 2024

Accepted after revision: 29 November 2024

Accepted Manuscript online:
02 December 2024

Article published online:
20 January 2025