Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-18T05:40:17.026Z Has data issue: false hasContentIssue false

Toxoplasma gondii in mollusks and cold-blooded animals: a systematic review

Published online by Cambridge University Press:  11 March 2021

Tooran Nayeri
Affiliation:
Toxoplasmosis Research Center, Mazandaran University of Medical Sciences, Sari, Iran Department of Parasitology, School of Medicine, Mazandaran University of Medical Sciences, Sari, Iran Student Research Committee, Mazandaran University of Medical Sciences, Sari, Iran
Shahabeddin Sarvi
Affiliation:
Toxoplasmosis Research Center, Mazandaran University of Medical Sciences, Sari, Iran Department of Parasitology, School of Medicine, Mazandaran University of Medical Sciences, Sari, Iran
Ahmad Daryani*
Affiliation:
Toxoplasmosis Research Center, Mazandaran University of Medical Sciences, Sari, Iran Department of Parasitology, School of Medicine, Mazandaran University of Medical Sciences, Sari, Iran
*
Author for correspondence: Ahmad Daryani, E-mail: [email protected]

Abstract

Toxoplasma gondii (T. gondii) is known for its ability to infect warm-blooded vertebrates. Although T. gondii does not appear to parasitize cold-blooded animals, the occurrence of T. gondii infection in marine mammals raises concerns that cold-blooded animals (frogs, toad, turtles, crocodiles, snakes, and fish) and shellfish are potential sources of T. gondii. Therefore, this systematic review aimed to determine the prevalence of T. gondii in mollusks and cold-blooded animals worldwide. We searched PubMed, ScienceDirect, ProQuest, Scopus, and Web of Science from inception to 1 August 2020 for eligible papers in the English language and identified 26 articles that reported the prevalence of T. gondii in mollusks and cold-blooded animals. These articles were subsequently reviewed and data extracted using a standard form. In total, 26 studies [involving 9 cross-sectional studies including 2988 samples of cold-blooded animals (129 positive cases for T. gondii) and 18 cross-sectional studies entailing 13 447 samples of shellfish (692 positive cases for T. gondii)] were included in this study. Although this study showed that shellfish and cold-blooded animals could be potential sources of T. gondii for humans and other hosts that feed on them, further investigations are recommended to determine the prevalence of T. gondii in shellfish and cold-blooded animals.

Type
Review Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aakool, AA and Abidali, SJ (2016) Molecular detection of Toxoplasma gondii in native freshwater fish Cyprinuscarpio in Wasit Province Iraq. International Journal of Scientific Engineering and Research 4, 710.Google Scholar
Aguirre, AA, Longcore, T, Barbieri, M, Dabritz, H, Hill, D, Klein, PN, Lepczyk, C, Lilly, EL, McLeod, R and Milcarsky, J (2019) The one health approach to toxoplasmosis: epidemiology, control, and prevention strategies. EcoHealth 16, 378390.CrossRefGoogle ScholarPubMed
Aksoy, U, Marangi, M, Papini, R, Ozkoc, S, Delibas, SB and Giangaspero, A (2014) Detection of Toxoplasma gondii and Cyclospora cayetanensis in Mytilus galloprovincialis from Izmir Province coast (Turkey) by real time PCR/high-resolution melting analysis (HRM). Food Microbiology 44, 128135.CrossRefGoogle Scholar
Anah, SA and Al-Mayali, HMH (2018) Molecular detection of Toxoplasma gondii and Cryptosporidium spp. of some snakes in AL-Diwaniyah province/Iraq. EurAsian Journal of BioSciences 12, 1926.Google Scholar
Arkush, KD, Miller, MA, Leutenegger, CM, Gardner, IA, Packham, AE, Heckeroth, AR, Tenter, AM, Barr, BC and Conrad, PA (2003) Molecular and bioassay-based detection of Toxoplasma gondii oocyst uptake by mussels (Mytilus galloprovincialis). International Journal for Parasitology 33, 10871097.CrossRefGoogle Scholar
Aspinall, TV, Marlee, D, Hyde, JE and Sims, PF (2002) Prevalence of Toxoplasma gondii in commercial meat products as monitored by polymerase chain reaction – food for thought? International Journal for Parasitology 32, 11931199.CrossRefGoogle ScholarPubMed
Bossart, GD (2011) Marine mammals as sentinel species for oceans and human health. Veterinary Pathology 48, 676690.CrossRefGoogle ScholarPubMed
Bustin, SA (2002) Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. Journal of Molecular Endocrinology 29, 2339.CrossRefGoogle ScholarPubMed
Cole, RA, Lindsay, D, Howe, D, Roderick, CL, Dubey, J, Thomas, N and Baeten, L (2000) Biological and molecular characterizations of Toxoplasma gondii strains obtained from southern sea otters (Enhydra lutris nereis). Journal of Parasitology 86, 526530.CrossRefGoogle Scholar
Cong, W, Zhang, N-Z, Hou, J-L, Wang, X-C, Ma, J-G, Zhu, X-Q and Chen, G-J (2017) First detection and genetic characterization of Toxoplasma gondii in market-sold oysters in China. Infection, Genetics and Evolution 54, 276278.CrossRefGoogle ScholarPubMed
Cong, W, Zhang, N-Z, Yuan, D-Q, Zou, Y, Li, S and Liang, Z-L (2019) Detection and genetic characterization of Toxoplasma gondii in market-sold mussels (Mytilus edulis) in certain provinces of China. Microbial Pathogenesis 136, 103687.CrossRefGoogle ScholarPubMed
Conrad, PA, Miller, M, Kreuder, C, James, E, Mazet, J, Dabritz, H, Jessup, D, Gulland, F and Grigg, M (2005) Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. International Journal for Parasitology 35, 11551168.CrossRefGoogle Scholar
Costa, J-M and Bretagne, S (2012) Variation of B1 gene and AF146527 repeat element copy numbers according to Toxoplasma gondii strains assessed using real-time quantitative PCR. Journal of Clinical Microbiology 50, 14521454.CrossRefGoogle ScholarPubMed
Coupe, A, Howe, L, Burrows, E, Sine, A, Pita, A, Velathanthiri, N, Vallée, E, Hayman, D, Shapiro, K and Roe, WD (2018) First report of Toxoplasma gondii sporulated oocysts and Giardia duodenalis in commercial green-lipped mussels (Perna canaliculus) in New Zealand. Parasitology Research 117, 14531463.CrossRefGoogle ScholarPubMed
Dardé, M (2008) Toxoplasma gondii, ‘new’ genotypes and virulence. Parasite, 15, 366371.CrossRefGoogle Scholar
Dardé, M, Ajzenberg, D and Smith, J (2007) Population structure and epidemiology of Toxoplasma gondii. In Weiss LM and Kim K (eds), Toxoplasma gondii the model apicomplexan: perspectives and methods. London, UK: Academic Press, 4980.CrossRefGoogle Scholar
de Souza Sampaio, D, Tagliaro, CH, Schneider, H and Beasley, CR (2019) Oyster culture on the Amazon mangrove coast: asymmetries and advances in an emerging sector. Reviews in Aquaculture 11, 88104.CrossRefGoogle Scholar
Di Guardo, G and Mazzariol, S (2013) Toxoplasma gondii: Clues From Stranded Dolphins. Los Angeles, CA: SAGE Publications Sage CA.Google ScholarPubMed
Dubey, JP and Beattie, C (1988) Toxoplasmosis of animals and man. Boca Raton, FL: CRC Press, Inc..Google Scholar
Dubey, JP, Lindsay, DS and Speer, CA (1998) Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clinical Microbiology Reviews 11, 267299.CrossRefGoogle ScholarPubMed
Dubey, JP, Sundar, N, Hill, D, Velmurugan, GV, Bandini, LA, Kwok, OC, Majumdar, D and Su, C (2008) High prevalence and abundant atypical genotypes of Toxoplasma gondii isolated from lambs destined for human consumption in the USA. International Journal for Parasitology 38, 9991006.CrossRefGoogle ScholarPubMed
Dumètre, A and Dardé, M-L (2003) How to detect Toxoplasma gondii oocysts in environmental samples? FEMS Microbiology Reviews 27, 651661.CrossRefGoogle ScholarPubMed
Eischeid, AC (2011) SYTO dyes and EvaGreen outperform SYBR Green in real-time PCR. BMC Research Notes 4, 263.CrossRefGoogle ScholarPubMed
Esmerini, PO, Gennari, SM and Pena, HF (2010) Analysis of marine bivalve shellfish from the fish market in Santos city, Sao Paulo state, Brazil, for Toxoplasma gondii. Veterinary Parasitology 170, 813.CrossRefGoogle Scholar
Fayer, R, Dubey, JP and Lindsay, DS (2004) Zoonotic protozoa: from land to sea. Trends in Parasitology 20, 531536.CrossRefGoogle ScholarPubMed
Feitosa, TF, Brasil, AWDL, Parentoni, RN, Vilela, VLR, Nety, TFL and Pena, HFDJ (2017) Anti-Toxoplasma gondii antibodies in mammals, birds and reptiles at the zoological-botanical park in João Pessoa, Paraíba, Brazil. Arquivos do Instituto Biológico 84, 1–5.Google Scholar
Ferreira, FB, de Macêdo-Júnior, AG, Lopes, CS, Silva, MV, Ramos, ELP, Júnior, ÁF, Vitaliano, SN, Santiago, FM, Santos, ALQ and Mineo, JR (2020) Serological evidence of Toxoplasma gondii infection in Melanosuchus niger (Spix, 1825) and Caimam crocodilus (Linnaeus, 1758). International Journal for Parasitology: Parasites and Wildlife 12, 42–45.Google Scholar
Forbes, LB, Measures, L and Gajadhar, A (2009) Infectivity of Toxoplasma gondii in northern traditional (country) foods prepared with meat from experimentally infected seals. Journal of Food Protection 72, 17561760.CrossRefGoogle ScholarPubMed
Havelaar, AH, Haagsma, JA, Mangen, M-JJ, Kemmeren, JM, Verhoef, LP, Vijgen, SM, Wilson, M, Friesema, IH, Kortbeek, LM and van Duynhoven, YT (2012) Disease burden of foodborne pathogens in the Netherlands, 2009. International Journal of Food Microbiology 156, 231238.CrossRefGoogle ScholarPubMed
Hoffman, LC and Cawthorn, D-M (2012) What is the role and contribution of meat from wildlife in providing high quality protein for consumption? Animal Frontiers 2, 4053.CrossRefGoogle Scholar
Homan, WL, Limper, L, Verlaan, M, Borst, A, Vercammen, M and van Knapen, F (1997) Comparison of the internal transcribed spacer, ITS 1, from Toxoplasma gondii isolates and Neospora caninum. Parasitology Research 83, 285289.CrossRefGoogle ScholarPubMed
Homan, W, Vercammen, M, De Braekeleer, J and 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. International Journal for Parasitology 30, 6975.CrossRefGoogle ScholarPubMed
Hurtado, A, Aduriz, G, Moreno, B, Barandika, J and García-Pérez, AL (2001) Single tube nested PCR for the detection of Toxoplasma gondii in fetal tissues from naturally aborted ewes. Veterinary Parasitology 102, 1727.CrossRefGoogle ScholarPubMed
Jauregui, L, Higgins, J, Zarlenga, D, Dubey, J and Lunney, J (2001) Development of a real-time PCR assay for detection of Toxoplasma gondii in pig and mouse tissues. Journal of Clinical Microbiology 39, 20652071.CrossRefGoogle ScholarPubMed
Jones, JL, Kruszon-Moran, D, Wilson, M, McQuillan, G, Navin, T and McAuley, JB (2001) Toxoplasma gondii infection in the United States: seroprevalence and risk factors. American Journal of Epidemiology 154, 357365.CrossRefGoogle ScholarPubMed
Kim, JH, Kang, KI, Kang, WC, Sohn, HJ, Jean, YH, Park, BK, Kim, Y and Kim, DY (2009) Porcine abortion outbreak associated with Toxoplasma gondii in Jeju Island, Korea. Journal of Veterinary Science 10, 147151.CrossRefGoogle ScholarPubMed
Koutsoumanis, K, Allende, A, Alvarez-Ordóñez, A, Bolton, D, Bover-Cid, S, Chemaly, M, Davies, R, De Cesare, A, Herman, L, Hilbert, F, Lindqvist, R, Nauta, M, Peixe, L, Ru, G, Simmons, M, Skandamis, P, Suffredini, E, Cacciò, S, Chalmers, R, Deplazes, P, Devleesschauwer, B, Innes, E, Romig, T, van der Giessen, J, Hempen, M, Van der Stede, Y and Robertson, L (2018) Public health risks associated with food-borne parasites. EFSA Journal 16, e05495.Google ScholarPubMed
Leal, DAG and Franco, R (2008) Moluscos bivalves destinados ao consumo humano como vetores de protozoários patogênicos: metodologias de detecção e normas de controle. Continente 1, 2.Google Scholar
Lehmann, T, Marcet, PL, Graham, DH, Dahl, ER and Dubey, J (2006) Globalization and the population structure of Toxoplasma gondii. Proceedings of the National Academy of Sciences 103, 1142311428.CrossRefGoogle ScholarPubMed
Levine, ND and Nye, RR (1976) Toxoplasma ranae sp. n. from the leopard frog Rana pipiens Linnaeus. The Journal of Protozoology 23, 488490.CrossRefGoogle Scholar
Li, YD, Chu, ZZ, Liu, XG, Jing, HC, Liu, YG and Hao, DY (2010) A cost-effective high-resolution melting approach using the EvaGreen dye for DNA polymorphism detection and genotyping in plants. Journal of Integrative Plant Biology 52, 10361042.CrossRefGoogle ScholarPubMed
Lindsay, DS, Collins, MV, Mitchell, SM, Wetch, CN, Rosypal, AC, Flick, GJ, Zajac, AM, Lindquist, A and Dubey, J (2004) Survival of Toxoplasma gondii oocysts in Eastern oysters (Crassostrea virginica). Journal of Parasitology 90, 10541057.CrossRefGoogle Scholar
Magnino, S, Colin, P, Dei-Cas, E, Madsen, M, McLauchlin, J, Nöckler, K, Maradona, MP, Tsigarida, E, Vanopdenbosch, E and Van Peteghem, C (2009) Biological risks associated with consumption of reptile products. International Journal of Food Microbiology 134, 163175.CrossRefGoogle ScholarPubMed
Mao, F, Leung, WY and Xin, X (2007) Characterization of EvaGreen and the implication of its physicochemical properties for qPCR applications. BMC Biotechnology 7, 76.CrossRefGoogle ScholarPubMed
Marangi, M, Giangaspero, A, Lacasella, V, Lonigro, A and Gasser, RB (2015) Multiplex PCR for the detection and quantification of zoonotic taxa of Giardia, Cryptosporidium and Toxoplasma in wastewater and mussels. Molecular and Cellular Probes 29, 122125.CrossRefGoogle ScholarPubMed
Marino, AMF, Giunta, RP, Salvaggio, A, Castello, A, Alfonzetti, T, Barbagallo, A, Aparo, A, Scalzo, F, Reale, S and Buffolano, W (2019) Toxoplasma gondii in edible fishes captured in the Mediterranean basin. Zoonoses and Public Health 66, 826834.CrossRefGoogle Scholar
Marquis, ND, Record, NR and Robledo, JA (2015) Survey for protozoan parasites in Eastern oysters (Crassostrea virginica) from the Gulf of Maine using PCR-based assays. Parasitology International 64, 299302.CrossRefGoogle ScholarPubMed
Marquis, ND, Bishop, TJ, Record, NR, Countway, PD and Fernández Robledo, JA (2019) Molecular epizootiology of Toxoplasma gondii and Cryptosporidium parvum in the Eastern Oyster (Crassostrea virginica) from Maine (USA). Pathogens 8, 125.CrossRefGoogle Scholar
Massie, GN, Ware, MW, Villegas, EN and Black, MW (2010) Uptake and transmission of Toxoplasma gondii oocysts by migratory, filter-feeding fish. Veterinary Parasitology 169, 296303.CrossRefGoogle ScholarPubMed
Miller, M, Miller, W, Conrad, PA, James, E, Melli, A, Leutenegger, C, Dabritz, H, Packham, A, Paradies, D and Harris, M (2008) Type X Toxoplasma gondii in a wild mussel and terrestrial carnivores from coastal California: new linkages between terrestrial mammals, runoff and toxoplasmosis of sea otters. International Journal for Parasitology 38, 13191328.CrossRefGoogle Scholar
Moher, D, Shamseer, L, Clarke, M, Ghersi, D, Liberati, A, Petticrew, M, Shekelle, P and Stewart, LA (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Systematic Reviews 4, 1.CrossRefGoogle ScholarPubMed
Monteiro, TR, Rocha, KS, Silva, J, Mesquita, GS, Rosário, MK, Ferreira, MF, Honorio, BE, Melo, HF, Barros, FN and Scofield, A (2019) Detection of Toxoplasma gondii in Crassostrea spp. oysters cultured in an estuarine region in eastern Amazon. Zoonoses and Public Health 66, 296300.CrossRefGoogle Scholar
Nasiri, V, Teymurzadeh, S, Karimi, G and Nasiri, M (2016) Molecular detection of Toxoplasma gondii in snakes. Experimental Parasitology 169, 102106.CrossRefGoogle ScholarPubMed
Omata, Y, Umeshita, Y, Murao, T, Kano, R, Kamiya, H, Kudo, A, Masukata, Y, Kobayashi, Y, Maeda, R and Saito, A (2005) Toxoplasma gondii does not persist in goldfish (Carassius auratus). Journal of Parasitology 91, 14961499.CrossRefGoogle Scholar
Opsteegh, M, Langelaar, M, Sprong, H, den Hartog, L, De Craeye, S, Bokken, G, Ajzenberg, D, Kijlstra, A and van der Giessen, J (2010) Direct detection and genotyping of Toxoplasma gondii in meat samples using magnetic capture and PCR. International Journal of Food Microbiology 139, 193201.CrossRefGoogle ScholarPubMed
Putignani, L, Mancinelli, L, Del Chierico, F, Menichella, D, Adlerstein, D, Angelici, M, Marangi, M, Berrilli, F, Caffara, M and di Regalbono, DF (2011) Investigation of Toxoplasma gondii presence in farmed shellfish by nested-PCR and real-time PCR fluorescent amplicon generation assay (FLAG). Experimental Parasitology 127, 409417.CrossRefGoogle Scholar
Reiling, SJ, Measures, L, Feng, S, Boone, R, Merks, H and Dixon, BR (2019) Toxoplasma gondii, Sarcocystis sp. and Neospora caninum-like parasites in seals from northern and eastern Canada: potential risk to consumers. Food and Waterborne Parasitology 17, e00067.CrossRefGoogle Scholar
Ribeiro, L, Santos, L, Brito, P Jr, Maciel, B, Da Silva, A and Albuquerque, G (2015) Detection of Toxoplasma gondii DNA in Brazilian oysters (Crassostrea rhizophorae). Genetics and Molecular Research: GMR 14, 46584665.CrossRefGoogle Scholar
Robertson, L (2007) The potential for marine bivalve shellfish to act as transmission vehicles for outbreaks of protozoan infections in humans: a review. International Journal of Food Microbiology 120, 201216.CrossRefGoogle ScholarPubMed
Santoro, M, Viscardi, M, Boccia, F, Borriello, G, Lucibelli, MG, Auriemma, C, Anastasio, A, Veneziano, V, Galiero, G and Baldi, L (2020) Parasite load and STRs genotyping of Toxoplasma gondii isolates from Mediterranean mussels (Mytilus galloprovincialis) in Southern Italy. Frontiers in Microbiology 11, 355.CrossRefGoogle Scholar
Shapiro, K, Krusor, C, Mazzillo, FF, Conrad, PA, Largier, JL, Mazet, JA and Silver, MW (2014) Aquatic polymers can drive pathogen transmission in coastal ecosystems. Proceedings of the Royal Society B: Biological Sciences 281, 20141287.CrossRefGoogle ScholarPubMed
Shapiro, K, VanWormer, E, Aguilar, B and Conrad, PA (2015) Surveillance for Toxoplasma gondii in California mussels (Mytilus californianus) reveals transmission of atypical genotypes from land to sea. Environmental Microbiology 17, 41774188.CrossRefGoogle ScholarPubMed
Silva, CM, Silva, ALP, Watanabe, KFC, Chaves Bezerra, NP, Bezerra, DC, Gomes, HM, Freire, TB, Santos, LSD, Carvalho Neta, AVD and Silva, EMC (2020) First report of detection of Toxoplasma gondii DNA in oysters (Crassostrea sp.) in the state of Maranhão. Revista Brasileira de Parasitologia Veterinária 29, e003720.CrossRefGoogle ScholarPubMed
Staggs, SE, Keely, SP, Ware, MW, Schable, N, See, MJ, Gregorio, D, Zou, X, Su, C, Dubey, J and Villegas, EN (2015) The development and implementation of a method using blue mussels (Mytilus spp.) as biosentinels of Cryptosporidium spp. and Toxoplasma gondii contamination in marine aquatic environments. Parasitology Research 114, 46554667.CrossRefGoogle ScholarPubMed
Stang, A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. European Journal of Epidemiology 25, 603605.CrossRefGoogle ScholarPubMed
Su, C, Shwab, E, Zhou, P, Zhu, X and Dubey, J (2010) Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii. Parasitology 137, 111.CrossRefGoogle ScholarPubMed
Sundar, N, Cole, RA, Thomas, N, Majumdar, D, Dubey, J and Su, C (2008) Genetic diversity among sea otter isolates of Toxoplasma gondii. Veterinary Parasitology 151, 125132.CrossRefGoogle ScholarPubMed
Taghadosi, C, Kojouri, GA and Taheri, MA (2010) Detection of Toxoplasma antibodies in sera of Salmonidae by ELISA. Comparative Clinical Pathology 19, 203206.CrossRefGoogle Scholar
Tedde, T, Marangi, M, Papini, R, Salza, S, Normanno, G, Virgilio, S and Giangaspero, A (2019) Toxoplasma gondii and other zoonotic protozoans in Mediterranean mussel (Mytilus galloprovincialis) and blue mussel (Mytilus edulis): a food safety concern? Journal of Food Protection 82, 535542.CrossRefGoogle ScholarPubMed
Tenter, AM, Heckeroth, AR and Weiss, LM (2000) Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 12171258.CrossRefGoogle ScholarPubMed
Tryland, M, Nesbakken, T, Robertson, L, Grahek-Ogden, D and Lunestad, B (2014) Human pathogens in marine mammal meat–a northern perspective. Zoonoses and Public Health 61, 377394.CrossRefGoogle ScholarPubMed
Walker, J, Nokes, D and Jennings, R (1992) Longitudinal study of Toxoplasma seroprevalence in South Yorkshire. Epidemiology & Infection 108, 99106.CrossRefGoogle ScholarPubMed
Wotton, RS (2004) The essential role of exopolymers (EPS) in aquatic systems. Oceanography and Marine Biology: An Annual Review 42, 5794.Google Scholar
Zhang, M, Yang, Z, Wang, S, Tao, L, Xu, L, Yan, R, Song, X and Li, X (2014) Detection of Toxoplasma gondii in shellfish and fish in parts of China. Veterinary Parasitology 200, 8589.CrossRefGoogle ScholarPubMed
Supplementary material: File

Nayeri et al. supplementary material

Table S1

Download Nayeri et al. supplementary material(File)
File 15.6 KB