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Research
(Published
online: 12-08-2014)
8. Molecular detection of Toxoplasma gondii
DNA in milk and risk factors analysis of seroprevalence in
pregnant women at Sharkia, Egypt - Heba A. Ahmed, Saleh
M. Shafik, Mahmoud E. M. Ali, Sanya T. Elghamry and Alshymaa A.
Ahmed
Veterinary World, 7(8): 594-600
doi:
10.14202/vetworld.2014.594-600
Heba A. Ahmed: Department of Zoonoses, Faculty of
Veterinary Medicine, Zagazig University, 44511, Zagazig, Egypt;
heba_ahmed@zu.edu.eg
Saleh M. Shafik: Food Hygiene Department, Animal Health
Research Institute, Mansoura, Egypt; Saleh_Shafik@yahoo.com
Mahmoud E. M. Ali: Food Hygiene Department, Animal Health
Research Institute, Mansoura, Egypt; dr_hashem59@yahoo.com
Sanya T. Elghamry: Food Hygiene Department, Animal Health
Research Institute, Mansoura, Egypt; sanyaelghamry@yahoo.com
Alshymaa A. Ahmed: Clinical pathology Department, Faculty
of Medicine, Zagazig University, Egypt; doaa_ahmed57@yahoo.com
Received: 10-05-2014, Revised: 26-06-2014, Accepted: 03-07-2014,
Published online: 12-08-2014
Corresponding author: Heba A. Ahmed, email: heba_ahmed@zu.edu.eg
Abstract
Aim: Toxoplasmosis is one of
the most important zoonotic parasitic diseases worldwide.
Infection is not only acquired by contact with the definitive
host, but also by ingestion of raw milk and milk products. The aim
of the study was to detect T. gondii DNA in milk samples, and to
estimate anti-T. gondii antibodies in pregnant women for the
analysis of the associated risk factors.
Materials and Methods: The study involved molecular
examination of 150 milk samples collected from rural settings at
Sharkia, Egypt. Seroprevalence of anti-T. gondii antibodies was
determined in 100 pregnant women by indirect haemagglutination
test. The analysis of risk factors associated with seropositive
results was assessed by univariate and multivariate logistic
regression.
Results: T. gondii DNA was detected in 8% and 2% of goat
and sheep milk samples, respectively, while none of cow milk
samples were positive. Seroprevalence of T. gondii antibodies in
pregnant women was 82%, anti-T. gondii-IgG and anti-T. gondii-IgM
were detected in 63% and 11% serum samples, respectively. The
results showed a significant correlation between the
seroprevalence and the contact with cats and consumption of raw
milk and homemade cheese.
Conclusion: The role of raw milk in transmission of T.
gondii cannot be excluded. Contact with cats remains the main risk
factor for acquiring T. gondii infection; also consumption of raw
milk and milk products is considered an important risk factor.
Further large scale studies are recommended to clarify the
association of T. gondii seroprevalence with different risk
factors.
Keywords: B1 gene, pregnant women, raw milk, risk factors,
seroprevalence, T. gondii.
References
1. Tenter, A. M. (2009) Toxoplasma gondii in animals used for
human consumption. Mem. Inst. Oswaldo. Cruz., 104 (2):
364-369.
http://dx.doi.org/10.1590/S0074-02762009000200033
PMid:19430665 |
|
|
2. Weiss, L. M. and Dubey, J. P. (2009) Toxoplasmosis: A
history of clinical observations. Int. J. Parasitol., 39 (8):
895-901.
http://dx.doi.org/10.1016/j.ijpara.2009.02.004
PMid:19217908 PMCid:PMC2704023 |
|
|
|
3. Jittapalapong, S., Sangwaranond, A., Inpankaew, T., Phasuk,
C., Pinyopanuwat, N., Chimnoi, W., Kengradomkij, C., Arunwipat,
P. and Maruyama, S. (2008) Seroprevalence of Toxoplasma gondii
infection in dairy cows in northeastern Thailand. Southeast
Asian J. Trop. Med. Public Health, 39 (suppl 1): 1-5. |
|
|
4. Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000)
Toxoplasma gondii: from animals to humans. Int. J. Parasitol.,
30 (12-13): 1217-1258.
http://dx.doi.org/10.1016/S0020-7519(00)00124-7 |
|
|
5. Havelaar, A. H., Kemmeren, J. M. and Kortbeek, L. M. (2007)
Disease burden of congenital toxoplasmosis. Clin. Infect.
Dis., 44 (11): 1467-1474.
http://dx.doi.org/10.1086/517511
PMid:17479945 |
|
|
6. Pappas, G., Roussos, N. and Falagas, M. E. (2009)
Toxoplasmosis snapshots: global status of Toxoplasma gondii
seroprevalence and implications for pregnancy and congenital
toxoplasmosis. Int. J. Parasitol., 39 (12): 1385- 1394.
http://dx.doi.org/10.1016/j.ijpara.2009.04.003
PMid:19433092 |
|
|
7. Camossi, L. G., Greca-Junior, H., Correa, A. P., Richini-
Pereira, V. B., Silva, R. C., Da Silva, A. V. and Langoni, H.
(2011) Detection of Toxoplasma gondii DNA in the milk of
naturally infected ewes. Vet. Parasitol., 177 (3-4): 256-261.
http://dx.doi.org/10.1016/j.vetpar.2010.12.007
PMid:21216534 |
|
|
8. Reischl, U., Bretagne, S., Kruger, D., Ernault, P. and
Costa, J. M. (2003) Comparison of two DNA targets for the
diagnosis of Toxoplasmosis by real-time PCR using fluorescence
resonance energy transfer hybridization probes. BMC Infect.
Dis., 3: 7.
http://dx.doi.org/10.1186/1471-2334-3-7
PMid:12729464 PMCid:PMC156600 |
|
|
9. Jones, C. D., Okhravi, N., Adamson, P., Tasker, S. and
Lightman, S. (2000) Comparison of PCR detection methods for
B1, P30, and 18S rDNA genes of T. gondii in aqueous humor.
Invest. Ophthalmol. Vis. Sci., 41 (3): 634-644.
PMid:10711675 |
|
|
10. Jackson, M. H. and Hutchison, W. M. (1989) The prevalence
and source of Toxoplasma infection in the environment. Adv.
Parasitol., 28: 55-105.
http://dx.doi.org/10.1016/S0065-308X(08)60331-0 |
|
|
11. Sroka, S., Bartelheimer, N., Winter, A., Heukelbach, J.,
Ariza, L., Ribeiro, H., Oliveira, F. A., Queiroz, A. J.,
Alencar, C., Jr. and Liesenfeld, O. (2010) Prevalence and risk
factors of toxoplasmosis among pregnant women in Fortaleza,
North-Eastern Brazil. Am. J. Trop. Med. Hyg., 83 (3): 528-
533.
http://dx.doi.org/10.4269/ajtmh.2010.10-0082
PMid:20810816 PMCid:PMC2929047 |
|
|
12. Murphy, M. A., Shariflou, M. R. and Moran, C. (2002) High
quality genomic DNA extraction from large milk samples. J.
Dairy Res., 69 (4): 645-649.
http://dx.doi.org/10.1017/S0022029902005848
PMid:12463700 |
|
|
13. Psifidi, A., Dovas, C. I. and Banos, G. (2010) A
comparison of six methods for genomic DNA extraction suitable
for PCR-based genotyping applications using ovine milk
samples. Mol. Cell. Probes, 24 (2): 93-98.
http://dx.doi.org/10.1016/j.mcp.2009.11.001
PMid:19900535 |
|
|
14. Bretagne, S., Costa, J. M., Vidaud, M., Nhieu, J. T. V.
and Feith, J. F. (1993) Detection of Toxoplasma gondii by
competitive DNA amplification of bronchoalveolar lavage
samples. J. Infect. Dis., 168 (6): 1585-1588.
http://dx.doi.org/10.1093/infdis/168.6.1585
PMid:8245552 |
|
|
|
15. Costa, V. M. and Langoni, H. (2010) Detection of
Toxoplasma gondii in the milk of experimentally infected
Wistar female rats. J. Venom Anim. Toxins incl. Trop. Dis., 16
(2): 368-374. |
|
|
16. Bonametti, A. M., Passos, J. N., Koga da Silva, E. M. and
Macedo, Z. S. (1997) Probable transmission of acute
toxoplasmosis through breast feeding. J. Trop. Pediatr., 43
(2): 116.
http://dx.doi.org/10.1093/tropej/43.2.116
PMid:9143185 |
|
|
17. Elamin, E. A., Elias, S., Daugschies, A. and Rommel, M.
(1992) Prevalence of Toxoplasma gondii antibodies in pastoral
camels (Camelus dromedarius) in the Butana plains, mid-Eastern
Sudan. Vet. Parasitol., 43 (3-4): 171-175.
http://dx.doi.org/10.1016/0304-4017(92)90158-6 |
|
|
18. Dubey, J. P. (1998) Re-examination of resistance of
Toxoplasma gondii tachyzoites and bradyzoites to pepsin and
trypsin digestion. Parasitol., 116 (Pt 1) 43-50.
http://dx.doi.org/10.1017/S0031182097001935 |
|
|
19. Riemann, H. P., Meyer, M. E., Theis, J. H., Kelso, G. and
Behymer, D. E. (1975) Toxoplasmosis in an infant fed
unpasteurized goat milk. J. Pediatr., 87 (4): 573-576.
http://dx.doi.org/10.1016/S0022-3476(75)80825-0 |
|
|
20. Sacks, J. J., Roberto, R. R. and Brooks, N. F. (1982)
Toxoplasmosis infection associated with raw goat's milk. JAMA,
248 (14): 1728-1732.
http://dx.doi.org/10.1001/jama.1982.03330140038029
PMid:7120593 |
|
|
21. Dehkordi, F. S., Borujeni, M. R., Rahimi, E. and Abdizadeh,
R. (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 (2): 120-125.
http://dx.doi.org/10.1089/fpd.2012.1311
PMid:23441913 |
|
|
|
22. Mancianti, F., Nardoni, S., D'Ascenzi, C., Pedonese, F.,
Mugnaini, L., Franco, F. and Papini, R. (2013) Sero-
prevalence, detection of DNA in blood and milk, and genotyping
of Toxoplasma gondii in a goat population in Italy. BioMed.
Res. Int., 2013: 6. |
|
|
23. Bezerra, M. J., Kim, P. C., Moraes, E. P., Sa, S. G.,
Albuquerque, P. P., Silva, J. G., Alves, B. H. and Mota, R. A.
(2013) Detection of Toxoplasma gondii in the milk of naturally
infected goats in the North-East of Brazil. Transbound Emerg.
Dis. DOI: 10.1111/tbed.12160.
http://dx.doi.org/10.1111/tbed.12160 |
|
|
|
24. Chiari, C. A., Lima, W. S., Antunes, C. M. F. and Lima, J.
D. (1987) Soroepidemiologia da toxoplasmose caprina em Minas
Gerais. Brasil Arq. Bras. Med. Vet. Zootec., 39: 587- 609. |
|
|
25. Chiari, C. A. and Neves, D. P. (1984) Toxoplasmose humana
adquirida através da ingestão de leite de cabra. Memórias do
Instituto. Oswaldo Cruz., 79: 337-340.
http://dx.doi.org/10.1590/S0074-02761984000300007 |
|
|
26. Skinner, L. J., Timperley, A. C., Wightman, D., Chatterton,
J. M. and Ho-Yen, D. O. (1990) Simultaneous diagnosis of
toxoplasmosis in goats and goatowner's family. Scand. J.
Infect. Dis., 22 (3): 359-361.
http://dx.doi.org/10.3109/00365549009027060
PMid:2371548 |
|
|
27. Walsh, C. P., Hammond, S. E., Zajac, A. M. and Lindsay, D.
S. (1999) Survival of Toxoplasma gondii tachyzoites in goat
milk: potential source of human toxoplasmosis.J. Eukaryot.
Microbiol., 46 (5): 73S-74S.
PMid:10519255 |
|
|
28. Hiramoto, R. M., Mayrbaurl-Borges, M., Galisteo, A. J.,
Jr., Meireles, L. R., Macre, M. S. and Andrade, H. F., Jr.
(2001) Infectivity of cysts of the ME-49 Toxoplasma gondii
strain in bovine milk and homemade cheese. Rev. Saude. Publica.,
35 (2): 113-118.
http://dx.doi.org/10.1590/S0034-89102001000200002
PMid:11359195 |
|
|
29. Fusco, G., Rinaldi, L., Guarino, A., Proroga, Y. T., Pesce,
A., Giuseppina, de M. and Cringoli, G. (2007) Toxoplasma
gondii in sheep from the Campania region (Italy). Vet.
Parasitol., 49 (3-4): 271-274.
http://dx.doi.org/10.1016/j.vetpar.2007.07.020
PMid:17764846 |
|
|
30. Dubey, J. P. (1991) Toxoplasmosis: an overview. South-East
Asian J. Trop. Med. Public Health, 22 88-92.
PMid:1822945 |
|
|
31. Dubey, J. P. and Thulliez, P. (1993) Persistence of tissue
cysts in edible tissues of cattle fed Toxoplasma gondii
oocysts. Am. J. Vet. Res., 54 (2): 270-273.
PMid:8430937 |
|
|
32. El Deeb, H. K., Salah-Eldin, H., Khodeer, S. and Allah, A.
A. (2012) Prevalence of Toxoplasma gondii infection in
antenatal population in Menoufia governorate, Egypt. Acta
Trop., 124 (3): 185-191.
http://dx.doi.org/10.1016/j.actatropica.2012.08.005
PMid:22921952 |
|
|
|
33. Zemene, E., Yewhalaw, D., Abera, S., Belay, T., Samuel, A.
and Zeynudin, A. (2012) Seroprevalence of Toxoplasma gondii
and associated risk factors among pregnant women in Jimma
town, Southwestern Ethiopia. BMC Infect. Dis., 12 (1): 1-6. |
|
|
|
34. Abd El-Ghany, A. M. and Merwad, A. M. A. (2012) Epi-
demiology and molecular detection of zoonotic Toxoplasma
gondii in cat feces and seroprevalence of anti-Toxoplasma
gondii antibodies in pregnant women and sheep. Life Sci. J., 9
(1s): 133-146. |
|
|
35. Azab, M. E., el-Shenawy, S. F., el-Hady, H. M. and Ahmad,
M. M. (1993) Comparative study of three tests (indirect
haemagglutination, direct agglutination, and indirect immuno-fluorescence)
for detection of antibodies to Toxoplasma gondii in pregnant
women. J. Egypt. Soc. Parasitol., 23 (2): 471-476.
PMid:8376864 |
|
|
|
36. Awadalla, H. N., El-Temsahy, M. M., Sharaki, O. A. and El
Zawawy, L. A. (2008) Validity of IgG avidity enzyme linked
immunosorbent assay and polymerase chain reaction for the
determination of Toxoplasma infections during pregnancy. PUJ,
1: 23-30. |
|
|
37. Ibrahim, H. M., Huang, P., Salem, T. A., Talaat, R. M.,
Nasr, M. I., Xuan, X. and Nishikawa, Y. (2009) Short report:
prevalence of Neospora caninum and Toxoplasma gondii
antibodies in northern Egypt. Am. J. Trop. Med. Hyg., 80 (2):
263-267.
PMid:19190225 |
|
|
|
38. Hussein, A. H., Ali, A. E., Saleh, M. H., Nagaty, I. M.
and Rezk, A. Y. (2001) Prevalence of Toxoplasma infection in
Qualyobia governorate, Egypt. J. Egypt. Soc. Parasitol., 31
(2): 355-363. |
|
|
39. El-Gozamy, B. R., Mohamed, S. A. and Mansour, H. A. (2009)
Toxoplasmosis among pregnant women in Qualyobia Governorate,
Egypt. J. Egypt. Soc. Parasitol., 39 (2): 389-401.
PMid:19795746 |
|
|
40. Attia, R. A., el-Zayat, M. M., Rizk, H. and Motawea, S.
(1995) Toxoplasma IgG. & IgM. antibodies. A case control
study. J. Egypt. Soc. Parasitol., 25 (3): 877-882.
PMid:8586880 |
|
|
41. Spalding, S. M., Amendoeira, M. R. R., Klein, C. H. and
Ribeiro, L. C. (2005) Serological screening and toxoplasmosis
exposure factors among pregnant women in South of Brazil. Rev.
Soc. Bras. Med. Trop., 38 173-177.
http://dx.doi.org/10.1590/S0037-86822005000200009
PMid:15821794 |
|
|
|
42. Bouhamdan, S. F., Bitar, L. K., Saghir, H. J., Bayan, A.
and Araj, G. F. (2010) Seroprevalence of Toxoplasma antibodies
among individuals tested at hospitals and private laboratories
in Beirut. Lebanese Med. J., 58: 8-11. |
|
|
43. Moura, F. L. d., Amendoeira, M. R. R., Bastos, O. M. P.,
Mattos, D. P. B. G. d., Fonseca, A. B. M., Nicolau, J. L.,
Neves, L. B. d. and Millar, P. R. (2013) Prevalence and risk
factors for Toxoplasma gondii infection among pregnant and
postpartum women attended at public healthcare facilities in
the City of Niterói, State of Rio de Janeiro, Brazil. Rev.
Soc. Bras. Med. Trop., 46: 200-207.
http://dx.doi.org/10.1590/0037-8682-1613-2013
PMid:23559345 |
|
|
44. Tekay, F. and Ozbek, E. (2007) The seroprevalence of
Toxoplasma gondii in women from Sanliurfa, a province with a
high raw meatball consumption. Turkiye Parazitol. Derg., 31
(3): 176-179.
PMid:17918053 |
|
|
45. Gebremedhin, E. Z., Abebe, A. H., Tessema, T. S., Tullu,
K. D., Medhin, G., Vitale, M., Di Marco, V., Cox, E. and Dorny,
P. (2013) Seroepidemiology of Toxoplasma gondii infection in
women of child-bearing age in central Ethiopia. BMC Infect.
Dis., 13: 101.
http://dx.doi.org/10.1186/1471-2334-13-101
PMid:23442946 PMCid:PMC3598201 |
|
|
46. Lee, S.E., Kim, J.Y., Kim, Y.A., Cho, S.H., Ahn, H.J.,
Woo, H.M., Lee, W.J. and Nam, H.W. (2010) Prevalence of
Toxoplasma gondii infection in stray and household cats in
regions of Seoul, Korea. Korean J. Parasitol., 48 (3): 267-
270.
http://dx.doi.org/10.3347/kjp.2010.48.3.267
PMid:20877509 PMCid:PMC2945805 |
|
|
47. Al-Kappany, Y. M., Rajendran, C., Ferreira, L. R., Kwok,
O. C. H., Abu-Elwafa, S. A., Hilali, M. and Dubey, J. P.
(2010) High prevalence of toxoplasmosis in cats from Egypt:
isolation of viable Toxoplasma gondii, tissue distribution,
and isolate designation. J. Parasitol., 96 (6): 1115-1118.
http://dx.doi.org/10.1645/GE-2554.1
PMid:21158619 |
|
|
48. Jones, J. L., Dargelas, V., Roberts, J., Press, C.,
Remington, J. S. and Montoya, J. G. (2009) Risk factors for
Toxoplasma gondii infection in the United States. Clin.
Infect. Dis., 49 (6): 878-884.
http://dx.doi.org/10.1086/605433
PMid:19663709 |
|
|
49. Minbaeva, G., Schweiger, A., Bodosheva, A., Kuttubaev, O.,
Hehl, A. B., Tanner, I., Ziadinov, I., Torgerson, P. R. and
Deplazes, P. (2013) Toxoplasma gondii infection in Kyrgyzstan:
seroprevalence, risk factor analysis, and estimate of
congenital and AIDS-related toxoplasmosis. PLoS Negl. Trop.
Dis., 7 (2): e2043.
http://dx.doi.org/10.1371/journal.pntd.0002043
PMid:23409201 PMCid:PMC3566989 |
|
