Haematology of N’Dama and West African Shorthorn cattle herds under natural Trypanosoma vivax challenge in Ghana

Introduction

Animal trypanosomosis, caused by trypanosomes mainly transmitted by tsetse flies results in annual economic losses in Africa in the range of US$ 1.0 - 1.2 billion in cattle production alone, and more than US$ 4.75 billion in terms of agricultural Gross Domestic Product (Enyaru et al., 2010). Among species of trypanosomes that cause nagana, Trypanosoma vivax is the predominant species in Ghana (Adam et al., 2012; Mahama et al., 2004; Turkson, 1993) agreeing with reports by Losos (1986) that T. vivax predominates in West Africa.

The usual consequence of trypanosome infection is anaemia, which is often accompanied by poor growth, weight loss, low milk yield, infertility, abortion and paralysis (Berthier et al., 2015; Dagnachew et al., 2015; Mattioli et al., 1999; Steverding, 2008; Trail et al., 1990). Death may result within a few weeks to several months after infection. The use of prophylactic and curative drugs has remained the most popular method for the management of animal trypanosomosis in sub-Saharan Africa (SSA) (Kinabo, 1993; Mahama et al., 2003; Turkson, 1993). However, the continued use for more than half a century of a limited number of closely related trypanocidal drugs has led to the emergence of drug resistant trypanosomes (Delespaux et al., 2008; Matovu et al., 2001; Sow et al., 2012). It is unlikely that a vaccine will become available in the foreseeable future (Nyame et al., 2004; Vale, 2009). Control of tsetse flies, the cyclical vectors of trypanosomes in SSA, is a significant factor in managing the disease in a holistic manner (Allsopp, 2001; Bouyer et al., 2015; Kgori et al., 2006; Leak et al., 1995; Mulla & Rickman, 1988; Vreysen et al., 2000). Nonetheless, local eradication successes have been limited to less than 2% of the infested area due to either resurgence of residual populations that were omitted from eradication campaigns or reinvasion from neighbouring infested areas (Bouyer et al., 2015). Landscape friction maps based on tsetse fly genetic distances and remotely sensed environmental data have identified natural barriers to isolated clusters of Glossina palpalis gambiensis in West Africa (Bouyer et al., 2015). This represents a major advance in locating and eradicating isolated tsetse populations without risk of reinvasion. However, this innovation has yet to be replicated at the continental level under the auspices of the Pan African Tsetse and Trypanosomoses Eradication Campaign (PATTEC) (Bouyer et al., 2015).

The use of trypanotolerant cattle has not been given adequate consideration in integrated tsetse and trypanosomosis control programmes (Agyemang, 2005; Hendrickx et al., 2004). Trypanotolerant breeds, although equally susceptible to initial infection by trypanosomes, possess the ability to survive, reproduce and remain productive in areas of high tsetse challenge without the need for the use of chemicals to control the vector or drugs to control the parasite (Dayo et al., 2009; Mattioli et al., 1998; Rege et al., 1994; Trail et al., 1990; Yaro et al., 2016), where other breeds rapidly succumb to the disease (Berthier et al., 2015; Mattioli et al., 1998; Murray & Dexter, 1988). The trypanotolerant trait is generally attributed to the taurine breeds of cattle in West and Central Africa, namely, the N’Dama and the West African shorthorn (WASH) (Hoste et al., 1992; Maganga et al., 2017; Mattioli et al., 1998; Mattioli et al., 1999; Roelants, 1986; Trail et al., 1990; Trail et al., 1994). Similar observations have been made for the Orma Boran X Maasai Zebu (Orma Zebu) crossbred cattle in East Africa (Maichomo et al., 2005; Mwangi et al., 1998a; Mwangi et al., 1998b). Studies have shown that the basis of this trait was associated with the capacity of these animals to develop less severe anaemia in the face of infection (Berthier et al., 2015; Mattioli et al., 1998; Murray et al., 1982; Murray & Dexter, 1988; Trail et al., 1990).

We previously reported natural T. vivax challenge in N’Dama and WASH cattle herds in Ghana using a sensitive PCR approach (Ganyo, 2014). This study examines the effect of natural T. vivax challenge on haematological parameters in these trypanotolerant cattle herds.

Methods

Results

Seven of the N’Dama samples (n=55) and 4 animals from the WASH samples (n=55) were positive for T. vivax infection. None of the 55 Sanga and 38 Zebu cattle sampled tested positive for T. vivax. The mean haematological values for trypanosome-positive and negative cattle are shown in Table 1. For the N’Dama cattle, significant differences were observed in PCV (p < 0.05), total RBC count, MCV (p < 0.01) and MCH (p < 0.01) values between infected and uninfected cattle, with PCV, MCV and MCH values being significantly higher in uninfected compared to infected cattle. The other parameters were similar for both groups (Table 1). For the WASH cattle, the PCV, Hb and RBC values for uninfected cattle were higher than those for infected cattle (Table 1). For the N’Dama cattle, the mean TWBC counts for infected animals were lower than that for uninfected animals. The mean values of neutrophils, lymphocytes and eosinophils were lower in infected N’Dama compared to uninfected N’Dama. The WASH cattle had higher mean TWBC counts for infected animals compared to uninfected animals. The mean values of neutrophils and eosinophils were higher in infected WASH compared with uninfected.

Discussion

The mean PCVs for infected N’Dama and WASH cattle in this study were lower than those for uninfected cattle, which is consistent with the pathological effect of anaemia in trypanosome infections. Our observations support the findings of Berthier et al. (2015) that N’Dama and Zebu cattle experimentally infected with Trypanosoma congolense had lower PCVs than uninfected animals. Trail et al. (1994) also showed that N’Dama naturally infected by trypanosomes in Zaire (now Congo) had lower PCV values and lower weight gain than non-infected N’Dama. A study in Ethiopia (Dagnachew et al., 2015) in Zebu cattle experimentally infected with T. vivax isolates showed that the mean PCV, Hb and total RBC count were lower in infected groups than in non-infected control animals. Additionally, an earlier survey conducted in cattle maintained under traditional management system in 8 villages in Hawagelan district, western Ethiopia (Bekele & Nasir, 2011) revealed that the mean PCV of trypanosome-infected animals was significantly lower than that of non-infected animals. Lower herd average PCVs for trypanosome-positive cattle compared to trypanosome-negative cattle have also been reported in Ankole cattle in Uganda (Waiswa & Katunguka-Rwakishaya, 2004), Angoni cattle in Zambia (Marcotty et al., 2008), Doayo and Zebu White Fulani cattle in Cameroun (Achukwi & Musongong, 2009) and Zebu cattle in Gabon (Cossic et al., 2017). In Nigeria, Ohaeri & Eluwa (2011) observed that in addition to cattle, other domestic ruminants that were naturally infected with trypanosomes had significantly lower (p < 0.05) PCV and RBC counts compared to uninfected animals.

The mean PCV, Hb and RBC values observed in both infected and uninfected N’Dama and WASH cattle in current study were within the established normal reference values (Jain, 1993). The presence of T. vivax parasites is associated with a reduction in the mean RBC values below the normal range, an indication of anaemia (Murray & Dexter, 1988; Silva et al., 1999). However, infected cattle had mean RBC values within the normal range, which could be attributed to their trypanotolerant trait.

With typical trypanotolerance, cattle have the capacity to develop less severe anaemia in the face of pathogenic Trypanosoma species infection, as assessed by packed cell volume (Berthier et al., 2015; Mattioli et al., 1998; Murray et al., 1982; Murray & Dexter, 1988; Trail et al., 1990). Our findings are in agreement with the report (Mbanasor et al., 2003) that the mean RBC, Hb and PCV values in natural T. vivax-infected trypanotolerant Muturu (WASH) cattle in Nigeria were well within accepted normal values for cattle. An earlier study involving trypanotolerant WASH cattle in Ghana also reported normal PCV value despite the presence of trypanosome parasites (Adam et al., 2012).

In this study, we sampled trypanosusceptible Sanga and Zebu cattle in the same agro-ecological zones as the trypanotolerant N’Dama and WASH. However, none of the trypanosusceptible cattle tested positive for T. vivax. Consequently, there was no T. vivax positive Sanga and Zebu for which haematological data could be generated for comparison with T. vivax positive N’Dama and WASH. Thus, it is not possible to know if the T. vivax strains that infected the N’Dama and WASH are highly pathogenic or not. However, such absence of positives is not surprising. Livestock keepers who kept the trypanosusceptible Zebu and Sanga used trypanocidal drugs regularly to control the infection. In contrast, none of the livestock keepers who kept trypanotolerant N’Dama and WASH cattle used trypanocidal drugs to control trypanosome infection. This could explain why some of the N’Dama and WASH tested positive for T. vivax, while all the Sanga and Zebu tested negative for T. vivax.

Although the importance of keeping trypanotolerant N’Dama and WASH cattle as a trypanosomosis control measure in SSA has long been recognized (Hoste et al., 1992; Mahama et al., 2003; Pierre, 1906 cited in Agyemang, 2005), these breeds constitute only a small proportion (6%) of the cattle population of Africa and only 17% of the total cattle population in the affected areas (Agyemang, 2005). The low number of these trypanotolerant animals is attributed in part to the prevalent notion that they are not productive because of their relatively small size. Indeed, in market oriented livestock production systems, livestock keepers by reason of access to cash and consequently to veterinary inputs tend to increase the size of their cattle through crossbreeding trypanotolerant N’Dama and WASH females with trypanosusceptible Zebu bulls. This phenomenon has resulted in the emergence of stabilized crosses such as Sanga in Ghana, Borgou in Togo and Benin, Keteku in Nigeria, Djokoré in Senegal, Bambara in Central African Republic, and Méré in Côte d’Ivoire, Burkina Faso and Mali (Hendrickx et al., 2004; Hoste et al., 1992). Agyemang (2005) reviewed productivity and economic data from numerous studies (including Agyemang et al., 1991; Agyemang et al., 1997; Lhoste, 1986; Otchere, 1983; Republic of Gambia, 2002; Shaw, 2003; Trail et al., 1979a; Trail et al., 1979b; Wagenaar et al., 1986 and Wilson, 1989) and reiterated the findings that trypanotolerant N’Dama and WASH compare favourably with Zebu in terms of productivity and economic indices even in zero- to low-tsetse challenge areas. Besides the threat that tsetse transmitted trypanosomosis poses to livestock, the productivity of more than one third of the total land area in West Africa is hampered by major physical constraints, the most important being soil fertility (Hendrickx et al., 2004). Studies indicate that integration of crop and livestock production or mixed crop–livestock farming is the most sustainable means of increasing land productivity in SSA (McIntire et al., 1992; Winrock, 1992). Accordingly, trypanotolerant cattle have been recommended for low-input traditional African farming systems in areas where tsetse challenge is considered to be medium, high or very severe (Hendrickx et al., 2004; Mattioli et al., 1998; Shaw & Hoste, 1987; Snow & Rawlings, 1999).

As was clearly demonstrated in the current study, infected trypanotolerant WASH and N’Dama maintained their mean RBC values in the normal range, which confirms their trypanotolerant trait. Further, none of the livestock keepers who kept such trypanotolerant breeds used trypanocidal drugs regularly to control the infection. According to various researchers (Dayo et al., 2009; Maganga et al., 2017; Mattioli et al., 1998; Rege et al., 1994; Yaro et al., 2016), trypanotolerant breeds possess the ability to survive, reproduce and remain productive in areas of high tsetse challenge without the need for the use of chemicals to control the vector or drugs to control the parasite, despite being equally susceptible to trypanosome infection. This study thus calls attention to the need to deploy trypanotolerant WASH and N’Dama cattle in integrated tsetse and trypanosomosis control programmes in low-input traditional African farming systems in medium, high and severe tsetse challenge areas. A key component of such programs should be education of farmers on advantages of N’Dama and WASH cattle to establish and rapidly increase their numbers.

The mean values of TWBC, neutrophil and lymphocyte counts for T. vivax infected N’Dama in the present study were lower than those for the uninfected N’Dama. Authie (1993) observed that leukopenia is induced by trypanosomosis. Silva et al. (1999) reported that the main haematological changes produced by T. vivax infections in cattle in the Bolivian Wetlands and Brazilian Pantanal were anaemia and severe leucopenia. Additionally, the natural occurrence of T. vivax in cattle in Mosul, Iraq, resulted in leucopenia due to lymphopenia and neutropenia in comparison with normal range for cattle (Rhaymah & Al-Badrani, 2012). Paling et al. (1991) and Berthier et al. (2015), however, observed leukocytosis in N’Dama cattle due to trypanosome infection. The mean TWBC, neutrophil and lymphocyte counts for T. vivax infected WASH cattle in this study were higher than those for the uninfected. Similar observations of leukocytosis due to trypanosome infection have been made in rabbits (Emeribe & Anosa, 1991), vervet monkeys (Kagira et al., 2006) and Zebu cattle (Berthier et al., 2015; Van Wyk et al., 2014). Ilemobade et al. (1982) suggested that trypanosome-induced severe leukopenia could compromise the protective immunity of cattle to other diseases. High levels of neutrophils, lymphocytes and eosinophils may indicate an active infection, whereas low counts may indicate a compromised immune system (Davidson et al., 1998; Spivak, 1984). The mean TWBC counts reported in this study were within the normal values for cattle (Jain, 1993), but were lower than those reported in both T. vivax infected and uninfected Muturu cattle in Nigeria (Mbanasor et al., 2003), which were higher than the normal values for cattle. The differential WBC counts in this study were within the normal range (Jain, 1993) and agree with what has been reported by Mbanasor et al. (2003).

Conclusion

We found that in spite of the presence of natural T. vivax infection, the haematological parameters of N’Dama and WASH cattle were within acceptable normal ranges, which confirms their trypanotolerant trait. This underscores the need for low-input traditional African farmers in medium, high and severe tsetse challenge areas to be educated on their advantages in order to establish and rapidly increase their numbers for effective deployment in integrated tsetse and trypanosomosis control programmes.

Data availability

Dataset 1: Haematological parameters of T. vivax infected and uninfected WASH and N'Dama cattle at Chegbani and Cape Coast, respectively. 10.5256/f1000research.14032.d213201 (Ganyo et al., 2018).

Author information

EYG holds a PhD in Parasitology. JNB is an Associate Professor in the Department of Biomedical and Forensic Sciences, and the Dean of the School of Biological Sciences. JV is a scientist and head of the Molecular Biology and Bioinformatics Unit, International Centre of Insect Physiology and Ecology Nairobi, Kenya. DKM is the head of Animal Health, International Centre of Insect Physiology and Ecology, Nairobi, Kenya. PKT is a Professor of Veterinary Epidemiology and Dean, School of Veterinary Medicine, University of Ghana, Legon, Accra, Ghana.