Dogs are the most successful canids, adapted to human habitation worldwide. They have contributed to physical, social and emotional well-being of their owners, particularly children 12. However, in spite of the beneficial effects, close bonds of dogs and humans (in combination with inappropriate human practices and behaviour) remain a major threat to public health, with dogs harbouring a bewildering number of infective stages of parasites transmissible to man and other domestic animals 234. For example, well-known and important zoonotic diseases are cutaneous and visceral larva migrans, hydatid disease and tungiasis 5678.

In low-income settings, treatments to eliminate these parasites are – if done at all - often applied in advanced stages of disease, causing distress on pets and their owners 910.

In many African countries, including Nigeria, appropriate policies regarding pet ownership and their effects on individual and community health are nonexistent. Prevalence of parasite infection in dogs with importance for human health is usually high, resulting in risk of zoonotic transmission from dogs to humans. The risk is further increased by non-favourable ecological and human behavioural factors 111213.

Previous epidemiological studies on dog parasites in Nigeria were focused on the prevalence with little or no information on quantitative measure of infection and/or were not community-based 14151617. Thus, we examined a representative population of dogs in urban and rural areas in a Nigerian city for the presence of possibly zoonotic parasites.

A total of 396 dogs, consisting of 180 (45.5%) males and 216 (54.5%) females was examined; 192 (48%) dogs lived in urban, and 204 (52%) in rural areas.

All dog owners agreed to participate and completed the questionnaires. Table 1 summarizes the differences in dog regimen and the perception of dog owners to diseases transmissible by their animals, stratified by urban and rural areas. In the rural area, significantly more individuals kept dogs for hunting and observed their dogs catching prey than in the city (p < 0.0001), whereas 29.2% and 18.1% of dog owners in the urban and rural areas kept dogs as watch dogs, respectively (Table 1). Treatment with antiparasitic drugs was a more frequent practice for dogs from urban than rural areas.

Interestingly, more than half of dog owners in the rural communities, and about a third in the urban area did not perceive diseases transmitted by dogs as a health problem (p < 0.0001). The bonds of humans with their animals were close, and children played with virtually all dogs included in the study (Table 1). When asked about possible diseases transmitted by their dogs, less than 10% of owners mentioned helminths ("worms") as a health problem, but about two third were aware of the risk of rabies transmission (Table 1).

The present study provides the first systematic assessment on quantitative estimates of parasites in dogs in Nigeria's Kwara State. The results show that ectoparasitic and intestinal helminth species were abundant, and that prevalence and density of infection was very high. The knowledge and perception of dog owners regarding zoonotic diseases transmitted by pets was insufficient.

The parasites reported in this study have been previously documented in dogs throughout the world, with a pronounced difference in prevalence and density between regions 16172021222324252627. In our study, the overall prevalence of intestinal helminths (68%) was similar to that reported from different ecological and epidemiological settings in Nigeria 1726 and to the prevalence of 71% reported from Spain 28. In South Africa (76%), Mexico (85%) and Morocco (100%), prevalences were even higher 222329.

This potential for human zoonotic disease has rarely been addressed in control programs in Nigeria and other low income countries. Considering the high prevalence of ectoparasites and intestinal helminth infections found in dogs, and the close bonds in which dogs live together with people, the risk of transmission of these parasites to humans seems to be obvious. For example, Toxocara infection in humans may cause visceral larva migrans, in severe cases leading to blindness 30, and dog hookworm infections put humans at risk for cutaneous larva migrans which is endemic in many resource-poor communities 31. Rhipicephalus ticks have been described to parasitize humans 32, and may transmit rickettsial disease and visceral leishmaniasis 33. Fleas may transmit human plague, rickettsioses and trypanosomes 34, and serve as intermediate hosts for the dog tapeworm, D. caninum.

Our data show that the prevalence pattern was age-dependent; T. canis decreased with age of dog, whereas A. caninum, T. vulpis, Taenidae, D. caninum and Strongyloides sp. increased with age, even though to a less extent. These patterns have been observed previously 1617202327. In Nigeria, Sowemimo and Asaolu 27 found by far the highest prevalence of toxocariasis in puppies, whereas the age dependency of hookworm infection was less pronounced. The high prevalence of ascarid infections in puppies is in accordance with the transmission pattern of the parasite, which is mainly by transplancental and transmammary routes; acquired age-dependent immunity may be caused by repeated exposure 3536. Increased infection rates in older dogs are caused by parasite species which are not transmitted to dogs at early age, and thus do not elicit a specific immune response.

The prevalence detected in our study differs from those of Sowemimo and Asaolu 27 who recorded 24% in a Nigerian city in a neighbouring state with similar characteristics as Ilorin. However, these data were not population-based, but included dogs presented to veterinary clinics. These authors also argued that the reduction of prevalence as compared to a study done in the 1970s 31 may be caused by increased awareness of pet holders regarding deworming practices. In contrast, our data can be regarded as representative for the dog population, as pet owners who bring their animals to veterinary clinics may deworm their animals more regularly. As a consequence, studies based on veterinary clinics underestimate prevalence of parasitic infections and infestations. Our data, though, show that the majority of dogs received antiparasitic treatment never or more than a year ago, and only few people were aware of the zoonotic potential of dog parasites; 60% of dogs examined had never visited a clinic for any form of treatment.

The reduced prevalence of D. caninum over time was claimed to be caused by the reduced prevalence of the intermediate host C. canis. This may hold true for pets brought to veterinary clinics, but our study shows that C. canis is very common in dogs in the community and thus probably continue being important for the transmission of D. caninum.

The intensities of T. canis, Taenidae and D. caninum were statistically higher in rural dogs than those in the urban area. Similarly, Habluetzel et al. 38 observed that twice as many dogs from rural areas had nematodes infections, as compared to urban dogs. These differences in the level of infection from different locations have been described also in other studies 3940 and may be partly due to variation in local environmental conditions affecting spatial aggregation and infective stages of parasites. Besides, differences in health care and animal management practices may account for these differing characteristics. Urban dog owners may feel encouraged by their proximity to veterinary clinics, which are nonexistent in rural areas.

The number of intestinal parasite species per host revealed that single infection was more common; polyparasitism with more than two parasites species was less frequently observed. A similar pattern was observed in ectoparasite infestation. These results are in agreement with Fontanarrosa et al. 24 who explained that interactions among parasite species depend on parasite burden rather than the mere presence of other species.

The high prevalence of ectoparasites (60%) was consistent with another study, where fleas and ticks were the most commonly found taxa 41. Ugochukwu and Nnadozie 42 recorded in Bendel State (Nigeria) a low prevalence of ectoparasites in dogs, including Demodex canis, R. sanguineus and C. canis. Bryson et al. 43 identified several species of ixodid ticks, fleas and lice from dogs in South Africa. However, C. felis and Echidnophaga gallinacea which were frequently reported in dogs in other study areas 39424344 were not encountered in our study.

The variation in distribution and prevalence of ectoparasites can be ascribed to differences in the availability of infective stages, host habitat/climatic factors and the sampling period. Peak prevalences of ectoparasites usually occur during the warm dry months 404546. Gracia et al. 40 revealed that accumulation of organic wastes and the presence of other pet animals influence the survival and abundance of ectoparasites, especially fleas. This also explains why P. irritans and T. penetrans, relatively low host-specific ectoparasites, occurred only in rural areas, where dogs were frequently in contact with other natural host animals, such as pigs, rats and small ruminants 474849.

Unfortunately, due to the absence of funding, we were unable to identify the prevalence of other zoonotic diseases and to specify the species in Taenidae encountered, such as Echinococcous granulosus causing hydatid disease. The diagnostic technique of parasites done in this study, based on the morphological characteristics of ova under light microscope, has the disadvantage that it fails to distinguish E. granulosus from other Taenidae. Thus, E. granulosus, a major zoonotic parasite of livestock and dogs in Nigeria 111415, has possibly been present but not reported in our survey. The fact that dogs enjoy unrestrained association with humans, scavenge for food in an environment contaminated with faecal material of potential intermediate hosts and feed on offal of slaughtered livestock in abattoirs (Ugbomoiko, personal communication) makes transmission of hydatid disease predictable in the setting studied.

In general, the trend in prevalence, density and species composition of parasites observed in this study may reflect the degree of environmental contamination and inequalities in the health care service between urban and rural areas. In particular, T. canis, A. caninum and D. caninum are zoonotic parasites constituting public health problems in the study areas.

Our study shows that parasites of importance for human health were highly prevalent in Nigerian dogs and that intervention measures are necessary to reduce the risk of transmission of parasites from dogs to humans. Interventions should focus on health education provided to dog owners and the establishment of a program based on zoonotic diseases.

USU: study design, conducted the study, statistical analysis, contributed to the manuscript; LA: statistical analysis, contributed to the manuscript; JH: study design, statistical analysis, contributed to the manuscript. All authors read and approved the final manuscript.