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Biology | 23 

2016) عام 2العدد (  29مجلة إبن الهيثم للعلوم الصرفة و التطبيقية                                                                            المجلد  

Ibn Al-Haitham J. for Pure & Appl. Sci.                                           Vol. 29 (2) 2016  

The Role of Some Cytokines and Trace Elements in 
Pregnant Women with Acute Toxoplasmosis  

Waheeda R. Ali  
Dept. of Biology/College of Education for Pure Science (Ibn Al-Haitham)/ 

University of Baghdad 
Received in :5 January2016, Accepted in :11May 2016 

Abstract 
     The present study was conducted on sixty five pregnant women that infected with    acute 
toxoplasmosis, serum samples were tested for detection specific anti-Toxoplasma gondii IgM 
using the rapid Toxo IgG/IgM Chromatographic immune assay test cassette and ELISA, and 
fifty healthy married women (not pregnant)  as  was considered as control group.   
    The level of serum IL-6, IL-8, IL-12, TNF-α, TGF-β1, IP-10, MIP-1, MIG and ICAM were 
significantly increased (P <0.005) in pregnant patients infected with acute toxoplasmosis, 
while serum level of MCP-1(14.46 ± 1.38pg/ml) was not significantly increased when 
compared to controls(11.25 ± 0.24pg/ml)  , these levels can be used as indicator to acute 
toxoplasmosis. 
   Trace elements concentrations in serum were measured during infection also, the results of 
this study revealed that serum Zn was markedly elevated (p<0.05) and serum Cu was 
significantly decreased (P<0.001) in Toxoplasmosis-seropositive women as compared with 
control.  
Key words: Toxoplasma gondii, Cytokines, Zn, Cu   

 

 

 

 

 

 

 

 

 

 

 

 

 



 

Biology | 24 

2016) عام 2العدد (  29مجلة إبن الهيثم للعلوم الصرفة و التطبيقية                                                                            المجلد  

Ibn Al-Haitham J. for Pure & Appl. Sci.                                           Vol. 29 (2) 2016  

Introduction                            
       Toxoplasma gondii is an obligate intracellular protozoan with unparalleled 
global distribution and mammalian host range. [1]. It is possible to differentiate 
between acute infections (initiated within Infection with the prior12 months) and 
chronic infections (more than one year since the initial infection) by using ELISA 
[2].Toxoplasmosis infection stimulates humoral immune response as antibody 
(Ab)production, in addition  T cell-mediated immunity (CMI) which is essential for 
the host and control of intracellular infection [3]. The macrophage, T- lymphocytes 
and Natural killer (NK) cells, and cytokines are the major elements involved in 
immune response against T. gondii. Cytokines are secreted by a variety of cell types, 
including inflammatory cells, and play crucial functions in immune-regulation and 
immune responses including responses to parasite infection [4, 5]. 
     Many studies have documented the role of cytokine in the resistance to acute and 
chronic infection to tachyzoite replication of T. gondii during pregnancy [6].IL-10, 
IL-12 and TNF-α play an important role in the innate immunity against T gondii and 
influence the adaptive immune response; these cytokines are important immune-
modulators that act during the early stage of infection [7,8].  
          Trace element plays an important role in biological systems through their action as 
activators or inhibitors of enzymatic reaction, or by its essential role of direct antioxidant 
enzyme, or by influencing the permeability of cell [9].Zinc (Zn) is essential for maintaining 
the integrity of immune function of T-cells has been associated with deficiency of Zinc, which 
acts as a growth hormone [10]. The element copper (Cu) is an integral part of cytochrome [8], 
and also required for normal red blood cells information [11].  
      The present study aimed to determine the serum levels of 10 cytokines IL-6, IL-8, IL-12, 
TNF-α, IP-10, MCP-1, MIP-1, MIG-1, TGF-β1 and ICAM, also it  is designed to investigate 
the effect of the infection with acute toxoplasmosis on the levels of essential trace elements 
Zn and Cu, such collective evaluations may aid in a better understanding of the 
immunological mechanisms that can lead to acute toxoplasmosis in Iraqi pregnant women. 
 

Materials and Methods   
       Sixty-five pregnant   women   at first trimesters of pregnancy suffering from problems of 
miscarriage were attending to Department of Gynecology and Pediatrics in Al-Yarmouk 
Teaching Hospital and Imamein Kadhimein Medical City in Baghdad during the period from 
October 2014 to March 2015 were conducted in this study. Their age ranged from 20-41 
years, in addition a group of 50 fertile healthy married women (not pregnant) were enrolled in 
this study as a control group.                               
Blood samples collection: 
       Five mL of venous blood were collected from each women and placed in plane tube 
where the serum was separated and stored at -20C until it is used. 
Serological tests: 
1-Rapid Toxo IgG/IgM Chromatographic Immune Assay Test Cassette: 
Detection of parasite antibody  ,the kit  is supplied by CTK Biotech, San Diego, USA. 
2-ELISA T. gondii –IgM:  
     The ELISA Toxo-IgM (From Biokit Diagnostics Company, Spain) is an IgM- capture 
immunoenzimatic assay for the determination of IgM antibodies against T.gondii in the 
patient's serum or plasma.                                                                         
Calculation of results:  
        The mean of duplicate absorbance of the low positive calibrator was calculated which 
represents the cut-off value: Cut-off = mean of low positive absorbance. The absorbance of  



 

Biology | 25 

2016) عام 2العدد (  29مجلة إبن الهيثم للعلوم الصرفة و التطبيقية                                                                            المجلد  

Ibn Al-Haitham J. for Pure & Appl. Sci.                                           Vol. 29 (2) 2016  
 
each sample was divided by the cut-off value, and then the results were compared with the 
following ratios to differentiate between positive, negative and equivocal samples.  
Positive sample: Ratio absorbance/cut-off ˃ 1.0 
Negative sample: Ratio absorbance/cut-off < 0.9 

1.0 sample was retested with a fresh  <off   ≥ 0.9 -Ratio absorbance/ cut :Equivocal sample
new sample after 2-4 weeks.   
Through a result of serological tests  that mentioned above, it was able to  diagnose 65 cases 
of acute toxoplasmosis infection of pregnant women (with high titer IgM antibody ) and 50 
healthy married women (not pregnant)   to measure serum level of cytokines and chemokines. 

3-Serum Level of Cytokines and Chemokines: 
      Sera of pregnant women that have a positive IgM antibody against T. gondii, and control 
group were enrolled to measure levels of cytokines IL‐6, IL‐8, IL-12, TNF‐ α and 
chemokine MCP-1, IP-10, MIP-1, ICM, MIG-1 and growth factor TGF‐β1 by using ELISA 
test. All kits were provided from Pepro Tech; USA. The manufacturer's protocols were 
followed for each kit and recombinant reference cytokine and chemokine samples were 
served as positive control for calibration. 
4-Serum level of Zn and Cu: 
      Serum diluted (0.1 ml) to total volume of 1ml using 6%n-butanol solution and analyzed 
for Zn and Cu levels using atomic absorption spectrophotometer (Shimadzu AA-646) using 
Zn and Cu hollow cathode lamps at wavelengths 213nm and 324.75nm respectively.  
Statistical analysis: 
      Statistical analysis was computer assisted using Statistical Package   for Social Science 
(SPSS) version 13.0 was applied and least significant difference (LSD) between groups.  

 
Results  
        Table (1) shows that serum sample from the study population were successfully analyzed 
for IgM by ELISA. The median values of IgM –Toxoplasma antibodies titer was statistically 
significant .It is higher in the group of pregnant women with positive diagnosis by ELISA 
(1.98±0.850), compared to those with negative diagnosis of toxoplasmosis (0.41±0.315) 
There were statistically significant differences between the two groups (P<0.001).The highest 
rate (27.0%) of Toxo-IgM was found in pregnant women from the age group 26-31 years old. 
       The results of cytokines and chemokines levels show in table (2) there was a significant 
increase in cytokines IL‐6, IL‐8, IL-12, NF‐ α, IP-10, MIP-1, ICM, MIG-1 and TGF‐β1 in 
pregnant women  that they were positive to T. gondii IgM serology which  significant increase 
(P < 0.05), while the mean of   MCP-1 serum concentration (14.46±1.38pg\ml) was 
significantly decreased (P <0.05) in patients in comparison to control 
group(11.25±0.24pg/ml) (Table 2).  

     In table (3) Zn and Cu levels analysis in sera of positive women and in control, the mean 
levels of serum Zn were significantly lower in patient group(p≤0.05) than in the healthy 
controls whereas serum Cu concentrations were significantly (p≤0.001) higher in patient 
group when compared with control.. 
 

Discussion 
        The results of the present study  showed that median value of  IgM- Toxoplasma  
antibodies in women with toxoplasmosis was 1.98±0.850, this result reflects that  infected 
women had acute toxoplasmosis .ELISA  technique  for detection of IgM and IgG  of T. 
gondii  must be used within  Toxoplasma serologic profile that included  different  



 

Biology | 26 

2016) عام 2العدد (  29مجلة إبن الهيثم للعلوم الصرفة و التطبيقية                                                                            المجلد  

Ibn Al-Haitham J. for Pure & Appl. Sci.                                           Vol. 29 (2) 2016  
agglutination and ELISA  ,which are routinely used to assess whether infection was acquired 
during pregnancy[6]. 
       The serum level of IL-6 was higher than its level in control group which is considered as 
an indicator for acute inflammation during infection and the results were compatible with that 
recorded by AL-Damoshi et al., [7]. This cytokine may occur early in infection before the 
immunological shift from Th2 into Th1 that might be responsible for the several cases of 
abortion [12].  
        IL-8 is a potent chemo attractant and activator of neutrophils. It is produced by wide 

variety of cell types, including macrophages, neutrophils, endothelial cells, fibroblasts, 
chondrocytes and osteoclasts, In agreement with the present results, Koumantaki et al., [13] 
found that IL-8 was significantly increased in acute with early acute inflammation or with a 
reactive from toxoplasmosis. The inflammatory cytokines, such as IL-8,may play a vital role 
in mechanism of protease induced neurogenic inflammation leading to labor or abortion by 
enrolling neutrophils and lymphocytes in the endometrium, whereas previous studies reported 
that women with spontaneous abortions had pointedly decreased plasma level of IL-8 
compared to those with normal pregnancies [7,8]. In addition to IL-8, the presence of a 
significant increase of serum level of IL-12 is a key cytokine that drives the inflammatory 
response mediated by Th1 cells. Monocyte /macrophage and dendritic cells are active in IL-
12 production during the first contact of Toxoplasma with innate immune system [14]. IL-12 
is required for resistance to acute and chronic   toxoplasmosis due to its essential role in 
stimulating production of IFN-ɣ, facilitates formation of Th1 type response and activates 
lymphocyte cytotoxicity. This present study showed high level IL-12 patients with 
toxoplasmosis in comparison with control group (Table- 2). This may be due to the fact that 
the infection with T. gondii induce strong CMI characterized by high Th1-cell response [15].  

                                                          
    TNF-α is a Th1 response cytokine produced by macrophage, T-lymphocyte, basophils and 
monocytes. In toxoplasmosis, TNF-α appears to be essential for macrophage activation and 
inhibition of parasite replication, of this cytokine documented in resistance to the acute and 
chronic Toxoplasmosis, the level of this cytokine increases, abortion occurs, the current 
results  in this regard is in consistency with Trowsdal and Betz [16].       
      The level of IP-10 cytokine that showed a significant increase in serum of infected group 
is a key mediator of the interferon response referentially attracts activated Th1                        
lymphocytes to sites of inflammation, and is an inhibitor of angiogenesis. The present study 
indicated that IP-10 is critical for survival following T. gondii infection and is essential for 
guiding antigen specific CD41 and CD81 T cells into infected organs. T. gondii evokes a 
strong humoral and cellular immune response in the infected host. The chemokine IP-10 a 
specific chemoat-tractant for activated T cells. These observations suggest that IP-10 may 
play a broader role in the localization and the function of effector T cells at sites of Th1 
inflammation [17]. 
                                                                                                             
     The chemokines, MCP-1 ,IP- 10 and MIP-1 are involved in the cellular recruitment and 
activation of several leukocytes such as monocytes/macrophages, polymorphonuclear cells, 
and lymphocyte infiltration to the sites of infection (19).The immune response against 
infection stimulate macrophages and lymphocytes that work on the  production of MCP-1 
.Low level MCP-1 (CCL2) were observed in pregnant women with acute toxoplasmosis 
(Table-2), because live tachyzoiest forms of T. gondii  inhibited the synthesis of MCP-
1(20),and T. gondii tachyzoites were found to modulate the synthesis of CCL2 in cell cultures 
of parturient and non-pregnant women[21]. 
    The results of present study showed that the increase in the level of ICAM -1(Table -2), in 
accordance with this study Pfaff et al.,[22] that demonstrates ICAM-1 is the principal receptor 
for increased monocyte adhesion to activate primary trophoblast. IFN-ɣ plays a pivotal role in  
 



 

Biology | 27 

2016) عام 2العدد (  29مجلة إبن الهيثم للعلوم الصرفة و التطبيقية                                                                            المجلد  

Ibn Al-Haitham J. for Pure & Appl. Sci.                                           Vol. 29 (2) 2016  
 
the cell adhesion process through up regulation of ICAM-1 and in the process of congenital 
transmission of T. gondii [22]. 
     The current study showed a significant increase in the level of MIG-1(CXCL9) in the 
blood serum of infected group compared to control, and this may be due to the CXCL9 is 
critical for the recruitment of T cells in the immune areas that breed tachyzoites to prevent 
chronic activate Toxoplasma infection [17]. 
      The present study showed that the serum levels of Transforming factor-beta TGF-β is 
significantly increased in infected women. TGF-β is a cytokine which plays key roles in the 
regulation of immune cell functions .This cytokine leads to inhibition of B and T lymphocytes 
proliferation and induces homeostasis [23].TGF-β also contributes to tissue remodeling which 
occurs after infections and injuries, this cytokine contributes to development of Th17 and T-
regulatory lymphocytes, activation and suppression of immune which play significant roles in 
parasite responses, against infection [24].                                                                                                            
   The results showed ,that there was significant decrease  in  serum Zn  levels in patients ,this 
can be  according to Kadham [25]refearing to  this lowering value , probably due to the 
shifting of this element from the transport media (serum) to the liver which is considered as a 
protective mechanism against the disease. 
       Zn is a metal essential for maintaining the integrity of immune system. The results 
showed that the specific cellular immunity is detectable in virtually all Toxoplasma-infected 
patients [10, 11]. Several investigators have found that Zn deficiency depresses antibody 
responses possibly owing to a loss of T- helper cell function. The increased serum level of Cu 
may be   explained to its form of serum which is formed in response to inflammation 
associated with the disease [26, 27]. 
 
 
References   
1- Montoya, J.G. and Liesnfeld,O.(2004).Toxoplasmosis.Lancet,12(9425):1965-19761.           

                                                                                                                   
2-Bliss,S.K.;Gavrilescu,C.;Alcaraz,A.and Denkers,E.Y.(2001).Neutrophil depletion    during 
Toxoplasma gondii infection leads to impaired immunity and lethal systemic pathology. 
Infect. Immun.,(69):4898-4905.                                                                      
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infection.  gondii Toxoplasma 10 in abnormal pregnancy outcome induced by-interleukin
Gynecol. Obstet. Invest., 73(3): 223–229.                                           
4-Aldebert, D.(2007).Toxoplasma gondii triggers secretion of  nterleukin-12 but low level of 
interleukin-10 from TH-1human monocytic cell line. Cytokine, 37(3):206-211. 
5-Pernas,L.;Ramirez,R.;Holmes,T.H.;Montoya,J.G.andBoothryd,J.C.(2014).Immune profiling 
of pregnant Toxoplasma-Infected US and Colombiabia pateints reveals surprising impacts of 
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6-Liesenfeld,O.; Montoya, G. J; Tathineni, J. N.; Davis, M.; Brown,W. B.;Cobb, L. K. and 
Parsonnet, J. (2001). Confirmatory serologic testing for acute toxoplasmosis and rate of 
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Biology | 28 

2016) عام 2العدد (  29مجلة إبن الهيثم للعلوم الصرفة و التطبيقية                                                                            المجلد  

Ibn Al-Haitham J. for Pure & Appl. Sci.                                           Vol. 29 (2) 2016  

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17 -Khan, I. A.; MacLean,J.A.; Lee, F.S.; Casciotti, L.; DeHaan,E.,  Schwartzman, J.D. and 
Luster, A.D. (2000). IP-10 is critical for effector T cell trafficking and host survival in 
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,M. and Candolfi , E. (2005). Toxoplasma gondii 
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Biology | 29 

2016) عام 2العدد (  29مجلة إبن الهيثم للعلوم الصرفة و التطبيقية                                                                            المجلد  

Ibn Al-Haitham J. for Pure & Appl. Sci.                                           Vol. 29 (2) 2016  
 
27-Rajeswari,S.and Swaminathan,S.(2014).Role of copper in health and diseases. Int. J. Cur. Sci., 10: 
94-107. 
 

      Table(1): The median values of T. gondii IgM antibodies   in pregnant women  
by  ELISA           

P value Diagnosis of Toxoplasmosis by 
ELISA(IU/ml) 

 IgM Toxoplasma 
antibody titer

Positive ±S.E.  Negative ±S.E. 
<0.001  0.17-0.8 1.20-2.9   Range 

  0.41±0.315 1.98 ±0.850   median 

 56  50 No. 

  Table(2): The mean level of cytokine and chemokine in sera of   pregnant               
women with acute toxoplasmosis and control.        

Cytokine 
Serum Level (Mean ± S.E.; pg/ml) 

LSD value Controls  
(No. = 50) 

Patients 
(No. = 65) 

IL-6 6.38 ± 0.78   27.01 ± 3.31 7.396* 
IL-8   0.611 ± 0.01   0.805 ± 0.03 0.083* 

IL-12 0.56 ± 0.12 2.47 ± 0.35 5.478* 
TNF-α     0.040 ± 0.002   0.056± 0.003 0.0087* 
IP-10 6.68 ± 0.76 26.39 ± 2.80 6.299* 
MIP-1 3.50-± 0.31 15.55 ± 1.63 3.628* 
MCP-1 11.25 ± 0.24 14.46 ± 1.38 3.845N.S. 
MIG-1 0.0004 ± 0.0047     0.009 ± 0.067 0.021* 
TGF-β1 1.52±0.05 20.99±4.13 9.05* 
1CAM  5.28 ± 0.61    13.33 ± 1.36  3.189*  

     N.S.: Not significant   : Significant*    (P < 0.05) 
 
Table -3: Serum Zn and Cu levels in pregnant women with acute toxoplasmosis  and 
control  

P value Mean(µM\L)±SD  Parameters 

Patients Controls  

p<0.05   5.68±0.61  9.99±1.44  Zn  
p<0.001 8.30±11.313 26.46±2.14  Cu 

      Significant    (P < 0.05), (p<0.001) 

 
 
 
 
 
 
 
 
 
 
 



 

Biology | 30 

2016) عام 2العدد (  29مجلة إبن الهيثم للعلوم الصرفة و التطبيقية                                                                            المجلد  

Ibn Al-Haitham J. for Pure & Appl. Sci.                                           Vol. 29 (2) 2016  
 

دور بعض الحركيات الخلوية  والعناصر النزرة لداء المقوسات الحاد في النساء 
  الحوامل

  
  وحيدة رشيد علي 

  / جامعة بغدادكلية التربية للعلوم الصرفة (ابن الهيثم )/قسم علوم الحياة
  

  2016ايار 11، قبل في: 2016كانون الثاني  5استلم في:
  

  الخالصة   
ى           ة عل ت الدراس ن   65اجري ف  ع د الكش اد بع ات الح داء المقوس ات ب ل المخمج اء الحوام ن النس م

داد ة االض ة الكوندي وع   للمقوس ن  ن تعمالبا IgMم ريع   س ائي الس اتوكرافي الثن يت)الكروم صو (كاس  فح
االنزيم  ( رتبط ب اعي الم اص المن زااالدمص ى  ,)االلي ا عل تملت ايض ن  50واش حاء م ات االص اء المتزوج النس

ل  ر الحوام يطرة  )(غي ة س ى  .كمجموع ري عل م التح ض ت والء بع دى  ه ج ل احبة للخم ة المص رات المناعي التغي
ة ات الخلوي ض الحركي تويات بع اس مس الل قي ن خ اد م ات الح داء المقوس ة ب ل المخمج اء الحوام  النس

ائج ارتفاع ة.اظهرت النت تويات   (P<0.005)امعنوي  اوالكيميائي -IL-6   ,IL8 ,IL-12,TNF-α, TGFبمس
β1,MIP-1, IP-10, MIG-1 ذلك جل ICAM وك م يس ا ل توى معنوي  -MCP  1بينم  (14.46   امس
يطرة ±1.38 ة بمجوعةالس ل ) مقارن وغرام /م ل ),0.24± (11.25بيك ذ بيكوغرام/م ن أن  هوه تتيمك  عملس

  لداء المقوسات الحاد. اتكمؤشر
ائج انخفاض رت النت وي p<0.05( امعنوي ااظه اع معن وحظ ارتف ا ل ل بينم ي المص ك ف ز الزن ي تركي ) ف

)p<0.001.في تركيز النحاس في مصل مريضات داء المقوسات الحاد مقارنة بالسيطرة غير المصابة (  
  

  رصين, النحاسامقوسات كوندي ,الحركيات الخلوية ,خ :الكلمات المفتاحية