Toxoplasma gondii genotypes and frequency in domestic cats from Romania.
Toxoplasma
Cats
Genotypes
Romania
Journal
BMC veterinary research
ISSN: 1746-6148
Titre abrégé: BMC Vet Res
Pays: England
ID NLM: 101249759
Informations de publication
Date de publication:
17 Aug 2024
17 Aug 2024
Historique:
received:
22
02
2023
accepted:
26
07
2024
medline:
17
8
2024
pubmed:
17
8
2024
entrez:
16
8
2024
Statut:
epublish
Résumé
Toxoplasma gondii is a zoonotic protozoan parasite with a heteroxenus life cycle that involves felids as the definitive hosts and any warm-blooded animal, including humans, as intermediate hosts. Cats are key players in parasite transmission as they are capable of shedding high numbers of oocysts in their feces that contaminate the environment. The study was performed on 31 domestic cats (31.23 ± 27.18 months old) originating from rural and urban areas (5.17:1) in the center and north-west Romania. Feces (n = 31), blood (n = 28), and heart samples (n = 27) were collected. Fecal samples were analyzed by flotation technique, and PCR (529 bp repetitive element). Fecal samples with T. gondii oocysts were bioassayed in mice. Serum samples were analyzed by modified agglutination test and ImmunoComb for the detection of specific anti-T. gondii IgG antibodies. Heart samples were bioassayed in mice, and analyzed by PCR. Toxoplasma gondii positive samples were genotyped by nPCR-RFLP targeting eleven genetic loci (SAG1, SAG2, alt-SAG2, SAG3, BTUB, GRA6, c22-8, c29-2, L358, PK1, and Apico). Toxoplasma gondii oocysts were found in 2 out of 31 fecal samples collected from a 3-months old stray kitten, and a 4-years old female. In total, 17 out of 27 sera were positive for T. gondii IgG antibodies. The antibody titers in MAT ranged from 1:6 to 1:384. Toxoplasma gondii DNA was detected in 7 out of 27 heart samples, and four of them were positive also by bioassay. Six T. gondii DNA samples from bioassayed mice could be assigned to ToxoDB PCR-RFLP genotype #1 or #3 (Type II) and one T. gondii DNA from heart digest to genotype #2 (Type III). Both of these genotypes are common in Europe. Our results revealed that the infection with T. gondii is still high in cats from Romania. The oocysts shedded by these cats represent an important source of infection for intermediate hosts, including humans. Further studies on a wider range of cases are necessary for a more exhaustive definition of the T. gondii genotypes circulating in Romania.
Sections du résumé
BACKGROUND
BACKGROUND
Toxoplasma gondii is a zoonotic protozoan parasite with a heteroxenus life cycle that involves felids as the definitive hosts and any warm-blooded animal, including humans, as intermediate hosts. Cats are key players in parasite transmission as they are capable of shedding high numbers of oocysts in their feces that contaminate the environment.
METHODS
METHODS
The study was performed on 31 domestic cats (31.23 ± 27.18 months old) originating from rural and urban areas (5.17:1) in the center and north-west Romania. Feces (n = 31), blood (n = 28), and heart samples (n = 27) were collected. Fecal samples were analyzed by flotation technique, and PCR (529 bp repetitive element). Fecal samples with T. gondii oocysts were bioassayed in mice. Serum samples were analyzed by modified agglutination test and ImmunoComb for the detection of specific anti-T. gondii IgG antibodies. Heart samples were bioassayed in mice, and analyzed by PCR. Toxoplasma gondii positive samples were genotyped by nPCR-RFLP targeting eleven genetic loci (SAG1, SAG2, alt-SAG2, SAG3, BTUB, GRA6, c22-8, c29-2, L358, PK1, and Apico).
RESULTS
RESULTS
Toxoplasma gondii oocysts were found in 2 out of 31 fecal samples collected from a 3-months old stray kitten, and a 4-years old female. In total, 17 out of 27 sera were positive for T. gondii IgG antibodies. The antibody titers in MAT ranged from 1:6 to 1:384. Toxoplasma gondii DNA was detected in 7 out of 27 heart samples, and four of them were positive also by bioassay. Six T. gondii DNA samples from bioassayed mice could be assigned to ToxoDB PCR-RFLP genotype #1 or #3 (Type II) and one T. gondii DNA from heart digest to genotype #2 (Type III). Both of these genotypes are common in Europe.
CONCLUSIONS
CONCLUSIONS
Our results revealed that the infection with T. gondii is still high in cats from Romania. The oocysts shedded by these cats represent an important source of infection for intermediate hosts, including humans. Further studies on a wider range of cases are necessary for a more exhaustive definition of the T. gondii genotypes circulating in Romania.
Identifiants
pubmed: 39152437
doi: 10.1186/s12917-024-04210-9
pii: 10.1186/s12917-024-04210-9
doi:
Substances chimiques
Antibodies, Protozoan
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
369Informations de copyright
© 2024. The Author(s).
Références
Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma Gondii: from animals to humans. Int J Parasitol. 2000;30(12–13):1217–58.
pubmed: 11113252
pmcid: 3109627
Dubey JP, Beattie CP. Toxoplasmosis of animals and man. Florida: CRC, Boca Raton; 1988. p. 220.
Dubey JP. Toxoplasmosis - a waterborne zoonosis. Vet Parasitol. 2004;126(1–2):57–72.
pubmed: 15567579
Dubey JP. Duration of immunity to shedding of Toxoplasma Gondii oocysts by cats. J Parasitol. 1995;81(3):410–5.
pubmed: 7776126
Zulpo DL, Sammi AS, Dos Santos JR, Sasse JP, Martins TA, Minutti AF, et al. Toxoplasma Gondii: a study of oocyst re-shedding in domestic cats. Vet Parasitol. 2018;249:17–20.
pubmed: 29279081
Dubey JP, Carpenter JL. Histologically confirmed clinical toxoplasmosis in cats: 100 cases (1952–1990). J Am Vet Med Assoc. 1993;203(11):1556–66.
pubmed: 8288479
Dubey JP. Toxoplasmosis of animals and humans. 2nd ed. Florida: CRC, Boca Raton; 2010. p. 313.
Dubey JP, Hoover EA. Attempted transmission of Toxoplasma Gondii infection from pregnant cats to their kittens. J Am Vet Med Assoc. 1977;170(5):538–40.
pubmed: 557468
Dubey JP, Carpenter JL. Neonatal toxoplasmosis in littermate cats. J Am Vet Med Assoc. 1993;203(11):1546–9.
pubmed: 8288476
Brennan A, Donahoe SL, Beatty JA, Belov K, Lindsay S, Briscoe KA, et al. Comparison of genotypes of Toxoplasma Gondii in domestic cats from Australia with latent infection or clinical toxoplasmosis. Vet Parasitol. 2016;228:13–6.
pubmed: 27692314
Dubey JP, Lappin MR, Thulliez P. Diagnosis of induced toxoplasmosis in neonatal cats. J Am Vet Med Assoc. 1995;207(2):179–85.
pubmed: 7601711
Dubey JP, Cerqueira-Cézar CK, Murata FHA, Kwok OCH, Yang YR, Su C. All about toxoplasmosis in cats: the last decade. Vet Parasitol. 2020;283:109145.
pubmed: 32645556
Dubey JP, Zajac A, Osofsky SA, Tobias L. Acute primary toxoplasmic hepatitis in an adult cat shedding Toxoplasma Gondii oocysts. J Am Vet Med Assoc. 1990;197(12):1616–8.
pubmed: 2276958
Dardé ML. Toxoplasma Gondii, new genotypes and virulence. Parasite. 2008;15(3):366–71.
pubmed: 18814708
Ajzenberg D, Yera H, Marty P, Paris L, Dalle F, Menotti J, et al. Genotype of 88 Toxoplasma Gondii isolates associated with toxoplasmosis in immunocompromised patients and correlation with clinical findings. J Infect Dis. 2009;199(8):1155–67.
pubmed: 19265484
Delhaes L, Ajzenberg D, Sicot B, Bourgeot P, Dardé ML, Dei-Cas E, et al. Severe congenital toxoplasmosis due to a Toxoplasma Gondii strain with an atypical genotype: case report and review. Prenat Diagn. 2010;30(9):902–5.
pubmed: 20582922
Amouei A, Sarvi S, Sharif M, Aghayan SA, Javidnia J, Mizani A, et al. A systematic review of Toxoplasma gondii genotypes and feline: geographical distribution trends. Transbound Emerg Dis. 2020;67(1):46–64.
pubmed: 31464067
Calero-Bernal R, Gennari SM. Clinical toxoplasmosis in Dogs and cats: an update. Front Vet Sci. 2019;6:54.
pubmed: 30863754
pmcid: 6399377
Dragomir C. Isolation on the animal (white mice) of a strain of Toxoplasma from a case of human toxoplasmosis. Microbio Parasitol Epid. 1956;4:18–26.
Dubey JP, Hotea I, Olariu TR, Jones JL, Dărăbuş G. Epidemiological review of toxoplasmosis in humans and animals in Romania. Parasitology. 2014;141(3):311–25.
pubmed: 24553077
Dărăbuş G, Afrenie M, Hotea I, Imre M, Morariu S. Endoparasites in mammals from seven zoological gardens in Romania. J Zoo Wildl Med. 2014;45(2):239–46.
pubmed: 25000683
Şuteu O, Mihalca AD, Paştiu AI, Györke A, Matei IA, Ionică A, et al. Red foxes (Vulpes vulpes) in Romania are carriers of Toxoplasma Gondii but not Neospora Caninum. J Wildl Dis. 2014;50(3):713–6.
pubmed: 24807364
Paştiu AI, Györke A, Kalmár Z, Bolfă P, Rosenthal BM, Oltean M, et al. Toxoplasma Gondii in horse meat intended for human consumption in Romania. Vet Parasitol. 2015;212(3–4):393–5.
pubmed: 26238654
Paştiu AI, Ajzenberg D, Györke A, Şuteu O, Balea A, Rosenthal BM, et al. Traditional goat husbandry may substantially contribute to human toxoplasmosis exposure. J Parasitol. 2015;101(1):45–9.
pubmed: 25003793
Bărburaș D, Gyӧrke A, Blaga R, Bărburaș R, Kalmár Z, Vişan S, et al. Toxoplasma Gondii in water buffaloes (Bubalus bubalis) from Romania: what is the importance for public health? Parasitol Res. 2019;118(9):2695–703.
pubmed: 31309289
Căpraru ID, Lupu MA, Horhat F, Olariu TR. Toxoplasmosis Seroprevalence in Romanian Children. Vector Borne Zoonotic Dis. 2019;19(11):867–9.
pubmed: 31216238
Paştiu AI, Cozma-Petruț A, Mercier A, Balea A, Galal L, Mircean V, et al. Prevalence and genetic characterization of Toxoplasma Gondii in naturally infected backyard pigs intended for familial consumption in Romania. Parasit Vectors. 2019;12(1):586.
pubmed: 31842955
pmcid: 6915976
Mircean V, Titilincu A, Cozma V. Prevalence of endoparasites in household cat (Felis catus) populations from Transylvania (Romania) and association with risk factors. Vet Parasitol. 2010;171(1–2):163–6.
pubmed: 20381250
Györke A, Opsteegh M, Mircean V, Iovu A, Cozma V. Toxoplasma Gondii in Romanian household cats: evaluation of serological tests, epidemiology and risk factors. Prev Vet Med. 2011;102(4):321–8.
pubmed: 21885135
Costache CA, Colosi HA, Blaga L, Györke A, Paştiu AI, Colosi IA, et al. First isolation and genetic characterization of a Toxoplasma gondii strain from a symptomatic human case of congenital toxoplasmosis in Romania. Parasite. 2013;20:11.
pubmed: 23537840
pmcid: 3718531
Nedișan ME, Ursache AL, Dumitrache MO, Mircean V, Cozma-Petruț A, Gyӧrke A. Intestinal toxoplasmosis in cats treated with Procox (case report). Sci Parasitol. 2019;20(1–2):19–24.
Su C, Zhang X, Dubey JP. Genotyping of Toxoplasma Gondii by Multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites. Int J Parasitol. 2006;36(7):841–8.
pubmed: 16643922
Mircean V, Cozma V, Gyorke A. Coproscopical diagnostic of parasitic diseases in animals [in Romanian]. Cluj-Napoca: Risoprint; 2011.
Villena I, Durand B, Aubert D, Blaga R, Geers R, Thomas M, et al. New strategy for the survey of Toxoplasma Gondii in meat for human consumption. Vet Parasitol. 2012;183(3–4):203–8.
pubmed: 21864981
Russell WMS, Burch RL. The principles of humane experimental technique. Wheathampstead (UK): Universities Federation for Animal Welfare; 1959.
Homan WL, Vercammen M, De Braekeleer J, Verschueren H. 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. 2000;30(1):69–75.
pubmed: 10675747
Dean AG, Arner TG, Sunki GG, Friedman R, Lantinga M, Sangam S, et al. Epi Info™, a database and statistics program for public health professionals. Atlanta, GA, USA: CDC; 2011.
Shwab EK, Zhu XQ, Majumdar D, Pena HF, Gennari SM, Dubey JP, Su C. Geographical patterns of Toxoplasma Gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitol. 2014;141(4):453–61.
Titilincu A, Mircean V, Blaga R, Chitimia L, Cernea M, Mirescu F, et al. Research regarding the prevalence of Toxoplasma gondii infection in cats [in Romanian]. Rev Sci Parasitol. 2007;8(2–3):68–77.
Hotea I, Dărăbuş G, Mederle N, Ilie MS, Imre K, Balint A, et al. Prevalence of Toxoplasma gondii infection in cats from Arad county [in Romanian]. Lucr Şt Med Vet Univ Șt Agr Med Vet Ion Ionescu De La Brad Iași. 2009;52(1):587–92.
Iovu AI. Toxoplasmosis in small ruminants and pigs – epidemiology, diagnosis and prevention of the disease [in Romanian]. PhD thesis. Cluj-Napoca: Univ. Agr Sc Vet Medicine. 2011.
Schares G, Vrhovec MG, Pantchev N, Herrmann DC, Conraths FJ. Occurrence of Toxoplasma Gondii and Hammondia Hammondi oocysts in the faeces of cats from Germany and other European countries. Vet Parasitol. 2008;152(1–2):34–45.
pubmed: 18226453
Schares G, Ziller M, Herrmann DC, Globokar MV, Pantchev N, Conraths FJ. Seasonality in the proportions of domestic cats shedding Toxoplasma Gondii or Hammondia Hammondi oocysts is associated with climatic factors. Int J Parasitol. 2016;46(4):263–73.
pubmed: 26820303
Berger-Schoch AE, Herrmann DC, Schares G, Müller N, Bernet D, Gottstein B, et al. Prevalence and genotypes of Toxoplasma Gondii in feline faeces (oocysts) and meat from sheep, cattle and pigs in Switzerland. Vet Parasitol. 2011;177(3–4):290–7.
pubmed: 21183278
Salant H, Markovics A, Spira DT, Hamburger J. The development of a molecular approach for coprodiagnosis of Toxoplasma Gondii. Vet Parasitol. 2007;146(3–4):214–20.
pubmed: 17395378
Mancianti F, Nardoni S, Ariti G, Parlanti D, Giuliani G, Papini RA. Cross-sectional survey of Toxoplasma gondii infection in colony cats from urban Florence (Italy). J Feline Med Surg. 2010;12(4):351–4.
pubmed: 19811938
Torrey EF, Yolken RH. Toxoplasma oocysts as a public health problem. Trends Parasitol. 2013;29(8):380–4.
pubmed: 23849140
Montoya A, Miró G, Mateo M, Ramírez C, Fuentes I. Detection of Toxoplasma Gondii in cats by comparing bioassay in mice and polymerase chain reaction (PCR). Vet Parasitol. 2009;160(1–2):159–62.
pubmed: 19038500
Opsteegh M, Haveman R, Swart AN, Mensink-Beerepoot ME, Hofhuis A, Langelaar MF, et al. Seroprevalence and risk factors for Toxoplasma gondii infection in domestic cats in the Netherlands. Prev Vet Med. 2012;104(3–4):317–26.
pubmed: 22305876
Zhu S, Shapiro K, VanWormer E. Dynamics and epidemiology of Toxoplasma Gondii oocyst shedding in domestic and wild felids. Transbound Emerg Dis. 2022;69(5):2412–23.
pubmed: 34153160
Sioutas G, Symeonidou I, Gelasakis AI, Tzirinis C, Papadopoulos E. Feline toxoplasmosis in Greece: a countrywide seroprevalence study and associated risk factors. Pathogens. 2022;11(12):1511.
pubmed: 36558845
pmcid: 9785270
National Reference Centre on toxoplasmosis/Toxoplasma Biological Resource Center, Reims CHU. General Koening Street, Reims, France. http://www.toxocrb.com/about-brc-toxoplasma/view?set_language=en
Jokelainen P, Simola O, Rantanen E, Näreaho A, Lohi H, Sukura A. Feline toxoplasmosis in Finland: cross-sectional epidemiological study and case series study. J Vet Diagn Invest. 2012;24(6):1115–24.
pubmed: 23012380
Maksimov P, Zerweck J, Dubey JP, Pantchev N, Frey CF, Maksimov A, et al. Serotyping of Toxoplasma Gondii in cats (Felis Domesticus) reveals predominance of type II infections in Germany. PLoS ONE. 2013;8(11):e80213.
pubmed: 24244652
pmcid: 3820565
Spycher A, Geigy C, Howard J, Posthaus H, Gendron K, Gottstein B, et al. Isolation and genotyping of Toxoplasma Gondii causing fatal systemic toxoplasmosis in an immunocompetent 10-year-old cat. J Vet Diagn Invest. 2011;23(1):104–8.
pubmed: 21217037
Pena HF, Soares RM, Amaku M, Dubey JP, Gennari SM. Toxoplasma Gondii infection in cats from São Paulo state, Brazil: seroprevalence, oocyst shedding, isolation in mice, and biologic and molecular characterization. Res Vet Sci. 2006;81(1):58–67.
pubmed: 16289158
Montoya A, Miró G, Mateo M, Ramírez C, Fuentes I. Molecular characterization of Toxoplasma Gondii isolates from cats in Spain. J Parasitol. 2008;94(5):1044–6.
pubmed: 18576763
Herrmann DC, Pantchev N, Vrhovec MG, Barutzki D, Wilking H, Fröhlich A, et al. Atypical Toxoplasma gondii genotypes identified in oocysts shed by cats in Germany. Int J Parasitol. 2010;40(3):285–92.
pubmed: 19695254
Can H, Döşkaya M, Ajzenberg D, Özdemir HG, Caner A, İz SG, et al. Genetic characterization of Toxoplasma Gondii isolates and toxoplasmosis seroprevalence in stray cats of İzmir, Turkey. PLoS ONE. 2014;9(8):e104930.
pubmed: 25127360
pmcid: 4134241