Introduction

Echinococcus granulosus is one of the smallest cestode parasites that cause cystic echinococcosis, which is of major public health importance worldwide. The distribution of E. granulosus is higher in developing countries especially in rural communities where there is close contact between the dogs, the definitive hosts, and various domestic animals, which may act as intermediate hosts (Eckert and Deplazes 2004; Radfar and Iranyar 2004). The outcome of infection in livestock is hydatid cyst development in the lung, liver or other organs (Eckert and Deplazes 2004; Jenkins et al. 2005). It has been suggested that E. granulosus may be maintained in an independent wildlife cycles in East Africa (Magambo et al. 2006). Cystic echinococcosis (CE) is highly endemic in sub-Saharan Africa. It has been reported in West African as well as the North African countries (Ahmad 2005). In all these areas, CE is prevalent in humans among the nomadic pastoralists (Magambo et al. 2006). The incidence in any country is closely related to the prevalence of the disease in domestic animals and is highest where dogs population is high (Magambo et al. 2006).

Studies in different parts of East Africa have shown varied distribution of CE. A recent study among the Karamojong community in Uganda has shown an average of 20 surgical cases of CE per year (Macpherson et al. 2004). In Turkana, the prevalence of CE in humans is about 2.5% (Zeyhle et al. unpublished data 2005) while Macpherson et al. 1989) reported a prevalence of 1.4% in Maasai people of Northern Tanzania. Hydatidosis has been recorded from several localities in the region. The most affected areas were the rural communities occupied by pastoralists and agro-pastoralists. Njoroge et al. (2002) reported a prevalence of 19.4%, 3.6%, 4.5% and 61.4% in cattle, sheep, goats and camels respectively in Kenya. The disease was also reported in domestic and wildlife in Uganda (Ocaido et al. 2004). Ngowi et al. (2004) reported a prevalence of 4.3% in pigs in northern Tanzania.

In Tanzania however, there is scanty information regarding the disease in both human and domestic animals. Ngorongoro district is one of the areas with large number of pastoralist societies who are normally considered to be the victims of the disease together with their animals. In order to design an effective control program, there is a need for reliable epidemiological data about the level of infection in various domestic animal species and the knowledge on risk factors that perpetuate the disease in the given locality. Therefore, the purpose of this study was to establish the prevalence of hydatidosis in livestock in Ngorongoro district through slaughter slabs survey.

Materials and methods

Study area

The study was conducted in Ngorongoro district of Arusha region, Northern Tanzania. The district is divided into two major parts, Loliondo Game Controlled Area and Ngorongoro Conservation Area. This is a multiple land use wildlife controlled area with total human population of 129,776 (Tanzania National Census 2002), inhabited predominantly by Maasai who practice traditional pastoralism, and of recently limited cultivation. Estimates of domestic dog densities, determined from the number of dogs per Maasai boma varied between 0.38 to 0.46 dogs/km2 from 1992 to 1994 (Cleaveland et al. 2003).

Geographically, Ngorongoro district is positioned between longitude 35° and 36°E and latitude 2° and 4°S. Climatically, the district has both unimodal and bimodal rainfall patterns, with short rains starting in September and ending in December and long rains starting in March and ending in May/June. There are significant variations in rainfall distribution between highlands and lowlands. The highlands are bimodal and receive between 800 mm to 1,200 mm of rainfall and lowlands are unimodal receiving 500 mm to 700 mm of rainfall. The mean monthly temperature is 20°C, however during the cooler period (June - August) the mean average temperature drops to 17°C.

Study animals and sampling method

The study was both retrospective and prospective. Secondary data on previous meat inspection were retrieved from veterinary office records on the proportion of carcasses affected with hydatid cysts as from January 1998 and October 2001.

In prospective part, a questionnaire survey was used to determine the awareness of the people with regard to hydatidosis. A total number of 64 households were interviewed using pre-tested structured questionnaire. The households were purposively selected based on their accessibility and willingness to participate in the study. Furthermore, a nine month meat inspection was done in five slaughter slabs namely Loliondo, Endulen, Nainokanoka, Makao and Olbalbal in which cattle, goats and sheep were centrally slaughtered. Home slaughters were also inspected. In the slaughter areas, thorough meat inspection was carried out with much empahasis on lungs, liver, spleen and heart. Each organ was assessed macroscopically either by visual inspection or palpation and where necessary one or more incisions were made in order to detect small hydatid cysts.

Hydatid cyst characterization: The infected organs from each positive animal were collected and recorded including the cyst location, morphology and volume of the fluid contents. Of the collected samples, individual cyst was carefully, opened and examined to identify whether it was a hydatid cyst and whether it was fertile, sterile or calcified. After opening, the cyst fluid was aspirated by using a 20 ml syringe to measure the volume of the cyst fluid. A drop of the cyst fluid was placed on the microscope glass slide and covered with cover slip and observed for presence of protoscolices on light microscope with X10 to X40 objective. For clear vision a drop of 0.1% aqueous eosin solution was added to equal volume of cyst fluid on microscope slide with the principle that viable protoscolices should completely or partially exclude the dye while the dead ones take it up. Infertile cysts were further classified as sterile or calcified. Sterile hydatid cysts were characterized by their smooth inner lining usually with slightly turbid fluid in its content with dead or without protoscolices. Typical calcified cysts produced a gritty sound feeling up on incision.

Data were analysed using Epi Info version 6 statistical software (Coulombier et al. 2001). Using statcalc, proportions of categorical variables were computed and further compared using chi-square test at critical probability of P < 0.05. The strength of associations between dependent and independent variables were determined using 2 × 2 contingency tables.

Results

Retrospective study results

A total of 6331 domestic livestock were slaughtered and inspected in the period between 1998 to 2001. All slaughtered animals were adult and included 2677 cattle, 3047 goats and 607 sheep. The overall prevalence of hydatidosis was found to be 47.9%. Furthermore, Loliondo area had the highest prevalence of the disease (51.7%) followed by Makao (50.0%), Nainokanoka (48.1%) and Endulen (26.5%) (Table 1). A significantly (p < 0.001, X2 = 128.7) higher infection rate was recorded in goats (48.1%) than in cattle (42.3%) and sheep (9.6%). The distribution of the cysts by organs showed that lungs (69.2%) were the most affected organ, followed by the liver (28.5%), spleen (2.3%) and there were no cysts on the heart.

Table 1 Prevalence of hydatidosis in Ngorongoro district, a retrospective study
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Prospective results

  1. (a)

    Questionnaire survey results

A total of 64 households were interviewed during the study period. It was found that 11 (17.2%) of the respondents were aware of the disease. Neither of the respondents were knowledgeable of the transmission between human and livestock. Furthermore, it was found that, 54 (84.4%) of the respondents had livestock including cattle, goats, sheep and donkeys while 57 (89.1%) had dogs. Of the households which had dogs, 11 (19.3%) had their dogs dewormed at least once during lifetime. Fifty (87.7%) households managed their dogs under free range system and 44 (77.2%) reported that school children (7-17 years) were the closest dog’s friend in the family. Home slaughter of food animals was preferred 58 (90.6%) than public slaughters. Up to 55 (85.9%) of the respondents reported to feed raw condemned materials to their dogs.

  1. (b)

    Meat inspection results

The total of 1081 livestock including cattle (357), goats (619) and sheep (105) were inspected. The overall prevalence of hydatidosis in slaughtered livestock was 456 (42.2%). Higher prevalence was observed in sheep 67 (63.8%) than cattle 174 (48.7%) and goats 255 (34.7). There was a significant difference in prevalence between species (p < 0.001, X 2 = 40.5). Location wise, the highest prevalence of hydatidosis was found at Makao (61.8%), followed by Olbalbal (44.3%), Nainokanoka (43.5%), Loliondo (35.9%) and Endulen (31.7%) (Table 2). There was a significant difference in the prevalence of the disease from one location to another (p < 0.001, X 2 = 40.7). Table 3 summarizes the location of cysts in inspected animals. Most of the cysts were located in the lungs (61.4%) and liver (28.5%) and were spherical in shape, unilocular and of variable sizes with cyst fluid ranging from 10 ml to 2000 ml.

Table 2 Prevalence of hydatidosis in different locations recorded in the prospective study
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Table 3 Location of cysts in the different animal species examined
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It was observed that there were a total of 116 (25.4%) fertile, 302 (66.2%) sterile and 38 (8.3%) calcified cysts (Table 4). The category of cysts by animal species is summarized in Table 5

Table 4 Category of cyst by organs of origin
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Table 5 Category of cysts by animals species
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Discussion

The findings of this study shows higher prevalence of hydatidosis in cattle, sheep and goats slaughtered at different slaughter slabs in Ngorogoro district. The overall prevalence of hydatidosis in the district observed in this study was 47.1% which is higher than that reported by WHO/OIE (Anonymous 2001) and Njoroge et al. (2002) in the Sub-Sahara Africa regions that showed prevalence between 1% to 10%. However, similar higher level of infection rates of hydatidosis was reported by Kebede et al. (2008) in Ethiopia, Elmahdi et al. (2004) in Sudan and Azlaf and Dakkak (2006) in Morocco. In contrast, a low prevalence of hydatidosis was reported in cattle, sheep and goats in Libya (Kassem 2006) and Algeria (Bardonnet et al. 2003). The differences in prevalence of hydatidosis may arise due to differences in environmental conditions that are conducive for the perpetuation of the parasite, abundance of infected definitive hosts, livestock husbandry, stocking rate, nature of the pasture and grazing patterns of animals. Generally, the prevalence of hydatidosis in Ngorongoro district may therefore reflect the actual situation of the same disease in other pastoral areas of the country where very little or no studies have been done.

This study has shown a remarkable variation in the prevalence of hydatidosis among locations within the district with the highest prevalence being recorded at Makao. The reason for the differences is not very clear, but may be due to the fact that Makao is a tourist center with high demand for meat such that animals slaughtered were from different locations within and outside the district, while animals slaughtered in other areas were from within the locality. Generally the variation in prevalence rate among different geographical regions could be ascribed to the strain differences of E. granulosus that may exist (McManus 2006). Other factors like difference in culture, social activities and attitudes to dogs may contribute to this variation (Craig and Zbigniew 2002; Arbabi and Hooshyar 2006).

Assessment of organ distribution of cysts indicated that in all the study areas, lungs (61.4%) and liver (28.5%) were the most frequently infected visceral organs in all the species. This is in agreement with the finding by Njoroge et al. 2002. This shows that the liver and lungs are the most common sites of hydatid cysts in domestic ruminants. The reason may be due to the fact that the lungs and liver posses the first great capillaries sites encountered by the migrating echinococcus oncosphere (hexacanth embryo) which adopt the portal vein route and primarily negotiate hepatic and pulmonary filtering system sequentially before any other peripheral organ is involved.

In examining the condition of cyst viability, it was revealed that, a higher proportion of the cysts were sterile (66.2%) and moderate proportions were fertile (25.4%). The cyst fertility rates was variable and high in sheep (38.8%), goats (24.7%) and cattle (21.3%) as was also reported by Dalimi et al. (2002) and Kebede et al. (2008). Thus the three hosts appear to be important intermediate hosts of E. granulosus in Sub-Sahara Africa. This finding contradicts that reported by Macpherson (1985) that cattle are poor hosts for E. granulosus and may therefore not be an important source of infection to dogs. The variation in fertility rate among different species and in different geographical zone could be due to the differences in strain of E. granulosus (McManus 2006). The greater infectivity of hydatid cysts from sheep and goats and the common practice of backyard slaughter may reflect their importance as intermediate hosts for the perpetuation of the domestic cycle of E. granulosus in the Ngorongoro district. Moreover, the higher fertility rates which was observed in this study in all infected animal species highlights the hazards that these animals may pose indirectly to people in Ngorongoro district and possibly other parts of the country where the pastoralism is practiced.

The study showed that majority (82.8%) of the respondents was not aware of hydatidosis and all were not knowledgeable on the transmission of the disease between human and livestock. This finding is in agreement with other studies in the world that have reported ignorance of the community as one of the risk factor for the existence of the disease in rural areas (Craig and Zbigniew 2002). It was further observed that majority of households (84.4%) in Ngorongoro district had livestock including cattle, goats, sheep and donkeys which are the intermediate host of the cestode parasite. Similarly, many households (89.1%) had dogs which were not dewormed regularly and were managed under free-range system. Backyard slaughter of small ruminants and disposal of raw condemned organs through offering to dogs were the common practice, a situation which may lead to the increased environmental parasitic load. Furthermore, school children (7-17 years old) being the closest friends of dogs signifies that they were a group at high risk of getting the infection. Indeed, our own data (Ernest et al. unpublished) showed that up to 76% of CE in humans in Ngorongoro district were diagnosed in school children.

It is therefore concluded that owing to the presence of socio-economic conditions favorable for hydatidosis and high level of infection in livestock signifies that the disease is of great importance in Ngorongoro district. This warrants serious attention for its prevention and control. We therefore advice the government to enforce legislation on meat inspection, improving the slaughter slabs, restrict backyard slaughter and improve veterinary services. However, public health education about the disease and its control is highly recommended to the community. The findings of this study merit for more extensive epidemiological investigations involving livestock, dogs, wildlife and humans within and outside the study area.