Bovine and small ruminant African animal trypanosomiasis in Nigeria – A review

Veterinary Parasitology: Regional Studies and Reports 13 (2018) 5–13

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Review

Bovine and small ruminant African animal trypanosomiasis in Nigeria – A review

T

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Paul Olalekan Odenirana,b, , Isaiah Oluwafemi Ademolaa, Ewan Thomas Macleodb, Susan Christina Welburnb,c a

University of Ibadan, Department of Veterinary Parasitology and Entomology, Faculty of Veterinary Medicine, Ibadan, Nigeria The University of Edinburgh, Deanery of Biomedical Sciences, Edinburgh Medical School, College of Medicine & Veterinary Medicine, 1 George Square, Edinburgh, EH8 9JZ, UK c University of Edinburgh Joint Institute, Zhejiang University, International Campus, 718 East Haizhou Road, Haining 314400, China b

A R T I C LE I N FO

A B S T R A C T

Keywords: African animal trypanosomiasis Glossina species Nigeria Development

Despite extensive attempts over many decades to control African Animal Trypanosomiasis (AAT) across the tsetse fly belt of Nigeria, AAT persists as major animal health problem causing severe morbidity and mortality in livestock. The large agricultural losses in turn have severe adverse impacts on sustainable agricultural development. Despite this, in the past 50 years there have been no significant national control programs against AAT. This review explores the history of AAT control in Nigeria, examining the successes and failures in measures adopted in Nigeria to control AAT and the changing disease epidemiology.

1. Introduction African animal trypanosomiasis (AAT), caused by infection by Trypanosoma vivax, Trypanosoma congolense and Trypanosoma brucei s.l. has severely impacted development of the livestock sector in Nigeria. Morbidity and mortality of cattle in particular results in large agricultural productivity losses (Swallow, 2000). Nigeria's ruminant population increased from 4.5 million cattle in the 1960s (Bourn and Milligan, 1983) to 7.3 million in the 1970s (Lamorde and Franti, 1975). Despite the rinderpest epidemic in 1983 claiming around 1 million cattle (FAO, 1987), the population increased to 12.2 million cattle, 13.2 million sheep and 26.0 million goats in late 1980s. In 2014, an estimated 19.4 million cattle, 40.6 million sheep and 71.0 million goats were reported (FAO, 2014). Cattle considered susceptible to AAT include White Fulani, Red Bororo, Adamawa Gudali and Sokoto Gudali and represented 78% of the total cattle population in Nigeria in 1985 (Swallow and Jabbar, 1994). Several insect species have been implicated in the transmission of Trypanosoma species in Nigeria including, Glossina, Tabanus, and Stomoxys (Molyneux and Ashford, 1983; Abebe and Jobre, 1996) and the relative vectorial capacity, distribution and abundance of these disease vectors is critical to development of control options for AAT. The Nigerian Government established the West African Institute for Trypanosomiasis Research in 1947 to specifically investigate AAT, (renamed the Nigerian Institute for Trypanosomiasis Research (NITR)

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in 1964). The remit of NITR was to undertake research and development for the control and elimination of AAT, to promote food security, rural development, improve human and animal health and facilitate sustainable agricultural practice through optimum land use. In the 1960s, the University of Ibadan and Ahmadu Bello University began researching livestock diseases including AAT (ILRI/NAPRI, 1984). AAT prioritization resulted in extensive tsetse control and research activity in Nigeria between 1968 and 1978, resulting in 20% of the northern Sahel savannah including the plateaus of Mambilla, Jos and Obudu being considered “tsetse free” (Ford, 1970; Davis, 1977; Jordan, 1986; Kalu, 1996a). Despite these notable efforts to control tsetse, there were reports of AAT and tsetse encroachment from neighboring Cameroon (Jordan, 1986) and AAT has been persistently reported in Nigeria (Kalu and Agu, 1984; Nawathe et al., 1988; Anene et al., 1991a; Majekodunmi et al., 2013a). Fulani pastoralists have traditionally been responsible for maintaining the majority of the cattle herds in Nigeria. Animal husbandry practices, knowledge and attitudes have been shown to have direct impact on the persistence of AAT in livestock in Nigeria (Majekodunmi et al., 2013a; Majekodunmi et al., 2013b). Improving livestock production systems in Nigeria through education of cattle keepers on appropriate application of trypanocides and insecticides can reduce drug and insecticide resistance and socioeconomic losses. Land pressure, and the pastoralist practice of transhumance resulted in persistent conflicts with indigene mixed farmers in Nigeria. Therefore, to provide a

Corresponding author at: University of Ibadan, Department of Veterinary Parasitology and Entomology, Faculty of Veterinary Medicine, Ibadan, Nigeria. E-mail address: [email protected] (P.O. Odeniran).

https://doi.org/10.1016/j.vprsr.2018.03.001 Received 11 August 2017; Received in revised form 13 March 2018; Accepted 13 March 2018 Available online 15 March 2018 2405-9390/ © 2018 Elsevier B.V. All rights reserved.

Veterinary Parasitology: Regional Studies and Reports 13 (2018) 5–13

P.O. Odeniran et al.

AAT control in this region is under supported and AAT is likely to be a persistent problem for sustainable ruminant health and development.

Table 1 Tsetse fly species in Nigeria. Riverine group

Savannah group

Forest group

a

a

a

a

a

Glossina palpalis Glossina tachinoides Glossina pallicera Glossina caliginea

Glossina morsitans Glossina longipalpalis

1.1. Multiple vectors of AAT in Nigeria

Glossina fusca Glossina medicorum Glossina tabaniformis Glossina nigrofusca Glossina haningtoni

Tsetse flies (Glossina spp.) are the only vector responsible for cyclical transmission of African trypanosomes and are also implicated in mechanical transmission of Trypanosoma vivax (Moloo et al., 2000). Eleven species of tsetse have been reported in Nigeria, including savannah (Morsitans species); forest (Fusca species) and riverine (Palpalis species) flies (Baldry and Riordan, 1967; Davis, 1977; NITR, 1983). Five species are commonly found in cattle rearing areas (Davis, 1977; Table 1, Fig. 1). Species are located in the tsetse belt between latitude 4° and 13°N (Onyiah et al., 1983). G. morsitans have been observed in pockets around the short and tall grass savannah vegetation in parts of northcentral and northeast while G. palpalis spreads from the guinea savannah down to the tropical rainforest areas (Fig. 1). The prevalence of AAT species observed within tsetse flies is shown in Table 2. Most studies report infection by dissection of the insect and examination of the parasites by microscopy. Early tsetse fly surveys reported Glossina tachinoides Westwood in Gboko, Benue Province (Kernaghan, 1961), Malumfashi, Kaduna Province (Glover, 1961) and Nsukka, Eastern region (Baldry, 1970). Glossina palpalis Robineau-Desvoidy was reported in Ibadan, Oyo state (Adeyemi and Esuruoso, 1997) and G. palpalis palpalis in eastern Nigeria (Omoogun et al., 1995). Low densities of G. tachinoides and G. palpalis were reported in Benue River Valley (Aiyedun and Amodu, 1976) and from Kamuku National Park (Okoh et al., 2011). G. tachinoides and G. palpalis were more recently reported in Kotangora town, Niger State (Ahmed, 2004). G. tachinoides and G. palpalis at an apparent density of 0.09 flies/trap/day of were reported in Jos Plateau (Kalu, 1996a). In Lafia town, Nasarawa state, relative abundance of caught G. palpalis

a Most important species in Nigeria (Baldry and Riordan, 1967; Davis, 1977; NITR, 1983).

solution the Nigerian government, during the period of the Third National Plan enacted the Grazing Bill Act (1965) that led to the Land Use Act of 1978 (ILCA/NAPRI, 1984). The Grazing Bill Act enables designated land within Nigeria to be constituted as a National Grazing Reserve to permit settlement of pastoralists and offers compensation to land owners affected by the Act. Grazing reserves were considered to be tsetse free to encourage the settlement of pastoralist cattle keepers. However, despite being settled within grazing reserves, Fulani continue to maintain traditional transhumance practices while often additionally engaging in mixed farming practices (Ducrotoy et al., 2016; Majekodunmi et al., 2017; Ducrotoy et al., 2017) all of which affects the epidemiology of AAT. Furthermore, recent political conflicts have been shown to have altered the population dynamics of herds maintained within the grazing reserves and this impacts on management practices (Ducrotoy et al., 2018). The sub-humid zones have been a strategic focus for promotion of cattle production (ILRI/NAPRI, 1984; Majekodunmi et al., 2013a; Majekodunmi et al., 2013b; Isaac et al., 2016; Ducrotoy et al., 2016). A major restructuring of the regional livestock industry is underway where humid zones are under pressure from immigration of incoming Fulani pastoralists with their livestock (Azuwike and Enwerem, 2010).

Fig. 1. Important Glossina species distribution in Nigeria. A- Glossina palpalis covers wide areas from the north to the south. B- Glossina tachinoides covers the north and part of the south. CGlossina morsitans is found in multilocation around sub-humid zone. D- Glossina fusca is found in southern region. E- Glossina longipalpis is found around the west of northcentral. Source: Davis (1977).

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Table 2 Trypanosome prevalence studies of Glossina species in Nigeria. Study year

Details

Area

Diagnostic

Reference

1963 1967

TP = 22.4% in Gms (n = 232) Tv and Tc observed TP = 67.3% in Gms (n = 364). PR = 86.5% Tv and 13.5% Tc. TP = 3.1% in Gp (n = 64) all Tv. No Gt (n = 3) infected For tsetse, 9% Tv, 7% Tc, 1.8% Tb and 0.9% Ui in Gm group captured. TP = 90% between 1963 and 1971, declined afterwards to 49% in 1973. Predominantly Tv was recorded. TP = 0.65% in Gt (n = 4620) with 40% Tc, 40% Tc and Tb and 20% Tb. No Gp (n = 17) infected No Gp (n = 152) and no Gt (n = 52) infected TP = 10.7% in Gt (n = 28) TP = 22.7% (n = 119 Gt) with Tv & Tc infections TP = 0% in Gt (n = 52) and Gp (n = 152) TP = 18.2% with Tv- 83% & Tb- 17% in tsetse flies. TP = 1.9% in Gpp (n = 454) TP = 2.8% in Gp (n = 72). No Gt (n = 34) infected TP = 3.1% in Gp (n = 96). TP = 9.4% in Gt (n = 117). TP = 7.1% in Gpp (n = 198). TP = 11.9% in Gt (n = 201). TP = 13.5% in Gms (n = 89) Tc, Tv, Ts and Tg were identified. TP =18.2% in Gp (n = 451). TP = 17.7% in Gt (n = 255). T. b. brucei and Tcs and Tcf were identified. TP =5.5% in Gp (n = 347). TP = 4.3% in Gt (n = 184) Tsetse were pooled for molecular analysis.

NE and NC SW

D D

Jordan (1965) Baldry (1969)

SW SW

D D

Yesufu and Mshelbwala (1973) Riordan (1977)

SE SW NC NE NC NC NC NE NC NE and NC

D D D D D D D D D PCR

Madubunyi (1987) Omoogun et al. (1991) Kalu (1991) Daniel et al. (1993) Omoogun and Akinboade (2000) Ahmed (2004) Oluwafemi et al. (2007) Karshima et al. (2011) Okoh et al. (2012) Isaac et al. (2016)

NE NE

PCR D and PCR

Karshima et al. (2016a) Karshima et al. (2016b)

NA 1963–1973 1984–1985 NA 1987 1990 1993–1994 1995–1999 NA 2010 2007 2012 2013–2014 2014

Abbreviations: NA – not available in the text, TP – total prevalence, PR – prevalence Tv – Trypanosoma vivax, Tc – Trypanosoma congolense, Tb – Trypanosoma brucei, Ts – Trypanosoma simiae, Tg – Trypanosoma godfreyi, Tcs – Trypanosoma congolense savannah, Tcf – Trypanosoma congolense forest, Tbg – Trypanosoma brucei gambiense, Mi – mixed infection, Ui – unidentified, NC – northcentral, NE – northeast. NW – northwest, SW – southwest, SE – southeast, SS – southsouth, Gp – Glossina palpalis, Gpp – Glossina palpalis palpalis, Gt – Glossina tachinoides, Gm – Glossina morsitans, Gms – Glossina morsitans submorsitans, D – dissection, PCR – polymerase chain reaction.

determined 30% of cattle to be infected with trypanosomes. Morphological examination indicated a T. vivax prevalence of 14.7% with prevalence of T. congolense of 14.1% and for T. brucei 0.09%. Other studies indicated very high infection rates prior to the implementation of extensive tsetse control, for example, 71.4% in trekked cattle in northern Nigeria (Godfrey et al., 1965). A reduction in AAT prevalence was observed in studies conducted after implementation of tsetse control, for example AAT prevalence in northern Nigeria of 4.3%, 1.6% and 1.0% in cattle, sheep and goats respectively between 1989 and 1991 (Onyiah, 1997). In the southern states, AAT prevalence values of between 2.7 and 14% were reported (Ikede et al., 1987; Opasina and Ekwuruke, 1987). An abattoir study in Ibadan, Oyo State, in 1997 reported an AAT prevalence of 19.9% (Isamah and Otesile, 1997) and Takeet et al. (2013) reported AAT at prevalence of 76.6% in Ogun state in the south and 25.3% for Kaduna state in the north. Many studies have been undertaken on the Jos Plateau since it was considered to be a tsetse-free zone (Kalu, 1991, 1996b; Kalu and Uzoigwe, 1996; Kalu and Lawani, 1996; Kalejaiye and Omotainse, 2001; Majekodunmi et al., 2013a, 2013b; Ducrotoy et al., 2016). Recent molecular studies have revealed higher prevalence, for example 46.8% in Jos Plateau (Majekodunmi et al., 2013a).

varied from 0.10–19.30/flies/trap/day prior to any control being implemented (Takken et al., 1986). Other biting flies are also implicated in transmission of Trypanosoma vivax in Nigeria. Tabanus species present in Nigeria include, T. taeniola, T. biguttatus, T. pluto, T. latipes, T. fasciatus, T. subangustus, T. gratus, T. fuscipes, T. par, T. pertinens, T. secedens, T. albipalpus, T. neocopinus and T. thoracinus (Dipeolu, 1977; Ahmed et al., 2005). Ahmed et al. (2005) observed Tabanus biguttatus as the most abundant while Tabanus taeniola was reported as the most abundant by Dipeolu (1977). Stable flies, Stomoxys spp, in Central African Republic and African tabanids (Atylotus agrestis and A. fuscipes) in Burkina Faso have been reported to transmit Trypanosoma vivax mechanically (D'Amico et al., 1996; Desquesnes and Dia, 2003; Desquesnes and Dia, 2004). Stomoxys comprise 60–75% of the biting flies caught in entomological surveys in Nigeria (Lloyd and Dipeolu, 1974; Dipeolu, 1977; Ahmed et al., 2005). While Stomoxys calcitrans and Stomoxys nigra are commonplace in Nigeria (Dipeolu, 1977; Ahmed et al., 2005), their capacity for mechanical transmission of T. vivax is unknown. Similarly, Haematopota and Chrysops may also potentially impact on mechanical transmission.

1.2. Prevalence of AAT in Nigeria 1.3. National control campaigns in Nigeria

Numerous studies have investigated the prevalence of AAT in Nigeria using microscopic, serological and molecular diagnostic methods for detection of parasites in both tsetse and animal hosts. Most reports of AAT are based on observations of poor body condition score, microscopy using thin/thick blood smears as well as low PCV in a susceptible host (OIE, 2008, 2013). For some surveys, haematocrit centrifugation technique and buffy coat examination under the microscope is applied with or without Giemsa staining. In Nigeria, over 75% of reported field cases of AAT are based on microscopy that lacks sensitivity and specificity (Picozzi et al., 2002; Uilenberg, 2011). Serological assays for ruminant AAT do not distinguish between mixed, past and current infections. PCR based surveillance methods provide a far more accurate epidemiological assessment for AAT prevalence in ruminants. (Picozzi et al., 2002). A summary of all studies examining AAT prevalence in ruminants published between 1950 and 2016 is shown in Table 3 and shows a wide range in AAT prevalence. An early study by MacLennan (1956)

The Nigerian Tsetse Eradication Campaign (NTEP) began in 1955 with the use of long-acting insecticides at northeastern regions of tsetse distribution in the country (Putt and Shaw, 1982). These projects progressively expanded to the eastern and western parts of the country along the sub-humid zone (ILRI/NAPRI, 1984). In 1978, US$ 72.6 million was allocated to an extensive ground spraying campaign with tsetse being removed from an area of 196,500 km2 (Putt et al., 1980; Putt and Shaw, 1982). This represented 0.2% of GDP at that time (total GDP US$ 36.5 billion). The Biological Control of Tsetse (BICOT) project in Vom, Nigeria operating between 1979 and 1987 targeted an area of 1500 km2 in Nasarawa state (including 450 km2 of linear riverine forest). Sterile insect technique (SIT) was applied after the wild population was reduced to less than 10% by the application of trapping and insecticideimpregnated targets for 6–12 weeks (Leak, 1998). One and a half 7

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Table 3 Trypanosomiasis prevalence studies of livestock in Nigeria. Study year

Details

Area

Diagnostic

Reference

1955–1956

TP = 30% with Tv- 14.7%, Tc- 14.1%, Tb- 0.09% & Mi- 1.2% in cattle.

WM

MacLennan (1956)

NA

TP = 44.6% (n = 193 cattle) with PR = 23.3% Tv, 76.7% Tc & 4.7% Tb.

NE, NW, NC NC

TTS,

1963 1974–1975 NA NA NA 1985–1986 1989

TP = 71.4% (n = 28 cattle) with Tv & Tc. TP = 8.5% in 1974 & 8.1% in 1975 with Tv infection only among trade cattle. TP = 64% with Tv- 54.7%, Tb- 6.7% & Tc- 2.7%. TP = 100% (n = 100 cattle) All Tb positive TP = 7.6% (n = 210 cattle). Tv was predominant. TP = 8.5% (n = 3387 cattle) with 7.7% Tv, 0.8% Tc in cattle TP = 9.6% (n = 323 cattle) with 4.6% Tv, 3.4% Tc & 1.5% Tb

NE & NC SW SW SW NC SW NC

NA 1989–1990 1987

SW NC NC

NA 1993–1994

Tv- 44% adult Fresian, 6.9% Fresian calves & 15% Fulani zebu cattle infected. Tv- 1.5% (n = 68 cattle) in August, Tv- 1.1% & Tb- 0.3% (n = 290 cattle) in February. TP = 38.6% (n = 629 cattle) with 67.9% Tv, others were Ui. TP = 20.6% (n = 165 sheep) with 61.8% Tv, 8.8% Tc & 29.4% Ui. TP = 30.7% (107 exotic & 43 local pigs), PR = Tb- 58.7%, Tc- 21.7% & Mi-19.6%. TP = 3.9% (n = 1065 cattle). PR = Tv- 64.3%, Tc- 31%, Tb- 4.8%. TP = 13.6% (n = 89 goats & n = 18 sheep), PR = Tv- 36%, Tb- 50% & Tc- 43% TP = 5.4% out of 53 N'dama & 0% in 11 Muturu cattle TP = 8.96% (268 trypanotolerant cattle), Tv- 3.4%, Tc- 3.0%, Tb- 0.8%, Mi- 0.8% & Ui1.0%. TP = 0.9% (664), 0.6% (350) sheep & 1.1% (314) goat positive of Tv only. TP = 16.4% (55 sedentary cattle), only Tv identified. TP = 37.6% in cattle TP = 5.3% (n = 1106 cattle), 1.2% (n = 166 sheep) & 0.7% (n = 152 goats). Tv accounted for 57.6% of all cases. TP = 6.4% & 9.1% in Barkin-Ladi and Bassa LGAs. Tv was most identified. TP = 14.3% (from 21 abattoir cattle), 0% from 181 cattle & 14 goats.

Killick-Kendrick and Godfrey (1963) Godfrey et al. (1965) Kilgour and Godfrey (1978) Yesufu and Mshelbwala (1973) Akinboade et al. (1983) Agu (1984) Opasina and Ekwuruke (1987) Joshua and Shanthikutmar (1989) Anene et al. (1991b) Anene et al. (1991a) Kalu (1991)

NA NA

SE NE SE SW NC

WM, TTS, WM WM, TTS, BC, GS TTS, GS STDM & HCT BC WM, TTS, BC, GS, mn ex, MI Thin sm BC, GS Thin sm BC, GS WM, thin sm, BC & HCT WM, GS, T/sm & HCT TTS, GS, STDM & HCT WM, TTS from BC. BC WM, TTS, BC & HCT.

Onah (1991) Daniel et al. (1993) Fakae and Chiejina (1993) Anene and Ezekwe (1995) Kalu (1995)

NE NC NC NW

WM, TTS TTS, BC & HCT WM, TTS, BC & HCT. BC & HCT

Nawathe et al. (1995) Kalu (1996b) Kalu and Uzoigwe (1996) Kalu and Lawani (1996)

NC NC

STDM, GS & HCT WM, HCT

TP = 11.7% in cattle & 17.9% in sheep

NC

WM, TTS, BC & HCT

NC

WM, TTS, STDM & HCT

NE & NC

TTS, BC, GS & HCT

Omotainse et al. (2001)

NC NC NC NC NC SW SE NC NC

Shamaki et al. (2002) Yanan et al. (2003) Abenga et al. (2004) Omotainse et al. (2004) Oluwafemi et al. (2007) Ameen et al. (2008) Ezeani et al. (2008) Qadeer et al. (2008) Samdi et al. (2008)

NC NC NC NC NC SE

TTS, BC TTS, BC BC & thin sm GS TTS, BC, GS & HCT TTS, HCT & BC WM, thin sm & HCT. ELISA STDM Thin sm, BC, GS & HCT ELISA BC, GS & HCT BC & GS STDM, HCT & MI STDM WM, TTS, GS

Enwezor et al. (2009a) Enwezor et al. (2009b) Enwezor et al. (2009c) Ezebuiro et al. (2009) Danbimi et al. (2010) Ohaeri (2010)

NC

HCT, BC & GS

Samdi et al. (2010)

SW NC NC NC NW

STDM, BC & HCT Thin sm & MI Thin sm, GS, BC Thin sm, GS, BC STDM & PCR

Sam-Wobo et al. (2010) Behnke et al. (2011) Enwezor and David (2011) Enwezor et al. (2011) Fajinmi et al. (2011)

2009 2008 NA 2010

TP = 27.6% (553 small ruminants) with 38.16% (304 sheep) & 14.23% (239 goats). Sheep (50.9% Tv, 13.7% Tc, 9.5% Tb, 12% Mi & 13.8% Ui) and goats (44.1% Tv, 20.6% Tc, 23.5% Mi, 11.8% Ui) infection rates reported. TP = 10% & 8.85% (cattle and sheep respectively in Gombe state), TP = 57.1%, 33.9%, 36.8% in sheep, goats & pigs respectively in Benue state. TP = 7.9% in cattle and sheep around Jos Plateau TP = 7.5% in trypanotolerant cattle in Jos Plateau TP = 9.1% (48/526 cattle), PR = 81% Tv, 15% Tc & 4% Tb. TP = 47.9% TP = 9% (n = 200 settled cattle) & 10.5% (200 slaughtered cattle). TP = 3.9%, 4.7% & 3.5% (465 cattle, 940 sheep and 675 goats respectively). TP = 18.6% (n = 264 cattle). Tv-7.58%, Tc- 7.96% & Tb- 3.03% TP = 13.8% (n = 1300 cattle). Tv was predominant. TP = 2.1% (n = 529) with 2.39% & 1.88% in sheep and goats respectively. Tv- 0.95%, Tc0.57% & Tb- 0.57%. TP = 65.9% (n = 545 cattle) TP = 8.4%, 17% & 17% from 1293 cattle, 215 sheep & 130 goats TP = 8.4% (n = 1293 cattle) TP = 5.0%, 4.67% & 3.33% in cattle, goats and sheep TP = 40% (n = 32 cattle) with all positive for Tv. TP = 1.9% (n = 1361). 3.7%, 1.2% & 1.1% in cattle, sheep & goat respectively). PR = Tc4.3%, Tv- 57.7%. TP = 1.73% (n = 347 goats) with PR of Tc-33.3%, Tv- 16.7% & Tb- 50%, TP = 1.16% (n = 172 sheep) with PR of Tc- 50% & Tb- 50% TP = 31.62% with Tv- 23.9%, Tc- 9.7% & Tb- 0.9% in cattle. TP = 3.98% (n = 1054 goats) with Tb 92.86% & Tc/Tv 7.14%. TP = 14.6% (n = 410 cattle) with Tv- 85%, Tb- 11.7% & Tc- 3.3%. TP = 22% (n = 964 cattle) with Tv- 21.1% & Tc- 0.7%. TP = 1.8% (n = 500 cattle). 1.2% Tv, 0.4% Tb & 0.2% Tc. TP = 4.4% (n = 500 cattle) for PCR with Tb group detected. TP = 1.7% (n = 1414 female goats), with Tc- 41.7%, Tv- 29.2% & Tb- 29.2%. TP = 6.53% (405/6203 cattle). TP = 2.2% (n = 634 cattle). PR = 50% Tc, 21.4% Tb, 14.2% Tv & 14.2% Mi. TP = 3.8% (n = 395) with Tv- 3.5% & Tc- 0.3% TP = 9.25% (n = 400 cattle) with Tbg. TP = 14.1% (n = 106 goats) with 66.7% Tv, 33.3% Tb.

Kalu (1996a) Omoogun and Akinboade (2000) Kalejaiye and Omotainse (2001) Kalu et al. (2001)

SW SS NC NC NE SE

TTS, BC & HCT TTS, GS STDM & HCT TTS, BC, GS & HCT CATT STDM & BC

2008 2012 NA

TP = 46.8% (n = 7143 cattle) with Tb- 3.2%, Tc- 27.7% & Tv-26.7%. TP = 7.4% in sheep & goats. Species not identified. TP = 71.7% (n = 205 goats) Only Tv was identified.

NC SE NW, NE & SW

PCR WM & BC. PCR

Leigh and Fayemi (2011) Owai (2011) Samdi et al. (2011) Enwezor et al. (2012) Karshima et al. (2012) Anyaegbunam and Okafor (2013) Majekodunmi et al. (2013a) Nwoha et al. (2013) Sanni et al. (2013)

1987 1990 1887–1988 1989–1991 NA 1991–1992 NA NA NA

2000 NA NA 2001 NA NA 2005–2006 NA 1999–2000 2004 NA 2004 2004–2005 1998–1999 NA 2003–2004 2009 NA 2006 2007 2008 2008 2008

(continued on next page)

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Table 3 (continued) Study year

Details

Area

Diagnostic

Reference

NA

TP = 63.7% (411 cattle) with Tc- 35%, Tv- 13.1%, Tb- 1.7% & Mi- 13.9% for PCR, while microscopy TP = 15% (411 cattle) with Tb- 3.4%, Tc- 4.6%, Tv- 6.1% & Mi- 0.9% in Kaduna & Ogun TP = 13.33% (n = 240 cattle) with Tv- 9.17% & Tc- 4.16%. TP = 4.96% (n = 320) with 66.67% Tv & 33.33% Tb. TP = 2.5% (n = 448 cattle) with Tv- 2.0%, Tc- 0.2% & Tb- 0.2%. TP = 0.8% & 9.3% (microscopy & PCR assessment on 118 cattle) with 10% Tv, 10% Tg & 80% Mi. TP = 31.6% (n = 133) with Tv- 20.3%, Tc- 8.3%, Tb- 0.75% & Mi- 2.3%. TP = 53.3% (n = 150 cattle) with Tv- 23.3%, Tc- 16.7% & Tb- 13.3%. TP = 16.6% (n = 712 pigs sampled) with Tb- 8.8%, Tcf- 2%, Tcs- 2.7% & Mi- 3.1%.

NC, SW

BC, TTS & GS. PCR

Takeet et al. (2013)

NE SW NE NW

WM, TTS & BC. BC & thin sm GS STDM, HCT & BC ITSI-PCR

Zubairu et al. (2013) Fasanmi et al. (2014) Obaloto et al. (2015) Yusuf et al. (2015)

SW NC NE

STDM HCT, BC & GS PCR

Abubakar et al. (2016) Hassan et al. (2016) Karshima et al. (2016a)

2002 2012 2008 NA NA 2016 2013–2014

Abbreviations: NA – not available in the text, TP – total prevalence, PR – prevalence, Tv – Trypanosoma vivax, Tc – Trypanosoma congolense, Tb – Trypanosoma brucei, Tg – Trypanosoma godfreyi, Tcs – Trypanosoma congolense savannah, Tcf – Trypanosoma congolense forest, Tbg – Trypanosoma brucei gambiense, Mi – mixed infection, Ui – unidentified, NC – northcentral, NE – northeast. NW – northwest, SW – southwest, SE – southeast, SS – southsouth, WM – wet mount, BC – buffy coat method, GS – Giemsa staining, HCT – haematocrit concentration technique, TTS – thick and thin smear, MI – mouse inoculation, ME – mini-anion exchange technique, STDM – standard trypanosome detection technique, CATT – card agglutination trypanosomiasis test, D – dissection, ELISA – enzyme-linked immunosorbent assay and PCR – polymerase chain reaction.

measure, chemotherapy strategies are currently protecting more cattle against the disease than any other method (Budd, 1999). However, prolonged and frequent use of trypanocides at sub-therapeutic concentrations in areas of high tsetse challenge can result in development of drug resistance (Clausen et al., 1992; Geerts and Holmes, 1998). Studies have identified substandard veterinary products as a major cause of drug resistance (Teko-Agbo, 2008; Gberindyer et al., 2014). There has been concern of the increasing circulation of low quality drugs (Erhun et al., 2001) and even though similar concerns were raised in the 1990s (Alubo, 1994), the government has not improved the state of drug quality in the livestock industry. Drug quality control is difficult to institute in Nigeria because of substandard trypanocides in the market, a lack of veterinary services in rural settlements and government neglect of livestock owners (Kingsley, 2015). Surveys have detected resistance to trypanocides in 18 African countries (Delespaux et al., 2008) but the significance of drug resistance to farmers remains poorly understood (Sinyangwe et al., 2004). Drug resistant trypanosomes were detected in Nigeria in the 1960s and 1970s (Jones-Davies, 1967; Na'isa, 1967; IIemobade, 1979) but more recent reports on trypanosome drug resistance in Nigeria are sparse, despite increased morbidity and mortality in the livestock industry (Adamu et al., 2011).

million sterile male Glossina palpalis palpalis were reared for a 10:1 release ratio (Oladunmade et al., 1990). A lack of sustainable finance to extend the target areas and maintain barriers led to reinvasion of tsetse (Leak, 1998; Oluwafemi et al., 2007). Out of 200 slaughtered and 200 sedentary cattle investigated in Nasarawa state in 2007, an AAT prevalence of 9% and 10.5% was reported. The infection rate with AAT, in 446 tsetse (majority Glossina palpalis palpalis was 1.9% by dissection (Oluwafemi et al., 2007)). The huge financial outlay for establishment of tsetse rearing facilities makes this method non-sustainable for Nigeria and the program was cancelled (Ahmed, 2010). The Pan African Tsetse and Trypanosomiasis Eradication Campaign (PATTEC) was launched in Burkina-Faso during the 26th International Scientific Council for Trypanosomiasis Research and Control conference in 2001. The aim was sustainability of tsetse eradication and adoption of an “area-wide approach” (Vreysen et al., 2000). PATTEC assisted Ghana, Burkina-Faso, Ethiopia, Mali, Uganda and Kenya to secure loans of US $70 million through the African Development Bank in 2004, to implement the first phase of AAT control activities. The remaining 18member countries including Nigeria used their own resources or support partners to implement AAT control. Livestock owners are yet to feel the benefit of the PATTEC-Nigeria initiative and any impact of PATTEC Nigeria on local farmers is unknown. A lack of structural support and planning for elimination means individual livestock owners are essentially saddled with the responsibilities for the health and wellbeing of their animals. Most PATTEC-Nigeria targets are far from being actualized. Trypanotolerant animal breeds were introduced to Nigeria as early as 1939 as a strategy against AAT. Between 1980 and 1983 approximately 5000 N'dama cattle were shipped to Nigeria from the Gambia (Swallow et al., 1994). Other trypanotolerant breeds include savanna and forest Muturu (which are like the Borgou of Benin (ILCA/FAO/ UNEP, 1979)) and the Keteku (White Fulani and savanna Muturu crosses). These crosses and West African short-horn comprised 70% of all trypanotolerant breeds in Nigeria in the 1980s (Akinwumi and Ikpi, 1985). This strategy is considered inherently flawed due to the low productivity of these breeds (FAO, 1987) and there are now very few trypanotolerant breeds (Muturu and N'dama) remaining in Nigeria (Adebambo, 2001). Trypanotolerant goats include, Sahel/Desert/West African longlegged goat, West African dwarf and Sokoto red (Ngere et al., 1984); while those of sheep include Balami, Yankasa, Uda and West African Dwarf (Adu and Ngere, 1979).

1.5. Conflict Fulani pastoralist migration southwards began in the early twentieth century as a response to a range of drivers, including desertification, population pressure that led to thinning out wildlife, persistent drought, environmental degradation, availability of trypanocides and insecticides to combat AAT challenge, extreme climate change and use of charms and daggers for self-protection (Gleditsch, 2001; Onyima and Iwuoha, 2015; Okoli and Atelhe, 2014). Persistent conflicts between farmers and Fulani herdsmen have interrupted the value chain and incurred monetary loses in the livestock industry. Fulani settlers have claimed lands which the original owners have disputed and this has led to a general lack of acceptance of the national grazing bill across the country. Agricultural activities and land use claims are increasing between community farmers and the migratory Fulani herdsmen (Onyima and Iwuoha, 2015). Twenty states in Nigeria have reported conflicts over grazing land areas arising from lack of understanding between local communities and migrating Fulani herdsmen (Abbas, 2000; Onyima and Iwuoha, 2015; Okoli and Atelhe, 2014). Conflicts, originally restricted to the northern region, have more recently been reported in southern regions namely; Ondo, Ogun, Oyo, Ekiti, Osun, Abia, Edo, Enugu and Niger-Delta states (Fabusoro, 2007; Onyima and Iwuoha, 2015). During the political conflicts in May 2013, along the border area of the states of Benue and Nasarawa thousands fled their homes and

1.4. Trypanocidal drug resistance and substandard drugs The use of trypanocidal drugs to control AAT represents the most widely used approach to control (d'Ieteren et al., 1998). As a control 9

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about 1000 homesteads were destroyed and others displaced (Okoli and Atelhe, 2014). Loss of life and property has been reported in northcentral Nigeria, some of which has led to communal clashes (Okoli and Atelhe, 2014). Recent political conflicts had been shown to have altered the population dynamics of herds maintained within the grazing reserves because of mass immigration into Kachia Grazing Reserve, impacting on management practices within the reserve that impact on AAT and animal health and productivity and livelihoods (Ducrotoy et al., 2018).

Rev. Elev. Med. Vet. Pays Trop. 57 (1–2), 45–48. Abubakar, A., Sabo, H.M., Abdulkadir, S., Halliru, S.N., Umar, R.B., Abdulkadir, D.A., 2016. Epidemiology of trypanosomiasis in derived savannah of Nigeria. J. Pharm. Biol. Sci. 11 (1), 51–54. Adamu, U.O., Haruna, M.K., Ovbagbedia, R.P., Bizi, R., Benjamin, W., Malala, U.O., Nwezor, F.N.C., Muhammed, M., 2011. Control of African trypanosomiasis in Nigeria: Time to strengthening integrated approaches (A review). Int. J. Anim. Vet. Adv. 3 (3), 138–143. Adebambo, O.A., 2001. The muturu: a rare sacred breed of cattle in NIGERIA. In: Animal Genetic Resources Information Bulletin Issue 31. Anim. Prod. & Hlth. Division FAO, Rome, pp. 27–36. Adeyemi, I., Esuruoso, G.O., 1997. City resident tsetse: preliminary epizootiological investigations in Ibadan, South-Western Nigeria. Epidemiol. Sante Anim. 1, 31–32. Adu, I.F., Ngere, L.O., 1979. The indigenous sheep of Nigeria. World Rev. Anim. Prod. 15, 51–62. Agu, W.E., 1984. Incidence of bovine trypanosomiasis in six villages of Kaduna State, Nigeria. In: Proceedings of the National Conference on Diseases of Ruminants, Vom, Nigeria. 3–6 October 1984. Ahmed, A.B., 2004. A peridomestic population of the tsetse fly Glossina palpalis palpalis Robineau-Desvoidy, 1830 (Diptera: Glossinidae) at Kontagora town, Niger state, Nigeria. Entomol. Vect. 11 (4), 599–610. Ahmed, A.B., 2010. A stake-holder based approach to tsetse fly control in central Nigeria. J. Agric. Ext. Rural Dev. 2 (8), 161–166. Ahmed, A.B., Okiwelu, S.N., Samdi, S.M., 2005. Species diversity, abundance and seasonal occurrence of some biting flies in southern Kaduna, Nigeria. Afr. J. Biomed. Res. 8, 113–118. Aiyedun, B.A., Amodu, A.A., 1976. Human sleeping sickness in the Gboko endemic area of Nigeria. Acta Trop. 33, 88–95. Akinboade, O.A., Ogunji, F.O., Dipeolu, O.O., 1983. 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2. Conclusions Only an integrated management approach that applies a combination of methods can lead to sustainable control for AAT (Holmes, 1997). Community involvement in decision making, program designing, program implementing, program evaluating and creating awareness are key (Dransfield and Brightwell, 2004; Sindato et al., 2008; Ahmed, 2010). The knowledge and perception of livestock keepers on the impacts of AAT and their participation in developing intervention strategies are prerequisites for effective implementation (Machila et al., 2003). Nigeria requires a comprehensive strategy for AAT elimination. Establishing grazing reserves across the states could be detrimental causing further decline in the cattle population if AAT is not addressed. There is no current national surveillance strategy for AAT in Nigeria. Monitoring AAT in affected animal populations and monitoring distribution and abundance of vector species is key to any control strategy. Evidence-based control needs to focus on regions where high prevalence of the most virulent pathogens are found and permit deployment of appropriate technologies to manage AAT. Furthermore, several groups of animals such as pigs and wildlife, need to be examined for AAT to determine their contribution to the epidemiology of the disease. Control of AAT demands regional focus on integration strategies, capacity building, administrative policy to include research funding and involvement of community leaders. Furthermore, the transboundary nature of the vector and disease requires ownership of the problem by affected regional governments and allocation of funds to operationalize control. Conflict of interest statement The authors have no conflict of interest. Ethical statement The study was conducted with the permission of the University of Ibadan Animal Ethics Committee (UI-ACUREC/App/12/2016/05) and in line with the guidelines of the committee. Acknowledgement This study was financially supported by Commonwealth Scholarship Commission and The University of Edinburgh, United Kingdom. Paul O. Odeniran is a Commonwealth scholar, funded by the UK government with reference number NGCN-2016-196. The University of Edinburgh is a charitable body, registered in Scotland, with registration number SC005336. Special gratitude to Professor Adejinmi J. O. for his kind support. References Abbas, I.M., 2000. No retreat, no surrender: conflict for survival between Fulani pastoralists and farmers in northern Nigeria. Eur. Sci. J. 8 (1), 331–346. Abebe, G., Jobre, Y., 1996. Trypanosomosis; a threat to cattle production in Ethiopia. Rev. Elev. Med. Vet. Pays Trop. 147, 897–902. Abenga, J.N., Enwezor, F.N.G., Lawani, F.G., Osue, H.O., Ikemereh, E.C.D., 2004. Trypanosome prevalence in cattle in Lere area in Kaduna State, North central Nigeria.

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