Wed, Jan 15, 2025
Volume 17, Issue 6 (Nov-Dec 2023)
mljgoums 2023, 17(6): 10-12 |
Back to browse issues page
Download citation:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
BibTeX | RIS | EndNote | Medlars | ProCite | Reference Manager | RefWorks
Send citation to:
Shahbazi A E, Barati N, Soleymani E, Khandan Del P, Khandan Del A, Azizi N, et al . Association between toxoplasmosis and COVID-19 infection: A cross-sectional study. mljgoums 2023; 17 (6) :10-12
URL: http://mlj.goums.ac.ir/article-1-1575-en.html
URL: http://mlj.goums.ac.ir/article-1-1575-en.html
Ali Ehsan Shahbazi1 
, Nastaran Barati2 , Eissa Soleymani3 , Pegah Khandan Del4 , Abolfazl Khandan Del5 , Nemat Azizi1 , Behjat Ranjouri1 , Mehran Bakhtiari3 , Seyedmousa Motavallihaghi 6
, Nastaran Barati2 , Eissa Soleymani3 , Pegah Khandan Del4 , Abolfazl Khandan Del5 , Nemat Azizi1 , Behjat Ranjouri1 , Mehran Bakhtiari3 , Seyedmousa Motavallihaghi 6
1- School of Nursing and Midwifery, Saveh University of Medical Sciences, Saveh, Iran
2- Research Center for Molecular Medicine, Hamadan University of Medical Sciences, Hamadan, Iran
3- Department of Medical Parasitology and Mycology, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran
4- Department of Microbiology, Gorgan Branch, Islamic AzadUniversity, Gorgan, Iran
5- Department of Microbiology, 5th Azar Hospital, Golestan University of Hospital, Golestan University of Medical Sciences, Gorgan, Iran
6- Department of Medical Parasitology and Mycology, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran ,m_motevali@umsha.ac.ir
2- Research Center for Molecular Medicine, Hamadan University of Medical Sciences, Hamadan, Iran
3- Department of Medical Parasitology and Mycology, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran
4- Department of Microbiology, Gorgan Branch, Islamic AzadUniversity, Gorgan, Iran
5- Department of Microbiology, 5th Azar Hospital, Golestan University of Hospital, Golestan University of Medical Sciences, Gorgan, Iran
6- Department of Medical Parasitology and Mycology, School of Medicine, Hamadan University of Medical Sciences, Hamadan, Iran ,
Full-Text [PDF 350 kb]
(447 Downloads)
| Abstract (HTML) (1521 Views)
Full-Text: (358 Views)
Introduction
In December 2019, the COVID-19 virus initiated a pandemic of respiratory disease that affected the lower respiratory tract and caused acute respiratory distress syndrome (ARDS). The disease was a global health emergency and was predominantly transmitted from person to person through respiratory droplets, contact, and secretions (1). The common symptoms of COVID-19 include fever, chills, cough, myalgia, shortness of breath, and headache. However, in severe cases, the disease can manifest as respiratory distress, acute kidney or liver failure, metabolic acidosis, coagulation disorders, and septic shock (1, 2).
Individuals with immunodeficiency, autoimmune disorders, and organ transplant recipients are at a high risk for COVID-19 infection. Studies have revealed an inverse relationship between toxoplasmosis and COVID-19, highlighting the significance of their association (3-8).
Toxoplasma is an intracellular protozoan that infects humans, birds, and mammals (9-11). Humans contract toxoplasmosis by eating raw or undercooked meat products containing tissue cysts or oocysts through contaminated food or by contact with infected cat feces. The prevalence of toxoplasmosis varies depending on factors such as health level, temperature, humidity, pet contact, and contact with soil (12-16). Most patients with a normal immune system remain asymptomatic, but 20-30% of cases show mild fever, lymphadenopathy, and skin rash. In congenital toxoplasmosis, patients with an immunocompromised state may develop severe manifestations such as central nervous system (CNS) disorders, encephalopathy, pneumonia, myocarditis, and brain calcification (12, 14, 17).
The level of community infection depends on many factors, such as health level, ambient temperature, humidity, contact with soil and pets, and the most common mode of transmission is through contact with infected cat feces (18). This opportunistic parasite is present in about one-third of the world's population. In Iran, some areas have reported a seroprevalence rate of more than 70%. Various methods are used to identify toxoplasmosis, including parasitology, histology, and various serological methods, such as the Sabin-Feldman dye test (DT), indirect hemagglutination (IHA), immunofluorescence assay (IFA), enzyme-linked immunosorbent assay (ELISA), and direct agglutination (DA). DNA-based methods, such as polymerase chain reaction (PCR) and real-time PCR, are also used for diagnosis (19, 20). This present study aimed to evaluate the seroprevalence of COVID-19 in individuals with toxoplasmosis infection and to establish the relationship between the two diseases.
Methods
The current study involved a cross-sectional descriptive analysis that included 360 patients referred to health centers in Saveh, Iran. Among the individuals, 50% were men and 50% were women. Blood samples were collected, and an ELISA kit provided by Pishtaz Teb, Iran, was used to classify 180 participants as COVID-positive, designating them as the experimental group. The remaining 180 participants tested negative and served as the control group. Demographic data, including sex, age range, and occupation, were also recorded through questionnaires. Finally, a comparison was made between the experimental group with anti-COVID-19 antibodies and an equal number of healthy individuals in the control group, with sex matching.
The study involved assessing the titers of IgG and IgM antibodies specific to anti-COVID-19 using the protocol provided by the kit manufacturer (Pishtaz Teb, Iran; SARS-COV-2 IgG & SARS-COV-2 IgM). Individual serum samples (100 μL) were transferred to 96-well plates coated with SARS-COV-2-specific antigens. The plates were then incubated for 30 minutes at 37 °C and washed 5 times using an ELISA washer. A conjugated enzyme (100 μL) was then added to each well and incubated for another 30 minutes before emptying and washing the contents 3 times. The next step involved adding 100 μL of the dye solution and keeping the plates in the dark for 15 minutes at room temperature. Afterward, 100 μL of the stop solution was added to complete the reaction. Finally, the plates' light absorption was read against the blank (100 μL of the dye solution, incubated in the dark for 15 minutes at room temperature, and then 100 μL of the stop solution) using an ELISA reader at a wavelength of 450 nm. A value above 1.1 was considered positive, while a value below 0.9 was deemed negative as per the manufacturer's instructions. The Pishtaz Teb kit had a sensitivity of 94.1 and 79.4 and specificity values of 98.3 and 99.3 for IgG and IgM antibody diagnostic tests for anti-COVID-19, respectively.
The present study utilized the Pishtaz Teb Company kit to measure the anti-Toxoplasma IgG antibody titer through the ELISA method. The kit utilizes the capture antibody approach, wherein the plate wells are coated with antihuman IgM and IgG antibodies. During testing, diluted serum samples are poured into the wells, where their IgG antibodies, including anti-Toxoplasma IgG, bind to the antihuman antibodies coated in the wells. After an initial washing step, the unbound antibodies are removed. Next, the Toxoplasma antigen is conjugated to Horseradish Peroxidase (HRP), and this antigen also binds to Toxoplasma-specific IgG antibodies in the serum samples and forms a complex. After another washing step, the dye solution is added to the wells, and the intensity of the resulting blue color is proportional to the immune complexes formed within the wells. The addition of the stop solution turns the blue solution into yellow, which has the best light absorption at 450 nm. Finally, the kit defines values above 1.1 as positive and values below 0.9 as negative.
Chi-square and Fisher's exact tests were utilized for data analysis, and a confidence level of 95% was set. The significance level was considered less than 0.05.
Results
Out of the 180 people with COVID-19, 57 individuals (31.7%) had toxoplasmosis antibodies. Additionally, among the 180 people in the control group who did not have COVID-19 antibodies, 38 individuals (21%) tested positive for toxoplasmosis antibodies. Statistically, no significant difference was observed between the 2 groups, although the rate of toxoplasmosis cases was higher in the COVID-19 group, such that the odds ratio was 1.73; this means that the probability of infection with COVID-19 in individuals with toxoplasmosis infection is 1.73 times higher than in people without toxoplasmosis antibodies.
Based on the age distribution of people who had COVID-19 and toxoplasmosis in the studied groups, the percentages of individuals aged 0-15, 16-30, 31-45, 46-60, and over 60 years old were 6%, 7%, 9%, 3%, and 6%, respectively. Moreover, as can be seen in Table 1, the results of the occupation survey of individuals who had both COVID-19 antibodies and toxoplasmosis indicated that the highest infection rate was observed among the self-employed group.
Discussion
Even with the frequent use of wide-ranging antimicrobial treatments among patients with respiratory infections related to the coronavirus, cases of co-infection with bacteria and fungi have been observed (21). COVID-19 patients often suffer from co-infection with Gram-negative bacilli and Candida. The virus can damage airway epithelial tissue, reduce mucosal clearance, and weaken immunity, leading to such co-infections (22). There have been reports indicating a negative correlation between COVID-19 incidence and certain parasitic diseases, such as malaria (where countries with endemic malaria were less likely to have cases of COVID-19), and the modulatory role of some parasites in the immune system based on some studies (23). However, other studies have shown conflicting results, indicating an increased risk of COVID-19 when a parasitic disease is present (24).
An infection with toxoplasmosis has been linked to higher severity of COVID-19 infection. This may be due to increased expression of Toxoplasma-associated PD-1 (programmed cell death protein 1) in lymphocytes, which is a critical checkpoint for T cell exhaustion. While it is a vital molecule for maintaining environmental tolerance, T cells become less effective when its expression is increased, leading to inhibitory signals that interfere with T cell proliferation, function, metabolic activity, and hemostatic self-renewal. These conditions, which compromise the first defense against the virus, are responsible for the considerable increase in the viral load, leading to severe clinical manifestations and potentially fatal outcomes (25-27).
An elevated level of serum anti-T. gondii IgG – which is also raised in COVID-19 patients – has been found to be even higher in cases classified as severe. This observation suggests that chronic toxoplasmosis reactivates more readily in COVID-19 patients due to the immune fatigue induced by the disease (24). This reactivation of toxoplasmosis exacerbates the intensity of COVID-19 and can be attributed to the significant increase in all cytokines, including IL-1β, IL-6, TNFα, IFN-γ, and IL-1α, which were the highest in severe COVID-19 cases among those infected with T. gondii (24). Serum cytokine levels play a crucial role in predicting the prognosis of COVID-19 and the likelihood of a cytokine storm. For instance, elevated levels of interleukin-6 in certain COVID-19 patients indicate a poor prognosis and may be suppressed with drugs such as tocilizumab (28). In this study, there was no significant relationship between COVID-19 and toxoplasmosis, but our results showed that the incidence rate in people who had toxoplasmosis antibodies was 1.73 times higher than those who did not have toxoplasmosis antibodies.
Experimental evidence indicates that cats and dogs can contract SARS-CoV-2 infections with or without displaying symptoms (29, 30). A recent study carried out in Spain revealed that stray cats were exposed to SARS-CoV-2 and had co-infections with other pathogens, including T. gondii. This suggests that animals with weakened immune systems may be more susceptible to SARS-CoV-2 infection (31). Latent toxoplasmosis, in general, appears to make human hosts more prone to experiencing various adverse effects from genetic factors and pathogens. In Minnesota, the USA, a study found that 8% and 1% of 239 domestic cats and 510 domestic dogs, respectively, had SARS-CoV-2 seroprevalence. Additionally, a study conducted in Germany reported a seroprevalence of 0.7% in cats during the first wave of COVID-19, which increased to 1.4% after the second wave (32). Latent toxoplasmosis, in general, appears to make human hosts more prone to experiencing numerous adverse effects from genetic factors and pathogens (33).
Meta-regression techniques used to analyze infection mortality rates based on age indicate an exponential correlation between age and COVID-19 infection mortality rates. The risk of mortality due to COVID-19 infection is believed to be very low in children and young adults but gradually increases with age. However, the results of the chi-square test performed in this study showed no correlation between age, occupation, and COVID-19 (34). Conversely, this analysis revealed a significant association between COVID-19 and sex, although other studies have reported an equal prevalence of the disease among both sexes. Regardless of age, men who contract COVID-19 face a higher risk of severe outcomes and death.
Conclusion
According to the study's findings, individuals who have a toxoplasmosis infection are more likely to contract COVID-19. There was no significant association found between age, occupation, and COVID-19 infection. The prevalence and activity of T. gondii were observed to be higher in severe cases of COVID-19 and were linked to increased levels of poorly prognostic cytokines in the bloodstream. Moreover, sex displayed a significant correlation with COVID-19 infection. Together, the outcomes of this and comparable studies propose that infectious agents may act as a predisposing factor, potentially due to changes in serum cytokine levels. Further investigation into cytokines and other factors is necessary to acquire a more comprehensive understanding of these associations.
Acknowledgement
The authors would like to acknowledge the financial support of the Student Research Committee of Saveh University of Medical Sciences, Saveh, Iran.
Funding sources
This study was supported by the Student Research Committee of Saveh University of Medical Sciences, Saveh, Iran (Project No. 990326).
Ethical statement
This study has ethical approval from the Ethics Committee of Saveh University of Medical Sciences (Code: IR.SAVEHUMS.REC.1399.035). Informed consent was obtained from all the participants. All the procedures were performed in accordance with relevant guidelines and regulations.
All the experiments were carried out in accordance with the guidelines of the Ethics Committee (R.SAVEHUMS.REC.1399.035) of Saveh University of Medical Sciences, Saveh, Iran.
Conflicts of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Author contributions
Seyedmousa Motavallihaghi, Nastan Barati, and Eissa Soleymani: Conceptualization, Methodology, Data analysis, Writing, and Editing. Ali Ehsan Shahbazi, Behjat Ranjouri, and Abolfazl Khandan Del: Investigation, Data collection, Data analysis, and Writing (Original Draft). Nemat Azizi, Pegah Khandan Del, and Mehran Bakhtiari: Methodology and Writing.
In December 2019, the COVID-19 virus initiated a pandemic of respiratory disease that affected the lower respiratory tract and caused acute respiratory distress syndrome (ARDS). The disease was a global health emergency and was predominantly transmitted from person to person through respiratory droplets, contact, and secretions (1). The common symptoms of COVID-19 include fever, chills, cough, myalgia, shortness of breath, and headache. However, in severe cases, the disease can manifest as respiratory distress, acute kidney or liver failure, metabolic acidosis, coagulation disorders, and septic shock (1, 2).
Individuals with immunodeficiency, autoimmune disorders, and organ transplant recipients are at a high risk for COVID-19 infection. Studies have revealed an inverse relationship between toxoplasmosis and COVID-19, highlighting the significance of their association (3-8).
Toxoplasma is an intracellular protozoan that infects humans, birds, and mammals (9-11). Humans contract toxoplasmosis by eating raw or undercooked meat products containing tissue cysts or oocysts through contaminated food or by contact with infected cat feces. The prevalence of toxoplasmosis varies depending on factors such as health level, temperature, humidity, pet contact, and contact with soil (12-16). Most patients with a normal immune system remain asymptomatic, but 20-30% of cases show mild fever, lymphadenopathy, and skin rash. In congenital toxoplasmosis, patients with an immunocompromised state may develop severe manifestations such as central nervous system (CNS) disorders, encephalopathy, pneumonia, myocarditis, and brain calcification (12, 14, 17).
The level of community infection depends on many factors, such as health level, ambient temperature, humidity, contact with soil and pets, and the most common mode of transmission is through contact with infected cat feces (18). This opportunistic parasite is present in about one-third of the world's population. In Iran, some areas have reported a seroprevalence rate of more than 70%. Various methods are used to identify toxoplasmosis, including parasitology, histology, and various serological methods, such as the Sabin-Feldman dye test (DT), indirect hemagglutination (IHA), immunofluorescence assay (IFA), enzyme-linked immunosorbent assay (ELISA), and direct agglutination (DA). DNA-based methods, such as polymerase chain reaction (PCR) and real-time PCR, are also used for diagnosis (19, 20). This present study aimed to evaluate the seroprevalence of COVID-19 in individuals with toxoplasmosis infection and to establish the relationship between the two diseases.
Methods
The current study involved a cross-sectional descriptive analysis that included 360 patients referred to health centers in Saveh, Iran. Among the individuals, 50% were men and 50% were women. Blood samples were collected, and an ELISA kit provided by Pishtaz Teb, Iran, was used to classify 180 participants as COVID-positive, designating them as the experimental group. The remaining 180 participants tested negative and served as the control group. Demographic data, including sex, age range, and occupation, were also recorded through questionnaires. Finally, a comparison was made between the experimental group with anti-COVID-19 antibodies and an equal number of healthy individuals in the control group, with sex matching.
The study involved assessing the titers of IgG and IgM antibodies specific to anti-COVID-19 using the protocol provided by the kit manufacturer (Pishtaz Teb, Iran; SARS-COV-2 IgG & SARS-COV-2 IgM). Individual serum samples (100 μL) were transferred to 96-well plates coated with SARS-COV-2-specific antigens. The plates were then incubated for 30 minutes at 37 °C and washed 5 times using an ELISA washer. A conjugated enzyme (100 μL) was then added to each well and incubated for another 30 minutes before emptying and washing the contents 3 times. The next step involved adding 100 μL of the dye solution and keeping the plates in the dark for 15 minutes at room temperature. Afterward, 100 μL of the stop solution was added to complete the reaction. Finally, the plates' light absorption was read against the blank (100 μL of the dye solution, incubated in the dark for 15 minutes at room temperature, and then 100 μL of the stop solution) using an ELISA reader at a wavelength of 450 nm. A value above 1.1 was considered positive, while a value below 0.9 was deemed negative as per the manufacturer's instructions. The Pishtaz Teb kit had a sensitivity of 94.1 and 79.4 and specificity values of 98.3 and 99.3 for IgG and IgM antibody diagnostic tests for anti-COVID-19, respectively.
The present study utilized the Pishtaz Teb Company kit to measure the anti-Toxoplasma IgG antibody titer through the ELISA method. The kit utilizes the capture antibody approach, wherein the plate wells are coated with antihuman IgM and IgG antibodies. During testing, diluted serum samples are poured into the wells, where their IgG antibodies, including anti-Toxoplasma IgG, bind to the antihuman antibodies coated in the wells. After an initial washing step, the unbound antibodies are removed. Next, the Toxoplasma antigen is conjugated to Horseradish Peroxidase (HRP), and this antigen also binds to Toxoplasma-specific IgG antibodies in the serum samples and forms a complex. After another washing step, the dye solution is added to the wells, and the intensity of the resulting blue color is proportional to the immune complexes formed within the wells. The addition of the stop solution turns the blue solution into yellow, which has the best light absorption at 450 nm. Finally, the kit defines values above 1.1 as positive and values below 0.9 as negative.
Chi-square and Fisher's exact tests were utilized for data analysis, and a confidence level of 95% was set. The significance level was considered less than 0.05.
Results
Out of the 180 people with COVID-19, 57 individuals (31.7%) had toxoplasmosis antibodies. Additionally, among the 180 people in the control group who did not have COVID-19 antibodies, 38 individuals (21%) tested positive for toxoplasmosis antibodies. Statistically, no significant difference was observed between the 2 groups, although the rate of toxoplasmosis cases was higher in the COVID-19 group, such that the odds ratio was 1.73; this means that the probability of infection with COVID-19 in individuals with toxoplasmosis infection is 1.73 times higher than in people without toxoplasmosis antibodies.
Based on the age distribution of people who had COVID-19 and toxoplasmosis in the studied groups, the percentages of individuals aged 0-15, 16-30, 31-45, 46-60, and over 60 years old were 6%, 7%, 9%, 3%, and 6%, respectively. Moreover, as can be seen in Table 1, the results of the occupation survey of individuals who had both COVID-19 antibodies and toxoplasmosis indicated that the highest infection rate was observed among the self-employed group.
|
Table 1. Frequency of co-infection with COVID-19 and toxoplasmosis based on the individuals' occupations
 |
Discussion
Even with the frequent use of wide-ranging antimicrobial treatments among patients with respiratory infections related to the coronavirus, cases of co-infection with bacteria and fungi have been observed (21). COVID-19 patients often suffer from co-infection with Gram-negative bacilli and Candida. The virus can damage airway epithelial tissue, reduce mucosal clearance, and weaken immunity, leading to such co-infections (22). There have been reports indicating a negative correlation between COVID-19 incidence and certain parasitic diseases, such as malaria (where countries with endemic malaria were less likely to have cases of COVID-19), and the modulatory role of some parasites in the immune system based on some studies (23). However, other studies have shown conflicting results, indicating an increased risk of COVID-19 when a parasitic disease is present (24).
An infection with toxoplasmosis has been linked to higher severity of COVID-19 infection. This may be due to increased expression of Toxoplasma-associated PD-1 (programmed cell death protein 1) in lymphocytes, which is a critical checkpoint for T cell exhaustion. While it is a vital molecule for maintaining environmental tolerance, T cells become less effective when its expression is increased, leading to inhibitory signals that interfere with T cell proliferation, function, metabolic activity, and hemostatic self-renewal. These conditions, which compromise the first defense against the virus, are responsible for the considerable increase in the viral load, leading to severe clinical manifestations and potentially fatal outcomes (25-27).
An elevated level of serum anti-T. gondii IgG – which is also raised in COVID-19 patients – has been found to be even higher in cases classified as severe. This observation suggests that chronic toxoplasmosis reactivates more readily in COVID-19 patients due to the immune fatigue induced by the disease (24). This reactivation of toxoplasmosis exacerbates the intensity of COVID-19 and can be attributed to the significant increase in all cytokines, including IL-1β, IL-6, TNFα, IFN-γ, and IL-1α, which were the highest in severe COVID-19 cases among those infected with T. gondii (24). Serum cytokine levels play a crucial role in predicting the prognosis of COVID-19 and the likelihood of a cytokine storm. For instance, elevated levels of interleukin-6 in certain COVID-19 patients indicate a poor prognosis and may be suppressed with drugs such as tocilizumab (28). In this study, there was no significant relationship between COVID-19 and toxoplasmosis, but our results showed that the incidence rate in people who had toxoplasmosis antibodies was 1.73 times higher than those who did not have toxoplasmosis antibodies.
Experimental evidence indicates that cats and dogs can contract SARS-CoV-2 infections with or without displaying symptoms (29, 30). A recent study carried out in Spain revealed that stray cats were exposed to SARS-CoV-2 and had co-infections with other pathogens, including T. gondii. This suggests that animals with weakened immune systems may be more susceptible to SARS-CoV-2 infection (31). Latent toxoplasmosis, in general, appears to make human hosts more prone to experiencing various adverse effects from genetic factors and pathogens. In Minnesota, the USA, a study found that 8% and 1% of 239 domestic cats and 510 domestic dogs, respectively, had SARS-CoV-2 seroprevalence. Additionally, a study conducted in Germany reported a seroprevalence of 0.7% in cats during the first wave of COVID-19, which increased to 1.4% after the second wave (32). Latent toxoplasmosis, in general, appears to make human hosts more prone to experiencing numerous adverse effects from genetic factors and pathogens (33).
Meta-regression techniques used to analyze infection mortality rates based on age indicate an exponential correlation between age and COVID-19 infection mortality rates. The risk of mortality due to COVID-19 infection is believed to be very low in children and young adults but gradually increases with age. However, the results of the chi-square test performed in this study showed no correlation between age, occupation, and COVID-19 (34). Conversely, this analysis revealed a significant association between COVID-19 and sex, although other studies have reported an equal prevalence of the disease among both sexes. Regardless of age, men who contract COVID-19 face a higher risk of severe outcomes and death.
Conclusion
According to the study's findings, individuals who have a toxoplasmosis infection are more likely to contract COVID-19. There was no significant association found between age, occupation, and COVID-19 infection. The prevalence and activity of T. gondii were observed to be higher in severe cases of COVID-19 and were linked to increased levels of poorly prognostic cytokines in the bloodstream. Moreover, sex displayed a significant correlation with COVID-19 infection. Together, the outcomes of this and comparable studies propose that infectious agents may act as a predisposing factor, potentially due to changes in serum cytokine levels. Further investigation into cytokines and other factors is necessary to acquire a more comprehensive understanding of these associations.
Acknowledgement
The authors would like to acknowledge the financial support of the Student Research Committee of Saveh University of Medical Sciences, Saveh, Iran.
Funding sources
This study was supported by the Student Research Committee of Saveh University of Medical Sciences, Saveh, Iran (Project No. 990326).
Ethical statement
This study has ethical approval from the Ethics Committee of Saveh University of Medical Sciences (Code: IR.SAVEHUMS.REC.1399.035). Informed consent was obtained from all the participants. All the procedures were performed in accordance with relevant guidelines and regulations.
All the experiments were carried out in accordance with the guidelines of the Ethics Committee (R.SAVEHUMS.REC.1399.035) of Saveh University of Medical Sciences, Saveh, Iran.
Conflicts of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Author contributions
Seyedmousa Motavallihaghi, Nastan Barati, and Eissa Soleymani: Conceptualization, Methodology, Data analysis, Writing, and Editing. Ali Ehsan Shahbazi, Behjat Ranjouri, and Abolfazl Khandan Del: Investigation, Data collection, Data analysis, and Writing (Original Draft). Nemat Azizi, Pegah Khandan Del, and Mehran Bakhtiari: Methodology and Writing.
Research Article: Research Article |
Subject:
Parasitology
Received: 2022/09/11 | Accepted: 2023/01/23 | Published: 2024/02/26 | ePublished: 2024/02/26
Received: 2022/09/11 | Accepted: 2023/01/23 | Published: 2024/02/26 | ePublished: 2024/02/26
References
1. Wang Y, Wang Y, Chen Y, Qin Q. Unique epidemiological and clinical features of the emerging 2019 novel coronavirus pneumonia (COVID‐19) implicate special control measures. Journal of medical virology. 2020;92(6):568-76. [View at Publisher] [DOI] [PMID] [Google Scholar]
2. Cao W. Clinical features and laboratory inspection of novel coronavirus pneumonia (COVID-19) in Xiangyang, Hubei. medRxiv. 2020. [View at Publisher] [DOI] [Google Scholar]
3. Manesh RM, Safa AH, Sharafi SM, Jafari R, Bahadoran M, Yousefi M, et al. Parasites and chronic renal failure. Journal of renal injury prevention. 2014;3(4):87. [View at Publisher] [Google Scholar]
4. Russell B, Moss C, George G, Santaolalla A, Cope A, Papa S, et al. Associations between immune-suppressive and stimulating drugs and novel COVID-19-a systematic review of current evidence. ecancermedicalscience. 2020;14. [View at Publisher] [DOI] [Google Scholar]
5. Slimano F, Baudouin A, Zerbit J, Toulemonde-Deldicque A, Thomas-Schoemann A, Chevrier R, et al. Cancer, immune suppression and Coronavirus Disease-19 (COVID-19): Need to manage drug safety (French Society for Oncology Pharmacy [SFPO] guidelines). Cancer treatment reviews. 2020;88. [View at Publisher] [DOI] [PMID] [Google Scholar]
6. Zadeh AE, Bamedi T, Etemadi S, Shahrakipour M, Saryazdipour K. Toxoplasmosis as a complication of transfusion in hemodialysis patients. Iranian journal of pediatric hematology and oncology. 2014;4(1):22. [View at Publisher] [Google Scholar]
7. Zhong J, Tang J, Ye C, Dong L. The immunology of COVID-19: is immune modulation an option for treatment? The Lancet Rheumatology. 2020. [View at Publisher] [DOI] [PMID] [Google Scholar]
8. Jankowiak Ł, Rozsa L, Tryjanowski P, Møller AP. Strong negative covariation between toxoplasmosis and CoVID-19 at a global scale: a spurious indirect effect? 2020. [View at Publisher] [DOI] [Google Scholar]
9. Alavi SM, Alavi L. Toxoplasmosis in Iran: A guide for general physicians working in the Iranian health network setting: A systematic review. Caspian Journal of Internal Medicine. 2016;7(4):233. [View at Publisher] [PMID] [Google Scholar]
10. Alghamdi J, Elamin MH, Alhabib S. Prevalence and genotyping of Toxoplasma gondii among Saudi pregnant women in Saudi Arabia. Saudi Pharmaceutical Journal. 2016;24(6):645-51. [View at Publisher] [DOI] [PMID] [Google Scholar]
11. Zeleke AJ, Melsew YA. Seroprevalence of Toxoplasma gondii and associated risk factors among HIV-infected women within reproductive age group at Mizan Aman General Hospital, Southwest Ethiopia: a cross sectional study. BMC Research Notes. 2017;10(1):70. [View at Publisher] [DOI] [PMID] [Google Scholar]
12. Maraghi S, Yadyad MJ, Sheikhi M, Shamakhteh F, Latifi SM. Study the anti-Toxoplasma antibodies (IgG and IgM) in hemodialysis patients of Abadan and Khoramshahr cities Southwest Iran in 2011 using ELISA. Jundishapur Journal of Microbiology. 2013;6(7). [View at Publisher] [DOI] [Google Scholar]
13. Motevalli Haghi SM, Fakhar M, Sharif M, Keyghobadi M. An overview on different diagnostic methods for babesiosis. Journal of Mazandaran University of Medical Sciences. 2014;23(109):283-95. [View at Publisher] [Google Scholar]
14. Norouzi M, TABAEI SJS, Niyyati M, Saber V, Behniafar H. Genotyping of Toxoplasma gondii Strains Isolated from Patients with Ocular Toxoplasmosis in Iran. Iranian Journal of Parasitology. 2016;11(3):316-24. [View at Publisher] [Google Scholar]
15. Motevalli Haghi SM, Najm M, Fakhar M, Gholami S, MotevalliHaghi S. Prevalence of Enterobius vermicularis infection among kindergartens of Sari and Babol cities during 2011. Journal of Mazandaran University of Medical Sciences. 2013;22(1):240-2. [View at Publisher] [Google Scholar]
16. Shen B, Yuan Y, Cheng J, Pan M, Xia N, Zhang W, et al. Activation of chronic toxoplasmosis by transportation stress in a mouse model. Oncotarget. 2016;7(52):87351-60. [View at Publisher] [DOI] [PMID] [Google Scholar]
17. Haghi MM, Khorshidvand Z, Khazaei S, Foroughi-Parvar F, Sarmadian H, Barati N, et al. Cryptosporidium animal species in Iran: a systematic review and meta-analysis. Tropical Medicine and Health. 2020;48(1):1-15. [View at Publisher] [DOI] [PMID] [Google Scholar]
18. Amany M, Eid R, Fahmy B. Biochemical studies on the effect of Toxoplasma infection on liver and kidney functions in mice. Egyptain Journal of Comparative Pathology and Clinical Pathology. 2010;23(1). [View at Publisher] [Google Scholar]
19. Gharavi M, Jalali S, Khademvatan S, Heydari S. Detection of IgM and IgG anti-Toxoplasma antibodies in renal transplant recipients using ELFA, ELISA and ISAGA methods: comparison of pre-and post-transplantation status. Annals of Tropical Medicine & Parasitology. 2011;105(5):367-71. [View at Publisher] [DOI] [PMID] [Google Scholar]
20. Shahbazi AE, Saidijam M, Maghsood AH, Matini M, Haghi MM, Fallah M. Genotyping of fresh and Parafinized human hydatid cysts using nad1 and cox1 genes in Hamadan Province, west of Iran. Iranian Journal of Parasitology. 2020;15(2):259. [View at Publisher] [DOI] [PMID] [Google Scholar]
21. Rawson TM, Moore LS, Zhu N, Ranganathan N, Skolimowska K, Gilchrist M, et al. Bacterial and fungal coinfection in individuals with coronavirus: a rapid review to support COVID-19 antimicrobial prescribing. Clinical Infectious Diseases. 2020;71(9):2459-68. [View at Publisher] [DOI] [PMID] [Google Scholar]
22. Chen X, Liao B, Cheng L, Peng X, Xu X, Li Y, et al. The microbial coinfection in COVID-19. Applied microbiology and biotechnology. 2020:1-9. [View at Publisher] [DOI] [PMID] [Google Scholar]
23. Ssebambulidde K, Segawa I, Abuga KM, Nakate V, Kayiira A, Ellis J, et al. Parasites and their protection against COVID-19-Ecology or Immunology? MedRxiv. 2020. [View at Publisher] [DOI] [Google Scholar]
24. Sharaf-El-Deen SA. Toxoplasma gondii as a possible risk factor for COVID-19 severity: a case-control study. Egyptian Journal of Medical Microbiology. 2021;30(2):125-32. [View at Publisher] [DOI] [Google Scholar]
25. Chiappelli F, Khakshooy A, Greenberg G. CoViD-19 immunopathology and immunotherapy. Bioinformation. 2020;16(3):219. [View at Publisher] [DOI] [PMID] [Google Scholar]
26. De Biasi S, Meschiari M, Gibellini L, Bellinazzi C, Borella R, Fidanza L, et al. Marked T cell activation, senescence, exhaustion and skewing towards TH17 in patients with COVID-19 pneumonia. Nature communications. 2020;11(1):1-17. [View at Publisher] [DOI] [PMID] [Google Scholar]
27. Winkler F, Bengsch B. Use of mass cytometry to profile human T cell exhaustion. Frontiers in immunology. 2020;10:3039. [View at Publisher] [DOI] [PMID] [Google Scholar]
28. Luo P, Liu Y, Qiu L, Liu X, Liu D, Li J. Tocilizumab treatment in COVID‐19: a single center experience. Journal of medical virology. 2020;92(7):814-8. [View at Publisher] [DOI] [PMID] [Google Scholar]
29. Dróżdż M, Krzyżek P, Dudek B, Makuch S, Janczura A, Paluch E. Current State of Knowledge about Role of Pets in Zoonotic Transmission of SARS-CoV-2. Viruses. 2021;13(6):1149. [View at Publisher] [DOI] [PMID] [Google Scholar]
30. Giraldo-Ramirez S, Rendon-Marin S, Jaimes JA, Martinez-Gutierrez M, Ruiz-Saenz J. SARS-CoV-2 clinical outcome in domestic and wild cats: A systematic review. Animals. 2021;11(7):2056. [View at Publisher] [DOI] [PMID] [Google Scholar]
31. Villanueva‐Saz S, Giner J, Tobajas AP, Pérez MD, González‐Ramírez AM, Macías‐León J, et al. Serological evidence of SARS‐CoV‐2 and co‐infections in stray cats in Spain. Transboundary and Emerging Diseases. 2021. [View at Publisher] [DOI] [PMID] [Google Scholar]
32. Michelitsch A, Schön J, Hoffmann D, Beer M, Wernike K. The Second Wave of SARS-CoV-2 Circulation-Antibody Detection in the Domestic Cat Population in Germany. Viruses. 2021;13(6):1009. [View at Publisher] [DOI] [PMID] [Google Scholar]
33. Flegr J. Toxoplasmosis is a risk factor for acquiring SARS-CoV-2 infection and a severe course of COVID-19 in the Czech and Slovak population: a preregistered exploratory internet cross-sectional study. Parasites & Vectors. 2021;14(1):1-11. [View at Publisher] [DOI] [PMID] [Google Scholar]
34. Levin AT, Hanage WP, Owusu-Boaitey N, Cochran KB, Walsh SP, Meyerowitz-Katz G. Assessing the age specificity of infection fatality rates for COVID-19: systematic review, meta-analysis, and public policy implications. European journal of epidemiology. 2020:1-16. [View at Publisher] [DOI] [Google Scholar]
Send email to the article author
| Rights and permissions | |
 |
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
Enamad
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.