Introduction
Nigeria is one of the four leading livestock producers in Sub-Saharan Africa (Aregheore, Reference Aregheore2009), contributing up to 12.7% of the total Nigerian agricultural gross domestic products (CBN, 1999). In the tropics, cattle are generally reared under transhumance husbandry systems with little supplementary feeding, resulting in low productivity and high pre-weaning mortality (Ulayi et al., Reference Ulayi, Umaru-Sule and Adamu2007). Also, acute shortage of feeds during the dry season remains a common occurrence, compelling these animals to graze around water bodies that are often heavily infested with potential intermediate hosts of trematode infections (Ulayi et al., Reference Ulayi, Umaru-Sule and Adamu2007).
Trematode infections of cattle, including fasciolosis (Babalola & Schillhorn van Veen, Reference Babalola and Schillhorn van Veen1976, Dipeolu et al., Reference Dipeolu, Dipeolu and Eruvbetine2000), paramphistomosis (Bogatko, Reference Bogatko1975), dicrocoeliasis (Schillhorn van Veen et al., Reference Schillhorn van Veen, Folaranmi, Usman and Ishaya1980; Ulayi et al., Reference Ulayi, Umaru-Sule and Adamu2007) and schistosomiasis (Pugh et al., Reference Pugh, Schillhorn Van Veen and Tayo1980; Ndifon et al., Reference Ndifon, Betterton and Rollinson1988) have all been reported in various parts of Nigeria. They are referred to as ‘digenetic’ because they require at least two different kinds of hosts for their full development. The first are the intermediate hosts of mollusc species (slugs, snails or shellfish) while the final hosts are vertebrates (Taylor, Reference Taylor1964). Mixed infection with more than one trematode species is a common occurrence in animals, due to similarities in life cycles. Fasciola infection has been reported to occur concurrently with Schistosoma and paramphistome species (Schillhorn van Veen et al., Reference Schillhorn van Veen, Folaranmi, Usman and Ishaya1980; Yabe et al., Reference Yabe, Phiri, Phiri, Chembensofu, Dorny and Vercruysse2008). It is also reported to occur concurrently with Dicrocoelium species (Schillhorn van Veen et al., Reference Schillhorn van Veen, Folaranmi, Usman and Ishaya1980; Ulayi et al., Reference Ulayi, Umaru-Sule and Adamu2007). Infection with trematode parasites can lead to severe losses to farmers, hence affecting sustainability of food production (Alvarez Rojas et al., Reference Alvarez Rojas, Jex, Gasser and Scheerlinck2014).
Fasciolosis, which is also referred to as distomatosis or liver-fluke disease, is a parasitic disease caused by the trematode of the genus Fasciola. The most important species are F. hepatica and F. gigantica, found in the temperate and tropical regions of the world, respectively. The geographical distribution of Fasciola species is determined by the distribution of the snail intermediate hosts (Boray, Reference Boray, Gaafar, Howard and Marsh1985). The temperate disease occurs in Europe, America and Oceania, while tropical fasciolosis is common in Africa, the Indian sub-continent, Central and South-East Asia, and other subtropical and tropical areas of the world (FAO, 1993). Both species overlap in many areas of Africa and Asia (Walker et al., Reference Walker, Makundi, Namuba, Kassuku, Keyyu, Hoey, Prodohl, Stothard and Trudgett2008). Adults of each species can occur concurrently in the same animal host, either because of local overlap or because of livestock movement (Mas-Coma et al., Reference Mas-Coma, Valero and Bargues2009). The two Fasciola species may thus interbreed, resulting in hybrid species (Agatsuma et al., Reference Agatsuma, Arakawa, Iwagami, Honzako, Cahyaningsih, Kang and Hong2000; Ashrafi et al., Reference Ashrafi, Valero, Panova, Periago, Massoud and Mas-Coma2006). They are hermaphrodites and are found in the bile ducts of a large number of herbivorous ruminants, equines, pigs and rabbits (FAO, 1993), and wild animals (Hammond, Reference Hammond1972). Humans are also suitable hosts (Boray, Reference Boray1969). The intermediate hosts of F. gigantica are true water snails belonging to the phylum Mollusca, class Gastropoda and subclass Pulmonata (Wright, Reference Wright1971). They belong to the family Lymnaedae and super species Lymnaea (Radix) auricularia sensu lato.
Paramphistomes Fischoeder 1901, also known as rumen flukes, are gastrointestinal trematodes belonging to the family of Paramphistomatidae (Soulsby, Reference Soulsby1982). These are conically shaped flukes measuring 5–12 mm × 2–4 mm. The adults' predilection sites are the rumen and reticulum of ruminants while the immature parasites are found in the small intestines and abomasum (Rojo-Vázquez et al., Reference Rojo-Vázquez, Meana, Valcárcel and Martínez-Valladares2012). Snails of the families Planorbidae, Bulinidae and Lymnaeidae act as intermediate hosts (Soulsby, Reference Soulsby1982; Castro-Trejo et al., Reference Castro-Trejo, García-Vasquez and Casildo-Nieto1990). They are largely non-pathogenic but clinical outbreaks have been reported to occur. The most important species in Africa is Paramphistomum microbothrium (Dinnik, Reference Dinnik1964). Others are Paramphistomum cervi (European Environment Agency, 2004), Paramphistomum ichikawar (Australasia) (FAO, 1993) and Paramphistomum daubneyi (first described in Kenya and common in Europe) (Abrous et al., Reference Abrous, Rondelaud and Dreyfuss1996). Recently, there have been reports of an increasing number of cases of rumen flukes, identified mainly as Calicophoron daubneyi, in cattle and sheep in the Republic of Ireland (Zintl et al., Reference Zintl, Garcia-Campos, Trudgett, Chryssafidis, Talavera-Arce, Fu, Egan, Lawlor, Negredo, Brennan, Hanna, De Waal and Mulcahy2014; Toolan et al., Reference Toolan, Mitchell, Searle, Sheehan, Skuce and Zadoks2015). The adult paramphistomes are regarded as commensals in the rumen, as heavy infections are tolerated without causing any damage to the rumen (Dinnik, Reference Dinnik1964), although immature parasites in the small intestine cause clinical disease (Aiello, Reference Aiello1998).
Dicrocoelium species, commonly referred to as lancet flukes, are found in the bile duct of domestic and wild ruminants (Otranto & Traversa, Reference Otranto and Traversa2002; Taylor et al., Reference Taylor, Coop and Wall2007). Other animals, such as rabbits, pigs, dogs, horses and humans, can also be infected (Rojo-Vázquez et al., Reference Rojo-Vázquez, Meana, Valcárcel and Martínez-Valladares2012). There are several species, with D. dendriticum (Otranto et al., Reference Otranto, Rehbein, Weigl, Cantacessi, Parisi, Lia and Olson2007) having the widest distribution worldwide while D. hospes is common in Africa (Aiello, Reference Aiello1998). Other species are D. chinensis and D. suppereri (Rojo-Vázquez et al., Reference Rojo-Vázquez, Meana, Valcárcel and Martínez-Valladares2012). Two intermediate hosts are required. The first intermediate host is a terrestrial snail of the genus Limicolaria, while the second intermediate hosts are brown ants of the genus Formica (Soulsby, Reference Soulsby1982).
Schistosoma species are elongate, unisexual trematodes, commonly referred to as blood flukes and widely distributed throughout Africa, the Middle East, Asia and some Mediterranean countries (Soulsby, Reference Soulsby1982). They are found in the blood vessels, such as the portal, mesenteric and intestinal veins, of domestic animals (Aiello, Reference Aiello1998). The species, Schistosoma matteei and S. bovis are common in Africa, the Middle East and southern Europe (Vercruysse & Gabriel, Reference Vercruysse and Gabriel2005; Taylor et al., Reference Taylor, Coop and Wall2007). Schistosoma bovis is the most pathogenic in animals in Africa (Vercruysse & Gabriel, Reference Vercruysse and Gabriel2005). It occurs in the portal and mesenteric vessels of cattle, sheep and goats. It is similar to the human parasite S. haematobium (Soulsby, Reference Soulsby1982). Schistosoma matteei has also been reported in sporadic human infections. Other African species in ruminants include S. curassoni (common in western Africa), S. margrebowiei and S. leiperi. In Asia, S. spindale, S. nasale (nasal worm), S. indicum, S. incognitum and S. japonicum are zoonotic in the Far East (De Bont & Vercruysse, Reference De Bont and Vercruysse1997). Aquatic snails such as Bulinus, Physopsis, Oncomelania, Lymnaea and Indoplanorbis act as the intermediate hosts (Taylor et al., Reference Taylor, Coop and Wall2007).
This review aims at describing the current status of bovine fasciolosis and other trematode infections in Nigeria and surrounding African countries, in relation to economic losses, distribution, molecular studies, control strategies and human infections. Data were collected from publications obtained from an online search as well as local national journals. Bovine fasciolosis reported in the literature across different states of Nigeria were mapped by using QGIS® software v2.12 (Lyon, France).
Economic losses from trematode infections
Tropical fasciolosis caused by Fasciola gigantica is regarded as one of the most important single helminth infections of ruminants in Asia and Africa (Boray, Reference Boray, Gaafar, Howard and Marsh1985; Fabiyi, Reference Fabiyi1987). Economic losses from fasciolosis are often difficult to estimate and may result directly from increased liver condemnation or indirectly from decreased livestock productivity (Taylor, Reference Taylor1964). Although direct losses are easier to measure, indirect losses are considered to be far more economically important (Kaplan, Reference Kaplan2001). With the total cattle population in Africa estimated at 201 million animals, an annual loss of about US$840 million from fasciolosis infection is predicted (Spithill et al., Reference Spithill, Smooker, Copeman and Dalton1999), but this cost is likely to have increased significantly in the past 18 years. Production losses in cattle infected with liver flukes often take the form of reduced milk production in dairy cattle and poor feed conversion in beef cattle (Armstrong, Reference Armstrong1982). A linear relationship between the burden of adult F. gigantica and weight gain of cattle has been described, with infected animals gaining only about half the annual weight compared to controls (Sewell, Reference Sewell1966). The amount of weight loss may also, however, be dependent on age, level of nutrition and intensity of infection (Spithill et al., Reference Spithill, Smooker, Copeman and Dalton1999). Other clinical manifestations are anaemia, reduced fertility and reduced work capacity (Hillyer, Reference Hillyer2005), and where there is massive infection with immature parasites, sudden death could occur and lead to serious economic losses (Torgerson & Claxton, Reference Torgerson, Claxton and Dalton1999; Rojo-Vázquez et al., Reference Rojo-Vázquez, Meana, Valcárcel and Martínez-Valladares2012).
Severe infection with immature paramphistomes can cause great economic losses due to reduced weight gain and decrease in milk production (Horak, Reference Horak1971). Paramphistomosis has been reported to cause between 30 and 40% mortality in cattle and sheep. These deaths may result from anaemia, hypo-proteinaemia, profuse diarrhoea and marked emaciation (Soulsby, Reference Soulsby1982), and a decrease in milk yield in dairy cattle (Spence et al., Reference Spence, Fraser and Chang1996).
Economic losses from dicrocoeliasis are less apparent compared to those from other trematode infections and are difficult to quantify, due to concurrent infection with other gastrointestinal parasites. This may also be largely due to the asymptomatic nature of the disease (Otranto & Traversa, Reference Otranto and Traversa2003). Clinical signs are mostly absent, but losses occur mainly from liver condemnation due to fibrosis of bile ducts and cirrhosis (Taylor et al., Reference Taylor, Coop and Wall2007).
An abattoir survey to determine the prevalence and species of cattle schistosomiasis in Zambia revealed an overall prevalence of 51%, with 93% of the infected animals having up to 100 worm pairs in the mesenteric veins; S. mattheei was the predominant species (75%); while S. leiperi (12%) and S. margrebowiei (2%) were also reported (De Bont et al., Reference De Bont, Vercruysse, Southgate, Rollinson and Kaukas1994). Schistosomiasis due to S. bovis has also been reported with a prevalence rate of 4.8% in Tanzania (Nzalawahe et al., Reference Nzalawahe, Kassuku, Stothard, Coles and Eisler2015). These parasites cause economic losses due to their long-term effect on growth and productivity, and also due to increased susceptibility to other parasitic and bacterial diseases (De Bont & Vercruysse, Reference De Bont and Vercruysse1998). The clinical signs associated with the intestinal and hepatic form of disease in ruminants are haemorrhagic enteritis, haematuria, anaemia and loss of weight, with death within a few months of the disease. Nasal schistosomiasis, on the other hand, is a chronic disease that causes coryza and dyspnoea in infected animals (Aiello, Reference Aiello1998). Production losses reported due to schistosomiasis in cattle are attributed mainly to losses occurring in animals aged between 6 and 30 months, and are due to reduced weight gain, liver condemnation, poor future reproductive performance and death (McCauley et al., Reference McCauley, Majid and Tayeb1984). Also, approximately 165 million cattle are likely to be infected with Schistosoma species worldwide (De Bont et al., Reference De Bont, Vercruysse, Southgate, Rollinson and Kaukas1994).
Many trematode infections are also zoonotic, and thus a public health concern (Wolfe, Reference Wolfe1966; Chen & Mott, Reference Chen and Mott1990; Mas-Coma et al., Reference Mas-Coma, Bargues and Valero2005). The World Health Organization has estimated that about 56 million people worldwide are infected by at least one zoonotic trematode species (Furst et al., Reference Furst, Keiser and Utzinger2012) and up to 750 million people are at risk of infection (Keiser & Utzinger, Reference Keiser and Utzinger2009). It has been suggested that recent environmental changes associated with global warming, which favours the development of snail intermediate hosts, contribute to an increase in disease outbreaks (Mitchell, Reference Mitchell2002).
Epidemiology of bovine fasciolosis in Nigeria
Tropical fasciolosis due to F. gigantica Cobbold 1855 has been reported in several parts of Africa (Schillhorn van Veen, Reference Schillhorn van Veen1980; Phiri et al., Reference Phiri, Phiri, Sikasunge and Monrad2005a; Abebe et al., Reference Abebe, Abunna, Berhane, Mekuria, Megersa and Regassa2010; Nzalawahe et al., Reference Nzalawahe, Kassuku, Stothard, Coles and Eisler2014) and is likely to be a problem throughout the continent. The two species of Fasciola – F. gigantica and F. hepatica – and their respective snail intermediate hosts have both been reported in Africa. Fasciolosis is endemic in Nigeria and is of great economic importance (Ogunrinade & Ogunrinade, Reference Ogunrinade and Ogunrinade1980). The disease has been reported with varying prevalence across the country and is one of the most common causes of liver condemnation in abattoirs. The prevalence distribution of bovine fasciolosis is mapped (fig. 1) according to available data published between 1980 and 2016 (Schillhorn van Veen, Reference Schillhorn van Veen1980, Nwosu & Srivastava, Reference Nwosu and Srivastava1993; Ngwu et al., Reference Ngwu, Ohaegbula and Okafor2004; Opara, Reference Opara2005; Ekwunife & Eneanya, Reference Ekwunife and Eneanya2006; Adedokun et al., Reference Adedokun, Ayinmode and Fagbemi2008; Umar et al., Reference Umar, Nwosu and Philip2009; Ibironke & Fasina, Reference Ibironke and Fasina2010; Sugun et al., Reference Sugun, Ehizibolo, Ogo, Timothy and Ngulukun2010; Gboeloh, Reference Gboeloh2012; Omoleye, Reference Omoleye, Qasim, Olugbon, Adu, Adam and Joachim2012; Odigie & Odigie, Reference Odigie and Odigie2013; Abraham & Jude, Reference Abraham and Jude2014; Ardo et al., Reference Ardo, Aliyara and Lawal2014; Magaji et al., Reference Magaji, Ibrahim, Salihu, Saulawa, Mohammed and Musawa2014; Ngele & Ibe, Reference Ngele and Ibe2014; Onyeabor, Reference Onyeabor2014; Yahaya & Tyav, Reference Yahaya and Tyav2014; Ejeh et al., Reference Ejeh, Paul, Lawan, Lawal, Ejeh and Hambali2015; Elelu et al., Reference Elelu, Ambali, Coles and Eisler2016). The high prevalence rate from liver condemnation in a 3-year period reported in Lagos State (Ibironke & Fasina, Reference Ibironke and Fasina2010) can be explained by the fact that this State is the commercial nerve centre of Nigeria, with a very large human population, and many cattle from all over the country are often slaughtered at the abattoir.
Fig. 1. Geographical distribution of bovine fasciolosis across different states of Nigeria (1980–2016) from published prevalence data (%) based on abattoir records, liver and coprological examination. States with 0% had no available data at the time of review.
Cattle total losses from Fasciola infection alone in Nigeria have been estimated to cost £32.5 million (Fabiyi & Adeleye, Reference Fabiyi and Adeleye1982). A survey of abattoirs in Nigeria showed that about 70% of organ condemnation, mainly of livers, was due to fasciolosis (Alonge & Fasanmi, Reference Alonge and Fasanmi1979). A recent study reported up to 88.1% liver condemnation due to liver flukes alone in Lagos abattoir (Ibironke & Fasina, Reference Ibironke and Fasina2010). These studies are in agreement with a 3-year abattoir study in south-western Nigeria in which losses from liver condemnation were estimated at US$134,000 (Ibironke & Fasina, Reference Ibironke and Fasina2010). These data translate into huge economic losses from cumulative condemnation across the country.
Acute fasciolosis due to the migration of juvenile flukes is rare in cattle; however, a few cases have been reported in Nigeria. For example, on a dairy farm in north-central Nigeria, a pregnant cow was reported to have died during parturition, where post-mortem examination revealed inflammatory lesions and fibrosis due to fasciolosis (Okaiyeto et al., Reference Okaiyeto, Salami, Danbirni, Allam and Onoja2012). The chronic form of the disease is the most common in cattle in Nigeria (Ogunrinade & Adegoke, Reference Ogunrinade and Adegoke1982) and it occurs when small numbers of flukes finally enter the bile duct and infection becomes patent. This results in a chronic wasting disease from slow acquisition of liver flukes for months or even years. The normal tissues of the liver are replaced by fibrous tissues, with hyperplastic cholangitis and macroscopically visible calcification of the bile ducts, giving rise to so-called ‘pipe-stem liver’ (Soulsby, Reference Soulsby1982; Taylor et al., Reference Taylor, Coop and Wall2007). Clinically, the condition is characterized by weight loss, anaemia and oedema at the jaw (bottle jaw), thoracic and lower abdominal regions (Radostits et al., Reference Radostits, Gay, Blood and Hinchcliff2000, Mitchell, Reference Mitchell2002, Taylor et al., Reference Taylor, Coop and Wall2007; Rojo-Vázquez et al., Reference Rojo-Vázquez, Meana, Valcárcel and Martínez-Valladares2012).
Factors influencing outbreaks of bovine fasciolosis
Season of the year
There are varying reports on the seasonal infection rates of F. gigantica across Nigeria. The majority of studies reported high infection rates at the beginning of the dry season (Schillhorn van Veen et al., Reference Schillhorn van Veen, Folaranmi, Usman and Ishaya1980; Umar et al., Reference Umar, Nwosu and Philip2009), which is in agreement with studies in other parts of Africa, such as Zambia, where bovine fasciolosis was also reported, with higher fluke abundance reported in the post-rainy season (Phiri et al., Reference Phiri, Phiri, Siziya, Sikasunge, Chembensofu and Monrad2005b). Similar observations were made in Zimbabwe, where Fasciola faecal egg counts were reported to follow a seasonal variation, with an increase during the end of the dry season and highest liver condemnation reported during the rainy season (reviewed by Pfukenyi et al., Reference Pfukenyi, Monrad and Mukaratirwa2005). However, another study carried out in the southern part of Nigeria reported an all-year occurrence of infection (Gboeloh, Reference Gboeloh2012). This all-year occurrence in the south was attributed to the favourable climatic condition (warm and humid), which favours development of parasites and the increase in the density of snail intermediate hosts (Gboeloh, Reference Gboeloh2012). The climatic conditions in southern Nigeria could be likened to those of highland areas of Iringa, Tanzania (Nzalawahe et al., Reference Nzalawahe, Kassuku, Stothard, Coles and Eisler2015) and Zimbabwe (Pfukenyi et al., Reference Pfukenyi, Mukaratirwa, Willingham and Monrad2006a), where wet/swampy grazing areas reportedly favour the availability and distribution of the snail intermediate host. In addition, a recent study in Tanzania has associated trematode infections, including Fasciola, with irrigation practices during the dry season that favour growth of intermediate snail hosts and development of trematode larval stages (Nzalawahe et al., Reference Nzalawahe, Kassuku, Stothard, Coles and Eisler2014).
Type of management system
The type of management system has been shown to influence significantly the prevalence of Fasciola infection (Keyyu et al., Reference Keyyu, Monrad, Kyvsgaard and Kassuku2005). A low prevalence rate was also reported to occur in cattle reared by a sedentary husbandry system in Lake Chad area (Jean-Richard et al., Reference Jean-Richard, Crump, Abicho, Naré, Greter, Hattendorf, Schelling and Zinsstag2014). While a high prevalence rate of 54.3% has been reported in cattle managed extensively in south-western Nigeria (Adediran et al., Reference Adediran, Adebiyi and Uwalaka2014), this is not surprising, because the cattle come into contact with a snail-infected habitat during extensive communal grazing. In contrast, under intensive management systems, metacercaria-free water and herbage can be supplied to the cattle, thereby minimizing the likelihood of outbreaks of fasciolosis.
Age of cattle
In a recent study from Nigeria, F. gigantica infection was reported to be higher in adult cattle than weaners (Elelu et al., Reference Elelu, Ambali, Coles and Eisler2016). This is in agreement with past studies in Africa with similar findings (Pfukenyi et al., Reference Pfukenyi, Mukaratirwa, Willingham and Monrad2006a; Nzalawahe et al., Reference Nzalawahe, Kassuku, Stothard, Coles and Eisler2014). The difference in prevalence within age group was attributed to a longer length of exposure to the infection in adults compared to weaners (Pfukenyi et al., Reference Pfukenyi, Monrad and Mukaratirwa2005; Nzalawahe et al., Reference Nzalawahe, Kassuku, Stothard, Coles and Eisler2014). It was also concluded that adult cattle act as a constant source of F. gigantica infection for the more susceptible young animals (Pfukenyi et al., Reference Pfukenyi, Monrad and Mukaratirwa2005).
Distribution of the snail intermediate host
The intermediate snail host Lymnaea (Radix) natalensis, which is widespread throughout Africa, is also widely distributed in Nigeria, although its occurrence is restricted to permanent water bodies (Ndifon & Ukoli, Reference Ndifon and Ukoli1989). Lymnaea is fairly common in regions with rainfall over 1000 mm (Schillhorn van Veen, Reference Schillhorn van Veen1980) and it tolerates relatively high temperatures (Njoku-Tony, Reference Njoku-Tony2011) consistent with tropical climates. In Uganda, L. (Radix) natalensis, the intermediate snail host of F. gigantica, is the vector commonly found abundantly at lower altitudes below 1800 m, while Galba truncatula (intermediate snail host of F. hepatica) was found only at altitudes above 3000 m (Howell et al., Reference Howell, Mugisha, Davies, Lacourse, Claridge, Williams, Kelly-Hope, Betson, Kabatereine and Stothard2012). The presence of the two vectors indicates the possibility of the two Fasciola parasites in Uganda. Other countries in Africa have reported the presence of the two species of Fasciola (Yilma & Mesfin, Reference Yilma and Mesfin2000; Walker et al., Reference Walker, Makundi, Namuba, Kassuku, Keyyu, Hoey, Prodohl, Stothard and Trudgett2008; Sisay & Nibret, Reference Sisay and Nibret2013). To date, the authors of this review are not aware of any report of G. truncatula in Nigeria, although specific studies to identify these species in areas of high altitude might be worthwhile.
In Nigeria, during the wet season, many of the developing Lymnaea snails are washed away in torrential streams after heavy rain and this may be important in the spread of Fasciola (Schillhorn van Veen, Reference Schillhorn van Veen1980). Snails were also reported to be more abundant during the beginning of the dry season, to reach a climax in the middle of the dry season, but to decrease towards the end of the dry season when most streams and pools dry up (Schillhorn van Veen, Reference Schillhorn van Veen1980). This is supported by a field study in south-western Nigeria showing that dry-season conditions favour snails, and this was said to be due to low turbidity, reduced currents and substantial growths of algae and macrophytes (Ndifon & Ukoli, Reference Ndifon and Ukoli1989). In the sub-tropical and tropical countries with distinct wet and dry seasons, optimal development of fluke eggs to miracidia occurs at the start of the wet season and development within the snail is complete by the end of the rains (Taylor et al., Reference Taylor, Coop and Wall2007). The dry season therefore coincides with the snail shedding of cercaria and more animals grazing closer to streams and ponds, thereby predisposing them to infection. Herdsmen migrate in search of water and grazing during the dry season, and thousands of cattle often converge on the few ponds that fail to dry up (Ikeme & Obioha, Reference Ikeme and Obioha1973).
Diagnosis of bovine fasciolosis
The most common method of diagnosis is by faecal egg counts and pathological lesions in the liver during abattoir examination. Serological diagnostic methods to detect antibodies, such as indirect enzyme-linked immunosorbent assay (ELISA) (Damwesh & Ardo, Reference Damwesh and Ardo2013; Aliyu et al., Reference Aliyu, Ajogi, Ajanusi and Reuben2014) and direct ELISA (Fagbemi et al., Reference Fagbemi, Aderibigbe and Guobadia1997), have been carried out in Nigeria. Testing for precipitating antibodies using the Agar Gel Precipitation Test (AGPT) is another method of diagnosis (Adedokun et al., Reference Adedokun, Ayinmode and Fagbemi2008). Comparatively, this method has been shown to detect more positive cases than faecal and bile egg counts (Adedokun et al., Reference Adedokun, Ayinmode and Fagbemi2008). In Kwara State, north-central Nigeria, a survey of cattle for fasciolosis revealed higher prevalence rates from faecal analysis compared to a previous abattoir study that utilized liver examination. This further showed the lack of sensitivity of the abattoir method of diagnosis, as positive samples are likely to be lost (Elelu et al., Reference Elelu, Ambali, Coles and Eisler2016).
Epidemiology of bovine paramphistomosis in Nigeria
Rumen flukes are paramphistome parasites commonly seen in the abattoir in Nigeria (Bunza et al., Reference Bunza, Ahmad and Fana2008). The snail vector of the disease (Lymnaea, Planorbis and Bulinus) has also been reported in Nigeria (Ndifon & Ukoli, Reference Ndifon and Ukoli1989; Brown & Kristensen, Reference Brown and Kristensen1993). The species reported to occur in Nigerian domestic livestock include P. microbothrium, Carmyerius gregarious, Carmyerius spatiosus, Cotylophorum cotylophorum (Schillhorn van Veen et al., Reference Schillhorn van Veen, Shonekan and Fabiyi1975) and P. cervi (Bogatko, Reference Bogatko1975). Other species recovered from Nigerian cattle are Ceylonocotyle dicranocoelium, Bothriophoron bothriophoron, Calicophoron calicophorum and Calicophoron microbothrioides (Dube et al., Reference Dube, Onyedineke and Aisien2013).
Prevalence rates of 2.2% (Edosomwan & Shoyemi, Reference Edosomwan and Shoyemi2012); 18.8% (Nwigwe et al., Reference Nwigwe, Njoku, Odikamnoro and Uhuo2013) and 16.1% (Elelu et al., Reference Elelu, Ambali, Coles and Eisler2016) have been reported for paramphistomes in past studies in Nigeria. A higher prevalence rate of 41.67% for P. cervi was reported in another abattoir study in northern Nigeria (Nnabuife et al., Reference Nnabuife, Dakul, Dogo, Egwu, Weka, Ogo, Onovoh and Obaloto2013). Similarly, also in northern Nigeria, a high paramphistome prevalence rate of up to 56.0% in slaughtered cattle has been reported in a study area around a marshy river valley. The grazing land associated with this river valley provides suitable breeding sites for snail intermediate hosts of the parasites (Bunza et al., Reference Bunza, Ahmad and Fana2008). The convergence of cattle in common grazing land during the dry season, as well as irrigation practices, have been implicated in the high prevalence of paramphistomosis (Nzalawahe et al., Reference Nzalawahe, Kassuku, Stothard, Coles and Eisler2014). In a cross-sectional study in Ethiopia, 51.8% of slaughtered cattle were positive for paramphistomosis, with peak prevalence rates observed during October to November (Ayalew et al., Reference Ayalew, Tilahun, Aylate, Teshale and Getachew2016). Although adult cattle were more likely to be infected with paramphistomes because they are more likely to be infected when taken out for grazing, several studies have shown that there is no statistically significant difference in paramphistome infection between age groups of cattle (Titi et al., Reference Titi, Mekroud, Sedraoui, Vignoles and Rondelaud2010; Khedri et al., Reference Khedri, Radfar, Borji and Mirzaei2015; Ayalew et al., Reference Ayalew, Tilahun, Aylate, Teshale and Getachew2016).
Epidemiology of bovine dicrocoeliasis in Nigeria
There are records of Dicrocoelium hospes infection in cattle in Nigeria (Nwosu & Srivastava, Reference Nwosu and Srivastava1993; Ulayi et al., Reference Ulayi, Umaru-Sule and Adamu2007), and snail species of Limicolaria flammea have been shown experimentally to be a suitable intermediate host of the disease (Fashuyi & Adeoye, Reference Fashuyi and Adeoye1986). The majority of prevalence data are based on abattoir surveys (FAO, 1992). Studies carried out in Zaria abattoir, northern Nigeria recorded high prevalence rates of 56.0% (Schillhorn van Veen et al., Reference Schillhorn van Veen, Folaranmi, Usman and Ishaya1980) and 35.4% (Ulayi et al., Reference Ulayi, Umaru-Sule and Adamu2007) for D. hospes from cattle. A low prevalence rate of 18.3% was reported in Borno State (Nwosu & Srivastava, Reference Nwosu and Srivastava1993), and 22.33% in Plateau State in the bile duct of cattle (Omowaye et al., Reference Omowaye, Idachaba and Falola2012). Seasonal infection rates have also been reported for of D. hospes in Nigeria, with the highest rate occurring during and directly after the rainy season (Schillhorn van Veen et al., Reference Schillhorn van Veen, Folaranmi, Usman and Ishaya1980).
Epidemiology of bovine schistosomiasis in Nigeria
Schistosoma curassoni and S. bovis have been reported in cattle in Nigeria (Ndifon et al., Reference Ndifon, Betterton and Rollinson1988; Elelu et al., Reference Elelu, Ambali, Coles and Eisler2016). The intermediate snail host (Bulinus globosus) of Schistosoma species is present in Nigeria (Ndifon & Ukoli, Reference Ndifon and Ukoli1989) and has been experimentally infected with S. bovis miracidia originating from a Nigerian cow (Ndifon et al., Reference Ndifon, Betterton and Rollinson1988). The transmission of S. mattheei has been reported, with occurrence throughout the year and with high prevalence during the wet months (Pfukenyi et al., Reference Pfukenyi, Monrad and Mukaratirwa2005). The prevalence rates reported in Nigeria were 7.8% for S. bovis and 2.2% for S. curassoni, based on examination of rectal scrapings; however, a higher prevalence of 31.1% (including both species of Schistosoma) was observed in 502 slaughtered cattle by examination of mesenteric and rectal veins (Ndifon et al., Reference Ndifon, Betterton and Rollinson1988). In another study that utilized a more sensitive ELISA technique, a higher prevalence rate (16.2%) was recorded in cattle of the Kuri breed compared with other breeds (Hambali et al., Reference Hambali, Adamu, Ahmed, Bokko, Mbaya, Tijjani, Biu, Jesse and Ambali2016). This is not surprising as this breed of cattle, with their characteristic bulbous horns, is adapted to swimming; they are therefore more likely to come in contact with Schistosoma-infected water. Schistosomiasis is transmitted via active skin penetration during contact with water. Other studies carried out in parts of north-western Ethiopia, located close to swampy areas, reported higher prevalence rates of up to 24% in cattle (Lulie & Guadu, Reference Lulie and Guadu2014). In addition, a significantly higher schistosomiasis prevalence was observed in the wet season compared to the dry season in cattle in Zimbabwe (Pfukenyi et al., Reference Pfukenyi, Mukaratirwa, Willingham and Monrad2006b). A higher prevalence rate (25.2%) has also been reported in cattle managed extensively compared to those under a semi-intensive management system (15.38%) (Lulie & Guadu, Reference Lulie and Guadu2014).
Molecular identification of trematode species
Several polymerase chain reaction (PCR)-based techniques have been used to identify digenetic trematodes (Lotfy et al., Reference Lotfy, Brant, Dejong, Le, Demiaszkiewicz, Rajapakse, Perera, Laursen and Loker2008, Reference Lotfy, Brant, Ashmawy, Devkota, Mkoji and Loker2010). Molecular identification has an important contribution to make in many areas where there are problems associated with definitive speciation. These areas include instances of species overlap as seen in Fasciola (Kendall, Reference Kendall1965); the existence of hybrids between different genotypes, the Japanese triploid forms for example (Itagaki & Tsutsumi, Reference Itagaki and Tsutsumi1998); the identification of sexually immature paramphistome species (Horak, Reference Horak1971); and difficulty in speciation based on morphology of parasite eggs (Itagaki et al., Reference Itagaki, Tsumagari, Tsutsumi and Chinone2003). Other reasons for molecular identification are the close relatedness between taxa, as seen between S. haematobium and S. bovis (human and animal parasites), as well as difficulty in cercarial identification (Webster et al., Reference Webster, Rollinson, Stothard and Huyse2010).
Molecular studies by analysis of the first (ITS1) and second (ITS2) internally transcribed spacer of the ribosomal rDNA and the mitochondrial cytochrome c oxidase I (COI) gene have been carried out for Fasciola (Mas-Coma et al., Reference Mas-Coma, Bargues and Valero2005; Ali et al., Reference Ali, Ai, Song, Ali, Lin, Seyni, Issa and Zhu2008; Amer et al., Reference Amer, Dar, Ichikawa, Fukuda, Tada, Itagaki and Nakai2011; Amor et al., Reference Amor, Farjallah, Salem, Lamine, Merella, Said and Ben Slimane2011), paramphistome (Lotfy et al., Reference Lotfy, Brant, Ashmawy, Devkota, Mkoji and Loker2010) and Dicrocoelium (Otranto et al., Reference Otranto, Rehbein, Weigl, Cantacessi, Parisi, Lia and Olson2007). ITS-1 and ITS-2 are highly conserved and useful for differentiating closely related taxa that have diverged relatively recently (<50 million years ago) (Mas-Coma & Bargues, Reference Mas-Coma and Bargues2009). The mitochondrial NADH dehydrogenase subunit 1 and COI were used recently to characterize F. gigantica from Nigeria (Ichikawa-Seki et al., Reference Ichikawa-Seki, Tokashiki, Opara, Iroh, Hayashi, Kumar and Itagaki2017). However, further molecular studies from different parts of Nigeria are recommended in order to understand these important pathogens.
Other genetic methods, such as the use of restriction fragment length polymorphism (PCR-RFLP) of ribosomal or mitochondrial genes using common restriction enzymes (such as AvaII and DraII), have been used to analyse the whole of mitochondrial DNA to distinguish Fasciola species (Marcilla et al., Reference Marcilla, Bargues and Mas-Coma2002), to identify species of paramphistomes (Itagaki et al., Reference Itagaki, Tsumagari, Tsutsumi and Chinone2003), to study genetic variability of Dicrocoelium species (Sandoval et al., Reference Sandoval, Manga-González, Campo, García, Castro and De La Vega1999), and also to distinguish between S. haematobium and S. bovis (Barber et al., Reference Barber, Mkoji and Loker2000; Webster et al., Reference Webster, Rollinson, Stothard and Huyse2010).
A PCR technique has also been used to detect the F. gigantica infection status of snail intermediate hosts (Velusamy et al., Reference Velusamy, Singh and Raina2004; Kaset et al., Reference Kaset, Eursitthichai, Vichasri-Grams, Viyanant and Grams2010). A PCR technique used to amplify specific fragments of mitochondrial DNA in faecal samples of sheep has shown promise in the early detection of F. hepatica infection (Martínez-Pérez et al., Reference Martínez-Pérez, Robles-Pérez, Rojo-Vázquez and Martínez-Valladares2012). Molecular identification of paramphistome species from Asia and elsewhere in Africa has been carried out (Lotfy et al., Reference Lotfy, Brant, Ashmawy, Devkota, Mkoji and Loker2010); however, at time of writing this review, there are no records of such studies having been carried out in Nigeria. However, PCR to amplify species-specific genes has been used in differentiating human species of Schistosoma in Nigeria (Akinwale et al., Reference Akinwale, Hock, Chia-Kwung, Zheng, Haimo, Ezeh and Gyang2014) and also to identify S. bovis in Kenya (Kamanja et al., Reference Kamanja, Githigia, Muchemi and Mwandawiro2011).
Control strategies for trematode infections
The principles behind the control of trematode infections are similar for all species (FAO, 1993). Conventional methods for control include strategic anthelmintic treatment to reduce environmental contamination (FAO, 1993), snail eradication by use of molluscicides and improved drainage systems to adversely influence the snail habitats (Armour, Reference Armour1975; De Bont & Vercruysse, Reference De Bont and Vercruysse1997). The current control of F. hepatica in cattle in temperate regions where the disease is prevalent is often based on strategically timed flukicide treatment, which is determined by studying the seasonal transmission dynamics in numerous locations throughout the world (Kaplan, Reference Kaplan2001). The tropical trematode infection caused by F. gigantica may be less amenable to this approach because the intermediate hosts L. (Radix) natalensis are true water snails (Sewell, Reference Sewell1966) and cattle can come into contact with infected snails while grazing around water bodies throughout the year. Control of Dicrocoelium infection is more difficult due to the complex life cycle, involving terrestrial intermediate hosts. Control is therefore based on chemotherapy and husbandry practices (avoiding grazing during early morning and late evening to avoid infective ants) (Otranto & Traversa, Reference Otranto and Traversa2002).
Strategic chemotherapy
Strategic anthelmintic treatment based on epidemiological and meteorological data is important for the control of flukes (FAO, 1993). There are several drugs for the treatment of fasciolosis. These include: halogenated phenol (niclofolan, bithionol, hexachlorophene and nitroxynil), salicylanides (rafoxanide, oxyclozanide and closantel), benzimidazoles (triclabendazole and albendazole), sulphonamides (clorsulon) and phenoxyalkanes (diamphenethides) (Fairweather & Boray, Reference Fairweather and Boray1999a). Triclabendazole has been the preferred drug for treating liver flukes since 1983, due to its high efficacy against early immature, immature and adult flukes (Boray et al., Reference Boray, Crowfoot, Strong, Allison, Schellenbaum, Von Orelli and Sarasin1983). These drugs differ in their effectiveness against adults and immature flukes. Strategic antihelminthic use at 12- to 13-week intervals is effective against both mature and immature flukes and reduces the intensity of infection over time. Suggestions for strategic antihelminthic treatments have been suggested: in the tropics, with fasciolosis outbreaks all year round, treatment up to four times per year is recommended (Torgerson & Claxton, Reference Torgerson, Claxton and Dalton1999). In Nigeria, some parts have reported seasonal trends in fasciolosis, while some southern parts of the country have reported an all-year-round occurrence (Gboeloh, Reference Gboeloh2012). Some authorities recommend that cattle should be dewormed regularly (Aliyu et al., Reference Aliyu, Ajogi, Ajanusi and Reuben2014), while others recommend treatment upon onset of clinical fasciolosis. Damwesh & Ardo (Reference Damwesh and Ardo2015) proposed 2–3 annual treatments: at the start of the rainy season, mid rainy season and at the start of the dry season.
The anthelminthic drugs currently in use in Nigeria include albendazole, nitroxynil, closulon and levamisole. However, a search in the available literature revealed that the preferred drug of choice against Fasciola (triclabendazole) is currently not available for use in Nigeria.
Neither triclabendazole nor niclofolan have been found to be effective against Dicrocoelium and paramphistome species (Güralp & Tinar, Reference Güralp and Tinar1984). The drugs of choice for paramphistome infection are resorantel, oxyclozanide and the combination of bithional and levamisole (Aiello, Reference Aiello1998). A combination of oxyclozanide and levamisole is most effective against paramphistomosis in cattle, given in two treatments 3 days apart (Rolfe & Boray, Reference Rolfe and Boray1987). Strategic treatment during the dry season may reduce contamination of the snails' habitat in the following rainy season (Rolfe et al., Reference Rolfe, Boray, Nichols and Collins1991).
Benzimidazoles (except triclabendazole) and pro-benzimidazoles (thiophanate, netobimin) at higher doses are effective against Dicrocoelium species (Otranto & Traversa, Reference Otranto and Traversa2002). Praziquantel is highly effective against all bovine visceral schistosomiasis (De Bont & Vercruysse, Reference De Bont and Vercruysse1997) but is advised only in severe outbreaks due to the risk of portal occlusion from heavy worm burdens (McCully & Kruger, Reference McCully and Kruger1969). A combination of praziquantel and artemether is also effective against mature and immature schistosomes (Pfunkenyi et al., Reference Pfukenyi, Monrad and Mukaratirwa2005).
Anthelmintic drug resistance
Resistance of parasites to anthelmintic drugs is a growing global problem (Wanyangu et al., Reference Wanyangu, Bain, Rugutt, Nginyi and Mugambi1996). Anthelmintic drug resistance is a real problem in the UK (Gordon et al., Reference Gordon, Zadoks, Stevenson, Sargison and Skuce2012) and Australia (Brockwell et al., Reference Brockwell, Elliott, Anderson, Stanton, Spithill and Sangster2014), and has also been reported in humans in The Netherlands (Winkelhagen et al., Reference Winkelhagen, Mank, De Vries and Soetekouw2012). Anthelmintic resistance has been demonstrated using faecal egg count reduction (Coles et al., Reference Coles, Bauer, Borgsteede, Geerts, Klei, Taylor and Waller1992), copro-antigen reduction tests (Brockwell et al., Reference Brockwell, Elliott, Anderson, Stanton, Spithill and Sangster2014) and egg-hatch assay (Fairweather et al., Reference Fairweather, McShane, Shaw, Ellison, O'Hagan, York, Trudgett and Brennan2012). Demonstration of resistance to triclabendazole (also the drug of choice in human fasciolosis) against immature and adult Fasciola indicates serious potential problems in controlling fasciolosis in the future (Fairweather & Boray, Reference Fairweather, Boray and Dalton1999b). Burdens of 20–34 drug-resistant flukes were observed in cattle following treatment with triclabendazole in Australia (Brockwell et al., Reference Brockwell, Elliott, Anderson, Stanton, Spithill and Sangster2014). However, studies have shown that the anthelmintic drugs nitroxynil and oxyclozanide were able to kill 100% and 99.6% of adult triclabendazole-resistant flukes, respectively. Also, albendazole caused up to 95% reduction in triclabendazole-resistant fluke egg counts, while clorsulon showed a 73.2% reduction (Coles & Stafford, Reference Coles and Stafford2001). This finding is consistent with those carried out recently, showing that the anthelmintic drugs clorsulon and oxyclozanide were effective in removing adult triclabendazole-resistant flukes (Elliott et al., Reference Elliott, Kelley, Rawlin and Spithill2015).
There are also reports of some isolates of F. hepatica being resistant to albendazole in sheep (Novobilsky et al., Reference Novobilsky, Averpil and Hoglund2012; Sanabria et al., Reference Sanabria, Ceballos, Moreno, Romero, Lanusse and Alvarez2013). A reduced efficacy of albendazole and oxyclozanide against F. gigantica in naturally infected cattle has also been reported in Tanzania (Keyyu et al., Reference Keyyu, Kassuku, Kyvsgaard and Monrad2008). This could probably be the case with F. gigantica in Nigeria, hence further validation tests may be needed. There are currently few, if any, data on anthelminthic drug resistance in Nigerian cattle. However, a recent study in small ruminants suggests low resistance to ivermectin and levamisole with susceptibility to albendazole (Adediran & Uwalaka, Reference Adediran and Uwalaka2015)
The incomplete elimination of infection leads to subclinical fasciolosis with continuous contamination of pasture, especially in sheep (Ollerenshaw, Reference Ollerenshaw1971). Use of a combination of drugs – synergistic drug usage (Fairweather & Boray, Reference Fairweather, Boray and Dalton1999b) – and treatment based on degree of infection (Malone & Craig, Reference Malone and Craig1990) may be practical treatment strategies.
Human trematodiasis in Nigeria
Human fasciolosis has been reported from 51 countries over the past 25 years in the continents of Africa, America, Asia, Europe and Oceania (Mas-Coma et al., Reference Mas-Coma, Esteban and Bargues1999). Fasciolosis is among the most neglected tropical diseases (Mas-Coma et al., Reference Mas-Coma, Valero and Bargues2009), with an estimated 180 million humans at risk of infection by Fasciola species worldwide (WHO, 1995) and with as many as 2.4–17 million humans infected (Hopkins, Reference Hopkins1992; Toledo et al., Reference Toledo, Esteban and Fried2012). Human infection with fasciolosis has been reported to occur from eating uncooked watercress derived from endemic areas where infected cattle range freely, and also probably from contaminated water (Stemmermann, Reference Stemmermann1953; Toledo et al., Reference Toledo, Esteban and Fried2012). Human fasciolosis is determined by the presence of the intermediate snail host, domestic herbivorous animals, climatic conditions and the dietary habits of man (Chen & Mott, Reference Chen and Mott1990). Mas-Coma et al. (Reference Mas-Coma, Esteban and Bargues1999) have reviewed the prevalence of Fasciola species reported in various parts of the world.
The main methods of diagnosing human trematodiasis are direct parasitological detection of fluke eggs in stools (Mas-Coma et al., Reference Mas-Coma, Bargues and Valero2006) and other biofluids (duodenal and biliary aspirates), and immune-diagnosis (indirect diagnosis). Other non-invasive diagnostic techniques, such as radiology, ultrasound, computed tomography and magnetic resonance imaging, can also be used (Esteban et al., Reference Esteban, Bargues and Mas-Coma1998; Mas-Coma et al., Reference Mas-Coma, Bargues and Valero2005; Keiser & Utzinger, Reference Keiser and Utzinger2009). In a recent review, stool and blood techniques have been reported to be improved for diagnosis of human fasciolosis and during surveys. However, the author also identified difficulties of diagnosing fascioliasis in humans due to different infection phases and parasite migration capacities, clinical heterogeneity, immunological complexity, different epidemiological situations and transmission patterns (Mas-Coma et al., Reference Mas-Coma, Bargues and Valero2014).
Human fasciolosis involving both species of Fasciola has been reported in Africa (Mas-Coma et al., Reference Mas-Coma, Esteban and Bargues1999). There are hardly any studies targeted at detecting the zoonotic effect of fasciolosis in Nigeria. There is a report of the positive detection of Fasciola species in HIV-infected human subjects in Nigeria, although at a low prevalence rate of 1% (Abaver et al., Reference Abaver, Nwobegahay, Goon, Iweriebor and Khoza2012). This suggests that human infection may be significant, although further research on risk factors as well as possible routes of transmission needs to be carried out.
Human cases of dicrocoeliasis are rare and often occur by accidental ingestion of infected ants on unwashed vegetables, or by drinking contaminated water (Haridy et al., Reference Haridy, Morsy, Ibrahim and Abdel-Aziz2003). Human cases of dicrocoeliasis have been reported in Nigeria (Roche, Reference Roche1948; Samaila et al., Reference Samaila, Shehu, Abubakar, Mohammed and Jabo2009), Czechoslovakia (Ondriska et al., Reference Ondriska, Sobota, Janosek and Joklova1989), Egypt (Massoud et al., Reference Massoud, Morsy and Haridy2003), Turkey (Cengiz et al., Reference Cengiz, Yilmaz, Dülger and Çiçek2010) and Kyrgyzstan (Jeandron et al., Reference Jeandron, Rinaldi, Abdyldaieva, Usubalieva, Steinmann, Cringoli and Utzinger2011). Spurious infection with D. hospes has also been reported in Ghana due to accidental ingestion of infected animal liver (Wolfe, Reference Wolfe1966). The subclinical form of the disease, which is most common, is characterized by cholangitis and adenomatous proliferation of the bile duct (Cabeza-Barrera et al., Reference Cabeza-Barrera, Cabezas-Fernández, Salas Coronas, Vázquez Villegas and Cobo2011). Other signs are constipation, diarrhoea, vomiting and abdominal pain (Ondriska et al., Reference Ondriska, Sobota, Janosek and Joklova1989). Human dicrocoeliasis has been reported in a 7-year-old Nigerian child of a nomadic pastoralist, showing clinical signs of fever, jaundice and anterior subcutaneous abdominal mass (Samaila et al., Reference Samaila, Shehu, Abubakar, Mohammed and Jabo2009).
The amphistome species reported in man is Gastrodiscoides hominis, which is widely distributed in Asia. It is located in the caecum and colon, with pigs being the main animal reservoir (Dutt & Srivastava, Reference Dutt and Srivastava1972) and has been reported in Nigeria in a malnourished child (Dada-Adegbola et al., Reference Dada-Adegbola, Falade, Oluwatoba and Abiodun2004).
Although S. bovis primarily infects ruminants, it has been isolated in humans in various parts of Africa (Raper, Reference Raper1951; Chunge et al., Reference Chunge, Katsivo, Kok, Wamivea and Kinoti1986; Kinoti & Mumo, Reference Kinoti and Mumo1988; Santoro, Reference Santoro1988). Moreover, the mesenteries of cattle, which may be infected with S. bovis, are usually sold at the local markets in Africa as edible tripe, thus making it a public health risk (Kamanja et al., Reference Kamanja, Githigia, Muchemi and Mwandawiro2011). Hybridization between S. bovis and S. haematobium (cattle and human infection) has been reported in Senegal, with an impending risk of the emergence of a new disease (Huyse et al., Reference Huyse, Webster, Geldof, Stothard, Diaw, Polman and Rollinson2009).
Several drugs for the effective treatment of human fasciolosis are available. These include dihydroemetine–emetine derivative, bithionol, praziquantel and triclabendazole (effective against both acute and chronic fasciolosis). These are currently the drugs of choice for human fasciolosis caused by both F. hepatica and F. gigantica (Esteban et al., Reference Esteban, Bargues and Mas-Coma1998; Savioli et al., Reference Savioli, Chistulo and Montresor1999). Praziquantel has also been used in the treatment of human dicrocoeliasis (Massoud et al., Reference Massoud, Morsy and Haridy2003). Mebendazole was effective in treatment of the human amphistomosis (Dada-Adegbola et al., Reference Dada-Adegbola, Falade, Oluwatoba and Abiodun2004).
The prevention of human trematode infections may be achieved by strict control of water cress and other metacercariae-carrying aquatic plants for human consumption, especially in endemic zones (Mas-Coma et al., Reference Mas-Coma, Bargues and Valero2005). Drinking water must be boiled or purified. Integrated control approaches and inter-sectoral collaboration between public health and veterinary medicine have also been suggested for control (Keiser & Utzinger, Reference Keiser and Utzinger2009).
Conclusions and recommendations
Trematode infections are a significant limiting factor in livestock production; therefore, the development of sustainable strategies for their control is a priority. In order to develop sustainable control, gaps in knowledge must be identified to guide research projects. The outcome of such research would enhance proper allocation of funds for disease control and policy formulation. In addition, it is also important to carry out detailed study on the overall economic losses due to trematode infections, in order to design and implement appropriate systematic disease prevention and control methods.
The prevalence rates of trematodes reported across the various abattoirs in Nigeria are an indication that trematode infection poses a widespread risk to livestock and, possibly, humans. However, it is worthy of note that neither oxyclozanide nor triclabendazole, which are the two drugs of choice for mixed and human Fasciola infection, respectively, is currently available for use in Nigeria. Availability of these two drugs could be helpful in reducing disease occurrence. These drugs could be made available by formulating favourable policies to ensure that drug retailers have basic training in identifying and stocking the appropriate drugs of choice and informing livestock farmers on the rationale for their use (an example is information on effectiveness of triclabendazole against both mature and immature flukes). The gap in technical knowledge needed by drug retailers for dispensing drugs has been identified in a previous study (Bett et al., Reference Bett, Machila, Gathura, Mcdermott and Eisler2004) and veterinarians have a huge responsibility for advising/training these retailers on the appropriate drugs to stock, based on the diseases prevalent to different localities.
There are hardly any studies targeted at detecting the zoonotic effect of fasciolosis infections in Nigeria. Although a few studies exist on other trematodes in Nigeria, these are often case reports. Further research on burden and risk factors, as well as possible routes of transmission of trematode infection to humans, needs to be carried out.
Molecular studies on trematodes in different species of livestock, including those targeted at understanding anthelmintic drug resistance, should also be carried out across Nigeria. These studies would be useful in providing more data on the diversity of these important trematodes.
Financial support
The research is funded by a PhD studentship from the Nigerian Tertiary Education Trust Fund, the Leverhulme–Royal Society African Award Scheme and the University of Bristol, UK.
Conflict of interest
None.
