Potential control of the infective stage of Taenia pisiformis using Bacillus thuringiensis GP526 strain

Parasites that infect farm animals contribute to establish poverty belts, disease and malnutrition, in a similar manner to parasitosis in humans (Rist et al., 2015), especially in poor and sparsely developed countries, resulting in a decrease in productivity and welfare of human beings and animals (Rushton and Bruce, 2017). The Taeniidae family encompasses the most economically and medically important cestodes, which are characterized by having indirect life cycles in which the adult phase develops in the intestine of the definitive hosts, and the larval or metacestode phase is housed in different tissues of the intermediate host (Hoberg, 2002). In the Taeniidae family, the egg is the infectious phase causing the larval stage in the intermediate host when ingested via oral, and the tapeworm stage in the definitive host. The egg has a similar microscopic structure between the different species and resist environmental factors such as desiccation and extreme temperatures, which allows prolonging their viability and infective capacity (Thevenet et al., 2017).

In particular, the eggs of Taenia pisiformis, the most frequent cestode in rabbits, have a high antigenic similarity with those of T. solium, that causes an important zoonosis. The antigenic similarity between these tapeworms has allowed the basic knowledge found in other species to be exploited in the search for drugs and vaccines against this zoonosis (García-Allan et al., 1996; Ito and Budke. 2014). It has been reported that T. pisiformis parasitosis has frequencies of <1% in laboratory rabbits (Owiny 2001; Mir et al., 2006), 67.7% in wild rabbits (Domínguez-Roldan et al., 2018) and 4.7% in rabbits intended for human consumption (Szkucik et al., 2014). The differences in the incidence rates of T. pisiformis have been little explored; they could be due to parasites control by farmers or by intrinsic characteristics of the hosts and of the parasite. In other Taeniasis like that caused by T. solium, the prevalence is also variable between regions in a same country and between countries of different continents. Likewise, the pathology may vary from asymptomatic to incapacitating or fatal. Host differences in human leukocyte antigens, gender and immune profiles are suspected to contribute to the variable incidence, clinical and immunological responses, but intrinsic factors to the parasite as genetic differentiation and variability could also be a significant source of heterogeneity of the infections (Vega et al., 2003). It has been reported that, there is a 50% decrease in the size of litters in rabbits experimentally infected with this Taenia (Hallal-Calleros et al., 2016), and in naturally infected rabbits, parasitosis occurs frequently in lactating females (Domínguez-Roldan et al., 2018). These reports demonstrate the productive impact that T. pisiformis can have on cuniculture and on endemic species endangered, and that hormonal status of the host also may contribute to the differences in the incidence rates of this parasitosis.

To control cestodiasis, including that produced by T. pisiformis, various strategies are proposed, such as educational campaigns, the use of gamma irradiation, vaccination, the use of drugs, among others (Flores-Pérez et al., 2003; Sciutto et al., 2007). Most of them are aimed at eliminating adult cestode or larval stage in the intermediate host; however, the use of niclosamide and praziquantel antiparasitic drugs have caused resistance against Taenias (Lateef et al., 2008), which has led to the need for new control methods. In this context, some strategies include biological control, such as Duddingtonia flagrans and Pochonia clamidospora fungi that destroy the egg cover of Taenia saginata (Araújo et al., 2009); Monacrosporium thaumasium fungi damages the Taenia taeniaeformis eggs (Braga et al., 2009), and Paecilomyces lilacinus decreases the viability of the oncospheres of Taenia hydatigena (Ciarmela et al., 2005). The proposed practical use for fungi with ovicidal activity is the oral administration in dogs, which allows the fungus to spread through the dog intestine to control the eggs of Taenia sp and other parasites such as Toxocara canis in feces (Araujo et al., 2012). Another alternative of antiparasitic biological control is the bacterium B. thuringiensis, widely used in the control of agricultural pests with the advantage of being safe for humans and pets. B. thuringiensis GP526 strain has been shown to be effective destroying the eggs of the zoonotic cestode Dipylidium caninum, and it also inhibits the motility of the adult cestode (Peña et al., 2013), with the advantage of inducing egg lethality in a shorter time with respect to that referred with fungi against other cestodes. Among the applications of bacteria with ovicidal activity, the treatment of wastewater with an anaerobic or aerobic process capable of reducing the viability of the parasites present in the water has been proposed (Shuva and Fattal, 2003). It is known that Taenia spp eggs can remain in the intestine of dogs, then, the spore-crystal complex of GP526 B. thuringiensis could be potentially applied as a probiotic with ovicidal activity in the dog intestine (Coman and Rickard, 1975). This propose supports the biotechnological importance of evaluating the ovicidal activity of harmless bacteria for humans and animals. Therefore, our study evaluates the use of GP526 strain of B. thuringiensis as a potential ovicidal agent against the infectious phase of the T. pisiformis cestode.

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