Molecular epidemiology of cystic echinococcosis in human and production animals in Tunisia.
Abstract
Cystic echinococcosis (CE) or hydatidosis is a widespread zoonose in the world. In Tunisia, despite the deployed prevention program, CE remains a serious public health problem. With a human surgical annual incidence averaging 12.6/100000 inhabitants, Tunisia is one of the most endemic areas amongst the Mediterranean countries. Three Echinococcus species have been described: E. granulosus sensu stricto (G1 and G3 genotypes), E. canadensis, and E. equinus. CE, which commonly starts during childhood and described as a young adult disease, may be observed at any age. The liver and the lungs are the most commonly involved organs but the cyst can occur almost anywhere in the body. In production animals, the prevalence of CE is ranged from 16.42% to 40.42% in sheep, 8.56% in cattle, 6% in dromedaries, 2.9% in goats, and 8.48% in donkeys. The elevated number of stray and semi-stray dogs and their frequent contamination by E. granulosus infected viscera is the major cause of the CE spread. A high prevalence of E. granulosus infection has been reported in Tunisian dogs ranging from 3.75% to 27.1%, depending on the regions. Thus, the sanitary education concerning hydatidosis should be reinforced and efforts should be made to implement a targeted educational program.
Keywords
- Cystic echinococcosis
- Tunisia
- molecular characterization
- epidemiology
- public health
1. Introduction
Cystic echinococcosis (CE) or hydatidosis, caused by
2. Echinococcus granulosus genotyping
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102 | ITS1 and cox1 | G1 (100%) | [13] |
33 | 12s rRNA | G1 (100%) | [18] | |
10 | Cox1 | G1 (100%) | [17] | |
33 | Cox1 and ef1a | G1 (100%) | [16] | |
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79 | ITS1 and cox1 | G1 (100%) | [13] |
4 | 12sRNA | G1 (100%) | [18] | |
10 | Cox1 | G1 (90%); G3 (10%) | [17] | |
19 | Cox1 and ef1a | G1 (100%) | [16] | |
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50 | ITS1 and cox1 | G1 (100%) | [13] |
10 | Cox1 | G1 (90%); G3 (10%) | [17] | |
241 | ITS1 and cox1 | G1 (100%) | [15] | |
25 | Cox1 and ef1a | G1 (100%) | [16] | |
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3 | ITS1 and cox1 | G6 (100%) | [13] |
13 | Cox1 | G1 (100%) | [14] | |
11 | Cox1 and ef1a | G1 (72%); G6 (28%) | [16] | |
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37 | Cox1 and ef1a | G1 (40%); G4 (60%) | [16] |
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14 | Cox1 and ef1a | G1 (100%) | [16] |
The Tunisian situation is grossly the same as other Maghreb countries (Algeria and Libya) where the G1 and the G6 genotypes were reported in livestock and camels [19–22].
In Tunisia, the most frequent genotype associated with CE is the G1 genotype (
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U50464 | C56T | A27V | Human, Sheep , Cattle | Lung and Liver | [13] |
AY679144 | T123C | None | Sheep | Liver | [13] |
AY679145 | G312A | None | Human | Lung | [13] |
AY679146 | T204G | None | Cattle | Lung | [13] |
KM014606 to KM014644 | - | - | Camels, cattle, goat sheep, human, jackals, donkey, wild boar | - | [16] |
3. Human disease with special focus on pediatric hydatidosis
The
CE remains an important public health problem in Tunisia and despite the deployed prevention program, a slight reduction in the mean annual surgical incidence rate (SI) from 15 to 12.6 cases/100,000 inhabitants was observed during the last 20 years [6, 28]. The endemic status differs from one region to another, based on the SI, and some areas have been defined as hyperendemic (SI>22.6), holoendemic (15 < SI <22.6), mesoendemic (7.5< SI <15), and hypoendemic regions (SI < 7.5) [6]. The geographical repartition of different endemic regions was shown in Figure 2. Hydatidosis is known to be more important in rural areas where the definitive hosts (domestic and wild Canid) and herbivore intermediate hosts are in close contact, but an extension in the urban zones was noted during the past decade.
In Tunisia, several human studies were focusing on pediatric hydatidosis [15, 27, 29–31]. Cystic echinococcosis, which commonly starts during childhood or adolescence and described as a young adult disease, may be observed at any age. Two studies on children hydatid cysts (161 and 241 cysts) were carried out between 1999 and 2009 and assessed that the greatest number of cases was observed in the age groups of 4–9 years [15, 31]. Another retrospective study conducted between 1985 and 2009 and based exclusively on 757 pulmonary cysts of young children (3–7 years) and older children (8–15 years) demonstrated a mean age of 5.7 and 12 years old, respectively [27]. This early infestation has already been described in Turkey [32], Palestine [33], and Jordan [34].
In children, the lungs are the most common sites for hydatid cysts followed by the liver (Table 3) [15, 27, 31]. This could be explained by noisier and earlier symptoms in children where cough, chest pain, and hemoptysis are the most frequently encountered signs [27, 30]. Some exceptional cyst localizations (central nervous system, orbit, spleen, kidney, and heart) were also described [15, 35, 36]. Several organs may be contaminated simultaneously and about 20% of cases reported in literature were involved in multiple cysts with essentially liver associated with lung [15, 27]. The growth of the hydatid is independent of children’s age since cysts of high diameter (15 cm) were found in children of 4 years old [15, 31].
Numerous pediatric studies have noted a slight male predominance compared to girls with a sex ratio of 1.2 to 1.8 [15, 27, 28, 31]. This observation was although reported in Algeria [37], Iran [38], Bulgaria [39], and Jordan [34]. The higher infestation of boys compared to girls in endemic countries is explained by the fact that school-age boys have more external activities than girls, with a greater promiscuity with dogs. In adults, in contrast to what is observed in children, women are more commonly affected than men [28, 40, 41]. This difference is due to their role in the home activities and that in rural areas, the women are more often at home and care very often for dogs and cattle, which increases the risk of contamination. In addition, the adult females have more regular medical follow-up (e.g., during pregnancy) that results in fortuitous cyst discoveries on ultrasound examinations.
The direct examination of the cyst allows studying its fertility (presence or absence of protoscoleces) and the protoscolex viability. The cyst fertility was analyzed by light microscopic observation. Protoscolex viability was determined using vital eosin 0.2% coloration (Figure 3). The fertility of the cyst is independent of its location and its size and no relation with the age of infected children was noticed (Table 3) [15, 27, 42]. The cyst fertility and protoscoleces viability in humans are not involved in the maintenance of the parasite life cycle because human is a dead-end host but they are parameters attesting of the perfect adaptation of the parasite to humans.
As mentioned before in the genotyping section, the most frequent species associated with human hydatidosis is the
4. Cystic echinococcosis in production animals
Livestock echinococcosis leads to economic repercussions because of animal liver and lung condemnations, decrease of the carcass weight, animal fertility, and milk production [43]. In Tunisia, breeding remains mainly traditional and the population practices extensive sheep farming. Livestock are ubiquitous all over Tunisia, especially in rural areas and about 4 million sheep female unit (FU), 700,000 goat FU, 420,000 cattle FU, and 17,000 camel FU are recorded [44]. The CE prevalence in food animals depends on the presence of the intermediate host of the parasite and their close contact with the final host (stray and semi-stray dogs). These intermediate hosts differ from one region to another in function of climatic factors and/or breeding or alimentary practices. Thus, dromedary breeding is essentially located in Southern Tunisia (desertic climate) where camels are most consumed, whereas sheep and cattle breedings are practiced throughout the country. Herbivores acquire the infection through ingestion of
CE prevalence in production animals was estimated by post-mortem examination of slaughtered animals at abattoirs. A series of studies carried out in Tunisia assessed that the prevalence of
Liver and lung are the only organs observed to be infected in production animals. The prevalence of the liver localization of the cyst was higher than that of pulmonary cysts except for the dromadaries where the pulmonary cysts are predominant (Table 4) [14, 45, 46, 53]. The co-infection of both organs in the same host is frequently observed and, contrary to what is usually described in humans, several cysts (up to 50 cysts) may develop in the same organ (Figure 7).
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Sheep | 2722 | 16.42 | Liver | 54.97 | 19.24 | 74.94 | 2003-2010 | [45] |
Lung | 45.02 | 11.01 | 66.49 | 2003-2010 | [45] | |||
1039 | 40.42 | liver | 40.42 | - | - | 2001-2004 | [45] | |
248 | - | Liver | 67.33 | 86 | - | 2000-2005 | [53] | |
- | Lung | 32.66 | 63 | - | 2000-2005 | [53] | ||
Cattle | 3913 | 8.56 | Liver | 62.58 | 0.55 | 67.9 | 2003-2010 | [45] |
Lung | 37.41 | 0.40 | 89 | 2003-2010 | [45] | |||
203 | - | Liver | 60.6 | 76.5 | - | 2000-2005 | [53] | |
- | Lung | 39.4 | 27.5 | - | 2000-2005 | [53] | ||
Goat | 3779 | 2.88 | Liver | 67.82 | 15.57 | 25.63 | 2003-2010 | [45] |
Lung | 32.14 | 14.75 | 14.8 | 2003-2010 | [45] | |||
Dromed-aries | 404 | 5.94 | Liver | 86.27 | 22.22 | 65.86 | 2003-2010 | [45] |
Lung | 13.72 | 22.22 | 13.72 | 2003-2010 | [45] | |||
291 | 6.5 | Liver | 7.69 | - | - | - | [14] | |
Lung | 92.30 | - | - | - | [14] | |||
8 | - | - | - | 100 | 100 | 2000-2005 | [53] | |
Donkey | 2040 | 8.48 | Liver | 89.9 | 3.58 | 35.80 | 2006-2007 and 2009 | [47] |
Lung | 10.09 | 15.38 | 32.96 | 2006-2007 and 2009 | [47] |
However, available CE prevalence in livestock species does not reflect the real endemic situation since it is not considered private or illegal slaughtering. Uncontrolled home slaughtering during religious or local festivities is very common in Tunisia and the infected viscera unsuitable for consumption are rejected and eaten by dogs. The knowledge of the parasite cycle and its transmission modalities are weak, in spite of a perception of the risk notably in rural areas. For example, a study conducted in 2007 (76 patients, 90 and 100 humans from urban and rural areas, respectively), has demonstrated that 40% of topics interrogated have the false notion that the humans’ contamination is consecutive to the consumption of viscera containing hydatic cysts, whereas only 25.8% among them incriminate the dog [54]. The livestock trade in Tunisia is mainly based on weekly markets and exchange of animals all over the country. Thus, the lack of information on the exact geographical origin of livestock makes very difficult the identification of grazing areas at risk and the targeting of prophylactic measures.
Molecular analyses have demonstrated that
5. Echinococcus in dogs
The CE is highly endemic in many North African countries and very high infection rates have been reported in dogs (55–58% in Morocco [49], 20–25.8% in Libya [57] and 19–42% in Algeria [58]). In Tunisia, although a sylvatic life cycle involving wild carnivores (golden jackals and red foxes) as definitive hosts was described [59], the
In rural, urban, and semi-urban areas, the canine density is one dog per 3.0 to 5.5 inhabitants, one dog per 16 inhabitants and one dog per 46 inhabitants, respectively. In urban regions, less than 20% of households own a dog, whereas in rural regions there are 7–30 dogs per km², and more than 80% of households own at least one dog [61].
The prevalence of
The study of the vital areas of stray dogs, based on 52 to 285 locations in a semi-urban area of Tunisia, has identified an area ranging between 0.06 and 8.53 km² [61]. Thus, considering that the average number of worms per dog is estimated at several thousands [59] and more than 8,000
6. Conclusion
Despite the control programs, essentially based on the systematic condemnation of infected offal in slaughterhouses, cystic echinococcosis remains a major public health in Tunisia. The endemic status differs from one region to another, and some areas have been defined as hyperendemic, holoendemic, mesoendemic, and hypoendemic regions. Hydatidosis is important in rural areas but an extension in the urban zones was noted during the past decade. The characterization of the species responsible for echinococcosis in Tunisia is a significant point that has to be taken into consideration in order to focus and to adapt the control measures. Three
Acknowledgments
The authors thank Imen Hizem-Attig for her assistance with the linguistic part of this paper.
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