A Bibliographic Assessment Using the Degrees of Publication Method: Medicinal Plants from the Rural Greater Mpigi Region (Uganda)

In ethnopharmacological research, many field assessment tools exist. Yet, these miss that critical point of how to really determine which species merit the costly lab studies, e.g., evaluation of traditional use via pharmacological assays and isolation of bioactive secondary metabolites. This gap can be filled with the introduction of a new tool for literature assessment: the Degrees of Publication (DoPs). In this study, its application is illustrated through an extensive bibliographic assessment of 16 medicinal plant species that were recently identified in the Greater Mpigi region of Uganda as being frequently used by local traditional healers in the treatment of medical disorders (namely, Albizia coriaria, Cassine buchananii, Combretum molle, Erythrina abyssinica, Ficus saussureana, Harungana madagascariensis, Leucas calostachys, Microgramma lycopodioides, Morella kandtiana, Plectranthus hadiensis, Securidaca longipedunculata, Sesamum calycinum subsp. angustifolium, Solanum aculeastrum, Toddalia asiatica, Warburgia ugandensis, and Zanthoxylum chalybeum). These species are suspected to be understudied, and a thorough bibliographic assessment has not been previously performed. Thus, the objectives of our study were to undertake a comparative assessment of the degree to which each of these plant species has been studied in the past, including evaluation of the quality of the journals where results were published in. The determination of the DoPs enabled successful assessment of the degrees to which each individual plant species has been studied so far, while also taking into account the methodological “research chain of ethnopharmacology” from ethnobotanical studies (“traditional use”) to pharmacological assays (“bioactivity”) and finally to pharmacognostic research (“structure elucidation”). The significance of a research paper was assessed by determining whether its journal and publishing house were members of the Committee on Publication Ethics (COPE). In total, 634 peer-reviewed publications were reviewed covering the period of 1960–2019, 53.3% of which were published in journals and by publishing houses affiliated with COPE (338 publications). The literature assessment resulted in the identification of understudied plants among the selected species. The majority of plants reviewed have not been sufficiently studied; six species were classified as being highly understudied and three more as being understudied: C. buchananii, F. saussureana, L. calostachys, M. lycopodioides, M. kandtiana, and S. calycinum subsp. angustifolium and A. coriaria, P. hadiensis, and S. aculeastrum, respectively. The newly introduced DoPs are a useful tool for the selection of traditionally used species for future laboratory studies, especially for pharmacological bioassays, isolation procedures, and drug discovery strategies.


Introduction
roughout human history and across the globe, plants were regarded as the major source of medicine and natural remedies. Traditional medicine is defined by the World Health Organization (WHO) as "the knowledge, skills, and practices based on the theories, beliefs, and experiences indigenous to different cultures, used in the maintenance of health and in the prevention, diagnosis, and improvement or treatment of physical and mental illness" [1]. In the developing world, over 80% of the population still rely on traditional herbal medicines for their day-to-day healthcare needs [2][3][4]. is is largely attributed to their ease of access, affordability, perceived fewer side effects, and cultural appropriateness, among other reasons [5]. Despite the general loss of cultural practices worldwide [6,7], traditional medicine practices and medicinal plant use are still the predominant form of healthcare services in East and Central Africa today [8,9]. e global importance of plants as a source of medicine is also often emphasized by scientists worldwide [10][11][12][13][14]. Around 25% of the Western drugs prescribed contain active ingredients that were initially isolated as natural products from plants [10]. Still, the majority of Earth's plant species has never been screened for pharmacological effects in a research facility [10,15].
In consideration of this global importance, there are many assessment tools applied when reporting field studies in the science of ethnopharmacology. ese include field assessment indices for medicinally used species, such as the frequency of citation, use value, informant consensus factor, and fidelity level, among others. However, none of these take into account how to really determine which species merit the costly lab studies. is is why we introduce the Degrees of Publication (DoPs), providing a standardized way to examine how well studied individual species are (or are not) in an ethnopharmacological context. In this study, 16 medicinal plant species from the Greater Mpigi region were selected to illustrate how the new tool works.
Situated in West-Central Uganda, the tropical Greater Mpigi region displays a high abundance of traditional medicine practitioners and diverse use of a vast amount of medicinal plant species [14,16,17]. Consequently, local people are still highly dependent on these traditional healers and their medicinal plants in order to secure their primary health care.
A recently published ethnobotanical survey from the Greater Mpigi region [14] and an ethnopharmacological study [18] identified 16 medicinal plant species that are often used in the treatment of medical disorders in the local traditional medicine system while displaying high pharmacological activity in our ongoing in vitro evaluation in a lab setting. A preliminary literature review resulted in a few results. erefore, these 16 plants are suspected to be understudied species, and a thorough literature review using the new DoP method for bibliographic assessment enables the selection of traditionally used species for pharmacological bioassays and drug discovery strategies. Our study, therefore, aims to undertake a comparative literature assessment, applying the DoP method, regarding (a) other reports of these species, (b) the quality of the journals where results were published in (assessment of international standards and best practice in scholarly publication ethics), and (c) the degree to which each plant species has been studied thus far.

Study Objects.
Our study objects are 16 tropical plant species identified to be frequently used by Ugandan traditional healers in treatment of diverse medical disorders in the Greater Mpigi region. is choice of species can be considered taxonomically diverse, representing 13 different plant families. Table 1 lists these species, stating their scientific names, local names at the study site (Luganda language), their plant families, and their Relative Frequencies of Citation (RFC), calculated from absolute values of the ethnobotanical survey (n � 39) previously published by Schultz et al. [14].

Literature Review.
Our research strategy included prioritization of some of the collected plant species for future pharmacological bioassays. Here, the results of the ethnobotanical survey on traditional use were the major indicator [14]. However, another parameter for this assessment was conducting a literature survey, identifying those medicinal plant species that are currently understudied, hereby limiting duplication of research efforts.
A literature search of electronic databases included GoogleScholar and the Web of Science Core Collection, using the scientific name of each plant as keywords (synonyms included). As suggested by Heinrich et al. [19], NAPRALERT®, a comprehensive natural-product database containing ethnomedical and pharmacological information of extracts and isolated compounds, was consulted as an additional tool (http://www.napralert.org). Membership in the Committee on Publication Ethics (COPE) was assessed by searching for an individual journal and the corresponding publishing house on the COPE website (http://www. publicationethics.org/members). Digitalized herbarium voucher specimens were obtained from the JSTOR Global Plants Database (https://plants.jstor.org).

Data Analysis: Degrees of Publication.
e results of the literature survey were analyzed by categorizing published studies on the 16 medicinal plant species. A new indicator was introduced: the Degrees of Publication (DoPs). DoPs were defined as "Traditional Use," "Bioactivity," "Structure Elucidation," "Other," and "Total (without <other>)." "Traditional use" are sources stating that a plant species i is used traditionally in an ethnopharmacological context. e 2 Evidence-Based Complementary and Alternative Medicine DoP "Bioactivity" describes the number of published studies investigating a potential pharmacological activity of an extract from a plant i. "Structure elucidation" includes studies that resulted in isolation of (bioactive) secondary metabolites and their structure elucidation. ese three DoPs are consecutive steps in the bioassay-guided discovery of novel bioactive natural products based on the ethnopharmacological approach of investigating traditional use reports.
is classification, therefore, may lead to an assessment of the degree to which each plant species has been studied so far. e DoP "Other" classifies all publications mentioning a plant species i in a non-ethnopharmacological context (e.g., studies on the morphology of the species, on the distribution of species, or on non-medicinal traditional use of a species).
e DoP "Total (without <other>)" summarizes the three ethnopharmacologically relevant DoPs and is defined as the sum of "Traditional Use," "Bioactivity," and "Structure Elucidation." For each DoP, absolute numbers were given as value N all and N COPE , whereas N all describes all publications discovered in the literature survey, and N COPE lists all publications in scientific journals whose publishing houses are members of the Committee on Publication Ethics (COPE, http://www. publicationethics.org). Members of the COPE must accept the international standards and best practice in the ethics of scholarly publishing, meaning that membership of the COPE is an appropriate indicator for high-quality research. A DoP "Total (without <other>)" of N all ranging from 0 to 14 classifies a plant species as being "highly understudied," while 15-29 is "understudied," 30-44 is "moderately studied," and 45-∞ is "highly studied." Figure 1 is a compilation of digitized herbarium voucher specimens to give an overview of the appearance of each of the 16 plant species. Sections 3.1.1-3.1.16 provide information on synonyms, geographical distribution (in Uganda, in particular), life forms, ecological growth conditions and climate zones, local names in East Africa, and some basic characteristics for each of the selected plants.

Leucas calostachys.
Synonyms are Leucas calostachys var. calostachys and Leucas calostachys var. fasciculata (Baker) Sebald. L. calostachys is an aromatic herb that occurs in some parts of Uganda, including the Greater Mpigi region [14]. However, there is limited literature on this species. e local name in Luganda language is as follows: kakuba musulo [14]. ere is one synonym: Myrica kandtiana Engl. M. kandtiana is an herb, shrub, or short multibranched tree that spreads. e flowers are on the inflorescences, which are greenish yellow. e inflorescences occur on the older rather than on the younger branches. It grows in grasslands, in seasonal swamps, or swampy areas, but is very rare nowadays [41,42]. Local names in different languages in Uganda are as follows: Luganda: mukikimbo, bowolola omusajja, and enkikimbo [14,41,43] and Runyankore/Runyoro: omujeje [41].

Sesamum calycinum Subsp. angustifolium.
ere are two synonyms: Sesamum angustifolium (Oliv.) Engl. and Sesamum indicum var. angustifolium Oliv. S. calycinum subsp. angustifolium is an erect, annual to perennial herb with or without side branches. It can reach a height of 0.4-2.0 m. e flowers appear pink or purple and often have spots within. Its distribution encompasses eastern tropical Africa, including Uganda, Tanzania, Democratic Republic of Congo, and Kenya and south to Malawi, Zambia, and Mozambique. It is occasionally cultivated as a vegetable and prefers sandy soil. It frequently grows by roadsides, in grasslands, and open woodlands [46]. Local names in different languages in Uganda are as follows: Luganda: lutungotungo [14,21] and Lusoga: lutungotungo [21].

Solanum aculeastrum.
is plant species is a large shrub or small tree, and it was reported to be cultivated in Rugazi, Bynyaruguru, and Ankole in western Uganda [41]. It can reach up to 6 m in height [20]. S. aculeastrum is a native African plant that occurs from the South African Cape to the Imatong mountains in Sudan and westwards to Cameroon [47]. Its branchlets are densely covered in woolly hairs and possess sharp, curved thorns [48]. It flowers from September to July, peaking in November and March, and fruits from April to January, peaking in June and November [49]. e fruits are extremely bitter and highly toxic due to the presence of the poisonous alkaloid solanine [24,50]. e species is regionally known as "bitter apple" [20]. Local names in Uganda are as follows: Luganda: ekitengo, entego eddene, and entengo lyabalalo [14,20,41]. Local names in other East African countries and languages are as follows: Kikuyu: mutura [20], Kipsigis: siganet [20], and Maasai: osigawai [20].

Literature Review.
e determination of the DoPs enabled successful assessment of the degrees to which each individual plant species has been studied so far, while also taking into account the methodological "research chain of ethnopharmacology" from ethnobotanical studies ("traditional use") to pharmacological assays ("bioactivity") and finally to pharmacognostic research ("structure elucidation"). e significance of a research paper was also assessed by determining whether its journal and publishing house were members of the COPE. e literature survey was completed on 31 July 2019 and covered the period of 1960-2019. In total, 634 peer-reviewed publications were reviewed, 53.3% of which were published in journals, and by publishing houses affiliated with the COPE (338 publications). ese articles were published in 304 different academic journals, of which 114 are COPE members. A cloud-based literature library was successfully created, first categorizing publications according to the selected plant species mentioned in the paper and subsequently, according to their individual DoPs ("Traditional use," "Bioactivity," "Structure elucidation," and "Other"). Excluding the DoP "Other," there were a total of 441 fieldrelated original research papers, of which 245 were published by journals with COPE membership (55.6%).

3.4.
Journal Analysis and COPE Assessment. Subsequently, the frequency of each DoP term's publication in individual peer-reviewed journals ("abundance of publication") was assessed. e results are shown in Figure 3. e significance of COPE member Journal of Ethnopharmacology (JEP) to the field can be affirmed, as by far the greatest proportion of related articles describing "Traditional use" and "Bioactivity" were published in the JEP, as well as the fourth-highest number of papers recorded for the DoP "Structure elucidation." Overall, 36.7 % of all publications categorized under the DoP "Traditional use" (51 articles) were printed in the JEP, 15.1% in the case of the DoP "Bioactivity" (28 articles), and 4.3% for the DoP "Structure elucidation" (5 articles).
Other journals that published the greatest proportion of "Traditional use"-related papers on the 16  In terms of the DoP "Bioactivity," the second-largest proportion of papers was published in the African Journal of Traditional, Complementary and Alternative Medicines (6.5%, 12 articles), followed by Phytotherapy Research (3.5%, 6 articles, COPE member) and African Health Sciences (2.7%, 5 articles). Ninety-seven other journals with minor article distribution (<2.5%) were identified and summarized under "Other" (72.6%, 135 articles). e majority of these journals are not COPE members (64 journals). e most dominant journals for the DoP "Structure elucidation" were the COPE members Phytotherapy (11.2%, 13 articles) and Journal of Natural Products (9.5%, 11 articles). ese journals are also followed by COPE members to the biggest part: Planta Medica (5.2, 6 articles), the JEP (4.3%, 5 articles, COPE member), Phytotherapy Research   Evidence-Based Complementary and Alternative Medicine

Assessment of Study Progress for Each Species.
e DoPs were used as a tool for assessment of the degree to which a species has been studied so far. Results on individual plants are shown in Figure 4 (accumulated DoPs, excluding the DoP "Other") and Table 2 (absolute values of individual DoP categories). Values in red or in square brackets state the total number of articles published in journals with COPE membership that committed themselves to reaching highest standards and best practice in scholarly publication ethics.
According to results of our literature review, M. lycopodioides has been studied and mentioned in a total of 63 journal articles over the past 60 years. However, the vast majority of these papers deal with non-medicinal use and are not part of drug discovery-related research. e papers mainly describe the occurrence of the fern species in the American tropical forests and its extraordinary morphology/biology; traditional medicinal use has only been mentioned in two publications so far. Here, it has been reported to be used for removal of lice and to treat anemia in South Africa and Tanzania [56]. e second publication  reports traditional use by the Zambo-Miskito ethnic group of Eastern Nicaragua to cure bewitchment and chase away evil spirits [57]. Traditional use of the shrub M. kandtiana has also only been previously described in two publications following ethnobotanical surveys. Just as in our ethnobotanical study in the Greater Mpigi region [14], its roots were cited to be used in treatment of HIV/AIDS in one of the four surveyed Ugandan districts [58]. e second paper names M. kandtiana bark, leaves, and fruits as a natural remedy in treatment of tuberculosis (fruits, leaves, roots, and bark used) in the Butambala and Mpigi Districts, which constitute a major part of the Greater Mpigi region [43]. In our ethnobotanical survey [14], we were able to confirm these citations of traditional use in the study area (root bark, leaves, and roots). ere were no other publications from any other field identified, mentioning M. kandtiana.    Figure 4: Summarized "total" DoPs (without "Other") for assessment of degree to which the species have been studied so far; blue � total number of journal articles; red � number of journal articles from publishing houses with COPE membership.
As far as M. lycopodioides and M. kandtiana are concerned, no studies on bioactivity or isolation and elucidation of active secondary metabolites have been published so far.
F. saussureana, S. calycinum subsp. angustifolium, and C. buchananii are still highly understudied, but research has progressed to the bioanalytical stage of structure identification.
Regarding F. saussureana, the intra-and interspecific variations in vacuolar flavonoids among Ficus species from the Budongo Forest, Uganda, were described [71]. Another paper, which undertook a pharmacological evaluation of bioactivity, investigated the vasodilating effect of the root bark extract of F. saussureana on the guinea pig aorta [72]. In addition, F. saussureana has also recently been mentioned in Ugandan traditional medicine for the use of its leaves and stem bark in the treatment of HIV/AIDS in parts of the Greater Mpigi region [17].
Only four publications mentioned the traditional use of S. calycinum subsp. angustifolium; however, there was one article on bioactive natural product structures isolated from this species. e first paper classifies S. calycinum subsp. angustifolium as a weed that is used medicinally as an emetic and contraceptive, as well as for treatment of eye diseases, diarrhea, burns, and wounds by the Haya people in the Kagera region, Tanzania [73]. In the second paper, Kibuuka and Anywar describe the traditional use of S. calycinum subsp. angustifolium against hernias in Central Uganda [16]. e third paper mentions the use of the fresh leaves in treatment of hypertension in Bulamogi county, Uganda (eaten together with Arachis hypogaea or Sesamum indicum) [74]. e fourth ethnobotanical study from the DoP traditional use was conducted in rural and urban areas across Central Uganda (including part of the Greater Mpigi region). e article mentions the use of the root powder (1 tablespoon) in 200 mL water, which is boiled for 5 minutes and then drunk twice a day to induce vomiting [75]. In terms of the DoP structure elucidation , Chidewe et al. isolated six compounds from S. calycinum subsp. angustifolium [76]. Two were already known (the hydrocarbon nonacosane and the glucosinolate glucoiberverin), while the other four remained unidentified and were not structure elucidated.
C. buchananii was mentioned twice as being used in other African countries and cultures, namely, as a natural remedy against fungal infections in the southern highlands of Tanzania [77] and against back pain, hernia, and erectile disfunction in the Kagera region, northwest Tanzania [78]. At our study site in the Greater Mpigi region [14], we also documented the common practice of using this plant medicinally in the treatment of erectile dysfunction. e Kagera region is relatively close to the Greater Mpigi region and also situated in the Lake Victoria basin. Among other Tanzanian medicinal plants traditionally used to treat fungal infections, C. buchananii has been investigated for cytotoxic, genotoxic, and CYP450 enzymatic competition effects [79]. In addition, in the 1990s, three compounds were isolated from C. buchananii: (1) elabunin, a novel dammarane triterpene from the root bark with moderate cytotoxic activity against L-1210 leukemic cells [80]; (2) mutangin, a novel sesquiterpene from the plant's fruit, with moderate antifeedant activity [81]; and (3) buchaninoside, a steroidal glycoside from the plant's fruit, with antifeedant activity against Spodoptera exempta larvae [82].
A. coriaria was reported to be used traditionally in 11 publications that show results of surveys conducted in Uganda, except for the one in Kenya. Forty traditional healers from the Greater Mpigi region named A. coriaria as one of their priority plants for the treatment of tuberculosis [43]. Two more studies from Mpigi district identified the stem bark and the leaves for treatment of HIV/AIDS and related medical disorders [17,58]. At another study site in Uganda, Katabi subcounty in Wakiso district, the leaves and the bark were used in treatment of wounds and skin rashes [97]. In Kakamega county, Kenya, the bark and the leaves were reported to be used in treatment of breast, uterine, and skin cancer [98]. Another publication assessed the ecological status and ethnobotany of A. coriaria in Budondo subcounty, eastern Uganda, highlighting its use, local harvesting patterns, and local attitudes towards its conservation. Community members consider the species as being rare, and abundance is declining in the region. Among many nonmedicinal uses, the root and the stem bark were used in the treatment of syphilis, skin diseases, jaundice, eye diseases, cough, sore throat, and to concentrate breast milk in humans [99]. Another study assessed the possibility of setting up multipurpose tree gardens to provide traditional healers with species used for medicine [100]. In the county of Bulamogi in Uganda, the bark is used by traditional healers in the treatment of diarrhea, "lameness" (butenge), syphilis, snake bites, and amoebiasis. e roots are used for the treatment of pyomyositis and amoebiasis. e leaves were also reported to be used against snake bites [74]. In Kibale rainforest, an aqueous decoction of the fresh stem bark is drunk to treat cough [101]. One Ugandan study assessed the Evidence-Based Complementary and Alternative Medicine domestication of medicinal tree species in the Victoria lakeshore region, including A. coriaria, and their distribution by vendors on local markets [102]. With regard to the DoP bioactivity , four publications were recorded. One article reported low antigiardial activity of a mixture of roots and bark against Giardia lambia at 500 µg/mL [64]. Another study investigated the stem bark and reported moderate in vitro antiplasmodial activity against Plasmodium falciparum D6 (IC 50 : 37.83 µg/mL) and low antileishmanial activity [103]. A dichloromethane extract of the stem bark displayed moderate antiplasmodial activity against P. falciparum D6 (IC 50 : 10.68 µg/mL) and the chloroquine-resistant P. falciparum W2 strain (IC 50 : 6.80 µg/mL) [104]. ree stem bark extracts with varying solvents displayed moderate to low growth inhibitory activity against five African livestock pathogens of the genus Mycoplasma [105]. Publications categorized under the DoP structure elucidation include reporting of the isolation of two new oleanane-type saponins, coriariosides A and B, along with a known saponin, gummiferaoside C, from the roots of A. coriaria. As part of this study, coriarioside A and gummiferaoside C displayed cytotoxic activity against the colorectal human HCT116 and HT29 cancer cells [83]. e same group of researchers published the isolation and structure elucidation of coriarioside C, D, and E from the roots shortly after [84].
Concerning S. aculeastrum and the DoP traditional use , multiple medicinal uses were recorded. ese include traditional use of (a) the berries and leaves in treatment of lymphatic filariasis in the KwaZulu-Natal and Mpumalanga regions of South Africa [121]; (b) the berries, leaves, roots, and bark against cancer in the Kakamega county of Kenya and Eastern Cape Province of South Africa [98,122]; (c) the roots to treat stomachache in Limpopo Province of South Africa [123]; and (d) the berry juice against ditlapedi (a facial skin condition) in the Central Sekhukhuneland of South Africa [124]. Although the practice is regarded by Rwandan women as "a positive force in their lives," S. aculeastrum has been described as being used as medicine applied during stretching sessions for elongation of the labia minora, which is classified as Type IV female genital mutilation by the World Health Organization [125]. Publications, categorized under the DoP bioactivity , reported low antioxidant activity of the berries and low antimicrobial activity of the berries and leaves against ten bacterial and five fungal strains [126][127][128][129]. A methanolic extract from the berries displayed low activity in inhibiting the growth of promastigotes in Leishmania major infection in BALB/c mice (IC 50 : 78.62 μg/ml) [130]. Methanolic extracts of the berries showed antiproliferative activity against human HeLa, MCF7, and HT29 tumour cell lines, while the leaf extracts displayed no cytotoxic activity [131]. In another study, the methanolic extracts of the leaves and the berries showed moderate activity against host snails of schistosomiasis [132]. MeOH-CH2Cl2 (1 :1, v/v) extracts from the stem bark and the berries showed growth inhibitory activity against five African livestock pathogens of the genus Mycoplasma, displaying a mean MIC value of 20 µg/mL [105]. One acute toxicity study of an extract of the unripe berries in Wistar rats resulted in toxicity symptoms such as respiratory distress, epistaxis, and hypoactivity that disappeared 72 h after treatment. Above 125 mg/kg body weight, the extract produced mortality in the Wistar rats, and the latency was inversely proportional to the doses [133]. Another study investigated the toxicological effect of the aqueous extract of fresh, dried, and boiled berries in male Wistar rats at 1, 10, and 25 mg/kg body weight for 28 days. e rats gained weight, but showed no signs of clinical toxicity at the doses tested [134]. Concerning the DoP structure elucidation , two new steroidal alkaloids were isolated from the root bark, along with known compounds such as solamargine and ß-solamargine [89,90]. Steroid alkaloids, namely, solasodine and tomatidine, isolated from the berries, displayed cytotoxic effects on the growth of HeLa, MCF7, and HT29 cancer cell lines and antioxidant properties [87,88]. Solamargine, isolated from the berries, induced nonselective cytotoxicity and P-glycoprotein inhibition [85]. Volatile oil fractions from the leaves and berries were investigated via GC-MS analysis and contained mainly alkanes and alkenes [86]. 12 Evidence-Based Complementary and Alternative Medicine  (22)) were classified as having been moderately studied in the past. A discussion of all the published literature was not conducted at this point because this would merit its own standalone review article for each of the three species. Review articles of the genera Warburgia [135,136], Zanthoxylum [137], and Erythrina [138] have been published.

Highly Studied
Species. Plant species identified as having been highly studied in the past are C. molle (DoP total � 49 (28)), H. madagascariensis (DoP total � 62 (27)), T. asiatica (DoP total � 64 (39)), and S. longipedunculata (DoP total � 66 (32)). A discussion of all the published literature was not conducted at this point because this would merit its own standalone review article for each of the four species. A review article of the genus Combretum [139], a minireview article of H. madagascariensis [140], and a review article of S. longipedunculata [141] have been published.

Conclusions
An extensive literature survey successfully assessed the degree to which a plant species has been studied so far, introducing a new indicator: the Degrees of Publication (DoPs). is literature assessment resulted in the identification of understudied plants among the selected 16 species. ree plant species were identified as being moderately studied (E. abyssinica, W. ugandensis, and Z. chalybeum), while four have already been highly studied over the past decades (C. molle, H. madagascariensis, S. longipedunculata, and T. asiatica). More importantly, the majority of plant species surveyed have not yet been investigated sufficiently. Six species were classified as being highly understudied (C. buchananii, F. saussureana, L. calostachys, M. lycopodioides, M. kandtiana, and S. calycinum subsp. angustifolium) and three more species as being understudied (A. coriaria, P. hadiensis, and S. aculeastrum). Due to the absence of any bioactivity-related publications for S. calycinum subsp. angustifolium, M. lycopodioides, and M. kandtiana, pharmacological evaluation of these species should be prioritized. e need for research and development of novel natural products is more vital than ever, making future studies on traditional herbal remedies justified and urgently required. Generally, there was no significant correlation between the DoPs (Figure 4) and the RFCs (Table 1) of individual plant species, previously published by Schultz et al. [14]. is is most likely due to the fact that the species are highly used within the study area (Greater Mpigi region, Uganda) but occur interregionally on the African continent, and some are even native to other continents (e.g., M. lycopodioides or T. asiatica). From the literature survey, it was noted that other natural plant habitats and ethnic groups than the people of the Greater Mpigi region were more often surveyed in the past, followed by ethnopharmacological lab studies of some of the plant species. In conclusion, the discrepancy between high regional medicinal use and low DoPs confirms the demand for studying the diverse cultures and ethnomedical practices of the Greater Mpigi region, in particular, and the 16 selected species, in general.
e new DoPs indicator proved to be a valuable tool that fills a gap compared to other ethnopharmacological tools. Other than existing field assessment tools, e.g., the relative frequency of citation, the fidelity level, the use value, and the informant consensus factor, the DoPs tool can be leveraged to better identify those species that are understudied and merit deeper investigation. is includes using the tool for selection of species for costly lab studies, thereby avoiding reproduction of results, while facilitating a more time-efficient approach to ethnopharmacological research. When applied by other researchers in the future, another value of the new tool will be that gaps in the literature could be filled more strategically, making ethnopharmacological research more targeted and efficient.
It should be noted that focusing on a logic approach to the field of ethnopharmacology, such as (a) starting with ethnobotanical/ethnopharmacological field studies; (b) continuing with validation of traditional medicine via in vitro and in vivo pharmacological assays in the lab, and (c) progressing to bioassay-guided fractionation, natural product isolation and structure elucidation studies, cannot always, though in most cases, be applied within the field. One such example would be ritual use or where pharmacological effects cannot be "measured," which would still be of value to the field, e.g., with symbolic significance to an indigenous community. Here, it would be categorized under the DoP traditional use , thus recognized, and lab studies may not follow.
Data Availability e data supporting this bibliographic assessment are from previously published studies, which have been cited. Individual information on publications categorized under different Degrees of Publication is available from the corresponding author upon request. Disclosure e content is solely the responsibility of the authors and does not necessarily reflect the official views of the funding agency. e funding agency had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflicts of Interest
e authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as potential conflicts of interest.

Authors' Contributions
FS designed the overall strategy of the study and the DoP concept, conducted the literature review, and processed the data. FS and CLQ interpreted the data. FS, GA, and CLQ wrote the manuscript. LAG directed the study. All authors read, revised, and approved the final manuscript.
Evidence-Based Complementary and Alternative Medicine 13