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Epidemiology of Toxoplasma gondii among blood donors in Iran: A systematic review and meta-analysis
Accepted Manuscript Title: Epidemiology of Toxoplasma gondii among Blood Donors in Iran: A Systematic Review and Meta-Analysis Author: Akram Mansouri Mohammad Reza Adhami Mojarad Gholamreza Badfar Lila Abasian Shoboo Rahmati Wesam Kooti Mohammad Hossein YektaKooshali Ali Soleymani Milad Azami PII: DOI: Reference:
S1473-0502(17)30052-6 http://dx.doi.org/doi:10.1016/j.transci.2017.03.011 TRASCI 2151
To appear in: Received date: Revised date: Accepted date:
17-11-2016 14-2-2017 14-3-2017
Please cite this article as: Akram M., Mohammad R.A.M., Gholamreza B., Lila A., Shoboo R., Wesam K., Mohammad H.Y., Ali S., Milad A., Epidemiology of Toxoplasma gondii among Blood Donors in Iran: A Systematic Review and Meta-Analysis, Transfusion and Apheresis Science (2017), http://dx.doi.org/10.1016/j.transci.2017.03.011 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Epidemiology of Toxoplasma gondii among Blood Donors in Iran: A
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Systematic Review and Meta-Analysis
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Akram Mansouri (M.Sc)1, Mohammad Reza Adhami Mojarad(MD)2, Gholamreza Badfar (MD)3, Lila Abasian (Msc)4, Shoboo Rahmati (M.Sc)5, Wesam Kooti (M.Sc)6, Mohammad Hossein YektaKooshali (B.Sc)7, Ali Soleymani (MSc)8, Milad Azami (M.D)9*
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1.
School of Nursing and Midwifery, Ahvaz jundishapour university of Medical science, Ahvaz, Iran ([email protected])
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2.
Assistant Professor, Department of Infectious Diseases, Faculty of Medicine, Ilam University of Medical Sciences, Ilam, Iran ([email protected])
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3.
Assistant Professor, Department of Pediatrics, Behbahan School of Medicine, Ahvaz jundishapour university of Medical science, Behbahan, Iran ([email protected])
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4.
M.Sc. of Parasitology, Student Research Committee, Ilam University of Medical Sciences , Ilam, Iran ( [email protected] )
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5.
M.Sc. of Epidemiology, Student Research Committee, Ilam University of Medical Sciences, Ilam, Iran ([email protected])
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6.
M.Sc. of Immunology, Student Research Committee, Kurdistan University of Medical Sciences, Sanandaj, Iran ([email protected])
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Student Research Committee, School of Nursing, Midwifery and Paramedicine, Guilan University of Medical Sciences, Rasht, Iran ([email protected])
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8.
Dezful University of Medical Sciences, Dezful, Iran ([email protected])
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9.
Student Research Committee, Faculty of Medicine, Dezful University of Medical Sciences, Dezful, Iran ([email protected])
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*Corresponding author: Milad Azami(MD), Faculty of Medicine, Dezful University of Medical Sciences, Dezful, Iran. Email: [email protected]. Tel: +989380316334
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Introduction: Asymptomatic T.gondii transmitted from blood donors to receiving patients has become a concern. Numerous articles have been published on the epidemiology of T.gondii in blood donors in Iran and a systematic review of the results shows quite different findings, hence this study was aimed to determine the seroprevalence of T.gondii in Iranian blood donors using meta-analysis.
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Methods: We searched for epidemiological studies that were published until by July 2016 in eight English databases including: Scopus, PubMed, Ovid, Science Direct, Cochrane, Web of Science, Springer, Wiley Online Library, and four Iranian databases: Magiran, Iranmedex, SID and Medlib; besides Google Scholar. To estimate pooled estimator, regarding that the high 1
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heterogeneity and the significance of I2 index, Random effects model was used. Data analysis was conducted using Review Manager Ver5.3.5 software and a significance level of 0.05 was considered significant.
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Results: Among 10 studies with a sample of 4538 Iranian blood donors, the seroprevalence of T.gondii was calculated 34.4% (CI95%: 24.9-43.9). The rate in males and females was 33.36% (CI95%: 19.92-46.81) and 37.63% (CI95%: 20.81-54.45), respectively. IgM and IgG antibodies seroprevalence among blood donors were 2.74% (CI95%: 0.55-4.92) and 31.84% (CI95%: 20.61-43.08), respectively. The seroprevalence of T.gondii was significantly associated with blood group (P=0.04), but this relation was not significant with blood transfusion (P=0.62).
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Conclusion: The results of this review indicate a high seroprevalence of T.gondii (about a third) is in Iranian blood donors and emphasizes the importance of screening seroprevalence of T.gondii of donated blood in Iranian Blood Transfusion Organization.
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Key words: Toxoplasma gondii, Blood Donors, Iran, Systematic Review, Meta-Analysis
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Introduction:
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T. gondii is an obligate intracellular parasites, from the sporozoites parasites, single-celled and
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an important parasite in the blood and tissues. Cats are the definitive host, and humans and other
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mammals are intermediate hosts for this parasite (1). Followed by digestion of oocysts,
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sporozoites are released in the digestive tract. They enter the tissue through the small intestine
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epithelium and transform to tachyzoite as a result of fast asexual division of T. gondii into host
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cells before the immune response is sufficient or if the lack of it Then tachyzoite can replicate in
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the host body (2) tachyzoite can cause chronic infection in adults, mortality in people with
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impaired immune systems and abortion in pregnant women. Infection in individuals with normal
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immune systems is often asymptomatic (2-3).
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T. gondii Serology detection methods include: Sabin Feldman test, IHA, IFA, ELISA, molecular,
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immunoblotting, and tissue biopsy, among which IgG and IgM antibody titers estimation can
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help to diagnose acute and chronic phases of the disease (5).
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The seroprevalence of T. gondii infection in human is different in different places depending on
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variables such as age, food habits, culture of life, keeping cats in the home, geographic region,
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the percentage of temperature and environment humidity (4)
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T. gondii transmitted from asymptomatic blood donors to patients receiving blood has become a
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concern; especially among the recipients have a weakened immune system. Because T. gondii
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infection is a lifelong disease and sufferers often have no clinical symptoms, tests for the
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detection of T. gondii in blood donors is required (6-7). On the other hand, T. gondii infection in
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blood donors is not investigated and sometimes blood recipients are people with impaired
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immune systems (8-9), which increases the importance of the issue.
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In recent years, numerous articles have been published on the Epidemiology of T. gondii in
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blood donors in Iran and systematic review of their results indicate different findings (9-18),
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hence, combined results using meta-analysis seems necessary for accurate estimation. Meta-
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analysis method collects the data of multiple researches with a common goal and analyzes them
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to provide a reliable estimation of the effect of some medical intervention or observations in the
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medicine (19-20). Obviously, by collecting the data of several studies in meta-analysis samples
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become more and therefore the range of differences and possibilities decrease, thus increasing
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the importance of statistical findings (21-22). This study was aimed to investigate the
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seroprevalence of T. gondii in Iranian blood donors using meta-analysis.
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Materials and methods:
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This study is based PRISMA checklist for systematic review and meta-analysis (21) to search,
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selection of studies, quality assessment and data extraction were done by two researchers
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independent of each other avoid bias. Results agreement and in case of discrepancies between
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the results was examined by a third researcher.
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Search strategy:
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We searched the epidemiological studies that had been conducted until the beginning of August
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2016 in eight English Databases including: Scopus, PubMed, Ovid, Science Direct, Cochrane,
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Web of Science, Springer, Wiley Online Library and four Iranian databases: Magiran,
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Iranmedex, SID and Medlib as well as Google Scholar search engine. The used keywords
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include: Prevalence, Epidemiology, Toxoplasma, Toxoplasma gondii, T. gondii, Blood donor,
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Transfusion, Blood pack, Iran and combination of words with AND and OR operators. Hand
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searching was done using the reference lists of searched articles in the database above. PubMed
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combination search is shown in Appendix 1.
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Inclusion and exclusion criteria:
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Eligible studies were: 1. Quantitative epidemiological cross sectional studies; 2. articles
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published in Persian or English Language, and 3. Evaluating T. gondii infection in blood donors.
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Exclusion criteria included: 1. Non-random sample; 2. Non-related subject; 3. insufficient data
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such as failing to report the seroprevalence; 4. Sample other than blood donors; 5. foreign
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studies; 6. review articles, case study reports and editorial 7. Replicated papers.
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Qualitative assessment:
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Using STROBE checklist i.e. an international standard checklist for quality assessment of
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studies, two researchers independently evaluated the selected articles qualitatively (23). The
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authors adopted a simple method for rating; 0 to 2 points were given to every part of the
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checklist. In the end, the point given to the papers by two researchers were compared, in case of
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disagreement discussion group was run. a minimum score of 16 was considered for inclusion in
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the meta-analysis.
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Data Extraction:
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To extract data based on pre-prepared list, factors included the author's name, year of study,
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place of study, study design, sample size, average age, general seroprevalence of T. Gondii,
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immunoglobulin (Ig) M and IgG seroprevalence of T. gondii, seroprevalence by sex, blood
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transfusion history and the blood group.
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Statistic analysis:
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Regarding that the main indicator of this study was seroprevalence; its variance was calculated
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using a binomial distribution and 95% confidence for the ratios were calculated. The index I2 and
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Cochran test were used to determine the homogeneity of studies. To estimate pooled estimator,
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regarding that the high heterogeneity and the significance of I2 index, Random effects model was
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used (24-25). Data analysis was conducted using Review Manager Version 5.3.5 and
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significance level was considered lower than 0.05.
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Findings:
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In systematic review, 217 studies were identified that after examining titles, 120 studies were
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excluded because of being duplicate; abstracts of likely-related 55 studies were reviewed among
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which the full text of 42 studies were entered into the final list. After reviewing the inclusion-
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exclusion criteria and qualitative evaluation, 10 papers published between 1999 and 2015 were
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eligible to be entered into the meta-analysis (Figure 1). Table 1 shows the characteristics of each
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of the studies.
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Based on the reviewed studies with a sample of 4538 people, the seroprevalence of T. gondii in
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Iran’s blood donors was 34.4% (CI95%: 24.9-43.9). The lowest and highest incidence was
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associated with the study of Ferdowsi (2011) in Gonabad (18.3%) and Ormazdi (2008) in Tehran
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(56.4%). (Figure 2)
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T. gondii seroprevalence among blood donors in Iran is shown based on the province in Figure 3;
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where T. gondii had the highest in Hamedan (56.3%) and the lowest in Khorasan (18.3%).
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T. gondii seroprevalence among blood donors in Iran was estimated in terms of gender, the
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seroprevalence in males and females as 33.36% (CI95%: 19.92-46.81) and 37.63% (CI95%:
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20.81-54.45) respectively. Given that the confidence intervals intersect, the difference was not
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statistically significant (P> 0.05) (Table 2).
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Based on reviewed studies with a sample of 4153 people, the seroprevalence of IgM and IgG
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antibodies of T. gondii in blood donors was obtained 2.74% (CI95%: 0.55-4.92) and 31.84%
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(CI95%: 20.61-43.08) (Figure 4 ).
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The seroprevalence of IgM and IgG antibodies by sex is shown in Table 2, and the difference
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was not statistically significant (P> 0.05).
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The seroprevalence of T. gondii in Iran’s blood donors by blood group shows the most common
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blood groups were B (38%) and AB (28%) and the difference was statistically significant (P =
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0.04) (Table 3).
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The relationship between blood transfusion and the seroprevalence of T. gondii was investigated
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and it was found that, although the seroprevalence of T. gondii in donors with a history of
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transfusion (27.9%) was less than the control group (33.4%), but this association was not
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statistically significant (P = 0.62) (table 4).
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Figure 1. Study flow diagram
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Table 1: Study characteristics of 10 studies on T. gondii gondii among blood donors in Iran Seroprevalence of T. gondii (%)
Seroprevalence of IgM antibody of T. gondii (%)
Seroprevalence of IgG antibody of T. gondii (%)
Authors name
Year
Place
8
Ferdowsi et al
2011
Gonabab
300
ELISA
18.3
2.3
17.7
9
Gholami et al
2013
Hamedan
540
ELISA
56.3
1.9
54.4
10
Jalayer et al
1996
Isfahan
385
ELISA
38.7
11
Mahmoudvand et al
2014
Kerman
500
12
Modrek et al
2014
Zahedan
375
ELISA
25
13
Ormazdi et al
2008
Tehran
250
ELISA
14
Sarkari et al
2012
Shiraz
1480
ELISA
15
Shaddel et al
2012
Tehran
223
ELISA
16
Shaddel et al
2013
Shiraz
250
ELISA
17
Zainodini et al
2013
Rafsanjan
235
ELISA
ELISA
cr
Method
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Ref
Sample size
3.2
28.8
0
25
56.4
3.6
52.8
19.32
7.02
13.85
38.55
4.5
36.8
23.6
0.40
23.2
35.7
1.71
34.04
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Figure 2. T. gondii seroprevalence among blood donors in Iran
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Figure 3. T. gondii seroprevalence among blood donors in Iran.(Sorted by Province)
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Table 2. T. gondii seroprevalence among blood donors in Iran.(Sorted by gender)
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Number of study
Sample size
Seroprevalence (%)
[CI95%]
I2(%)
Male
6
2610
33.36
[19.92-46.81]
100
Female
6
377
37.63
[20.81-54.45]
100
Male
5
1241
1.96
[1.22-2.70]
99
Female
5
293
5.92
[1.21-10.63]
100
Male
5
1241
33.90
[19.50-48.30]
100
Female
5
293
39.06
[19.60-58.51]
100
Variable
Overall prevalence
Seroprevalence of IgM antibody
Seroprevalence of IgG antibody
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Figure 4. The seroprevalence of IgM and IgG antibodies of T. gondii infection among blood donors in Iran
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Table 3. T. gondii seroprevalence among blood donors in Iran.(Sorted by Blood group)
A B AB O
Number of study
Weight (%)
Seroprevalence (%)
[CI95%]
I2 (%)
P-Value
5
25.4
21
[17-25]
100
P<0.00001
5
24.4
37
[26-48]
100
P<0.00001
5
24.6
28
[21-35]
100
P<0.00001
5
25.5
23
[17-28]
99
P<0.00001
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Subgroup Differences: Chi² = 8.46, df = 3 (P = 0.04), I² =64.4%
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Table 4. T. gondii seroprevalence among blood donors in Iran.(Sorted by Blood transfusion) Blood transfusion
Number of study
Weight (%)
Seroprevalence (%)
[CI95%]
I2 (%)
P-Value
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Yes
3
49.3
27.9
[11.2-44.7]
100
P<0.00001
No
3
50.7
33.4
[19.4-42]
100
P<0.00001
Subgroup Differences: Chi² = 0.25, df = 1 (P = 0.62), I² = 0%
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Discussion:
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This study is the first systematic review and metaanalysis on T. gondii in blood donors in Iran.
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Due to the high homogeneity of studies, the random effects model in the meta-analysis was used.
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In reviewing 10 papers with a sample of 4538 people, T. gondii seroprevalence among blood
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donors was calculated based on the ELISA method as 34.4% (CI95%: 24.9-43.9). Subgroup
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analysis was used to find the heterogeneity of the studies, and only the seroprevalence of T.
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gondii was significantly correlated with blood group but no correlation was found with sex and
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blood transfusion. In a systematic review and meta-analysis the seroprevalence of T. gondii in
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the general population of Iran has been reported 39.3% (26) that is consistent with our study on
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blood donors. T. gondii seroprevalence among blood donors in other countries was variable
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between 1 and 75% (27-30). This difference in seroprevalence can be relate with dietary habits,
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culture of life, keeping cats in the home, geographic region, the percentage of heat and humidity
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in different areas related to the environment (4).
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Although infection in adults is usually benign, but during pregnancy may it have serious
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symptoms such as mental retardation or severe neurological and ocular complications in the fetus
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(2). Parasitic agents are the cause of death in AIDS patients and people with weakened immune
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systems by causing encephalitis and death in patients. Blood and blood products are one of the
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modes of transmission of T. gondii from one person to another. High titer of T. gondii antibody
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has a direct relationship with exposure to cats and due to the fact that keeping cats in the house is
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not common in Iran, so contamination occurs in other ways and indirect contact with cats. One of
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the possible ways of receiving T. gondii infected blood is blood transfusion (31). On the other
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hand, most blood recipients are people with impaired immune systems and children with
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thalassemia,
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sickle
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anemia,
aplastic
anemia
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women;
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and these people are prone to blood-borne Toxoplasmosis. Since these people are not completely
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immune, the risk of involvement in dangerous phase of disease is high (16-18).
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The seroprevalence of T. gondii in female blood donors was (37.6%) and higher than men
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(33.4%) but not statistically significant; therefore, sex cannot be a risk factor for toxoplasmosis.
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In the review article of Daryani et al. in the general population of Iran, the seroprevalence of T.
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gondii in women and men is reported 42 and 44 percent respectively (26), which is not in line
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with the results of this study.
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The most important limitations of this study include: 1. the national databases did not allow
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combination search of keywords 2. Seroprevalence of T. gondii was not studied in terms of year
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of study, region, age, education, urban / rural, and occupation.
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Conclusion:
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This meta-analysis provides information about the high seroprevalence of T. gondii in Iranian
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donor blood. seroprevalence was not meant active infection of toxoplasma, but since the majority
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of blood recipients are high-risk patients due to not completely immune, the importance of
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screening donated bloods at Iranian Blood Transfusion Organization for T. gondii. Since the
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donated blood is not checked in terms of T. gondii at the Blood Transfusion Organization of Iran,
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therefore it is advised that this organization performs the screening programs in this area.
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Conflict of interest:
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In this study, the authors have no conflict of interest.
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Appendix 1:
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1. exp Prevalence/
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2. exp Epidemiology/
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3. exp Toxoplasma/
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4. exp Toxoplasma gondii/
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5. exp T. gondii/
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6. exp Blood donor/
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7. exp Transfusion/
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8. exp Blood pack/
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9. exp Iran/
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10. 1 OR 2
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11. 3 OR 4 OR 5
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12. 6 OR 7 OR 8
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13. 10 AND 11 AND 9
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14. 10 AND 11 AND 9 OR 10
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References:
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23. Von Elm E, Altman DG, Egger M, et al. The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 2007; 370(9596):1453-7. 24. Higgins JPT, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in metaanalyses. Br Med J. 2003; 327(7414): 557–60. 25. Harbord RM, Harris RJ, Sterne JAC. Updated tests for small-study effects in meta-analyses. Stata J. 2009;9(2):197. 26. Daryani A, Sarvi S, Aarabi M, Mizani A, Ahmadpour E, Shokri A, et al. Seroprevalence of Toxoplasma gondii in the Iranian general population: a systematic review and meta-analysis. Acta tropica. 2014 Sep;137:185-94. PubMed PMID: 24887263. 27. Van der Colf BE, Noden BH,Wilkinson R, Chipare I. Low seroprevalence of antibodies to Toxoplasma gondii in blood donors in Central Namibia: original research. S Afr J Infect Dis 2014;29:101–4. 28. John LN, McBride WJ, Millan J, Wilson K. Seroprevalence of anti–Toxoplasma gondii antibodies in HIV/AIDS patients and healthy blood donors at the Port Moresby general Hospital, Papua New Guinea. P N G Med J 2012;55:88–93. 29. Yilmaz GR, Babur C, Kilic S, Taylan Ozkan A, Beyaz E, Karakoc AE. Short communication: investigation of Toxoplasma gondii antibodies in blood donors by SabinFeldman Dye test [article in Turkish]. Mikrobiyol Bul 2006;40:375–81. 30. Coêlho RA, Kobayashi M, Carvalho Jr LB. Prevalence of IgG antibodies specific to Toxoplasma gondii among blood donors in Recife, Northeast Brazil. Rev Inst Med Trop Sao Paulo 2003;45:229–31. 31. John DT, Petri WA. Examinations of stool specimens. In: Markell EK, Editor. Medical parasitology. Missouri: Saunders; 2006. P. 393-415.
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S1473-0502(17)30052-6 http://dx.doi.org/doi:10.1016/j.transci.2017.03.011 TRASCI 2151
To appear in: Received date: Revised date: Accepted date:
17-11-2016 14-2-2017 14-3-2017
Please cite this article as: Akram M., Mohammad R.A.M., Gholamreza B., Lila A., Shoboo R., Wesam K., Mohammad H.Y., Ali S., Milad A., Epidemiology of Toxoplasma gondii among Blood Donors in Iran: A Systematic Review and Meta-Analysis, Transfusion and Apheresis Science (2017), http://dx.doi.org/10.1016/j.transci.2017.03.011 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
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Epidemiology of Toxoplasma gondii among Blood Donors in Iran: A
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Systematic Review and Meta-Analysis
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Akram Mansouri (M.Sc)1, Mohammad Reza Adhami Mojarad(MD)2, Gholamreza Badfar (MD)3, Lila Abasian (Msc)4, Shoboo Rahmati (M.Sc)5, Wesam Kooti (M.Sc)6, Mohammad Hossein YektaKooshali (B.Sc)7, Ali Soleymani (MSc)8, Milad Azami (M.D)9*
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1.
School of Nursing and Midwifery, Ahvaz jundishapour university of Medical science, Ahvaz, Iran ([email protected])
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2.
Assistant Professor, Department of Infectious Diseases, Faculty of Medicine, Ilam University of Medical Sciences, Ilam, Iran ([email protected])
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3.
Assistant Professor, Department of Pediatrics, Behbahan School of Medicine, Ahvaz jundishapour university of Medical science, Behbahan, Iran ([email protected])
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4.
M.Sc. of Parasitology, Student Research Committee, Ilam University of Medical Sciences , Ilam, Iran ( [email protected] )
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5.
M.Sc. of Epidemiology, Student Research Committee, Ilam University of Medical Sciences, Ilam, Iran ([email protected])
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6.
M.Sc. of Immunology, Student Research Committee, Kurdistan University of Medical Sciences, Sanandaj, Iran ([email protected])
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Student Research Committee, School of Nursing, Midwifery and Paramedicine, Guilan University of Medical Sciences, Rasht, Iran ([email protected])
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8.
Dezful University of Medical Sciences, Dezful, Iran ([email protected])
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9.
Student Research Committee, Faculty of Medicine, Dezful University of Medical Sciences, Dezful, Iran ([email protected])
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*Corresponding author: Milad Azami(MD), Faculty of Medicine, Dezful University of Medical Sciences, Dezful, Iran. Email: [email protected]. Tel: +989380316334
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Introduction: Asymptomatic T.gondii transmitted from blood donors to receiving patients has become a concern. Numerous articles have been published on the epidemiology of T.gondii in blood donors in Iran and a systematic review of the results shows quite different findings, hence this study was aimed to determine the seroprevalence of T.gondii in Iranian blood donors using meta-analysis.
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Methods: We searched for epidemiological studies that were published until by July 2016 in eight English databases including: Scopus, PubMed, Ovid, Science Direct, Cochrane, Web of Science, Springer, Wiley Online Library, and four Iranian databases: Magiran, Iranmedex, SID and Medlib; besides Google Scholar. To estimate pooled estimator, regarding that the high 1
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heterogeneity and the significance of I2 index, Random effects model was used. Data analysis was conducted using Review Manager Ver5.3.5 software and a significance level of 0.05 was considered significant.
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Results: Among 10 studies with a sample of 4538 Iranian blood donors, the seroprevalence of T.gondii was calculated 34.4% (CI95%: 24.9-43.9). The rate in males and females was 33.36% (CI95%: 19.92-46.81) and 37.63% (CI95%: 20.81-54.45), respectively. IgM and IgG antibodies seroprevalence among blood donors were 2.74% (CI95%: 0.55-4.92) and 31.84% (CI95%: 20.61-43.08), respectively. The seroprevalence of T.gondii was significantly associated with blood group (P=0.04), but this relation was not significant with blood transfusion (P=0.62).
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Conclusion: The results of this review indicate a high seroprevalence of T.gondii (about a third) is in Iranian blood donors and emphasizes the importance of screening seroprevalence of T.gondii of donated blood in Iranian Blood Transfusion Organization.
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Key words: Toxoplasma gondii, Blood Donors, Iran, Systematic Review, Meta-Analysis
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Introduction:
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T. gondii is an obligate intracellular parasites, from the sporozoites parasites, single-celled and
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an important parasite in the blood and tissues. Cats are the definitive host, and humans and other
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mammals are intermediate hosts for this parasite (1). Followed by digestion of oocysts,
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sporozoites are released in the digestive tract. They enter the tissue through the small intestine
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epithelium and transform to tachyzoite as a result of fast asexual division of T. gondii into host
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cells before the immune response is sufficient or if the lack of it Then tachyzoite can replicate in
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the host body (2) tachyzoite can cause chronic infection in adults, mortality in people with
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impaired immune systems and abortion in pregnant women. Infection in individuals with normal
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immune systems is often asymptomatic (2-3).
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T. gondii Serology detection methods include: Sabin Feldman test, IHA, IFA, ELISA, molecular,
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immunoblotting, and tissue biopsy, among which IgG and IgM antibody titers estimation can
68
help to diagnose acute and chronic phases of the disease (5).
69
The seroprevalence of T. gondii infection in human is different in different places depending on
70
variables such as age, food habits, culture of life, keeping cats in the home, geographic region,
71
the percentage of temperature and environment humidity (4)
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T. gondii transmitted from asymptomatic blood donors to patients receiving blood has become a
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concern; especially among the recipients have a weakened immune system. Because T. gondii
74
infection is a lifelong disease and sufferers often have no clinical symptoms, tests for the
75
detection of T. gondii in blood donors is required (6-7). On the other hand, T. gondii infection in
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blood donors is not investigated and sometimes blood recipients are people with impaired
77
immune systems (8-9), which increases the importance of the issue.
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In recent years, numerous articles have been published on the Epidemiology of T. gondii in
79
blood donors in Iran and systematic review of their results indicate different findings (9-18),
80
hence, combined results using meta-analysis seems necessary for accurate estimation. Meta-
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analysis method collects the data of multiple researches with a common goal and analyzes them
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to provide a reliable estimation of the effect of some medical intervention or observations in the
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medicine (19-20). Obviously, by collecting the data of several studies in meta-analysis samples
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become more and therefore the range of differences and possibilities decrease, thus increasing
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the importance of statistical findings (21-22). This study was aimed to investigate the
86
seroprevalence of T. gondii in Iranian blood donors using meta-analysis.
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Materials and methods:
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This study is based PRISMA checklist for systematic review and meta-analysis (21) to search,
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selection of studies, quality assessment and data extraction were done by two researchers
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independent of each other avoid bias. Results agreement and in case of discrepancies between
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the results was examined by a third researcher.
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Search strategy:
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We searched the epidemiological studies that had been conducted until the beginning of August
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2016 in eight English Databases including: Scopus, PubMed, Ovid, Science Direct, Cochrane,
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Web of Science, Springer, Wiley Online Library and four Iranian databases: Magiran,
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Iranmedex, SID and Medlib as well as Google Scholar search engine. The used keywords
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include: Prevalence, Epidemiology, Toxoplasma, Toxoplasma gondii, T. gondii, Blood donor,
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Transfusion, Blood pack, Iran and combination of words with AND and OR operators. Hand
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searching was done using the reference lists of searched articles in the database above. PubMed
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combination search is shown in Appendix 1.
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Inclusion and exclusion criteria:
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Eligible studies were: 1. Quantitative epidemiological cross sectional studies; 2. articles
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published in Persian or English Language, and 3. Evaluating T. gondii infection in blood donors.
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Exclusion criteria included: 1. Non-random sample; 2. Non-related subject; 3. insufficient data
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such as failing to report the seroprevalence; 4. Sample other than blood donors; 5. foreign
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studies; 6. review articles, case study reports and editorial 7. Replicated papers.
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Qualitative assessment:
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Using STROBE checklist i.e. an international standard checklist for quality assessment of
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studies, two researchers independently evaluated the selected articles qualitatively (23). The
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authors adopted a simple method for rating; 0 to 2 points were given to every part of the
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checklist. In the end, the point given to the papers by two researchers were compared, in case of
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disagreement discussion group was run. a minimum score of 16 was considered for inclusion in
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the meta-analysis.
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Data Extraction:
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To extract data based on pre-prepared list, factors included the author's name, year of study,
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place of study, study design, sample size, average age, general seroprevalence of T. Gondii,
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immunoglobulin (Ig) M and IgG seroprevalence of T. gondii, seroprevalence by sex, blood
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transfusion history and the blood group.
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Statistic analysis:
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Regarding that the main indicator of this study was seroprevalence; its variance was calculated
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using a binomial distribution and 95% confidence for the ratios were calculated. The index I2 and
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Cochran test were used to determine the homogeneity of studies. To estimate pooled estimator,
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regarding that the high heterogeneity and the significance of I2 index, Random effects model was
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used (24-25). Data analysis was conducted using Review Manager Version 5.3.5 and
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significance level was considered lower than 0.05.
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Findings:
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In systematic review, 217 studies were identified that after examining titles, 120 studies were
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excluded because of being duplicate; abstracts of likely-related 55 studies were reviewed among
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which the full text of 42 studies were entered into the final list. After reviewing the inclusion-
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exclusion criteria and qualitative evaluation, 10 papers published between 1999 and 2015 were
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eligible to be entered into the meta-analysis (Figure 1). Table 1 shows the characteristics of each
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of the studies.
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Based on the reviewed studies with a sample of 4538 people, the seroprevalence of T. gondii in
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Iran’s blood donors was 34.4% (CI95%: 24.9-43.9). The lowest and highest incidence was
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associated with the study of Ferdowsi (2011) in Gonabad (18.3%) and Ormazdi (2008) in Tehran
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(56.4%). (Figure 2)
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T. gondii seroprevalence among blood donors in Iran is shown based on the province in Figure 3;
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where T. gondii had the highest in Hamedan (56.3%) and the lowest in Khorasan (18.3%).
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T. gondii seroprevalence among blood donors in Iran was estimated in terms of gender, the
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seroprevalence in males and females as 33.36% (CI95%: 19.92-46.81) and 37.63% (CI95%:
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20.81-54.45) respectively. Given that the confidence intervals intersect, the difference was not
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statistically significant (P> 0.05) (Table 2).
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Based on reviewed studies with a sample of 4153 people, the seroprevalence of IgM and IgG
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antibodies of T. gondii in blood donors was obtained 2.74% (CI95%: 0.55-4.92) and 31.84%
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(CI95%: 20.61-43.08) (Figure 4 ).
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The seroprevalence of IgM and IgG antibodies by sex is shown in Table 2, and the difference
147
was not statistically significant (P> 0.05).
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The seroprevalence of T. gondii in Iran’s blood donors by blood group shows the most common
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blood groups were B (38%) and AB (28%) and the difference was statistically significant (P =
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0.04) (Table 3).
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The relationship between blood transfusion and the seroprevalence of T. gondii was investigated
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and it was found that, although the seroprevalence of T. gondii in donors with a history of
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transfusion (27.9%) was less than the control group (33.4%), but this association was not
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statistically significant (P = 0.62) (table 4).
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Figure 1. Study flow diagram
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Table 1: Study characteristics of 10 studies on T. gondii gondii among blood donors in Iran Seroprevalence of T. gondii (%)
Seroprevalence of IgM antibody of T. gondii (%)
Seroprevalence of IgG antibody of T. gondii (%)
Authors name
Year
Place
8
Ferdowsi et al
2011
Gonabab
300
ELISA
18.3
2.3
17.7
9
Gholami et al
2013
Hamedan
540
ELISA
56.3
1.9
54.4
10
Jalayer et al
1996
Isfahan
385
ELISA
38.7
11
Mahmoudvand et al
2014
Kerman
500
12
Modrek et al
2014
Zahedan
375
ELISA
25
13
Ormazdi et al
2008
Tehran
250
ELISA
14
Sarkari et al
2012
Shiraz
1480
ELISA
15
Shaddel et al
2012
Tehran
223
ELISA
16
Shaddel et al
2013
Shiraz
250
ELISA
17
Zainodini et al
2013
Rafsanjan
235
ELISA
ELISA
cr
Method
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Ref
Sample size
3.2
28.8
0
25
56.4
3.6
52.8
19.32
7.02
13.85
38.55
4.5
36.8
23.6
0.40
23.2
35.7
1.71
34.04
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Figure 2. T. gondii seroprevalence among blood donors in Iran
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Figure 3. T. gondii seroprevalence among blood donors in Iran.(Sorted by Province)
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Table 2. T. gondii seroprevalence among blood donors in Iran.(Sorted by gender)
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Number of study
Sample size
Seroprevalence (%)
[CI95%]
I2(%)
Male
6
2610
33.36
[19.92-46.81]
100
Female
6
377
37.63
[20.81-54.45]
100
Male
5
1241
1.96
[1.22-2.70]
99
Female
5
293
5.92
[1.21-10.63]
100
Male
5
1241
33.90
[19.50-48.30]
100
Female
5
293
39.06
[19.60-58.51]
100
Variable
Overall prevalence
Seroprevalence of IgM antibody
Seroprevalence of IgG antibody
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Figure 4. The seroprevalence of IgM and IgG antibodies of T. gondii infection among blood donors in Iran
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Table 3. T. gondii seroprevalence among blood donors in Iran.(Sorted by Blood group)
A B AB O
Number of study
Weight (%)
Seroprevalence (%)
[CI95%]
I2 (%)
P-Value
5
25.4
21
[17-25]
100
P<0.00001
5
24.4
37
[26-48]
100
P<0.00001
5
24.6
28
[21-35]
100
P<0.00001
5
25.5
23
[17-28]
99
P<0.00001
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Subgroup Differences: Chi² = 8.46, df = 3 (P = 0.04), I² =64.4%
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Table 4. T. gondii seroprevalence among blood donors in Iran.(Sorted by Blood transfusion) Blood transfusion
Number of study
Weight (%)
Seroprevalence (%)
[CI95%]
I2 (%)
P-Value
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Yes
3
49.3
27.9
[11.2-44.7]
100
P<0.00001
No
3
50.7
33.4
[19.4-42]
100
P<0.00001
Subgroup Differences: Chi² = 0.25, df = 1 (P = 0.62), I² = 0%
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Discussion:
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This study is the first systematic review and metaanalysis on T. gondii in blood donors in Iran.
183
Due to the high homogeneity of studies, the random effects model in the meta-analysis was used.
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In reviewing 10 papers with a sample of 4538 people, T. gondii seroprevalence among blood
185
donors was calculated based on the ELISA method as 34.4% (CI95%: 24.9-43.9). Subgroup
186
analysis was used to find the heterogeneity of the studies, and only the seroprevalence of T.
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gondii was significantly correlated with blood group but no correlation was found with sex and
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blood transfusion. In a systematic review and meta-analysis the seroprevalence of T. gondii in
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the general population of Iran has been reported 39.3% (26) that is consistent with our study on
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blood donors. T. gondii seroprevalence among blood donors in other countries was variable
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between 1 and 75% (27-30). This difference in seroprevalence can be relate with dietary habits,
192
culture of life, keeping cats in the home, geographic region, the percentage of heat and humidity
193
in different areas related to the environment (4).
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Although infection in adults is usually benign, but during pregnancy may it have serious
195
symptoms such as mental retardation or severe neurological and ocular complications in the fetus
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(2). Parasitic agents are the cause of death in AIDS patients and people with weakened immune
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systems by causing encephalitis and death in patients. Blood and blood products are one of the
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modes of transmission of T. gondii from one person to another. High titer of T. gondii antibody
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has a direct relationship with exposure to cats and due to the fact that keeping cats in the house is
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not common in Iran, so contamination occurs in other ways and indirect contact with cats. One of
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the possible ways of receiving T. gondii infected blood is blood transfusion (31). On the other
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hand, most blood recipients are people with impaired immune systems and children with
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thalassemia,
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sickle
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aplastic
anemia
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women;
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and these people are prone to blood-borne Toxoplasmosis. Since these people are not completely
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immune, the risk of involvement in dangerous phase of disease is high (16-18).
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The seroprevalence of T. gondii in female blood donors was (37.6%) and higher than men
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(33.4%) but not statistically significant; therefore, sex cannot be a risk factor for toxoplasmosis.
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In the review article of Daryani et al. in the general population of Iran, the seroprevalence of T.
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gondii in women and men is reported 42 and 44 percent respectively (26), which is not in line
210
with the results of this study.
211
The most important limitations of this study include: 1. the national databases did not allow
212
combination search of keywords 2. Seroprevalence of T. gondii was not studied in terms of year
213
of study, region, age, education, urban / rural, and occupation.
214
Conclusion:
215
This meta-analysis provides information about the high seroprevalence of T. gondii in Iranian
216
donor blood. seroprevalence was not meant active infection of toxoplasma, but since the majority
217
of blood recipients are high-risk patients due to not completely immune, the importance of
218
screening donated bloods at Iranian Blood Transfusion Organization for T. gondii. Since the
219
donated blood is not checked in terms of T. gondii at the Blood Transfusion Organization of Iran,
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therefore it is advised that this organization performs the screening programs in this area.
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Conflict of interest:
222
In this study, the authors have no conflict of interest.
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Appendix 1:
224
1. exp Prevalence/
225
2. exp Epidemiology/
226
3. exp Toxoplasma/
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4. exp Toxoplasma gondii/
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5. exp T. gondii/
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6. exp Blood donor/
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7. exp Transfusion/
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8. exp Blood pack/
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9. exp Iran/
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10. 1 OR 2
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11. 3 OR 4 OR 5
235
12. 6 OR 7 OR 8
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13. 10 AND 11 AND 9
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14. 10 AND 11 AND 9 OR 10
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References:
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1. Sundar P, Mahadevan A, Jayshree R.S, Subbakrishna D.K , Shankar S.K. Toxoplasma seroprevalence in healthy voluntary blood donors from urban Karnataka. Indian J Med Res 2007; 126(1):50-5. 2. Rostami Nejad M, Mahbobipour H, Fazeli Z, Mashayekhi R, Mirsatari D, Nazemalhosseini Mojarad E, et al. Celiac disease in Iranian dyspeptic patients. Koomesh 2011; 12: 209-214. 3. Hoseini SA, Dehgani N, Sharif M, Daryani A, Gholami S, Ebrahimi F, et al. Serological survey of toxoplasmosis in pregnant women. J Mazand Univ Med Sci. 2014;24(114):146-50. 4. Martin PA, Bouza PE. Blood and tissue protozoa. In: Cohen J, Powderly WG, editors. Infectious diseases. 2nd ed. Philadelphia, PA: Mosby; 2004. 5. Koshini E, Takahashi J. Some epidemiological aspects of toxoplasma infections in a population of farmers in Japan. Int J Epidemiol. 1987;16(2):277-81. 6. Elsheikha HM, Azab MS, Abousamra NK, RahbarMH, ElghannamDM, Raafat D. Seroprevalence of and risk factors for Toxoplasma gondii antibodies among asymptomatic blood donors in Egypt. Parasitol Res 2009;104:1471–6. 7. Zarkovic A, McMurray C, Deva N, Ghosh S,Whitley D, Guest S. Seropositivity rates for Bartonella henselae, Toxocara canis and Toxoplasma gondii in New Zealand blood donors. Clin Experiment Ophthalmol 2007;35:131–4. 8. Karimi G, Mardani A, Zadsar M. Prevalence of Toxoplasma gondii among Iranian Blood Donors: A Narrative Review Article. Iranian journal of parasitology. 2016;11(1):10.
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