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Epidemiology and diversity of gastrointestinal tract helminths of wild ruminants in sub-Saharan Africa: a review

Published online by Cambridge University Press:  03 June 2024

V. Phetla Open the ORCID record for V. Phetla [Opens in a new window] ,
M. Chaisi  and
M.P. Malatji
V. Phetla*
Affiliation:
Foundational Biodiversity Science, South African National Biodiversity Institute, P.O. Box 754, Pretoria 0001, South Africa
M. Chaisi
Affiliation:
Foundational Biodiversity Science, South African National Biodiversity Institute, P.O. Box 754, Pretoria 0001, South Africa Department of Veterinary Tropical Diseases, University of Pretoria, Onderstepoort 0110, South Africa
M.P. Malatji
Affiliation:
School of Life Science, College of Agriculture, Engineering and Science, University of KwaZulu-Natal, Westville Campus, Durban 4001, South Africa
*
Corresponding author: V. Phetla; Email: [email protected]
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Abstract

This review summarises studies on distribution, diversity, and prevalence of gastrointestinal helminth infections in wild ruminants in sub-Saharan Africa. The results showed that 109 gastrointestinal tract (GIT) helminth species or species complexes were recorded in 10 sub-Saharan African countries. South Africa reported the highest number of species because most studies were carried out in this country. Eighty-eight nematode species or species complexes were recorded from 30 wild ruminant species across eight countries. The genus Trichostrongylus recorded the highest number of species and utilised the highest number of wild ruminant species, and along with Haemonchus spp., was the most widely distributed geographically. Fifteen trematode species or species complexes were reported from seven countries. The genus Paramphistomum recorded the highest number of species, and Calicophoron calicophoron was the most commonly occurring species in sub-Saharan African countries and infected the highest number of hosts. Six cestode species or species complexes from one family were documented from 14 wild hosts in seven countries. Moniezia spp. were the most commonly distributed in terms of host range and geographically. Impala were infected by the highest number of nematodes, whilst Nyala were infected by the highest number of trematode species. Greater kudu and Impala harbored the largest number of cestodes. The prevalence amongst the three GIT helminths taxa ranged between 1.4% and 100% for nematodes, 0.8% and 100% for trematodes, and 1.4% and 50% for cestodes. There is still limited information on the distribution and diversity of GIT helminths in wild ruminants in most sub-Saharan African countries.

Keywords

Gastrointestinal tract (GIT)helminthsdistributionprevalencesub-Saharan Africa
Type
Review Article
Information
Journal of Helminthology , Volume 98 , 2024 , e45
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Introduction

Helminths are a diverse group of parasitic worms that infect both animals and humans (MacDonald et al., Reference MacDonald, Araujo and Pearce2002).

Infectious diseases caused by helminth infections are among the most significant global health concerns, impacting both human and animal populations (Lustigman et al., Reference Lustigman, Geldhof, Grant, Osei-Atweneboana, Sripa and Basanez2012; Rehman & Abidi, Reference Rehman and Abidi2022). These parasites play a critical role in both wildlife and domestic animals, regulating host populations in natural environments, and influencing survival, reproduction, and trophic equilibrium (Grenfell, Reference Grenfell1992; Holmes, Reference Holmes1995; Hudson et al., Reference Hudson, Dobson and Newborn1998; Tompkins & Begon, Reference Tompkins and Begon1999; van Wyk & Boomker, Reference van Wyk and Boomker2011; Watson, Reference Watson2013). Furthermore, they pose significant threats to conservation efforts, restricting the ranges of host species and endangering species of conservation concern (Dobson & Hudson, Reference Dobson and Hudson1986; Laurenson et al., Reference Laurenson, Sillero-Zubiri, Thompson, Shiferaw, Thirgood and Malcolm1998; Morgan et al., Reference Morgan, Shaikenov, Torgerson, Medley and Milner-Gulland2005; Page, Reference Page2013), such as the African buffalo, Nile lechwe, Mountain reedbuck, Mountain gazelle, and Walia ibex that occur in sub-Saharan Africa but have been considered endangered, near threatened, or vulnerable, with slowly decreasing populations in the wild according to the International Union for Conservation of Nature Red List of Threatened species (https://www.iucnredlist.org/). In wildlife and at the livestock-wildlife interface, parasitic infections can have severe consequences, including acute clinical signs leading to production losses and mortality (Meurens et al., Reference Meurens, Dunoyer, Fourichon, Gerdts, Haddad, Kortekaas, Lewandowska, Monchatre-Leroy, Summerfield, Schreur and van der Poel2021).

These parasites can cause a wide range of diseases and health problems, including gastrointestinal tract (GIT) disturbances in animals and humans (Slifko et al., Reference Slifko, Smith and Rose2000; Góralska & Blaszkowska, Reference Góralska and Blaszkowska2015). It has been established that GIT helminths may lead to nutritional deficiencies and poor health in wildlife (Gillespie, Reference Gillespie2006; Egbetade et al., Reference Egbetade, Akinkuotu, Jayeola, Niniola, Emmanuel, Olugbogi and Onadeko2014). Wildlife serves as carriers or reservoirs of various economically important helminths, which can be transmitted to domestic ruminants (Ogunji et al., Reference Ogunji, Akinboade, Dipeolu, Ayeni and Okaeme1984; Muriuki et al., Reference Muriuki, Murugu, Munene, Karere and Chai1998; Oyeleke & Edungbola Reference Oyeleke and Edungbola2001; Karere & Munene, Reference Karere and Munene2002; Moudgil & Singla Reference Moudgil and Singla2013; Rose et al., Reference Rose, Hoar, Kutz and Morgan2014; Modabbernia et al., Reference Modabbernia, Meshgi and Eslami2021; Barone et al., Reference Barone, Wit, Hoberg, Gilleard and Zarlenga2020). Wild ruminants such as Impala, African buffalo, Blue wildebeest, Eland, Nyala, and Greater kudu inhabit a variety of habitats in the savannas, woodlands, and open grasslands, and have a wide geographic distribution, making it possible for them to harbour a wide variety of gastrointestinal helminths in sub-Saharan African regions such as South Africa, Nigeria, Tanzania, and Kenya (Fuentes, Reference Fuentes2021). According to Sepulveda and Kinsella (Reference Sepulveda and Kinsella2013), wild animals are susceptible to different types of gastrointestinal helminths, including “roundworms” (nematodes), “flukes” (trematodes), and “tapeworms” (cestodes). Despite these parasitic infections, both wild and domestic animals have developed natural immune responses, allowing them to coexist with parasites without significant harm to the host (Borkovcova & Kopřiva, Reference Borkovcova and Kopřiva2005). Understanding the impact of these parasites and the potential for interspecies transmission requires robust parasitological research (Begon et al., Reference Begon, Hazel, Baxby, Bown, Cavanagh, Chantrey, Jones and Bennett1999). Additionally, to mitigate the impact of parasites on population dynamics, it is crucial to assess the incidence and prevalence of parasitic infections (Morner, Reference Morner2002; Williams et al., Reference Williams, Espie, Van Wilpe and Matthee2002; Junge & Louis, Reference Junge and Louis2005).

Gregory (Reference Gregory1997) classified the primary possible determinants of parasite distribution in a particular host population into three components: host population factors (abundance, range, and migration), host individual parameters (such as age, sex, body size, diet), and environmental factors (habitat and climate). Animal ecology is impacted by the changing environment and living conditions of the host, which also makes them more susceptible to helminth infections (Goossens et al., Reference Goossens, Dorny, Boomker, Vercammen and Vercruysse2005; Singh et al., Reference Singh, Gupta, Singla, Singh and Sharma2006). According to Body et al. (Reference Body, Ferté, Gaillard, Delorme, Klein and Gilot-Fromont2011), the infection rates of parasites in the host population may rise directly or indirectly as a result of factors such as weather, the quantity and quality of feed, or the lack of major predators. Climatic variables may directly impact the survival of free-living larval stages of the parasites and indirectly affect vertebrate hosts by affecting the frequency and intensity in which helminths are spread, and their geographic expansion (Mas-Coma et al., Reference Mas-Coma, Valero and Bargues2008). Temperature and moisture-related variables have more frequently been linked to the distribution and abundance of helminths (Mas-Coma et al., Reference Mas-Coma, Valero and Bargues2008).

The population of wild animals is seriously threatened by parasitic infections and associated complications, which have the potential to cause extinction (Harvell et al., Reference Harvell, Mitchell, Ward, Altizer, Dobson, Ostfeld and Samuel2002). Although wildlife populations might seem to have adjusted to the existence of parasites, they have not adapted to the detrimental consequences of parasitism (Bliss, Reference Bliss2009; Opara et al., Reference Opara, Osuji and Opara2010). It is therefore critical to know the helminth infections in the wildlife of a given area (van Wyk & Boomker, Reference van Wyk and Boomker2011), and baseline measures of parasite richness, prevalence, and intensity in wild populations in conservation biology, so that the emergence of new parasites or changes in abundance or disease conditions associated with existing parasites can be determined (Hahn et al., Reference Hahn, Ritchie and Moore2003; Brooks & Hoberg, Reference Brooks and Hoberg2006). Hence, the review collated existing scientific data highlighting the distribution, diversity, and prevalence of GIT helminths in wild ruminants in sub-Saharan Africa.

Methodology

Scoping review

The scoping review was designed to address the following questions: Which GIT helminth species of wild ruminants occur in sub-Saharan African countries? What is the distribution of GIT parasite infection in sub-Saharan Africa? What is the prevalence of GIT parasites in sub-Saharan Africa? To address these questions, published peer-reviewed articles from accredited journals explicitly reporting on the GIT helminths infections in wild ruminants in the sub-Saharan African region were identified and reviewed following the recommended standards (Munn et al., Reference Munn, Peters, Stern, Tufanaru, McArthur and Aromataris2018) and guidelines for reporting from the Preferred Reporting Items for Systematic Reviews and Meta-Analyses. The scoping review followed the approach outlined by Arksey and O’Malley (Reference Arksey and O’Malley2005), which included the (i) identification of research question(s); (ii) searching of relevant literature; (iii) selection of relevant literature; (iv) charting of data; and last (v) systematising, summarising, and reporting the results.

Search strategy

Three electronic databases, Google Scholar (https://scholar.google.com), Science Direct (https://www.sciencedirect.com/), and PubMed (http://www.ncbi.nlm.nih.gov/pubmed/), were searched for relevant literature. The following keywords and Boolean operators (AND, OR) were used in the search: GIT helminths OR Occurrences OR Distribution OR Prevalence AND “GIT nematodes OR roundworms” AND “GIT trematodes OR flukes OR rumen flukes OR conical flukes OR Platyhelminths” AND “GIT cestodes OR Tapeworms” AND wild ruminants in sub-Saharan Africa (Angola, Benin, Botswana, Burkina Faso, Burundi, Cape Verde, Cameroon, Comoros, Ivory Coast [Côte d’Ivoire], Eritrea, Ethiopia, Gabon, Gambia, Ghana, Guinea, Guinea-Bissau, Equatorial Guinea, Kenya, Lesotho, Liberia, Madagascar, Malawi, Mali, Mauritius, Mauritania, Mozambique, Namibia, Niger, Nigeria, Uganda, Central African Republic, Democratic Republic of the Congo, Rwanda, Sao Tome, and Principe, Senegal, Seychelles, Sierra Leone, Somalia, South Africa, South Sudan, Sudan, Swaziland, Tanzania, Chad, Togo, Zambia, Zimbabwe). The scope of the literature search was limited to articles written and published in English between 1980 and 2022. Relevant articles were first identified by screening through their titles and abstracts. Reference lists of selected articles were also screened as potential leads for additional relevant studies for review. Zotaro reference manager version 6.0.26 was used to manage the full texts of the retrieved articles.

Inclusion and exclusion criteria

Articles were considered if they had been published in ISI peer-reviewed accredited journals and specifically reported on the following: (i) occurrence or distribution of GIT helminths (nematodes, trematodes, and cestodes) in wild ruminants, (ii) prevalence of GIT helminths in wild ruminants, (iii) studies were conducted in the sub-Saharan African region; and (iv) studies were conducted and published from 1980 to 2022.

The review excluded studies reporting on (i) GIT parasites in non-ruminant wildlife; (ii) parasites that pass through the GIT during development but do not use the GIT as the predilection site of the adult parasite, e.g. Fasciola spp.; (iii) redescription of specimens collected before 1980; (iv) relevant studies but conducted in nations outside of the sub-Saharan African region, (v) GIT parasites other than helminths which fall outside of the three groups (nematodes, trematodes, and cestodes), and (vi) all reviews, books, dissertations and non-peer-reviewed reports.

Charting, collating, and summarising data

Data was extracted from articles with information that met the inclusion criteria after appraisal and contributed to answering the review questions. The aim or objectives of the study, the country in which the study was conducted, the outcomes of the study, and information relevant to the review questions were recorded on MS Word.

For this review, nomenclature updates for family/genus/species names were based on the following studies: Durette-Desset (Reference Durette-Desset1985), Durette-Desset et al. (Reference Durette-Desset, Hugot, Darlu and Chabaud1999), Boomker & Taylor (Reference Boomker and Taylor2004), Beveridge et al. (Reference Beveridge, Spratt and Durette-Desset2013), Hosseinnezhad et al. (Reference Hosseinnezhad, Sharifdini, Ashrafi, Roushan, Mirjalali and Rahmati2021) and Hodda (Reference Hodda2022) for nematodes; Eduardo (Reference Eduardo1982, Reference Eduardo1985) and Pfukenyi and Mukaratirwa (Reference Pfukenyi and Mukaratirwa2018) for trematodes (paramphistomes); and Mariaux et al. (Reference Mariaux, Tkach, Vasileva, Waeschenbach, Beveridge, Dimitrova, Haukisalmi, Greiman, Littlewood, Makarikov, Phillips, Razafiarisolo, Widmer and Georgiev2017) for cestodes (Anoplocephalidae).

Results

A literature search from the three databases yielded a total of 6164 hits, consisting of books, reviews, dissertations, unpublished reports, abstracts, and duplicate articles (Fig. 1). In addition, 12 articles were obtained through bibliographic searches from relevant articles. A total of 89 duplicating studies were removed, and a total of 6087 articles, books, reviews, and dissertations were deemed irrelevant and excluded after screening their titles and abstracts. The full text of 77 articles were downloaded and screened for eligibility, and 39 studies were deemed ineligible because they did not explicitly report on the GIT helminths found in wild ruminants and were not conducted in sub-Saharan countries. A total of 38 articles met the criteria and were included in the scoping review.

Figure 1. PRISMA diagram.

The distribution of the studies that fulfilled the inclusion criteria on a geographical scale and scope varied across the sub-Saharan Africa region. Of the 38 articles reviewed, 23 were from South Africa, four were from Zambia, two were from Kenya, two were from Nigeria, two from Sudan, one from Congo, one from Tanzania, one was from Rwanda, one from Ethiopia, and one study was conducted in both South Africa and Namibia. All the studies included in the scoping review were field studies or case reports. Most studies focused on the microscopic examination of faecal specimens using sedimentation and/or flotation methods, and the rest of the studies identified immature or adult specimens microscopically (Supplementary Table 1). Only one study (Ikeuchi et al., Reference Ikeuchi, Kondoh, Halajian and Ichikawa-Seki2022) used molecular methods; thus, some helminths could only be identified to genus level. The checklists were arranged according to taxa (i.e. nematodes, trematodes, and cestodes) (Tables 1–3).

Checklist and distribution of GIT nematodes in wild ruminants in sub-Saharan Africa from 1980 to 2022

The results showed that a total of 40 genera, 78 species, and 31 unidentified species complexes of GIT helminths were documented in 10 sub-Saharan African countries. Of these, 64 species and 24 unidentified species or species complexes were nematodes belonging to 29 genera from 17 nematode families (Ancylostomatidae, Ascarididae, Chabertiidae, Cooperiidae, Gongylonematidae, Habronematidae, Haemonchidae, Molineidae, Onchocercidae, Oxyuridae, Protostrongylidae, Strongylidae, Strongyloididae, Trichostrongylidae, Trichuridae, Trichonematidae, and Toxocaridae), and these were documented across Ethiopia, Kenya, Namibia, Nigeria, South Africa, Sudan, Tanzania and Zambia (Table 1, Supplementary Table 1). These nematode species infected approximately 30 species of wild ruminants.

The nematode families Cooperidae and Haemonchidae were the most diverse. Both families recorded five genera, with the Cooperidae family represented by 17 defined species and three undefined species complexes, whereas Haemonchidae represented recorded 16 defined species and three unidentified species complexes. However, the genus Trichostrongylus recorded the highest number of species. Furthermore, the genera Haemonchus and Trichostrongylus were the most distributed, reported in seven countries each (Table 1). Furthermore, the results showed that the Trichostrongylus genus infected the highest number of wild ruminants (n = 22), followed by Haemonchus contortus (n = 12). Impala were more susceptible and were infected by the highest number of nematode species, followed by the African buffalo and the Greater kudu.

Table 1. Checklist of GIT nematode species and their hosts reported in sub-Saharan Africa (1980-2022)

Checklist and distribution of GIT trematodes in wild ruminants in sub-Saharan Africa from 1980 to 2022

Eleven (n = 11) trematode species (Calicophoron raja, Cal. calicophorum, Cal. microbothrium, Cotylophoron cotylophorum, Cot. jacksoni, Paramphistomum cephalophi, Leiperocotyle gretillati, Leiperocotyle congolense, Stephanopharynx compactus, Bilatorchis papillogenitalis, and Schistosoma mattheei) and four species complexes (Calicophoron spp., Fischoederius spp., Gastrothylax spp., and Paramphistomum spp.) belonging to the families Gastrothylacidae, Paramphistomidae, and Schistosomatidae were identified. These were recorded from 17 species of wild ruminants and were distributed across Congo, Kenya, Nigeria, Rwanda South Africa, Tanzania, and Zambia (Table 2, Supplementary Table 1). The results also showed that Paramphistomum was the most widely distributed genus geographically, but species from the genus Calicophoron infected the most number of wild ruminants. Nyala were more susceptible to trematode infection and were infected by the highest number of trematode species, followed by the African buffalo.

Table 2. Checklist of GIT trematodes species and their hosts reported in sub-Saharan Africa (1980-2022)

Checklist and distribution of GIT cestodes in wild ruminants in sub-Saharan Africa from 1980 to 2022

Cestodes were the least reported GIT parasites. Six cestode species or species complexes, belonging to one (n = 1) cestode family (Anoplocephalidae) were documented across seven countries (Ethiopia, Kenya, Namibia, Nigeria, South Africa, Sudan, and Zambia (Table 3, Supplementary Table 1). However, the results also showed that the majority of these species were recorded in South Africa. These infections were recorded in 14 species of wild ruminants. The results also showed that Moniezia was the most common cestode genus, reported in Namibia, Kenya, South Africa, Nigeria, Ethiopia, Sudan, and Zambia (Table 3). Furthermore, the results obtained showed that Moniezia benedeni infected the highest number of wild ruminant species (n = 7). The results also indicated that the Greater kudu and Impala were more susceptible to cestode infection as they haboured the greatest numbers of species.

Table 3. Checklist of GIT cestodes species and their hosts reported in sub-Saharan Africa (1980-2022)

Prevalence of gastrointestinal helminths in wild ruminants in the sub-Saharan African region from 1980 to 2022

The results showed that the prevalence of nematode infections ranged from 1.4% to 100% (Table 4). The lowest prevalence of 1.4% (1/74) was in Nyala that were infected with Impalaia spp. and Oesophagostomum spp. in South Africa (Boomker et al., Reference Boomker, Horak and Flamand1991c). The highest prevalences of 100% were recorded in Gray rhebok (4/4) and Mountain reedbuck (66/66) infected with Cooperia yoshidaii in South Africa (Taylor et al., Reference Taylor, Boomker, Krecek, Skinner and Watermeyer2005). The following hosts also recorded high prevalences of nematode infection: 97.3% (72/74) of Nyala infected with Ostertagia harrisi (Boomker et al., Reference Boomker, Horak and Flamand1991c), 94% (62/64) of Mountain reedbuck infected with Haemonchus contortus (Taylor et al., Reference Taylor, Boomker, Krecek, Skinner and Watermeyer2005), and 90% (9/10) of Impala infected with Cooperia hungi (Van Wyk and Boomker, Reference van Wyk and Boomker2011) in South Africa (Table 4).

Table 4. Prevalence of GIT nematode infections in wild ruminants in sub-Saharan Africa (1980-2022)

The prevalence of trematode infections ranged from 0.8% to 100% (Table 5). The lowest prevalence was recorded in African buffalo infected with Fischoederius spp. (1/123, 0.8%) and Gastrothylax spp. (2/123, 1.6%) in Tanzania (Senyael et al., Reference Senyael, Kuya, Eblate, Katale and Keyyu2013). The highest prevalence of 100% (6/6) was reported in the Defassa waterbuck in Zambia, infected with Calicophoron spp. (Zieger et al., Reference Zieger, Boomker, Cauldwell and Horak1998). Reviewed studies showed that the lowest recorded cestode infections were reported in South Africa, with 1.4% (1/74) Nyala infected with Thysaniezia spp. (Boomker et al., Reference Boomker, Horak, Watermeyer and Booyse2000, Table 6). The highest prevalence of 50.0% (1/2) was observed in an Eland in Zambia that was infected with Moniezia benedeni (Zieger et al., Reference Zieger, Boomker, Cauldwell and Horak1998).

Table 5. Prevalence of gastrointestinal tract trematode infections in wild ruminants in sub-Saharan African countries (1980-2022)

Table 6. Prevalence of cestode infections in sub-Saharan African wild ruminants (1980-2022)

Discussion

The results of this study indicated that gastrointestinal helminth infections in wild ruminants in sub-Saharan Africa are common and diverse, with a total of 40 genera, 78 species, and 31 unidentified species or species complexes recorded from 31 species of wild ruminates across 10 countries. This rich diversity of GIT helminths is consistent with the wide diversity of wild animals in sub-Saharan Africa, which is also home to some of the world’s most iconic species (Chapman et al., Reference Chapman, Abernathy, Chapman, Downs, Effiom, Gogarten, Golooba, Kalbitzer, Lawes, Mekonnen, Omeja, Razafindratsima, Sheil, Tabor, Tumwesigye and Sarkar2022; O’Connell et al., Reference O’Connell, Nasirwa, Carter, Farmer, Appleton, Arinaitwe, Bhanderi, Chimwaza, Copsey, Dodoo and Duthie2019). South Africa reported the highest diversity of both parasites and hosts, which is a reflection of the country’s diverse fauna (Junker et al., Reference Junker, Horak and Penzhorn2015). Additionally, South Africa’s diverse climatic conditions, ranging from arid to temperate and subtropical regions provide a suitable environment for the survival and transmission of GIT helminths (Nalubamba et al., Reference Nalubamba, Bwalya, Mudenda, Munangandu, Munyeme and Squarre2015; Mosala, Reference Mosala2017). Thirty-one species complexes were not described to species level in the reviewed studies. Except for the study by Ikeuchi et al. (Reference Ikeuchi, Kondoh, Halajian and Ichikawa-Seki2022), molecular methods (DNA barcoding) were not used for species identification. Although microscopy is indispensable in the identification of helminth parasites (Halton, Reference Halton2004), DNA barcoding allows for species identification and discovery, which is fundamental in assessing biodiversity (Mampang et al., Reference Mampang, Auxtero, Caldito, Abanilla, Santos and Caipang2023). It is therefore likely that the diversity of parasites in wild ruminants reported in the reviewed studies in sub-Saharan African countries has been underestimated.

Nematodes were by far the most diverse and widely distributed (in host and geographic range) GIT species with 88 species or species or complexes from 17 distinct families, infecting 30 host species, recorded from nine sub-Saharan countries. Nematode infections are generally common in both domestic and wild animals across sub-Saharan Africa (Nalubamba et al., Reference Nalubamba, Bwalya, Mudenda, Munangandu, Munyeme and Squarre2015). They have a well-adapted life cycle that involves free-living stages in the environment (such as larvae in grass or soil), thereby exposing them to grazing animals (Morgan & van Dijk, Reference Morgan and van Dijk2012). This review therefore indicated that wild ungulates play an important role in the transmission of these parasites to livestock. The families Cooperidae and Haemonchidae were the most diverse nematode families. Some genera of these families, such as Haemonchus, Ostertagia, and Cooperia, are significant parasites of veterinary importance in endemic countries (Szewc et al., Reference Szewc, De Waal and Zintl2021), and are among the most important GIT parasites in domestic ruminants globally (Santos et al., Reference Santos, Salgado, Drummond, Bastianetto, Santos, Brasil, Taconeli and Oliveira2019). According to Hoberg et al. (Reference Hoberg, Kocan and Rickard2001) and Barone et al. (Reference Barone, Wit, Hoberg, Gilleard and Zarlenga2020), Cooperia spp. and Haemonchus spp. are most commonly found in the southern temperate and boreal zones, and have only rarely been recognised among sylvatic hosts at higher latitudes of the subarctic and arctic regions. Moreover, Haemonchus (including H. contortus) and Trichostrongylus species were the most commonly recorded in most countries and infected the greatest number of host species. This was not surprising as species from these genera have a global distribution and have been reported from different hosts (including roe deer, fallow deer, red deer, and mouflon) in Europe (Halvarsson et al., Reference Halvarsson, Baltrušis, Kjellander and Höglund2022). In South Africa, Boomker et al. (Reference Boomker, Booyse, Watermeyer, De Villiers, Horak and Flamand1996) and van Wyk and Boomker (Reference van Wyk and Boomker2011) noted that the subtropical regions of Limpopo and KwaZulu-Natal provinces, distinguished by elevated temperatures and humidity, provided favorable conditions for the presence and spread of Haemonchus species.

The results of this study indicated that browsers (Bushbuck, Greater kudu, Grey duiker, Eland, Red duiker, Eland, Gray rhebok, Springbok) harbored the highest number of nematode infections. Although it is expected that the prevalence of infection in these wild ruminants species would be low because of their feeding patterns as observed in Nyala (1.4%), which are predominantly browsers, Gray rhebok also recorded a 100% infection with Cooperia yoshidai in South Africa. The high prevalence of nematode infections recorded in Mountain reedbuck, Common reedbuck, and Lichtenstein’s hartebeest infected with Cooperia yoshidai, and Haemonchus contortus respectively, may have been due to them feeding on vegetation close to the ground where free-living infective stages of nematodes may be abundant (Atuman et al., Reference Atuman, Kudi, Abdu and Abubakar2019). Furthermore, the ability of the infective larvae of Cooperia spp. to resist desiccation and low temperatures, and their ability to survive winter on irrigated pastures increases their chance to infect browsers that graze during the dry season and reedbucks which are known to utilise irrigated pastures during winter (Boomker et al., Reference Boomker, Horak, Flamand and Keep1989a).

The results of this review indicated that 17 species of wild ruminants, distributed across Congo, Kenya, Nigeria, Rwanda South Africa, Tanzania, and Zambia were infected by 15 trematode species or species complexes from three genera. Nyala and African buffalo were more susceptible to infection by trematode species. These infections in African buffalo are not surprising as they are widely distributed across sub-Saharan Africa and regarded as an important reservoir for livestock diseases (Eygelaar et al., Reference Eygelaar, Jori, Mokopasetso, Sibeko, Collins, Vorster, Troskie and Oosthuizen2015). However, the water dependency of Waterbucks and the wallowing habit of the African buffalo, and their subsequent grazing of grasses near water sources predispose them to metacercariae (Saha et al., Reference Saha, Bhowmik and Chowdhury2013; Nath et al., Reference Nath, Das, Dixit, Agrawal, Singh, Kumar and Katuri2016; Atuman et al., Reference Atuman, Kudi, Abdu and Abubakar2019). This was corroborated by the observed high prevalence of 100% (6/6) Calicophoron spp. infection in the Zambian Defassa waterbuck (Zieger et al., Reference Zieger, Boomker, Cauldwell and Horak1998). The lowest prevalence of Fischoederius spp. (1/123, 0.8%) in African buffalo in Tanzania (Senyael et al., Reference Senyael, Kuya, Eblate, Katale and Keyyu2013) may have been due to Fischoederius spp. generally detected at low prevalence in ruminant infections (Buddhachat et al., Reference Buddhachat, Sriuan, Nak-On and Chontananarth2022).

Geographically, Paramphistomum was the most widely distributed trematode genus, however, Calicophoron species infected the highest number of hosts species. Reports from as early as the 1920s have shown that Cal. microbothrium is the most common paramphistome species in Africa (Pfukenyi et al., Reference Pfukenyi, Mukaratirwa, Willingham and Monrad2005; Pfukenyi & Mukaratirwa, Reference Pfukenyi and Mukaratirwa2018), and this could have been factored by the ability of this species to infect a high number of both wild and domestic ruminants (Pfukenyi & Mukaratirwa, Reference Pfukenyi and Mukaratirwa2018; Sibula et al., Reference Sibula, Nyagura, Malatji and Mukaratirwa2024). The current study corroborates this observation, suggesting that Cal. calicophorum is prevalent among wild ruminants across numerous sub-Saharan African countries. This species has been identified from Water buffalo and Sika deer in South Africa and Kenya (Eduardo, Reference Eduardo1983; Boomker et al., Reference Boomker, Horak and Flamand1991c) according to this review. Other studies have reported Cal. calicophorum from other wildlife such as the African buffalo, Blesbuck, Black wildebeest, Blue wildebeest, Impala, Lelwel’s hartebeest, Red hartebeest, Springbok, and others in other parts of Africa (Pfukenyi & Mukaratirwa, Reference Pfukenyi and Mukaratirwa2018; Sibula et al., Reference Sibula, Nyagura, Malatji and Mukaratirwa2024) and from domestic ruminants in Angola, Kenya, Mozambique, South Africa, Zambia, and Zimbabwe (Pfukenyi & Mukaratirwa, Reference Pfukenyi and Mukaratirwa2018).

The results of this review showed that Greater kudu has shown to be highly susceptible to infection. High number of cestode infections in Greater kudu have been documented in Namibia and South Africa (Cilliers, Reference Cilliers2019). However, the density of the Greater kudu population especially in South Africa where most infections by a wide diversity of GIT nematodes and cestodes have been recorded may have been the contributing factor (Müller et al., Reference Müller, Hassel, Jago, Khaiseb, van der Westhuizen, Vos, Calvelage, Fischer, Marston, Fooks and Höper2022). The most diverse and widely distributed GIT cestode species was Moniezia. This could be expected because Moniezia species have a cosmopolitan distribution (Demiaszkiewicz et al., Reference Demiaszkiewicz, Pyziel, Lachowicz and Filip-Hutsch2020; Nagarajan et al., Reference Nagarajan, Thirumaran, Pachaiyappan, Thirumurugan, Rajapandai, Rajendiran, Velusamy, Vannish and Kanagarajadurai2022), with at least 12 species currently described in domestic and wild ruminants based on their morphological features (Ohtori et al., Reference Ohtori, Aoki and Itagaki2015). Although they use both domestic and wild ruminants as their definitive hosts, infections of these tapeworms have also been documented in primates and angulates from the orders Artiodactyla and Perissodactyla. Their life cycle involves oribatid mites, which act as intermediate hosts (Nagarajan et al., Reference Nagarajan, Thirumaran, Pachaiyappan, Thirumurugan, Rajapandai, Rajendiran, Velusamy, Vannish and Kanagarajadurai2022).

Despite the high prevalence of Moniezia benedeni (50.0%) observed in Zambian Elands (Zieger et al., Reference Zieger, Boomker, Cauldwell and Horak1998), infection by Moniezia spp., including Moniezia benedeni, are typically common in domestic ruminants (Ohtori et al., Reference Ohtori, Aoki and Itagaki2015). Monieziasis pathogeneicity is mild and is associated with moderate infection (Kumar & Kaur, Reference Kumar and Kaur2023). However, heavy infections do occur and often lead to considerable economic losses associated with detrimental clinical manifestations such as pot-belly, poor growth rate, diarrhoea, anaemia, intestinal pathology, poor quality of wool, and even death of the ruminant host (Fagbemi & Dipeolu, Reference Fagbemi and Dipeolu1983; Zhao et al., Reference Zhao, Zhang, Bo, Li and Fu2009; Yan et al., Reference Yan, Bo, Liu, Lou, Ni, Shi, Zhan, Ooi and Jia2013).

Conclusion

This review has indicated that wild ruminants in sub-Saharan African are infected by a wide range of GIT species of conservation, economic and zoonotic importance, and act a reservoir hosts of helminths of domestic ruminants. Furthermore, this study has highlighted limitations in the studies reporting on GIT helminths, especially trematodes and cestodes, in sub-Saharan Africa, with data available for only 10 countries. Moreover, these are mostly case reports or involved a low sample size, which created bias in the prevalence of infection. Therefore, we recommend surveys in all sub-Saharan African countries, equally focusing on screening all GIT helminths in wild ruminants, targeting a larger number of animals and species, and using a combination of a wide variety of diagnostic and identification tools such as the traditional method (coprology), morphological identification of adult specimens, and molecular techniques to allow identification to species level. Furthermore, standardised and improved diagnostic tools such as next-generation sequencing should be used for identification and characterisation of infections to distinguish between species and further ensure proper identification to species level that will bridge the gap of misidentification of species.

Supplementary material

The supplementary material for this article can be found at http://doi.org/10.1017/S0022149X24000361.

Acknowledgements

To Don Nkwane and Hlumela Nkwelo for assisting with sourcing additional articles and refining the tables.

Financial support

The study was supported by resources of the South African National Biodiversity Institution (SANBI).

Competing interest

None.

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Figure 0

Figure 1. PRISMA diagram.

Figure 1

Table 1. Checklist of GIT nematode species and their hosts reported in sub-Saharan Africa (1980-2022)

Figure 2

Table 2. Checklist of GIT trematodes species and their hosts reported in sub-Saharan Africa (1980-2022)

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Table 3. Checklist of GIT cestodes species and their hosts reported in sub-Saharan Africa (1980-2022)

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Table 4. Prevalence of GIT nematode infections in wild ruminants in sub-Saharan Africa (1980-2022)

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Table 5. Prevalence of gastrointestinal tract trematode infections in wild ruminants in sub-Saharan African countries (1980-2022)

Figure 6

Table 6. Prevalence of cestode infections in sub-Saharan African wild ruminants (1980-2022)

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