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Alma Rosa Pérez-Álamos Institute for Scientific Research “Dr. Roberto Rivera-Damm”, Juárez University of Durango State, Durango, Mexico

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Marisela Aguilar-Durán Institute for Scientific Research “Dr. Roberto Rivera-Damm”, Juárez University of Durango State, Durango, Mexico

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Sergio Estrada Martínez Institute for Scientific Research “Dr. Roberto Rivera-Damm”, Juárez University of Durango State, Durango, Mexico

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Agar Ramos-Nevárez Clínica de Medicina Familiar, Instituto de Seguridad y Servicios Sociales de los Trabajadores del Estado, Durango, Mexico

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Carlos Alberto Guido-Arreola Clínica de Medicina Familiar, Instituto de Seguridad y Servicios Sociales de los Trabajadores del Estado, Durango, Mexico

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Antonio Sifuentes-Álvarez Biomedical Research Laboratory, Faculty of Medicine and Nutrition, Juárez University of Durango State, Durango, Mexico

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Sandra Margarita Cerrillo-Soto Clínica de Medicina Familiar, Instituto de Seguridad y Servicios Sociales de los Trabajadores del Estado, Durango, Mexico

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Raúl Graciano Ibarra Biomedical Research Laboratory, Faculty of Medicine and Nutrition, Juárez University of Durango State, Durango, Mexico

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Cosme Alvarado-Esquivel Biomedical Research Laboratory, Faculty of Medicine and Nutrition, Juárez University of Durango State, Durango, Mexico

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Open access

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.

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.

Table 1.

Socio-demographic characteristics of participants and prevalence of T. gondii infection

CharacteristicParticipants testedPrevalence of T. gondii infectionP value
No.No.%
Age groups (years)
 30 or less461326.90.37
 31–501,1411039.0
 >50451368.0
Gender
 Male351318.80.70
 Female1,7021408.2
Birthplace
 Durango State1,8161387.60.001
 Other Mexican State2253314.7
 Abroad900.0
Residence place
 Durango State2,0311698.30.72
 Other Mexican State16212.5
 Abroad300.0
Residence area
 Urban1,6331096.70.00
 Suburban2493815.3
 Rural1632213.5
Educational level
 No education20630.00.00
 1–6 years2794014.3
 7–12 years1,033787.6
 >12 years714466.4
Occupation
 Agriculture20315.00.13
 Housewife7867910.1
 Business10265.9
 Construction7228.6
 Employee520428.1
 Student9733.1
 Cattle raising4125.0
 Day laborer100.0
 Factory worker15213.3
 Professional314185.7
 Miner12216.7
 Sex worker200.0
 None4536.3
 Other12397.3
Socio-economic status
 Low5146512.60.00
 Medium1,5251056.9
 High7114.3

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).

Table 2.

Distribution of ABO and Rh blood groups and seroreactivity to T. gondii in the population studied

Blood groupPeople studiedPositive serology

to T. gondii
Negative serology

to T. gondii
OR*95% CIP
No.No.%No.%
ABO group
 A4483822.241021.81.080.73–1.590.68
 B16274.11558.20.460.20–1.070.07
 AB4321.2412.20.520.1–2.200.37
 O1,40012472.51,27667.81.180.82–1.690.35
Total2,0531718.31,88291.7
Rh group
 Negative154116.41437.60.780.41–1.500.46
 Positive1,89916093.61,73992.4

*Adjusted by age, sex, birthplace, residence area, education, and socioeconomic status using logistic regression.

Table 3.

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 groupPeople

studied
≥150 IU mL−1<150 IU mL−1OR*95% CIP
anti-T. gondiianti-T. gondii
IgG levelsIgG levels
No.No.%No.%
ABO group
 A4481726.243121.71.440.80–2.560.21
 B16211.51618.1
 AB4300432.2
 O1,4004772.31,35368.11.120.63–1.980.70
Total2,053653.21,98896.8
Rh group
 Negative15457.71497.50.990.38–2.570.99
 Positive1,8996092.31,83992.5

*Adjusted by age, sex, birthplace, residence area, education, and socioeconomic status using logistic regression.

Table 4.

Distribution of ABO and Rh blood groups and positivity to anti-T. gondii IgM antibodies in the population studied

Blood groupPeople

studied
Positive serology forNegative serology forOR*95% CIP
anti-T. gondii IgManti-T. gondii IgM
No.No.%No.%
ABO group
 A381027.82820.71.710.68–4.250.24
 B712.864.40.490.04–5.460.56
 AB212.810.74.960.21–113.60.31
 O1242466.710074.10.600.25–1.460.26
Total1713621.113578.9
Rh group
 Negative1125.696.71.000.17–5.780.99
 Positive1603494.412693.3

*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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The author instruction is available in PDF.
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Senior editors

Editor(s)-in-Chief: Dunay, Ildiko Rita

Editor(s)-in-Chief: Heimesaat, Markus M.

Editorial Board

  • Berit Bangoura (University of Wyoming, USA)
  • Stefan Bereswill (Charité - University Medicine Berlin, Germany)
  • Dunja Bruder (University of Magdeburg, Germany)
  • Jan Buer (University of Duisburg, Germany)
  • Edit Buzas (Semmelweis University, Hungary)
  • Renato Damatta (UENF, Brazil)
  • Maria Deli (Biological Research Center, HAS, Hungary)
  • Olgica Djurković-Djaković (University of Belgrade, Serbia)
  • Jean-Dennis Docquier (University of Siena, Italy)
  • Zsuzsanna Fabry (University of Washington, USA)
  • Ralf Ignatius (Charité - University Medicine Berlin, Germany)
  • Achim Kaasch (Otto von Guericke University Magdeburg, Germany)
  • Oliver Liesenfeld (Roche, USA)
  • Matyas Sandor (University of Wisconsin, USA)
  • Ulrich Steinhoff (University of Marburg, Germany)
  • Michal Toborek (University of Miami, USA)
  • Susanne A. Wolf (MDC-Berlin, Germany)

 

Dr. Dunay, Ildiko Rita
Magdeburg, Germany
E-mail: ildiko.dunay@med.ovgu.de

Indexing and Abstracting Services:

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2022  
Web of Science  
Total Cites
WoS
717
Journal Impact Factor 2.2
Rank by Impact Factor

n/a

Impact Factor
without
Journal Self Cites
2.2
5 Year
Impact Factor
2.8
Journal Citation Indicator 0.66
Rank by Journal Citation Indicator

Microbiology (Q2)

Scimago  
Scimago
H-index
11
Scimago
Journal Rank
0.614
Scimago Quartile Score Microbiology (Q3)
Microbiology (medical) (Q3)
Immunology and Allergy (Q3)
Immunology (Q3)
Scopus  
Scopus
Cite Score
8.3
Scopus
CIte Score Rank
Microbiology 33/163 (80th PCTL)
Microbiology (medical) 28/124 (77th PCTL)
Immunology and Allergy 63/211 (70th PCTL)
Immunology 69/217 (68th PCTL)
Scopus
SNIP
1.221

 

2021  
Web of Science  
Total Cites
WoS
790
Journal Impact Factor not applicable
Rank by Impact Factor not applicable
Impact Factor
without
Journal Self Cites
not applicable
5 Year
Impact Factor
not applicable
Journal Citation Indicator 0,64
Rank by Journal Citation Indicator Microbiology 81/157
Scimago  
Scimago
H-index
not indexed
Scimago
Journal Rank
not indexed
Scimago Quartile Score not indexed
Scopus  
Scopus
Cite Score
not indexed
Scopus
CIte Score Rank
  not indexed
Scopus
SNIP
not indexed

2020  
CrossRef Documents 23
WoS Cites 708
Wos H-index 27
Days from submission to acceptance 219
Days from acceptance to publication 176
Acceptance Rate 70%

2019  
WoS
Cites
558
CrossRef
Documents
24
Acceptance
Rate
92%

 

European Journal of Microbiology and Immunology
Publication Model Gold Open Access
Submission Fee none
Article Processing Charge 600 EUR/article
Regional discounts on country of the funding agency World Bank Lower-middle-income economies: 50%
World Bank Low-income economies: 100%
Further Discounts Editorial Board / Advisory Board members: 50%
Corresponding authors, affiliated to an EISZ member institution subscribing to the journal package of Akadémiai Kiadó: 100%
Subscription Information Gold Open Access
Purchase per Title  

European Journal of Microbiology and Immunology
Language English
Size A4
Year of
Foundation
2011
Volumes
per Year
1
Issues
per Year
4
Founder Akadémiai Kiadó
Founder's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Publisher Akadémiai Kiadó
Publisher's
Address
H-1117 Budapest, Hungary 1516 Budapest, PO Box 245.
Responsible
Publisher
Chief Executive Officer, Akadémiai Kiadó
ISSN 2062-509X (Print)
ISSN 2062-8633 (Online)

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