DNA Amplification Techniques for the Detection of Toxoplasma gondii Tissue Cysts in Meat Producing Animals: A Narrative Review Article
AbstractBackground: Toxoplasma gondii is an intracellular parasite, which infects one-third population of world. Humans and animals acquire infection by ingesting oocytes from feces of cats or by meat of other animals having cysts that may lead to congenital, ocular or cephalic toxoplasmosis. Either it is important to detect T. gondii from meat of food animals from retail shops or directly at slaughterhouses, which is meant for export.Methods: The current research was done without time limitation using such terms as follows: “Toxoplasma gondii”, “Meat”, “Tissue cyst”, “PCR”, “LAMP”, “Screening” and “Immunological assay” alone or in combination, in English language. The used electronic databases for searching included as follows: PubMed, Scopus, Google Scholar, Web of Science and Science Direct. The searches were limited to the published papers to English language.Results: Sensitivity of different molecular techniques for diagnosis of Toxoplasma is real-time PCR > LAMP > conventional PCR. In addition to these DNA analysis tools, bioassay in mice and cats is considered as “gold standard” to detect T. gondii. Conclusion: This review article will help the readers for grasping advantages and limitations of different diagnostic tools for screening meat samples for T. gondii. This review also makes bibliography about the type of meat sample to be processed for diagnosis and different primers or sequences to be targeted for T. gondii by number of researches for its detection from meat or tissue sample using DNA amplification techniques.
Weiss LM, Dubey JP. Toxoplasmosis: A history of clinical observations. Int J Parasitol. 2009; 39(8):895-901.
Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol. 2000; 30(12-13):1217-58.
Conrad PA, Miller MA, Kreuder C, James ER, Mazet J, Dabritz H, et al. Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. Int J Parasitol. 2005; 35(11-12):1155-68.
Glor SB, Edelhofer R, Grimm F, Deplazes P, Basso W. Evaluation of a commercial ELISA kit for detection of antibodies against Toxoplasma gondii in serum, plasma and meat juice from experimentally and naturally infected sheep. Parasit Vectors. 2013; 6:85.
Sarkari B, Asgari Q, Bagherian N, Ashkani Esfahani S, Kalantari M, Mohammadpour I, et al. Molecular and Serological Evaluation of Toxoplasma gondii Infection in Reared Turkeys in Fars Province, Iran. Jund J Microbiol. 2014; 7(7):e11598.
Ferguson DJ. Use of molecular and ultrastructural markers to evaluate stage conversion of Toxoplasma gondii in both the intermediate and definitive host. Int J Parasitol. 2004; 34(3):347-60.
Hong SH, Jeong YI, Kim JY, Cho SH, Lee WJ, Lee SE. Prevalence of Toxoplasma gondii infection in household cats in Korea and risk factors. Korean J Parasitol. 2013; 51(3):357-61.
Boyer KM, Holfels E, Roizen N, Swisher C, Mack D, Remington J, et al. Risk factors for Toxoplasma gondii infection in mothers of infants with congenital toxoplasmosis: Implications for prenatal management and screening. Am J Obstet Gynecol. 2005; 192(2):564-71.
Cook AJ, Gilbert RE, Buffolano W, Zufferey J, Petersen E, Jenum PA, et al. Sources of toxoplasma infection in pregnant women: European multicentre case-control study. European Research Network on Congenital Toxoplasmosis. BMJ. 2000; 321(7254):142-7.
Jones JL, Dargelas V, Roberts J, Press C, Remington JS, Montoya JG. Risk factors for Toxoplasma gondii infection in the United States. Clin Infect Dis. 2009; 49(6):878-84.
Halos L, Thebault A, Aubert D, Thomas M, Perret C, Geers R, et al. An innovative survey underlining the significant level of contamination by Toxoplasma gondii of ovine meat consumed in France. Int J Parasitol. 2010; 40(2):193-200.
Dubey JP. Toxoplasmosis of animals and humans: CRC press; 2009.
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.
Wastling JM, Nicoll S, Buxton D. Comparison of two gene amplification methods for the detection of Toxoplasma gondii in experimentally infected sheep. J Med Microbiol. 1993; 38(5):360-5.
Hänscheid T. Diagnosis of malaria: a review of alternatives to conventional microscopy. Clin Lab Haematol. 1999; 21(4):235-45.
Burg JL, Grover CM, Pouletty P, Boothroyd JC. Direct and sensitive detection of a pathogenic protozoan, Toxoplasma gondii, by polymerase chain reaction. J Clin Microbiol. 1989; 27(8):1787-92.
Tonkal AM. PCR versus ELISA in diagnosis of human toxoplasmosis in Jeddah, Saudi Arabia. J Egypt Soc Parasitol. 2008; 38(3):707-14.
Hafid J, Flori P, Raberin H, Tran Manh Sung R. Comparison of PCR, capture ELISA and immunoblotting for detection of Toxoplasma gondii in infected mice. J Med Microbiol. 2001; 50(12):1100-4.
Smith CJ, Osborn AM. Advantages and limitations of quantitative PCR (Q-PCR)-based approaches in microbial ecology. FEMS Microbiol Ecol. 2009; 67(1):6-20.
Kompalic-Cristo A, Frotta C, Suarez-Mutis M, Fernandes O, Britto C. Evaluation of a real-time PCR assay based on the repetitive B1 gene for the detection of Toxoplasma gondii in human peripheral blood. Parasitol Res. 2007; 101(3):619-25.
Calderaro A, Piccolo G, Gorrini C, Peruzzi S, Zerbini L, Bommezzadri S, et al. Comparison between two real-time PCR assays and a nested-PCR for the detection of Toxoplasma gondii. Acta Biomed. 2006; 77(2):75-80.
Teixeira LE, Kanunfre KA, Shimokawa PT, Targa LS, Rodrigues JC, Domingues W, et al. The performance of four molecular methods for the laboratory diagnosis of congenital toxoplasmosis in amniotic fluid samples. Rev Soc Bras Med Trop. 2013:0.
Opsteegh M, Langelaar M, Sprong H, den Hartog L, De Craeye S, Bokken G, et al. Direct detection and genotyping of Toxoplasma gondii in meat samples using magnetic capture and PCR. Int J Food Microbiol. 2010; 139(3):193-201.
Bretagne S, Costa JM. Towards a nucleic acid-based diagnosis in clinical parasitology and mycology. Clinica chimica acta. Int J Clin Chem. 2006; 363(1-2):221-8.
Notomi T, Okayama H, Masubuchi H, Yonekawa T, Watanabe K, Amino N, et al. Loop-mediated isothermal amplification of DNA. Nucleic Acids Res. 2000; 28(12):E63.
Zhang H, Thekisoe OMM, Aboge GO, Kyan H, Yamagishi J, Inoue N, et al. Toxoplasma gondii: Sensitive and rapid detection of infection by loop-mediated isothermal amplification (LAMP) method. Exp Parasitol. 2009; 122(1):47-50.
Lin Z, Zhang Y, Zhang H, Zhou Y, Cao J, Zhou J. Comparison of loop-mediated isothermal amplification (LAMP) and real-time PCR method targeting a 529-bp repeat element for diagnosis of toxoplasmosis. Vet parasitol. 2012; 185(2–4):296-300.
Wang Y, Wang G, Zhang D, Yin H, Wang M. Detection of acute toxoplasmosis in pigs using loop-mediated isothermal amplification and quantitative PCR. Korean J Parasitol. 2013; 51(5):573-7.
Kong QM, Lu SH, Tong QB, Lou D, Chen R, Zheng B, et al. Loop-mediated isothermal amplification (LAMP): early detection of Toxoplasma gondii infection in mice. Parasit Vectors. 2012; 5:2.
Macpherson CN. Human behaviour and the epidemiology of parasitic zoonoses. Int J Parasitol. 2005; 35(11-12):1319-31.
Kapperud G, Jenum PA, Stray-Pedersen B, Melby KK, Eskild A, Eng J. Risk factors for Toxoplasma gondii infection in pregnancy. Results of a prospective case-control study in Norway. Am J Epidemiol. 1996; 144(4):405-12.
Tenter AM. Toxoplasma gondii in animals used for human consumption. Mem Inst Oswaldo Cruz. 2009; 104(2):364-9.
Gencay YE, Yildiz K, Gokpinar S, Leblebicier A. A potential infection source for humans: Frozen buffalo meat can harbour tissue cysts of Toxoplasma gondii. Food control. 2013; 30(1):86-9.
Wang H, Wang T, Luo Q, Huo X, Wang L, Liu T, et al. Prevalence and genotypes of Toxoplasma gondii in pork from retail meat stores in Eastern China. Int J Food Microbiol. 2012; 157(3):393-7.
Dubey JP, Lopez B, Alvarez M, Mendoza C, Lehmann T. Isolation, tissue distribution, and molecular characterization of Toxoplasma gondii from free-range chickens from Guatemala. J Parasitol. 2005; 91(4):955-7.
Esteban-Redondo I, Maley SW, Thomson K, Nicoll S, Wright S, Buxton D, et al. Detection of T. gondii in tissues of sheep and cattle following oral infection. Vet Parasitol. 1999; 86(3):155-71.
Warnekulasuriya MR, Johnson JD, Holliman RE. Detection of Toxoplasma gondii in cured meats. Int J Food Microbiol. 1998; 45(3):211-5.
Aspinall TV, Marlee D, Hyde JE, Sims PF. Prevalence of Toxoplasma gondii in commercial meat products as monitored by polymerase chain reaction--food for thought? Int J Parasitol. 2002; 32(9):1193-9.
Sreekumar C, Rao JR, Mishra AK, Ray D, Joshi P, Singh RK. Detection of toxoplasmosis in experimentally infected goats by PCR. Vet Rec. 2004; 154(20):632-5.
Hill DE, Chirukandoth S, Dubey JP, Lunney JK, Gamble HR. Comparison of detection methods for Toxoplasma gondii in naturally and experimentally infected swine. Vet Parasitol. 2006; 141(1-2):9-17.
Belfort-Neto R, Nussenblatt V, Rizzo L, Muccioli C, Silveira C, Nussenblatt R, et al. High prevalence of unusual genotypes of Toxoplasma gondii infection in pork meat samples from Erechim, Southern Brazil. An Acad Bras Cienc. 2007; 79(1):111-4.
Berger-Schoch AE, Herrmann DC, Schares G, Muller 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.
Jiang HH, Huang SY, Zhou DH, Zhang XX, Su C, Deng SZ, et al. Genetic characterization of Toxoplasma gondii from pigs from different localities in China by PCR-RFLP. Parasit Vectors. 2013; 6:227.
Boughattas S, Ayari K, Sa T, Aoun K, Bouratbine A. Survey of the parasite Toxoplasma gondii in human consumed ovine meat in Tunis City. PLoS One. 2014; 9(1):e85044.
Hamidinejat H, Nabavi L, Mayahi M, Ghourbanpoor M, Pourmehdi Borojeni M, Norollahi Fard S, et al. Comparison of three diagnostic methods for the detection of Toxoplasma gondii in free range chickens. Trop Biomed. 2014; 31(3):507-13.
Van de Ven E, Melchers W, Galama J, Camps W, Meuwissen J. Identification of Toxoplasma gondii infections by BI gene amplification. J Clin Microbiol. 1991; 29(10):2120-4.
Gamble HR, Dubey JP, Lambillotte DN. Comparison of a commercial ELISA with the modified agglutination test for detection of Toxoplasma infection in the domestic pig. Vet Parasitol. 2005; 128(3-4):177-81.
Dubey JP. Comparative infectivity of oocysts and bradyzoites of Toxoplasma gondii for intermediate (mice) and definitive (cats) hosts. Vet Parasitol. 2006; 140(1-2):69-75.
Dubey JP. Oocyst shedding by cats fed isolated bradyzoites and comparison of infectivity of bradyzoites of the VEG strain Toxoplasma gondii to cats and mice. J Parasitol. 2001; 87(1):215-9.
Basso W, Hartnack S, Pardini L, Maksimov P, Koudela B, Venturini MC, et al. Assessment of diagnostic accuracy of a commercial ELISA for the detection of Toxoplasma gondii infection in pigs compared with IFAT, TgSAG1-ELISA and Western blot, using a Bayesian latent class approach. Int J Parasitol. 2013; 43(7):565-70.
Dubey JP, Thulliez P, Weigel RM, Andrews CD, Lind P, Powell EC. Sensitivity and specificity of various serologic tests for detection of Toxoplasma gondii infection in naturally infected sows. Am J Vet Res. 1995; 56(8):1030-6.
Sousa S, Canada N, Correia da Costa JM, Darde ML. Serotyping of naturally Toxoplasma gondii infected meat-producing animals. Vet Parasitol. 2010; 169(1-2):24-8.
Herrmann DC, Maksimov P, Hotop A, Gross U, Daubener W, Liesenfeld O, et al. Genotyping of samples from German patients with ocular, cerebral and systemic toxoplasmosis reveals a predominance of Toxoplasma gondii type II. Int J Med Microbiol. 2014; 304(7):911-6.
Mancianti F, Nardoni S, D'Ascenzi C, Pedonese F, Mugnaini L, Franco F, et al. Seroprevalence, detection of DNA in blood and milk, and genotyping of Toxoplasma gondii in a goat population in Italy. BioMed Res Int. 2013; 2013:905326.
Gibson AK, Raverty S, Lambourn DM, Huggins J, Magargal SL, Grigg ME. Polyparasitism is associated with increased disease severity in Toxoplasma gondii-infected marine sentinel species. PLoS Negl Trop Dis. 2011; 5(5):e1142.
Waltman WD, Dreesen DW, Prickett MD, Blue JL, Oliver DG. Enzyme-linked immunosorbent assay for the detection of toxoplasmosis in swine: interpreting assay results and comparing with other serologic tests. Am J Vet Res. 1984; 45(9):1719-25.
Wingstrand A, Lind P, Haugegaard J, Henriksen SA, Bille-Hansen V, Sorensen V. Clinical observations, pathology, bioassay in mice and serological response at slaughter in pigs experimentally infected with Toxoplasma gondii. Vet Parasitol. 1997; 72(2):129-40.
Lind P, Haugegaard J, Wingstrand A, Henriksen SA. The time course of the specific antibody response by various ELISAs in pigs experimentally infected with Toxoplasma gondii. Vet Parasitol. 1997; 71(1):1-15.