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Eimeria bateri Natural Infection: Oocysts Reductions in Grey Quail (Coturnix coturnix) Treated with Bacillus thuringensis var. israelensis

Abstract

Coccidiosis, a disease caused by the parasitic Eimeria spp., affects birds of all ages, particularly young birds more intensely. Infected poultry presents significant economic losses. Bacillus thuringiensis var israelensis (Bti) is a Gram-positive, spore-forming bacterium that produces proteins with high specific parasiticidal activity against various orders of parasites. Thus, the aim of the present study was to evaluate the parasiticidal potential of Bti in quails that were naturally infected with Eimeria bateri. Twenty 12-week-old male quails (Coturnix coturnix coturnix), naturally infected with Eimeria bateri, were randomly divided into two groups of 10 birds: Bti treated and control. The treated group was supplemented with Bti (1×108 spores∙g-1) in the feed, while; the control group received the same feed without Bti. To evaluate the occurrence of oocysts, samples of feces were collected every week for four weeks. Significant (P < 0.05) oocysts reductions of 56.64% and 94.51% were noted in the Bti treated group at 2nd and 4th week of study, respectively. The Bti supplementation may contribute to the reduction of oocysts in quails and environmental contamination. Bacillus thuringiensis var israelensis appeared to be a promising complementary alternative in E. bateri control.

Keywords:
biological control; Coccidiosis; intestinal protozoa

GRAPHICAL ABSTRACT

HIGHLIGHTS

Coccidiosis cause important economic losses for poultry industry.

Bti produce proteins with high specific parasiticidal effect.

Bti reduce the number of Eimeria bateri oocysts in quail.

INTRODUCTION

Coccidiosis is a parasitic disease that has sever adverse economic impact on the poultry industry worldwide. Most of the loss is caused due to the costs incurred in prophylactic measures, mortality, feed malabsorption, and reduction in egg production [11 Chapman HD. Milestones in avian coccidiosis research: a review. Poult Sci. 2014 Mar;93(3):501-11.]. The life cycle of Eimeria includes extracellular/intracellular and sexual/asexual stages, with a complex immune response by the host [22 Lillehoj HS. Role of T lymphocytes and cytokines in coccidiosis. Int J Parasitol. 1998 Jul;28(7):1071-81.]. Immunity to Eimeria spp. is species-specific; therefore, birds immune to one Eimeria species may not have protection against other Eimeria species. Two species of quail are breed commercially. They are "Gray quail" (Coturnix coturnix) a broiler quail, and Japanese quail (Coturnix japonica) used for laying. In this quails, different Eimeria species have been reported, and three of them have been described in Brazil in C. japonica, Eimeria bateri, E. tsunodai and E. uzura [33 Berto BP, Borba HR, Lima VM, Flausino W, Teixeira-Filho WL, Lopes CWG. Eimeria spp. from Japanese quails (Coturnix japonica): new characteristic features and diagnostic tools [Internet]. Vol. 33, Pesquisa Veterinária Brasileira. 2013. p. 1441-7. Available from: http://dx.doi.org/10.1590/s0100-736x2013001200008
http://dx.doi.org/10.1590/s0100-736x2013...
]. Eimeria bateri was originally described from Indian quails and is present all around the world [44 Shah HL, Johnson CA. Eimeria bateri Bhatia, Pandey and Pande, 1965 from the Hungarian quail Coturnix c. coturnix in the United States and its attempted transmission to the chicken. J Protozool. 1971 May;18(2):219-20.]. Eimeria bateri can infect and develop its entire life cycle in quails, and it shed a greater quantity of oocysts during the infection. Nonetheless, E. bateri infection is considered an important disease since its endogenous stages and high number of oocysts in feces might be associated with intestinal lesions [55 Norton CC, Peirce MA. The Life Cycle of Eimeria bateri(Protozoa, Eimeriidae) in the Japanese Quail Coturnix coturnix japonicum [Internet]. Vol. 18, J. Parasitol. 1971.p. 57-62. Available from: http://dx.doi.org/10.1111/j.1550-7408.1971.tb03280.x
http://dx.doi.org/10.1111/j.1550-7408.19...
].

Currently, there are two main procedures to control coccidiosis: drugs and vaccines [66 Dalloul RA, Lillehoj HS. Poultry coccidiosis: recent advancements in control measures and vaccine development. Expert Rev vaccines, 2006,5.1:143-63.]. Drugs need to be managed regularly due to development of resistance [77 Abbas RZ, Iqbal Z, Blake D, Khan MN, Saleemi MK. Anticoccidial drug resistance in fowl coccidia: the state of play revisited. Worlds Poult Sci J, 2011, 67.2:337-50.]. With the development of resistance to drugs, importance has been given to vaccines. The commercially available coccidiosis vaccines are based on the principle that Eimeria spp. can induce a protective immunity when consecutives low dose infection occurs, and by doing so developing robust immunity [88 Conway DP, Mckenzie, ME. Poultry coccidiosis: diagnostic and testing procedures. John Wiley & Sons, 2007]. Currently, the available coccidiosis vaccines can be divided basically in three groups: live virulent strains, live attenuated strains, and live strains that are relatively tolerant to the ionophore compounds. This last one gives a new prospective to the anticoccidial vaccine development [99 Vermeulen AN, Schaap DC, Schetters, ThPM. Control of coccidiosis in chickens by vaccination. Vet. Parasitol, 2001,100.1-2:13-20.]. The advantage of these vaccines is that they allow the use of ionophores during the first weeks when the birds are still susceptible, and immunity is not achieved. However, each one of these vaccines has its limitation, been a major drawback of live vaccines is their limited shelf life and relatively high production costs associated with attenuation [1010 Shah MAA. DNA vaccines as sustainable Coccidiosis control strategies in chickens. Sci Lett. 2013,1:1-4.].

Bacillus thuringiensis is a Gram-positive bacterium that produces crystal inclusions upon sporulation. These inclusions are comprised mostly of crystal (Cry) and cytotoxic (Cyt) proteins, which are toxic to a wide range of insect classes, such as Lepidopteran, Diptera, Coleoptera and Nematode [1111 Elshaghabee FMF, Rokana N, Gulhane RD, Sharma C, Panwar H. Bacillus As Potential Probiotics: Status, Concerns, and Future Perspectives [Internet]. Vol. 8, Frontiers in Microbiology. 2017. Available from: http://dx.doi.org/10.3389/fmicb.2017.01490
http://dx.doi.org/10.3389/fmicb.2017.014...
,1212 Bravo A, Likitvivatanavong S, Gill SS, Soberón M. Bacillus thuringiensis: A story of a successful bioinsecticide. Insect. Biochem Mol Biol. 2011 Jul;41(7):423-31.]. Bacillus sp. strains, including the B. thuringiensis var. israelensis (Bti), has significant toxic activity against larvae of the important livestock parasite [1313 Sinott MC, Cunha Filho NA, Castro LLD, Lorenzon LB, Pinto NB, Capella GA, et al. Bacillus spp. toxicity against Haemonchus contortus larvae in sheep fecal cultures [Internet]. Vol. 132, Exp Parasitol. 2012. p. 103-8. Available from: http://dx.doi.org/10.1016/j.exppara.2012.05.015
http://dx.doi.org/10.1016/j.exppara.2012...

14 Sinott MC, de Castro LLD, Leite FLL, Gallina T, De-Souza MT, Santos DFL, et al. Larvicidal activity of Bacillus circulans against the gastrointestinal nematode Haemonchus contortus in sheep [Internet]. Vol. 90, J. Helminthol. 2016. p.68-73. Available from: http://dx.doi.org/10.1017/s0022149x14000844
http://dx.doi.org/10.1017/s0022149x14000...
-1515 De Lara APDESS, Lorenzon LB, Vianna AM, Santos FDS, Pinto LS, et al. Larvicidal activity of Bacillus thuringiensis var. israelensis Cry11Aa toxin against Haemonchus contortus [Internet]. Vol. 143, Parasitol. 2016. p. 1665-71. Available from: http://dx.doi.org/10.1017/s0031182016001451
http://dx.doi.org/10.1017/s0031182016001...
]. The toxins present in the proteins produced by Bti make pores in the membrane and subsequent lysis [1616 Parker MW, Feil SC. Pore-forming protein toxins: from structure to function. Progress in biophysics and molecular biology, 2005. 88(1), 91-142.].

There is an important increase in the resistance of coccidia to the control drugs. And the high costs of vaccines associated with their short protection make it necessary to find alternative methods for coccidiosis controls. Nevertheless, there is scarce information of Bti and its possible role in the controlling of Eimeria species-induced infections in quails [1717 Dalloul RA, Lillehoj HS, Tamim NM, Shellem TA, Doerr JA. Induction of local protective immunity to Eimeria acervulina by a Lactobacillus-based probiotic. Comp Immunol Microbiol Infect Dis. 2005 Sep;28(5-6):351-61.,1818 Lee S, Lillehoj HS, Park DW, Hong YH, Lin JJ. Effects of Pediococcus - and Saccharomyces-based probiotic (MitoMax(r)) on coccidiosis in broiler chickens [Internet]. Vol. 30, Comparative Immunology, Microbiology and Infectious Diseases. 2007.p.261-8. Available from: http://dx.doi.org/10.1016/j.cimid.2007.02.002
http://dx.doi.org/10.1016/j.cimid.2007.0...
]. Thus, this study evaluated the activity of Bti in E. bateri in quails.

MATERIAL AND METHODS

Bacillus thuringiensis var. israelensis

Spores of the Bti strain (from the collection of the Universidade Federal de Pelotas, Departamento de Microbiologia e Parasitologia), was used in this study. Briefly, the Bti was cultured in a 1-L Erlenmeyer flask containing 200 mL of Nutrient Yeast Extract Salt Medium (NYSM) [1919 Yousten AA. Bacillus sphaericus: microbiological factors related to its potential as a mosquito larvicide. Adv Biotechnol Processes. 1984;3:315-43.] and grown at 30 °C with rotary shaking at 150 rpm for 72 h. Then, the culture was checked for purity, sporulation, and colony-forming units per milliliter. The culture was centrifuged at 8500 × g for 20 min at 4 °C. The pellets were washed twice in saline (0.9% NaCl, Sigma-Aldrich, St. Louis, Missouri, USA, and purified water) to remove cell debris and secretory products, then suspended in saline (pH 7.0), and stored at 4 °C until further use.

Quails

The experiment was conducted in the Laboratório de Ensino e Experimentação Zootécnica e Prof. Renato R. Peixoto (LEEZO) at Departamento de Ciência Animal - FAEM - UFPel, with gray quails which has been developed of in the same department by individual selection for body weight. Twenty gray quail’s male twelve weeks old, weighting ~ 297.2 grams and naturally infected with E. bateri were used in this study. The birds were individually housed in metal cages equipped with gutter-type metal feeders and nipple drinkers, in the same room, with controlled temperature around 25 ºC and cycles of 17 h of light and 7 h of darkness. During the experimental period, the birds received water ad libitum and the feed was provided daily. Two groups of 10 birds each were separated randomly to form a Bti-treated group and a control group. The birds were weighted at the beginning (day zero) and at the last day of the experiment. The control birds were fed on commercial feeds without any antimicrobial agent (MigCodor, Mig-Plus agroindustrial, RS, Brazil), while the Bti-treated group was fed on the same feed supplemented with 1×108 g-1 of viable Bti spores daily. The birds have been kept in sanitary and well-being conditions within international animal production standards, with a Veterinarian supervision.

Fecal samples

Feces were collected directly from the cages, every week, and the fecal samples were placed into plastic bags, identified, for later processing at the Laboratory of Parasitic Diseases, School of Veterinary medicine, Federal University of Pelotas. For oocysts preparation, three aliquots of each sample were separated and diluted in 2.5% aqueous potassium dichromate (K2Cr2O7) and kept in Petri dishes for sporulation at room temperature. After sporulation, the oocysts were recovered by centrifugation with a saturated sugar solution as described by Duszynski and Wilber (1997) [2020 Duszynski DW, Wilber PG. A guideline for the preparation of species descriptions in the Eimeriidae. J Parasitol. 1997 Apr;83(2):333-6.] and were used in subsequent analysis. For the counting of the oocysts, a Carl Zeiss binocular microscope with immersion objective (100 x) was used. The number of oocysts per gram of feces was determined according to the technique described by Menezes and Lopes [2121 Menezes RCA, Lopes CWG. [Epizootiology of Eimeria arloingi in goats in the Serrana Fluminense microregion, Rio de Janeiro, Brazil]. Journal of the Federal Rural University of Rio de Janeiro. 1995. 5:12-2. Portuguese.]. The Eimeria characterization was base in its sporulated oocysts morphology following Teixeira and coauthors and Berto and coauthors [2222 Teixeira Filho WL, Lopes CWG. Coccidiosis in japanese quails (Coturnix japonica): characterization of a naturally occurring infection in a commercial rearing farm [Internet]. Vol. 6, Revista Brasileira de Ciência Avícola. 2004. p. 129-34. Available from: http://dx.doi.org/10.1590/s1516-635x2004000200010
http://dx.doi.org/10.1590/s1516-635x2004...
,33 Berto BP, Borba HR, Lima VM, Flausino W, Teixeira-Filho WL, Lopes CWG. Eimeria spp. from Japanese quails (Coturnix japonica): new characteristic features and diagnostic tools [Internet]. Vol. 33, Pesquisa Veterinária Brasileira. 2013. p. 1441-7. Available from: http://dx.doi.org/10.1590/s0100-736x2013001200008
http://dx.doi.org/10.1590/s0100-736x2013...
]. Briefly, oocysts subspherical to ellipsoidal, bi-layered and smooth, ~1.0 thick were characterized as E. bateri.

All analyzes were performed in triplicate and the protocols were reviewed and approved by the Ethics Committee on Animal Experimentation (CEEA No. 7087) of the Universidade Federal de Pelotas (UFPel). The UFPel-CEEA agreement has been approved by the Brazilian National Council for Animal Experimentation Control (CONCEA).

Statistical analysis

The number of oocysts per group (Bti-treated and control) was analyzed using Statistix 8.0®, (Statistix, Tallahassee, FL, USA). The difference in the quantity between the groups were determined using the Shapiro-Wilk Normality Test, followed by Tukey's HSD all-pairwise comparisons, with P < 0.05. For the weight difference between groups a Student t test with a P< 0.05 were used. The figures were drawn in GraphPad Prism 5.0 program (GraphPad Software Inc., San Diego, CA, USA). In order to evaluate the efficacy of treatment by the end of the fourth week, following equation was used:

E ( % ) = 100 × ( t h e n u m b e r o f o o c y s t s i n c o n t r o l t h e n u m b e r o f o o c y s t s i n B t i sup p l e m e n t e d g r o u p ) / n u m b e r o f o o c y s t s o f c o n t r o l .

RESULTS

In fecal exams, a sporulated oocysts subspherical, ovoid or ellipsoid were observed. The oocyst wall was smooth, double layered, with brownish inner layer and colorless outer layer. In the first week of the experiment there was no statistical difference in the number of oocysts between the control group (n = 5683) and the group Bti-treated (n = 7900).

From the second week of treatment onwards, a progressive reduction in oocyst numbers was observed in the Bti-treated group. In the second week this reduction was 37.73% (n = 3550), in the third week it was 43.96% (n = 1316), and in the fourth week 80.76% (n = 433), compared to the control group (Figure 1A).

Compared with infection at the beginning of treatment, a significant reduction (P < 0.05) in oocytes of the Bti-treated group was observed amounting to 56.64% and 94.51% at the second- and fourth-weeks post-treatment, respectively (Figure 1B).

Figure 1
Percentage of oocysts reduction. A. The data represent the oocysts reduction in feces of treated Bti compared with the control groups oocysts reduction, during the 2nd, 3rd and 4th weeks post-treatment. B. The data represent the oocysts reduction in feces of treated Bti compared with the control groups oocysts reduction from the first week of experiment. Asterisk (*) represent statistic difference (P < 0.05) between supplemented and control group.

Evaluating the weight of the birds at the end of period of study we observed that the Bti group had mean weight of 339.68 g representing a gain of 40.32 g (+/- 7.79 S.D), and the control group a mean weight of 327.52 g representing a gain of 31.93 g (+/- 3.43 S.D). However, the weight gain difference was not significant (P=0.236) between the groups.

DISCUSSION

The identification of the species of Eimeria that infected the quails was made based on the observed morphological characteristics and comparing with the description of Teixeira and coauthors [2222 Teixeira Filho WL, Lopes CWG. Coccidiosis in japanese quails (Coturnix japonica): characterization of a naturally occurring infection in a commercial rearing farm [Internet]. Vol. 6, Revista Brasileira de Ciência Avícola. 2004. p. 129-34. Available from: http://dx.doi.org/10.1590/s1516-635x2004000200010
http://dx.doi.org/10.1590/s1516-635x2004...
] and Berto and coauthors [33 Berto BP, Borba HR, Lima VM, Flausino W, Teixeira-Filho WL, Lopes CWG. Eimeria spp. from Japanese quails (Coturnix japonica): new characteristic features and diagnostic tools [Internet]. Vol. 33, Pesquisa Veterinária Brasileira. 2013. p. 1441-7. Available from: http://dx.doi.org/10.1590/s0100-736x2013001200008
http://dx.doi.org/10.1590/s0100-736x2013...
].

In this study, a significant effect on the reduction of E. bateri oocysts in the feces of Bti-supplemented quails was observed. By the second week of Bti administration, a significant (P < 0.05) reduction (37.73%) in oocysts was observed and this reduction was more pronounced at the fourth week, amounting to 80.76%. During the same time period, the variation in the oocysts number in the control group was 5.2% and 5.6%, respectively. Sun and coauthors also found a significant reduction of 62.5% of Eimeria tenella oocysts in chicken after 4 weeks of treatment with another probiotic microorganism, Saccharomyces cerevisiae [2323 Sun H, Wang L, Wang T, Zhang J, Liu Q, Chen P, et al. Display of Eimeria tenella EtMic2 protein on the surface of Saccharomyces cerevisiae as a potential oral vaccine against chicken coccidiosis. Vaccine. 2014 Apr 1;32(16):1869-76.].

In other studies performed by our group, it was possible to demonstrate that Bti, administered to cattle and sheep, has a larvicidal effect on the nematode Haemonchus contortus, which is an important livestock parasite [1313 Sinott MC, Cunha Filho NA, Castro LLD, Lorenzon LB, Pinto NB, Capella GA, et al. Bacillus spp. toxicity against Haemonchus contortus larvae in sheep fecal cultures [Internet]. Vol. 132, Exp Parasitol. 2012. p. 103-8. Available from: http://dx.doi.org/10.1016/j.exppara.2012.05.015
http://dx.doi.org/10.1016/j.exppara.2012...

14 Sinott MC, de Castro LLD, Leite FLL, Gallina T, De-Souza MT, Santos DFL, et al. Larvicidal activity of Bacillus circulans against the gastrointestinal nematode Haemonchus contortus in sheep [Internet]. Vol. 90, J. Helminthol. 2016. p.68-73. Available from: http://dx.doi.org/10.1017/s0022149x14000844
http://dx.doi.org/10.1017/s0022149x14000...
-1515 De Lara APDESS, Lorenzon LB, Vianna AM, Santos FDS, Pinto LS, et al. Larvicidal activity of Bacillus thuringiensis var. israelensis Cry11Aa toxin against Haemonchus contortus [Internet]. Vol. 143, Parasitol. 2016. p. 1665-71. Available from: http://dx.doi.org/10.1017/s0031182016001451
http://dx.doi.org/10.1017/s0031182016001...
]. In protozoa, experimental studies using Bacillus spores on the control of Cryptosporidium, Giardia, and Eimeria demonstrated the toxic activity that can inhibit parasite development [2424 Borchers AT, Selmi C, Meyers FJ, Keen CL, Gershwin ME. Probiotics and immunity. J Gastroenterol. 2009 Jan 22;44(1):26-46.]. However, to the best of our knowledge, no Bti active molecule has thus far been reported as acting against Eimeria spp. that could reduce oocyte production.

One might suggest that a possible role mediated by Bti is to compete with Eimeria for nutrients and/or the ecological environment in the intestinal tract [2525 Pinchuk IV, Bressollier P, Verneuil B, Fenet B, Sorokulova IB, Mégraud F, et al. In vitro anti-Helicobacter pylori activity of the probiotic strain Bacillus subtilis 3 is due to secretion of antibiotics. Antimicrob Agents Chemother. 2001 Nov;45(11):3156-61.]. Eimeria need to invade the cell to replicate, however, first it needs to adhere to the cell surface, so if the Bacillus dispute for the same site less Eimeria will adhere, penetrate and replicate, and as a result less oocysts shedding may occur. Another mechanism used by Bacillus against pathogens is the capacity of stimulating both innate and adaptive immune responses by activating intestinal epithelial cells and immune cells, providing protection in the intestinal mucosa of the host [2626 Forsythe P, Bienenstock J. Immunomodulation by commensal and probiotic bacteria. Immunol Invest. 2010;39(4-5):429-48.]. Dalloul and coauthors demonstrated that chickens supplemented with probiotics had more intestinal intraperitoneal lymphocytes expressing surface-marked CD4+, CD8+, and αβTCR and a reduced number of Eimeria oocysts in the feces [2727 Dalloul RA, Lillehoj HS, Shellem TA, Doerr JA. Enhanced mucosal immunity against Eimeria acervulina in broilers fed a Lactobacillus-based probiotic. Poult Sci. 2003 Jan;82(1):62-6.]. We recently demonstrated that Bacillus toyonensis have the ability to stimulate cytokine production, which drives the development of the local and systemic immune responses [2828 Santos FDS, Menegon YA, Piraine REA, Rodrigues PRC, Cunha RC, Leite FPL. Bacillus toyonensis improves immune response in the mice vaccinated with recombinant antigen of bovine herpesvirus type 5. Benef Microbes. 2018 Jan 29;9(1):133-42., 2929 Habil N, Al-Murrani W, Beal J, Foey A. Probiotic bacterial strains differentially modulate macrophage cytokine production in a strain-dependent and cell subset-specific manner [Internet]. Vol. 2, Benef Microbes. 2011. p. 283-93. Available from: http://dx.doi.org/10.3920/bm2011.0027
http://dx.doi.org/10.3920/bm2011.0027...
]. Therefore, cytokines expressed during Bti treatment may have a major role by leading a more rapid immune response to Eimeria. Lillehoj and Choi showed the role of interferon gamma (IFN-g) in the development of resistance to Eimeria, demonstrating that IFN-g inhibits E. tenella development in vitro and reduces oocysts production [3030 Lillehoj HS, Choi KD. Recombinant chicken interferon-gamma-mediated inhibition of Eimeria tenella development in vitro and reduction of oocyst production and body weight loss following Eimeria acervulina challenge infection. Avian Dis. 1998 Apr;42(2):307-14.].

Even not observing statistical difference in weight gain for the Bti group, one may suggest that the difference of 9 grams in the mean weight in favor of the Bti group might be relevant, considering the weeks and the number of birds evaluated.

Nevertheless, proposing the use of Bti as an alternative to conventional treatments, such as drugs or vaccines to control Eimeria spp. appears unreasonable. However, it is suggested that Bti may be used as a complementary method to reduce oocyst infestation to improve Eimeria control. A better understanding of molecular mechanisms underlying the beneficial effects of Bti on Eimeria infection control is essential to validate the approach.

REFERENCES

  • 1
    Chapman HD. Milestones in avian coccidiosis research: a review. Poult Sci. 2014 Mar;93(3):501-11.
  • 2
    Lillehoj HS. Role of T lymphocytes and cytokines in coccidiosis. Int J Parasitol. 1998 Jul;28(7):1071-81.
  • 3
    Berto BP, Borba HR, Lima VM, Flausino W, Teixeira-Filho WL, Lopes CWG. Eimeria spp. from Japanese quails (Coturnix japonica): new characteristic features and diagnostic tools [Internet]. Vol. 33, Pesquisa Veterinária Brasileira. 2013. p. 1441-7. Available from: http://dx.doi.org/10.1590/s0100-736x2013001200008
    » http://dx.doi.org/10.1590/s0100-736x2013001200008
  • 4
    Shah HL, Johnson CA. Eimeria bateri Bhatia, Pandey and Pande, 1965 from the Hungarian quail Coturnix c. coturnix in the United States and its attempted transmission to the chicken. J Protozool. 1971 May;18(2):219-20.
  • 5
    Norton CC, Peirce MA. The Life Cycle of Eimeria bateri(Protozoa, Eimeriidae) in the Japanese Quail Coturnix coturnix japonicum [Internet]. Vol. 18, J. Parasitol. 1971.p. 57-62. Available from: http://dx.doi.org/10.1111/j.1550-7408.1971.tb03280.x
    » http://dx.doi.org/10.1111/j.1550-7408.1971.tb03280.x
  • 6
    Dalloul RA, Lillehoj HS. Poultry coccidiosis: recent advancements in control measures and vaccine development. Expert Rev vaccines, 2006,5.1:143-63.
  • 7
    Abbas RZ, Iqbal Z, Blake D, Khan MN, Saleemi MK. Anticoccidial drug resistance in fowl coccidia: the state of play revisited. Worlds Poult Sci J, 2011, 67.2:337-50.
  • 8
    Conway DP, Mckenzie, ME. Poultry coccidiosis: diagnostic and testing procedures. John Wiley & Sons, 2007
  • 9
    Vermeulen AN, Schaap DC, Schetters, ThPM. Control of coccidiosis in chickens by vaccination. Vet. Parasitol, 2001,100.1-2:13-20.
  • 10
    Shah MAA. DNA vaccines as sustainable Coccidiosis control strategies in chickens. Sci Lett. 2013,1:1-4.
  • 11
    Elshaghabee FMF, Rokana N, Gulhane RD, Sharma C, Panwar H. Bacillus As Potential Probiotics: Status, Concerns, and Future Perspectives [Internet]. Vol. 8, Frontiers in Microbiology. 2017. Available from: http://dx.doi.org/10.3389/fmicb.2017.01490
    » http://dx.doi.org/10.3389/fmicb.2017.01490
  • 12
    Bravo A, Likitvivatanavong S, Gill SS, Soberón M. Bacillus thuringiensis: A story of a successful bioinsecticide. Insect. Biochem Mol Biol. 2011 Jul;41(7):423-31.
  • 13
    Sinott MC, Cunha Filho NA, Castro LLD, Lorenzon LB, Pinto NB, Capella GA, et al. Bacillus spp. toxicity against Haemonchus contortus larvae in sheep fecal cultures [Internet]. Vol. 132, Exp Parasitol. 2012. p. 103-8. Available from: http://dx.doi.org/10.1016/j.exppara.2012.05.015
    » http://dx.doi.org/10.1016/j.exppara.2012.05.015
  • 14
    Sinott MC, de Castro LLD, Leite FLL, Gallina T, De-Souza MT, Santos DFL, et al. Larvicidal activity of Bacillus circulans against the gastrointestinal nematode Haemonchus contortus in sheep [Internet]. Vol. 90, J. Helminthol. 2016. p.68-73. Available from: http://dx.doi.org/10.1017/s0022149x14000844
    » http://dx.doi.org/10.1017/s0022149x14000844
  • 15
    De Lara APDESS, Lorenzon LB, Vianna AM, Santos FDS, Pinto LS, et al. Larvicidal activity of Bacillus thuringiensis var. israelensis Cry11Aa toxin against Haemonchus contortus [Internet]. Vol. 143, Parasitol. 2016. p. 1665-71. Available from: http://dx.doi.org/10.1017/s0031182016001451
    » http://dx.doi.org/10.1017/s0031182016001451
  • 16
    Parker MW, Feil SC. Pore-forming protein toxins: from structure to function. Progress in biophysics and molecular biology, 2005. 88(1), 91-142.
  • 17
    Dalloul RA, Lillehoj HS, Tamim NM, Shellem TA, Doerr JA. Induction of local protective immunity to Eimeria acervulina by a Lactobacillus-based probiotic. Comp Immunol Microbiol Infect Dis. 2005 Sep;28(5-6):351-61.
  • 18
    Lee S, Lillehoj HS, Park DW, Hong YH, Lin JJ. Effects of Pediococcus - and Saccharomyces-based probiotic (MitoMax(r)) on coccidiosis in broiler chickens [Internet]. Vol. 30, Comparative Immunology, Microbiology and Infectious Diseases. 2007.p.261-8. Available from: http://dx.doi.org/10.1016/j.cimid.2007.02.002
    » http://dx.doi.org/10.1016/j.cimid.2007.02.002
  • 19
    Yousten AA. Bacillus sphaericus: microbiological factors related to its potential as a mosquito larvicide. Adv Biotechnol Processes. 1984;3:315-43.
  • 20
    Duszynski DW, Wilber PG. A guideline for the preparation of species descriptions in the Eimeriidae. J Parasitol. 1997 Apr;83(2):333-6.
  • 21
    Menezes RCA, Lopes CWG. [Epizootiology of Eimeria arloingi in goats in the Serrana Fluminense microregion, Rio de Janeiro, Brazil]. Journal of the Federal Rural University of Rio de Janeiro. 1995. 5:12-2. Portuguese.
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  • 2
    There was no unnecessary cruelty in animal experimentation.

Edited by

Editor-in-Chief:

Paulo Vitor Farago

Associate Editor:

Cheila Roberta Lehnen

Publication Dates

  • Publication in this collection
    19 Apr 2021
  • Date of issue
    2021

History

  • Received
    27 July 2020
  • Accepted
    18 Feb 2021
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