Toxoplasma gondii in Milk of Human and Goat from the Desert Area in Central Iran
-
Esmat Mohammadi Khamsian
,
Bahador Hajimohammadi
,
Gilda Eslami
,
Mohammad Hossein Fallahzadeh
,
Saeede Sadat Hosseini
Abstract
Background: Toxoplasma gondii, an obligate intracellular protozoan, causes toxoplasmosis. The aim of this study was molecular detection of T. gondii in breast and goat milk samples by the molecular method in the central Iran.
Methods: Totally, 300 human' and 200 goats' milk samples were collected randomly from different regions of central Iran in 2018. DNA extraction was performed by the salting-out method. Molecular detection of the parasite was done by nested-PCR using the specific primer pairs. Statistical analysis was performed by SPSS 23 using descriptive and Chi-square tests.
Results: Out of 300 human milk samples, 1 sample (0.3%) was infected with T. gondii. Out of 200 samples of goat milk, 11 samples (5.5%) showed infection with T. gondii. The frequency of infection in goat's milk samples was 4.36% in the south and west, 1.9% in northern regions, and 2% in eastern regions of the province. The statistical analysis showed no significant difference between toxoplasmosis and different geographical regions in the province.
Conclusion: Because of the popularity of the goat milk and the transfection probability with the milk to humans, it is recommended to boil milk prior to use. Furthermore, case contamination of T. gondii in the human milk sample showed one of the important paths for infection transmission, which requires further studies.
1. Dehkordi FS, Borujeni MR, Rahimi E, et al. 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. 2013; 10 (2): 120-5.
2. Reischl U, Bretagne S, Krüger D, et al. Comparison of two DNA targets for the diagnosis of toxoplasmosis by real-time PCR using fluorescence resonance energy transfer hybridization probes. BMC Infect Dis. 2003; 3: 7.
3. Eshratkhah Mohammadnejad A, Eslami G, Shamsi F,et al. Prevalence of Food-Borne Toxoplasma in Pregnant Women Population of Urmia, Iran. J Food Qual Hazards Control. 2018; 5 (1): 17-23.
4. Tavassoli M, Esmaeilnejad B, Malekifard F, et al. Detection of Toxoplasma gondii DNA in Sheep and Goat Milk in Northwest of Iran by PCR-RFLP. J Food Qual Hazards Control. 2013; 6 (10): e8201.
5. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol. 2000; 30 (12-13): 1217-1258.
6. Amairia S, Rouatbi M, Rjeibi MR, et al. Molecular prevalence of Toxoplasma gondii DNA in goats’ milk and seroprevalence in Northwest Tunisia. Vet Med Sci. 2016; 2 (3): 154-160.
7. De Oliveira L, Junior LC, De Melo C, et al. Toxoplasma gondii isolates from free-range chickens from the northeast region of Brazil. J Parasitol. 2009; 95 (1): 235-7.
8. Ragozo AMA, Yai LEO, Oliveira L, et al. Isolation of Toxoplasma gondii from goats from Brazil. J Parasitol. 2009; 95 (2): 323-6.
9. Fajardo HV, D’ávila S, Bastos RR, et al. Seroprevalence and risk factors of toxoplasmosis in cattle from extensive and semi-intensive rearing systems at Zona da Mata, Minas Gerais state, Southern Brazil. Parasit Vectors. 2013; 6: 191.
10. Bezerra R, Carvalho F, Guimarães L, et al. Genetic characterization of Toxoplasma gondii isolates from pigs intended for human consumption in Brazil. Veterinary Parasitology. 2012; 189 (2-4): 153-61.
11. Edwards JF, Dubey J. Toxoplasma gondii abortion storm in sheep on a Texas farm and isolation of mouse virulent atypical genotype T. gondii from an aborted lamb from a chronically infected ewe. Vet Parasitol. 2013; 192 (1-3): 129-36.
12. Boughattas S, Someeh R, Ajamein V, et al. A case report of cerebral toxoplasmosis in an hiv-positive patient: risk of possible transmission through contaminated water/food. J Food Qual Hazards Control. 2017; 4 (1): 32-34.
13. Ghaffari AD, Dalimi A. Molecular Identification of Toxoplasma gondii in the Native Slaughtered Cattle of Tehran Province, Iran. Journal of Food Quality and Hazards Control. 2019; 6 (4): 153-161.
14. Jittapalapong S, Sangwaranond A, Inpunkaew T, et al. Seroprevalence of Toxoplasma gondii infection in dairy cows in Northeastern Thailand. The Southeast Asian journal of tropical medicine and public health. 2008; 39 (1): 1-5.
15. Tenter AM. Toxoplasma gondii in animals used for human consumption. Mem Inst Oswaldo Cruz. 2009;104 (2): 364-9.
16. Boughattas S, Bouratbine A. Genetic Characterization of Toxoplasma gondii isolated from chicken meats in Tunisia. J Food Qual Hazards Control 2015; 2 (3): 97-100.
17. Boughattas S, Bouratbine A. Prevalence of food-borne Toxoplasma gondii in free-ranging chickens sold in Tunis, Tunisia. J Food Qual Hazards Control. 2014; 1 (3): 89-92.
18. Sadek OA, Abdel-Hameed ZM, Kuraa HM. 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. 2015; 61 (145): 166-77.
19. Bresciani KDS, Toniollo GH, da Costa AJ, et al. Clinical, parasitological and obstetric observations in pregnant bitches with experimental toxoplasmosis. Cienc Rural. 2001; 31 (6): 1039-43.
20. Powell CC, Brewer M, Lappin MR. Detection of Toxoplasma gondii in the milk of experimentally infected lactating cats. Vet Parasitol. 2001; 102 (1-2): 29-33.
21. Ishag MY, Magzoub E, Majid M. Detection of Toxoplasma gondii tachyzoites in the milk of experimentally infected lactating She-Camels. J Anim Vet Adv. 2006; 5 (6): 456-8.
22. Costa V, Langoni H. Detection of Toxoplasma gondii in the milk of experimentally infected Wistar female rats. J Venom Anim Toxins Incl Trop Dis. 2010; 16 (2): 368-74.
23. Heidari MS, Yadollahpour MH, Hoseiny Z, et al. Comparative Study of the Importance of Breast Milk from the Qur'an's Viewpoint and Medical Knowledge. J Islam Health. 2014; 1 (3): 69-77.
24. Dubey JP. Re-examination of resistance of Toxoplasma gondii tachyzoites and bradyzoites to pepsin and trypsin digestion. Parasitology. 1998; 116 (1): 43-50.
25. Bonametti AM, Passos JN, Koga da Silva EM, et al. Probable transmission of acute toxoplasmosis through breast feeding. J Trop Pediatr. 1997; 43 (2): 116.
26. Pokorska J, Kułaj D, Dusza M, et al. New rapid method of DNA isolation from milk somatic cells. Anim Biotechnol. 2016; 27 (2): 113-117.
27. Bourdin C, Busse A, Kouamou E, et al. PCR-based detection of Toxoplasma gondii DNA in blood and ocular samples for diagnosis of ocular toxoplasmosis. J Clin Microbiol. 2014; 52 (11): 3987-3991.
28. Olfaty-Harsini S, Shokrani H, Nayebzadeh H. Toxoplasma gondii infection in slaughtered ewes in Khorramabad, west of Iran: a preliminary molecular study. Iran J Vet Med. 2017; 11 (3): 209-15.
29. Tasawar Z, Lashari MH, Hanif M, et al. Seroprevalence of Toxoplasma gondii in domestic goats in Multan, Punjab, Pakistan. Pak J Life Soc Sci. 2011; 9 (1): 24-7.
30. Mancianti F, Nardoni S, D'Ascenzi C, 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; 905326.
31. Bezerra M, Kim P, Moraes ÉP, et al. Detection of Toxoplasma gondii in the milk of naturally infected goats in the N ortheast of B razil. Transbound Emerg Dis. 2015; 62 (4): 421-4.
32. da Silva JG, Alves BHLS, Melo RPB, et al. 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. 2015; 142: 145-8.
33. Sroka J, Kusyk P, Bilska-Zając E, et al. 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 (Praha). 2017; 64: 023.
34. Saad NM, Hussein AAA, Ewida RM. Occurrence of Toxoplasma gondii in raw goat, sheep, and camel milk in Upper Egypt. Vet World. 2018; 11 (9): 1262-1265.
35. Iacobucci E, Taus N, Ueti M, et al. Detection and genotypic characterization of Toxoplasma gondii DNA within the milk of Mongolian livestock. Parasitol Res 2019; 118 (6): 2005-2008.
36. Tonouhewa ABN, Akpo Y, Sherasiya A, et al. A serological survey of Toxoplasma gondii infection in sheep and goat from Benin, West-Africa. J Parasit Dis. 2019; 43 (3): 343-349.
37. Gazzonis AL, Zanzani SA, Villa L, et al. 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. 2019; 170: 104738.
38. Rehman F, Shah M, Ali A, et al. Unpasteurised milk consumption as a potential risk factor for toxoplasmosis in females with recurrent pregnancy loss. J Obstet Gynaecol. 2020; 40 (8): 1106-1110.
39. Azab ME, Kamel AM, Makled KM, et al. Naturally occurring Toxoplasma antibodies in serum and milk of lactating women. J Egypt Soc Parasitol. 1992; 22 (2): 561-8.
40. Saso A, Bamford A, Grewal K, et al. Fifteen-minute consultation: Management of the infant born to a mother with toxoplasmosis in pregnancy. Arch Dis Child Educ Pract Ed. 2020; 105 (5): 262-269.
41. Saki J, Foroutan M, Khodkar I, et al. Seroprevalence and molecular detection of Toxoplasma gondii in healthy blood donors in southwest Iran. Transfus Apher Sci. 2019;58 (1):79-82.
42. Wassef R, Abdel-Malek R. Validity of a new immunochromatographic test in detection of Toxoplasma gondii in cancer patients. J Parasit Dis. 2019;43 (1):83-36.
43. Rahimi Esboei B, Kazemi B, Zarei M, et al. Evaluation of RE and B1 genes as targets for detection of Toxoplasma gondii by nested PCR in blood samples of patients with ocular toxoplasmosis. Acta Parasitol. 2019;64 (2):384-389.
44. Murata FHA, Ferreira MN, Pereira-Chioccola VL, et al. Evaluation of serological and molecular tests used to identify Toxoplasma gondii infection in pregnant women attended in a public health service in São Paulo state, Brazil. Diagn Microbiol Infect Dis. 2017;89 (1):13-19.
2. Reischl U, Bretagne S, Krüger D, et al. Comparison of two DNA targets for the diagnosis of toxoplasmosis by real-time PCR using fluorescence resonance energy transfer hybridization probes. BMC Infect Dis. 2003; 3: 7.
3. Eshratkhah Mohammadnejad A, Eslami G, Shamsi F,et al. Prevalence of Food-Borne Toxoplasma in Pregnant Women Population of Urmia, Iran. J Food Qual Hazards Control. 2018; 5 (1): 17-23.
4. Tavassoli M, Esmaeilnejad B, Malekifard F, et al. Detection of Toxoplasma gondii DNA in Sheep and Goat Milk in Northwest of Iran by PCR-RFLP. J Food Qual Hazards Control. 2013; 6 (10): e8201.
5. Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: from animals to humans. Int J Parasitol. 2000; 30 (12-13): 1217-1258.
6. Amairia S, Rouatbi M, Rjeibi MR, et al. Molecular prevalence of Toxoplasma gondii DNA in goats’ milk and seroprevalence in Northwest Tunisia. Vet Med Sci. 2016; 2 (3): 154-160.
7. De Oliveira L, Junior LC, De Melo C, et al. Toxoplasma gondii isolates from free-range chickens from the northeast region of Brazil. J Parasitol. 2009; 95 (1): 235-7.
8. Ragozo AMA, Yai LEO, Oliveira L, et al. Isolation of Toxoplasma gondii from goats from Brazil. J Parasitol. 2009; 95 (2): 323-6.
9. Fajardo HV, D’ávila S, Bastos RR, et al. Seroprevalence and risk factors of toxoplasmosis in cattle from extensive and semi-intensive rearing systems at Zona da Mata, Minas Gerais state, Southern Brazil. Parasit Vectors. 2013; 6: 191.
10. Bezerra R, Carvalho F, Guimarães L, et al. Genetic characterization of Toxoplasma gondii isolates from pigs intended for human consumption in Brazil. Veterinary Parasitology. 2012; 189 (2-4): 153-61.
11. Edwards JF, Dubey J. Toxoplasma gondii abortion storm in sheep on a Texas farm and isolation of mouse virulent atypical genotype T. gondii from an aborted lamb from a chronically infected ewe. Vet Parasitol. 2013; 192 (1-3): 129-36.
12. Boughattas S, Someeh R, Ajamein V, et al. A case report of cerebral toxoplasmosis in an hiv-positive patient: risk of possible transmission through contaminated water/food. J Food Qual Hazards Control. 2017; 4 (1): 32-34.
13. Ghaffari AD, Dalimi A. Molecular Identification of Toxoplasma gondii in the Native Slaughtered Cattle of Tehran Province, Iran. Journal of Food Quality and Hazards Control. 2019; 6 (4): 153-161.
14. Jittapalapong S, Sangwaranond A, Inpunkaew T, et al. Seroprevalence of Toxoplasma gondii infection in dairy cows in Northeastern Thailand. The Southeast Asian journal of tropical medicine and public health. 2008; 39 (1): 1-5.
15. Tenter AM. Toxoplasma gondii in animals used for human consumption. Mem Inst Oswaldo Cruz. 2009;104 (2): 364-9.
16. Boughattas S, Bouratbine A. Genetic Characterization of Toxoplasma gondii isolated from chicken meats in Tunisia. J Food Qual Hazards Control 2015; 2 (3): 97-100.
17. Boughattas S, Bouratbine A. Prevalence of food-borne Toxoplasma gondii in free-ranging chickens sold in Tunis, Tunisia. J Food Qual Hazards Control. 2014; 1 (3): 89-92.
18. Sadek OA, Abdel-Hameed ZM, Kuraa HM. 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. 2015; 61 (145): 166-77.
19. Bresciani KDS, Toniollo GH, da Costa AJ, et al. Clinical, parasitological and obstetric observations in pregnant bitches with experimental toxoplasmosis. Cienc Rural. 2001; 31 (6): 1039-43.
20. Powell CC, Brewer M, Lappin MR. Detection of Toxoplasma gondii in the milk of experimentally infected lactating cats. Vet Parasitol. 2001; 102 (1-2): 29-33.
21. Ishag MY, Magzoub E, Majid M. Detection of Toxoplasma gondii tachyzoites in the milk of experimentally infected lactating She-Camels. J Anim Vet Adv. 2006; 5 (6): 456-8.
22. Costa V, Langoni H. Detection of Toxoplasma gondii in the milk of experimentally infected Wistar female rats. J Venom Anim Toxins Incl Trop Dis. 2010; 16 (2): 368-74.
23. Heidari MS, Yadollahpour MH, Hoseiny Z, et al. Comparative Study of the Importance of Breast Milk from the Qur'an's Viewpoint and Medical Knowledge. J Islam Health. 2014; 1 (3): 69-77.
24. Dubey JP. Re-examination of resistance of Toxoplasma gondii tachyzoites and bradyzoites to pepsin and trypsin digestion. Parasitology. 1998; 116 (1): 43-50.
25. Bonametti AM, Passos JN, Koga da Silva EM, et al. Probable transmission of acute toxoplasmosis through breast feeding. J Trop Pediatr. 1997; 43 (2): 116.
26. Pokorska J, Kułaj D, Dusza M, et al. New rapid method of DNA isolation from milk somatic cells. Anim Biotechnol. 2016; 27 (2): 113-117.
27. Bourdin C, Busse A, Kouamou E, et al. PCR-based detection of Toxoplasma gondii DNA in blood and ocular samples for diagnosis of ocular toxoplasmosis. J Clin Microbiol. 2014; 52 (11): 3987-3991.
28. Olfaty-Harsini S, Shokrani H, Nayebzadeh H. Toxoplasma gondii infection in slaughtered ewes in Khorramabad, west of Iran: a preliminary molecular study. Iran J Vet Med. 2017; 11 (3): 209-15.
29. Tasawar Z, Lashari MH, Hanif M, et al. Seroprevalence of Toxoplasma gondii in domestic goats in Multan, Punjab, Pakistan. Pak J Life Soc Sci. 2011; 9 (1): 24-7.
30. Mancianti F, Nardoni S, D'Ascenzi C, 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; 905326.
31. Bezerra M, Kim P, Moraes ÉP, et al. Detection of Toxoplasma gondii in the milk of naturally infected goats in the N ortheast of B razil. Transbound Emerg Dis. 2015; 62 (4): 421-4.
32. da Silva JG, Alves BHLS, Melo RPB, et al. 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. 2015; 142: 145-8.
33. Sroka J, Kusyk P, Bilska-Zając E, et al. 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 (Praha). 2017; 64: 023.
34. Saad NM, Hussein AAA, Ewida RM. Occurrence of Toxoplasma gondii in raw goat, sheep, and camel milk in Upper Egypt. Vet World. 2018; 11 (9): 1262-1265.
35. Iacobucci E, Taus N, Ueti M, et al. Detection and genotypic characterization of Toxoplasma gondii DNA within the milk of Mongolian livestock. Parasitol Res 2019; 118 (6): 2005-2008.
36. Tonouhewa ABN, Akpo Y, Sherasiya A, et al. A serological survey of Toxoplasma gondii infection in sheep and goat from Benin, West-Africa. J Parasit Dis. 2019; 43 (3): 343-349.
37. Gazzonis AL, Zanzani SA, Villa L, et al. 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. 2019; 170: 104738.
38. Rehman F, Shah M, Ali A, et al. Unpasteurised milk consumption as a potential risk factor for toxoplasmosis in females with recurrent pregnancy loss. J Obstet Gynaecol. 2020; 40 (8): 1106-1110.
39. Azab ME, Kamel AM, Makled KM, et al. Naturally occurring Toxoplasma antibodies in serum and milk of lactating women. J Egypt Soc Parasitol. 1992; 22 (2): 561-8.
40. Saso A, Bamford A, Grewal K, et al. Fifteen-minute consultation: Management of the infant born to a mother with toxoplasmosis in pregnancy. Arch Dis Child Educ Pract Ed. 2020; 105 (5): 262-269.
41. Saki J, Foroutan M, Khodkar I, et al. Seroprevalence and molecular detection of Toxoplasma gondii in healthy blood donors in southwest Iran. Transfus Apher Sci. 2019;58 (1):79-82.
42. Wassef R, Abdel-Malek R. Validity of a new immunochromatographic test in detection of Toxoplasma gondii in cancer patients. J Parasit Dis. 2019;43 (1):83-36.
43. Rahimi Esboei B, Kazemi B, Zarei M, et al. Evaluation of RE and B1 genes as targets for detection of Toxoplasma gondii by nested PCR in blood samples of patients with ocular toxoplasmosis. Acta Parasitol. 2019;64 (2):384-389.
44. Murata FHA, Ferreira MN, Pereira-Chioccola VL, et al. Evaluation of serological and molecular tests used to identify Toxoplasma gondii infection in pregnant women attended in a public health service in São Paulo state, Brazil. Diagn Microbiol Infect Dis. 2017;89 (1):13-19.
| Files | ||
| Issue | Vol 16 No 4 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijpa.v16i4.7873 | |
| Keywords | ||
| Toxoplasmosis Milk Human Goats Polymerase chain reaction | ||
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How to Cite
1.
Mohammadi Khamsian E, Hajimohammadi B, Eslami G, Fallahzadeh MH, Hosseini SS. Toxoplasma gondii in Milk of Human and Goat from the Desert Area in Central Iran. Iran J Parasitol. 2021;16(4):601-609.
