Experimental infection with Toxoplasma gondii in broiler chickens (Gallus domesticus): seroconversion, tissue cyst distribution, and prophylaxis

Nedişan, Maria E.; Györke, Adriana; Ştefănuţ, Cristina L.; Kalmár, Zsuzsa; Friss, Zsuzsa; Blaga, Radu; Blaizot, Amandine; Toma-Naic, Andra; Mircean, Viorica; Schares, Gereon; Djurković-Djaković, Olgica; Klun, Ivana; Villena, Isabelle; Cozma, Vasile

doi:10.1007/s00436-020-06984-x

Protozoology - Original Paper
Published: 08 January 2021

Experimental infection with Toxoplasma gondii in broiler chickens (Gallus domesticus): seroconversion, tissue cyst distribution, and prophylaxis

Maria E. Nedişan^na1^nAff1,
Adriana Györke ORCID: orcid.org/0000-0001-6453-2370^na1^nAff1,
Cristina L. Ştefănuţ¹,
Zsuzsa Kalmár¹,
Zsuzsa Friss²,
Radu Blaga³,
Amandine Blaizot³,
Andra Toma-Naic¹,
Viorica Mircean¹,
Gereon Schares⁴,
Olgica Djurković-Djaković⁵,
Ivana Klun⁵,
Isabelle Villena⁶ &
Vasile Cozma¹

Parasitology Research volume 120, pages 593–603 (2021)Cite this article

383 Accesses
1 Citations
Metrics details

Abstract

Toxoplasma gondii is a widespread zoonotic protozoan that infects most species of mammals and birds, including poultry. This study aimed to investigate the course of T. gondii infection and the efficacy of diclazuril and Artemisia annua in preventing infection in experimentally infected chickens. Seventy-five 1-month-old chickens, female and male, were randomly divided into five groups (n = 15 each) as follows: (1) uninfected untreated (negative control, NC); (2) infected with T. gondii genotype II/III isolated from a wild cat (group WC); (3) infected with T. gondii genotype II isolated from a domestic cat (group DC); (4) infected with T. gondii domestic cat strain and treated with the anticoccidial diclazuril (group DC-D); and (5) infected with T. gondii domestic cat strain and treated with the medicinal plant Artemisia annua (group DC-A). Clinical signs, body temperature, mortality rate, weight gain, feed conversion ratio, hematological parameters, and the presence of T. gondii–specific IgY antibodies were recorded in all groups. Five chickens per group were euthanized 28 days post-infection (p.i.) and their brains, hearts, and breast muscle tested for T. gondii by mouse bioassay and polymerase chain reaction (PCR). No clinical signs related to the experimental infection were observed throughout the study period. T. gondii–specific antibodies were detected by day 28 p.i., but not in all infected chickens. Overall, T. gondii DNA was detected (bioassay or tissue digests) in all infected and untreated chickens (10/10), while viable parasite (bioassay) was isolated from 7 out of 10 chickens. The parasite was most frequently identified in the brain (7/10). There were no differences in the T. gondii strains regarding clinical infection and the rate of T. gondii detection in tissues. However, higher antibody titers were obtained in chickens infected with T. gondii WC strain (1:192) comparing with T. gondii DC strain (1:48). A. annua reduced replication of the parasite in 3 out of 5 chickens, while diclazuril did not. In conclusion, broiler chickens were resistant to clinical toxoplasmosis, irrespective of the strain (domestic or wild cat strain). The herb A. annua presented prophylactic efficacy by reduced parasite replication. However, further studies are required aiming at the efficacy of diclazuril and A. annua for the prevention of T. gondii infection in chickens using quantitative analysis methods.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Data availability

Not applicable.

References

Allen PC, Lydon J, Danforth H (1997) Effects of components of Artemisia annua on coccidia infections in chickens. Poult Sci 76(8):1156–1163. https://doi.org/10.1093/ps/76.8.1156
CAS Article PubMed Google Scholar
Alves CF, Vitor RWA (2005) Efficacy of atovaquone and sulfadiazine in the treatment of mice infected with Toxoplasma gondii strains isolated in Brazil. Parasite 12(2):171–177. https://doi.org/10.1051/parasite/2005122171
CAS Article PubMed Google Scholar
Bresciani KDS, Galvão ALB, de Vasconcellos AL, dos Santos TR, Kaneto CN, Viol MA, Gomes JF, Bilsland E (2016) Epidemiological aspects of feline toxoplasmosis. Arch Vet Sci 21(2):1–8. https://doi.org/10.5380/avs.v21i2.39997
Article Google Scholar
Breuer E, Efferth T (2014) Treatment of iron-loaded veterinary sarcoma by Artemisia annua. Nat Prod Bioprospect 4(2):113–118. https://doi.org/10.1007/s13659-014-0013-7
CAS Article PubMed PubMed Central Google Scholar
Christensen K, Vizzier Thaxton Y, Thaxton JP, Scanes CG (2012) Changes in body temperature during growth and in response to fasting in growing modern meat type chickens. Br Poult Sci 53(4):531–537. https://doi.org/10.1080/00071668.2012.715744
CAS Article PubMed Google Scholar
de Almeida GF, Horsted K, Thamsborg SM, Kyvsgaard NC, Ferreira JF, Hermansen JE (2012) Use of Artemisia annua as a natural coccidiostat in free-range broilers and its effects on infection dynamic and performance.Vet. Parasitol 186(3–4):178–187. https://doi.org/10.1016/j.vetpar.2011.11.058
Article Google Scholar
Desmonts GE, Remington JS (1980) Direct agglutination test for diagnosis of Toxoplasma infection: method for increasing sensitivity and specificity. J Clin Microbiol 11(6):562–568
CAS Article Google Scholar
Djurković-Djaković O, Nikolić A, Bobić B, Klun I, Aleksić A (2005) Stage conversion of Toxoplasma gondii RH parasites in mice by treatment with atovaquone and pyrrolidine dithiocarbamate. Microbes Infect 7(1):49–54. https://doi.org/10.1016/j.micinf.2004.09.016
CAS Article PubMed Google Scholar
Drăgan L, Györke A, Ferreira JF, Pop IA, Dunca I, Drăgan M, Mircean V, Dan I, Cozma V (2014) Effects of Artemisia annua and Foeniculum vulgare on chickens highly infected with Eimeria tenella (phylum Apicomplexa). Acta Vet Scand 56:22. https://doi.org/10.1186/1751-0147-56-22
Article PubMed PubMed Central Google Scholar
Dubey JP (2010) Toxoplasma gondii infections in chickens (Gallus domesticus): prevalence, clinical disease, diagnosis and public health significance. Zoonoses Public Health 57(1):60–73. https://doi.org/10.1111/j.1863-2378.2009.01274
CAS Article PubMed Google Scholar
Dubey JP, Frenkel JK (1973) Experimental toxoplasma infection in mice with strains producing oocysts. J Parasitol 59(3):505–512
CAS Article Google Scholar
Dubey JP, Ruff MD, Camargo ME, Shen SK, Wilkins GL, Kwok OC, Thulliez P (1993) Serologic and parasitologic responses of domestic chickens after oral inoculation with Toxoplasma gondii oocysts. Am J Vet Res 54:1668–1672
CAS PubMed Google Scholar
Dubey JP, Levy MZ, Sreekumar C, Kwok OCH, Shen SK, Dahl E, Thulliez P, Lehmann T (2004) Tissue distribution and molecular characterization of chicken isolates of Toxoplasma gondii from Peru. J Parasitol 90(5):1015–1018. https://doi.org/10.1645/GE-329R
CAS Article PubMed Google Scholar
Dunay IR, Chan WC, Haynes RK, Sibley LD (2009) Artemisone and artemiside control acute and reactivated toxoplasmosis in a murine model. Antimicrob Agents Chemother 53(10):4450–4456. https://doi.org/10.1128/aac.00502-09
CAS Article PubMed PubMed Central Google Scholar
Elmore SA, Jones JL, Conrad PA, Patton S, Lindsay DS, Dubey JP (2010) Toxoplasma gondii: epidemiology, feline clinical aspects, and prevention. Trends Parasitol 26(4):190–196. https://doi.org/10.1016/j.pt.2010.01.009
Article PubMed Google Scholar
FAO/WHO (2000) Food additives. Guidelines for the preparation of toxicological working papers for the Joint FAO/WHO Expert Committee on Food Additives
Ferreira JFS, Gonzalez JM (2009) Analysis of underivatized artemisinin and related sesquiterpene lactones by high-performance liquid chromatography with ultraviolet detection. Phytochem Anal 56:91–97. https://doi.org/10.1002/pca.1101
CAS Article Google Scholar
Geuthner AC, Koethe M, Ludewig M, Pott S, Schares G, Daugschies A, Bangoura B (2014) Persistence of Toxoplasma gondii tissue stages in poultry over a conventional fattening cycle. Parasitol 141:1359–1364. https://doi.org/10.1017/s003118201400078x
CAS Article Google Scholar
Geuthner AC, Koethe M, Ludewig M, Pott S, Schares G, Maksimov P, Daugschies A, Bangoura B (2019) Development of an in vivo model for toxoplasma gondii infections in chickens and turkeys simulating natural routes of infection. Vet Parasitol 276:108956. https://doi.org/10.1016/j.vetpar.2019.108956
CAS Article PubMed Google Scholar
Godoi FSLD, Nishi SM, Pena HFDJ, Gennari SM (2010) Toxoplasma gondii: diagnosis of experimental and natural infection in pigeons (Columba livia) by serological, biological and molecular techniques. Rev Bras Parasitol Vet 19(4):237–243. https://doi.org/10.1590/S1984-29612010000400009
Article Google Scholar
Gyӧrke A, Pop LM, Mircean M, Kalmár Z, Tăbăran AF, Paștiu AI, Dumitrache MO, Magdaș C, Balea A, Bărburaș D, Mircean V, Cozma V (2019) Metabolic and tissular effects of artemisinin supplemented diets in broiler chicken. Pol J Vet Sci 22(2):297–304. https://doi.org/10.24425/pjvs.2019.129220
CAS Article PubMed Google Scholar
Hencken CP, Jones-Brando L, Bordón C, Stohler R, Mott BT, Yolken R, Woodard LE (2010) Thiazole, oxadiazole, and carboxamide derivatives of artemisinin are highly selective and potent inhibitors of Toxoplasma gondii. J Med Chem 53(9):3594–3601. https://doi.org/10.1021/jm901857d
CAS Article PubMed PubMed Central Google Scholar
Hiob L, Koethe M, Schares G, Goroll T, Daugschies A, Bangoura B (2017) Experimental Toxoplasma gondii and Eimeria tenella co-infection in chickens. Parasitol Res 116(11):3189–3203. https://doi.org/10.1007/s00436-017-5636-2
Article PubMed Google Scholar
Homan WL, Vercammen M, De Braekeleer J, Verschueren H (2000) Identification of a 200-to 300-fold repetitive 529 bp DNA fragment in Toxoplasma gondii, and its use for diagnostic and quantitative PCR. Int J Parasitol 30(1):69–75. https://doi.org/10.1016/S0020-7519(99)00170-8
CAS Article PubMed Google Scholar
Islamuddin M, Chouhan G, Farooque A, Dwarakanath BS, Sahal D, Afrin F (2015) Th1-biased immunomodulation and therapeutic potential of Artemisia annua in murine visceral leishmaniasis. PLoS Negl Trop Dis 9(1):3321. https://doi.org/10.1371/journal.pntd.0003321
CAS Article Google Scholar
Khan A, Taylor S, Su C, Mackey AJ, Boyle J, Cole R, Glover D, Tang K, Paulsen IT, Berriman M, Boothroyd JC (2005) Composite genome map and recombination parameters derived from three archetypal lineages of Toxoplasma gondii. Nucleic Acids Res 33(9):2980–2992. https://doi.org/10.1093/nar/gki604
CAS Article PubMed PubMed Central Google Scholar
Koethe M, Straubinger RK, Pott S, Bangoura B, Geuthner AC, Daugschies A, Ludewig M (2015) Quantitative detection of Toxoplasma gondii in tissues of experimentally infected turkeys and in retail Turkey products by magnetic-capture PCR. Food Microbiol 52:11–17. https://doi.org/10.1016/j.fm.2015.06.005
CAS Article PubMed Google Scholar
Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174
CAS Article Google Scholar
Lappin MR (2010) Update on the diagnosis and management of Toxoplasma gondii infection in cats. Top Companion Anim Med 25(3):36–141. https://doi.org/10.1053/j.tcam.2010.07.002
Article Google Scholar
Lindsay DS, Blagburn BL (1994) Activity of Diclazuril against Toxoplasma gondii in cultured cells and mice. Am J Vet Res 55(4):530–533
CAS PubMed Google Scholar
Lindsay DS, Rippey NS, Blagburn BL (1995) Treatment of acute Toxoplasma gondii infections in mice with Diclazuril or a combination of Diclazuril and pyrimethamine. J Parasitol 81:315–318. https://doi.org/10.2307/3283944
CAS Article PubMed Google Scholar
Malkwitz I, Berndt A, Daugschies A, Bangoura B (2013) Long-term investigations on Toxoplasma gondii-infected primary chicken macrophages. Parasitol Res 112(9):3115–3122. https://doi.org/10.1007/s00436-013-3486-0
Article PubMed Google Scholar
Maxwell MH (1993) Avian blood leucocyte responses to stress. World Poultry Sci J 49:34–43. https://doi.org/10.1079/WPS19930004
Article Google Scholar
Mirzaalizadeh B, Sharif M, Daryani A, Ebrahimzadeh MA, Zargari M, Sarvi S, Mehrzadi S, Rahimi MT, Mirabediny Z, Golpour M, Montazeri M (2018) Effects of Aloe vera and Eucalyptus methanolic extracts on experimental toxoplasmosis in vitro and in vivo. Exp Parasitol 192:6–11. https://doi.org/10.1016/j.exppara.2018.07.010
CAS Article PubMed Google Scholar
Montoya A, Miro G, Mateo M, Ramirez C, Fuentes I (2009) Detection of Toxoplasma gondii in cats by comparing bioassay in mice and polymerase chain reaction (PCR). Vet Parasitol 160:159–162. https://doi.org/10.1016/j.vetpar.2008.10.029
CAS Article PubMed Google Scholar
Müller J, Balmer V, Winzer P, Rahman M, Manser V, Haynes RK, Hemphill A (2015) In vitro effects of new artemisinin derivatives in Neospora caninum-infected human fibroblasts. Int J Antimicrob Agents 46(1):88–93. https://doi.org/10.1016/j.ijantimicag.2015.02.020
CAS Article PubMed Google Scholar
Nagamune K, Beatty WL, Sibley SD (2007) Artemisinin induces calcium-dependent protein secretion in the protozoan parasite Toxoplasma gondii. Eukaryot Cell 6(11):2147–2156. https://doi.org/10.1128/ec.00262-07
CAS Article PubMed PubMed Central Google Scholar
Nedișan ME, Ursache AL, Dumitrache MO, Mircean V, Cozma-Petruț A, Gyӧrke A (2019) Intestinal toxoplasmosis in cats treated with Procox (case report). Sci Parasitol 20(1–2):19–24
Google Scholar
Ognean L, Cernea LC (2011) Practical applications in animal physiology. Ed. Academic Pres, Cluj-Napoca
Ogolla KO, Gathumbi PK, Waruiru RM, Okumu PO, Chebet J, Kitala PM (2018) Efficacy of sulphachloropyrazine, amprolium hydrochloride, trimethoprim-sulphamethoxazole, and Diclazuril against experimental and natural rabbit coccidiosis. J Vet Med 5402469:1–11. https://doi.org/10.1155/2018/5402469
CAS Article Google Scholar
Opsteegh M, Schares G, Blaga R, van der Giessen J (2016) Experimental studies of Toxoplasma gondii in the main livestock species (GP/EFSA/BIOHAZ/2013/01) Final report. EFSA Support Public EN-995:161. https://doi.org/10.2903/sp.efsa.2016.EN-995
Article Google Scholar
Paştiu AI, Cozma-Petruț A, Mercier A, Balea A, Galal L, Mircean V, Pusta DL, Bogdan L, Györke A (2019) Prevalence and genetic characterization of Toxoplasma gondii in naturally infected backyard pigs intended for familial consumption in Romania. Parasit Vectors 12(1):586. https://doi.org/10.1186/s13071-019-3842-8
Article PubMed PubMed Central Google Scholar
Pop L, Györke A, Tǎbǎran AF, Dumitrache MO, Kalmár Z, Magdaş C, Mircean V, Zagon D, Balea A, Cozma V (2015) Effects of artemisinin in broiler chickens challenged with Eimeria acervulina, E. maxima and E. tenella in battery trials. Vet Parasitol 214(3–4):264–271. https://doi.org/10.1016/j.vetpar.2015.10.011
Quéré P, Pierre J, Hoang MD, Esnault E, Domenech J, Sibille P, Dimier- Poisson I (2013) Presence of dendritic cells in chicken spleen cell preparations and their functional interaction with the parasite Toxoplasma gondii. Vet Immunol Immunopathol 153:57–69. https://doi.org/10.1016/j.vetimm.2013.02.007
CAS Article PubMed Google Scholar
Rodrigues FT, Moreira FA, Coutinho T, Dubey JP, Cardoso L, Lopes AP (2019) Antibodies to Toxoplasma gondii in slaughtered free-range and broiler chickens. Vet Parasitol 271:31–53. https://doi.org/10.1016/j.vetpar.2019.06.007
Article Google Scholar
Schares G, Bangoura B, Randau F, Goroll T, Ludewig M, Maksimov P, Opsteegh M (2017) High seroprevalence of Toxoplasma gondii and probability of detecting tissue cysts in backyard laying hens compared with hens from large free-range farms. Int J Parasitol 47(12):765–777. https://doi.org/10.1016/j.ijpara.2017.07.003
CAS Article PubMed Google Scholar
Schmidt S (2015) Top 5 leukogram patterns. Available at: <Available at: http://www.cliniciansbrief.com >.
Sergeant ESG (2018) Epitools epidemiological calculators. Ausvet. Available at: http://epitools.ausvet.com.au
Su C, Zhang X, Dubey JP (2006) Genotyping of Toxoplasma gondii by multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites. Int J Parasitol 36(7):841–848. https://doi.org/10.1016/j.ijpara.2006.03.003
CAS Article PubMed Google Scholar
Tajehmiri A, Issapour F, Moslem MN, Lakeh MT, Kolavani MH (2014) In vitro antimicrobial activity of Artemisia annua leaf extracts against pathogenic bacteria. Adv Stud Biol 6(3):93–97. https://doi.org/10.12988/asb.2014.4525
Article Google Scholar
Villena I, Durand B, Aubert D, Blaga R, Geers R, Thomas M, Perret C, Alliot A, Escotte-Binet S, Thébault A, Boireau P (2012) New strategy for the survey of Toxoplasma gondii in meat for human consumption. Vet Parasitol 183(3–4):203–208. https://doi.org/10.1016/j.vetpar.2011.08.001
Article PubMed Google Scholar
Watson PF, Petrie A (2010) Method agreement analysis: a review of correct methodology. Theriogenology 73:1167–1179. https://doi.org/10.1016/j.theriogenology.2010.01.003
CAS Article PubMed Google Scholar
Yan C, Yue CL, Yuan ZG, Lin RQ, He Y, Yin CC, Xu MJ, Song HQ, Zhu XQ (2010) Molecular and serological diagnosis of Toxoplasma gondii infection in experimentally infected chickens. Vet Parasitol 173:179–183. https://doi.org/10.1016/j.vetpar.2010.07.011
CAS Article PubMed Google Scholar
Zechner G, Bauer C, Jacobs J, Goossens L, Vertenten G, Taylor MA (2015) Efficacy of Diclazuril and toltrazuril in the prevention of coccidiosis in dairy calves under field conditions. Vet Rec 176:126–126. https://doi.org/10.1136/vr.102237

Download references

Acknowledgments

AG, RB and GS are part of the TOXOSOURCES consortium, supported by funding from the European Union’s Horizon 2020 Research and Innovation programme under grant agreement No 773830: One Health European Joint Programme.

Funding

This work was supported by the University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca through internal research grant number 6142/10.04.2017 and by COST Action FA 1408 through 2 STSM in the Institute for Medical Research, Belgrade, Serbia, and National Veterinary School of Alfort, UMR BIPAR, ANSES, INRA, University Paris-Est, Maisons-Alfort Animal Health Laboratory, Maisons-Alfort, France.

Author information

Maria E. Nedişan & Adriana Györke
Present address: Department of Parasitology and Parasitic Diseases, Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca, 3-5 Mănăştur Street, 400372, Cluj-Napoca, Romania
Maria E. Nedişan and Adriana Györke contributed equally to this work.

Affiliations

Department of Parasitology and Parasitic Diseases, Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca, 3-5 Mănăştur Street, 400372, Cluj-Napoca, Romania
Cristina L. Ştefănuţ, Zsuzsa Kalmár, Andra Toma-Naic, Viorica Mircean & Vasile Cozma
Research and Development Station for Cattle Breeding, 547530, Târgu Mureș, Romania
Zsuzsa Friss
Ecole Nationale Vétérinaire d’Alfort, UMR BIPAR, ANSES, INRA, Université Paris-Est, Laboratoire de Santé Animale de Maisons-Alfort, Maisons-Alfort, Paris, France
Radu Blaga & Amandine Blaizot
Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute of Epidemiology, National Reference Centre for Toxoplasmosis, Greifswald-Insel Riems, Germany
Gereon Schares
Institute for Medical Research, Dr. Subotića 4, PO Box 102, Belgrade, 11000, Serbia
Olgica Djurković-Djaković & Ivana Klun
National Reference Centre for Toxoplasmosis, Laboratory of Parasitology, Hospital Maison Blanche, EA 7510, University of Reims Champagne-Ardenne, Reims, France
Isabelle Villena

Authors

Maria E. Nedişan
View author publications
You can also search for this author in PubMed Google Scholar
Adriana Györke
View author publications
You can also search for this author in PubMed Google Scholar
Cristina L. Ştefănuţ
View author publications
You can also search for this author in PubMed Google Scholar
Zsuzsa Kalmár
View author publications
You can also search for this author in PubMed Google Scholar
Zsuzsa Friss
View author publications
You can also search for this author in PubMed Google Scholar
Radu Blaga
View author publications
You can also search for this author in PubMed Google Scholar
Amandine Blaizot
View author publications
You can also search for this author in PubMed Google Scholar
Andra Toma-Naic
View author publications
You can also search for this author in PubMed Google Scholar
Viorica Mircean
View author publications
You can also search for this author in PubMed Google Scholar
Gereon Schares
View author publications
You can also search for this author in PubMed Google Scholar
Olgica Djurković-Djaković
View author publications
You can also search for this author in PubMed Google Scholar
Ivana Klun
View author publications
You can also search for this author in PubMed Google Scholar
Isabelle Villena
View author publications
You can also search for this author in PubMed Google Scholar
Vasile Cozma
View author publications
You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: A.G., M.E.N., and V.C.; methodology: M.E.N., C.Ș., Z.K., Z.F., A.B., A.T.N., G.S., I.K., and I.V.; formal analysis: M.E.N., A.G., C.Ș., R.B., V.M., and G.S.; writing—original draft preparation: M.E.N. and A.G.; writing—review and editing: A.G, G.S., O.D.D., and I.V. All authors have read and agreed to the published version of the manuscript.

Corresponding authors

Correspondence to Maria E. Nedişan or Adriana Györke.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

The experiment was approved by the Animal Ethics Committee of UASVM CN (protocol no. 92/20.12.2017).

Consent to participate

Not applicable.

Code availability

Not applicable.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Section Editor: Berit Bangoura

Supplementary information

ESM 1

(DOCX 19 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Nedişan, M.E., Györke, A., Ştefănuţ, C.L. et al. Experimental infection with Toxoplasma gondii in broiler chickens (Gallus domesticus): seroconversion, tissue cyst distribution, and prophylaxis. Parasitol Res 120, 593–603 (2021). https://doi.org/10.1007/s00436-020-06984-x

Download citation

Received: 01 April 2020
Accepted: 22 November 2020
Published: 08 January 2021
Issue Date: February 2021
DOI: https://doi.org/10.1007/s00436-020-06984-x

Keywords

Artemisia annua
Chickens
Diclazuril
Mouse bioassay
Tissue cysts
Toxoplasma gondii

Abstract

Access options

Buy single article

Data availability

References

Acknowledgments

Funding

Author information

Affiliations

Contributions

Corresponding authors

Ethics declarations

Conflict of interest

Ethics approval

Consent to participate

Code availability

Additional information

Publisher’s note

Supplementary information

ESM 1

Rights and permissions

About this article

Cite this article

Share this article

Keywords