Abstract
We aimed to determine the association between the seropositivity to Toxoplasma gondii and the ABO and Rh blood groups in 2,053 people. ABO and Rhesus blood groups and anti-T. gondii IgG and IgM antibodies were determined using commercially available assays. Of the 2,053 people studied, 171 (8.3%) were positive for anti-T. gondii IgG antibodies. Sixty-five (38.0%) and 36 (21.1%) of these 171 individuals had high anti-T. gondii IgG antibody levels (≥150 IU mL−1) and anti-T. gondii IgM antibodies, respectively. We found the following prevalences of T. gondii infection among the ABO groups: 8.5% in group A, 4.3% in group B, 4.7% in group AB, and 8.9% in group O (P = 0.19). The prevalences of T. gondii infection among Rh groups were: 8.4% in the Rh-positive group and 7.1% in the Rh-negative group (P = 0.58). Logistic regression analysis showed that the frequencies of ABO and Rh blood groups were similar (P > 0.05) among people with positive and negative serology for anti-T. gondii IgG antibodies, with high (≥150 IU mL−1) and lower (<150 IU mL−1) levels of anti-T. gondii IgG antibodies, and with positive and negative serology for anti-T. gondii IgM antibodies. Results does not support an association between T. gondii infection and ABO and Rh blood groups.
Introduction
Toxoplasmosis is the disease caused by the protozoan parasite Toxoplasma gondii (T. gondii) [1]. Infections with T. gondii occurs in all warm-blooded animals including humans [2], and these infections are common worldwide [3]. Major sources of foodborne transmission of T. gondii for humans include ingestion of undercooked meat, especially pork, lamb, and wild game meat, and soil contaminated with cat feces on raw fruits and vegetables [4]. Primary infection with T. gondii in pregnant women can lead to vertical transmission resulting in congenital toxoplasmosis [5]. This congenital disease may result in mild to deep injuries occurring in the newborn or later in its development or in adolescence [6]. Infections with T. gondii cause no clinical signs in 80% of cases in immunocompetent people, causing immunization characterized by the persistence of cysts in brain, muscles, and retina [7]. Reactivation of latent infections in immunocompromised patients can cause life-threatening encephalitis [8]. Infections with T. gondii have been associated with suicide attempts [9, 10], schizophrenia [11, 12], mixed anxiety and depressive disorder [13], and obsessive-compulsive disorder [14].
The ABO blood groups system consists of four types (A, B, AB, and O) [15]. Antigens of this blood group system are not confined to red cells but are widely expressed in body fluid and tissues [16]. Rh blood group system consists of two types (Rh-negative and Rh-positive), has at least 45 independent antigens, and next to the ABO system, is the most clinically significant in transfusion medicine [17]. ABO and Rh blood groups have been linked to several bacterial, viral, and parasitic infections and severity of disease, and there are excellent reviews of this topic [15–18]. Few studies to determine the association between ABO and Rh blood groups and infection with T. gondii have been reported. Results of these studies are conflictive. For instance, in a study of military personnel in the Czech Republic, multivariate analysis showed that blood group types A, B, or AB vs, O were independent predictors of T. gondii seropositivity [19]. In a study of women with miscarriages, a significant relation between Rh blood group and T. gondii seropositivity was found while no significant relationship was observed between ABO blood groups and toxoplasmosis [20]. In a Brazilian study of pregnant women, no association between anti-T. gondii antibodies and ABO blood groups was found [21]. Therefore, we sought to determine the association between the presence of anti-T. gondii antibodies and the ABO and Rh blood groups in a sample of people in Durango City, Mexico.
Materials and methods
Study design and study population
A cross sectional study of 2,053 people in Durango, Mexico was performed. The inclusion criteria for enrollment of participants in the study were: people attending public health care centers in Durango, Mexico; aged 15 years and older, who voluntarily accepted to participate. Participants were enrolled from June 2014 to May 2018. Their mean age was 40.3 ± 12.8 years (range: 15–84 years).
Laboratory tests
A blood sample was obtained from each participant and tested for ABO and Rh blood groups using commercially available kits (Dominion Biological Limited, Nova Scotia, Canada). In addition, blood samples were centrifuged, and sera obtained was kept frozen at −20 °C until analyzed. Serum samples were tested for anti-T. gondii IgG antibodies using a commercially available enzyme immunoassay “T. gondii IgG” kit (Diagnostic Automation/Cortez Diagnostics, Inc., Woodland Hills, California. USA). Those sera positive for anti-T. gondii IgG antibodies were additionally tested for anti-T. gondii IgM antibodies by a commercially available enzyme immunoassay “T. gondii IgM” kit (Diagnostic Automation/Cortez Diagnostics, Inc.).
Statistical analysis
Statistical analysis was performed with the aid of the software SPSS for windows version 15.0 (SPSS Inc. Chicago, IL. USA). For calculation of the sample size we used 654,876 as the size of population from which the sample was selected, a reference seroprevalence of 4.2% of AB blood group [21], a confidence level of 95%, and a precision of 1.0%. The result of the calculation was 1,543 subjects. Comparison of the frequency of T. gondii infection among the groups was performed using the Chi-squared and the Fisher's exact tests. The association between the seropositivity to T. gondii and the ABO and Rh blood groups was determined using unconditional logistic regression analysis with calculation of odds ratios (OR) and 95% confidence intervals (CI). Adjusted by age and sociodemographic variables with a P < 0.05 obtained in the bivariate analysis was used in the logistic regression analysis. A P < 0.05 was considered as statistically significant.
Ethical aspects
This study was approved by the Institutional Ethical Committee of the General Hospital of the Secretary of Health in Durango City, Mexico. Participation in the study was voluntary. A written informed consent was obtained from all participants and from the next of kin of minor participants.
Results
Of the 2,053 people studied, 171 (8.3%) were positive for anti-T. gondii IgG antibodies. Sixty-five (38.0%) of these 171 individuals had high anti-T. gondii IgG antibody levels (≥150 IU mL−1). Thirty-six (21.1%) of these 171 IgG positive individuals were also positive for anti-T. gondii IgM antibodies. General sociodemographic characteristics of the study population and the seroprevalence of T. gondii infection is shown in Table 1. Seroprevalence of T. gondii infection varied significantly with birthplace, residence area, education, and socioeconomic status of the study population.
Socio-demographic characteristics of participants and prevalence of T. gondii infection
| Characteristic | Participants tested | Prevalence of T. gondii infection | P value | |
| No. | No. | % | ||
| Age groups (years) | ||||
| 30 or less | 461 | 32 | 6.9 | 0.37 |
| 31–50 | 1,141 | 103 | 9.0 | |
| >50 | 451 | 36 | 8.0 | |
| Gender | ||||
| Male | 351 | 31 | 8.8 | 0.70 |
| Female | 1,702 | 140 | 8.2 | |
| Birthplace | ||||
| Durango State | 1,816 | 138 | 7.6 | 0.001 |
| Other Mexican State | 225 | 33 | 14.7 | |
| Abroad | 9 | 0 | 0.0 | |
| Residence place | ||||
| Durango State | 2,031 | 169 | 8.3 | 0.72 |
| Other Mexican State | 16 | 2 | 12.5 | |
| Abroad | 3 | 0 | 0.0 | |
| Residence area | ||||
| Urban | 1,633 | 109 | 6.7 | 0.00 |
| Suburban | 249 | 38 | 15.3 | |
| Rural | 163 | 22 | 13.5 | |
| Educational level | ||||
| No education | 20 | 6 | 30.0 | 0.00 |
| 1–6 years | 279 | 40 | 14.3 | |
| 7–12 years | 1,033 | 78 | 7.6 | |
| >12 years | 714 | 46 | 6.4 | |
| Occupation | ||||
| Agriculture | 20 | 3 | 15.0 | 0.13 |
| Housewife | 786 | 79 | 10.1 | |
| Business | 102 | 6 | 5.9 | |
| Construction | 7 | 2 | 28.6 | |
| Employee | 520 | 42 | 8.1 | |
| Student | 97 | 3 | 3.1 | |
| Cattle raising | 4 | 1 | 25.0 | |
| Day laborer | 1 | 0 | 0.0 | |
| Factory worker | 15 | 2 | 13.3 | |
| Professional | 314 | 18 | 5.7 | |
| Miner | 12 | 2 | 16.7 | |
| Sex worker | 2 | 0 | 0.0 | |
| None | 45 | 3 | 6.3 | |
| Other | 123 | 9 | 7.3 | |
| Socio-economic status | ||||
| Low | 514 | 65 | 12.6 | 0.00 |
| Medium | 1,525 | 105 | 6.9 | |
| High | 7 | 1 | 14.3 | |
The ABO blood groups found in the 2,053 participants were as follows: group A in 448 (21.8%) individuals, group B in 162 (7.9%), group AB in 43 (2.1%), and group O in 1,400 (68.2%). Whereas the Rh-positive and Rh-negative groups were found in 1,899 (92.5%) and 154 (7.5%) individuals, respectively. We found the following prevalences of T. gondii infection among the ABO groups: 8.5% in group A, 4.3% in group B, 4.7% in group AB, and 8.9% in group O. No statistically significant difference in the seroprevalence of T. gondii infection among the ABO groups was found (P = 0.19). Whereas the prevalences of T. gondii infection among Rh groups were: 8.4% in the Rh-positive group and 7.1% in the Rh-negative group (P = 0.58). The frequencies of high (≥150 IU mL−1) anti-T. gondii IgG antibody levels among the ABO blood groups were: 3.8% in group A, 0.6% in group B, 0.0% in group AB, and 3.4% in group O (P = 0.13). Individuals with Rh-positive and Rh-negative blood groups had a similar (3.2%) frequency of high anti-T. gondii IgG antibody levels (P = 0.95). The frequencies of IgM positive serology among the ABO groups in the 171 individuals who were positive for anti-T. gondii IgG antibodies were as follows: 26.3% in group A, 14.3% in group B, 50.0% in group AB, and 19.4% in group O (P = 0.56). Whereas the frequencies of IgM positive serology among the Rh groups were 21.3% in Rh-positive group and 18.2% in Rh-negative group (P = 1.00). Further analysis using logistic regression with adjustment by age, sex, birthplace, residence area, education, and socioeconomic status showed that the frequencies of ABO and Rh blood groups were similar among people with positive and negative serology for anti-T. gondii IgG antibodies (Table 2), with high (≥150 IU mL−1) and lower (<150 IU mL−1) levels of anti-T. gondii IgG antibodies (Table 3), and with positive and negative serology for anti-T. gondii IgM antibodies (Table 4).
Distribution of ABO and Rh blood groups and seroreactivity to T. gondii in the population studied
| Blood group | People studied | Positive serology to T. gondii | Negative serology to T. gondii | OR* | 95% CI | P | ||
| No. | No. | % | No. | % | ||||
| ABO group | ||||||||
| A | 448 | 38 | 22.2 | 410 | 21.8 | 1.08 | 0.73–1.59 | 0.68 |
| B | 162 | 7 | 4.1 | 155 | 8.2 | 0.46 | 0.20–1.07 | 0.07 |
| AB | 43 | 2 | 1.2 | 41 | 2.2 | 0.52 | 0.1–2.20 | 0.37 |
| O | 1,400 | 124 | 72.5 | 1,276 | 67.8 | 1.18 | 0.82–1.69 | 0.35 |
| Total | 2,053 | 171 | 8.3 | 1,882 | 91.7 | |||
| Rh group | ||||||||
| Negative | 154 | 11 | 6.4 | 143 | 7.6 | 0.78 | 0.41–1.50 | 0.46 |
| Positive | 1,899 | 160 | 93.6 | 1,739 | 92.4 | |||
*Adjusted by age, sex, birthplace, residence area, education, and socioeconomic status using logistic regression.
Distribution of ABO and Rh blood groups and rate of high (≥150 IU mL−1) anti-T. gondii IgG antibody levels in the population studied
| Blood group | People studied | ≥150 IU mL−1 | <150 IU mL−1 | OR* | 95% CI | P | ||
| anti-T. gondii | anti-T. gondii | |||||||
| IgG levels | IgG levels | |||||||
| No. | No. | % | No. | % | ||||
| ABO group | ||||||||
| A | 448 | 17 | 26.2 | 431 | 21.7 | 1.44 | 0.80–2.56 | 0.21 |
| B | 162 | 1 | 1.5 | 161 | 8.1 | – | – | |
| AB | 43 | 0 | 0 | 43 | 2.2 | – | – | |
| O | 1,400 | 47 | 72.3 | 1,353 | 68.1 | 1.12 | 0.63–1.98 | 0.70 |
| Total | 2,053 | 65 | 3.2 | 1,988 | 96.8 | |||
| Rh group | ||||||||
| Negative | 154 | 5 | 7.7 | 149 | 7.5 | 0.99 | 0.38–2.57 | 0.99 |
| Positive | 1,899 | 60 | 92.3 | 1,839 | 92.5 | |||
*Adjusted by age, sex, birthplace, residence area, education, and socioeconomic status using logistic regression.
Distribution of ABO and Rh blood groups and positivity to anti-T. gondii IgM antibodies in the population studied
| Blood group | People studied | Positive serology for | Negative serology for | OR* | 95% CI | P | ||
| anti-T. gondii IgM | anti-T. gondii IgM | |||||||
| No. | No. | % | No. | % | ||||
| ABO group | ||||||||
| A | 38 | 10 | 27.8 | 28 | 20.7 | 1.71 | 0.68–4.25 | 0.24 |
| B | 7 | 1 | 2.8 | 6 | 4.4 | 0.49 | 0.04–5.46 | 0.56 |
| AB | 2 | 1 | 2.8 | 1 | 0.7 | 4.96 | 0.21–113.6 | 0.31 |
| O | 124 | 24 | 66.7 | 100 | 74.1 | 0.60 | 0.25–1.46 | 0.26 |
| Total | 171 | 36 | 21.1 | 135 | 78.9 | |||
| Rh group | ||||||||
| Negative | 11 | 2 | 5.6 | 9 | 6.7 | 1.00 | 0.17–5.78 | 0.99 |
| Positive | 160 | 34 | 94.4 | 126 | 93.3 | |||
*Adjusted by age, sex, birthplace, residence area, education, and socioeconomic status using logistic regression.
Discussion
The clinical significance of the ABO blood group system extends beyond the immunohematology [22]. Associations between ABO blood groups and diseases including infectious diseases have been reported [16]. ABO blood groups have been associated with parasitic, bacterial, and viral infections; for instance: malaria, cholera, Helicobacter pylori infection, and norovirus infection [16, 22]. However, the link between T. gondii infection and ABO and Rh blood groups has been scantily studied, and studies about this link have reported conflicting results. The antigens of the ABO blood group system are complex carbohydrate molecules expressed on the surface of red blood cells along with a variety of human cells and tissues including the epithelium, sensory neurons, platelets, and the vascular endothelium [22]. Infection with T. gondii occurs through the gastrointestinal tract where the expression of the ABO blood groups glycoconjugates also occurs and thus ABO blood groups may influence the human susceptibility of this infection [21]. The combined action of glycosyltransferases encoded by genes from the human ABO, Lewis, and Secretor histo-blood group systems strongly influences cell, tissue, mucosa, and exocrine secretion carbohydrate phenotypes, including those serving as habitat for mutualistic and pathogenic microorganism [23]. Therefore, we determined the association between T. gondii infection and ABO and Rh blood groups in a large sample of people in Durango, Mexico. We found that the frequencies of anti-T. gondii IgG seropositivity, high anti-T. gondii IgG antibody levels, and anti-T. gondii IgM antibodies were similar among ABO and Rh blood groups. Comparisons were adjusted by sociodemographic variables including age, gender, birthplace, residence area, education, and socioeconomic status of the study population using logistic regression analysis. Therefore, results of our study do not support an association between T. gondii seropositivity and ABO and Rh blood groups. Our results agree with those reported in a study of 1,006 pregnant women in Brazil, where researchers found that the frequencies of ABO blood groups phenotypes where similar in women with and without anti-T. gondii antibodies [21]. In a study of blood donors in Ivoire Coast, West Africa, investigators found that the presence of anti-T. gondii IgG and IgM antibodies was not linked to the blood group [24]. In addition, in a study of women with miscarriages, no significant relationship between ABO blood groups and toxoplasmosis was found [20]. Furthermore, a recent study of pregnant women in Sudan showed that the ABO blood group system was not related to the absence or presence of anti-T. gondii antibodies [25]. In contrast our results conflict with those found in a study of military personnel in Prague, Czech Republic, where multivariate analysis showed that blood group type A, B, or AB vs. O were independent predictors of T. gondii seropositivity [19]. Our results also conflict with a significant relation between Rh blood group and T. gondii seropositivity found in a study of women with miscarriages [20]. However, our results agree with those reported in a meta-analysis that included 10,910 people of 21 studies and showed that no significant association was found between anti-T. gondii antibodies and Rh blood group [24]. In such meta-analysis researchers studied individuals of 3 continents including Asia, Europe and Africa but there was no available data on America and Australia [26]. Blood group systems other than the ABO system have been assessed on their association with T. gondii infection. In a recent study, researchers assessed the association between T. gondii infection and the Duffy blood group system and found that phenotypes and antigens of this blood group system do not constitute risk factors for infection by T. gondii and the development of ocular toxoplasmosis [27]. In a study of pregnant women in Brazil, investigators showed that the Lewisb profile appears to protect against T. gondii infection [28].
A limitation of the study was a low number of cases with B and AB blood groups. Further studies to determine the association between T. gondii infection and B and AB blood groups with larger sample sizes are need.
Conclusion
Results of the present study indicate that T. gondii infection is not associated with ABO and Rh blood groups.
Funding
This research study was funded by Juárez University of Durango State, Mexico.
Author's contributions
ARPA, ARN, CAGA, and SMCS obtained samples and data of the study population. ARPA, MAD, ASA, SEM, and RGI performed the data analysis. SEM performed the statistical analysis. CAE performed study concept and design, laboratory tests, data analysis, and wrote the manuscript.
Conflicts of interest
The authors declare that no conflict of interest exists.
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