|
 |
SYMPOSIUM |
|
Year : 2016 | Volume
: 6
| Issue : 2 | Page : 129-135 |
|
|
Toxoplasmosis in HIV infection: An overview
Anuradha Basavaraju
Department of Microbiology, Mamata Medical College, Khammam, Telangana, India
Date of Acceptance | 30-Aug-2016 |
Date of Web Publication | 19-Sep-2016 |
Correspondence Address: Dr. Anuradha Basavaraju Department of Microbiology, Mamata Medical College, Khammam - 507 002, Telangana India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/2229-5070.190817
Abstract | | |
Toxoplasma gondii is an obligate intracellular protozoan parasite presenting as a zoonotic infection distributed worldwide. In HIV-positive individuals, it causes severe opportunistic infections, which is of major public health concern as it results in physical and psychological disabilities. In healthy immunocompetent individuals, it causes asymptomatic chronic persistent infections, but in immunosuppressed patients, there is reactivation of the parasite if the CD4 counts fall below 200 cells/μl. The seroprevalence rates are variable in different geographic areas. The tissue cyst or oocyst is the infective form which enters by ingestion of contaminated meat and transform into tachyzoites and disseminate into blood stream. In immunocompetent persons due to cell-mediated immunity the parasite is transformed into tissue cyst resulting in life long chronic infection. In HIV-infected people opportunistic infection by T. gondii occurs due to depletion of CD4 cells, decreased production of cytokines and interferon gamma and impaired cytotoxic T-lymphocyte activity resulting in reactivation of latent infection. The diagnosis can be done by clinical, serological, radiological, histological or molecular methods, or by the combination of these. There is various treatment regimen including acute treatment, maintenance therapy should be given as the current anti T. gondii therapy cannot eradicate tissue cysts. In HIV patients, CD4 counts <100; cotrimoxazole, alternately dapsone + pyrimethamine can be given for 6 months. Hence, early diagnosis of T. gondii antibodies is important in all HIV-positive individuals to prevent complications of cerebral toxoplasmosis. Keywords: CD4 counts, HIV infection, toxoplasmosis
How to cite this article: Basavaraju A. Toxoplasmosis in HIV infection: An overview. Trop Parasitol 2016;6:129-35 |
Introduction | |  |
Toxoplasma gondii is a protozoan parasite present world-wide and causes major opportunistic infections in HIV infected people. Cell-mediated immunity (CMI) will be developed after acute infection with T. gondii and infection is controlled but not eradicated. In this chronic or latent phase of infection, the organisms persist in the tissues of infected individuals such as brain, skeletal muscle, and heart. In HIV infection, symptomatic disease most often occurs as a result of reactivation of latent infection. [1] Toxoplasmosis has been reported as the most common opportunistic infection in HIV/AIDS in developed countries and most common cause of focal brain lesions, coma and death. It commonly causes encephalitis in HIV-infected patients. [2],[3]
Infection occurs by ingestion of contaminated water, food from oocysts excreted by cats, or infected meat which is improperly cooked. [4],[5],[6] Toxoplasma pneumonia occurs by respiratory route, transplacental route responsible for abortion and neonatal pathology, nosocomial through blood-transfusion, organ transplants, and laboratory accidents. [7],[8],[9]
Morphology | |  |
T. gondii has three morphological forms - oocyst, tachyzoites, and tissue cysts containing bradyzoites. Cats act as the definitive hosts and bring oocysts which are infective forms. Following ingestion by humans, the sporozoites present in the oocyst develop into tachyzoites, and enter into the nucleated cells of the host. These tachyzoites are invasive forms, multiply rapidly, lead to cell rupture and invade nearby cells and transported to other parts of the body via blood and lymphatic circulation. As a result of inflammatory response, tachyzoites are transformed into tissue cysts, which are dormant form containing numerous bradyzoites. The sites of cyst formation are brain, skeletal muscle, and cardiac muscle. In immuno-compromised persons, bradyzoites can be released from the cysts and transformed into tachyzoites.
In HIV/AIDS patients, toxoplasma encephalitis is one of the most common opportunistic infections. Central nervous system (CNS) disease occurs when CD4 cell count is <200 cells/microliter. The greatest risk is in patients with CD4 count <50 cells/microliter. [10],[11],[12] Patients with cerebral toxoplasmosis presented with higher titres of anti-T. gondii IgG antibodies than patients with other diseases. [13]
Pathogenesis | |  |
Following ingestion of contaminated food, tachyzoites disseminate throughout the body, infect all nucleated cells, leading to production of necrotic focus surrounded by inflammation. As a result of CMI, tachyzoites are transformed into tissue cysts resulting in life-long infection. Cellular immunity mediated by T-cells, macrophages, and activity of Type-1 cytokines (interleukin-12 [IL-12] and interferon [INF] gamma) is necessary for maintaining the quiescence of chronic T. gondii infection. [14] The production of IL-12 and INF gamma is stimulated by CD154 (also known as CD40 ligand) in human models of T. gondii infection. CD154 acts by triggering dendritic cells and macrophages to secrete IL-12, which in turn enhances the production of INF gamma by T-cells. [15]
In HIV infection due to immunosuppression, opportunistic infection occurs with T. gondii due to depletion of CD4 T-cells, impaired production of IL-12 and INF gamma and impaired cytotoxic T-lymphocyte activity. [16] There is decreased in vitro production of IL-12, INF gamma, and decreased expression of CD154 in response to T. gondii. [17],[18],[19]
Clinical Manifestations | |  |
Toxoplasmosis in HIV-infected patients manifests mainly as encephalitis, chorioretinitis, and pneumonitis or disseminated infection depending upon the immune status of the host. It is sub-acute in onset with focal neurological signs associated with fever, altered sensorium, and headache. Cerebellar, sub-cortical, or cortical lesions can be present in over 50% of infected cases resulting in hemiparesis, ambulatory gait, and speech abnormalities. [20] Some people with encephalitis can also present with neuropsychiatric disorders including psychosis, dementia, anxiety, and personality disorders. [21]
In HIV-infected patients, toxoplasmosis may present extracerebrally with or without encephalitis. The most common presentations can be ocular and pulmonary disease. [22] Patients with chorioretinitis presents with blurred vision, scotoma, pain, or photophobia. Pulmonary manifestations are similar to pneumocystis jeroveci pneumonia. In HIV-infected patients, a disseminated toxoplasmosis may occur with fever, sepsis-like syndrome with hypotension, disseminated intravascular coagulation, elevated lactate dehydrogenase, and pulmonary dehydrogenase. [22],[23],[24]
Epidemiology | |  |
The prevalence of toxoplasma infection varies depending on the geographical area and population groups and also with the age. In Europe and other tropical countries, the prevalence is over 50%. [25] In Hong Kong, it was 9.8%. [21] In US, about 1/3 rd of HIV-infected patients have antibodies against T. gondii and seroprevalence data of HIV-infected patients come from small, predominantly male cohorts in which the range of prevalence is 3-22%. [26],[27]
The prevalence in Nigeria is 75.4%, [28] 58.4% in Tunisia, [29] 28.5% in HIV-infected women in Benin, [30] 40.2% in Senegal. [31] Spalding et al. [32] reported 74.5% in South Brazil, Jeannel et al. [33] reported 63.7% in Paris, Kodym et al. [34] reported 30% in Chezech republic, Xiao et al. [35] reported 12.5% of Toxoplasma seropositivity in HIV-positive patients in China.
In India, one study by Anuradha and Preethi, observed seroprevalence of 34.78% among HIV-positive patients. [36] In one study by Sucilathangam et al. observed 15% of Toxoplasma seropositivity in HIV-positive people. [37] In one study by Meisheri et al., [38] seropositivity was 67.8% in HIV-infected people when compared to immunocompetent adults (30.9%). [38] The variation in prevalence rates could be due to differences within the geographical areas, infection is more common in tropical conditions and at lower altitudes than in cold and mountainous region. [39] Another reason could be due to the recruited subjects, using different assay and the year of study. [40],[41],[42]
The two largest toxoplasma seroprevalence studies of HIV-infected US women included 169 and 139 women and reported seroprevalence is 22% and 20%, respectively. [43],[44] In one study by Falusi et al. observed 15.3% seropositivity in HIV-infected women and 14.3% positivity in uninfected women. [45] In one study, conducted by Anuradha and Preethi showed the seropositivity in HIV patients was 34.78% with 28.95% in males and 38.89% in females and the most common age group affected was 31-40 years. [36] In one study by Meisheri et al. showed that highest prevalence at third and fourth decade of life. [38] The increase in prevalence rate with increase in age may be due to the increase risk of exposure with infection with increase in age.
Association with CD4 Counts | |  |
There is an association between CD4 count and prevalence of toxoplasmosis. In a study conducted by Anuradha and Preethi [36] in patients with CD4 count 51-100 cells/mm 3 without any neurological symptoms, toxoplasma IgG antibodies are present in 75% of cases. In one study by Osunkalu et al. reported that 79.4% of HIV-positive patients without neurological symptoms has CD4 count <100 cells/mm 3 . [46] In one study by Eliaszewicz M et al., in France, showed that 79% of patients with neurological symptoms had CD4 counts <150 cells/mm 3 . [47] In one study by Sucilathangam et al., CD4 counts were <100 cells/mcl in toxoplasma seropositive patients. [37] These findings are also correlating with other studies. [48],[49]
Differential Diagnosis of Toxoplasmosis in HIV Patients | |  |
Differential diagnosis of toxoplasma encephalitis may be lymphoma of CNS, progressive multifocal encephalopathy, tuberculosis including tuberculoma, focal CNS lesions caused by fungi such as Cryptococcus neoformans, Aspergillus spp., Nocardia spp., cytomegalovirus and herpes simplex encephalitis, and bacterial brain abscess.
Diagnosis | |  |
Cerebral toxoplasmosis is common in HIV/AIDS positive patients and causes more serious manifestations. Hence, definitive diagnosis for cerebral toxoplasmosis is important. Presumptive diagnosis can be made by clinical presentation, radiological findings, molecular studies, serological tests, and also response to therapy. The clinical diagnosis can be made in HIV positive patients with CD4 count <100 cells/μL presenting with compatible focal neurological lesions. In case of cerebral toxoplasmosis, there is an improvement of clinical and radiological features after 2-3 weeks of empirical therapy and outcome will be good.
Serological Diagnosis | |  |
Anti T. gondii IgG antibodies start increasing after 1-2 weeks of infection and reaches peak in 6-8 weeks. They decline gradually over next 1-2 years but they can persist for life time in some cases. [50] Demonstration of high titers of anti-T. gondii IgG antibodies with high IgG avidity gives serological evidence of infection and also indicates the secondary reactivation of latent or chronic toxoplasma infection. [51] Hence, it is important to detect toxoplasma seropositivity status in all HIV-infected patients to estimate the risk for cerebral toxoplasmosis.
Radiological Diagnosis | |  |
Computed tomography (CT) or MRI gives presumptive diagnosis of cerebral toxoplasmosis. The findings are observed as hypodense lesions with ring enchancing and peri-lesional edema, which are seen in majority of patients. In 20% of patients, the findings will be hypodense lesions without contrast enhancing and without focal lesions. An unusual and highly suggestive imaging of cerebral toxoplasmosis is the eccentric target sign in which small asymmetric nodule along the wall of enhancing ring is seen. A computerized axial tomography scan is sensitive diagnostic method for focal neurological deficits but it may not diagnose the minimal inflammatory response seen in early stages. Magnetic resonance imaging is more sensitive than computed tomography scan in diagnosing toxoplasmosis from brain lesions. However, newer imaging techniques such as signal photon emission CT or positron emission tomography can enhance the specificity to rule out other CNS lesions such as lymphoma.
Brain Biopsy | |  |
For the demonstration of tachyzoites and tissue cysts, it gives definitive diagnosis but it is not considered because the empirical therapy of suspected toxoplasmosis can usually confirm the diagnosis.
Molecular Diagnosis | |  |
Direct detection of T. gondii DNA in biological samples by polymerase chain reaction has provided a breakthrough for the diagnosis of toxoplasmosis. [52] For cerebrospinal fluid and blood samples, it gives poor results and variable sensitivity. [53]
Prevention of Toxoplasmosis in HIV/Aids | |  |
All HIV-infected individuals should be tested for baseline IgG antibodies to toxoplasma to detect latent infection. All HIV-infected individuals should be counseled regarding the exposure to toxoplasma infections. [54] Eating of raw or undercooked meat must be avoided. Proper hand washing should be done after contact with raw meat, gardening or contact with soil. Fruits and vegetables should be washed well before eating them raw. Handling cat's litter is to be avoided. Pet animals such as cats should be fed with canned or dried commercial food or well cooked food but not raw, undercooked meat.
Diagnostic management, treatment and prophylaxis of toxoplasmosis are shown in [Figure 1] and [Table 1], [Table 2], [Table 3]. [52],[55]
Newer Approaches | |  |
Further studies can be done for the prevention not only by giving chemoprophylaxis but also by immunization. In one study by Meng et al. [56] worked on animal models and compared the protective efficacy of different immunization strategies in BALB/c mice. They suggested that vaccination regimens can trigger significantly high levels of CMI and humoral immune response than the control groups injected with phosphate buffer saline or pEGFP (eukaryotic expression vector). DNA vaccines followed by peptide boosting significantly increased the levels of IgG, IgG2a, and INF-gamma. Cytokines play an important role in the host resistance against T. gondii and gives protection in the early infection and controls the replication of the protozoa. [57] They also estimated the levels of cytokine production IN4, INF-gamma from spleen cells of the mice. INF-gamma is important in restricting the growth of T. gondii in acute infections and preventing the reactivation of parasites from dormant cysts. [58] In their study high levels of TNF-gamma production was induced in experimental animals and compared to controls.
A study by Maggi et al. suggested that INF-gamma correlates with the differentiation of TH1 cells and INF4 cells. [59] Hence, INF-gamma is also an important marker for the protective immunity against T. gondii.
Further studies can be done and systemic evaluation of immune response can be generated by different experimental parameters.
Conclusions | |  |
T. gondii , coccidian protozoan intracellular parasite, is one of the most causative agents of opportunistic infections in HIV/AIDS patients. Their epidemiological and clinical aspect in association with HIV-infected patients was reported worldwide. In HIV infection due to immunosuppression, there is reactivation of chronic latent infection resulting in Toxoplasma encephalitis. The prevalence rates of toxoplasma infection in HIV-positive patients are variable across different geographical areas. The prevalence rates are increasing with age. The risk of infection is more when the CD4 counts are <100 cells/μL. Diagnosis can be made by clinical, serological, radiological, histological, and molecular methods. Due to the high rate of reactivation in HIV-positive patients and complications of cerebral toxoplasmosis, all HIV-positive patients must be tested for the presence of T. gondii antibodies. Those who tested positive for anti T. gondii antibodies should be considered for chemoprophylaxis. Proper treatment and prophylaxis with maintenance therapy will control the infection. However, proper preventive measures and counseling regarding the exposure to toxoplasma infection can also help in prophylaxis. Further research can be done on the immunization methods, which will enhance the CMI.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References | |  |
1. | Porter SB, Sande MA. Toxoplasmosis of the central nervous system in the acquired immunodeficiency syndrome. N Engl J Med 1992;327:1643-8.  [ PUBMED] |
2. | Winstanley P. Drug treatment of toxoplasmic encephalitis in acquired immunodeficiency syndrome. Postgrad Med J 1995;71:404-8.  [ PUBMED] |
3. | McCabe R, Chirurgi V. Issues in toxoplasmosis. Infect Dis Clin North Am 1993;7:587-604.  [ PUBMED] |
4. | Baril L, Ancelle T, Goulet V, Thulliez P, Tirard-Fleury V, Carme B. Risk factors for Toxoplasma infection in pregnancy: A case-control study in France. Scand J Infect Dis 1999;31:305-9.  [ PUBMED] |
5. | Kapperud G, Jenum PA, Stray-Pedersen B, Melby KK, Eskild A, Eng J. Risk factors for Toxoplasma gondii infection in pregnancy. Results of a prospective case-control study in Norway. Am J Epidemiol 1996;144:405-12.  [ PUBMED] |
6. | Cook AJ, Gilbert RE, Buffolano W, Zufferey J, Petersen E, Jenum PA, et al. Sources of toxoplasma infection in pregnant women: European multicentre case-control study. European Research Network on Congenital Toxoplasmosis. BMJ 2000;321:142-7.  [ PUBMED] |
7. | Kimball AC, Kean BH, Kellner A. The risk of transmitting toxoplasmosis by blood transfusion. Transfusion 1965;5:447-51.  [ PUBMED] |
8. | Segall L, Moal MC, Doucet L, Kergoat N, Bourbigot B. Toxoplasmosis-associated hemophagocytic syndrome in renal transplantation. Transpl Int 2006;19:78-80.  [ PUBMED] |
9. | Rawal BD. Laboratory infection with toxoplasma. J Clin Pathol 1959;12:59-61.  [ PUBMED] |
10. | Kaplan JE, Benson C, Holmes KK, Brooks JT, Pau A, Masur H; Centers for Disease Control and Prevention (CDC); National Institutes of Health; HIV Medicine Association of the Infectious Diseases Society of America. Guidelines for prevention and treatment of opportunistic infections in HIV-infected adults and adolescents: Recommendations from CDC, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. MMWR Recomm Rep 2009;58:1-207. |
11. | Leport C, Chêne G, Morlat P, Luft BJ, Rousseau F, Pueyo S, et al. Pyrimethamine for primary prophylaxis of toxoplasmic encephalitis in patients with human immunodeficiency virus infection: A double-blind, randomized trial. ANRS 005-ACTG 154 Group Members. Agence Nationale de Recherche sur le SIDA. AIDS Clinical Trial Group. J Infect Dis 1996;173:91-7. |
12. | Luft BJ, Brooks RG, Conley FK, McCabe RE, Remington JS. Toxoplasmic encephalitis in patients with acquired immune deficiency syndrome. JAMA 1984;252:913-7.  [ PUBMED] |
13. | Colombo FA, Vidal JE, de Oliveira AC, Hernandez AV, Bonassar-Filho F. Nogueira RS. Diagnosis of cerebral toxoplasmosis in AIDS patients in Brazil: Importance of molecular and immunological methods using peripheral blood samples J Clin Microbiol 2005;43:5044-7. |
14. | Subauste CS, Remington JS. Immunity to Toxoplasma gondii. Curr Opin Immunol 1993;5:532-7.  [ PUBMED] |
15. | Subauste CS. CD154 and type-1 cytokine response: From hyper IgM syndrome to human immunodeficiency virus infection 2002;185 Suppl 1:S83-9. |
16. | Cohen O, Weissmal D, Fauci KS. The immune pathogenesis of HIV infection. In: Paul WE, editor. Fundamental Immunology. Philadelphia: Lippincott-Raven; 1999. p. 1455-509. |
17. | Murray HW, Rubin BY, Masur H, Roberts RB. Impaired production of lymphokines and immune (gamma) interferon in the acquired immunodeficiency syndrome. N Engl J Med 1984;310:883-9.  [ PUBMED] |
18. | Subauste CS, Wessendarp M, Smulian AG, Frame PT. Role of CD40 ligand signaling in defective type 1 cytokine response in human immunodeficiency virus infection. J Infect Dis 2001;183:1722-31. |
19. | Subauste CS, Wessendarp M, Portilllo JA, Andrade RM, Hinds LM, Gomez FJ, et al. Pathogen-specific induction of CD154 is impaired in CD4+T cells from human immunodeficiency virus-infected patients. J Infect Dis 2004;189:61-70.  [ PUBMED] |
20. | Luft BJ, Remington JS. Toxoplasmic encephalitis in AIDS. Clin Infect Dis 1992;15:211-22.  [ PUBMED] |
21. | Ko RC, Wong FW, Todd D, Lam KC. Prevalence of Toxoplasma gondii antibodies in the Chinese population of Hong Kong. Trans R Soc Trop Med Hyg 1980;74:351-4.  [ PUBMED] |
22. | Rabaud C, May T, Amiel C, Katlama C, Leport C, Ambroise-Thomas P, et al. Extracerebral toxoplasmosis in patients infected with HIV. A French National Survey. Medicine (Baltimore) 1994;73:306-14. |
23. | Oksenhendler E, Duarte M, Soulier J, Cacoub P, Welker Y, Cadranel J, et al. Multicentric Castleman′s disease in HIV infection: A clinical and pathological study of 20 patients. AIDS 1996;10:61-7.  [ PUBMED] |
24. | Huang L, Schnapp LM, Gruden JF, Hopewell PC, Stansell JD. Presentation of AIDS-related pulmonary Kaposi′s sarcoma diagnosed by bronchoscopy. Am J Respir Crit Care Med 1996;153 (4 Pt 1):1385-90. |
25. | Tenter AM, Heckeroth AR, Weiss LM. Toxoplasma gondii: From animals to humans. Int J Parasitol 2000;30:1217-58.  [ PUBMED] |
26. | Grant IH, Gold JW, Rosenblum M, Niedzwiecki D, Armstrong D. Toxoplasma gondii serology in HIV-infected patients: The development of central nervous system toxoplasmosis in AIDS. AIDS 1990;4:519-21.  [ PUBMED] |
27. | Wong B, Gold JW, Brown AE, Lange M, Fried R, Grieco M, et al. Central-nervous-system toxoplasmosis in homosexual men and parenteral drug abusers. Ann Intern Med 1984;100:36-42.  [ PUBMED] |
28. | Onadeko MO, Joynson DH, Payne RA, Francis J. The prevalence of toxoplasma antibodies in pregnant Nigerian women and the occurrence of stillbirth and congenital malformation. Afr J Med Med Sci 1996;25:331-4.  [ PUBMED] |
29. | Bouratbine A, Saia E, Chahed MK, Auon K, Ben Ismail R. Seroepidemiological profile of toxoplasmosis in Northern Tunisia. Parasite Immunol 2001;8:61-6. |
30. | Rodier MH, Berthonneau J, Bourgoin A, Giraudeau G, Agius G, Burucoa C, et al. Seroprevalences of Toxoplasma, malaria, rubella, cytomegalovirus, HIV and treponemal infections among pregnant women in Cotonou, Republic of Benin. Acta Trop 1995;59:271-7. |
31. | Assob JC, Njunda AL, Nsagha DS, Kamga HL, Weledji PE, Che VB. Toxoplasma antibodies amongst HIV/AIDS patients attending the university teaching hospital Yaounde, in Cameroon. AFR. J Clin Exp Microbiol 2011;12:1119-23. |
32. | Spalding SM, Amendoeira MR, Klein CH, Ribeiro LC. Serological screening and toxoplasmosis exposure factors among pregnant women in South of Brazil. Rev Soc Bras Med Trop 2005;38:173-7.  [ PUBMED] |
33. | Jeannel D, Niel G, Costagliola D, Danis M, Traore BM, Gentilini M. Epidemiology of toxoplasmosis among pregnant women in the Paris area. Int J Epidemiol 1988;17:595-602. |
34. | Kodym P, Hrdá S, Machala L, Rozsypal H, Stanková M, Malý M. Prevalence and incidence of toxoplasma infection in HIV-positive patients in the Czech Republic. J Eukaryot Microbiol 2006;53 Suppl 1:S160-1. |
35. | Xiao Y, Yin J, Jiang N, Xiang M, Hao L, Lu H, et al. Seroepidemiology of human Toxoplasma gondii infection in China. BMC Infect Dis 2010;10:4.  [ PUBMED] |
36. | Anuradha B, Preethi C. Seroprevalence of toxoplasma IgG antibodies in HIV positive patients in and around Khammam, Telangana State. J Clin Diagn Res 2014;8:DL01-2. |
37. | Sucilathangam G, Palaniappan N, Sreekumar C, Anna T. Serological survey of toxoplasmosis in a district in Tamil Nadu: Hospital-based study. Indian J Med Res 2013;137:560-3.  [ PUBMED] |
38. | Meisheri YV, Mehta S, Patel U. A prospective study of seroprevalence of toxoplasmosis in general population, and in HIV/AIDS patients in Bombay, India. J Postgrad Med 1997;43:93-7.  [ PUBMED] |
39. | Nissapatorn V, Lee CK, Cho SM, Rohela M, Anuar AK, Quek KF, et al. Toxoplasmosis in HIV/AIDS patients in Malaysia. Southeast Asian J Trop Med Public Health 2003;34 Suppl 2:80-5.  [ PUBMED] |
40. | Kelesidis T, Tozzi S, Mitty R, Worthington M, Fleisher J. Cytomegalovirus pseudotumor of the duodenum in a patient with AIDS: An unrecognized and potentially treatable clinical entity. Int J Infect Dis 2010;14:e274-82. |
41. | Mostafavi SN, Ataei B, Nokhodian Z, Yaran M, Babak A. Seroepidemiology of Toxoplasma gondii infection in Isfahan province, central Iran: A population based study. J Res Med Sci 2011;16:496-501.  [ PUBMED] |
42. | Shimelis T, Tebeje M, Tadesse E, Tegbaru B, Terefe A. Sero-prevalence of latent Toxoplasma gondii infection among HIV-infected and HIV-uninfected people in Addis Ababa, Ethiopia: A comparative cross-sectional study. BMC Res Notes 2009;2:213.  [ PUBMED] |
43. | Ruiz R, Cu-Uvin S, Fiore T, Flanigan TP. Toxoplasmosis in HIV-positive women: Seroprevalence and the role of prophylaxis in preventing disease. AIDS 1997;11:119-20.  [ PUBMED] |
44. | Minkoff H, Remington JS, Holman S, Ramirez R, Goodwin S, Landesman S. Vertical transmission of toxoplasma by human immunodeficiency virus-infected women. Am J Obstet Gynecol 1997;176:555-9.  [ PUBMED] |
45. | Falusi O, French AL, Seaberg EC, Tien PC, Watts DH, Minkoff H, et al. Prevalence and predictors of toxoplasma seropositivity in women with and at risk for human immunodeficiency virus infection. Clin Infect Dis 2002;35:1414-7.  [ PUBMED] |
46. | Osunkalu VO, Akanmu SA, Ofomah NJ, Onyiaorah IV, Adediran AA, Akinde RO, et al. Seroprevalence of Toxoplasma gondii IgG antibody in HIV-infected patients at the Lagos University Teaching Hospital. HIV AIDS (Auckl) 2011;3:101-5.  [ PUBMED] |
47. | Eliaszewicz M, Lecomte I, Da SA. Relation between decreasing series CD4 lymphocyte count and outcome of toxoplasmosis in AIDS patients: A basis for primary prophylaxis. Int Conf AIDS 1990;6:20-3. |
48. | Kasper DL, Braunwald E, Fauci AS, Hauser SL, Longo DL, Jameson JL. Toxoplasmosis Infection. Harrisons Principles of Internal Medicine. 16 th ed., Vol.2, New York: Mc Graw Hill Inc;2005:1243-8. |
49. | Kumarasamy N, Solomon S, Flanigan TP, Hemalatha R, Thyagarajan SP, Mayer KH. Natural history of human immunodeficiency virus disease in Southern India. Clin Infect Dis 2003;36:79-85.  [ PUBMED] |
50. | Montoya JG, Kovacs JA, Remington JS. Toxoplasma gondii. In: Mandell GL, Bennett JE, Dolin R 6 th , editors. Principles and Practice of Infectious Diseases. Philadelphia: Churchill Livingstone; 2005. p. 3170-98. |
51. | Colombo FA, Vidal JE, Penalva de Oliveira AC, Hernandez AV, Bonasser-Filho F, Nogueira RS, et al. Diagnosis of cerebral toxoplasmosis in AIDS patients in Brazil: Importance of molecular and immunological methods using peripheral blood samples. J Clin Microbiol 2005;43:5044-7.  [ PUBMED] |
52. | Reischl U, Bretagne S, Krüger D, Ernault P, Costa JM. Comparison of two DNA targets for the diagnosis of toxoplasmosis by real-time PCR using fluorescence resonance energy transfer hybridization probes. BMC Infect Dis 2003;3:7. |
53. | Parmley SF, Goebel FD, Remington JS. Detection of Toxoplasma gondii in cerebrospinal fluid from AIDS patients by polymerase chain reaction. J Clin Microbiol 1992;30:3000-2.  [ PUBMED] |
54. | 1999 USPHS/IDSA guidelines for the prevention of opportunistic infections in persons infected with human immunodeficiency virus. U.S. Public Health Service (USPHS) and Infectious Diseases Society of America (IDSA). MMWR Recomm Rep 1999;48:1-59, 61-6. |
55. | Chan K, Wong KH, Lee SS. HIV manual 2001. Department of Health, Red Ribbon Centre 2002;193-8. |
56. | Meng M, Zhou A, Lu G, Wang L, Zhao G, Han Y, et al. DNA prime and peptide boost immunization protocol encoding the Toxoplasma gondii GRA4 induces strong protective immunity in BALB/c mice. BMC Infect Dis 2013;13:494. |
57. | Sher A, Denkers EY, Gazzinelli RT. Induction and regulation of host cell-mediated immunity by Toxoplasma gondii. Ciba Found Symp 1995;195:95-104.  [ PUBMED] |
58. | Suzuki Y, Orellana MA, Schreiber RD, Remington JS. Interferon-gamma: The major mediator of resistance against Toxoplasma gondii. Science 1988;240:516-8.  [ PUBMED] |
59. | Maggi E, Parronchi P, Manetti R, Simonelli C, Piccinni MP, Rugiu FS, et al. Reciprocal regulatory effects of IFN-gamma and IL-4 on the in vitro development of human Th1 and Th2 clones. J Immunol 1992;148:2142-7.  [ PUBMED] |
[Figure 1]
[Table 1], [Table 2], [Table 3]
This article has been cited by | 1 |
Rare cardiac complication of toxoplasmosis in immunocompetent host |
|
| Erni Juwita Nelwan, Sharifah Shakinah, Gabriella Clarissa, Fransiscus Nikodemus Hosea, Dwi Yuda Herdanto, Jacub Pandelaki | | IDCases. 2022; 29: e01533 | | [Pubmed] | [DOI] | | 2 |
Toxoplasma metabolic flexibility in different growth conditions |
|
| Daniel Walsh, Nicholas J. Katris, Lilach Sheiner, Cyrille Y. Botté | | Trends in Parasitology. 2022; | | [Pubmed] | [DOI] | | 3 |
Formulation of Neem oil-loaded solid lipid nanoparticles and evaluation of its anti-Toxoplasma activity |
|
| Sara Nemati, Hanieh Mohammad Rahimi, Zahra Hesari, Meysam Sharifdini, Nooshin Jalilzadeh Aghdam, Hamed Mirjalali, Mohammad Reza Zali | | BMC Complementary Medicine and Therapies. 2022; 22(1) | | [Pubmed] | [DOI] | | 4 |
Analysis of Deaths among HIV-Infected Patients Hospitalized in 2009–2018 in Main Centre of Infectious Disease in Region of Lower Silesia in Poland, Detailing Lesions in the Central Nervous System |
|
| Justyna Janocha-Litwin, Aleksander Zinczuk, Sylwia Serafinska, Anna Szymanek-Pasternak, Krzysztof Simon | | Medicina. 2022; 58(2): 270 | | [Pubmed] | [DOI] | | 5 |
Cerebral Toxoplasmosis As the Initial Presentation of HIV: A Case Series |
|
| Akshita Khosla, Sachi Singhal, Pooja Jotwani, Robert Kleyman | | Cureus. 2022; | | [Pubmed] | [DOI] | | 6 |
The New Status of Parasitic Diseases in the COVID-19 Pandemic—Risk Factors or Protective Agents? |
|
| Kinga Gluchowska,Tomasz Dzieciatkowski,Aleksandra Sedzikowska,Anna Zawistowska-Deniziak,Daniel Mlocicki | | Journal of Clinical Medicine. 2021; 10(11): 2533 | | [Pubmed] | [DOI] | | 7 |
Central Nervous System Toxoplasmosis and Cytomegalovirus Colitis in an Asymptomatic HIV Positive Patient |
|
| Bernard O Emuze,Molly S Jain,Enkhmaa Luvsannyam,Paro Bhaya,Carlos Vaquero | | Cureus. 2021; | | [Pubmed] | [DOI] | | 8 |
Seroprevalence Estimates of Latent and Acute Toxoplasma Infections in HIV+ People—Call for Action in Underprivileged Communities |
|
| Ali Rostami,Seyed Mohammad Riahi,Shayan Abdollahzadeh Sagha,Ali Taghipour,Mahdi Sepidarkish,Mousa Mohammadnia-Afrouzi,Soheil Ebrahimpour,Peter J. Hotez,Ray Gamble,Robin B. Gasser | | Microorganisms. 2021; 9(10): 2034 | | [Pubmed] | [DOI] | | 9 |
Transcriptomic Analysis of the Effects of Chemokine Receptor CXCR3 Deficiency on Immune Responses in the Mouse Brain during Toxoplasma gondii Infection |
|
| Kousuke Umeda, Youta Goto, Kenichi Watanabe, Nanako Ushio, Ragab M. Fereig, Fumiaki Ihara, Sachi Tanaka, Yutaka Suzuki, Yoshifumi Nishikawa | | Microorganisms. 2021; 9(11): 2340 | | [Pubmed] | [DOI] | | 10 |
Toxoplasmosis: Current and Emerging Parasite Druggable Targets |
|
| Rana El Hajj, Lina Tawk, Shaymaa Itani, Maguy Hamie, Jana Ezzeddine, Marwan El Sabban, Hiba El Hajj | | Microorganisms. 2021; 9(12): 2531 | | [Pubmed] | [DOI] | | 11 |
Comprehensive Overview of Toxoplasma gondii-Induced and Associated Diseases |
|
| Darine Daher, Ahmad Shaghlil, Eyad Sobh, Maguy Hamie, Malika Elhage Hassan, Mohamad Bahij Moumneh, Shaymaa Itani, Rana El Hajj, Lina Tawk, Marwan El Sabban, Hiba El Hajj | | Pathogens. 2021; 10(11): 1351 | | [Pubmed] | [DOI] | | 12 |
Statistical models for analyzing count data: predictors of length of stay among HIV patients in Portugal using a multilevel model |
|
| Ahmed Nabil Shaaban,Bárbara Peleteiro,Maria Rosario O. Martins | | BMC Health Services Research. 2021; 21(1) | | [Pubmed] | [DOI] | | 13 |
Neurologic Complications of Human Immunodeficiency Virus |
|
| Marie F. Grill | | CONTINUUM: Lifelong Learning in Neurology. 2021; 27(4): 963 | | [Pubmed] | [DOI] | | 14 |
Investigating the risk factors for seroprevalence and the correlation between CD4+ T-cell count and humoral antibody responses to Toxoplasma gondii infection amongst HIV patients in the Bamenda Health District, Cameroon |
|
| Eugene Enah Fang, Raymond Babila Nyasa, Emmanuel Menang Ndi, Denis Zofou, Tebit Emmanuel Kwenti, Edith Pafoule Lepezeu, Vincent P. K. Titanji, Roland N. Ndip, Mohammed Abdelfatah Mosa Alhoot | | PLOS ONE. 2021; 16(12): e0256947 | | [Pubmed] | [DOI] | | 15 |
Anti-Toxoplasmic Immunoglobulin G Quantitation Correlates with Immunovirological Parameters of HIV-Infected Cameroonians |
|
| Aude Christelle Ka’e,Samuel Martin Sosso,Joseph Fokam,Rachel Kamgaing Simo,Sara Riwom Essama,Alex Durand Nka,Bouba Yagai,Cédric Joël Ninsu Dzukou,Michel Carlos Tommo Tchouaket,Collins Chenwi,Aissatou Abba,Nadine Fainguem,Marie Krystel Nnomo Zam,Junie Flore Yimga,Vittorio Colizzi,Alexis Ndjolo | | Current HIV Research. 2021; 19(1): 73 | | [Pubmed] | [DOI] | | 16 |
P18 (SRS35/TgSAG4) Plays a Role in the Invasion and Virulence of Toxoplasma gondii |
|
| Maguy Hamie,Nadim Tawil,Rana El Hajj,Rania Najm,Sara Moodad,Rita Hleihel,Martin Karam,Sana El Sayyed,Sébastien Besteiro,Marwan El-Sabban,Jean-Francois Dubremetz,Maryse Lebrun,Hiba El Hajj | | Frontiers in Immunology. 2021; 12 | | [Pubmed] | [DOI] | | 17 |
A rare case of an HIV-seronegative patient with Toxoplasma gondii meningoencephalitis |
|
| L. Pekova,P. Parusheva,M. Mitev,I. Dochev,C. Naydenov | | IDCases. 2021; 26: e01271 | | [Pubmed] | [DOI] | | 18 |
Prevalence and risk factors for exposure to Toxoplasma gondii in slaughterhouse workers in western Kenya |
|
| Elizabeth Anne Jessie Cook,Nduhiu Gitahi,William Anson de Glanville,Lian F. Thomas,Samuel Kariuki,Erastus Kang’ethe,Eric Maurice Fèvre | | BMC Infectious Diseases. 2021; 21(1) | | [Pubmed] | [DOI] | | 19 |
Estado epiléptico refractario en un varón de 76?años con antecedentes de trasplante renal |
|
| Carlos Lázaro, Lourdes Naranjo Ruiz-Atienza, Silvana Sarria, Elena Martínez Saez, María Sueiras, Carles Lorenzo, Estevo Santamarina | | Medicina Clínica Práctica. 2021; 4: 100302 | | [Pubmed] | [DOI] | | 20 |
Treatment of toxoplasmic encephalitis with the combination of clindamycin plus azithromycin in an HIV-infected patient: A case report |
|
| Keyhan Mohammadi,Hossein Khalili,Sirous Jafari,Shakila Yaribash | | Clinical Case Reports. 2021; 9(5) | | [Pubmed] | [DOI] | | 21 |
Toxoplasma gondii – gegenwärtige Arzneimittel und zukünftige Impfstoffe gegen eine unterschätzte Protozoonose |
|
| Yannick Borkens | | Der Internist. 2021; | | [Pubmed] | [DOI] | | 22 |
Neurologic Manifestations of Systemic Disease: Seizure |
|
| Santoshi Billakota,Claude Steriade,Jacqueline French | | Current Treatment Options in Neurology. 2020; 22(10) | | [Pubmed] | [DOI] | | 23 |
Risk factors associated with seropositivity for Toxoplasma gondii in population-based studies among immunocompromised patients (pregnant women, HIV patients and children) in West African countries, Cameroon and Gabon: a meta-analysis |
|
| Paul Olalekan Odeniran,Kehinde Foluke Omolabi,Isaiah Oluwafemi Ademola | | Acta Tropica. 2020; 209: 105544 | | [Pubmed] | [DOI] | | 24 |
The Changing Global Epidemic of HIV and Ocular Disease |
|
| Remco P. H. Peters,Philippe G. Kestelyn,Manfred Zierhut,John H. Kempen | | Ocular Immunology and Inflammation. 2020; 28(7): 1007 | | [Pubmed] | [DOI] | | 25 |
Molecular Detection of Toxoplasma gondii in the Slaughter Sheep and Goats from Shandong Province, Eastern China |
|
| Kang Ai,Cui-Qin Huang,Jing-Jing Guo,Hua Cong,Shen-Yi He,Chun-Xue Zhou,Wei Cong | | Vector-Borne and Zoonotic Diseases. 2020; 20(3): 193 | | [Pubmed] | [DOI] | | 26 |
Educational Case: Opportunistic Infections of the Central Nervous System |
|
| Steven Toffel, Lymaries Velez, Jorge Trejo-Lopez, Stacy G. Beal, Jesse L. Kresak | | Academic Pathology. 2020; 7: 2374289520 | | [Pubmed] | [DOI] | | 27 |
Global status of Toxoplasma gondii infection and associated risk factors in people living with HIV |
|
| Hanie Safarpour,Muge Cevik,Mehdi Zarean,Aleksandra Barac,Kareem Hatam-Nahavandi,Mohammad T. Rahimi,Hossein Bannazadeh Baghi,Tohid J. Koshki,Abdol S. Pagheh,Firooz Shahrivar,Mina Ebrahimi,Ehsan Ahmadpour | | AIDS. 2020; 34(3): 469 | | [Pubmed] | [DOI] | | 28 |
Update on the use of dapsone in dermatology |
|
| Nohra Ghaoui,Edith Hanna,Ossama Abbas,Abdul-Ghani Kibbi,Mazen Kurban | | International Journal of Dermatology. 2020; 59(7): 787 | | [Pubmed] | [DOI] | | 29 |
Comparison of serologic status of
Toxoplasma gondii
infection in pre- and post-heart transplantation in a pediatric population: A preliminary study |
|
| Elahe Orang,Shirin Sayyahfar,Mohammad Mahdavi,Khadijeh Khanaliha,Mehri Amiri | | Transplant Infectious Disease. 2020; 22(4) | | [Pubmed] | [DOI] | | 30 |
Transcriptional Analyses Identify Genes That Modulate Bovine Macrophage Response to Toxoplasma Infection and Immune Stimulation |
|
| Anton Gossner,Musa A. Hassan | | Frontiers in Cellular and Infection Microbiology. 2020; 10 | | [Pubmed] | [DOI] | | 31 |
Immunodiagnostics of cerebral toxoplasmosis depending on permeability of blood-brain barrier |
|
| Andriy V. Bondarenko,Dmitro V. Katsapov,Anatoliy V. Gavrylov,Tatiana V. Didova,Ivan A. Nahornyi | | Wiadomosci Lekarskie. 2020; 73(2): 285 | | [Pubmed] | [DOI] | | 32 |
Prediction of Toxoplasma gondii virulence factor ROP18 competitive inhibitors by virtual screening |
|
| Kun Yin,Guihua Zhao,Chao Xu,Xiao Qiu,Biwei Wen,Hui Sun,Gongzhen Liu,Ye Liu,Qingsong Zhao,Qingkuan Wei,Bingcheng Huang,Ge Yan,Jianping Cao | | Parasites & Vectors. 2019; 12(1) | | [Pubmed] | [DOI] | | 33 |
Impact of Interleukin-27p28 on T and B Cell Responses during Toxoplasmosis |
|
| Jeongho Park,Jonathan H. DeLong,James J. Knox,Christoph Konradt,Elia D. Tait Wojno,Christopher A. Hunter,Andreas J. Bäumler | | Infection and Immunity. 2019; 87(12) | | [Pubmed] | [DOI] | | 34 |
Transcriptome analysis of the effect of C-C chemokine receptor 5 deficiency on cell response to Toxoplasma gondii in brain cells |
|
| Kaoru Kobayashi,Kousuke Umeda,Fumiaki Ihara,Sachi Tanaka,Junya Yamagishi,Yutaka Suzuki,Yoshifumi Nishikawa | | BMC Genomics. 2019; 20(1) | | [Pubmed] | [DOI] | | 35 |
Sero-molecular evaluation of Toxoplasma gondii infection among HIV-positive patients |
|
| Ehsan Ahmadpour,Reza Pishkarie-Asl,Adel Spotin,Hossein Samadi Kafil,Hasan Didarlu,Yaghob Azadi,Aleksandra Barac | | Transactions of The Royal Society of Tropical Medicine and Hygiene. 2019; 113(12): 771 | | [Pubmed] | [DOI] | | 36 |
Actualización de la toxoplasmosis |
|
| Elizabeth Heavey | | Nursing (Ed. española). 2019; 36(2): 44 | | [Pubmed] | [DOI] | | 37 |
Focal Intramedullary Spinal Cord Lesion in Human Immunodeficiency Virus/Acquired Immunodeficiency Syndrome: Toxoplasmosis Versus Lymphoma |
|
| Jyodi Mohole,Allen L. Ho,Eric S. Sussman,Arjun V. Pendharkar,Marco Lee | | World Neurosurgery. 2019; 127: 227 | | [Pubmed] | [DOI] | | 38 |
HIV Initial Assessment and Routine Follow-up |
|
| Daniel A. Solomon | | Infectious Disease Clinics of North America. 2019; 33(3): 647 | | [Pubmed] | [DOI] | | 39 |
Acute disseminated encephalomyelitis and reactivation of cerebral toxoplasmosis in a child: Case report |
|
| Sami Bannoura,Rana El Hajj,Ibrahim Khalifeh,Hiba El Hajj | | IDCases. 2018; 13: e00434 | | [Pubmed] | [DOI] | | 40 |
Empiric neurocognitive performance profile discovery and interpretation in HIV infection |
|
| Daniela Gomez,Christopher Power,M. John Gill,Noshin Koenig,Roberto Vega,Esther Fujiwara | | Journal of NeuroVirology. 2018; | | [Pubmed] | [DOI] | | 41 |
The association between Toxoplasma gondii infection and hypertensive disorders in T2DM patients: a case-control study in the Han Chinese population |
|
| Yajing Han,Lihong Nie,Xiaohong Ye,Zixing Zhou,Shiqi Huang,Chengli Zeng,Congcong Guo,Meiling Ou,Di Xiao,Baohuan Zhang,Chuican Huang,Xingguang Ye,Chunxia Jing,Guang Yang | | Parasitology Research. 2018; | | [Pubmed] | [DOI] | | 42 |
Synthesis, molecular docking, ctDNA interaction, DFT calculation and evaluation of antiproliferative and anti-Toxoplasma gondii activities of 2,4-diaminotriazine-thiazole derivatives |
|
| Krzysztof Z. Laczkowski,Joanna Anusiak,Marta Switalska,Katarzyna Dzitko,Joanna Cytarska,Angelika Baranowska-Laczkowska,Tomasz Plech,Agata Paneth,Joanna Wietrzyk,Joanna Bialczyk | | Medicinal Chemistry Research. 2018; | | [Pubmed] | [DOI] | | 43 |
Toxoplasmosis update |
|
| Elizabeth Heavey | | Nursing. 2018; 48(7): 62 | | [Pubmed] | [DOI] | | 44 |
Cerebral toxoplasmosis in a patient with prolonged CD4 lymphopenia post autologous hemopoietic stem cell transplant |
|
| Arielle van Mourik,Andrew Grigg | | Leukemia & Lymphoma. 2018; : 1 | | [Pubmed] | [DOI] | | 45 |
Association between Toxoplasma gondii infection and history of blood transfusion: a case-control seroprevalence study |
|
| Cosme Alvarado-Esquivel,Luis Francisco Sánchez-Anguiano,Jesús Hernández-Tinoco,Agar Ramos-Nevarez,Sergio Estrada-Martínez,Sandra Margarita Cerrillo-Soto,Gonzalo Elías Medina-Heredia,Carlos Alberto Guido-Arreola,Araceli Alejandra Soto-Quintero,Isabel Beristain-Garcia | | Journal of International Medical Research. 2018; 46(4): 1626 | | [Pubmed] | [DOI] | | 46 |
Risk Assessment of Etanercept in Mice Chronically Infected With Toxoplasma gondii |
|
| Jing Yang,Luyao Wang,Dongmei Xu,Ding Tang,Senyang Li,Fen Du,Lixia Wang,Junlong Zhao,Rui Fang | | Frontiers in Microbiology. 2018; 9 | | [Pubmed] | [DOI] | | 47 |
Functional characterization of a unique cytochrome P450 in Toxoplasma gondii |
|
| Xiao Zhang,Taotao Zhang,Jing Liu,Muzi Li,Yong Fu,Jianhai Xu,Qun Liu | | Oncotarget. 2017; 8(70): 115079 | | [Pubmed] | [DOI] | | 48 |
Toxoplasma gondii and HIV: a never-ending story |
|
| Veeranoot Nissapatorn | | The Lancet HIV. 2017; | | [Pubmed] | [DOI] | |
|
 |
 |
|