Abstract

INTRODUCTION

The livestock industry is a major source of income and livelihood for most Nigerians, who are rural settlers, and contributes approximately 5.2% to the National Gross Domestic Product [1]. In Nigeria, the practice of moving cattle and small ruminants under a semi-extensive system is still common. In rural areas of southern Nigeria, a subsistence management system is mostly practiced as many farmers allow their animals to move freely within the community, searching for food and water [2]. Similarly, many ‘local’ dogs move around the villages and towns untamed, which exposes these roaming/moving animals to a high risk of acquiring a range of parasites through various sources [3]. Several factors (environmental, nutritional, immunological, and grazing system) could influence parasitic disease conditions in animals [4,5].

The parasites acquired by these animals can adversely affect their economic value and pose serious public health challenges [6,7,8]. The effects of parasitic infections could be exacerbated in places where there is little or no veterinary care with inadequate policies on disease control [9], which is largely the case in rural Edo. In Nigeria, most studies reporting the prevalence of intestinal parasites in a locality indicate that the samples were from abattoirs [10]. The implication is that some of the prevalence results, including the parasite distribution, may misrepresent the local situation because many of the animals in abattoirs within southern Nigeria are not sourced from local breeders.

Thus far, studies on the prevalence of helminths infections among small ruminants and cattle in Nigeria have shown a significant level of heterogeneity [10]. However, there is a paucity of data on the prevalence and distribution of intestinal parasites in roaming/stray and migrating animals (goats, sheep, cattle, and dogs) in Edo state. In this case, sample collection was not concentrated in a location but obtained across all local government areas (LGAs) within the state to represent the general prevalence and spread of various parasites. These data are expected to assist in intervention programs for parasitic disease control [11] and provide insights into the parasites likely to affect public health. In addition, this study used molecular tools to identify Toxocara canis as the major potential parasite of dogs in the state.

MATERIALS AND METHODS

Study area

Edo State (6.6342°N, 5.9304°E) is in South-South Nigeria with an area of 17,802 km² that comprises 18 LGAs (Fig. 1). Edo is largely rural with a rainforest vegetation type. Two seasons are seen: dry (November to March) and wet (April to October). Many homes in Edo, especially those in rural communities, rear goats and sheep at the subsistence level that are allowed to stray, while cattle rearing is done by more economically endowed persons. Cattle are moved regularly from one point to another in search of food and water. Dogs are seen roaming house premises, streets, and in unfenced schools.

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Fig. 1

Map of Edo showing sampling locations.

LGA, local government area.

RESULTS

Compared to the other groups of parasites, the prevalence of nematodes in goats was higher in 14 LGAs, while protozoan parasites occurred the most in 4 LGAs (Table 1). The number of goats in which trematodes were isolated was relatively low (4.66 ± 1.63, 95% CI, 1.21–8.12). On the other hand, the infection pattern with trematode by LGA showed that most LGAs in the central region recorded non-positive results. In most LGAs in southern and northern Edo, some goats tested positive for trematodes (4.66 ± 1.63, 95% CI, 1.21–8.12). Moneiza spp. were isolated in a goat from Ovia North East. The parasite prevalence in goats was higher with nematodes (37.71 ± 5.27, 95% CI, 28.66–50.83) than protozoans (24.02 ± 4.64; 95% CI, 15.59 ± 35.18), but the difference was not statistically significant.

More protozoan parasites were isolated in sheep than other groups of parasites in 10 LGAs (Table 2). In the other 8 LGAs, nematode parasites were more prevalent than other groups of parasites. Trematodes were isolated in 7 LGAs (4.55 ± 1.91, 95% CI, 0.51–8.58). Cestodes (Moneiza spp.) were recovered in samples from 2 LGAs. The prevalence was higher with nematodes (45.07 ± 5.95, 95% CI, 23.04–48.18) than protozoans (32.53 ± 4.64, 95% CI, 18.76–38.34) but not statistically significant.

Nematodes recovered from cattle were most prevalent in 5 LGAs, while protozoan parasites were most common in 4 LGAs (Table 3). Trematodes were isolated in Esan North East only. The prevalence of nematodes in cattle was significantly higher (22.17 ± 6.41, 95% CI, 10.62–37.82) than protozoan parasites (13.91 ± 3.26, 95% CI, 7.49–21.35) (t = 1.36; p = 0.04).

Nematodes were isolated in dogs located in 12 LGAs, while protozoan parasites were recovered in dogs from 9 LGAs (Table 4). Trematodes in dogs were observed in 2 LGAs. The prevalence of nematode parasites in dogs was higher (10.54 ± 2.75, 95% CI, 5.15–16.91) than protozoans (4.29 ± 2.41, 95% CI, 1.54–11.81), but the difference was not significant.

Eighteen parasites were observed (Table 5). For small ruminants, among the nematode parasites recovered, Haemonchus was most prevalent, followed by Strongyloides, while Eimeria had the highest prevalence among protozoans. Trematodes were relatively rare, but Fasciola was more prevalent. For cattle, Strongyloides were most prevalent among nematodes, followed by Bunostomum spp., while Eimeria was most prevalent among protozoans. Frequently occurring parasites in dogs among nematodes were Strongyloides, hookworm, and Toxocara, while Eimeria was observed the most among the protozoan group. Trematodes (Fasciola and Schistosoma) were relatively rare in few dogs.

Two dog samples were sequenced and showed 99.66% similarity, with differences in only 2 nucleotide sites: positions 54 and 410. The final and usable sequences were 583 bp long. The T. canis nad1 sequence obtained was deposited in the GenBank database under accession numbers MN635719 and MN0635720. Phylogenetic analysis revealed more than 99% similarity with the samples from Europe (EU730761) and China (AM411108) (Fig. 2).

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Fig. 2

Maximum-likelihood phylogenetic tree of Toxocara canis from dogs in Edo, Nigeria inferred using partial nad1 mitochondrial gene. sequences (529 bp). Sequences from this study are asterisked (*). Where available, ‘host’ and ‘country’ of isolation are added to each of the GenBank sequences. Figures on the branches are bootstrap probabilities (in %) based on 1,000 bootstrapped trees.

DISCUSSION

The West African Dwarf (WAD) is the major goat breed in the state. Nematodes (Haemonchus and Strongyloides) followed by protozoan infections (Eimeria) were the most common in these goats with Fasciola spp. being highest among trematodes. Haemonchus has been reported to have little impact on the health status because of the resistance of WAD to such infections [16]. On the other hand, one study reported the pathologic impact of Haemonchus on WAD because it significantly reduced the packed cell volume, body weight, and body condition score [17]. Similarly, infections with Strongyloides could lead to a gamut of symptoms (maceration of pedal skin, diarrhea, dehydration, anorexia, and anemia) [18], including death in some heavy infections [19]. Most reported coccidian infections among goats are due to Eimeria spp. Although goats can be parasitized by 16 different Eimeria spp., most do not cause visible clinical coccidiosis [20]. E. ninakohlyakimovae and E. arloingi are considered the most pathogenic species [21]. The incidence of infections with Fasciola spp. was higher than other species of trematodes, of which its presence could cause huge economic losses [22]. The host animals are at high risk of infection with Fasciola when they ingest contaminated vegetation close to or within the water bodies [23].

The breed of sheep observed in Edo is predominantly WAD, having similar infection patterns to goats. Although results showed a higher infection rate in sheep than goats for both nematode and protozoan infections (Tables 1 and ​and2),2), the signs and symptoms of infections are closely related in most cases. Eimeria occurs more in sheep than other animal hosts and is clinically characterized by diarrhea, while growth impairment has been reported in the subclinical form [24,25]. The pathogenic species of Eimeria in sheep are E. ovinoidalis, E. ovina, E. crandallis, and E. ashata [26].

The 2 most frequently occurring parasites in these migrating cattle were Strongyloides and Bunostomum spp. As these cattle move within the community in search of pasture, they litter the environment with feces, thereby exposing the inhabitants to a risk of infections. Filariform larvae of Bunostomum spp. can penetrate the skin and potentially cause cutaneous larva migrans, while some others could move into deeper body tissues resulting in visceral larva migrans.

The major nematode parasites isolated from these roaming/stray dogs were Strongyloides spp., hookworms, and Toxocara spp. The clinical signs of dogs with Strongyloides spp. include asymptomatic to severe conditions [27]. The zoonotic potential of Strongyloides stercoralis has been reported in dogs [28], which may be the case in Edo. Canine hookworm infections can pose a risk to humans because hookworm species recovered from dogs were also seen among residents in close contact [29]. Two dog samples were identified as T. canis, and being a zoonosis, humans could acquire infection via the ingestion of embryonated/larvated eggs in the soil or contaminated food [30]. Although infections in humans can be asymptomatic, extra-intestinal pathologies may be seen [31].

In the communities surveyed, goats and sheep may harbor zoonotic parasites. They are allowed to move and defecate within home premises and wander farther from their residence to areas, such as schools that are not fenced [8]. Consequently, children play with soil within and around home premises and even in open fields in schools, exposing them to potential zoonotic infections. These animals should be treated regularly, and the practice of intensive breeding systems should be encouraged. Open grazing, which demands many cattle movements within the communities, poses a serious threat to human health. Therefore, open grazing in Nigeria should be discouraged and replaced with absolute ranching systems. In managing hookworm and other major parasites of dogs, as it relates to public health, dog-roaming should be discouraged through local policies in which mandatory provision of shelter and restricted movement of pets are strongly advocated. With these approaches, the possible risk of human infection would be reduced significantly [32].

The traditional method (microscopy) used for diagnosis in this study is limited to ova/oocyst and larva identification. Consequently, the species presence and profile may have been marginally under-reported. On the other hand, as this is the first comprehensive survey for the state, we believe that these results have enriched epidemiological data with the potential of stimulating further studies. As culturing some parasites for identification purposes is laborious and requires special skills, future studies should incorporate complementary microscopy. Furthermore, although T. canis was confirmed by sequencing, all other major parasites (Haemonchus, Strongyloides, Hookworm, Bunostomum, Eimeria, and Fasciola) recovered should be profiled at the species level. If this can be achieved, a clearer picture of the level of zoonotic infections occurring in these animal hosts can be obtained. In addition, by deploying molecular techniques in epidemiological studies, disease mapping becomes more reliable, and targeted approaches with anthelmintics can be adopted easily. This targeted anthelmintic application can reduce the rate of parasite resistance to anthelmintic drugs caused by overuse, in addition to providing greater protection for consumers of animal products.

ACKNOWLEDGEMENTS

Footnotes

References