Keywords

Blood donors; Serology; ELISA; Blood transfusion; Toxoplasma gondii; Immunoglobulin M; Immunoglobulin G

Introduction

The majority of attention has been focused on infections of the blood supply. Although it is extremely safe, the risk of transfusion transmitted disease is not zero. Blood transfusions are a common medical procedure in which blood is injected into a patient's body via a narrow tube connected to a vein in their arm or hand. Toxoplasma gondii is a parasitic protozoan that can be carried by most warm blooded animal species and infects nearly one-third of the world's human population [1]. Although toxoplasmosis is found worldwide, the seroprevalence of T. gondii infection varies greatly between countries (10%-80%) and even within a single country [2]. T. gondii infections are usually mild and self-limiting in immunocompetent people. However, severe disease and complications can occur in immunocompromised people and newborns [3]. Food borne transmission (consuming undercooked, contaminated meat), animal to human transmission (ingesting oocysts shed in the feces of infected cats) and vertical transmission from mother to fetus through the placenta during pregnancy are the three main routes of infection. T. gondii can also be transmitted through blood transfusion [4]. Toxoplasmosis appears to be transmitted through blood or leukocyte transfusions, especially if parasitized leukocytes are transfused in high concentrations [5,6]. Since T. gondii may be alive in the citrated blood at 5°C for up to 50 days and the buffy coat, multiple units of blood from different donors are regularly used in children with thalassemia, sickle cell anemia and a plastic anemia who need regular, frequent and multiple transfusions for survival. Many studies have found a high prevalence of T. gondii antibodies in healthy voluntary blood donors and while screening for T. gondii antibodies before transfusion blood is not currently being considered, the information about the epidemiology of T. gondii infection in blood donors is low. The epidemiology of T. gondii infection has been poorly studied in Libya. In Libya, a few previous research on the seroprevalence of T. gondii antibodies has concentrated on specific populations, such as pregnant women 9.1 [7]. Seroprevalence rates among pregnant women in Libya were documented as 27.5% to 34.1% [8,9]. The seroprevalence of toxoplasmosis in Benghazi, however, was found to be as high as 41.7%.

This study aims to investigate the seroprevalence of Toxoplasma antibodies (IgM, IgG) in blood donor sera from a blood transfusion center by the Enzyme Linked Immunosorbent Assay (ELISA) in Benghazi, Libya; and investigate the relationship between this disease (acute, chronic) and associated risk factors among healthy blood donors.

Materials and Methods

Data collection

A questionnaire was filled for each subject and the data were collected after convenient interview. The questions included: Personal information, demography data, social and economic data, nutritional behavior and health data (Index).

Design and setting: A prospective and cross-sectional study six hundred blood samples were collected from healthy blood donors (males and females) in the national blood transfusion central blood bank, Benghazi city, during the period from March 2013 to May 2013. The mean age of the blood donors was 32.85 years and the age range was between 18 and 62 years.

Sample preparation and preservatio

Latex agglutination test: Totally, 600 randomly selected samples were collected from healthy blood donors. About five ml of venous blood was collected from each five mL of blood samples from 600 healthy blood donors were randomly selected for serological testing in sterile containers and tested for blood groups detection

Anti-A, B blend test

• According to the manufacturer's procedure.

• Anti-D blend.

• A slide test based on the agglutination method for Rhesus (Rh) typing in serum using.

• A monoclonal/polyclonal blend reagent.

Serological testing: One of the few methods frequently used in the detection of T. gondii infection in humans and animals is Enzyme-Linked Immunosorbent Assay (ELISA). The presence of antibodies to T. gondii was determined by the conventional ELISA technique, according to the manufacturer,s instructions (Biokit Diagnostics Company, Spain). The optical density of IgG antibody titers were read at 450 nm using automatic ELISA reader (BioTek Plate Reader, Spain); Divide the sample absorbance by the cut-off value. Positive ≥ 1.0 , Negative <0.9 ,E quivocal ≥ 0.9 <1.0

Data nalysis Statistical Package for Social Sciences (SPSS) Version 17 and MedCalc (statistical software) were used for the analysis. A chi-square test was used to analyze the distribution of ABO and Rh blood groups.

Results

The current study was to estimate the actual percentage of toxoplasmosis in blood donors in national blood transfusion center ‘blood bank center in Benghazi. Libya, by using more specific tests ELISA IgM and IgG antibodies. The results revealed that overall infected donor 280 (46.7%) and non infected donor 320 (53.3%). Out of 600 samples only 98 (16.3%) had acute toxoplasmosis characterized by the presence of positive IgM antibodies. While 253 (42.2%) of samples had chronic toxoplasmosis characterized by the presence of positive IgG antibodies only. with high significant differences between them (p<0.01) (Table 1).

Table 1: Seroprevalence of Toxoplasma gondi specific antibodies of blood donors from blood bank center according to ELISA test.

Seroprevalence of toxoplasma antibodies according to age groups and gender

The results showed that Seroprevalence of T. gondii IgG level among blood donor at age groups 18-28, 29-39, 40-51, 52-62 was 31.2%, 49.1%, 50% and 47% respectively. While seroprevalence rate of T. gondii IgM at age groups 18-28, 29-39, 40-51 and 52-62 were 17.7%, 17.4%, 12.0% and 10.5% respectively. In relation to age group the results showed high positive percentage samples, 30 (50%) in ELISA IgG test at age group of (40-51) years, whereas the lowest one was 7 (31.2%) as noticed at the age group of (18-28) years. There was a significant difference between them (P=0.00). While, ELISA-IgM showed variable results characterized by the presence of high percentage 3 (17.7%) at the age group of (18-28) years and the lowest 1 (10.5%) at the age group of (52-62) years. There was no significant difference between them (P=.485) (Table 2). The results revealed that Seroprevalence of T. gondii IgG level among 560 tested blood donors males was 241 (43.03%) and among 40 tested females donors was 12 (30%). On the other the Seroprevalence rate of T. gondii IgM level among 560 tested males donors was 95 (16.96%) and among 40 tested females donors was 3 (7.55%).

Table 2: Seroprevalence of IgG and IgM Toxoplasma gondi-specific antibodies by age and gender among blood donors from blood bank centre according to ELISA test.

Seroprevalence of T. gondii infection according to blood groups

Seroprevalence of T. gondii infection according to blood groups: In this study the relationship between Seroprevalence of anti T. gondii IgG and IgM antibodies and blood groups revealed that, the Seroprevalence rate of IgG to: A negative tested 33 was 15 (45.45%), A positive tested 190 was 79 (41.6%), AB positive tested 30 was 18 (60%), B negative tested 17 was 6 (35.3%), B positive tested 115 was 51 (44.3%), O negative tested 31 was 8 (25.8%) and O positive tested 177 was 27 (40.7%); and the Seroprevalence rate of IgM to: A negative tested 33 was 3 (9.1%), A positive tested 190 was 28 (14.7%), AB negative tested 7 was 0 (0.0%), AB positive tested 30 was 7 (23.3%), B negative tested 17 was 1 (5.9%), B positive tested 115 was 28 (24.3%), O negative tested 31 was 5 (16.1%) and O positive tested 177 was 26 (14.6%). The frequencies of ABO blood group phenotypes, in respect to results of the serological test (positive IgG and/or IgM and negative) for anti-T. gondii antibodies do not demonstrate statistically significant differences. Seroprevalence of T. gondii infection according to blood groups: In this study the relationship between Seroprevalence of anti T. gondii IgG and IgM antibodies and blood groups revealed that, the Seroprevalence rate of IgG to: A negative tested 33 was 15 (45.45%), A positive tested 190 was 79 (41.6%), AB positive tested 30 was 18 (60%), B negative tested 17 was 6 (35.3%), B positive tested 115 was 51 (44.3%), O negative tested 31 was 8 (25.8%) and O positive tested 177 was 27 (40.7%) and the Seroprevalence rate of IgM to: A negative tested 33 was 3 (9.1%), A positive tested 190 was 28 (14.7%), AB negative tested 7 was 0 (0.0%), AB positive tested 30 was 7 (23.3%), B negative tested 17 was 1 (5.9%), B positive tested 115 was 28 (24.3%), O negative tested 31 was 5 (16.1%) and O positive tested 177 was 26 (14.6%) (Table 3). The frequencies of ABO blood group phenotypes, in respect to results of the serological test (positive IgG and/or IgM and negative) for anti-T. gondii antibodies do not demonstrate statistically significant differences.

Table 3: Seroprevalence of IgG and IgM Toxoplasma gondi specific antibodies of blood donors from blood bank centre according to ABO phenotypes by ELISA test.

Seroprevalence of T. gondii infection according to occupation

The relationship between Seroprevalence of T. gondii IgG and IgM antibodies and occupation of blood donors revealed that the presence of anti-toxoplasma IgG antibodies in priva te workers was 42.1% (53/126), no job was48.6% (51/105), student was 27.4% (17/62) and governmental workers was 43.0%(132/307) and seroprevalence rate of T. gondii IgM level in private workers was 18.25% (23/126), No job was 18.09%(19/105), student was 20.96% (13/62) and those having governmental workers was 14.0% (43/307). Toxoplasmosis in those without job which showed included in this study, higher percentage 51 (48.6%) than those having governmental workers 132 (43.0%), private workers was 53 (42.1%) and student 17 (27.4%) in the presence of antitoxoplasma IgG antibodies. While the presence of antitoxoplasma IgM antibodies, this result revealed higher percentage 13 (20.96%) in student and 23 (18.25%) in private workers, without job 19 (18.09) and 43 (14.0%) hose having governmental workers. There was significant differences between them (P<0.01) (Table 4).

Table 4: Seroprevalenceof IgG Toxoplasma gondi specific antibodies their occupation of blood donors from blood bank center according to ELISA test.

Seroprevalence of T. gondii IgG and IgM antibodies in relation to nationality: The results reveald that Seroprevalence of T. gondii IgG in Libyan tested 544 was 233 (42.8%) and non-Libyan tested 56 was 20 (35.7%) and Seroprevalence of T. gondii IgM in Libyan tested 544 was 91 (16.7%) and non-Libyan tested 56 was 7 (12.5%). The seroprevalence rate of infection IGg and IgM antibodies were highest in Libyan tnan non Libyan (Table 5). IgG=X²=13.705, df=13, P=0.395, IgM=X²=12.759, df=13, P=0.467.

Table 5: Seroprevalence of IgG and IgM Toxoplasma gondi specific antibodies of blood donors from blood bank centre according their nationality.

Seroprevalence of T. gondii IgG and IgM antibodies in relation to regions: In this study the incidence of T. gondii IgG and IgM antibodies in correlation to region are showed that incidence of T. gondii IgG in Benghazi tested 453 was 195 (43.1%) and out Benghazi tested 147 was 58 (39.45%); and incidence of T. gondii IgM in Benghazi tested 453 was 79 (17.4%) and out Benghazi tested 147 was 19 (12.9%) (Table 6).

Table 6: Seroprevalence of IgG and IgM Toxoplasma gondi specific antibodies of Blood donors from blood transfusion center according to region.

Discussion

Toxoplasmosis is a very common parasitic disease caused by an obligate intracellular protozoon parasite spread among young adults in different parts of the world. An acute infection of toxoplasmosis can be transmitted transplacentally during pregnancy from mother to fetus [8]. In various regions of the world, the percentage of toxoplasma antibodies among young adults varies from 5% to 95% [9]. Due to the T. gondii parasites' ability to resist at 4°C and for a period of fifty days, there is a high risk of infection spreading to recipients during blood transfusion. To our knowledge, this is the first study to be carried out on the seroprevalence of Toxoplasma gondii among healthy blood donors. Six hundred random healthy blood donors from the blood bank center were tested by ELISA to determine the T. gondii infection (IgG and IgM antibodies for T. gondii). The results revealed that the overall seroprevalence of toxoplasma antibodies among apparently healthy blood donors was 46.7% by ELISA test. This rate is comparable to previous reports at 41.7% and 43.6% [10]. The present finding was higher than previous reports, 3.4%, 3.7% [11]. On the other hand, the present results are lower than other results by 52.1% [12]. The reason for similarities and differences refers to the regional variations in the seroprevalence of T. gondii rates from one to another country or even within the same country. This variation has been attributed to climate, cultural differences pertaining to hygiene and feeding habits [13]. The seroprevalence of Toxoplasma gondii IgG and IgM antibodies was 42.2% and 16.3%, respectively, compared to previous reports of 7.4% and 1.9% 20.3 and 3.6 for IgG and IgM antibodies, respectively [14]. Different researchers' explanations for previous percentage differences may be related to T. gondii. Seropositivity in the human population. It varies greatly across geographical areas within a single country and even within a single city. These differences may be related to several other factors, including cultural level, nutritional habits, age and rural or urban area, even to the use of different kit origins. The current study showed that the infection increases with age. The results showed a high percentage of positive IgG samples (30, 50%) by ELISA test at the age group of 40-51 years, whereas the lowest one was (31.2%) at the age group of 18-28 years. While IgM showed variable results distinguished by the presence of a high percentage (17.7%) in the age group 18-28 years and the lowest.(10.5%) at age group 52-62 years. This finding is in agreement with previous results, for IgG was 52.9% in age group 41-50 years and the lowest percentage(15%) at age group <20, the highest infection rate occurred in age group (31-35) years. Similar findings have been reported by some studies, that incidence of toxoplasma infection is well known to increase with age [15,16]. On the other hand, the present results disagree with some previous results from different regions [17]. These differences between several previous results and our results may be due to the specificity and sensitivity of the immunodiagnostics method and the immune response of each host to the parasitic strain [18]. Furthermore, the IgM antibody was located near the middle age group, meaning the donors in this group had a recent infection by T. gondii, this infection may have come from drinking contaminated water, vegetables or by eating raw infected meat. Whereas the previous infection IgG antibody was found in donors aged 41-50 years, this indicates that the donors in this age group had previously been infected by the infective agent toxoplasma parasite, which causes an immune response and the formation of memory cells for the parasite [19]. The IgM antibody was in the middle age group, meaning the donors in this group had a recent infection by T. gondii. This infection may have come from drinking contaminated water or vegetables or from eating raw infected meat. Whereas the previous infection IgG antibody was found in donors aged 41-50 years, this indicates that the donors in this age group had previously been infected by the infective agent toxoplasma parasite, which causes an immune response and the formation of memory cells for the parasite. The results revealed that th IgM antibody was in the middle age group, indicating that the donors in this group had recently been infected with T. gondii. This infection could have been contracted by drinking contaminated water or vegetables or by eating raw infected meat. Previous infection IgG antibodies were found in donors aged 41-50 years, indicating that these donors had previously been infected by the infective agent toxoplasma parasite, which causes an immune response and the formation of memory cells for the parasite [20]. The results revealed that the prevalence of T. gondii IgG level among 560 tested blood donors males was (43.03%) and among 40 tested females donors was (30%). On the other the incidence rate of T. gondii IgM level among 560 tested males’ donors was 95 (16.96%) and among 40 tested female’s donors was (7.55%). Different previous studies showed that males are more susceptible than females to many parasites. The current study disagree with in Iran, Davarpanah, et al., who showed that the seroprevalence of toxoplasmosis was higher in males than in female [21]. This variability may be due to different sample size, geographical location, type of kit used and the resistance of different strains of T. gondii that plays an important role in differences of infection rates. Also animal petting and exposure to contaminated soil is another reseons for infection. In Iran, Davarpanah, et al., revealed seroprevalence of toxoplasmosis was (48.8%) in males and (55.2%) in females. Toxoplasmosis in those without job which showed included in this study, higher percentage 51 (48.6%) than those having governmental workers 132 (43.0%), private workers was 53 (42.1%) and student 17 (27.4%) in the presence of antitoxoplasma IgG antibodies. While the presence of antitoxoplasma IgM antibodies, this result revealed higher percentage 13 (20.96%) in student and 23 (18.25%) in private workers, without job19 (18.09) and 43 (14.0%) in those having governmental workers. In Iraq, found that all seropositive rate was (33.42%), barbers had the highest prevalence rate (72.73%), followed by food handlers (41.18 %), housewives (38.9 %), donated blood (24.30 %) and medical staff (21.43%). Davarpanah, et al. [21]. Farmers had the highest anti- Toxoplasma antibody rate (47.4%), according to Davarpanah, et al., compared to other occupations (clerks, 31%; teachers, 42.1%; students, 21.2% and workers, 37.5%) [22]. These findings could be explained by the fact that farmers were more likely to be uneducated or that their exposure to soil and other risk factors was greater than that of others. Cook, et al., found that contact with soil, contaminated vegetables and fruit were identified as a risk factor for Toxoplasma infection which was confirmed by Buffolano, et al. indicated that seroprevalence Toxoplasma antibodies was significantly higher amongst individuals who keep livestock (52.2%) and abattoir workers (46.3%) and he suggested exposure to T. gondii infection is present among residents of Tanga district in Tanzania whom consume raw meat or under cooked meat and petting especially cats that presents more risk factors than other occupational groups. He also emphasized on the necessity to create awareness of this disease and advocate protection of risky In Iran Davarpanah, et al. revealed the demographic and base line characteristics of occupation were clerks (20%) merchant (58.6%) students (33.3%) unemployed (50%) other jobs (48.91%). Zhou, et al. in China showed that some occupations was from required people to have contact with animals and meats and these frequently posses higher risk of infection with the parasite. Such as dairy workers (45.0%) slaughter house workers (25.6%) veterinarians (12.5%), meat processing workers (13.7%) meat sellers and cooks (29.7%). Another investigators demonstrated that out of the 200 fruit and vegetable workers, 15 (7.5%) of them were positive for anti-Toxoplasma IgG antibodies while, anti-Toxoplasma IgM, antibodies were found in 2 (1%) of the fruit workers [23]. It is important to note that the current study discovered an association between the blood group system and Toxoplasma infection, with the highest prevalence among samples tested by ELISA IgG with blood group AB+(60%) and the lowest prevalence among samples tested by group O-19 (25.8%). On the other hand, ELISA IgM antibodies test showed highly toxoplasmosis percentage 28 (24.3%) with blood group B+ and lowest percentage 0 (0.0%) in AB- blood group. A study among blood donors in Russia has reported similar findings, with toxoplasmosis seroprevalence being twice as high among subjects with blood group AB (54%) than among subjects with blood group O (27%) [24]. Other studies report no significant difference between toxoplasmosis and the ABO factor [25]. The A, B and O blood group system are determined by the presence or absence of A and B carbohydrate antigens on the surface of red blood cells. This determines natural resistance in human to many infection disease agents that have cell surface antigens similar to the antigens of different blood group types. This mechanism may, in part, explain the higher susceptibility of individual with blood type AB to several infections diseases, since the blood of those individuals does not contain the corresponding natural antibodies. Previous studies have interpreted and reported the possible relationship between the ABO group system and the presence of anti-T. gondii antibodies. Such as an association between this parasite infection and the B and AB blood groups, these studies suggest that the B antigen could be a T. gondii receptor. However, other similar investment organizations on the other hand, found no evidence of this association [26]. It has been proposed that B antigen represents a T. gondii receptor, which did not appear to be valid in different populations [27]. The results reveald that seroprevalence of T. gondii IgG in Libyan tested 544 was 233 (42.8%) and non-Libyan tested 56 were 20 (35.7%) and the seroprevalence of T. gondii IgM in Libyan tested 544 was 91 (16.7%) and non-Libyan tested 56 was 7 (12.5%). The seroprevalence rate of infection IgG and IgM antibodies were highest in Libyan than non-Libyan. In this study, the seroprevalence of T. gondii IgG and IgM antibodies in correlation to the region are shown that the seroprevalence of T. gondii IgG in Benghazi (urban) was (43.1%) and Benghazi (rural) was (39.45%) and the seroprevalence of T. gondii IgM in Benghazi was (17.4%) and out of Benghazi was 19 (12.9%). This result was consistent with the study conduct by Munoz, et al. which was about the positive cases of toxoplasmosis in the rural and urban women was (63.4%) and (54.5%) respectively. Munoz, et al. mentioned that, the ratio of infection between rural women is greater than urban women, Salibay, et al. in Philippines, where they showed that the rate of toxoplasmosis was higher in suburban patients than urban residents. Another study by Zoe, et al. in Romania found that higher seropositivity of toxoplasmosis was in rural environments (63.68%) compared to urban one (55.12%) Sroka, et al. [28]. In Poland, they showed that people living on farms had a significantly higher percentage of anti- Toxoplasma antibodies (59% compared to urban dwellers 41.0%). Al-Mayahi in his study has noticed the same results in the presence of higher anti-toxoplasma antibodies in women lived in rural area in comparison to those lived in urban area. Therefore the difference in seropositivity between rural and urban area may be due to the hygienic and socio economic status that relates to oocyst shedding by cats and peoples contact with the soil, specifically, the pavement widely seen in the urban area is considered to contribute to the reduced surviving period of oocysts shed by cats, interpreted that, the people in the rural regions had a history of contact with cats as well as the ingestion of the oocysts with the inadequate washing of vegetables, in addition to the increase of domestic animals which are regarded as good carriers of the disease [29].

Conclusion

In Libya, healthy voluntary donors had a high seroprevalence of T. gondii, according to our findings. Regular blood testing for T. gondii antibodies may be regarded as a necessary component of the battery of serological screening tests used to identify endemic infectious diseases in our nation. Additionally, it may be appropriate to incorporate screening tests (ELISA) for T. gondii into the routine blood testing performed prior to transfusion, especially since many pregnant women are exposed to a lack of blood, which necessitates a blood transfusion, which negatively affects both the mother and fetus, so it is necessary to take these tests into consideration.

References

1. Hill DE, Chirukandoth S, Dubey JP (2005) Biology and epidemiology of Toxoplasma gondii in man and animals. Anim Health Res Rev 6:41-61

   [Crossref] [Googlescholar] [Indexed]

2. Sukthana Y (2006) Toxoplasmosis: beyond animals to humans. Trends Parasitol 22:137-142

   [Crossref] [Googlescholar] [Indexed]

3. Robert-Gangneux F, Darde ML (2012) Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev 25:264-96

   [Crossref] [Googlescholar] [Indexed]

4. Tenter AM, Heckeroth AR, Weiss LM (2000) Toxoplasma gondii from animals to humans. Int J Parasitol 30:1217-1258

   [Crossref] [Googlescholar] [Indexed]

5. Siegel SE, Lunde MN, Gelderman AH, Halterman RH, Brown JA, et al. (1971) Transmission of toxoplasmosis by leukocyte transfusion. Blood 37:388-394

   [Googlescholar] [Indexed]

6. Sundar P, Mahadevan A, Jayshree RS, Subbakrishna DK, Shankar SK (2007) Toxoplasma seroprevalence in healthy voluntary blood donors from urban Karnataka. Indian J Med Res 126:50-55

   [Googlescholar] [Indexed]

7. Abdel-Hameed AA (1991) Sero-epidemiology of toxoplasmosis in Gezira, Sudan. J Trop Med Hyg 94:329-32

   [Googlescholar] [Indexed]

8. Villena I, Chemla C, Quereux C, Dupouy D, Leroux B, et al. (1998) Prenatal diagnosis of congenital toxoplasmosis transmitted by an immunocompetent woman infected before conception. Reims Toxoplasmosis Group. Prenat Diagn 18:1079-1081

   [Crossref] [Googlescholar] [Indexed]

9. Stagno S (1980) Congenital toxoplasmosis. Am J Dis Child 134:635-637
10. Khalil M, Aziz K, Ahmed A (2012) Sero-prevalence of Toxoplasma gondii infection in humans in Khartoum State, Sudan. Int J Trop Med 7:143-150
11. Han K, Shin DW, Lee TY, Lee YH (2008) Seroprevalence of Toxoplasma gondii infection and risk factors associated with seropositivity of pregnant women in Korea. J Parasitol 94:963-965

    [Crossref] [Googlescholar] [Indexed]

12. Amari OM (1994) Prevalence of antibodies to Toxoplasma gondii among blood donors in Abha, Asir Region, South-Western Saudi Arabia. J Egypt Public Health Assoc 69:77-88

    [Googlescholar] [Indexed]

13. Remington JS, Mcleod R, Thulliez P (2001) Infectious diseases of the fetus and newborn infant. J Egypt Public Health Assoc 205-346
14. Pinlaor S, Ieamviteevanich K, Pinlaor P, Maleewong W, Pipitgool V (2000) Seroprevalence of specific total Immunoglobulin (Ig), IgG and IgM antibodies to Toxoplasma gondii in blood donors from Loei province, Northeast Thailand. Southeast Asian J Trop Med Public Health 31:123-127

    [Googlescholar] [Indexed]

15. Jasim AN (1979) Seroepidemiological studies on toxoplasmosis in Iraq, evaluation of serological tests used in diagnosis. Southeast Asian J Trop Med Public Health 82
16. Yaneza A, Kumari P (1994) Prevalence of toxoplasma antibodies in blood donors in Al-Hassa. Ann Saudi Med 14:230-232

    [Crossref] [Googlescholar] [Indexed]

17. Smith KL, Wilson M, Hightower AW, Kelley PW, Struewing JP, et al. (1996) Prevalence of Toxoplasma gondii antibodies in US military recruits in 1989: Comparison with data published in 1965. Clin Infect Dis 23:1182-1183

    [Crossref] [Googlescholar] [Indexed]

18. Suzuki Y, Joh, K (1994) Effect of the strain of Toxoplasma gondii on the development of toxoplasmic encephalitis in mice treated with antibody to interferon-gamma. Parasitol Res 80:125-130

    [Crossref] [Googlescholar] [Indexed]

19. Davarpanah MA, Mehrabani D, Neirami R, Ghahremanpoori M, Darvishi (2007) Toxoplasmosis in HIV⁄AID patient in Shiraz, southern Iran. Iranian Red Crescent Med J 9:22-27

    [Googlescholar]

20. Cook AJ, Gilbert RE, Buffolano W, Zufferey J, Petersen E, et al. (2000) Sources of toxoplasma infection in pregnant women: European multicentre case-control study. European Research Network on Congenital Toxoplasmosis. BMJ 321:142-147

    [Crossref] [Googlescholar] [Indexed]

21. Buffolano W, Gilbert RE, Holland FJ, Fratta D, Palumbo F, et al. (1996) Risk factors for recent toxoplasma infection in pregnant women in Naples. Epidemiol Infect 116:347-351

    [Crossref] [Googlescholar] [Indexed]

22. Alvarado-Esquivel C, Liesenfeld O, Estrada-Martinez S, Felix-Huerta J (2011) Toxoplasma gondii infection in workers occupationally exposed to raw meat. Occup Med 61:265-269

    [Crossref] [Googlescholar] [Indexed]

23. Henry SM (2001) Molecular diversity in the biosynthesis of GI tract glycoconjugates. A blood-group-related chart of microorganism receptors. Transfus Clin Biol 8:226-230

    [Crossref] [Googlescholar] [Indexed]

24. Rodrigues A, Uezatos S, Vono M, Pandossio T, Spegiorin LCJF, et al. (2011) Association between anti Toxoplasma gondii antibodies ABO blood group system. J venom Anim Toxins incl Trop Dis 17:184-189

    [Googlescholar] [Indexed]

25. Gill HS (1985) Occurrence of Toxoplasma gondii antibodies in Tanzanian blood donors. East Afr Med J 62:585-588

    [Googlescholar] [Indexed]

26. Munoz-Zanzi C, Campbell C, Berg S (2016) Seroepidemiology of toxoplasmosis in rural and urban communities from Los Rios Region, Mar. Infect Ecol Epidemiol 6:30597

    [Crossref] [Googlescholar] [Indexed]

27. Salibay CC, Dung CA, Claveria FG (2008) Serological survey of Toxoplasma gondii infection among urban. (Manila) and suburban (Dasmarinas, cavite) Residents, Philippines. J proto zool Res 18:26-33

    [Crossref] [Googlescholar] [Indexed]

28. Coroiu Z, Radu R, Molnar A, Bele J (2009) Seroprevalence of anti-Toxoplasma gondii antibodies in the healthy population from North-Western and central Romania. Sci Parasite 1:37-42

    [Googlescholar]

29. Sroka J, Wojcik-Fatla A, Dutkiewicz J, Zajac V, Zajac V, et al. (2010) The occurrence of Toxoplasma gondii infection in people and animals from rural environment of Lublin region-estimate of potential role of water as a source of infection. Ann Agric Environ Med 17:125-132

    [Googlescholar] [Indexed]