Hindawi

Journal of Parasitology Research

Volume 2024, Article ID 7955692, 11 pages
https://doi.org/10.1155/2024/7955692

Review Article
A Review of Ethnomedicinal Plants as Potential Anthelmintic
Agents to Alternatively Control Gastrointestinal Nematodes of
Ruminants in South Africa

Lindokuhle Christopher Mhlongo ,1 Cresswell Mseleku ,2 Thando Tenza ,2

Sylvester Werekeh Fomum ,2 Lyndy Joy McGaw ,3 Abubeker Hassen ,4
and Ignatius Verla Nsahlai 2
1
Department of Animal Science, University of the Free State, Bloemfontein, South Africa
2
Department of Animal and Poultry Science, University of KwaZulu-Natal, Pietermaritzburg, South Africa
3
Department of Paraclinical Sciences, University of Pretoria, Onderstepoort, South Africa
4
Department of Animal and Wildlife Sciences, University of Pretoria, Hatfield, South Africa

Correspondence should be addressed to Lindokuhle Christopher Mhlongo; [email protected]

Received 28 September 2023; Revised 29 November 2023; Accepted 30 December 2023; Published 16 January 2024

Academic Editor: Bernard Marchand

Copyright © 2024 Lindokuhle Christopher Mhlongo 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.

Small ruminant production is one of the most important animal productions for food security in the world, especially in the
developing world. Gastrointestinal nematode (GIN) infection is a threat to this animal’s production. Conventional drugs that
are used to control these parasites are losing their efficacy due to the development of resistant parasites. These drugs are not
biologically degradable, taint meat products and are also expensive for communal farmers. Hence, research is now exploring
ethnomedicinal anthelmintic plants for an alternative remedy. The objective of this paper was to review ethnomedicinal plants
as a potential alternative to unsustainable commercial anthelmintics. This review sought to understand common GINs
infecting ruminants, resistance manifestation in GINs to conventional treatment, reasons communal farmers choose
ethnomedicine, and modes of action in anthelmintic plants. It also examined the usage of plants and plant parts, dosage forms,
methods for improving bioactivity, convectional validation procedures, and restrictions on ethnomedicinal plant use as
anthelmintics in ethnomedicine. Such insight is essential, as it highlights the importance of ethnoveterinary medicine and ways
to adopt or improve it as a potential alternative to conventional anthelmintics.

1. Introduction Conditions that increase GIN infections in ruminants

are summer conditions, which favor infectious larva forma-
Small ruminant production is important for food security tion and higher grazing rates, as well as lower immunity
for resource-poor farmers as they are sold for cash, serve against GINs, especially in younger ruminants [4]. Rota-
as a source of food, generate much needed income for med- tional grazing, anthelmintic plants, or the FAMACHA chart
ical needs, contribute to off-farm investments, and generate can all be used to control GIN infections. Moreover, vaccines
income for the purchase of additional stock [1]. A common such as Barbervax can be used to prevent GIN infections [5].
constraint of small ruminant production is GIN infections Unlike commercial farmers, most small stock owners do not
[2]. Small-stock farmers are the ones that are affected the have access to commercial anthelmintics and lack informa-
most by this constraint. Infection with GINs is transmitted tion to help manage this challenge [6]. Even when they have
through the consumption of infected pastures by small access to these anthelmintics, they cannot administer them
ruminants [3]. correctly due to inadequate knowledge, resulting in wrong
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2 Journal of Parasitology Research

dosing [7]. These farmers are constrained to using ethnove- common helminths that affect ruminants belong to the
terinary medicinal plants exerting anthelmintic activities to nemathelminths phylum and include Trichostrongyloidea,
control GIN in their stock. These plants are locally available Strongyloidea, Metastrongyloidea, Ancylostomatoidea, Rha-
to them. Ethnoveterinary medicine is the practice of control- ditoidea, Trichuroidea, Filarioidea, Oxyliroidea, Ascaridoi-
ling diseases in animals using indigenous knowledge [8]. dea, and Spiruoidea [10]. Predisposing factors for
Worldwide, commercial farmers use commercial anthelmin- ruminants with GINs include low immunity, contaminated
tics, some of which include benzimidazole, imidazothiazoles, pastures, highly humid and wet areas, genetic make-up, over-
praziquantel, levamisole, ivermectin, doramectin, and moxi- stocking of pastures, and resistance to anthelmintic drugs [11].
dectin to control GINs in ruminants. Ruminants are born without GIN infection but get GIN
However, with the widespread development of drug infection through grazing contaminated pasture with infec-
resistance, these anthelmintics are becoming less effective. tive larvae (L3) [12]. Infective larvae migrate to a specific
Resistance is defined by the lack of GIN susceptibility to part of the gastrointestinal tract, where they grow from a
anthelmintics [9]. This has left the animal production preadult larva (L4) to a developed adult form (L5). Adult nem-
industry with a need to look for potential alternative atodes (male and female) live in the target site of the host
anthelmintics. Unlike commercial anthelmintics, potential (Table 1). Adult female nematodes lay 5000–10,000 eggs per
anthelmintic alternatives should be biodegradable, have no day, which are passed in feces to contaminate pastures [12].
contaminants in meat, and be highly effective. Consequently, Under favorable conditions, such as a warm and moist envi-
research is exploring plants with potential anthelmintic ronment, eggs hatch into larvae (L1). Thereafter, L1 larvae
activities used by resource-poor farmers. These plants have moult into L2 and L3 stages and accumulate in the pasture.
not been sufficiently evaluated in vitro and in vivo for their It is known that GINs mainly feed on the erythrocytes of the
anthelmintic effects, toxicity and residual effects on the host host, causing compromised productivity (Tables 1 and 2)
animal(s). Hence, traditional practice needs to be improved and anemia, which sometimes leads to death [11].
so that active natural chemicals can be identified. It is, there-
fore, essential to understand the common GINs that affect 3.2. Anthelmintic Resistance by Gastrointestinal Nematodes.
ruminants sheep and how resistance develops. The objective Resistance poses a large threat to the economic returns of
of this review is to evaluate ethnomedicinal plants with ruminant farming. This is because almost all major broad-
anthelmintic properties. This review discusses, but is not spectrum commercial anthelmintics are now ineffective
limited to, how parasitized small ruminants are identified against GINs [13]. Different broad-spectrum commercial
and the identification of ethnomedicinal plants and their anthelmintics are commonly used to control GIN infections.
collection time, preparation methods, plant parts used, dos- These drugs include benzimidazoles, imidazothiazoles, prazi-
age, activity improvements, and limitations. quantel, levamisole, ivermectin, doramectin, and moxidectin
[9]. Resistance occurs when animals exposed to GINs show a
2. Methods decreased response to an anthelmintic drug. Similarly, resis-
tance results when a certain population of GINs possesses a
Databases of academic papers, including ScienceDirect, gene associated with resistance [14]. This can be due to genetic
ResearchGate, and Google Scholar, were used to search litera- disorders such as mutation, deletion, or amplification. Fur-
ture for this review. We chose English-language written articles thermore, epigenetics through methylation of promoter
from peer-reviewed publications using “ethnoveterinary + regions or promoter regions reduces GIN’s susceptibility to
endoparasites/gastrointestinal nematodes+ sheep/ goat / cattle,” anthelmintics [9]. Full drug resistance is confirmed when the
“ethnomedicinal plants + endoparasites/gastrointestinal nema- maximum dosage shows less efficacy [15].
todes+ sheep/ goat / cattle,” “ethnobotany + endoparasites/gas- Resistance manifests in two ways: decreased efficacy and
trointestinal nematodes+ sheep/ goat / cattle,” and “traditional delayed effectiveness of the anthelmintic against GINs. Host
medicine + endoparasites/gastrointestinal nematodes+ sheep/ animals infected with drug-resistant GINs need frequent dos-
goat/cattle” as keywords. The consideration of studies for inclu- ing compared to host animals without drug-resistant GINs. As
sion was based on the study being a survey or review and having a result, this can increase drug residues in meat products. Per-
been conducted in sub-Saharan Africa then parasitology sistent drug resistance in ruminants is a major challenge.
research papers from all over the world were used for explana- Hence, anthelmintic plants used in ethnoveterinary medicine
tions on some of the findings of the literature review. are a potential alternative. This is because ethnomedicinal
plants have been used for years to control GINs, with fewer
3. Results reports of inefficacy. A survey reported that 79% of Ethiopian
communal farmers noticed no GIN resistance, while 21%
3.1. Gastrointestinal Nematodes of Ruminants. The presence noticed GIN resistance in their anthelmintic medicinal plants
of GIN infections causes loss of ruminant production’s pro- [16]. The lack of resistance in anthelmintic plants might be
ductivity and profit, as well as low ruminant’s body condi- due to the vast diversity in chemical composition as compared
tion scores in most farming communities. This results in to commercial anthelmintics [17].
food insecurity in the communal areas, where they depend
on small ruminants in times of crop failure because of 3.3. Reasons for Ethnomedicinal Plant Preference. Different
drought or inclement weather conditions. Resistant GINs plants are used by communal farmers to combat GIN bur-
are more common in small ruminants (Table 1). The most den in ruminants. Ethnoveterinary medicine is orally passed
 9582, 2024, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1155/2024/7955692 by Universidad Autonoma del Estado de Morelos, Wiley Online Library on [09/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Journal of Parasitology Research 3

Table 1: Gastrointestinal site of infection per different gastrointestinal nematodes that infect ruminants.

Oesophagus and
Abomasum Small intestines Large intestines
omasum
Avitellina centripunctata, Bunostomum
trigonocephalum, Cooperia curticei,
Cotylophoron spp, Haemonchus contortus, Cooperia surnabada, Gaigeria
Chabertia ovina, Oesophagostomum
Gongylonema Teladorsagia circumcincta, pachyscelis, Moniezia expansa,
columbianum, Oesophagostomum
pulchrum, and Teladorsagia trifurcata, Nematodirus battus, Nematodirus
venulosum, Skrjabinema ovis, Trichuris
Paramphistomum Parabonema spp., and filicollis, Nematodirus spathiger,
ovis, and Trichuris skrjabini
spp. Trichostrongylus axei Strongyloides papillosus,
Trichostrongylus capricola, and
Trichostrongylus vitrinus
[12] [12] [12] [12]
Information contained per column is from the reference placed below each column.

Table 2: Characteristics of different gastrointestinal nematodes that infect ruminants.

Scientific (common) name Morphology Prepatent period Signs Source

Length, 10-30 mm; Acute anemia, intense blood loss,
Haemonchus contortus
white uteri and ovaries; 18-22 d bottle jaw, stool, pale gums, and [12]
(barber-pole)
barber-pole look inner eyelids.
Length, 10-30 mm;
Nematodirus spp. Inappetence, stool,
thin exterior; 15-28 d [12]
(thread-necked strongyle) weight, and wool loss.
swollen head
Trichostrongylus spp. Weight loss, reduced growth rate,
No filament 20-25 d [12]
(bankrupt worm/stomach hairworm) inflammations, stool, and inappetence
Cooperia spp. Length; 4-6 mm;
15-20 d Inappetence, stool, and weight loss. [12]
(small intestine worm) brownish-red
Oesophagostomum spp. Length, 20 mm; Stool, swelling large intestinal wall, and
6-7 d [12]
(nodular worm) thin front mucus-covered feces.
Length, 35-80 mm;
Trichuris spp. (whipworm) thin neck; thick hind end; 1-3 months Caecal wall swelling and stool. [12]
curved tail

on from one generation to the next. Therefore, this might mintic withdrawal period [16]. Hence, this suggests that,
influence acceptance by communal farmers. Eighty percent unlike commercial anthelmintics, ethnoveterinary practices
of Africans depend on ethnoveterinary medicine to control might be beneficial to communal farmers as they do not
and treat diseases in ruminants [18]. Different tribes use dif- contaminate meat products. This is because most of the
ferent ethnoveterinary medicines to treat diseases. Thus, medicinal plants used to treat GINs, including C. papaya,
there are a lot of anthelmintic plants available as alternatives A. vanbalenii, A. comosus, A. sativum, and A. cepa, are edible
when others become ineffective due to resistance. Commu- [22]. Communal farmers were reported to prefer ethnoveter-
nal farmers’ preference of ethnoveterinary medicine over inary medicine to treat GINs in ruminants because it does
anthelminthic drugs might be because of high commercial not taint the meat products [23]. The fact that these treat-
anthelmintic cost [16], uncertainty of commercial anthel- ments work well against GINs and that communal farmers
mintic’s advantage over anthelmintic plants, absence of side believe they are better than synthetic medications are further
effects, high efficacy, easy accessibility and usage, and lack of considerations that may have contributed to their choice for
veterinarians in communal areas [19]. ethnoveterinary medicine. It can also be the case that they
Most communal farmers depend on animal products, are biodegradable and do not pollute the environment.
including milk and meat, but are ignorant of the drug resi-
dues in these products. Anthelmintic residues in meat and 3.4. Diagnosis of Gastrointestinal Nematode Infection. Diag-
related products are a large challenge. Thus, anthelmintic nosis of GIN infection in ruminants by communal farmers
remedies used to treat GINs are passed on to consumers is sometimes carried out via the senses of taste, touch, smell,
and can be potentially harmful [20]. Synthetic drugs leave and sight [24]. Common signs for monitoring GIN infection
residues in hair, skin, and subcutaneous adipose tissue [21]. in ruminants are loss of body condition, loss of appetite, and
A survey reported that 77% of communal farmers in rubbing against poles [25]. Nevertheless, there are limita-
Ethiopia lacked knowledge about the commercial anthel- tions that come with common signs, since helminthiasis
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4 Journal of Parasitology Research

can be confused with other diseases that have similar signs, Phytochemicals
such as fluke [23] and coccidiosis [26]. Therefore, using and digestive
enzymes
common signs such as body condition scores can be limited
because low body weight is not a distinct sign of GIN infec-
tion [27]. Hence, there is little correlation between body con-
dition scores and fecal egg count in terms of accurately Neurotransmitter
control
detecting GIN infection in ruminants [28].
Adoption of these diagnostic symptoms can affect the Decreased GINs
efficacy of anthelmintics, dosage, and validity of the anthel-
mintic ability of the plant [19]. Distinct signs can be used
Entry route
to make an accurate GIN infection diagnosis because com-
munal farmers cannot afford accurate modern methods such
as the McMaster technique. One of such distinct signs of
GIN parasitism is bottle jaw. This condition is caused by Trace mineral content
the depletion of blood protein when GINs suck blood from
Figure 1: Mode of action’s factors for ethnomedicinal plants with
the host. However, clinical signs are not enough to diagnose
anthelmintic activity.
GIN infection in ruminants. Hence, more reliable techniques
have been developed to detect these parasites with accuracy.
One of such methods for the accurate diagnosis of GIN bur- (Figure 1). It is believed that the effect of anthelmintic
den in ruminants is the FAMACHA chart [28]. medicinal plants on GINs depends on phytochemical and
FAMACHA chart method identifies animals suffering trace mineral content, GIN neurotransmitter control, and
from anemia, which is a common GIN infection symptom, entry routes used by ethnomedical plants to penetrate GINs.
by checking the eye color [29]. It compares the eye color of
the membrane with that on the chart showing five levels of
3.5.1. Phytochemicals and Digestive Enzymes. Different
anemia. Level 1 signifies the absence of anemia, while level
plants, used in ethnoveterinary medicine to control GINs,
5 represents a highly anemic condition [29]. Anemia is a
contain different anthelmintic phytochemicals and enzymes
sign of severe GIN infection by Haemonchus contortus.
(Table 3). It is not fully known how all phytochemicals of
The disadvantage of this method is that anemia may be
different plants used by communal farmers control GINs,
due to a nonparasitic infection [28].
except for a few like those mentioned in Table 4. Plants like
Presently, fecal egg count is the most commonly used
papaya and fig trees have latex, which contains a lot of pro-
method [28]. This method uses a microscope to evaluate
teolytic enzymes, while pineapples have cysteine proteinases.
GINs in feces and is very accurate for detecting parasites
These enzymes digest GINs. Ficus spp. has also been
within the host [28]. Animals with a higher nematode, egg
reported to have ficin [31]. Saba senegalensis has compounds
shed, and count have the highest GIN burden. The main dis-
such as tannins, saponins, triter, pene glycoside, and ste-
advantage of using the fecal egg count method is that com-
roids. These compounds attach to free proteins within tubes
munal farmers cannot adopt it without the use of a
for larval nutrition, thus killing the GINs [32]. While com-
laboratory, which can be challenging for these farmers
mercial anthelmintics contain one molecule acting on the
[28]. Moreover, this method does not identify the types of
parasite(s), anthelmintic plants possess numerous active
GINs affecting the herd. For instance, Trichostrongylus colu-
molecules that act together in synergy against gastrointesti-
briformis, Cooperia spp., and Bunostomum trigonocephalum
nal parasites. This increases efficiency and reduces the devel-
highly affect sheep; on the other hand, Oesophagostomum
opment of resistant GINs [33]. Aloe has amino acids such as
columbianum and Haemonchus contortus affect goats [30].
sterols and phenols, which negatively affect the protein and
There are two types of fecal egg count tests, one of which
body repair of GINs [34]. While ginger’s anthelmintic activ-
is qualitative and the other is quantitative. A qualitative test
ity is due to gingerols, shogaols, zingerone, and paradol [35],
is the floatation of contaminated fecal samples under a
these phytochemicals activate cholinergic receptors. This
microscope to examine GINs [28]. The results are reported
causes a contraction of the gastrointestinal tract, which
as positive or negative as proof of infection progress over
expels parasites [36].
time [28]. A quantitative test uses eggs per gram of known
weight of a sample of feces, a McMaster slide, and floatation
solution. Two chambers of the slide are filled with fecal solu- 3.5.2. Neurotransmitter Control. Active phytochemical in an
tion multiplied by the dilution factor, and the type of nema- anthelmintic plant extract is the one with the ability to
tode eggs is identified under the microscope [28]. The inhibit acetylcholinesterase of GINs [37]. Acetylcholinester-
quantitative evaluation technique is easier, more inexpen- ase is a serine hydrolase that is responsible for the catalysis
sive, and more reusable compared to the qualitative fecal of a neurotransmitter called acetylcholine into acetate and
egg count method [28]. choline. This results in the formation of a substrate-
enzyme complex. This is followed by acetylation of the
3.5. Modes of Action for Anthelmintic Ethnomedicinal Plants. hydroxyl group of the amino acid serine, which is present
Anthelmintic medicinal plants are believed to have various in the esteratic site that is finally deacetylated. Its inhibition
strategies of controlling GINs which are listed below leads to paralysis and death of the GINs [38].
 9582, 2024, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1155/2024/7955692 by Universidad Autonoma del Estado de Morelos, Wiley Online Library on [09/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Journal of Parasitology Research 5

Table 3: Different anthelmintic phytochemicals found in plant extracts and their effect on gastrointestinal nematodes that infect ruminants.

Anthelmintic phytochemicals Mode of action

Saponins Targets the permeability of the cuticle of the parasites.
Benzyl isothiocyanate Paralyses the motor activity and metabolism of the parasite.
Contains proteolytic chymopapain and papain, which are responsible for the
Cysteine proteinases
breakdown of the parasites’ cuticle.
Isoflavones Affects the glycolysis and glycogenolysis activity enzymes and calcium ions of the parasite.
Causes the cleavage of endoperoxide bridges by iron-producing free radicals.
Artemisinin
This stresses the biological molecules of the parasite through oxidation.
Uncouple the oxidative phosphorylation mechanism and disturb the
Phenolic compounds
glycoprotein of the cell surface, resulting in the death of the parasite.
Uncouple the oxidative phosphorylation, attach to free glycoproteins of the
Tannins gastrointestinal wall, and attach to the glycoproteins of the
parasites causing death to the parasite.
Paralyse the central nervous system, steroidal alkaloids, and oligoglycosides which
Alkaloids suppress sucrose from travelling from the stomach to the small intestines; alkaloids act as an
antioxidant, thus inhibiting homeostasis condition excellent for parasite development.
[12] [12]
Information contained per column is from the reference placed below each column.

Helicotylenchus dihystera treated with Punica granatum, 3.6. Common Anthelmintic Ethnomedicinal Plants. Table 4
Thymus vulgaris, and Artemisia absinthium extracts were shows that there is a wide range of plant families that are
reported for suppression of acetylcholine in nematodes used for anthelmintic ethnomedicinal medicine. Previous
[37]. It was then concluded that the efficacy of these extracts surveys reported that communal farmers predominantly
shows a relation between nematode poisoning and the inhi- use plants of the Fabaceae family [45–47]. Other studies dif-
bition of acetylcholine. This suggests that the observed effi- fer; Asphoedelaceae was the most frequently used plant fam-
cacy of the used plant extracts is partly due to the ily by communal farmers in Kwezi and Ntambethemba
inhibition of acetylcholine activity. villages in Eastern Cape province [19]. Respondents in
Nhema village, Zimbabwe, frequently used plants of the
families Fabaceae, Solanaceae, and Asphoedelaceae [26].
3.5.3. Entry Route. Anthelmintic drugs penetrate GINs com- The use of different families of plant species in various
monly via oral access or transcuticular diffusion. It is argued regions seems to be influenced by plant population distri-
that the latter route is the most common way of entry for bution and their multiple biological activities [26]. This is
anthelmintic drugs in GINs [39]. Hence, an effective extract exemplified by plant species including Clerodendrum
against GINs must have phytochemicals that can penetrate glaum, which is used in treating helminths, diarrhea, bile,
the cuticle of GINs [39]. Lipophilic anthelmintics exert their and cough, while Gnidia kraussiana is used in treating bile
effects through transcuticular diffusion easily compared to and cough in addition to its anthelmintic activity. Besides
hydrophobic ones [40]. This suggests that the extract type their anthelmintic activity, Laportea peduncularis, on the
that is more effective might contain more lipophilic than other hand, is used to treat diarrhea and cough; Salvadora
hydrophilic chemicals. australis is used to treat foam in cattle; and Ziziphus
mucronata also treats diarrhea [48]. Similarly, Zingiber
3.5.4. Trace Mineral Content. For reducing GIN infection, officinale is used in ethnoveterinary medicine to treat
taking supplements of trace minerals (iron, zinc and cop- arthritis, rheumatism, sprains, muscular aches, pains, sore
per) boosts immunity, particularly at critical physiological throats, cramps, indigestion, nausea, hypertension, demen-
periods [41]. This is due to a positive correlation between tia, and fever in addition to treating GINs [49]. Plant spe-
white blood cells and trace mineral content [42]. Presence cies families that can treat human or multiple livestock
of trace minerals can improve plant extract efficacy against diseases in addition to GINs of livestock seem to be
GINs. In a previous study, efficacious anthelmintic extracts prioritized.
tended to have a high content of zinc, copper, and protein
in addition to flavonoids and tannins [43]. Supplementa- 3.7. Anthelmintic Ethnomedicinal Plant’s Preparation. It is
tion with copper kills GINs and decreases egg counts believed that ethnomedicinal plant parts should be harvested
[44]. Hence, nutritious plants with high trace minerals under certain conditions for the preparation of ethnomedic-
and anthelmintic phytochemical content are potential inal plants that sufficiently control GINs. Because they con-
alternative pastures. Such types of pastures can eliminate tinuously store phytochemicals, roots are picked every year;
the need for laborious vaccination and harvesting of bark is harvested while sap is running; and fruit and seeds
anthelmintic plants. are harvested early in the fruit ripening season [50]. Leaves
 9582, 2024, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1155/2024/7955692 by Universidad Autonoma del Estado de Morelos, Wiley Online Library on [09/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
6 Journal of Parasitology Research

Table 4: Anthelmintic plant species used by South African communal farmers to control ruminant’s gastrointestinal nematodes.

Plant family Scientific (common) name Plant part Preparation Reference

Apocynaceae Acokanthera oppositifolia (Bushman’s poison) Leaves Boiling [68]
Apocynaceae Dichrostachys cinerea (sickle bush) Leaves Boiling [48]
Apocynaceae Salvadora australis (mustard tree) Leaves Boiling [48]
Agapanthaceae Agapanthus praecox (African lily) Leaves Infusion [68]
Amaryllidaceae Crinum macowanii (Cape coast lily) Leaves Boiling [48]
Anacardiaceae Harpephyllum caffrum (wild plum) Bark Boiling [68]
Apiaceae Centella coriacea (swamp pennywort) Bark Boiling [68]
Araliaceae Cussonia spicata (Natal cabbage tree) Bark Infusion [68]
Asphodelaceae Aloe ferox (bitter aloe) Leaves Boiling [68]
Asphodelaceae Gasteria bicolor (elephant’s Foot) Leaves Infusion [68]
Asphodelaceae Bulbine latifolia (broad-leaved bulbine) Leaves Boiling [68]
Asphodelaceae Bulbine frutescens (cat’s tail) Whole plant, Infusion [68]
Asphodelaceae Bulbine abyssinica (snake flower) Leaves Boiling [68]
Asphoedelaceae Aloe arborescens (bitter aloe) Leaves Boiling [68]
Asteraceae Vernonia neocorymbosa (Vernonia) Leaves Boiling [47]
Bignoniaceae Kigelia africana (sausage tree) Leaves Boiling [48]
Capparidaceae Capparis sepiaria (caper bush) Roots Infusion [68]
Euphorbiaceae Ricinus communis (castor bean) Leaves Boiling [68]
Fabaceae Elephantorrhiza elephantina (elephant’s root) Roots Boiling [48]
Fabaceae Schotia latifolia (bush boer bean) Bark Boiling [19, 68]
Fabaceae Erythrina caffra (coral tree) Leaves Boiling [68]
Geraniaceae Pelargonium reniforme (Pelargonium) Tuber Boiling [68]
Gunneraceae Gunnera perpensa (river pumpkin) Tuber Boiling [48]
Hyacinthaceae Albuca setosa (soldier in the box) Tuber, Boiling [68]
Hypoxidaceae Hypoxis argentea (yellow stars) Tuber Boiling [19]
Lamiaceae Teucrium trifidum (Dutchmen’s fever plant) Leaves Infusion [68]
Lamiaceae Leonotis leonurus (wild dagga) Leaves Boiling [68]
Lamiaceae Ocotea bullata (black stinkwood) Bark Boiling [68]
Loganiaceae Strychnos henningsii (red bitter berry) Bark Boiling [68]
Moraceae Ficus ingens (fig tree) Leaves Boiling [48]
Pittosporaceae Pittosporum viridiflorum (cheese wood) Bark Infusion [48]
Polygonaceae Rumex lanceolatus (common dock) Roots Boiling [48]
Ptaeroxylaceae Ptaeroxylon obliquum (sneeze wood) Leaves Boiling [48]
Rhamnaceae Ziziphus mucronata (buffalo thorn) Leaves Infusion [68]
Rutaceae Zanthoxylum capense (small knob wood) Roots Boiling [68]
Sterculiaceae Hermannia incana (sweet yellow bells) Whole plant Boiling [68]
Thymelaeaceae Gnidia kraussiana (wellow heads) Leaves Boiling [48]
Tiliaceae Grewia occidentalis (cross berry) Bark Boiling [68]
Urticaceae Laportea peduncularis (river nettle) Leaves Boiling [48]

are collected before the flowering season, as plants use tochemical, increases during winter but decreases during
metabolites for flowering. Leaves are usually collected in summer months [52].
the summer [24] since there is a supply of effective medicinal Ethnoveterinary medicinal plants with anthelmintic
plants [18], as phytochemicals peak at this time. To avoid activities can be prepared through boiling and infusion.
harvesting during a peak GIN infection [51], the harvest Table 4 shows that boiling (aqueous solution) is the most
period must be during the off-peak GIN infection period commonly used method of preparation of anthelmintic
to avoid contamination of ethnomedicinal plants with GINs. plant species per plant part by communal farmers [19, 25,
The advantage of this is that peak anthelmintic phytochem- 48]. Boiling is suggested to either deactivate toxic thermola-
icals coincide with winter, an off-peak GIN infection season. bile components of plants that can be poisonous to the GIN
For example, tannin content, a common anthelmintic phy- infected animal [19] or deactivating some of the active
 9582, 2024, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1155/2024/7955692 by Universidad Autonoma del Estado de Morelos, Wiley Online Library on [09/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Journal of Parasitology Research 7

anthelmintic phytochemicals that are thermolabile [19]. avoid extinction, as opposed to using roots or stems [8, 19].
Water may dilute the concentration of plant extracts and Consequently, picking leaves for ethnoveterinary medicine
render crude extracts less poisonous [8]. The choice of aque- tends to lead to plant extinction, especially if the leaves picked
ous extracts by communal farmers might be because water is are the younger ones instead of the old ones since leaves are
easily accessible. This method of preparation is also easy to biologically important for the survival of plants [56]. On the
master, as it only requires water to boil for a certain time. other hand, some communal farmers use the whole plant to
The solvent used seems to influence the efficacy of prepare medicine because they believe it increases efficacy
anthelmintic plant extracts. Aqueous plant extracts, which [57]. It is also suggested that plant parts with a higher shelf life
are a common extract type, have lower efficacy compared are highly preferred, such as bark, bulbs, fruits, and seeds [58]
to ethanolic and methanolic plant extracts [33]. This might and shrubs, tubers, and whole plants [26].
be due to aqueous extract characteristics such as low anthel- One survey reported that 58.3% of farmers in the Benoue
mintic activity, biological activity, and type of phytochemi- region of Cameroon were commonly using stem and bark
cals [45, 53]. Differences between aqueous and other types [25], perhaps the trees used are in abundance. This suggests
of extracts might be attributed to the different proportions that different plant parts have different levels of activity in
of phytochemicals extracted by solvent types resulting in dif- combatting GINs in ruminants. These commonly used plant
ferent effects on GINs [39]. Therefore, water might be part(s) might be chosen based on relative efficacy to other
extracting fewer phytochemicals compared to other solvents plant parts. For instance, pineapple has more anthelmintic
such as ethanol, acetone, chloroform, and methanol due to phytochemical(s) (bromelain) in the stem compared to other
being used to extract phytochemicals from plants containing parts and will most likely exert greater efficacy if used as a
less water extractable phytochemicals. source of extract.
Iris kashmiriana aqueous extract from sheep showed Thus, this suggests that plant parts with a higher propor-
superior in vitro efficacy against Haemonchus contortus tion of phytochemicals than others should be isolated and
compared to methanolic extracts (100 vs. 85%, respectively) used to control GIN in small ruminants. This is because
[54]. In the same study using the in vivo method, the aque- the leaves are part of the browse that goats feed on. Hence,
ous extract remained superior compared to the methanolic GINs of goats might be adapted to phytochemicals within
extract (70.2 vs. 33.2%, respectively). The superiority of the browse. Goats also seem to acquire a weak immune sys-
aqueous extracts was explained to be due to the high concen- tem towards GINs as goat GINs develop resistance quicker
tration of water-soluble active molecules within the extracts. compared to sheep GINs [53]. Therefore, anthelmintic
Aqueous plant extract effect on GINs can also be expected to plants which are effective in goats are also expected to be
increase with immediate use after preparation while fresh more effective in sheep against GINs.
since aqueous anthelmintic plant extracts have a low shelf
life because water allows microbial growth [55]. There is a 3.9. Dosages of Anthelmintic Ethnomedicinal Plant Extract.
need for a solvent that can extract polar and nonpolar Ethnoveterinary medicine doses used to control GINs are
anthelmintic phytochemicals. This is because the plant cell measured using spoons, calabash bottles, clay pots, hand
contains water-soluble and non-water-soluble bioactive che- palms, and finger pinches [24]. Sometimes, qualitative mea-
micals. Therefore, a mixture of water and other solvents can sures determine concentrations, such as color change, once
be used for extraction for improved efficacy against GINs. the plant material is soaked in water [24]. As a result, most
For instance, aqueous-ethanol is a better solvent than pure ethnoveterinary medicines may be toxic compared to mod-
ethanol because a proportion of bioactive chemicals are ern anthelmintics [17]. Therefore, there is no exact amount
polar or nonpolar and can be extracted to increase plant of plant material per volume of water that is suitable to effec-
extract efficacy [54]. Other types of solvents can be used tively treat GINs without adding negative effects on the
for plant extraction; acetone extracts for both hydrophilic GIN-infected ruminants. Hence, ethnoveterinary medicine
and lipophilic phytochemicals in plants, which is useful needs to be standardized for effective concentration, as this
especially when phenolic plants need to be extracted [54]. can prevent underdosing or overdosing [23]. Thus, stan-
Moreover, ether is better suited for the extraction of fatty dardization of ethnoveterinary medicine concentration can
acids and coumarin compounds from the plant’s anthelmin- limit the death of ruminants from toxicity and residues in
tic activity [54]. Similarly, chloroform is also better at meat products. For instance, treatment of GINs by ethnove-
extracting terpenoids and lactones. terinary medicine focuses more on plant extract volume
than phytochemical concentration per volume of plant
3.8. Common Plant Parts Used in Anthelmintic extract. For example, it is reported that the dosing of plant
Ethnomedicinal Plants. Commonly used plant parts to con- extracts is limited to using 0.75–1 L cold drink bottles per
trol GINs are the leaves of anthelminthic plants (Table 4) animal without being precise about the phytochemical con-
[19, 26]. This might be because leaves are infective larvae- centration, which may lead to under- or over-dosing of eth-
free since they are at the top of trees and dry compared to noveterinary medicine [59].
roots and bark, which can be close to contaminated grass.
Communal farmers were found to prefer using leaves 3.10. Improvement of Anthelmintic Activity in
because harvesting them is easier compared to collecting Ethnomedicinal Plant Extracts. Different anthelmintic plants
other plant parts [47]. The other reason communal farmers are mixed by communal farmers with one another for syner-
prefer leaves is because they want to conserve the plants to gistic purposes or with other nonplant substances to increase
 9582, 2024, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1155/2024/7955692 by Universidad Autonoma del Estado de Morelos, Wiley Online Library on [09/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
8 Journal of Parasitology Research

the efficacy of treatment. These nonplant substances used This might be attributed to the change in anthelmintic prop-
include flour (laxative effect), butter (increased flavour), rock erties of the plant by the gut microorganisms in the gastro-
salt (emulsification), oil cake (labile secretion), and Epsom intestinal tract of the host [42]. To counter the in vivo
salt [19]. Therefore, to prevent inconsistent anthelmintic inactivation of plant extracts, communal farmers concen-
activities, studies need to determine whether plant extracts trate extracts to increase the number of compounds prone
work best individually or in combination [60]. Some plant to inactivation by ruminal microorganisms [7]. Thus,
combinations are synergistic when the dose ratio is different in vivo, there is a need to identify plant extracts with phyto-
between plants involved in the combination. It has been chemicals that are resistant to digestion by the microflora of
found that the synergistic effect tends to happen at lower the gut as concentrating plant extracts can potentially lead to
concentration of tannin types in flavonoids and condensed the poisoning of ruminants. However, the disadvantage of
tannin combination [60]. in vivo bioassay is that it uses few control animals. Hence,
Combination of Vernonia anthelmintica and Embelia this inhibits the statistical analysis of data because it is
ribes have also shown 83-93% efficacy in controlling the expensive and labor-intensive. In addition, in vivo methods
GINs [61]. Synergism defines a condition where two or more have a lot of indirect and direct factors that influence the
agents are combined to result in an effect that is greater than results, such as nutrition, age, and season, but it is the most
that of a single agent [60]. Synergistic effect is calculated by useful method of anthelmintic plant validation.
monitoring additive individual effects from treatments [62].
They are then compared to effects from a combination of 3.12. Limitations of Anthelmintic Plants as Alternatives to
treatments on the assumption that they have independent Conventional Products. The use of plants as an alternative
effects. The additive effect is compared with the combination control for GINs in ruminants is limited by their mysterious
effect of treatment. If the additive effect is less than the com- compounds and direct and indirect mechanisms of action on
bined effect, then there is synergism, while if it is more than parasites and hosts. There is also a lack of a conventional
a combined effect, then there is antagonism [63]. Synergism preparation method for these plants [66]. This is because it
is advantageous because that is where a plant combination is difficult to prepare ethnomedicine as communal farmers
which is effective in both sheep and goats can be identified, do [66]. Hence, using bioassays such as in vitro and in vivo
since these plants produce different anthelmintic activities might exaggerate the efficacy of ethnomedicinal plants
in these ruminants [22]. [66]. Thus, the adoption of an incorrect dose is possible.
There is also the advantage of discovering a combination As a result, this might increase the toxicity of these plants.
of plants with phytochemicals that can combat resistance by Toxicity increases with efficacy due to dose dependence.
targeting different GIN species. This is due to different plant Hence, an efficacious dose might be too toxic to be used in
extracts being specific on GIN species and growth stage [64]. animals [66] to obtain the desired efficacy.
For instance, Fagara extracts have been shown to specifically Other factors, such as ease of plant cultivation, harvest-
affect GIN eggs and adult GINs [65]. Therefore, this suggests ing, supply, and mode of administration, can limit the use
that combining different plant extracts can enhance their of plant extracts. Palatability, stability, biodegradation of
broad-spectrum effects on GIN species and growth stages anthelmintic compounds within the plants, and lack of accu-
since GIN-infected ruminants contain GINs of various par- rate dosage can also lead to the poisoning of animals [67].
asitic growth stages and species. Some plants, such as Lotus spp. and H. coronarium, are
weak, cannot tolerate grazing and stamping by ruminants,
3.11. Anthelmintic Activity Validation in Ethnomedicinal and die easily [67]. Furthermore, communal farmers tend
Plants. Out of 250 000 plant species in the world, only 4– to give a single collective name to a group of plants based
5% have been studied for bioactive chemicals [66]. There- on their resemblance or characteristics. Plants producing
fore, most anthelmintic plants still need to be discovered latex are collectively called Mithuri by Kenyan communal
and studied for their anthelmintic activities [66]. This is farmers, regardless of plant family or medical purpose [56],
because these plants have different phytochemical composi- which makes anthelmintic plant identification difficult. Tra-
tions that produce different anthelmintic activities [66]. Bio- ditional healers are also very secretive about ethnoveterinary
assays used for isolating plants with anthelmintic activities medicine. This limits the identification of most anthelmintic
should be simple, accurate, and affordable. This is vital for plants [17]. Communal farmers in the Nhema midlands of
the easy identification of small concentrations of effective Zimbabwe explained that the reason for secrecy about eth-
and ineffective compounds [66]. The in vitro method is the noveterinary medicine knowledge is jealousy among custo-
most commonly used bioassay to isolate anthelmintic plants dians of this practice [19]. Secrecy might also be because
because it is ethical, less laborious, and cheap [66]. This this knowledge is passed down orally and strictly through
study has a laboratory imitation of biological conditions family lineages [56]. Furthermore, herbalists use plants of
without using an animal. In vivo studies involve feeding a different efficacies to make ethnoveterinary medicines. Cus-
parasitized host animal a certain amount of anthelmintic tomers tend to prefer the herbalist with the most effective
plants [46]. In vivo studies produce more accurate results ethnoveterinary medicine. Therefore, the explanation for
than in vitro studies, but due to animal welfare rules in many secrecy might be the competition between herbalists to
countries, they have limited use [66]. attract more customers. This limits the discovery of plants
In vitro, tanniferous plant extracts affected GIN burden with effective compounds because full information is not
[22]; however, in vivo, the effect on GIN was absent [52]. given [59].
 9582, 2024, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1155/2024/7955692 by Universidad Autonoma del Estado de Morelos, Wiley Online Library on [09/05/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Journal of Parasitology Research 9

4. Conclusion alizing an elephant,” Journal of Ethnopharmacology, vol. 110,

no. 3, pp. 391–400, 2007.
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plants are a potential source of ingredients to develop sus- “In-vitro anthelminthic activity of crude aqueous extracts of
tainable commercial anthelmintics. However, their activity Aloe ferox, Leonotis leonurus and Elephantorrhiza elephan-
is anecdotal, as it is not standardized for scientific use. tina against Haemonchus contortus,” Tropical Animal Health
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Disclosure [11] M. L. Leite-Browning, Haemonchus contortus (barber pole
This review was carried out at the University of KwaZulu- worm) infestation in goats, Barber Pole Worm Infest goats,
2006.
Natal, Pietermaritzburg campus, partially satisfying the
requirements for an MSc in Agric in Animal Science degree [12] F. Roeber, A. R. Jex, and R. B. Gasser, “Impact of gastrointes-
tinal parasitic nematodes of sheep, and the role of advanced
as stated in the first author’s thesis [49].
molecular tools for exploring epidemiology and drug
resistance-an Australian perspective,” Parasites & Vectors,
Conflicts of Interest vol. 6, no. 1, pp. 1–13, 2013.
[13] R. M. Kaplan, “Drug resistance in nematodes of veterinary
The authors declare no conflict of interest. importance: a status report,” Trends in Parasitology, vol. 20,
no. 10, pp. 477–481, 2004.
Acknowledgments [14] J. P. Crilly, “Guide to advances in the control of gastrointesti-
nal roundworms in sheep,” In Practice, vol. 45, no. 4,
This work was supported by the South African National pp. 211–221, 2023.
Research Foundation, Collaborative Postgraduate Pro- [15] G. C. Coles, “Drug resistance and drug tolerance in parasites,”
gramme (Grant number: 105290). Open Access funding is Trends in Parasitology, vol. 22, no. 8, p. 348, 2006.
enabled and organized by SANLiC Gold. [16] D. Belina, A. Giri, S. Mengistu, and A. Eshetu, “Gastrointestinal
nematodes in ruminants: the parasite burden, associated risk
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