Abstract
Background:
Toxoplasma gondii is an opportunistic protozoan parasite that causes a life-threatening disease – toxoplasmosis – in immunocompromised individuals, including patients with cancer. This prospective cross-sectional study set out to determine the prevalence of toxoplasmosis in patients with cancer compared with that of healthy individuals.
Methods:
A prospective cross-sectional study was conducted in Sulaimani City of Iraq from November 2019 to May 2020. Anti-T. gondii IgG and IgM antibodies were measured in the blood samples of 113 patients with cancer (80 with solid organ tumors and 33 with haematological malignancies) entered to Hiwa Cancer Hospital and 82 healthy controls, who were referred to the Directorate of Blood Transfusion for blood donation, using chemiluminescence microparticle immunoassay (CMIA).
Results:
The prevalence of anti-T. gondii IgG was 39.8% in the patient group and 24.4% in the control group, which amounted to a significant difference (P = 0.024). Only one case of anti-T. gondii IgM positivity was observed in the patient group, and no IgM seropositivity was reported in the control group. Moreover, the seroprevalence of anti-T. gondii IgG was non-significantly higher (P = 0.102) in the patients with haematological malignancies (51.5%) than in those with solid organ tumors (35%). Occupation was the only risk factor which had a significant association with T gondii infection (odds ratio [OR]: 1.3, 95% confidence interval [CI]: 0.6746163 - 2.4282788, P = 0.029).
Conclusion:
The prevalence of T. gondii infection is higher in patients with cancer than in healthy individuals. Therefore, T. gondii screening in patients with cancer is recommended.
Keywords: Toxoplasma gondii, Seroprevalence, Cancer, Opportunistic infection, Immunocompromised patients
Introduction
Toxoplasma gondii is an apicomplexan parasite and an obligatory zoonotic intracellular opportunistic pathogen (1–3). It is ubiquitous, infecting a wide range of warm-blooded animals, including one-third of the world’s human population (4). The seroprevalence of toxoplasmosis varies markedly among regions worldwide, ranging between 0.5% and 87.7% (5), depending on the degree of exposure to the oocysts (infective stage) or on climatic conditions, socioeconomic standards, and nutritional behaviors (6–8).
Humans are primarily infected by the disease when they eat undercooked or raw meat that contains tissue cysts from an infected host or any food contaminated with oocysts shed in the feces of infected cats (9). Although uncommon, T. gondii can also be transmitted through drinking water (10, 11), mother-to-child transmission during pregnancy (12), blood transfusion, and organ transplants (13–15).
In individuals with a normal immune system, T. gondii infection is usually asymptomatic (latent) and harmless and often passes unnoticed; however, in immunosuppressed and immunodeficient individuals (e.g., patients with AIDS, patients receiving hemodialysis, organ transplant recipients, and patients receiving chemotherapy for cancer), it is complicated and fatal, if not treated (16–19). Patients with cancer are often considered immunocompromised because of the nature of the anti-neoplastic treatment they receive (e.g., chemotherapy and/or radiotherapy) or the primary disease. In such cases, the infection is the result of reactivation of the latent phase (chronic infection) and transition into the active phase (acute phase) rather than a primary infection (20, 21).
In immunocompromised patients, IgM antibodies, which are the first antibodies to be detected after 7–15 days of infection, indicate the presence of acute infection; meanwhile, IgG antibodies indicate the presence of chronic infection, and elevated titers may show reactivation of infection (22). Serological techniques are commonly used. They remain the primary routine diagnostic tool for identifying anti-T. gondii antibodies in patients with cancer (23). Serological evidence of the presence of anti-T. gondii IgG and IgM have been related to numerous cancer cases in various regions worldwide (24–26). For instance, a study conducted in Saudi Arabia showed that the seropositivity rate was 30.6% (anti-T. gondii IgM and IgG) among patients with cancer (27). In Jordan, 39.5% and 2.5% of 200 patients with cancer were seropositive for anti-T. gondii IgG and IgM compared with 12.2% and 1.1% of 90 controls, respectively (28).
To the best of our knowledge, however, only one study has investigated the seroprevalence and risk factors of T. gondii infection in patients with cancer (i.e., leukemia) in the Kurdistan Region (29), while several studies have been carried out on pregnant women and women of childbearing age (30–32). Therefore, this study set out to examine the prevalence of anti-T. gondii antibodies in patients with cancer at Hiwa Cancer Hospital (HCH) in Sulaymaniyah City, Kurdistan Region, Iraq, compared with that in healthy individuals.
Materials and Methods
Study Population and Blood Sampling
This prospective cross-sectional study was conducted from November 2019 to May 2020. Serum and plasma samples were collected from 195 individuals aged between 9 and 86 years. The study population consisted of 113 patients with cancer who visited HCH and 82 immunocompetent healthy controls, who were referred to the Directorate of Blood Transfusion for blood donation. The patients with cancer were categorized into two subgroups: patients with solid organ tumors (n = 80) and those with hematological malignancies (n = 33).
The study was approved by the research Ethics Committee of the College of Science, University of Sulaimani (Certificate No. 7/12/4110 dated on 12 Nov. 2019). Before blood sample collection, each participant signed a written consent form.
The aims of the experiment were explained to all participants. Socio-demographic data (age, gender, occupation, residency, and contact with cats) were collected from the patient and control groups using a structured questionnaire. In addition, the type of cancer was recorded for the cancer patients. Venous blood samples were obtained from each participant. After centrifugation, the sera and plasma were separated and preserved in labelled Eppendorf tubes at a temperature of −20°C until further examination.
Anti-Toxoplasma antibody determination:
To identify anti-T. gondii IgG and IgM antibodies, chemiluminescence microparticle immunoassay (Abbott ARCHITECT i100-0SR) was performed using ARCHITECT Toxo. IgG and IgM commercial kits (Architect i Systems, Germany), respectively. The procedures were performed following the manufacturer’s instructions. Specimens with a concentration of ≥ 3.0 IU/mL were considered reactive (positive) for T. gondii IgG antibodies, while those with an index of ≥ 0.60 (≥ 1.00 S/CO) were considered reactive for T. gondii IgM antibodies.
Statistical analysis
The collected data of the population groups were entered into Excel sheets and then were analyzed using SPSS for Windows, version 20 (IBM Corp., Armonk, N.Y., USA). The seroprevalence of toxoplasmosis among the patient and control groups was calculated, and its associations with variables were evaluated. The chi-square test was used to compare qualitative variables, and associations that showed P-values of < 0.05 were considered significant.
Results
The age of the patient group ranged between 9 and 86 years (M ± SD: 52.6 ± 16.9 years). More specifically, the group consisted of 69 women aged between 18 and 86 years (M ± SD: 51.8 ± 16.1 years) and 44 men aged between 9 and 82 years (M ± SD: 53.9 ± 18.4 years). Meanwhile, the age of the control group ranged between 10 and 70 years (M ± SD: 36.2 ± 11.2 years). More specifically, the group consisted of 37 women aged between 10 and 69 years (M ± SD: 32.2 ± 11.7 years) and 45 men aged between 22 and 70 years (M ± SD: 39.4 ± 9.8 years).
As shown in Table 1, the difference in the IgG seropositivity between the patient and control groups was significant (P < 0.024).
Table 1:
Anti-Toxoplasma gondii IgG antibodies between the patients with cancer and controls
| Anti-Toxoplasma Abs | Patients n = 113 (%) | Controls n = 82 (%) | P. value | |
|---|---|---|---|---|
| IgG | Reactive (positive) | 45 (39.8) | 20 (24.4) | |
| Non-reactive (negative) | 68 (60.2) | 62 (75.6) | 0.024 * | |
The patient group included 80 patients with solid organ tumors and 33 patients with haematological malignancies (Table 2). The prevalence of anti-T. gondii IgG antibodies in the patients with haematological malignancies (51.5%; n = 17) were non-significantly (P < 0.102) higher than that in the patients with solid organ tumors (35%; n = 28) (Table 2).
Table 2:
Association of the seropositivity for Toxoplasma gondii IgG in all cancer types and its distribution between the patients with haematological malignancies and solid organ tumors
| Cancer types (n = 113) | IgG (+ve) | Classification of Tumors | No. | IgG (+ve) | |
|---|---|---|---|---|---|
|
| |||||
| No. | P. value | ||||
| Hematological malignancies (n = 33) | 17 (51.5%) | Leukemia | 13 | 7 | |
| Lymphoma | 8 | 4 | 0.102 | ||
| Hodgkin lymphoma | 5 | 2 | |||
| Multiple myeloma | 5 | 2 | |||
| Chronic myeloproliferative disease | 2 | 2 | |||
| Solid organ tumors (n = 80) | 28 (35%) | Breast cancer | 20 | 7 | |
| Rectum cancer | 11 | 3 | |||
| Colon cancer | 10 | 5 | |||
| Stomach cancer | 6 | 5 | |||
| Ovary cancer | 5 | 0 | |||
| Lung cancer | 4 | 3 | |||
| Prostate cancer | 3 | 1 | |||
| Testis cancer | 3 | 0 | |||
| Other solid organ tumor | 3 | 0 | |||
| Bone cancer | 2 | 0 | |||
| Brain cancer | 2 | 0 | |||
| Gallbladder cancer | 2 | 1 | |||
| Endometrial cancer | 2 | 1 | |||
| Submandibular cancer | 1 | 0 | |||
| Pancreas cancer | 1 | 1 | |||
| Placental cancer | 1 | 0 | |||
| Larynx cancer | 1 | 0 | |||
| Small intestine cancer | 1 | 1 | |||
| Cervical cancer | 1 | 0 | |||
| Thyroid gland cancer | 1 | 0 | |||
As shown in Table 3, the seropositivity rates in the women and men were 55.5% and 44.4% in the patient group and 40% and 60% in the control group, respectively. Thus, there was no significant difference in the seropositivity for anti-T. gondii IgG antibodies according to sex (OR: 0.4892367, 95% CI: 0.2452735 - 0.9525424, P = 0.246). The occupation of each group was categorized as follows: non-employee, employee, student, and worker. The seroprevalence of T. gondii IgG was significantly higher (OR: 1.3, 95% CI: 0.6746163 - 2.4282788, P = 0.029) in the non-employees (46.1%; n = 30) than in the employees (27.7%; n = 18). In the patient and control groups, 42 (64.6%) and 23 (35.4%) participants resided in urban and rural areas, respectively. Among the patient group, the seropositivity rate in those living in urban areas was higher none significantly (OR: 0.7, 95% CI: 0.3538155 - 1.3990835, P = 0.553) than in those living in rural areas. Furthermore, contact with cats yielded no significant (OR: 1.9, 95% CI: 0.7756925 - 4.6564191, P = 0.1311) difference in the seropositivity rate between the patient and control groups (Table 3). Anti-T. gondii IgM was detected in one (1.13%) patient with stomach cancer, while no IgM antibodies were detected among the controls.
Table 3:
Association between the different variables and the overall anti-Toxoplasma gondii seropositivity
| Variables | Groups | IgG Seropositive controls, n = 20 (%) | Total n=65 (%) | OR (CI) | P. value | Patients n =113 vs Controls n = 82 | |
|---|---|---|---|---|---|---|---|
|
|
|
||||||
| IgG Seropositive patients, n = 45 (%) | P. value | ||||||
| Sex | Male (n = 89) | 20 (44.4) | 12 (60) | 32 (49.2) | 1.3 (0.245–0.952) | 0.246 | 0.447 |
| Female (n = 106) | 25 (55.6) | 8 (40) | 33 (50.7) | ||||
| Residency | Urban (n = 136) | 27 (60) | 15 (75) | 42 (64.6) | 0.7 (0.674–2.428) | 0.553 | 0.321 |
| Rural (n = 59) | 18 (40) | 5 (25) | 23 (35.4) | ||||
| Contact with cat | Yes | 35 (77.7) | 16 (80) | 51 (78.4) | 1.9 (0.775–4.656) | 0.097 | 0.1311 |
| No | 10 (22.3) | 4 (20) | 14 (21.5) | ||||
| Occupation | Non-employee | 23 (51.1) | 7 (35) | 30 (46.1) | 1.3 (0.674–2.428) | 0.029* | 0.0029* |
| Employee | 11 (24.4) | 7 (35) | 18 (27.7) | ||||
| Student | 0 (0.00) | 0 (0.00) | 0 (0.00) | ||||
| Worker | 11 (24.4) | 6 (30) | 17 (26.1) | ||||
Discussion
The immune system plays a critical role in controlling and clearing parasitic infections (33). Hence, those with weakened immune systems, such as immunocompromised individuals, including patients with cancer, may become infected with life-threatening opportunistic infections such as toxoplasmosis (34).
In the present study, the seroprevalence of anti T. gondii IgG antibodies in the patient group (39.8%) was significantly (P = 0.024) higher than that in the control group (24.4%), indicating that patients with cancer are at a higher risk for infection by T. gondii than healthy individuals (35). This is attributed to weak immune systems in patients with cancer, which may facilitate the reactivation of previous chronic toxoplasmosis or even increase the potential risk of acquiring new infections (36).
Close to our results, in two previous global (24, 34) systematic review and meta-analysis studies, the IgG seropositivity against T. gondii was 30.8% and 42.1%, respectively. Similarly, in another systematic review conducted in Iran (25), the authors reported the prevalence rate of toxoplasmosis in 45.06% of patients with cancer. In consistence with the present study; similar results were found in different geographical populations in the world. For example, in Jordan (21), Turkey (22) and China (37), the seropositivity rates of Toxoplasma in patients with cancer were
(61.2%), (63%) and (35.56%), respectively, which were significantly higher than that in the healthy individual controls. In contrast to our study, an investigation performed in Iran revealed that the seroprevalence of anti T. gondii antibodies in the controls was non-significantly higher than that in patients with cancer (38). These variations may be associated with the presence of different demographical, social, cultural, and environmental factors (39, 40).
In the current study, the prevalence of toxoplasmosis was found to be non-significantly higher in patients with haematological malignancies (51.5%) than in those with solid organ tumors (35%). This finding is supported by another study that also suggests that haematological malignancy cases have higher seropositivity rates than solid organ tumor cases (36). This may be attributed to the fact that the majority of patients with haematological malignancy have weakened cellular immunity. These patients are regarded as being at high risk for neutropenia because chemotherapeutic drugs kill both rapidly growing cancer cells and healthy white blood cells. Furthermore, the difference in the results may be related to the use of corticosteroids, which are commonly used in most chemotherapy treatments for patients with haematological malignancy (36). However, in contrast to those findings and suggestions, a study conducted in Egypt showed that the seropositivity rate was higher in patients with solid organ tumors than in those with haematological malignancies (41).
Some social and cultural factors affect the prevalence of toxoplasmosis in patients with cancer. For example, concerning sex, the positivity rate in women (50.7%) was non-significantly higher than that among men (49.2%) in both patients and control groups in our study. Similarly, another study (36) showed that women (56.6%) had significantly higher seropositivity rates than men (40.4%). This result may be related to the high indoor activity levels of women along with the consumption of raw or undercooked meat and unwashed vegetables and fruits or farming activities and also more frequent contact with cats or other animals (36). Having said all this, though, in other studies, a higher prevalence of toxoplasmosis has been reported in men than in women (42, 43).
An individual’s occupation was found to affect significantly the positivity of T. gondii IgG in both the patient and control groups. A significant (P = 0.029) higher positivity rate was observed in the non-employees (46.1%) than in the employees (27.7%) (P = 0.029). In contrast, another study conducted in Iran revealed a non-significant difference in the occupation between patients with cancer and controls (38).
Findings of the current study reported that the seropositive rate in the participants living in urban areas was non-significantly (P = 0.553) higher (64.6%) than that in the rural areas (35.4%). Similar results were obtained in other studies, Ali et al. (36) reported non-significant (0.889) higher seroprevalence (57.6%) for toxoplasmosis in individuals living in urban areas and (42.4%) in those living in rural areas. This may be due to changes in health services and cultural development that have improved rural lifestyles in recent years and brought them closer to urban dwellers (37).
Finally, contact with a cat had no significant (P = 0.097) role in parasitic transmission in either the patient (77.7%) or control (78.4%) group. This result coincides with a previous study performed in Iran, where no significant difference was observed between those who did and those who did not have contact with cats (44). These results may be attributed to the fact that many stray cats are present around the neighborhoods of participants (44). While, in a study conducted in China (45), exposure to cats had a significant effect (0.017) on the incidence of toxoplasma infection in cancer patients compared with the control group. This is because in China, keeping cats indoors is a common habit (46).
Conclusion
The results showed a high prevalence toxoplasmosis among patients with cancer. Therefore, it is recommended for patients with cancer to be screened periodically for toxoplasmosis. Cancer patients with IgG positive results are at risk of T gondii reactivation and patients with negative results are subjected to acute toxoplasmosis. Therefore, oncologists should be aware of this opportunistic parasite in patients with cancer. At the same time, raising awareness among patients with cancer on how to avoid exposure to risk factors can reduce infection with this opportunistic parasite. To better explore the prevalence of toxoplasmosis and its risk factors in patients with cancer and for an effective strategy for the control and prevention of toxoplasmosis, future studies with larger populations are highly recommended.
Acknowledgements
This study was supported by the administration and lab staff of Hiwa Cancer Hospital (HCH). All of them are acknowledged for providing excellent working facilities within the different departments of the hospital. We are grateful to all the participants, those who donated their valuable blood, with our best wishes for a fast recovery for the cancer patients.
Footnotes
Conflicts of Interest
The authors declare that there are no conflicts of interest regarding the publication of this article.
References
- 1.Robert-Gangneux F, Dardé ML. Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev. 2012; 25(2):264–296. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Liu XC, He Y, Han DG, et al. Detection of Toxoplasma gondii in chicken and soil of chicken farms in Nanjing region, China. Infect Dis Poverty. 2017; 6(62):1–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Fallahi S, Rostami A, Shiadeh MN, Behniafar H, Paktinat S. An updated literature review on maternal-fetal and reproductive disorders of Toxoplasma gondii infection. J Gynecol Obstet Hum Reprod. 2018; 47(3):133–140. [DOI] [PubMed] [Google Scholar]
- 4.Montoya J, Liesenfeld O. Toxoplasmosis. Lancet. 2004; 363(9425):1965–1976. [DOI] [PubMed] [Google Scholar]
- 5.Molan A, Nosaka K, Hunter M, Wang W. Global status of Toxoplasma gondii infection: systematic review and prevalence snapshots. Trop Biomed. 2019; 36(4):898–925. [PubMed] [Google Scholar]
- 6.Furtado JM, Smith J R, Belfort R, Jr, Gattey D, Winthrop KL. Toxoplasmosis: a global threat. J Glob Infect Dis. 2011; 3(3):281–284. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Pappas G, Roussos N, Falagas ME. Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int J Parasitol. 2009; 39(12):1385–1394. [DOI] [PubMed] [Google Scholar]
- 8.El Deeb HK, Salah-Eldin H, Khodeer S, Allah AA. Prevalence of Toxoplasma gondii infection in antenatal population in Menoufia governorate, Egypt. Acta Trop. 2012; 124(3):185–191. [DOI] [PubMed] [Google Scholar]
- 9.Yan C, Liang LJ, Zheng KY, Zhu XQ. Impact of environmental factors on the emergence, transmission and distribution of Toxoplasma gondii. Parasites Vectors. 2016; 9:37. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Jones JL, Dubey JP. Waterborne toxoplasmosis–recent developments. Exp Parasitol. 2010; 124(1):10–25. [DOI] [PubMed] [Google Scholar]
- 11.Grothen DC, Zach SJ, Davis PH. Detection of intestinal pathogens in river, shore, and drinking water in Lima, Peru. J Genomics. 2017; 5:4–11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Ahmed M, Sood A, Gupta J. Toxoplasmosis in pregnancy . Eur J Obstet Gynecol Reprod Biol. 2020; 255:44–50. [DOI] [PubMed] [Google Scholar]
- 13.Karimi G, Mardani A. Zadsar M. Toxoplasma and blood transfusion. Iran J Parasitol. 2014; 9(4):597–598. [PMC free article] [PubMed] [Google Scholar]
- 14.Alvarado-Esquivel C, Sánchez-Anguiano LF, Hernández-Tinoco J, et al. Association between Toxoplasma gondii infection and history of blood transfusion: a case-control seroprevalence study. J Int Med Res. 2018; 46(4):1626–1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Fernàndez-Sabé N, Cervera C, Fariñas MC, et al. Risk factors, clinical features, and outcomes of toxoplasmosis in solid-organ transplant recipients: a matched case-control study. Clin Infect Dis. 2012; 54(3):355–361. [DOI] [PubMed] [Google Scholar]
- 16.Agrawal SR, Singh V, Ingale S, Jain AP. Toxoplasmosis of the spinal cord in acquired immunodeficiency syndrome patient presenting as paraparesis: a rare entity. J Glob infect Dis. 2014; 6(4):178–181. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Conrad A, LeMaréchal M, Dupont D, et al. A matched case–control study of toxoplasmosis after allogeneic haematopoietic stem cell transplantation: still a devastating complication. Clin Microbiol Infect. 2016; 22(7):636–641. [DOI] [PubMed] [Google Scholar]
- 18.Zadeh AE, Bamedi T, Etemadi S, Shahrakipour M, Saryazdipour K. Toxoplasmosis as a complication of transfusion in hemodialysis patients. Iran J Ped Hematol Oncol . 2014; 4(1):22–25. [PMC free article] [PubMed] [Google Scholar]
- 19.Bajnok J, Tarabulsi M, Carlin H, et al. High frequency of infection of lung cancer patients with the parasite Toxoplasma gondii. ERJ Open Res. 2019; 5(2):00143–2018. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Weiss LM, Dubey JP. Toxoplasmosis: a history of clinical observations. Int J Parasitol. 2009; 39(8):895–901. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Khabaz MN, Elkhateeb L, Al-Alami J. Reactivation of latent Toxoplasma gondii in immunocompromised cancer patients. Comp Clin Path. 2011; 20(2):183–186. [Google Scholar]
- 22.Yazar S, Yaman O, Eser B, Altuntaş F, Kurnaz F, Şahin I. Investigation of anti-Toxoplasma gondii antibodies in patients with neoplasia. J Med Microbiol. 2004; 53(Pt 12):1183–1186. [DOI] [PubMed] [Google Scholar]
- 23.Dupont D, Hidalgo FH, Brenier-Pinchart MP, Garnaud C, Wallon M, Pelloux H. Serology for Toxoplasma in immunocompromised patients: still useful. Trends Parasitol. 2021; 37(3):205–213. [DOI] [PubMed] [Google Scholar]
- 24.Anvari D, Sharif M, Sarvi S, et al. Seroprevalence of Toxoplasma gondii infection in cancer patients: a systematic review and meta-analysis. Microb Pathog. 2019; 129:30–42. [DOI] [PubMed] [Google Scholar]
- 25.Ahmadpour E, Daryani A, Sharif M, et al. Toxoplasmosis in immunocompromised patients in Iran: a systematic review and meta-analysis. J Infect Dev Ctries. 2014; 8(12):1503–1510. [DOI] [PubMed] [Google Scholar]
- 26.Alim M, Ozcelik S, Ozpinar N. Seroprevalence of Toxoplasma gondii in patients receiving cancer treatment. Çumhur Medical J. 2018; 40(1):19–24. [Google Scholar]
- 27.Imam A, Al-Anzi FG, Al-Ghasham MA, Al-Suraikh MA, Al-Yahya AO, Rasheed Z. Serologic evidence of Toxoplasma gondii infection among cancer patients. A prospective study from Qassim region, Saudi Arabia. Saudi Med J. 2017; 38(3):319–321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Hijjawi NS, Al-Khreisat MJ, Abuyaman OM, et al. Seroprevalence of Toxoplasma gondii in Cancer Patients admitted to hospital; of the royal medical services in Jordan. Jordan J Biol Sci. 2018; 11(5):537–540. [Google Scholar]
- 29.Mawlood HH. Seroprevalence of Toxoplasma gondii Immunoglobulin G and Immunoglobulin M Antibodies among Leukemia Patients in Erbil City-Kurdistan Region/Iraq by Enzyme-linked Immunosorbent Assay Technique. Polytechnic J. 2021; 11(2):1–6. [Google Scholar]
- 30.Hussein N, Balatay AA. The Seroprevalence of Toxoplasma, Cytomegalovirus and Rubella Infections in Women with Abortion in Kurdistan Region of Iraq: A Brief Report. Int J Infect. 2019; 6(1):1–3. [Google Scholar]
- 31.Mikaeel FB, AL-Saeed ATM. Seroprevalence and molecular detection of Toxoplasma gondii among women in Duhok province /Iraq. J Duhok Univ. 2019; 22(2):85–92. [Google Scholar]
- 32.Mero WMS, Mizuri SSM. Seroprevalence of anti-Toxoplasma gondii antibodies among women of childbearing age in Zakho City, Kurdistan Region/Iraq. ZJPAS. 2020; 32(3):75–84. [Google Scholar]
- 33.Garung P, Kanneganti TD. Immune responses against protozoan parasites: A focus on the emerging role of Nod-like receptors. Cell Mol Life Sci. 2016; 73(16):3035–3051. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Wang ZD, Liu HH, Ma ZX, et al. Toxoplasma gondii infection in immunocompromised patients: a systematic review and meta-analysis. Front Microbiol. 2017; 8:389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Yu Y, Dong Guo, Qu T, Zhao Sh, Xu Ch, Wang L, et al. Increased Risk of Toxoplasma gondii Infection in Patients with Colorectal Cancer in Eastern China: Seroprevalence, Risk Factors, and a Case–Control Study. Biomed Res Int. 2020; 2020:2539482. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36.Ali MI, Abd El Wahab WM, Hamdy DA, Hassan A. Toxoplasma gondii in cancer patients receiving chemotherapy: seroprevalence and interferon gamma level. J Parasit Dis. 2019; 43(3):464–471. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Cong W, Liu GH, Meng QF, et al. Toxoplasma gondii infection in cancer patients: prevalence, risk factors, genotypes and association with clinical diagnosis. Cancer lett. 2015; 359(2):307–313. [DOI] [PubMed] [Google Scholar]
- 38.Arefkhah N, Hosseini SA, Karimzade R, et al. Seroprevalence and risk factors of Toxoplasma gondii infection among Cancer and Hemodialysis Patients in southwest Iran. Clin Epidemiol Glob Health. 2019; 7(4):596–599. [Google Scholar]
- 39.Hashmi SM, Mahmoodi S, Mahravaran A, et al. Serological and molecular evaluation of Serological and molecular evaluation of toxoplasmosis in patient undergoing chemotherapy for malignancies in southeast of Iran. Gene Rep. 2021; 23(101163):1–4. [Google Scholar]
- 40.Hasanzadah MM, Sarmadian H, Ghasemikhah R, et al. Evaluation of Toxoplasma gondii infection in western Iran: Seroepidemiology and risk factors analysis. Trop Med Health. 2020; 48:35. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41.Wassef RM, Abdel Malek RR, Rizk EM, Boghdady AM. Toxoplasmosis: an overlooked infection in cancer patients. Ann. Oncol. 2016; 27(Suppl-6): vi479. [Google Scholar]
- 42.Mostafa N, Hamed EF, Rashed H, Mohamed S, Abdelgawad M, Elasbali AM. The relationship between toxoplasmosis and different types of human tumors. J Infect Dev Ctries. 2018; 12(02):137–141. [DOI] [PubMed] [Google Scholar]
- 43.Jones JL, Kruszon-Moran D, Rivera HN, Price C, Wilkins PP. Toxoplasma gondii seroprevalence in the United States 2009–2010 and comparison with the past two decades. Am J Trop Med Hyg. 2014; 90(6):1135–1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 44.Al-Daoody AA, Suad TS, Hashim HR, Babasheikh OD, Akram HY, Ali SK. Detection of Toxoplasma gondii among Healthy Populations by Different Techniques in Erbil Province. ZJPAS. 2019; 31(6):75–83. [Google Scholar]
- 45.Duan Y, Zhi Y, Liu Y, et al. Toxoplasma gondii infection in children with lymphoma in Eastern China: seroprevalence, risk factors and case–control studies. Epidemiol Infect. 2019; 147:e305. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46.Zhou N, Zhang XY, Li YX, Wang L, Wang LL, Cong W. Seroprevalence and risk factors of Toxoplasma gondii infection in oral cancer patients in China: a case–control prospective study. Epidemiol Infect. 2018; 146(15):1891–5. [DOI] [PMC free article] [PubMed] [Google Scholar]