Review Article

Milk as a Non-Invasive and Alternative Sample for Serum in the Diagnosis of Animal Toxoplasmosis: A Systematic Review

Abstract

Background: Toxoplasmosis is one of the most important zoonotic parasitic diseases worldwide with a high impact on human and animal health. Body fluids such as milk are used to diagnose many parasitic diseases, including toxoplasmosis. Therefore, this study aimed to investigate the role of milk as a non-invasive and alternative sample for serum in the diagnosis of animal toxoplasmosis.

Methods: Five English-language databases (ScienceDirect, PubMed, ProQuest, Scopus, and Web of Science) were explored for published articles before Dec 2020.

Results: In total, 42 out of 2256 published articles were included in this systematic review. In 21 articles, serum and milk samples were evaluated simultaneously with serological or molecular tests, and the results were compared. The results of descriptive studies and a review of nine experimental studies showed that milk could be used as a non-invasive and alternative sample for the serum in the diagnosis of toxoplasmosis.

Conclusion: Due to the relatively high prevalence of Toxoplasma gondii (T. gondii) infection in milk, consumption of raw milk from infected animals can be a potential source of human infection and a significant threat to public health. On the other hand, due to the ease and cheapness of collecting milk samples, the use of milk is recommended for the diagnosis of toxoplasmosis.

1. Stelzer S, Basso W, Silván JB, et al (2019). Toxoplasma gondii infection and toxoplasmosis in farm animals: risk factors and economic impact. Food Waterborne Parasitol, 15:e00037.
2. Ouchetati I, Ouchene N, Khelifi-Ouchene NA, et al (2020). Prevalence of Toxoplasma gondii infection among animals in Algeria: a systematic review and meta-analysis. Comp Immunol Microbiol Infect Dis, 101603.
3. Rouatbi M, Amairia S, Amdouni Y, et al (2019). Toxoplasma gondii infection and toxoplasmosis in North Africa: a review. Parasite, 26: 6.
4. Pleyer U, Gross U, Schlüter D, et al (2019). Toxoplasmosis in Germany: epidemiology, diagnosis, risk factors, and treatment. Dtsch Ärztebl Int,116:435.
5. De Barros LD, Garcia JL, Bresciani KDS, et al (2020). A review of toxoplasmosis and neosporosis in water Buffalo (Bubalus bubalis). Front vet sci, 7:455.
6. Abdullah R, Amarasekera S (2018). Detection of Toxoplasma gondii in cow fresh milk using pcr technique. J Manag Sci,16.
7. Hill D, Dubey J (2002). Toxoplasma gondii: transmission, diagnosis and prevention. Clin Microbiol Infect, 8:634-40.
8. Wang Y-L, Meng Q (2020). Short reports low prevalence of Toxoplasma gondii DNA in the fresh milk of cattle in China. Research Square, 1-10.
9. Ahmedani EI, Elagib AA, Mohamed K, et al (2020). Detection of Toxoplasma gondii by loop-mediated isothermal amplification in blood and urine samples from women, Saudi Arabia. J Clin Diagn Res, 14:DC15-DC18 .
10. Lynch MI, Cordeiro F, Ferreira S, et al (2004). Lacrimal secretory IgA in active posterior uveitis induced by Toxoplasma gondii. Mem Inst Oswaldo Cruz, 99:861-4.
11. Moher D, Liberati A, Tetzlaff J, et al (2010). Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg, 8:336-41.
12. Veronesi F, Chiesa F, Zanet S, et al (2018). Screening of Toxoplasma gondii positive sheep flocks in Perugia province (Umbria Region, central Italy) using bulk milk analyses. Large Anim Rev, 24:185-187.
13. Abdel-Rahman M, EL-Manyawe SM, Khateib A, et al (2012). Occurrence of Toxoplasma antibodies in caprine milk and serum in Egypt. Assiut Vet Med J, 58:145-52.
14. Dehkordi FS, Haghighi Borujeni MR, Rahimi E, et al (2013). Detection of Toxoplasma gondii in raw caprine, ovine, buffalo, bovine, and camel milk using cell cultivation, cat bioassay, capture ELISA, and PCR methods in Iran. Foodborne Pathog Dis, 10:120-5.
15. Skinner LJ, Timperley AC, Wightman D, et al (1990).Simultaneous diagnosis of toxoplasmosis in goats and goatowner's family. Scand J Infect Dis, 22:359-61.
16. Fusco G, Rinaldi L, Guarino A, et al (2007). Toxoplasma gondii in sheep from the Campania region (Italy). Vet Parasitol, 149:271-4.
17. Mancianti F, Nardoni S, Papini R, et al (2014). Detection and genotyping of Toxoplasma gondii DNA in the blood and milk of naturally infected donkeys (Equus asinus). Parasites Vectors, 7:1-3.
18. Mancianti F, Nardoni S, D'Ascenzi C, et al (2013). Seroprevalence, detection of DNA in blood and milk, and genotyping of Toxoplasma gondii in a goat population in Italy. BioMed Res Int, 2013:6.
19. Martini M, Altomonte I, Mancianti F, et al (2014). A preliminary study on the quality and safety of milk in donkeys positive for Toxoplasma gondii. Animal, 8:1996-8.
20. Vismarra A, Barilli E, Miceli M, et al (2017). Toxoplasma gondii and pre-treatment protocols for polymerase chain reaction analysis of milk samples: a field trial in sheep from Southern Italy. Ital J Food Saf, 6:6501.
21. Gazzonis AL, Zanzani SA, Villa L, et al (2019). Toxoplasma gondii in naturally infected goats: Monitoring of specific IgG levels in serum and milk during lactation and parasitic DNA detection in milk. Prev Vet Med, 170:104738.
22. Gazzonis A, Zanzani S, Stradiotto K, et al (2018). Toxoplasma gondii antibodies in bulk tank milk samples of caprine dairy herds. J Parasitol, 104:560-5.
23. Ranucci D, Battisti E, Veronesi F, et al (2020). Absence of viable Toxoplasma gondii in artisanal raw-milk ewe cheese derived from naturally infected animals. Microorganisms, 8:143.
24. Spišák F, Turčeková Ľ, Reiterová K, et al (2010). Prevalence estimation and genotypization of Toxoplasma gondii in goats. Biologia, 65:670-4.
25. Luptakova L, Benova K, Rencko A, et al (2015). DNA detection of Toxoplasma gondii in sheep milk and blood samples in relation to phase of infection. Vet Parasitol, 208:250-3.
26. Amairia S, Rouatbi M, Rjeibi MR, et al (2016). Molecular prevalence of Toxoplasma gondii DNA in goats’ milk and seroprevalence in northwest Tunisia. Vet Med Sci, 2:154-60.
27. Cisak E, Zając V, Sroka J, et al (2017). Presence of pathogenic Rickettsiae and protozoan in samples of raw milk from cows, goats, and sheep. Foodborne Pathog Dis, 14:189-94.
28. Sroka J, Kusyk P, Bilska-Zając E, et al (2017). Seroprevalence of Toxoplasma gondii infection in goats from the south-west region of Poland and the detection of T. gondii DNA in goat milk. Folia Parasitol, 64:1-5.
29. Iacobucci E, Taus N, Ueti M, et al (2019). Detection and genotypic characterization of Toxoplasma gondii DNA within the milk of Mongolian livestock. Parasitol Res, 118:2005-8.
30. Alipour Amroabadi M, Rahimi E, Shakerian A (2020). Seasonal and age distribution of Toxoplasma gondii in milk of naturally infected animal species and dairy samples. EJVS, 51:171-80.
31. Alipour M, Rahimi E, Shakerian A (2018). Retracted: prevalence of Toxoplasma gondii and Neospora caninum in different types of raw milk and traditional dairy product samples. J Food Saf, 38:e12575.
32. Razmi G, Barati M (2017). Prevalence of Neospora caninum and Toxoplasma gondii antibodies in bulk milk of dairy cattle, Mashhad, Iran. Arch Razi Inst, 72:265-9.
33. Tavassoli M, Esmaeilnejad B, Malekifard F, et al (2013). Detection of Toxoplasma gondii DNA in sheep and goat milk in northwest of Iran by PCR-RFLP. Jundishapur J Microbiol, 6:e8201.
34. Camossi L, Greca-Júnior H, Corrêa A, et al (2011). Detection of Toxoplasma gondii DNA in the milk of naturally infected ewes. Vet Parasitol, 177:256-61.
35. Bezerra M, Kim P, Moraes ÉP, et al (2015). Detection of Toxoplasma gondii in the milk of naturally infected goats in the northeast of Brazil. Transbound Emerg Dis, 62:421-4.
36. Da Silva AS, Tonin AA, Camillo G, et al (2014). Ovine toxoplasmosis: indirect immunofluorescence for milk samples as a diagnostic tool. Small Rumin Res, 120:181-4.
37. da Silva JG, Alves BHL, Melo RPB, et al (2015). Occurrence of anti-Toxoplasma gondii antibodies and parasite DNA in raw milk of sheep and goats of local breeds reared in northeastern Brazil. Acta Trop, 142:145-8.
38. de Santana Rocha D, de Sousa Moura R, Maciel B, et al (2015). Detection of Toxoplasma gondii DNA in naturally infected sheep’s milk. Genet Mol Biol, 14:8658-62.
39. Ossani R, Borges H, Souza A, Sartor A, et al (2017). Toxoplasma gondii in milk of naturally infected dairy ewes on west mesoregion of Santa Catarina state, Brazil. Arq Bras Med Vet Zootec, 69:1294-300.
40. Ahmed HA, Shafik SM, Ali ME, et al (2014). Molecular detection of Toxoplasma gondii DNA in milk and risk factors analysis of seroprevalence in pregnant women at Sharkia, Egypt. Vet World, 7:594-600.
41. Attia MM, Saad M, Abdel-Salam AB (2017). Milk as a substitute for serum in diagnosis of toxoplasmosis in goats. J Egypt Soc Parasitol, 47:227-34.
42. Sadek O, Abdel-Hameed ZM, Kuraa HM (2015). Molecular detection of Toxoplasma gondii DNA in raw goat and sheep milk with discussion of its public health importance in Assiut Governorate. Assiut Vet Med J, 61:166-77.
43. Saad NM, Hussein AA, Ewida RM (2018). Occurrence of Toxoplasma gondii in raw goat, sheep, and camel milk in Upper Egypt. Vet World, 11:1262.
44. Mohamed HM, Hussein AA, Lila M, et al (2019). Serological survey on Toxoplasma gondii in some dairy animals and pregnant women in Qena, Egypt. J Adv Vet Res, 9:97-101.
45. Alkanaq MN SZ, Salih H, Alrammah NSAA, et al (2020). Detection of Toxoplasma gondii in blood and milk of infected goats and pregnant women by rapid test cassette and conventional-PCR methods in AL-Qadisiyah province, Iraq. Int J Pharm Sci Res, 12:2170-2176.
46. Chardes T, Bourguin I, Mevelec M, et al (1990). Antibody responses to Toxoplasma gondii in sera, intestinal secretions, and milk from orally infected mice and characterization of target antigens. Infect Immun, 58:1240-6.
47. Powell CC, Brewer M, Lappin MR (2001). Detection of Toxoplasma gondii in the milk of experimentally infected lactating cats. Vet Parasitol, 102:29-33.
48. Dubey J, Verma S, Ferreira L, et al (2014). Detection and survival of Toxoplasma gondii in milk and cheese from experimentally infected goats. J Food Prot, 77:1747-53.
49. Hiramoto R, Mayrbaurl-Borges M, Galisteo Jr A, et al (2001). Infectivity of cysts of the ME-49 Toxoplasma gondii strain in bovine milk and homemade cheese. Rev Saude Publica, 35:113-8.
50. Costa V, Langoni H (2010). Detection of Toxoplasma gondii in the milk of experimentally infected wistar female rats. J Venom Anim Toxins Incl Trop Dis, 16:368-74.
51. Ishag MY, Magzoub E, Majid M (2006). Detection of Toxoplasma gondii tachyzoites in the milk of experimentally infected lactating She-Camels. J Anim Vet Adv, 5:456-458.
52. Lafi SQ, Giadinis ND, Papadopoulos E, et al (2014). Ovine and caprine toxoplasmosis: experimental study. Pak Vet J, 34:50-3.
53. Masala G, Porcu R, Madau L, et al (2003). Survey of ovine and caprine toxoplasmosis by IFAT and PCR assays in Sardinia, Italy. Vet Parasitol, 117:15-21.
54. Tenter AM, Heckeroth AR, Weiss LM (2000). Toxoplasma gondii: from animals to humans. Int J Parasitol, 30:1217-58.
55. Suzuki Y (2002). Host resistance in the brain against Toxoplasma gondii. J Infect Dis, 185:S58-S65.
56. Buxton D (1990). Ovine toxoplasmosis: a review. J R Soc Med, 83:509-11.
57. Dubey J (1980). Persistence of encysted Toxoplasma gondii in caprine livers and public health significance of toxoplasmosis in goats. J Am Vet Med Assoc, 177:1203-1207.
58. Walsh C, Hammond S, Zajac A, et al (1999). Survival of Toxoplasma gondii tachyzoites in goat milk: potential source of human toxoplasmosis. J Eukaryot Microbiol, 46:73S-74S.
59. Tenter AM (2009). Toxoplasma gondii in animals used for human consumption. Mem Inst Oswaldo Cruz, 104:364-9.
60. Dubey J (1998). Re-examination of resistance of Toxoplasma gondii tachyzoites and bradyzoites to pepsin and trypsin digestion. Parasitology, 116:43-50.
61. Riemann H, Meyer M, Theis J, et al (1975). Toxoplasmosis in an infant fed unpasteurized goat milk. J Pediatr, 87:573-6.
62. Sacks JJ, Roberto RR, Brooks NF (1982). Toxoplasmosis infection associated with raw goat's milk. JAMA, 248:1728-32.
63. Pettersen EK (1984). Transmission of toxoplasmosis via milk from lactating mice. Acta Pathol Microbiol Scand, 92:175-6.
64. Deyrup-Olsen I, Luchtel D (1998). Secretion of mucous granules and other membrane-bound structures: a look beyond exocytosis. Int Rev Cytol Suppl, 183:95-141.
65. Dubey J (1991). Toxoplasmosis: an overview. Southeast Asian J Trop Med Public Health, 22:88-92.
66. Sudan V, Jaiswal AK, Shanker D (2013). Recent trends in the diagnosis of toxoplasmosis. Clin Rev Opinions, 5:11-7.
67. Switaj K, Master A, Skrzypczak M, et al (2005). Recent trends in molecular diagnostics for Toxoplasma gondii infections. Clin Microbiol Infect, 11:170-6.
68. Martins TB, Hillyard DR, Litwin CM, et al (2000). Evaluation of a PCR probe capture assay for the detection of Toxoplasma gondii: Incorporation of uracil N-glycosylase for contamination control. Am J Clin Pathol, 113:714-21.
69. Held T, Krüger D, Switala A, et al (2000). Diagnosis of toxoplasmosis in bone marrow transplant recipients: comparison of PCR-based results and immunohistochemistry. Bone Marrow Transplant, 25:1257-62.
70. Homana WL, Vercammen M, Braekeleer J, et al (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, 30:69-75.
71. Boughattas S (2015). Commentary on:“Detection of Toxoplasma gondii in raw caprine, ovine, buffalo, bovine, and camel milk using cell cultivation, cat bioassay, capture ELISA, and PCR methods in Iran”. Front Microbiol, 6:215.
72. Schares G, Bärwald A, Staubach C, et al (2004). Adaptation of a commercial ELISA for the detection of antibodies against Neospora caninum in bovine milk. Vet Parasitol, 120:55-63.
73. Grundy MS, Cartwright-Taylor L, Lundin L, et al (1983). Antibodies against Entamoeba histolytica in human milk and serum in Kenya. J Clin Microbiol, 17:753-8.
74. Malamud D (2011). Saliva as a diagnostic fluid. Dent Clin, 55:159-78.
Files
IssueVol 51 No 9 (2022) QRcode
SectionReview Article(s)
DOI https://doi.org/10.18502/ijph.v51i9.10551
Keywords
Toxoplasma gondii Non-invasive samples Milk Serological Molecular

Rights and permissions
Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
How to Cite
1.
Nayeri T, Sarvi S, Abedian R, Gohardehi S, Hosseini SA, Daryani A. Milk as a Non-Invasive and Alternative Sample for Serum in the Diagnosis of Animal Toxoplasmosis: A Systematic Review. Iran J Public Health. 2022;51(9):1964-1976.