Anthelmintic Agents from African Medicinal Plants: Review and Prospects

Jato, Jonathan; Orman, Emmanuel; Duah Boakye, Yaw; Oppong Bekoe, Emelia; Oppong Bekoe, Samuel; Asare-Nkansah, Samuel; Spiegler, Verena; Hensel, Andreas; Liebau, Eva; Agyare, Christian

doi:https://doi.org/10.1155/2022/8023866

Evidence-Based Complementary and Alternative Medicine

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Abstract Introduction Conclusion Abbreviations Data Availability Conflicts of Interest Acknowledgments References Copyright Related Articles

Review Article | Open Access

Volume 2022 | Article ID 8023866 | https://doi.org/10.1155/2022/8023866

Anthelmintic Agents from African Medicinal Plants: Review and Prospects

Jonathan Jato,^1,2,3Emmanuel Orman,^3,4Yaw Duah Boakye,²Emelia Oppong Bekoe,⁵Samuel Oppong Bekoe,⁶Samuel Asare-Nkansah,⁶Verena Spiegler,³Andreas Hensel,³Eva Liebau,⁷and Christian Agyare²

Academic Editor: Harish Chandra

Received12 Sept 2022

Revised26 Nov 2022

Accepted16 Dec 2022

Published31 Dec 2022

Abstract

Soil-transmitted helminthiasis affects more than 1.5 billion people globally and largely remains a sanitary problem in Africa. These infections place a huge economic burden on poor countries and affect livestock production, causing substantial economic losses and poor animal health. The emergence of anthelmintic resistance, especially in livestock, and the potential for its widespread in humans create a need for the development of alternative therapies. Medicinal plants play a significant role in the management of parasitic diseases in humans and livestock, especially in Africa. This report reviews anthelmintic studies that have been conducted on medicinal plants growing in Africa and published within the past two decades. A search was made in various electronic databases, and only full articles in English were included in the review. Reports show that aqueous and hydroalcoholic extracts and polar fractions obtained from these crude extracts form the predominant (80%) form of the extracts studied. Medicinal plants, extracts, and compounds with different chemical groups have been studied for their anthelmintic potential. Polyphenols and terpenoids are the most reported groups. More than 64% of the studies employed in vitro assays against parasitic and nonparasitic nematode models. Egg hatch inhibition, larval migration inhibition, and paralysis are the common parameters assessed in vitro. About 72% of in vivo models involved small ruminants, 15% rodents, and 5% chicken. Egg and worm burden are the main factors assessed in vivo. There were no reports on interventions in humans cited within the period under consideration. Also, few reports have investigated the potential of combining plant extracts with common anthelmintic drugs. This review reveals the huge potential of African medicinal plants as sources of anthelmintic agents and the dire need for in-depth clinical studies of extracts, fractions, and compounds from African plants as anthelmintic agents in livestock, companion animals, and humans.

1. Introduction

Parasitic worms affect more than one-quarter of the world’s population, with soil-transmitted helminthiases (STH) accounting for about 1.5 billion infections [1, 2]. STH is one of the neglected tropical diseases (NTDs) that affects mainly people living in regions of high poverty, without adequate sanitation, and in close contact with infectious vectors, domestic animals, and livestock [2, 3]. They occur globally in the tropics and subtropics, including the Americas, Asia, and sub-Saharan Africa. These areas are more impacted because of the low levels of development [2, 4].

Helminth infection is largely a sanitary problem and is associated with the human-animal food chain. Parasite eggs present in human faeces contaminate the soil where they embryonate and are taken back into the intestinal tract through poorly treated drinking water and foods [5]. This creates a vicious cycle of recurrent infections that is often difficult to break or interrupt [3, 6].

Although helminthiases have a low fatality rate, they have a huge impact on human health and livestock production. The severity of symptoms in humans depends on the worm burden and whether monospecific or mixed infections are involved [2, 7]. Whilst children constitute the most vulnerable group to worm infestation, pregnant women also suffer impaired immunity and a lower quality of life [5, 8–10].

Based on the location of the adult parasite in the body, helminthiases may clinically present as intestinal (whipworms, intestinal roundworms, and hookworms), or tissue (trematodes, hydatid tapeworms, and tissue roundworms) parasites [5, 11]. The most common and widespread intestinal nematodes in humans include Ascaris lumbricoides, Ancylostoma duodenale, Necator americanus, Trichuris trichiura, and Strongyloides stercoralis, which have been classified as soil-transmitted helminthiases [3, 12]. Mild symptoms include abdominal pain, nausea, diarrhoea, and loss of appetite, and in children, severe cases may lead to anaemia, eosinophilia, stunted growth, malnutrition, pneumonia, and poor physical and cognitive development [3, 13]. High-intensity infections could result in intestinal obstruction requiring surgery and death in cases of Strongyloides stercoralis [14].

Unlike for some viral and bacterial diseases, there are currently no vaccines developed for human intestinal parasites [5, 15, 16]. In livestock, however, the first vaccine (Barbervax®) against H. contortus, which is derived from an intestinal surface antigen of the nematode, has proven to be a sustainable control measure in small ruminants [17]. Control measures mainly include periodic deworming, health education, and improvements in environmental sanitation. Seasonal chemotherapy with synthetic anthelmintics remains the primary measure to eliminate or reduce infecting helminths. Health education helps to prevent reinfection, while improved sanitary conditions reduce egg transfer to soil [14].

Morbidity due to helminthiases has been greatly reduced by the annual or biannual mass drug administration (MDA) in vulnerable populations. The two benzimidazole drugs, mebendazole and albendazole, are the core agents recommended by the World Health Organization (WHO) for MDA in children of school age. Both drugs are effective, cheap, easy to administer, and have been used in large populations for several years with minor side effects [14]. Other classes of anthelmintic drugs available include macrocyclic lactones, imidazothiazoles, tetrahydropyrimidines, and amino-acetonitrile derivatives. Other drugs, including levamisole, pyrantel pamoate, niclosamide, ivermectin, and piperazine, have contributed immensely to tackling livestock and human parasites [18].

The increase in cost, availability, continual reinfection, emergence of drug-resistant parasites, adverse events associated with population-wide drug use [9, 17, 19], and lack of coverage for other infectious agents like Strongyloides have become major drawbacks to the success of anthelmintic chemotherapy [20]. These threats have spurred the quest to discover and develop new, innovative, sustainable, effective, safe, alternative, and complementary treatment options, mostly from natural products [21–24].

In Africa, about 80% of the population largely depend on traditional remedies for their primary healthcare needs [25–27]. Compared to orthodox medicines, these remedies are relatively accessible and cheaper, perceived to be safe and effective, and form part of folkloric practices [22, 24, 28]. Plants form the larger part of these traditional remedies and have historically been used in treating internal parasites and other diseases in humans and livestock [15, 29, 30]. They constitute a viable source of chemically diverse molecules with broad-spectrum activity and can be a ready means to combat parasite resistance. From January 1981 to September 2019, 71 new approved drugs were entirely derived from natural products, 14 as natural botanicals, and 356 as semisynthetic derivatives of natural molecules [31]. However, there is currently no anthelmintic drug product approved that has been developed from plant sources [18].

Even though the chemical constituents and mechanisms by which medicinal plants elicit the observed activities are less known [28, 32], technological advancement has reignited research using in vitro and in vivo assays to evaluate ethnopharmacological claims and, where possible, identify such chemical entities and their mechanisms [22, 28].

This review is unique in the sense that it gathers information on anthelmintic extracts, fractions, and compounds from African medicinal plants. It seeks to reveal the potential of African medicinal plants as sources of new anthelmintic molecules and alternative therapies against helminthiases.

Whereas the African continent has a huge natural resource pool that is widely used by local people, especially indigenous people, for the management of many disease conditions, the continent remains one of the hardest hits by intestinal parasites [2]. There is increasing research into natural products, especially medicinal plants, as sources of new antiparasitic agents. Despite efforts to gather the library of these plant products, be they extracts, fractions, or purified compounds [7, 23, 33], those available from African medicinal plants are scattered and limited to certain geographical regions. This review, therefore, sought to expand this pool of information and to create a clear picture of the situation as far as studies of anthelmintic agents from African medicinal plants are concerned. Here, we elaborate on the various studies that have been conducted on medicinal plants native to Africa and espoused on the very promising plant families and species.

1.1. Methodology

1.1.1. Inclusion and Exclusion Criteria

For the scope of this review, full-text articles published in credible peer-reviewed journals, publishers, and repositories (see below) whose studies focused on the anthelmintic activities of medicinal plants that grow in Africa were included. Only articles written in English and published between January 2002 and December 2021 were included, no matter where the study was conducted.

Articles written before 2001 and after 2021 were excluded. Articles that focused on extracts, fractions, and/or compounds isolated from medicinal plants not growing in Africa were also excluded. Even though this review is extensive, it is not a systematic review. The review also significantly focused on gastrointestinal nematode-related studies than other types of helminthiases.

1.1.2. Literature Search and Data Extraction

Articles were identified through literature searches in relevant electronic databases and search engines, including Scopus, Science Direct, Academic Journals, African Journals Online (AJOL), HINARI, BioMed Central, Google Scholar, JSTOR, and PubMed. Bibliographies of included articles were further searched, and pertinent, relevant information retrieved in primary searches was added. This search was conducted between April 2020 and April 2022.

Articles that were retrieved were independently screened by at least three authors, and those that met the inclusion criteria were selected for review.

Data were often obtained from relevant portions of the articles, including the “materials and methods” and “results” sections. The extraction focused on the botanical source of plant material, the nature of extracts, fractions, or compounds, and the type of assay employed, including in vitro and in vivo studies. The relevant measures of efficacy in the test system, including IC₅₀, EC_50, LC₅₀, and LD₅₀, were used to assess the anthelmintic potential of the study samples. Mendeley Desktop (version 1.19.4, copyright 2008–2020, Mendeley Ltd.) was used to manage the citations.

The botanical identities of plants and their habitats in Africa were verified against information from https://www.worldfloraonline.org/search (formerly https://www.theplantlist.org) and https://plants.jstor.org/plants/browse.

2. Anthelmintic Resistance in Humans and Livestock

Parasite susceptibility to the existing anthelmintic drugs continues to rapidly decline, leading to the emergence of drug-resistant parasites. Several studies have reported the development and spread of resistance to all major classes of anthelmintics [34–36], especially in livestock and, to a lesser extent, in companion animals and humans [9, 37]. The main contributing factors to drug resistance include selective pressure induced by high treatment frequencies, single-drug regimens, preventive mass treatments, inadequate dosing, indiscriminate use, and overreliance on synthetic drugs to control helminthiases [18, 34, 38].

High-frequency preventive chemotherapy in humans and livestock, as a result of the high disease burden and limited number of anthelmintics, causes a reduction in worm refugia-enhancing mutations and resistance development [5, 21, 39]. Prolonged use of single drugs, for example, the use of ivermectin for Onchocerciasis control in West Africa and praziquantel against Schistosomiasis in Egypt, has been associated with widespread resistance [34].

The development and spread of drug-resistant traits at the molecular level have been well investigated in the model organism C. elegans [40] and the barber’s pole worm (H. contortus) [41]. Mutations in genes coding for drug receptor sites or the expression of genes involved in drug efflux, detoxification, or amphidial drug uptake have for instance been reported as possible causes of drug resistance [42, 43]. Resistance to the benzimidazoles in trichostrongylid nematodes in ruminants has been ascribed to mutations in the isotype 1 β-tubulin gene (E198A, E198L, F167Y, and F200Y) [44–46].

Nematodes, generally upon hatching, undergo multiple larval developmental stages into adult worms [5], and this multistage cycle poses a challenge to drugs that target just a few stages. Broad-spectrum activity against egg hatching, larval metamorphosis, and adult worms is therefore an ideal requirement for anthelmintic agents [7].

The use of plant extracts may significantly delay and reduce the spread of resistance among parasite populations [47, 48]. These multicomponent systems with natural products from very different classes could interact with multiple developmental stages, help reduce natural selection pressures, and delay resistance development, which are typically found in such multitarget systems [49–51]. Selective treatment of individuals, multidrug therapy, and environmental parasite control strategies slow down the emergence of selective resistance alleles [38].

3. Anthelmintic Drug Development from Natural Products: Prospects and Challenges

Since the beginning of the use of modern anthelmintics era in the 1950s, only a handful of such drugs are available for use in humans [52]. The rate of anthelmintic drug development by the pharmaceutical industry has nosedived over the past four decades, partly due to high costs and low returns from investments in this area [16, 53–55]. Following the successful introduction of ivermectin in 1987 against onchocerciasis in humans [56], two other agents, namely emodepside and tribendimidine, are well advanced in human clinical trials against this disease [5, 57, 58]. On the other hand, monepantel, emodepside, and derquantel have recently been approved for use in livestock [16].

Natural products, including those from plants, animals, fungi, marine organisms, and bacteria, have been acclaimed as the panacea to synthetic drug discovery challenges [54, 59]. Many studies end with the evaluation of plant extracts, fractions, and some isolated compounds for anthelmintic activities [50], with no plant-derived compound currently in use as an anthelmintic drug in humans [18]. Pyrethrum, nicotine, and rotenone are some drug products of plant origin that have been used as antiparasitic agents in veterinary practice [60].

The discovery and development of anthelmintic agents from natural sources and the isolation and characterization of bioactive constituents have therefore become the end goal of research in this less-funded area [7, 60]. Whereas several efforts have been made towards the isolation and characterization of antiparasitic compounds from plant sources in the past two decades, little is seen in other organisms such as bacteria and fungi [7]. The disadvantage of the isolation approach, however, is the unavoidable loss of so-called pharmacological synergy or toxicological antagonism associated with multicomponent extracts and fractions [7].

Issues of availability of bioactive minor compounds from the plant material in sufficient amounts, stability, formulation, delivery, compatibility, and many years of development have also kept some promising plant molecules out of the market. Because of their bulky nature, semisynthetic measures to modify the chemical structures and properties of plant molecules have proven difficult and expensive [60].

Generally, medicinal plants have not competed favourably with orthodox medicines as anthelmintics. The expensive human clinical efficacy and safety trials and bureaucratic licensing procedures, accompanied by a limited drug market, disincentivize the pharmaceutical industry from plant-based anthelmintic product development. The yield and nature of phytoconstituents are also variedly influenced by environmental factors like climate, altitude, soil type, rainfall, and herbivore predation. This erratic and unpredictable outcome affects the establishment of consistent quality control measures and hence reduces the interest of pharmaceutical investors [7].

Proprietary issues of ownership, royalties, access, government charges, and patency for plant-based drugs further deflate the hopes of drug-producing companies, which have high expectations for investment returns [60]. The presence of “pan assay interference compounds,” often referred to as “PAINS,” is militating against the advancement of preliminary bioassays on plant extracts. PAINS is an unorganised group of promiscuous molecules that occur as unspecific hits in several enzyme assays and in vitro screenings. These subversive compounds have often been considered for optimisation steps but end up consuming a lot of resources of investigators [61]. The presence of these molecules in high-throughput screens, on the other hand, should be recognised as a cautious group requiring further assessment rather than an outright rejection as irrelevant [62].

Contrary to the popular notion, not all natural compounds are innocuous [7]. Often produced as defence mechanisms or in response to external stress, some natural products from plants are potentially toxic to humans and animals and can be deleterious to physiological functions [63, 64]. An investigation by Ali et al. [65], for instance, revealed that even though the crude saponins from aerial parts of Achillea wilhelmsii and Teucrium stocksianum have significant anthelmintic activities, they were cytotoxic in the brine shrimp assay. This, therefore, implies that any anthelmintic hit from plant extracts must be verified for its safety in mammalian cells [66] and, if possible, in living organisms.

With the emergence and rapid spread of multidrug resistance to existing synthetic anthelmintics, the prospects for drug development from natural sources remain high [67]. To attract investors, herbal anthelmintics must be developed to a stage where rigorous and reproducible quality control can be assured. Standardized extracts have a huge market potential due to the current drive for organic food supplements [60]. Multicomponent plant extracts may potentiate efficacy, counter toxicity, enhance bioavailability, or improve the stability of each other in formulations [68–71].

A more interesting addition to the herbal industry is the advancement in the genetic engineering of specific metabolic pathways [72]. Genetic modification and tissue cultures can increase the yield of target molecules and improve the turnover rate [59]. This also counters the risk of plant depletion through wild harvesting and reduces the impact of an unfavourable climate on raw materials [72].

4. Brief Comparison of In Vitro and In Vivo Anthelmintic Assays

Preliminary screening of natural products for pharmacological activities requires the use of validated methods to guarantee reproducible outcomes [73]. Since helminth infections are complex and often involve mixed parasites with varied lifecycles, models for testing for antiparasitic activities also widely differ between species. These investigations are grouped into the in vitro and in vivo techniques [74].

Most primary investigations of plant materials for anthelmintic activity employ in vitro bioassays [22, 74–76], which rapidly screen large numbers of samples, are simple in design, easy to perform, cheap to implement, require minimal ethical considerations, require a small quantity of samples, and quickly churn out reproducible results [49, 75, 77, 78]. These assays target various stages of the parasite lifecycle, including egg laying or hatching, larval development, migration, motility, motor paralysis, and lethality [5, 79]. The current gold standard for assessing the susceptibility of adult and larval worms to drugs is in vitro worm motility assays using read out by microscopy [53]. Some in vitro assays use nonparasitic worm models, whereas others involve the isolation of eggs or larvae from experimentally or naturally infected animal hosts and the growth of larvae in vitro, during which periods the test substances can be applied and activity evaluated [80].

The results of basic in vitro assays of test samples (“hits”) are confirmed by the higher test models, which are specialized in vitro and in vivo studies to define possible “lead” status [78]. It is however often difficult to reproducibly extrapolate results from in vitro investigations to in vivo activity owing to pharmacokinetics issues [81]. The growth and maintenance of parasitic nematodes for long periods outside the host is often a laborious, expensive, and slow process that hinders effective in vitro studies [82]. The versatility, availability, ease of culture maintenance, and high proliferation rate make C. elegans, a free-living, nonparasitic nematode, a suitable model for many nematocidal and mechanistic studies [40, 76, 82].

In vivo assays involve the use of whole animals and are models that remain close to the patient, which is the final target for drug development [73]. Studies involve the in vivo investigation of anthelmintic potential using animals infected with the relevant parasites. The outcomes of in vivo studies are influenced by the mode of administration, nature, and dose of the test substance, host organism, and parasite species involved. Faecal worm, egg count, worm shedding, and host immune response are usually the parameters evaluated. Egg counts evaluate the effect of treatment on adult parasite fecundity, whereas parasite load depicts the effect on larvae or adult worms. The density-dependent fecundity effect, however, limits the significance of the FECR assay [49, 53] and cannot be used for Strongyloides spp., whose eggs are not passed in stool but larvae.

Although in vivo studies provide superior and reliable outcomes for pharmacological screening due to the natural, biological, pharmacological, pharmacokinetic, and toxicological environments, they are expensive, slow for large-scale investigations, labour-intensive, and often bedevilled with ethical and animal welfare issues [73, 75].

5. General Overview of Anthelmintic Evaluation of African Medicinal Plants

From this review, it is evident that African medicinal plants have great potential as sources of anthelmintic agents. An ideal anthelmintic agent should have broad spectrum activity, affecting almost all stages of the lifecycle of the nematodes and sufficient safety. Whereas some studies that considered more than one parasite stage reported such broad spectrum activities, a few others reported disparities in efficacy against various forms of the parasites [83–85].

The majority (78%) of the studies or reports reviewed employed in vitro assays in evaluating the anthelmintic activities of medicinal plants. In vitro models mainly focused on the ability of drug candidates to inhibit egg hatching, larval migration, motility, larval development or exsheathment, and survival [86–94].

The in vitro test models involve parasitic nematodes such as Haemonchus contortus, Ancylostoma caninum, Ascaris suum, Heligmosomoides bakeri, Heligmosomoides polygyrus, Trichostrongylus axei, Strongyloides papillosus, Trichuris ovis, Oesophagostomum columbianum, and Oesophagostomum venulosum [95–97]. Nonparasitic earthworms, including Pheretima posthuma, Lumbricus terrestris, Eisenia fetida, and Eudrilus eugeniae, have also been used as in vitro models for studying the anthelmintic effects of many extracts [98–103], cited in [104]. The free-living nematode, C. elegans, continues to remain the most widely used non-parasitic test model for in vitro anthelmintic studies [105–110].

H. contortus and related gastrointestinal nematodes (GIN) of small ruminants are the most widely investigated organisms in in vivo models, whereas sheep and goats are the major animals in which such clinical investigations have been reported [86, 87, 111, 112]. There are few reports involving trials in pigs, chickens, goldfish, snails, rats, and mice [113–117]. The ability of test substances to reduce faecal egg count (FEC), a typical measure of effects on fecundity, and postmortem intestinal worm burden are the parameters measured in in vivo assays. A few other studies evaluated the physiological impact of test substances on haematological indices of host animals in addition to the antiparasitic investigations [95, 111, 116, 118–120]. There was no report cited that investigated the clinical efficacy of extracts or isolated compounds in human subjects, neither was any activity testing reported on commercially available herbal anthelmintic products from these medicinal plants. There is, therefore, is a need to clinically evaluate some of these plant products and establish quality parameters for their development into standardised remedies for helminthiases.

The anthelmintic activities reported vary widely depending on the plant species, type of extract, strain of nematode, and its parasitic stage of development. A similar observation was reported in a review of anthelmintic agents used in goats [74]. Most in vivo studies, however, produced lower efficacies compared to their in vitro counterparts regarding the same plant samples [74]. The effects of pharmacokinetic processes such as absorption and metabolism and the biological variations of host animals could be accountable for these observations [75]. Also, many of the studies report activity lower than that observed for the standard anthelmintic drugs often used as positive controls [121–124]. An in vitro study of Carica papaya extracts against the Indian earthworm P. posthuma, however, was reported to show better paralytic () and wormicidal () activity than albendazole [6].

Almost 80% of the studies evaluated aqueous or hydroalcoholic extracts evaluated aqueous or hydroalcoholic extracts of various plant materials including root barks, stem barks, flowers, seeds, and whole plants, oils, and latex or exudates (Table 1). A few organic extracts, fractions, and crude powdered plant materials (mostly as feed) have also been studied [65, 84, 112, 169, 172, 197]. This trend is expected since many studies seek to replicate traditional applications of the study materials.

The pharmacological potential of medicinal plants is attributed to their specific natural product composition, which can be influenced by various factors, including changes in environmental conditions [203]. To assess the pharmacological activities of individual constituents, they must first be isolated and characterized. The elucidated chemical structures provide grounds for quality control, structural modification, syntheses, elucidation of biosynthesis pathways, and quantitative structure-activity relations (QSAR) studies [7]. In this review, several bioactive anthelmintic compounds belonging to different biosynthetical classes have been isolated from medicinal plants native to Africa. Though there have been efforts to gather these antiparasitic phytochemical libraries [7, 23, 33], there exists no such profile for African medicinal plants. The majority of the studies reporting anthelmintic activities of medicinal plants focused on extracts or fractions with limited bioactive constituents [8]. Like the extracts, most of their activities have only been evaluated at the in vitro stage, with not much clinical reporting in animals or humans.

Some specific compounds isolated from plants have been reported to exhibit anthelminthic activity (Table 2 and Figure 1). Phenolic compounds such as tannins and flavonoids constitute a large class of natural molecules with potential anthelmintic or antiparasitic activities [74, 79, 244]. Because of their bulky structure and ability to bind several macromolecules, phenolic compounds have been reported to possess a broad range of biological activities. Oligomeric and polymeric proanthocyanidins, hydrolysable tannins, and flavonoids, for example, have been more intensively studied than any other class of natural anthelmintic compounds [79, 245]. A study conducted by Engström et al. [244] isolated and studied the in vitro activity of 33 hydrolysable tannins and gallic acid against egg hatching and larval motility of H. contortus. These compounds, isolated from various plants in Finland, showed varying anthelmintic activities [244]. Other studies isolated different types of proanthocyanidins from P. pinnata root bark and C. mucronatum leaves and reported varied activities against C. elegans and some animal intestinal parasites [150, 200]. Recent reviews on polyphenolics with anthelmintic potential have been published by Spiegler et al. [79] and Mukherjee et al. [246]. Alkaloids, coumarins, triterpenes, terpenoids, lignoids, prenylated derivatives, isothiocyanates formed after fermentation from glucosinolates, and saponins have also been widely isolated and studied [74]. Several fatty acids and aromatic compounds have also been reported to possess anthelmintic activities [247, 248]. Pineda-Alegría et al. [249] recently reported that long-chain fatty acids, including β-sitosterol, palmitic, pentadecanoic, stearic, and linoleic acids have nematocidal activity.

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With the ever-increasing emergence of drug-resistant parasites and polyparasitism in animal and human helminthiases, there is a great need to explore the potential of developing some of the studied plants and their compounds into commercial drug products. The African herbal drug market should, therefore, explore the possibility of developing polyherbal formulations especially for use in livestock and companion animals, and as chemopreventive food supplements for humans.

6. Anthelmintic Activities of African Medicinal Plants

Medicinal plants belonging to different genera and families have been reported to have anthelmintic activities. However, some families have been frequently reported than others.

6.1. Fabaceae

This is the plant family with the highest reported number of plants with anthelmintic activities. Acacia nilotica (L.) Del. (Fabaceae), for instance, is a popular remedy for helminthiasis in Kenya [250]. Bachaya et al. [97] reported significant in vitro and in vivo activity of methanolic extracts of its fruits against the eggs (LC₅₀ = 512.86 μg/mL) and larvae (LC₅₀ = 194.98 μg/mL) of H. contortus and related ovine gastrointestinal nematodes. It also induced 78.5% reduction in FEC on day 13 post 3.0 g/kg treatment in sheep [97]. Similar effects were reported of its hydroalcoholic extracts against the larvae of C. elegans (wild type strain) and Onchocerca ochengi microfilariae with LC₅₀ of 350 ± 1.1 μg/mL and 10.8 ± 0.3 μg/mL, respectively [110].

The aqueous extract of the root bark of Albizia anthelmintica Brongn, a plant traditionally used as an anthelmintic [251, 252], revealed potent in vitro ovicidal (ED₅₀ of 144.2 μg/mL) and larvicidal (ED₅₀ of 65.2 μg/mL) activities against strongyle nematodes of sheep [86]. Gathuma et al. [157] also reported 89.8% in vivo efficacy of similar extracts of the plant in FECR assays against mixed GIN infections in sheep.

Other Acacia spp. have been reported to possess promissory anthelmintic activities against various test models. This included the leaves of A. polyacantha Wild [112], A. senegal, A. seyal, and A. tortilis [141]. Extracts of other fabaceous plants, such as leaves of Afrormosia laxiflora, Butea monosperma, Millettia ferruginea, Mimosa pudica, Senna occidentalis, Tephrosia spinosa, Tephrosia vogelii, and Tephrosia villosa, stem barks of Afzelia africana, Albizia schimperiana, Daniellia oliveri, and the seed kernel of Caesalpinia crista, have all been reported to exhibit a varying spectrum of anthelmintic activities [88, 89, 94, 98, 109, 118, 127, 141, 145, 158].

6.2. Combretaceae

One important species in the family Combretaceae is Anogeissus leiocarpus (DC.) Guill. and Perr. (common name: Axlewood tree). It is widely used in African traditional practices and by livestock farmers for managing various parasitic disease conditions [89, 143, 145, 178]. Aqueous extracts of A. leiocarpus leaves caused 39.5% reduction in faecal egg count and 33% reduction in faecal worm burden in sheep treated with 400 mg/kg extract [143]. It also exhibited in vitro ovicidal (ED₅₀ = 409.5 μg/mL) and larvicidal (100% excludability inhibition at 1.2 mg/mL) actions against H. contortus [89], whereas its acetone extract inhibited egg hatch (LC₅₀ = 360 μg/ml) and larval development (LC₅₀ = 509 μg/ml) [92]. Ndjonka et al. [144] reported that an ethanolic extract of A. leiocarpus bark was more active than an aqueous extract with LC₅₀ of 380 μg/ml, significantly retarding the development of larvae into adult worms [144]. Another study reported significant in vitro activity of methanol and DCM extracts of leaves, roots, and bark against larvae of Rhabditis pseudoelongata with EC₅₀ between 2.5 and 10 μg/ml [145].

Combretum mucronatum Schumach and Thonn, traditionally used for various ailments including helminthiases in Africa [149, 253], has also been reported to exhibit anthelmintic activities against various test models. Ethanolic extract of C. mucronatum leaves exhibited in vitro nematocidal effects with 10 μg/mL minimum lethal concentration against T. muris and induced 85.3% reduction of worm burden in mice [148]. Hydroalcoholic extracts also inhibited C. elegans larvae with LC₅₀ of 1.67 mg/mL. A partition of this extract revealed that the ethyl acetate portion possessed stronger anthelmintic activity than the remaining aqueous fraction. The respective activity can be related to the presence of oligomeric proanthocyanidins with different structures [150]. Subsequent ultrastructural studies showed that the tannin-rich extract caused visible effects on the cuticle without overt effects on the intestines/gut of the worms [151].

Other plants from this family with reported potential anthelmintic activities include Anogeissus schimperi, Combretum mole, Guiera senegalensis, Terminalia catappa, and Terminalia glaucescens [106, 145–147, 153].

6.3. Cucurbitaceae

Some plants belonging to this taxonomic family have also been investigated for anthelmintic effects. Ethanolic extracts of Momordica charantia leaves collected from different ecological zones in Togo exhibited varying degrees of inhibition against C. elegans larvae with LC₅₀ values between 473 and 997 μg/ml [155]. Similar extracts of its fruits also caused 100% mortality of GIN larvae at 100 mg/mL in vitro and 78% FECR on day 9 posttreatment of goats with 100 mg/kg [126]. Aqueous and ethanolic extracts of seeds of Citrullus lanatus, Cucurbita pepo, and Telfairia occidentalis all exhibited significant mortality and paralysis in vitro against the earthworm Lumbricus terrestris at 50 mg/mL [154].

6.4. Lamiaceae

Some plants belonging to the Lamiaceae have been reported to possess anthelmintic properties. These include Ocimum sanctum L., whose essential oils and eugenol inhibited C. elegans larvae with ED₅₀ of 62.1 μg/mL [108]. The aqueous extracts of roots of Leonotis ocymifolia (Burm.f.) Iwarsson and aerial parts of Leucas martinicensis (Jacq) R.Br. showed ovicidal (ED₅₀ = 0.25 μg/mL and ED₅₀ = 0.09 μg/mL, respectively), and larvicidal (100% and 99.85% inhibition, respectively, at 50 mg/mL) effects against H. contortus [158]. Whereas the fruits of O. basilicum L. were active against the earthworm E. eugeniae [159], the leaves of O. gratissimum and essential oils of Thymus bovei Benth., respectively, inhibited H. placei (LC₅₀ of 17.70 mg/mL) [160] and P. posthuma (μg/mL) [161].

6.5. Meliaceae

Azadirachta indica A. Juss. (neem) is a widely known plant in African traditional medicine and contributes immensely to the management of livestock diseases and pests [254–256]. Almost every part of this plant has been reported to have anthelmintic activity. Polar extracts of neem seeds exhibited significant ovicidal and larvicidal action in vitro against H. contortus, with the ethyl acetate fraction causing 83% wormicidal effects at 50 mg/ml 1 h postexposure [162]. Aqueous and methanolic extracts of the seeds induced 29.3% and 40.2% reduction in EPG in sheep naturally infected with H. contortus and Trichostrongyus spp. on day 15 posttreatment with 3 g/kg [163]. Neem leaves also exhibited in vitro anthelmintic effects against the earthworm Pheretima posthuma, the tapeworm Raillietina spiralis, and the roundworm Ascaridia galli [164]. In vivo studies of feed in sheep reported significant inhibition of bovine nematodes, causing 98% reduction in FEC on day 14 posttreatment [165]. The leaf extracts also inhibited microfilariae of Setaria cervi in vitro [166] and caused a significant reduction in FEC and TWC against H. polygyrus in mice [84]. Sujon et al. [126] reported a 100% in vitro mortality at 100 mg/mL against GIN with 81% reduction in EPG on day 9 posttreatment of goats [126]. Leaves, stems, and root barks extracts inhibit strongyle nematodes, causing over 90% mortality of larvae at 100 mg/mL [167].

Another medicinally relevant species from the family Meliaceae is Khaya senegalensis (Mahogany). Ethanolic extract of K. senegalensis bark induced in vitro LC₅₀ of 0.51 mg/mL and 88.82% FECR at 500 mg/kg in sheep against strongyle nematodes [168]. Similar extracts of the bark and leaves had LC₅₀ of 470 μg/mL and 1.0 mg/mL, respectively, against C. elegans larvae [144]. Methanol-dichloromethane extract of the whole plant of Lansium domesticum also inhibited adult C. elegans, significantly reducing their survival to 59% [107].

6.6. Musaceae

Musa spp. is the only genus in this family that has been reported to possess anthelmintic properties. Species such as M. x paradisiaca, M. sapientum, and M. nana inhibited the sheep tapeworm (Moniezia benedeni), roundworm (Ascaris lumbricoides), and adult earthworm (Esenia fetida), with M. x paradisiaca exhibiting the highest activity against the three worms [173]. M. x paradisiaca also caused significant FECR when fed to lambs infected with H. contortus [172] and in vitro ovicidal effects (LC₅₀ = 2.13 μg/mL) against the same parasite [181]. Other preparations of various parts of Musa spp. demonstrated ovicidal activities against T. colubriformis in sheep [169], in vitro ovicidal and larvicidal effects against H. contortus, and reduction of FEC in sheep infected with H. contortus [170, 171].

6.7. Rubiaceae

Morinda lucida and Nauclea latifolia are two plants from this family for which anthelmintic potential has been widely reported. Methanol and DCM extracts of leaves and roots of M. lucida inhibited larvae of R. pseudoelongata with EC₅₀ of 2.5 μg/mL [145], whereas hydroethanolic extracts of the stem bark induced dose-dependent paralysis (18.17 ± 0.03 min) and death (24.34 ± 0.21 min) at 50 mg/mL against P. posthuma [176]. Ethanolic extract of M. lucida leaves demonstrated concentration-dependent ovicidal action against T. colubriformis [177]. The aqueous and ethanolic extracts of N. latifolia leaves induced ovicidal activities (LC₅₀ of 0.704 and 0.650 mg/ml, respectively) against ovine GIN and reduced faecal egg count when administered to naturally parasitised sheep [95]. Onyeyili et al. [178] reported significant reduction (93.8%) in FEC when sheep, infected with nematodes were treated with 1600 mg/kg body weight of aqueous extract of N. latifolia stem bark for 5 consecutive days [178]. Ethanolic extract of Canthium mannii stem bark induced 90% inhibition of egg hatching against Ancylostoma caninum at 1 mg/mL after 48 h incubation [96].

6.8. Other Plant Species with Anthelmintic Activities

6.8.1. Carica papaya L. (Caricaceae)

Although the only plant in this family whose anthelmintic activities have been reported, Carica papaya (pawpaw) is one African medicinal plant whose anthelmintic potential has been widely investigated. Investigations on various extracts and parts of this plant have all reported some level of anthelmintic activity. Latex exudate from unripe fruits of C. papaya significantly reduced FEC (77.7%) of Ascaridia galli and Cappilaria spp. in poultry after one week of treatment [186]. After one week of posttreatment with 100 mg/mL, aqueous extracts of papaya seeds caused 100% reduction in FEC of GIN in goats [187] and sheep [188]. The seed extract also induced 100% reduction in FEC two weeks posttreatment in chicks [116] and goats [111]. In vitro studies reported that C. papaya seed extracts caused significant paralysis and death of adult P. posthuma [142] and inhibited egg hatch, larvae, and adult worms of T. colibriformis [177]. An in vitro comparative study of the leaves, stem bark, and seeds extracts of C. papaya reported that the seed extracts were the most active against adult P. posthuma [6]. Aqueous extract of papaya seeds was again reported to have more active LD₅₀ of 49.94 and 49.32 mg/ml against H. contortus egg hatch and larval development, respectively [94]. The anthelmintic activity of pawpaw can be related to the isothiocyanates, which are formed from the genuine glucosinolates.

6.8.2. Vernonia amygdalina Del. (Asteraceae)

Vernonia amygdalina (bitter leaf) is an important vegetable in West and Central African dishes [99] and widely used in the treatment of intestinal worms across Africa [253, 254]. Anthelmintic studies of aqueous and ethanolic extracts of its leaves revealed significant paralytic effects (59.94 ± 8.25 and 33.18 ± 12.41 min, respectively) against the adult earthworm L. terrestris [99]. Acetone extract of V. amygdalina leaves exhibited 42% ovicidal effect, 70% larval migration inhibition and 90% adulticidal effects at 300 μg/mL against H. contortus [141]. Alawa et al. [131] reported no significant ovicidal effects of V. amygdalina leaves extract at 11.2 mg/mL against H. contortus [131]. Another study revealed that the chloroformic extract of the stem bark was more active against P. posthuma, inducing paralysis (11.95 ± 0.28 min) and death (41.74 ± 2.21 min), than its ethanolic counterpart [142]. The anthelmintic activity might be related to the presence of sesquiterpene lactones.

6.8.3. Garcinia kola Heckel (Clusiaceae)

Commonly referred to as “bitter kola,” Garcinia kola is used to treat gastrointestinal helminthiases [190] and has been shown to possess this activity in pharmacological screenings. Hydroethanolic extract of G. kola seeds induced 76.5% irreversible paralysis of H. bakeri larvae at 50 mg/mL [91] whilst its aqueous extract exhibited 53.3% larvicidal effects against strongylid nematodes of goats at same concentration [189]. At 50 mg/mL, the stem bark extract induced dose-dependent paralysis and death of the adult P. posthuma at 39.29 ± 0.12 and 54.29 ± 0.01 min, respectively, for 50 mg/mL [176]. Both the seed and stem bark extracts were ovicidal (98.9% and 100%, respectively) at 100 mg/mL against strongylid nematodes [190].

6.8.4. Paullinia pinnata L. (Sapindaceae)

Paullinia pinnata is used in sub-Saharan Africa as an anthelmintic agent, especially for treating ancylostomiases [149, 258]. The anthelmintic properties of its root bark and leaves have been explored, revealing a huge potential as a source of nematocidal molecules, mainly oligomeric proanthocyanidins in the bark. Okpekon et al. [145] reported that extracts of both leaves and root bark of P. pinnata have in vitro inhibitory effects on R. pseudoelongata with EC₅₀ of 2.5 μg/ml each [145]. The hydroethanolic extract of the root bark also reduced the survival of C. elegans larvae to 85.2% at 1 mg/mL [149]. Further in vitro investigations of this extract against some animal parasites and C. elegans revealed that the extract had significant activity against C. elegans (LC₅₀ = 2.5 mg/mL), Toxocara cati (LC₅₀ = 112 μg/mL) and Trichuris vulpis (LC₅₀ = 17 μg/mL) [199]. Fractionation of water-acetone extracts leads to an ethyl acetate partition with better anthelmintic activity (LC₅₀ = 1.1 mg/mL) than the water fraction (LC₅₀ = 2.9 mg/mL) and the crude extract (LC₅₀ = 1.9 mg/mL) [200]. Bioassay-guided studies led to the isolation of Cinnamtannin B1, a trimeric A-type procyanidin, which had significant inhibition of C. elegans (86.5% at 72 h incubation). The respective B-type trimer, procyanidin C1, isolated from C. mucronatum, was less active (47.3%), indicating a strong influence of the interflavan linkage and the different fine structures of the procyanidins [150, 200].

7. Conclusion

The World Health Organization’s 2030 targets for STH can only be achieved with renewed investments in new and effective drugs. African medicinal plants will serve as a useful source of remedies for integrated parasite control, along with other measures such as education and the provision of sanitation facilities to at-risk populations.

The foregoing data validate the claims that African medicinal plants have huge potential for the discovery and development of new, innovative, and alternative anthelmintic agents. The majority of reports and studies evaluated extracts of plants, with a few isolated compounds also characterized. Even though in vivo animal studies abound, 78% of the studies reported in vitro activities against parasitic nematodes. There are no reports available on clinical investigations of extracts or purified compounds in humans, nor have any commercial products been reported or evaluated for their effectiveness. Therefore, clinical evaluation of these plant products and mechanistic studies, especially on isolated compounds, will advance the goal of identifying and developing drug candidates from plant sources. [256].

Abbreviations

DCM:	Dichloromethane
EC₅₀:	Half maximal effective concentration
ED₅₀:	Half maximal effective dose
EHIA:	Egg hatch inhibition assay
EPG:	Egg per gram
FEC:	Faecal egg count
FECR:	Faecal egg count reduction
GIN:	Gastrointestinal nematodes
IC₅₀:	Half maximal inhibitory concentration
LC₅₀:	Half maximal lethal concentration
LD₅₀:	Half maximal lethal dose
LMIA:	Larval migration inhibition assay
MDA:	Mass drug administration
QSAR:	Quantitative structure-activity relations studies
STH:	Soil-transmitted helminthiases
WHO:	World Health Organization.

Data Availability

No data were used to support this study.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

This work was part of a project funded by the German Research Foundation (Deutsche Forschungsgemeinschaft DFG) under grant number LI 793/16-1, Projekt nummer 423277515.

References

B. Bharti, S. Bharti, and S. Khurana, “Worm infestation: diagnosis, treatment and prevention,” Indian Journal of Pediatrics, vol. 85, no. 11, pp. 1017–1024, 2018.
View at: Publisher Site | Google Scholar
Who, in Ending the Neglect to Attain the Sustainable Development Goals: A Road Map for Neglected Tropical Diseases 2021–2030, World Health Organization, Geneva, Geneva, Switzerland, 2020.
WHO, Neglected Tropical Diseases − Summary, World Health Organization, Geneva, Geneva, Switzerland, 2020.
S. Lustigman, R. K. Prichard, A. Gazzinelli et al., “A research agenda for helminth diseases of humans: the problem of helminthiases,” PLoS Neglected Tropical Diseases, vol. 6, no. 4, Article ID e1582, 2012.
View at: Publisher Site | Google Scholar
M. Liu, S. K. Panda, and W. Luyten, “Plant-based natural products for the discovery and development of novel anthelmintics against nematodes,” Biomolecules, vol. 10, no. 3, p. 426, 2020.
View at: Publisher Site | Google Scholar
P. E. Goku, E. Orman, A. N. K. Quartey, G. T. Ansong, and E. B. Asare-Gyan, “Comparative evaluation of the in vitro anthelminthic effects of the leaves, stem, and seeds of carica papaya (linn) using the Pheretima posthuma model,” Evidence-based Complementary and Alternative Medicine, vol. 2020, Article ID 9717304, 8 pages, 2020.
View at: Publisher Site | Google Scholar
J. F. Garcia-Bustos, B. E. Sleebs, and R. B. Gasser, “An appraisal of natural products active against parasitic nematodes of animals,” Parasites & Vectors, vol. 12, no. 1, pp. 306–322, 2019.
View at: Publisher Site | Google Scholar
J. C. Romero-Benavides, A. L. Ruano, R. Silva-Rivas, P. Castillo-Veintimilla, S. Vivanco-Jaramillo, and N. Bailon-Moscoso, “Medicinal plants used as anthelmintics: ethnomedical, pharmacological, and phytochemical studies,” European Journal of Medicinal Chemistry, vol. 129, pp. 209–217, 2017.
View at: Publisher Site | Google Scholar
J. Vercruysse, M. Albonico, J. M. Behnke et al., “Is anthelmintic resistance a concern for the control of human soil-transmitted helminths?” International Journal for Parasitology: Drugs and Drug Resistance, vol. 1, no. 1, pp. 14–27, 2011.
View at: Publisher Site | Google Scholar
Who, Integrating Neglected Tropical Diseases into Global Health and Development: Fourth WHO Report on Neglected Tropical Diseases, World Health Organization, Geneva, Switzerland, 2017.
M. B. Manke, S. C. Dhawale, and P. G. Jamkhande, “Helminthiasis and medicinal plants: a review,” Asian Pacific Journal of Tropical Disease, vol. 5, no. 3, pp. 175–180, 2015.
View at: Publisher Site | Google Scholar
L. J. Stuyver and B. Levecke, “The role of diagnostic technologies to measure progress toward who 2030 targets for soil-transmitted helminth control programs,” PLoS Neglected Tropical Diseases, vol. 15, no. 6, Article ID e0009422, 2021.
View at: Publisher Site | Google Scholar
P. J. Hotez, P. J. Brindley, J. M. Bethony, C. H. King, E. J. Pearce, and J. Jacobson, “Helminth infections: the great neglected tropical diseases,” The Journal of Clinical Investigation, vol. 118, pp. 1311–1321, 2008.
View at: Publisher Site | Google Scholar
WHO, WHO Factsheet: Soil-Transmitted Helminthiases, World Health Organization, Geneva, Switzerland, 2020.
D. Ndjonka, E. D. Abladam, B. Djafsia, I. Ajonina-Ekoti, M. D. Achukwi, and E. Liebau, “Anthelmintic activity of phenolic acids from the axlewood tree Anogeissus leiocarpus on the filarial nematode Onchocerca ochengi and drug-resistant strains of the free-living nematode Caenorhabditis elegans,” Journal of Helminthology, vol. 88, no. 4, pp. 481–488, 2013.
View at: Publisher Site | Google Scholar
S. Preston, P. K. Korhonen, L. Mouchiroud et al., “Deguelin exerts potent nematocidal activity via the mitochondrial respiratory chain,” The FASEB Journal, vol. 31, no. 10, pp. 4515–4532, 2017.
View at: Publisher Site | Google Scholar
D. E. Reyes-Guerrero, A. Olmedo-Juárez, and P. Mendoza-De Gives, “Control y prevención de nematodosis en pequeños rumiantes: antecedentes, retos y perspectivas en México,” Revista Mexicana De Ciencias Pecuarias, vol. 12, pp. 186–204, 2021.
View at: Publisher Site | Google Scholar
B. Joshi, S. K. Panda, R. S. Jouneghani et al., “Antibacterial, antifungal, antiviral, and anthelmintic activities of medicinal plants of Nepal selected based on ethnobotanical evidence,” Evidence-based Complementary and Alternative Medicine, vol. 2020, Article ID 1043471, 14 pages, 2020.
View at: Publisher Site | Google Scholar
D. Humphries, S. Nguyen, D. Boakye, M. Wilson, and M. Cappello, “The promise and pitfalls of mass drug administration to control intestinal helminth infections,” Current Opinion in Infectious Diseases, vol. 25, no. 5, pp. 584–589, 2012.
View at: Publisher Site | Google Scholar
A. Olsen, L. V. Lieshout, H. Marti et al., “Strongyloidiasis — the most neglected of the neglected tropical diseases ?” Transactions of the Royal Society of Tropical Medicine & Hygiene, vol. 103, 2009.
View at: Publisher Site | Google Scholar
T. G. Geary, “Are new anthelmintics needed to eliminate human helminthiases?” Current Opinion in Infectious Diseases, vol. 25, no. 6, pp. 709–717, 2012.
View at: Publisher Site | Google Scholar
R. G. Mali and A. A. Mehta, “A review on anthelmintic plants,” Indian Journal of Natural Products and Resources, vol. 7, no. 5, pp. 466–475, 2008.
View at: Google Scholar
K. A. Tariq and M. A. Tantry, “Preliminary studies on plants with anthelmintic properties in kashmir the north-west temperate himalayan region of India,” Chinese Medicine, vol. 3, no. 2, pp. 106–112, 2012.
View at: Publisher Site | Google Scholar
A. R. Williams, J. Soelberg, and A. K. Jäger, “Anthelmintic properties of traditional African and Caribbean medicinal plants: identification of extracts with potent activity against Ascaris suum in vitro,” Parasite, vol. 23, p. 24, 2016.
View at: Publisher Site | Google Scholar
C. Agyare, A. Asase, M. Lechtenberg, M. Niehues, A. Deters, and A. Hensel, “An ethnopharmacological survey and in vitro confirmation of ethnopharmacological use of medicinal plants used for wound healing in Bosomtwi-Atwima-Kwanwoma area, Ghana,” Journal of Ethnopharmacology, vol. 125, no. 3, pp. 393–403, 2009.
View at: Publisher Site | Google Scholar
M. M. Tabi, M. Powell, and D. Hodnicki, “Use of traditional healers and modern medicine in Ghana,” International Nursing Review, vol. 53, no. 1, pp. 52–58, 2006.
View at: Publisher Site | Google Scholar
Who, WHO Global Report on Traditional and Complementary Medicine 2019, World Health Organization, Geneva, Switzerland, 2019.
V. D. Rajeswari, “Anthelmintic activity of plants: a review,” Research Journal of Phytochemistry, vol. 8, no. 3, pp. 57–63, 2014.
View at: Publisher Site | Google Scholar
D. S. Fabricant and N. R. Farnsworth, “The value of plants used in traditional medicine for drug discovery,” Environmental Health Perspectives, vol. 109, no. 1, pp. 69–75, 2001.
View at: Publisher Site | Google Scholar
C. Waterman, R. A. Smith, L. Pontiggia, and A. Dermarderosian, “Anthelmintic screening of Sub-Saharan African plants used in traditional medicine,” Journal of Ethnopharmacology, vol. 127, no. 3, pp. 755–759, 2010.
View at: Publisher Site | Google Scholar
D. J. Newman and G. M. Cragg, “Natural products as sources of new drugs over the nearly four decades from 01/1981 to 09/2019,” Journal of Natural Products, vol. 83, no. 3, pp. 770–803, 2020.
View at: Publisher Site | Google Scholar
P. J. Waller, R. L. Baker, J. B. Githiori, and J. Ho, “Evaluation of anthelmintic properties of some plants used as livestock dewormers against Haemonchus contortus infections in sheep,” Parasitology, vol. 129, 2004.
View at: Publisher Site | Google Scholar
M. Liu, P. Kipanga, A. H. Mai et al., “Bioassay-guided isolation of three anthelmintic compounds from Warburgia ugandensis Sprague subspecies ugandensis, and the mechanism of action of polygodial,” International Journal for Parasitology, vol. 48, no. 11, pp. 833–844, 2018.
View at: Publisher Site | Google Scholar
S. Geerts and B. Gryseels, “Anthelmintic resistance in human helminths: a review,” Tropical Medicine and International Health, vol. 6, no. 11, pp. 915–921, 2001.
View at: Publisher Site | Google Scholar
A. S. Peregrine, M. B. Molento, R. M. Kaplan, and M. K. Nielsen, “Anthelmintic resistance in important parasites of horses: does it really matter?” Veterinary Parasitology, vol. 201, no. 1–2, pp. 1–8, 2014.
View at: Publisher Site | Google Scholar
D. Traversa, G. V. Samson-himmelstjerna, J. Demeler et al., “Parasites & Vectors Anthelmintic resistance in cyathostomin populations from horse yards in Italy, United Kingdom and Germany,” Parasites & Vectors, vol. 7, pp. 1–7, 2009.
View at: Publisher Site | Google Scholar
P. D. Jimenez Castro, S. B. Howell, J. J. Schaefer, R. W. Avramenko, J. S. Gilleard, and R. M. Kaplan, “Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat?” Parasites & Vectors, vol. 12, no. 1, pp. 576–615, 2019.
View at: Publisher Site | Google Scholar
A. Raza, A. G. Qamar, K. Hayat, S. Ashraf, and A. R. Williams, “Anthelmintic resistance and novel control options in equine gastrointestinal nematodes,” Parasitology, vol. 146, no. 4, pp. 425–437, 2019.
View at: Publisher Site | Google Scholar
J. A. Van Wyk, “Refugia - overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance,” Onderstepoort Journal of Veterinary Research, vol. 68, no. 1, pp. 55–67, 2001.
View at: Google Scholar
T. G. Geary and D. P. Thompson, “Caenorhabditis elegans: how good a model for veterinary parasites?” Veterinary Parasitology, vol. 101, no. 3-4, pp. 371–386, 2001.
View at: Publisher Site | Google Scholar
J. S. Gilleard, “Haemonchus contortus as a paradigm and model to study anthelmintic drug resistance,” Parasitology, vol. 140, no. 12, pp. 1506–1522, 2013.
View at: Publisher Site | Google Scholar
A. C. Kotze, P. W. Hunt, P. Skuce et al., “Recent advances in candidate-gene and whole-genome approaches to the discovery of anthelmintic resistance markers and the description of drug/receptor interactions,” International Journal for Parasitology: Drugs and Drug Resistance, vol. 4, no. 3, pp. 164–184, 2014.
View at: Publisher Site | Google Scholar
L. R. Stuchlíková, P. Matoušková, I. Vokřál et al., “Metabolism of albendazole, ricobendazole and flubendazole in Haemonchus contortus adults: sex differences, resistance-related differences and the identification of new metabolites,” International Journal for Parasitology: Drugs and Drug Resistance, vol. 8, no. 1, pp. 50–58, 2018.
View at: Publisher Site | Google Scholar
M. S. G. Kwa, F. N. J. Kooyman, J. H. Boersema, and M. H. Roos, “Effect of selection for benzimidazole resistance in Haemonchus contortus on β-tubulin isotype 1 and isotype 2 genes,” Biochemical and Biophysical Research Communications, vol. 191, no. 2, pp. 413–419, 1993.
View at: Publisher Site | Google Scholar
M. S. G. Kwa, J. G. Veenstra, and M. H. Roos, “Benzimidazole resistance in Haemonchus contortus is correlated with a conserved mutation at amino acid 200 in β-tubulin isotype 1,” Molecular and Biochemical Parasitology, vol. 63, no. 2, pp. 299–303, 1994.
View at: Publisher Site | Google Scholar
M. S. G. G. Kwa, J. G. Veenstra, M. Van Dijk, M. H. Roos, and M. H. Roos, “β-Tubulin genes from the parasitic nematode Haemonchus contortus modulate drug resistance in Caenorhabditis elegans,” Journal of Molecular Biology, vol. 246, no. 4, pp. 500–510, 1995.
View at: Publisher Site | Google Scholar
A. R. Williams, C. Fryganas, A. Ramsay, I. Mueller-Harvey, and S. M. Thamsborg, “Direct anthelmintic effects of condensed tannins from diverse plant sources against Ascaris suum,” PLoS One, vol. 9, no. 5, Article ID e97053, 2014.
View at: Publisher Site | Google Scholar
G. Zirintunda, S. Biryomumaisho, K. I. Kasozi et al., “Emerging anthelmintic resistance in poultry: can ethnopharmacological approaches offer a solution?” Frontiers in Pharmacology, vol. 12, Article ID 774896, 2021.
View at: Publisher Site | Google Scholar
J. B. Githiori, S. Athanasiadou, and S. M. Thamsborg, “Use of plants in novel approaches for control of gastrointestinal helminths in livestock with emphasis on small ruminants,” Veterinary Parasitology, vol. 139, no. 4, pp. 308–320, 2006.
View at: Publisher Site | Google Scholar
S. H. Tinkler, “Preventive chemotherapy and anthelmintic resistance of soil-transmitted helminths – can we learn nothing from veterinary medicine?” One Health, vol. 9, Article ID 100106, 2020.
View at: Publisher Site | Google Scholar
S. F. Vuuren, “A review of the traditional use of southern African medicinal plants for the treatment of selected parasite infections affecting humans,” Journal of Ethnopharmacology, vol. 220, pp. 250–264, 2018.
View at: Publisher Site | Google Scholar
S. O. Enejoh and M. M. Suleiman, “Anthelmintics and their application in veterinary medicine,” Research in Medical & Engineering Sciences, vol. 2, no. 3, pp. 117–126, 2017.
View at: Publisher Site | Google Scholar
M. J. Smout, A. C. Kotze, J. S. Mccarthy, and A. Loukas, “A novel high throughput assay for anthelmintic drug screening and resistance diagnosis by real-time monitoring of parasite motility,” PLoS Neglected Tropical Diseases, vol. 4, no. 11, p. e885, 2010.
View at: Publisher Site | Google Scholar
M. Wink, “Medicinal plants: a source of anti-parasitic secondary metabolites,” Molecules, vol. 17, no. 11, Article ID 12771, 2012.
View at: Publisher Site | Google Scholar
A. Hilou, F. Rappez, and P. Duez, “Ethnoveterinary management of cattle helminthiasis among the Fulani and the Mossi (Central Burkina Faso): plants used and modes of use,” International Journal of Brain and Cognitive Sciences, vol. 8, no. 5, p. 2207, 2015.
View at: Publisher Site | Google Scholar
W. C Campbell, “History of avermectin and ivermectin, with notes on the history of other macrocyclic lactone antiparasitic agents,” Current Pharmaceutical Biotechnology, vol. 13, no. 6, pp. 853–865, 2012.
View at: Publisher Site | Google Scholar
Y. Hu, S. H. Xiao, and R. V. Aroian, “The new anthelmintic tribendimidine is an L-type (Levamisole and Pyrantel) nicotinic acetylcholine receptor agonist,” PLoS Neglected Tropical Diseases, vol. 3, no. 8, pp. 4999–e510, 2009.
View at: Publisher Site | Google Scholar
I. J. Onakpoya, “Antihelminthic drugs,” in Side Effects of Drugs Annual, Elsevier B.V, Amsterdam, The Netherlands, 2019.
View at: Publisher Site | Google Scholar
A. L. Harvey, R. Edrada-Ebel, and R. J. Quinn, “The re-emergence of natural products for drug discovery in the genomics era,” Nature Reviews Drug Discovery, vol. 14, no. 2, pp. 111–129, 2015.
View at: Publisher Site | Google Scholar
J. M. Behnke, D. J. Buttle, G. Stepek, A. Lowe, and I. R. Duce, “Developing novel anthelmintics from plant cysteine proteinases,” Parasites & Vectors, vol. 1, pp. 29–18, 2008.
View at: Publisher Site | Google Scholar
J. B. Baell, “Feeling nature’s PAINS: natural products, natural product drugs, and Pan assay interference compounds (PAINS),” Journal of Natural Products, vol. 79, no. 3, pp. 616–628, 2016.
View at: Publisher Site | Google Scholar
J. B. Baell and J. W. M. Nissink, “Seven year itch: pan-assay interference compounds (PAINS) in 2017 - utility and limitations,” ACS Chemical Biology, vol. 13, no. 1, pp. 36–44, 2018.
View at: Publisher Site | Google Scholar
M. Boukandou Mounanga, L. Mewono, and S. Aboughe Angone, “Toxicity studies of medicinal plants used in sub-Saharan Africa,” Journal of Ethnopharmacology, vol. 174, pp. 618–627, 2015.
View at: Publisher Site | Google Scholar
M. Levine, A. M. Ruha, K. Graeme, D. E. Brooks, J. Canning, and S. C. Curry, “Toxicology in the ICU - Part 3: natural toxins,” Chest, vol. 140, no. 5, pp. 1357–1370, 2011.
View at: Publisher Site | Google Scholar
N. Ali, S. W. A. Shah, I. Shah, G. Ahmed, M. Ghias, and I. Khan, “Cytotoxic and anthelmintic potential of crude saponins isolated from Achillea Wilhelmsii C. Koch and Teucrium Stocksianum boiss,” BMC Complementary and Alternative Medicine, vol. 11, no. 1, p. 106, 2011.
View at: Publisher Site | Google Scholar
A. Okem, J. F. Finnie, and J. Van Staden, “Pharmacological, genotoxic and phytochemical properties of selected South African medicinal plants used in treating stomach-related ailments,” Journal of Ethnopharmacology, vol. 139, no. 3, pp. 712–720, 2012.
View at: Publisher Site | Google Scholar
D. J. Newman and G. M. Cragg, “Natural products as sources of new drugs from 1981 to 2014,” Journal of Natural Products, vol. 79, no. 3, pp. 629–661, 2016.
View at: Publisher Site | Google Scholar
J. Kalmobé, D. Ndjonka, D. Boursou, J. D. Vildina, and E. Liebau, “Phytochemical analysis and in vitro anthelmintic activity of Lophira lanceolata (Ochnaceae) on the bovine parasite Onchocerca ochengi and on drug resistant strains of the free-living nematode Caenorhabditis elegans,” BMC Complementary and Alternative Medicine, vol. 17, no. 1, p. 404, 2017.
View at: Publisher Site | Google Scholar
A. O. Aremu, O. A. Fawole, J. C. Chukwujekwu, M. E. Light, J. F. Finnie, and J. Van Staden, “In vitro antimicrobial, anthelmintic and cyclooxygenase-inhibitory activities and phytochemical analysis of Leucosidea sericea,” Journal of Ethnopharmacology, vol. 131, no. 1, pp. 22–27, 2010.
View at: Publisher Site | Google Scholar
M. Karonen, J. R. Ahern, L. Legroux et al., “Ellagitannins inhibit the exsheathment of Haemonchus contortus and Trichostrongylus colubriformis larvae: the efficiency increases together with the molecular size,” Journal of Agricultural and Food Chemistry, vol. 68, no. 14, pp. 4176–4186, 2020.
View at: Publisher Site | Google Scholar
S. Karole, S. Shrivastava, S. Thomas et al., “Polyherbal formulation concept for synergic action: a review,” Journal of Drug Delivery and Therapeutics, vol. 9, no. 1-s, pp. 453–466, 2019.
View at: Publisher Site | Google Scholar
S. Gomez-Galera, A. M. Pelacho, A. Gene, T. Capell, and P. Christou, “The genetic manipulation of medicinal and aromatic plants,” Plant Cell Reports, vol. 26, no. 10, pp. 1689–1715, 2007.
View at: Publisher Site | Google Scholar
P. Cos, A. J. Vlietinck, D. V. Berghe, and L. Maes, “Anti-infective potential of natural products: how to develop a stronger in vitro “proof-of-concept,” Journal of Ethnopharmacology, vol. 106, no. 3, pp. 290–302, 2006.
View at: Publisher Site | Google Scholar
F. Oliveira Santos, A. Ponce Morais Cerqueira, A. Branco, M. José Moreira Batatinha, and M. Borges Botura, “Anthelmintic activity of plants against gastrointestinal nematodes of goats: a review,” Parasitology, vol. 146, no. 10, pp. 1233–1246, 2019.
View at: Publisher Site | Google Scholar
A. O. Aremu, J. F. Finnie, and J. Van Staden, “Potential of South African medicinal plants used as anthelmintics – their ef fi cacy, safety concerns and reappraisal of current screening methods,” South African Journal of Botany, vol. 82, pp. 134–150, 2012.
View at: Publisher Site | Google Scholar
K. G. Simpkin and G. C. Coles, “The use of Caenorhabditis elegans for anthelmintic screening,” Journal of Chemical Technology and Biotechnology, vol. 31, no. 1, pp. 66–69, 2007.
View at: Publisher Site | Google Scholar
F. Nouri, S. R. Nourollahi-Fard, H. R. Foroodi, and H. Sharifi, “In vitro anthelmintic effect of Tobacco (Nicotiana tabacum) extract on parasitic nematode, Marshallagia marshalli,” Journal of Parasitic Diseases, vol. 40, no. 3, pp. 643–647, 2014.
View at: Publisher Site | Google Scholar
A. S. Verkman, “Drug discovery in academia,” American Journal of Physiology - Cell Physiology, vol. 286, no. 3, pp. C465–C474, 2004.
View at: Publisher Site | Google Scholar
V. Spiegler, E. Liebau, and A. Hensel, “Medicinal plant extracts and plant-derived polyphenols with anthelmintic activity against intestinal nematodes,” Natural Product Reports, vol. 34, no. 6, pp. 627–643, 2017.
View at: Publisher Site | Google Scholar
B. Yadav, K. Wennerberg, T. Aittokallio, and J. Tang, “Searching for drug synergy in complex dose-response landscapes using an interaction potency model,” Computational and Structural Biotechnology Journal, vol. 13, pp. 504–513, 2015.
View at: Publisher Site | Google Scholar
T. Eguale and M. Giday, “In vitro anthelmintic activity of three medicinal plants against Haemonchus contortus,” International Journal of Green Pharmacy, vol. 3, no. 1, pp. 29–34, 2009.
View at: Publisher Site | Google Scholar
L. M. Katiki, J. F. S. Ferreira, A. M. Zajac et al., “Caenorhabditis elegans as a model to screen plant extracts and compounds as natural anthelmintics for veterinary use,” Veterinary Parasitology, vol. 182, no. 2–4, pp. 264–268, 2011.
View at: Publisher Site | Google Scholar
M. Adamu, V. Naidoo, and J. N. Eloff, “Efficacy and toxicity of thirteen plant leaf acetone extracts used in ethnoveterinary medicine in South Africa on egg hatching and larval development of Haemonchus contortus,” BMC Veterinary Research, vol. 9, no. 1, p. 38, 2013.
View at: Publisher Site | Google Scholar
J. B. Githiori, J. Höglund, P. J. Waller, and R. Leyden Baker, “Evaluation of anthelmintic properties of extracts from some plants used as livestock dewormers by pastoralist and smallholder farmers in Kenya against Heligmosomoides polygyrus infections in mice,” Veterinary Parasitology, vol. 118, no. 3–4, pp. 215–226, 2003.
View at: Publisher Site | Google Scholar
R. Kumarasingha, A. V. Karpe, S. Preston et al., “Metabolic profiling and in vitro assessment of anthelmintic fractions of Picria fel-terrae Lour,” International Journal for Parasitology: Drugs and Drug Resistance, vol. 6, no. 3, pp. 171–178, 2016.
View at: Publisher Site | Google Scholar
G. N. Thoithi, N. Maingi, D. Karume, P. K. Gathumbi, J. W. Mwangi, and I. O. Kobwage, “Anthelminitic and other Pharmacological activities of the root bark extracts of Albizia anthelmintica Brongn,” East and Central African Journal of Pharmaceutical Sciences, vol. 5, pp. 60–66, 2002.
View at: Publisher Site | Google Scholar
C. O. Nwosu, E. Onu, and E. Alalade, “Anthelmintic efficacy of aqueous extract of seeds of some plants used traditionally as spices in Nigeria,” Global Journal of Medical Sciences, vol. 6, no. 2, pp. 81–84, 2008.
View at: Publisher Site | Google Scholar
K. Simon and O. Jegede, “Anthelmintic properties of Afzelia africana&lt sw: an in-vitro egg hatch assay,” Animal Production Research Advances, vol. 4, no. 3–4, 2010.
View at: Publisher Site | Google Scholar
K. Adama, B. A. M. Gaston, H. ., T. Hamidou, T. Amadou, and S. Laya, “In vitro anthelmintic effect of two medicinal plants (Anogeissus leiocarpus and Daniellia oliveri) on Haemonchus contortus, an abosomal nematode of sheep in Burkina Faso,” African Journal of Biotechnology, vol. 8, no. 18, pp. 4690–4695, 2009.
View at: Publisher Site | Google Scholar
M. Adamu, O. D. Oshadu, and C. I. Ogbaje, “Anthelminthic efficacy of aqueous extract of Acanthus montanus leaf against strongylid nematodes of small ruminants,” African Journal of Traditional, Complementary and Alternative Medicines: AJTCAM, vol. 7, no. 4, pp. 279–285, 2010.
View at: Publisher Site | Google Scholar
I. W. Onyenwe, L. A. Ngongeh, C. C. Udekwu, and G. O. Ezeugwu, “Preliminary studies on the anthelmintic effects of ethanolic extract of Garcinia kola (Heckel) seed and methanolic extract of sacoglottis gabonensis (baillon) stem bark on Heligmosomoides bakeri larvae in nsukka, Nigeria,” Global Journal of Pure and Applied Sciences, vol. 16, no. 1, pp. 161–164, 2010.
View at: Publisher Site | Google Scholar
I. O. Ademola and J. N. Eloff, “In vitro anthelmintic effect of Anogeissus leiocarpus (DC.) Guill. & Perr. leaf extracts and fractions on developmental stages of Haemonchus contortus,” African Journal of Traditional, Complementary and Alternative Medicines: AJTCAM, vol. 8, no. 2, pp. 134–139, 2011.
View at: Publisher Site | Google Scholar
S. M. Muema, K. O. Abuga, A. Yenesew, and G. N. Thoithi, “Phytochemical and anthelmintic study of the root bark of teclea trichocarpa, engl. (Rutaceae),” East and Central African Journal of Pharmaceutical Sciences, vol. 17, pp. 44–47, 2014.
View at: Google Scholar
C. Odhong, R. G. Wahome, M. Vaarst et al., “In vitro anthelmintic effects of crude aqueous extracts of Tephrosia vogelii, Tephrosia villosa and Carica papaya leaves and seeds,” African Journal of Biotechnology, vol. 13, no. 52, pp. 4667–4672, 2014.
View at: Publisher Site | Google Scholar
I. O. Ademola, B. O. Fagbemi, and S. O. Idowu, “Anthelmintic efficacy of Nauclea latifolia&lt extract against gastrointestinal nematodes of sheep:in vitro&lt and in vivo&lt studies,” African Journal of Traditional, Complementary and Alternative Medicines, vol. 4, no. 2, pp. 148–156, 2008.
View at: Publisher Site | Google Scholar
J. Pone, B. C. F. Bilong, M. Mpoame, C. F. Ngwa, and G. C. Coles, “In vitro activity of ethanol, cold water and hot water extracxts of the bark of Canthium mannii (Rubiaceae) stem on agasints Ancylostoma caninum eggs,” East and Central African Journal of Pharmaceutical Sciences, vol. 9, pp. 14–18, 2006.
View at: Google Scholar
H. A. Bachaya, Z. Iqbal, M. N. Khan, Z. ud D. Sindhu, and A. Jabbar, “Anthelmintic activity of Ziziphus nummularia (bark) and Acacia nilotica (fruit) against Trichostrongylid nematodes of sheep,” Journal of Ethnopharmacology, vol. 123, no. 2, pp. 325–329, 2009.
View at: Publisher Site | Google Scholar
K. Ilango, R. A. Xavier, and T. Subburaju, “Original research article open access anthelmintic activity of extracts of aerial parts of Tephrosia spinosa (L.f.) pres,” International Journal of Health Research, vol. 4, pp. 53–56, 2011.
View at: Publisher Site | Google Scholar
C. A. Danquah, G. A. Koffuor, K. Annan, and E. C. Ketor, “The anthelmintic activity of Vernonia amygdalina and Alstonia boonei De Wild,” Journal of Medicine and Biomedical Sciences, vol. 1, no. 1, pp. 21–27, 2012.
View at: Google Scholar
F. Adu, C. Agyare, G. H. Sam, Y. Duah Boakye, and V. E. Boamah, “Anthelmintic resistance modifying properties of extracts of Cyperus difformis L. (Cyperiaceae),” Investigational Medicinal Chemistry and Pharmacology, vol. 1, no. 1, p. 3, 2018.
View at: Google Scholar
E. Asante-Kwatia, A. Y. Mensah, and A. D. Forkuo, “The Ghanaian flora as a potential source of anthelmintic and anti-schistosomal agents,” in Natural Medicinal Plants Among, IntechOpen, London, UK, 2021.
View at: Publisher Site | Google Scholar
G. W. Thorn, R. D. Adams, K. Braunwald, K. J. Isselbacher, and R. G. Petersdorf, “Harrison’s. Principles of Internal Medicine. In McGraw Hill Co,” 1997.
View at: Google Scholar
Z. Vigar, “Atlas of Medicinal Parasitology,” In P. G. Publication House, 1984.
View at: Google Scholar
S. M. Chittoor, A. J. R. Binny, S. K. Yadlapalli, A. Cheruku, C. Dandu, and Y. Nimmanapalli, “Anthelmintic and antimicrobial studies of Drimia indica (Roxb.) Jessop. bulb aqueous extracts,” Journal of Pharmacy Research, vol. 5, no. 5, pp. 3677–3686, 2012.
View at: Google Scholar
E. W. Karumi, C. K. Maitai1, F. A. Okalebo et al., “Anthelmintic and antibacterial activity of hagenia abyssinica (bruce) J.F. Gmel (rosaceae),” East and Central African Journal of Pharmaceutical Sciences, vol. 16, pp. 75–80, 2013.
View at: Publisher Site | Google Scholar
A. H. Gagman, H. Ahmad, N. Ahmad, I. Izzaudin, and N. Him, “The efficacy of Vitex doniana and Boswellia dalzielii against egg hatch of Caenorhabditis elegans,” Bayero Journal of Pure and Applied Sciences, vol. 12, no. 1, pp. 737–742, 2019.
View at: Publisher Site | Google Scholar
R. Kumarasingha, E. A. Palombo, M. Bhave et al., “Enhancing a search for traditional medicinal plants with anthelmintic action by using wild type and stress reporter Caenorhabditis elegans strains as screening tools,” International Journal for Parasitology, vol. 44, no. 5, pp. 291–298, 2014.
View at: Publisher Site | Google Scholar
M. K. Asha, D. Prashanth, B. Murali, R. Padmaja, and A. Amit, “Anthelmintic activity of essential oil of Ocimum sanctum and eugenol,” Fitoterapia, vol. 72, no. 6, pp. 669-670, 2001.
View at: Publisher Site | Google Scholar
D. Prashanth, M. K. Asha, A. Amit, and R. Padmaja, “Anthelmintic activity of Butea monosperma,” Fitoterapia, vol. 72, no. 4, pp. 421-422, 2001.
View at: Publisher Site | Google Scholar
J. Dikti Vildina, J. Kalmobe, B. Djafsia, T. J. Schmidt, E. Liebau, and D. Ndjonka, “Anti-Onchocerca and anti-Caenorhabditis activity of a hydro-alcoholic extract from the fruits of Acacia nilotica and some proanthocyanidin derivatives,” Molecules, vol. 22, no. 5, pp. 748–819, 2017.
View at: Publisher Site | Google Scholar
S. A. Ameen, O. M. Azeez, Y. A. Baba et al., “Anthelmintic potency of carica papaya seeds against gastro-intestinal helminths in red sokoto goat,” Ceylon Journal of Science, vol. 47, no. 2, p. 137, 2018.
View at: Publisher Site | Google Scholar
R. A. Max, A. E. Kimambo, A. A. A. Kassuku, L. A. La Mtenga, and P. J. Buttery, “Effect of tanniniferous browse meal on nematode faecal egg counts and internal parasite burdens in sheep and goats,” South African Journal of Animal Science, vol. 37, no. 2, pp. 97–106, 2007.
View at: Publisher Site | Google Scholar
Y. Wang, Z. F. Wu, G. X. Wang et al., “In vivo anthelmintic activity of bruceine A and bruceine D from Brucea javanica against Dactylogyrus intermedius (Monogenea) in goldfish (Carassius auratus),” Veterinary Parasitology, vol. 177, no. 1–2, pp. 127–133, 2011.
View at: Publisher Site | Google Scholar
S. Hosseinzadeh, M. J. Ghalesefidi, M. Azami, M. A. Mohaghegh, S. H. Hejazi, and M. Ghomashlooyan, “In vitro and in vivo anthelmintic activity of seed extract of Coriandrum sativum compared to Niclosamid against Hymenolepis nana infection,” Journal of Parasitic Diseases, vol. 40, no. 4, pp. 1307–1310, 2016.
View at: Publisher Site | Google Scholar
S. Niaz, T. Akhtar, S. Shams et al., “Treatment of bovine schistosoiasis with medicinal plant Vernonia anthelmintica (Kaliziri), an alternative approach,” African Journal of Traditional, Complementary and Alternative Medicines, vol. 12, pp. 78–83, 2015.
View at: Publisher Site | Google Scholar
S. A. Ameen, “Anthelmintic efficacy of pawpaw (Carica papaya) seeds in commercial layers,” African Journal of Biotechnology, vol. 11, no. 1, pp. 126–130, 2011.
View at: Publisher Site | Google Scholar
N. E. Nweze and I. U. Asuzu, “The anthelmintic effects of Buchholzia coriacea seed,” Nigerian Veterinary Journal, vol. 27, no. 2, pp. 60–65, 2006.
View at: Publisher Site | Google Scholar
T. A. Nzeakor, M. I. Udobi, I. G. Eke et al., “Evidence-based investigations into the ethnoveterinary use of Mimosa pudica L. (Fabaceae) as an anthlemintic,” Tropical Journal of Pharmaceutical Research, vol. 19, no. 12, pp. 2623–2630, 2021.
View at: Publisher Site | Google Scholar
M. B. Botura, G. D. Silva, H. G. Lima et al., “In vivo anthelmintic activity of an aqueous extract from sisal waste (Agave sisalana Perr.) against gastrointestinal nematodes in goats,” Veterinary Parasitology, vol. 177, no. 1–2, pp. 104–110, 2011.
View at: Publisher Site | Google Scholar
J. B. Githiori, J. Höglund, P. J. Waller, and R. L. Baker, “Anthelmintic activity of preparations derived from Myrsine africana and Rapanea melanophloeos against the nematode parasite, Haemonchus contortus, of sheep,” Journal of Ethnopharmacology, vol. 80, no. 2–3, pp. 187–191, 2002.
View at: Publisher Site | Google Scholar
Z. Iqbal, M. Lateef, A. Jabbar, G. Muhammad, and M. N. Khan, “Anthelmintic activity of Calotropis procera (Ait.) Ait. F. flowers in sheep,” Journal of Ethnopharmacology, vol. 102, no. 2, pp. 256–261, 2005.
View at: Publisher Site | Google Scholar
I. O. Ademola and J. N. Eloff, “Anthelmintic efficacy of cashew (Anarcadium occidentale L.) on in vitro susceptibility of the ova and larvae of Haemonchus contortus,” African Journal of Biotechnology, vol. 10, no. 47, pp. 9700–9705, 2011.
View at: Publisher Site | Google Scholar
S. S. Rosa, F. O. Santos, H. G. Lima et al., “In vitro anthelmintic and cytotoxic activities of extracts of Persea willdenovii Kosterm (Lauraceae),” Journal of Helminthology, vol. 92, no. 6, pp. 674–680, 2018.
View at: Publisher Site | Google Scholar
G. Fouche, B. M. Sakong, O. T. Adenubi et al., “Anthelmintic activity of acetone extracts from South African plants used on egg hatching of Haemonchus contortus,” Onderstepoort Journal of Veterinary Research, vol. 83, no. 1, pp. 1–7, 2016.
View at: Publisher Site | Google Scholar
I. E. Assiak, B. E. Olufemi, G. O. Ayonde, and M. Onigemo, “Preliminary studies on the effects of Amaranthus spinosus Leaf Extract as an Anthelmintic in growing pigs,” Tropical Veterinarian, vol. 20, no. 2, 2002.
View at: Publisher Site | Google Scholar
M. A. Sujon, M. Mostofa, M. S. Jahan, A. R. Das, and S. Rob, “Studies on medicinal plants against gastroinstestinal nematodes of goats,” Bangladesh Journal of Veterinary Medicine, vol. 6, no. 2, pp. 179–183, 1970.
View at: Publisher Site | Google Scholar
A. Jabbar, M. A. Zaman, Z. Iqbal, M. Yaseen, and A. Shamim, “Anthelmintic activity of Chenopodium album (L.) and Caesalpinia crista (L.) against trichostrongylid nematodes of sheep,” Journal of Ethnopharmacology, vol. 114, no. 1, pp. 86–91, 2007.
View at: Publisher Site | Google Scholar
A. A. Gbolade and A. A. Adeyemi, “Anthelmintic activities of three medicinal plants from Nigeria,” Fitoterapia, vol. 79, no. 3, pp. 223–225, 2008.
View at: Publisher Site | Google Scholar
A. N. Ogedengbe, S. O. Idowu, and I. O. Ademola, “Anthelmintic screening of phytomedicines using Haemonchus placei Adult motility assay,” Nigerian Journal of Pharmaceutical Research, vol. 15, no. 1, pp. 75–83, 2019.
View at: Google Scholar
L. E. Ferreira, P. M. N. Castro, A. C. S. Chagas, S. C. França, and R. O. Beleboni, “In vitro anthelmintic activity of aqueous leaf extract of Annona muricata L. (Annonaceae) against Haemonchus contortus from sheep,” Experimental Parasitology, vol. 134, no. 3, pp. 327–332, 2013.
View at: Publisher Site | Google Scholar
C. B. I. Alawa, A. M. Adamu, J. O. Gefu et al., “In vitro screening of two Nigerian medicinal plants (Vernonia amygdalina and Annona senegalensis) for anthelmintic activity,” Veterinary Parasitology, vol. 113, no. 1, pp. 73–81, 2003.
View at: Publisher Site | Google Scholar
L. V. Chisara, N. J. Cosmas, H. Chidozie, R. Ikechukwu, A. N. Chris, and S. Nnah, “Anthelmintic activities of Polyalthia longifolia leaf and stem bark extracts in Heligmosimoides bakeri infected mice,” Animal Research International, vol. 18, no. 2, pp. 4125–4133, 2021.
View at: Google Scholar
M. M. Suleiman, M. Mamman, Y. O. Aliu, and J. O. Ajanusi, “Anthelmintic activity of the crude methanol extract of Xylopia aethiopica against Nippostrongylus brasiliensis in rats,” Veterinarski Arhiv, vol. 75, no. 6, pp. 487–495, 2005.
View at: Google Scholar
J. A. Apenteng, M. Ogundeyi, E. E. Oppong, C. Osei-asare, and M. G. Brookman-Amissah, “In vitro Anti-infective and Antioxidant activity of Xylopia aethiopica [Dun.] A. Rich: a comparison of the fruits and leaves extracts,” Journal of Medicinal Plants Studies, vol. 4, no. 5, pp. 24–29, 2016.
View at: Google Scholar
W. K. Michael, A. A. John, N. M. David, S. A. Bright, N. D. Ivan, and B. A. Samuel, “In vitro anthelmintic activity of stem and root barks of Alstonia boonei De Wild,” Journal of Medicinal Plants Research, vol. 10, no. 13, pp. 179–182, 2016.
View at: Publisher Site | Google Scholar
Y. M. Shivkar and V. L. Kumar, “Anthelmintic activity of latex of Calotropis procera,” Pharmaceutical Biology, vol. 41, no. 4, pp. 263–265, 2003.
View at: Publisher Site | Google Scholar
A. Francis, A. A. John, G. A. William, H. S. George, N. M. David, and B. B. Edna, “Antioxidant and in-vitro anthelminthic potentials of methanol extracts of barks and leaves of Voacanga africana and Rauwolfia vomitoria,” African Journal of Microbiology Research, vol. 9, no. 35, pp. 1984–1988, 2015.
View at: Publisher Site | Google Scholar
M. G. R. Merveille, N. L. Célestine, K. A. Brice, M.-B. J. Akhanovna, B. Yves-Alain, and O. Jean-Maurille, “Phytochemical study and anthelmintic activity of nine Congolese medicinal plants,” Journal of Pharmaceutical Research International, vol. 33, no. 14, pp. 63–76, 2021.
View at: Publisher Site | Google Scholar
K. A. Tariq, M. Z. Chishti, F. Ahmad, and A. S. Shawl, “Anthelmintic activity of extracts of Artemisia absinthium against ovine nematodes,” Veterinary Parasitology, vol. 160, no. 1–2, pp. 83–88, 2009.
View at: Publisher Site | Google Scholar
Z. Iqbal, M. Lateef, M. Ashraf, and A. Jabbar, “Anthelmintic activity of Artemisia brevifolia in sheep,” Journal of Ethnopharmacology, vol. 93, no. 2–3, pp. 265–268, 2004.
View at: Publisher Site | Google Scholar
A. Sisay, T. Negesse, and A. Nurfeta, “Anthelminthic effects of extracts of indigenous browses from mid rift valley of Ethiopia,” Ethiopian Veterinary Journal, vol. 25, no. 2, pp. 132–143, 2021.
View at: Publisher Site | Google Scholar
A. Quartey, A. Oppong, I. Ayensu, J. Apenteng, D. Mintah, and C. Ikeani, “Synergistic in-vitro anthelmintic potentials of Vernonia amygdalina Delile stem and Carica papaya Lin. seeds,” in Proceedings of the 65th International Congress and Annual Meeting of the Society for Medicinal Plant and Natural Product Research (Ga 2017), Basel, Switzerland, September 2017.
View at: Publisher Site | Google Scholar
B. M. Agaie and P. A. Onyeyili, “Anthelmintic activity of the crude aqueous leaf extracts of Anogeissus leiocarpus in sheep,” African Journal of Biotechnology, vol. 6, no. 13, pp. 1511–1515, 2007.
View at: Google Scholar
D. Ndjonka, C. Agyare, K. Lüersen et al., “In vitro activity of Cameroonian and Ghanaian medicinal plants on parasitic (Onchocerca ochengi) and free-living (Caenorhabditis elegans) nematodes,” Journal of Helminthology, vol. 85, no. 3, pp. 304–312, 2011.
View at: Publisher Site | Google Scholar
T. Okpekon, S. Yolou, C. Gleye et al., “Antiparasitic activities of medicinal plants used in Ivory Coast,” Journal of Ethnopharmacology, vol. 90, no. 1, pp. 91–97, 2004.
View at: Publisher Site | Google Scholar
O. C. Jegede, M. S. Abubakar, B. D. J. George, O. J. Ajanusi, and S. Obeta, “Anthelmintic efficacy trials using fractions of ethanolic crude extract of Anogeissus schimperi hoechst against nippostrongylus braziliensis in rats,” Nigerian Veterinary Journal, vol. 36, no. 2, pp. 1175–1183, 2015.
View at: Google Scholar
I. O. Ademola and J. N. Eloff, “In vitro anthelmintic activity of Combretum molle (R. Br. ex G. Don) (Combretaceae) against Haemonchus contortus ova and larvae,” Veterinary Parasitology, vol. 169, no. 1–2, pp. 198–203, 2010.
View at: Publisher Site | Google Scholar
W. M. Koné, M. Vargas, and J. Keiser, “Anthelmintic activity of medicinal plants used in Côte d’Ivoire for treating parasitic diseases,” Parasitology Research, vol. 110, no. 6, pp. 2351–2362, 2012.
View at: Publisher Site | Google Scholar
C. Agyare, V. Spiegler, H. Sarkodie, A. Asase, E. Liebau, and A. Hensel, “An ethnopharmacological survey and in vitro confirmation of the ethnopharmacological use of medicinal plants as anthelmintic remedies in the Ashanti region , in the central part of Ghana,” Journal of Ethnopharmacology, vol. 158, pp. 255–263, 2014.
View at: Publisher Site | Google Scholar
V. Spiegler, J. Sendker, F. Petereit, E. Liebau, and A. Hensel, “Bioassay-Guided fractionation of a leaf extract from combretum mucronatum with anthelmintic activity: oligomeric procyanidins as the active principle,” Molecules, vol. 20, no. 8, Article ID 14810, 2015.
View at: Publisher Site | Google Scholar
F. C. Herrmann and V. Spiegler, “Caenorhabditis elegans revisited by atomic force microscopy – ultra-structural changes of the cuticle, but not in the intestine after treatment with Combretum mucronatum extract,” Journal of Structural Biology, vol. 208, no. 2, pp. 174–181, 2019.
View at: Publisher Site | Google Scholar
H. A. Gagman, N. A. Irwan, and H. B. Ahmad, “In vitro&lt study of the anthelmintic activity of aqueous and methanol extract of Guiera senegalensis&lt against egg hatch and larval developmental of Caenorhabditis elegans&lt,” Bayero Journal of Pure and Applied Sciences, vol. 11, no. 2, p. 274, 2019.
View at: Publisher Site | Google Scholar
A. B. Olukotun, I. A. Bello, and O. A. Oyewale, “Phytochemical and anthelmintic activity of Terminalia catappa (Linn) leaves,” Journal of Applied Sciences & Environmental Management, vol. 22, no. 8, p. 1343, 2018.
View at: Publisher Site | Google Scholar
S. Okpo and O. Nnajekwu, “In vitro&lt anthelmintic activity of the seed extracts of three plants of the Cucurbitaceae family on Lumbricus terrestris&lt,” Journal of Pharmacy & Bioresources, vol. 9, no. 2, pp. 92–98, 2013.
View at: Publisher Site | Google Scholar
N. Beloin, M. Gbeassor, K. Akpagana et al., “Ethnomedicinal uses of Momordica charantia (Cucurbitaceae) in Togo and relation to its phytochemistry and biological activity,” Journal of Ethnopharmacology, vol. 96, no. 1-2, pp. 49–55, 2005.
View at: Publisher Site | Google Scholar
C. O. Akoto, A. Acheampong, Y. D. Boakye, D. Akwata, and M. Okine, “In vitro anthelminthic, antimicrobial and antioxidant activities and FTIR analysis of extracts of Alchornea cordifolia leaves,” Journal of Pharmacognosy and Phytochemistry, vol. 8, no. 4, pp. 2432–2442, 2019.
View at: Google Scholar
J. M. Gathuma, J. M. Mbaria, J. Wanyama, H. F. A. Kaburia, L. Mpoke, and J. N. Mwangi, “Efficacy of Myrsine africana, Albizia anthelmintica and Hilderbrantia sepalosa herbal remedies against mixed natural sheep helminthosis in Samburu district, Kenya,” Journal of Ethnopharmacology, vol. 91, no. 1, pp. 7–12, 2004.
View at: Publisher Site | Google Scholar
T. Eguale, D. Tadesse, and M. Giday, “In vitro anthelmintic activity of crude extracts of five medicinal plants against egg-hatching and larval development of Haemonchus contortus,” Journal of Ethnopharmacology, vol. 137, no. 1, pp. 108–113, 2011.
View at: Publisher Site | Google Scholar
C. Osei Akoto, A. Acheampong, Y. D. Boakye, A. A. Naazo, and D. H. Adomah, “Anti-inflammatory, antioxidant, and anthelmintic activities of Ocimum basilicum (sweet basil) fruits,” Journal of Chemistry, vol. 2020, Article ID 2153534, 9 pages, 2020.
View at: Publisher Site | Google Scholar
S. A. Aderibigbe and S. O. Idowu, “Anthelmintic activity of Ocimum gratissimum and Cymbopogon citratus leaf extracts against Haemonchus placei adult worm,” Journal of Pharmacy & Bioresources, vol. 17, no. 1, pp. 8–12, 2020.
View at: Publisher Site | Google Scholar
N. Jaradat, L. Adwan, S. K’aibni, N. Shraim, and A. N. Zaid, “Chemical composition, anthelmintic, antibacterial and antioxidant effects of Thymus bovei essential oil,” BMC Complementary and Alternative Medicine, vol. 16, no. 1, p. 418, 2016.
View at: Publisher Site | Google Scholar
Z. Iqbal, W. Babar, Z. Sindhu, D. ud, R. Z. Abbas, and M. S. Sajid, “Evaluation of anthelmintic activity of different fractions of Azadirachta indica A. Juss Seed Extract,” Pakistan Veterinary Journal, vol. 32, no. 4, pp. 579–583, 2012.
View at: Google Scholar
Z. Iqbal, M. Lateef, A. Jabbar, and A. H. Gilani, “In vivo anthelmintic activity of Azadirachta indica A. Juss seeds against gastrointestinal nematodes of sheep,” Veterinary Parasitology, vol. 168, no. 3–4, pp. 342–345, 2010.
View at: Publisher Site | Google Scholar
H. Rabiu and M. Subhasish, “Investigation of in vitro anthelmintic activity of Azadirachta indica Leaves,” International Journal of Drug Development & Research, vol. 3, no. 4, pp. 94–100, 2011.
View at: Google Scholar
N. Jamra, G. Das, P. Singh, and M. Haque, “Anthelmintic efficacy of crude neem (Azadirachta indica) leaf powder against bovine strongylosis,” Journal of Parasitic Diseases, vol. 39, no. 4, pp. 786–788, 2015.
View at: Publisher Site | Google Scholar
S. Kausar, “In vitro evaluation of antifilarial effect of Azadirachta indica leaves extract in different solvents on the microfilariae of Setaria cervi,” Journal of Parasitic Diseases, vol. 41, no. 1, pp. 9–15, 2017.
View at: Publisher Site | Google Scholar
C. O. Nwosu, S. Yakubu, A. Ummate, and G. Abdullahi, “In-vitro anthelmintic efficacy of crude aqueous extracts of neem (Azadirachta indica) leaf, stem and root on nematode,” Animal Research International, vol. 3, no. 3, pp. 549–552, 2006.
View at: Google Scholar
I. O. Ademola, B. O. Fagbemi, and S. O. Idowu, “Evaluation of the anthelmintic activity of Khaya senegalensis extract against gastrointestinal nematodes of sheep: in vitro and in vivo studies,” Veterinary Parasitology, vol. 122, no. 2, pp. 151–164, 2004.
View at: Publisher Site | Google Scholar
L. Gregory, E. Yoshihara, L. K. F. Silva et al., “Anthelmintic effects of dried ground banana plant leaves (Musa spp.) fed to sheep artificially infected with Haemonchus contortus and Trichostrongylus colubriformis,” African Journal of Traditional, Complementary and Alternative Medicines, vol. 14, no. 1, pp. 138–144, 2016.
View at: Publisher Site | Google Scholar
L. N. Oliveira, E. R. Duarte, F. A. Nogueira, R. B. d. Silva, D. E. d. Faria Filho, and L. C. Geraseev, “Eficácia de resíduos da bananicultura sobre a inibição do desenvolvimento larval em Haemonchus spp. provenientes de ovinos,” Ciência Rural, vol. 40, no. 2, pp. 458–460, 2009.
View at: Publisher Site | Google Scholar
F. A. Nogueira, L. N. Oliveira, R. B. Da Silva et al., “Anthelminthic efficacy of banana crop residues on gastrointestinal nematodes of sheep: in vitro and in vivo tests,” Parasitology Research, vol. 111, no. 1, pp. 317–323, 2012.
View at: Publisher Site | Google Scholar
C. Marie-Magdeleine, M. Boval, L. Philibert, A. Borde, and H. Archimède, “Effect of banana foliage (Musa x paradisiaca) on nutrition, parasite infection and growth of lambs,” Livestock Science, vol. 131, no. 2–3, pp. 234–239, 2010.
View at: Publisher Site | Google Scholar
B. O. Ezea, O. O. Ogbole, and E. O. Ajaiyeoba, “In vitro&lt anthelmintic properties of root extracts of three Musa&lt species,” Journal of Pharmacy & Bioresources, vol. 16, no. 2, pp. 145–151, 2019.
View at: Publisher Site | Google Scholar
V. K. Payne, J. Poneacute, N. Kollins et al., “In vitro comparative effect of extracts of the seeds of Embelia rowlandii (Myrsinaceae) on the eggs and L1 and L2 larval stages of the parasitic nematode Heligmosomoides bakeri (Nematoda; Heligmosomatidae),” African Journal of Biotechnology, vol. 12, no. 2, pp. 205–211, 2013.
View at: Publisher Site | Google Scholar
N. Ali, U. Aleem, S. W. Ali Shah et al., “Acute toxicity, brine shrimp cytotoxicity, anthelmintic and relaxant potentials of fruits of Rubus fruticosus Agg,” BMC Complementary and Alternative Medicine, vol. 13, no. 1, p. 138, 2013.
View at: Publisher Site | Google Scholar
A. A. John, N. M. David, W. K. Michael et al., “In vitro anti-infective and antioxidant activities of Garcinia cola Heckel and Morinda lucida Benth,” Journal of Medicinal Plants Research, vol. 11, no. 32, pp. 507–512, 2017.
View at: Publisher Site | Google Scholar
S. Hounzangbe-Adote, I. Fouraste, K. Moutairou, and H. Hoste, “In vitro effects of four tropical plants on the activity and development of the parasitic nematode, Trichostrongylus colubriformis,” Journal of Helminthology, vol. 79, no. 1, pp. 29–33, 2005.
View at: Publisher Site | Google Scholar
P. A. Onyeyili, C. O. Nwosu, J. D. Amin, and J. I. Jibike, “Anthelmintic activity of crude aqueous extract of Nauclea latifolia stem bark against ovine nematodes,” Fitoterapia, vol. 72, 2001.
View at: Publisher Site | Google Scholar
T. Kiambom, M. K. Kouam, C. D. Ngangoum, B. Kate, and A. Teguia, “In vivo anthelmintic effect of ginger (zingiber officinale) powder against gastointestinal nematodes of artificially infected pigs,” Archives of Veterinary Science and Medicine, vol. 4, no. 1, pp. 1–12, 2020.
View at: Publisher Site | Google Scholar
Z. Iqbal, M. Lateef, M. S. Akhtar, M. N. Ghayur, and A. H. Gilani, “In vivo anthelmintic activity of ginger against gastrointestinal nematodes of sheep,” Journal of Ethnopharmacology, vol. 106, no. 2, pp. 285–287, 2006.
View at: Publisher Site | Google Scholar
A. Hussain, M. N. Khan, Z. Iqbal, M. S. Sajid, and M. K. N. Khan, “Anthelmintic activity of Trianthema portulacastrum L. and Musa paradisiaca L. against gastrointestinal nematodes of sheep,” Veterinary Parasitology, vol. 179, no. 1–3, pp. 92–99, 2011.
View at: Publisher Site | Google Scholar
T. Eguale, G. Tilahun, A. Debella, A. Feleke, and E. Makonnen, “In vitro and in vivo anthelmintic activity of crude extracts of Coriandrum sativum against Haemonchus contortus,” Journal of Ethnopharmacology, vol. 110, no. 3, pp. 428–433, 2007.
View at: Publisher Site | Google Scholar
T. Eguale, G. Tilahun, A. Debella, A. Feleke, and E. Makonnen, “Haemonchus contortus: in vitro and in vivo anthelmintic activity of aqueous and hydro-alcoholic extracts of Hedera helix,” Experimental Parasitology, vol. 116, no. 4, pp. 340–345, 2007.
View at: Publisher Site | Google Scholar
L. M. B. Oliveira, C. M. L. Bevilaqua, C. T. C. Costa et al., “Anthelmintic activity of Cocos nucifera L. against sheep gastrointestinal nematodes,” Veterinary Parasitology, vol. 159, no. 1, pp. 55–59, 2009.
View at: Publisher Site | Google Scholar
E. V. B. Azando, M. S. Hounzangbé-Adoté, P. A. Olounladé et al., “Involvement of tannins and flavonoids in the in vitro effects of Newbouldia laevis and Zanthoxylum zanthoxyloïdes extracts on the exsheathment of third-stage infective larvae of gastrointestinal nematodes,” Veterinary Parasitology, vol. 180, no. 3–4, pp. 292–297, 2011.
View at: Publisher Site | Google Scholar
O. A. Adu, K. A. Akingboye, and A. Akinfemi, “Potency of pawpaw (carica papaya) latex as an anthelmintic in poultry production,” Botany Research International, vol. 2, no. 3, pp. 139–142, 2009.
View at: Google Scholar
A. Effendy, N. Suparjo, S. Ameen, and O. Abdullah, “Evaluation of anthhelmintic potential of pawpaw (carica papaya) seeds administered in-feed and in-water for west african dwarf (WAD) goats,” Journal of Biology, Agriculture and Healthcare, vol. 4, no. 16, pp. 29–32, 2014.
View at: Google Scholar
S. A. Ameen, O. S. Adedeji, L. O. Ojedapo, T. Salihu, and C. O. Fabusuyi, “Anthelmintic potency of pawpaw (carica papaya) seeds in West African Dwarf (WAD) sheep,” Global Veterinaria, vol. 5, no. 1, pp. 30–34, 2010.
View at: Google Scholar
D. Attah and J. I. Amaka, “In-vitro anthelmintic activity of Garcinia kola aqueous seed extract on the infective stage of strongylid nematodes of goats,” Journal of Innovative Research in Life Sciences, vol. 1, no. 1, pp. 63–68, 2019.
View at: Google Scholar
C. O. Nwosu, K. M. Mobee, I. G. Gulani, I. O. Igbokwe, and V. O. Ogubuaja, “Anthelminthic efficacy of aqueous extracts of Garcina kola&lt seed and stem bark against strongylid nematodes of small ruminants in Nigeria,” Nigerian Journal of Parasitology, vol. 25, no. 1, pp. 1–5, 2006.
View at: Publisher Site | Google Scholar
J. Luka, A. W. Mbaya, A. A. Biu, and C. O. Nwosu, “The effect of Diospyros mespiliformis (Ebenaceae) extracts on the haemato-biochemical parameters of Yankasa Sheep experimentally infected with Haemonchus contortus&lt,” Nigerian Journal of Parasitology, vol. 38, no. 2, pp. 271–277, 2017.
View at: Publisher Site | Google Scholar
N. E. Nweze and L. A. Ngongeh, “In vitro anthelmintic activity of Anthocleista djalonensis,” Nigerian Veterinary Journal, vol. 28, no. 1, pp. 9–13, 2007.
View at: Publisher Site | Google Scholar
R. Kumarasingha, S. Preston, T. C. Yeo et al., “Anthelmintic activity of selected ethno-medicinal plant extracts on parasitic stages of Haemonchus contortus,” Parasites & Vectors, vol. 9, no. 1, pp. 187–7, 2016.
View at: Publisher Site | Google Scholar
O. C. Jegede, J. O. Ajanusi, A. O. Adaudi, and R. I. S. Agbede, “Anthelmintic efficacy of extracts of Spigelia anthelmia Linn on experimental Nippostrongylus braziliensis in rats,” Journal of Veterinary Science, vol. 7, no. 3, pp. 229–232, 2006.
View at: Publisher Site | Google Scholar
B. Asha, M. Krishnappa, and R. Kenchappa, “In vitro anthelmintic activity of different extracts of memecylon umbellatum&ltBurm,” Science, Technology and Arts Research Journal, vol. 4, no. 4, pp. 127–130, 2016.
View at: Publisher Site | Google Scholar
A. A. Gbolade and A. A. Adeyemi, “Investigation of in vitro anthelmintic activities of Pycnanthus angolensis and Sphenocentrum jollyanum,” Fitoterapia, vol. 79, no. 3, pp. 220–222, 2008.
View at: Publisher Site | Google Scholar
I. F. Aboagye, D. Mensah, and F. Boadu, “Anthelmintic effect of moringa oleifera lam. In wild caught Achatina achatina linnaeus, 1758 from the sefwi wiawso district, Ghana,” West African Journal of Applied Ecology, vol. 23, no. 2, pp. 27–33, 2015.
View at: Google Scholar
J. A. Apenteng, M. G. Brookman-Amissah, C. Osei-Asare, E. E. Oppong, and M. Ogundeyi, “In vitro anti-infective and antioxidant activity of plumbago zeylanica linn,” International Journal of Current Research in Biosciences and Plant Biology, vol. 3, no. 8, pp. 131–137, 2016a.
View at: Publisher Site | Google Scholar
V. Spiegler, E. Liebau, C. Peppler et al., “A hydroalcoholic extract from paullinia pinnata LRoots exerts anthelmintic activity against free-living and parasitic nematodes,” Planta Medica, vol. 82, no. 13, pp. 1173–1179, 2016.
View at: Publisher Site | Google Scholar
V. Spiegler, “Anthelmintic A-type procyanidins and further characterization of the phenolic composition of a root extract from paullinia pinnata,” Molecules, vol. 25, no. 10, p. 2287, 2020.
View at: Publisher Site | Google Scholar
N. Ali, S. W. Ali Shah, I. Shah et al., “Anthelmintic and relaxant activities of Verbascum thapsus Mullein,” BMC Complementary and Alternative Medicine, vol. 12, no. 1, p. 29, 2012.
View at: Publisher Site | Google Scholar
Z. Iqbal, M. Lateef, A. Jabbar, M. N. Ghayur, and A. H. Gilani, “In vitro and in vivo anthelmintic activity of Nicotiana tabacum L leaves against gastrointestinal nematodes of sheep,” Phytotherapy Research, vol. 20, no. 1, pp. 46–48, 2006.
View at: Publisher Site | Google Scholar
A. R. Williams, H. M. Ropiak, C. Fryganas, O. Desrues, I. Mueller-Harvey, and S. M. Thamsborg, “Assessment of the anthelmintic activity of medicinal plant extracts and purified condensed tannins against free-living and parasitic stages of Oesophagostomum dentatum,” Parasites & Vectors, vol. 7, no. 1, pp. 518–612, 2014.
View at: Publisher Site | Google Scholar
L. J. McGaw, A. K. Jäger, J. Van Staden, and J. Eloff, “Isolation of β-asarone, an antibacterial and anthelmintic compound, from Acorus calamus in South Africa,” South African Journal of Botany, vol. 68, no. 1, pp. 31–35, 2002.
View at: Publisher Site | Google Scholar
A. A. Bosman, S. Combrinck, R. Roux-Van Der Merwe, B. M. Botha, R. I. Mccrindle, and P. Houghton, “Isolation of an anthelmintic compound from Leucosidea sericea,” South African Journal of Botany, vol. 70, no. 4, pp. 509–511, 2004.
View at: Publisher Site | Google Scholar
S. A. T. Fobofou, K. Franke, G. Sanna et al., “Isolation and anticancer, anthelminthic, and antiviral (HIV) activity of acylphloroglucinols, and regioselective synthesis of empetrifranzinans from Hypericum roeperianum,” Bioorganic & Medicinal Chemistry, vol. 23, no. 19, pp. 6327–6334, 2015.
View at: Publisher Site | Google Scholar
V. F. Carvalho, L. D. A. Ramos, C. A. Da Silva et al., “In vitro anthelmintic activity of Siparuna guianensis extract and essential oil against Strongyloides venezuelensis,” Journal of Helminthology, vol. 94, p. e50, 2020.
View at: Publisher Site | Google Scholar
N. M. Enwerem, J. I. Okogun, C. O. Wambebe, D. A. Okorie, and P. A. Akah, “Anthelmintic activity of the stem bark extracts of Berlina grandiflora and one of its active principles, Betulinic acid,” Phytomedicine, vol. 8, no. 2, pp. 112–114, 2001.
View at: Publisher Site | Google Scholar
L. J. Shai, E. S. Bizimenyera, V. Bagla, L. J. Mcgaw, and J. N. Eloff, “Curtisia dentata (Cornaceae) leaf extracts and isolated compounds inhibit motility of parasitic and free-living nematodes,” Onderstepoort Journal of Veterinary Research, vol. 76, no. 2, pp. 249–256, 2009.
View at: Publisher Site | Google Scholar
M. A. Chama, G. A. Dziwornu, R. Waibel et al., “Isolation, characterization, and anthelminthic activities of a novel dichapetalin and other constituents of Dichapetalum filicaule,” Pharmaceutical Biology, vol. 54, no. 7, pp. 1179–1188, 2016.
View at: Publisher Site | Google Scholar
L. E. Ferreira, B. I. Benincasa, A. L. Fachin et al., “Thymus vulgaris L. essential oil and its main component thymol: anthelmintic effects against Haemonchus contortus from sheep,” Veterinary Parasitology, vol. 228, pp. 70–76, 2016.
View at: Publisher Site | Google Scholar
T. Banerjee, A. Singh, S. Kumar et al., “Ovicidal and larvicidal effects of extracts from leaves of Andrographis paniculata (Burm. f.) Wall.ex Nees against field isolates of human hookworm (Ancylostoma duodenale),” Journal of Ethnopharmacology, vol. 235, pp. 489–500, 2019.
View at: Publisher Site | Google Scholar
V. Samoylenko, D. C. Dunbar, M. A. Gafur et al., “Antiparasitic, nematicidal and antifouling constituents from juniperus berries,” Phytotherapy Research, vol. 22, no. 12, pp. 1570–1576, 2008.
View at: Publisher Site | Google Scholar
H. Qi, W. X. Wang, J. L. Dai, and L. Zhu, “In vitro anthelmintic activity of Zanthoxylum simulans essential oil against Haemonchus contortus,” Veterinary Parasitology, vol. 211, no. 3–4, pp. 223–227, 2015.
View at: Publisher Site | Google Scholar
L. Van Puyvelde, M. Liu, C. Veryser et al., “Active principles of Tetradenia riparia. IV. Anthelmintic activity of 8(14), 15-sandaracopimaradiene-7α, 18-diol,” Journal of Ethnopharmacology, vol. 216, pp. 229–232, 2018.
View at: Publisher Site | Google Scholar
H. M. P. Dilrukshi Herath, S. Preston, A. Hofmann et al., “Screening of a small, well-curated natural product-based library identifies two rotenoids with potent nematocidal activity against Haemonchus contortus,” Veterinary Parasitology, vol. 244, pp. 172–175, 2017.
View at: Publisher Site | Google Scholar
M. Liu, C. Veryser, J. G. Lu et al., “Bioassay-guided isolation of active substances from Semen Torreyae identifies two new anthelmintic compounds with novel mechanism of action,” Journal of Ethnopharmacology, vol. 224, pp. 421–428, 2018b.
View at: Publisher Site | Google Scholar
E. Ortu, G. Sanna, A. Scala, G. Pulina, P. Caboni, and G. Battacone, “In vitro anthelmintic activity of active compounds of the fringed rue Ruta chalepensis against dairy Ewe gastrointestinal nematodes,” Journal of Helminthology, vol. 91, no. 4, pp. 447–453, 2017.
View at: Publisher Site | Google Scholar
W. M. Forbes, W. A. Gallimore, A. Mansingh, P. B. Reese, and R. D. Robinson, “Eryngial (trans-2-dodecenal), a bioactive compound from Eryngium foetidum: its identification, chemical isolation, characterization and comparison with ivermectin in vitro,” Parasitology, vol. 141, no. 2, pp. 269–278, 2014.
View at: Publisher Site | Google Scholar
A. R. Williams, A. Ramsay, T. V. A. Hansen et al., “Anthelmintic activity of trans-cinnamaldehyde and A-andB-type proanthocyanidins derived from cinnamon (Cinnamomum verum),” Scientific Reports, vol. 5, no. 1, Article ID 14791, 2015.
View at: Publisher Site | Google Scholar
M. M. C. Souza, C. M. L. Bevilaqua, S. M. Morais, C. T. C. Costa, A. R. A. Silva, and R. Braz-Filho, “Anthelmintic acetogenin from Annona squamosa L. Seeds,” Anais da Academia Brasileira de Ciências, vol. 80, no. 2, pp. 271–277, 2008.
View at: Publisher Site | Google Scholar
C. García-Hernández, R. Rojo-Rubio, A. Olmedo-Juárez et al., “Galloyl derivatives from Caesalpinia coriaria exhibit in vitro ovicidal activity against cattle gastrointestinal parasitic nematodes,” Experimental Parasitology, vol. 200, pp. 16–23, 2019.
View at: Publisher Site | Google Scholar
G. F. Castillo-Mitre, A. Olmedo-Juárez, R. Rojo-Rubio et al., “Caffeoyl and coumaroyl derivatives from Acacia cochliacantha exhibit ovicidal activity against Haemonchus contortus,” Journal of Ethnopharmacology, vol. 204, pp. 125–131, 2017.
View at: Publisher Site | Google Scholar
G. S. Castañeda-Ramírez, J. F. D. J. Torres-Acosta, C. A. Sandoval-Castro et al., “Bio-guided fractionation to identify Senegalia gaumeri leaf extract compounds with anthelmintic activity against Haemonchus contortus eggs and larvae,” Veterinary Parasitology, vol. 270, pp. 13–19, 2019.
View at: Publisher Site | Google Scholar
R. J. Lin, C. Y. Chen, L. Y. Chung, and C. M. Yen, “Larvicidal activities of ginger (Zingiber officinale) against Angiostrongylus cantonensis,” Acta Tropica, vol. 115, no. 1–2, pp. 69–76, 2010.
View at: Publisher Site | Google Scholar
G. Jasso Díaz, G. T. Hernández, A. Zamilpa et al., “In vitro assessment of Argemone mexicana, Taraxacum officinale, Ruta chalepensis and Tagetes filifolia against Haemonchus contortus nematode eggs and infective (L3) larvae,” Microbial Pathogenesis, vol. 109, pp. 162–168, 2017.
View at: Publisher Site | Google Scholar
G. S. Cavalcante, S. M. de Morais, W. P. P. Andre et al., “Chemical composition and in vitro activity of Calotropis procera (Ait.) latex on Haemonchus contortus,” Veterinary Parasitology, vol. 226, pp. 22–25, 2016.
View at: Publisher Site | Google Scholar
M. Deepak, G. Dipankar, D. Prashanth, M. K. Asha, A. Amit, and B. V. Venkataraman, “Tribulosin and β-sitosterol-D-glucoside, the anthelmintic principles of Tribulus terrestris,” Phytomedicine, vol. 9, no. 8, pp. 753–756, 2002.
View at: Publisher Site | Google Scholar
G. X. Wang, J. Han, L. W. Zhao, D. X. Jiang, Y. T. Liu, and X. L. Liu, “Anthelmintic activity of steroidal saponins from Paris polyphylla,” Phytomedicine, vol. 17, no. 14, pp. 1102–1105, 2010.
View at: Publisher Site | Google Scholar
M. Doligalska, K. Jóźwicka, K. Donskow-Łysoniewska, and M. Kalinowska, “The antiparasitic activity of avenacosides against intestinal nematodes,” Veterinary Parasitology, vol. 241, pp. 5–13, 2017.
View at: Publisher Site | Google Scholar
X. B. Wang, G. H. Li, L. J. Zheng et al., “Nematicidal cardenolides from nerium indicum mill,” Chemistry and Biodiversity, vol. 6, no. 3, pp. 431–436, 2009.
View at: Publisher Site | Google Scholar
T. Satou, N. Akao, R. Matsuhashi, K. Koike, K. Fujita, and T. Nikaido, “Inhibitory effect of isoquinoline alkaloids on movement of second-stage larvae of Toxocara canis,” Biological and Pharmaceutical Bulletin, vol. 25, no. 12, pp. 1651–1654, 2002.
View at: Publisher Site | Google Scholar
A. Paul, M. Adnan, M. Majumder et al., “Anthelmintic activity of Piper sylvaticum Roxb. (family: piperaceae): in vitro and in silico studies,” Clinical Phytoscience, vol. 4, no. 1, p. 17, 2018.
View at: Publisher Site | Google Scholar
G. X. Wang, Z. Zhou, D. X. Jiang et al., “In vivo anthelmintic activity of five alkaloids from Macleaya microcarpa (Maxim) Fedde against Dactylogyrus intermedius in Carassius auratus,” Veterinary Parasitology, vol. 171, no. 3–4, pp. 305–313, 2010.
View at: Publisher Site | Google Scholar
S. Ayers, D. L. Zink, K. Mohn et al., “Anthelmintic activity of aporphine alkaloids from Cissampelos capensis,” Planta Medica, vol. 73, no. 3, pp. 296-297, 2007.
View at: Publisher Site | Google Scholar
E. Barrau, N. Fabre, I. Fouraste, and H. Hoste, “Effect of bioactive compounds from Sainfoin (Onobrychis viciifolia Scop.) on the in vitro larval migration of Haemonchus contortus: role of tannins and flavonol glycosides,” Parasitology, vol. 131, 2005.
View at: Publisher Site | Google Scholar
P. Wangchuk, M. S. Pearson, P. R. Giacomin et al., “Compounds derived from the Bhutanese daisy, ajania nubigena, demonstrate dual anthelmintic activity against schistosoma mansoni and Trichuris muris,” PLoS Neglected Tropical Diseases, vol. 10, no. 8, Article ID e0004908, 2016.
View at: Publisher Site | Google Scholar
A. Soldera-Silva, M. Seyfried, L. H. Campestrini et al., “Assessment of anthelmintic activity and bio-guided chemical analysis of Persea americana seed extracts,” Veterinary Parasitology, vol. 251, pp. 34–43, 2018.
View at: Publisher Site | Google Scholar
D. Mukai, N. Matsuda, Y. Yoshioka, M. Sato, and T. Yamasaki, “Potential anthelmintics: polyphenols from the tea plant Camellia sinensis L. are lethally toxic to Caenorhabditis elegans,” Journal of Natural Medicines, vol. 62, no. 2, pp. 155–159, 2008.
View at: Publisher Site | Google Scholar
R. Kermanshai, B. E. Mccarry, J. Rosenfeld, P. S. Summers, E. A. Weretilnyk, and G. J. Sorger, “Benzyl isothiocyanate is the chief or sole anthelmintic in papaya seed extracts,” Phytochemistry, vol. 57, no. 3, pp. 427–435, 2001.
View at: Publisher Site | Google Scholar
M. C. Navarro-Moll, M. C. Romero, M. P. Montilla, and A. Valero, “In vitro and in vivo activity of three sesquiterpenes against L3 larvae of Anisakis type I,” Experimental Parasitology, vol. 127, no. 2, pp. 405–408, 2011.
View at: Publisher Site | Google Scholar
E. von Son-de Fernex, M. Á. Alonso-Díaz, B. Valles-de la Mora, P. Mendoza-de Gives, M. González-Cortazar, and A. Zamilpa, “Anthelmintic effect of 2H-chromen-2-one isolated from Gliricidia sepium against Cooperia punctata,” Experimental Parasitology, vol. 178, pp. 1–6, 2017.
View at: Publisher Site | Google Scholar
B. C. Q. Nguyen, J. Chompoo, and S. Tawata, “Insecticidal and nematicidal activities of novel mimosine derivatives,” Molecules, vol. 20, no. 9, Article ID 16741, 2015.
View at: Publisher Site | Google Scholar
M. T. Engström, M. Karonen, J. R. Ahern et al., “Chemical structures of plant hydrolyzable tannins reveal their in vitro activity against egg hatching and motility of Haemonchus contortus nematodes,” Journal of Agricultural and Food Chemistry, vol. 64, no. 4, pp. 840–851, 2016.
View at: Publisher Site | Google Scholar
H. Hoste and J. F. J. Torres-acosta, “Veterinary Parasitology Non chemical control of helminths in ruminants adapting solutions for changing worms in a changing world,” Veterinary Parasitology, vol. 180, pp. 144–154, 2011.
View at: Publisher Site | Google Scholar
N. Mukherjee, S. Mukherjee, P. Saini, P. Roy, and S. P Sinha Babu, “Phenolics and terpenoids; the promising new search for anthelmintics: a critical review,” Mini-Reviews in Medicinal Chemistry, vol. 16, no. 17, pp. 1415–1441, 2016.
View at: Publisher Site | Google Scholar
N. Hirazawa, S. I. Oshima, T. Mitsuboshi, and K. Hata, “The anthelmintic effect of medium-chain fatty acids against the monogenean Heterobothrium okamotoi in the tiger puffer Takifugu rubripes: evaluation of doses of caprylic acid at different water temperatures,” Aquaculture, vol. 195, no. 3–4, pp. 211–223, 2001.
View at: Publisher Site | Google Scholar
G.-H. Li and K. Zhang, “Nematode-toxic fungi and their nematicidal metabolites,” in Nematode-Trapping Fungi, Springer, Berlin, Germany, 2014.
View at: Publisher Site | Google Scholar
J. A. Pineda-Alegría, J. E. Sánchez, M. González-Cortazar et al., “In vitro nematocidal activity of commercial fatty acids and β-sitosterol against Haemonchus contortus,” Journal of Helminthology, vol. 94, pp. 1355–e144, 2020.
View at: Publisher Site | Google Scholar
N. Bizimana, “Traditional veterinary practice in Africa,” in Deutsche Gesellschaft Fur Technische Zusammenarbeit (GTZ), TZ-Verlag-Ges, Hanau, Germany, 1994.
View at: Google Scholar
F. N. Gachathi, Kikuyu Botanical Dictionary of Plant Names and Uses, Tropical Botany, Gituamba, Kenya, 1989.
W. S. Koko, M. Galal, and H. S. Khalid, “Fasciolicidal efficacy of Albizia anthelmintica and Balanites aegyptiaca compared with albendazole,” Journal of Ethnopharmacology, vol. 71, no. 1–2, pp. 247–252, 2000.
View at: Publisher Site | Google Scholar
Science and Technology Policy Research Institute and K. Busia, Ghana herbal pharmacopoeia, Science and Technology Policy Research Institute, Council for Scientific and Industrial Research, Ghana, West Africa, 2007.
West African Health Organisation, West African Herbal Pharmacopoeia, West African Health Organisation, Burkina Faso, West African, 2013.
E. B. Twumasi, P. I. Akazue, K. Kyeremeh et al., “Antischistosomal, antionchocercal and antitrypanosomal potentials of some Ghanaian traditional medicines and their constituents,” PLoS Neglected Tropical Diseases, vol. 14, no. 12, Article ID e0008919, 2020.
View at: Publisher Site | Google Scholar
I. Hashmat, H. Azad, and A. Ahmed, “Neem (azadirachta indica A . Juss) - a nature’s drugstore: an overview,” International Research Journal of Biological Sciences, vol. 1, no. 6, pp. 76–79, 2012.
View at: Google Scholar
F. U. Fomum, “PROTA4U vernonia amygdalina delile,” in Ressources Végétales de l’Afrique Tropicale, PROTA Plant Resources of Tropical Africa, Wageningen, Netherlands, 2004.
View at: Google Scholar
S. C. Chhabra, R. Mahunnah, and E. Mshiu, “Plants used in traditional medicine in eastern Tanzania. V. Angiosperms (passifloraceae to sapindaceae),” Journal of Ethnopharmacology, vol. 33, no. 1-2, pp. 143–157, 1991.
View at: Publisher Site | Google Scholar

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Copyright © 2022 Jonathan Jato et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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