International Scholarly Research Notices

International Scholarly Research Notices / 2013 / Article

Research Article | Open Access

Volume 2013 |Article ID 123858 | https://doi.org/10.1155/2013/123858

Dagnachew Muluye, Yitayih Wondimeneh, Yeshambel Belyhun, Feleke Moges, Mengistu Endris, Getachew Ferede, Gashaw Yitayew, Digsu Negese, "Prevalence of Toxoplasma gondii and Associated Risk Factors among People Living with HIV at Gondar University Hospital, Northwest Ethiopia", International Scholarly Research Notices, vol. 2013, Article ID 123858, 5 pages, 2013. https://doi.org/10.1155/2013/123858

Prevalence of Toxoplasma gondii and Associated Risk Factors among People Living with HIV at Gondar University Hospital, Northwest Ethiopia

Academic Editor: R. Dey
Received18 Jun 2013
Accepted10 Jul 2013
Published12 Aug 2013

Abstract

Background. Toxoplasma gondii is an obligate intracellular protozoan parasite and is a major opportunistic pathogen in immune-compromised hosts. This study assessed the prevalence of T. gondii and associated risk factors among people living with HIV. Methods and Materials. A cross-sectional study was carried out among people living with HIV attending Gondar University Hospital. A structured and pretested questionnaire was used to collect sociodemographic factors, and 10mL of venous blood was collected for anti-Toxoplasma antibody test and determination of CD4 levels. Serum was tested in duplicate for anti-Toxoplasma antibody using rapid slide agglutination test. Results. A total of 170 study subjects were enrolled in the study. Seroprevalence of T. gondii among the study participants was 76.5% (95% CI: 69.0–82.8). High proportions of seropositive individuals (64.7%) were found under the child bearing age groups. The mean CD4+ lymphocyte count of HIV monoinfected participants was cells/mm3 while coinfected study participants had mean CD4+ lymphocyte count of cells/mm3 with value of 0.01. Conclusion. The seroprevalence of T. gondii among people living with HIV was high. Cautious followup of HIV-positive patients is needed to prevent development of toxoplasmic encephalitis and other related complications.

1. Introduction

Toxoplasma gondii  is an obligate intracellular protozoan of worldwide distribution and is a major opportunistic pathogen in immunocompromised hosts. Infection is mainly acquired by ingestion of food, water or soil that is contaminated with oocysts shed by cats or by eating undercooked or raw meat containing tissue cysts [1].

Toxoplasmosis in patients with AIDS is usually the result of reactivation of latent infection. In HIV-positive people, without previous exposure to T. gondii, the acute infection could not be well controlled and in these susceptible hosts a wide range of infections is expected [2]. Toxoplasmosis occurs mostly in brain that is the frequent clinical finding [3, 4] even in patients with latent toxoplasmosis. Seroprevalence varies greatly in geographical regions within a country and within different ethnic groups according to different environments, social customs, and habits of different populations [5, 6].

There is wide geographic variation in the prevalence of latent Toxoplasma infection. Studies from Latin America, Europe, Asia, and Africa have reported a range of prevalence estimates of 30%–75% and prevalence estimates from US studies have had a range of 3%–42% [7, 8]. Worldwide prevalence rate of latent Toxoplasma infections in HIV-infected patients including Ethiopia has been found to vary greatly from 3% to 97% [9, 10].

It is usually subacute in onset with focal neurologic signs frequently accompanied by fever, altered mental state, and headache. Cerebellar, subcortical, or cortical lesions can be present in over 50% of the infected cases, resulting in hemiparesis, ambulatory, and gait or speech abnormalities [11]. A significant proportion of encephalitic patients can also present with neuropsychiatric disorders including psychosis, dementia, anxiety, and personality disorder [12]. However, despite the recognized public health importance of T. gondii in different parts of the world, studies on the prevalence of toxoplasmosis among people living with HIV are scanty in Ethiopia and unavailable in the study area.

Despite complications of HIV/AIDS patients due to rampant opportunistic infections, reports on the magnitude of T. gondii in such population groups are very minimal. The epidemiology of toxoplasmosis in HIV/AIDS patients should be able to provide us with a better understanding of the clinical scenario. Therefore, the present study assessed the prevalence of T. gondii and associated factors among people living with HIV.

2. Methods

2.1. Study Design, Area, and Period

An institution-based cross-sectional study was carried out among people living with HIV from November 2012 to February 2013 at Gondar University Hospital, Northwest Ethiopia.

2.2. Study Population and Sampling Procedures

The source populations for this study were all HIV-positive patients attending Gondar University Hospital. A single population proportion formula was used to estimate sample size. The following assumptions have been made: 95% confidence interval, 93% proportion of T. gondii seropositivity among HIV-positive individuals [9], 4% margin of error, and 10% expected nonresponse rate. As a result a total of 170 study subjects were enrolled in the study. Systematic random sampling technique was used to select study participants.

2.3. Data Collection Procedures

Interview using structured and pretested questionnaire was performed to investigate risk factors associated with  T. gondii  infection, including consumption of raw meat and keeping pets (cats and dogs), and to collect data on sociodemographic characteristics of study subject. Ten milliliter (10 mL) of venous blood was aseptically collected for the determination of T. gondii seroprevalence and CD4+ levels from each study participant. The CD4+ levels were determined by using BD FACS count flow cytometry [13]. Sera were tested in duplicate for anti-Toxoplasma antibody using Toxo Latex manufactured by Linear chemicals S.L, Barcellona, Spain, with a sensitivity of 92% and specificity of 95%. Positive and negative controls were included per each batch of test run to ensure that reagents are working properly, and technical procedures are carried out correctly.

2.4. Data Analysis Procedure

Data were entered and analyzed using SPSS version 20 statistical package. The association between selected variables and seropositivity was analyzed using Chi-square test and -test was used to see the association between mean CD4+ values and seropositivity. value ≤0.05 was considered as significant.

2.5. Ethical Considerations

Ethical clearance was obtained from Ethical Review Board of University of Gondar, College of Medicine and Health Sciences. Informed and written consent was obtained from each study participant prior to data collection and all results were kept confidential.

3. Results

3.1. Sociodemographic Characteristics

A total of 170 study subjects were enrolled in the study. Out of these, 96 (56.5%) were females. The mean age of study participants was years. The majority of study participants (91.2%) were from urban residents. More than 89% of the participants were orthodox religion followers and 43.5% were married. Out of the total study participants, 42 (24.7%) were governmental employees followed by daily laborers (21.2%) and housewives (21.1%). More than one-third of study participants were secondary school and above in educational status (Table 1).


CharacteristicsNumber ( )Percent (%)

Age of the respondents
 <182011.8
 18–304828.2
 31–406135.9
 41–503218.8
 >5095.3
Sex
 Female9656.5
 Male7443.5
Residency
 Urban 15591.2
 Rural158.8
Religion
 Orthodox15289.4
 Muslim169.4
 Protestant21.2
Marital status
 Single3922.9
 Married7443.5
 Divorced3319.4
 Windowed2414.1
Educational status
 No formal education 5029.4
 Primary education5834.1
 Secondary and above6236.5
Occupation
 Government employee4224.7
 Housewife3621.2
 Student1911.2
 Merchant2212.9
 Daily laborer3621.2
 Farmer105.9
 Others52.9

3.2. Prevalence of T. gondii

Seroprevalence of T. gondii among study participants was 130/170 (76.5%) (95% CI: 69.0–82.8). Among seropositive study participants, 71 (54.6%) were females. More than 38% of seropositive individuals were under the age group of 31–40 years followed by 18–30 years (26.2%). All farmers were found to be infected by T. gondii. Of all study participants, 137 (80.6%) were on ART while 19.4% were pre-ART and 80% of seropositive study participants were on ART. Among 27 study participants who had contact with dog, 22 (81.5%) were seropositive for T. gondii.  Of 45 study participants who had contact with cats, 35 (77.8%) were seropositive for T. gondii. More than 30% of study participants had frequent experience of raw meat consumption. Of these, 76.9% were seropositive for T. gondii. Seventy-nine (60.8%) of seropositive study participants had CD4+ lymphocyte count of ≥350 cells/mm3. The mean CD4+ lymphocyte count of HIV monoinfected participants was  cells/mm3, and T. gondii seropositive study participants had mean CD4+ lymphocyte count of  cells/mm3 with value of 0.01 (Table 2). Statistical analysis was performed to see the association between variables suspected as risk factors and seroprevalence of T. gondii; meanwhile all the variables did not show statistically significant association.


CharacteristicsT. gondii
Positive (%)Negative (%)

Age of the respondents
 <1815 (11.5)5 (12.5)
 18–3034 (26.2)14 (35.0)
 31–4050 (38.5)11 (27.5)
 41–5023 (17.7)9 (22.5)
 >508 (6.2)1 (2.5)
Sex
 Female71 (54.6)25 (62.5)
 Male59 (45.4)15 (37.5)
Residency
 Urban 119 (91.5)36 (90.0)
 Rural11 (8.5)4 (10.0)
Religion
 Orthodox115 (88.5)37 (92.5)
 Muslim13 (10.0)3 (7.5)
 Protestant2 (1.5)0 (0.0)
Marital status
 Single28 (21.5)11 (27.5)
 Married55 (42.3)19 (47.5)
 Divorced26 (20.0)7 (17.5)
 Window21 (16.2)3 (7.5)
Educational status
 Illiterate41 (31.5)9 (22.5)
 Primary education42 (32.3)16 (40.0)
 Secondary and above47 (36.2)15 (37.5)
Occupation
 Govt. employee33 (25.4)9 (22.5)
 Housewife24 (18.5)12 (30.0)
 Student13 (10)6 (15.0)
 Merchant16 (12.3)6 (15.0)
 Daily laborer30 (23.1)6 (15.0)
 Farmer10 (7.7)0 (0.0)
 Other4 (3.1)1 (2.5)
ART
 Pre-ART 26 (20.0)7 (17.5)
 On ART104 (80.0)33 (82.5)
CD4+ lymphocyte count
 <200 cells/mm323 (17.7)4 (10.0)
 200–349 cells/mm328 (21.5)12 (30.0)
 ≥350 cells/mm379 (60.8)24 (60.0)
Do you have contact with the cat?
 Yes35 (26.9)10 (25.0)
 No95 (73.1)30 (75.0)
Do you have contact with the dog?
 Yes22 (16.9)5 (12.5)
 No108 (83.1)35 (87.5)
Source of water for drinking
 Pipe water123 (94.6)38 (95.0)
 River3 (2.3)2 (5.0)
 Well3 (2.3)0 (0.0)
 Other1 (0.8)0 (0.0)
Do you boil the water before drinking
 Yes5 (3.8)4 (10.0)
 No125 (96.2)36 (90.0)
Raw meat consumption
 Yes40 (30.8)12 (30.0)
 No90 (69.2)28 (70.0)

4. Discussion

Worldwide prevalence rate of latent Toxoplasma infections in HIV-infected patients including Ethiopia has been found to vary greatly from 3% to 97% [9, 10]. In this study, 76.5% of study participants were seropositive for T. gondii. This result was lower than study findings of Addis Ababa, Ethiopia (93.3%) [9]. The lower result in our study could be due to the diagnostic method used. In contrast, this result was higher than findings in Iran (38.01%) and Malaysia (44.8%) [14, 15]. The difference might be due to the sociocultural differences in keeping dogs and cats at home. Moreover, consumption of raw and insufficiently cooked meat consumption is higher in Ethiopia which is supposed to be a risk factor for T. gondii infection.

In this study, more than two-thirds of study participants had cats and/or dogs at their home. Unpredictably, ownership of cats and/or dogs, age, and sex were not statistically significant with seroprevalence of T. gondii. This could be due to the small sample size we used as well as the mass coverage of supposed factors irrespective of age and sex. In addition, a study conducted in South Africa, with the same sample size of study participants, showed lower (18.1%) prevalence compared to the current study [16]. Age and sex were not statistically significant which is in agreement with our study. All farmers were seropositive in this study which is supported by previously recognized risk factors which are common among farmers.

The majority of seropositive individuals (64.7%) were found under the child bearing age groups (18–40 year) which was also reported in other studies [14, 17]. This might cause congenital anomalies for newborns born from infected mothers not only HIV-positive mothers but also among the general population.

The mean CD4+ lymphocyte count of HIV monoinfected participants was  cells/mm3 while T. gondii seropositive study participants had mean CD4+ lymphocyte count of  cells/mm3 with value of 0.01. However, it is difficult to explain the effect of CD4+ lymphocyte count level on T. gondii infection as recent or remote infection is not determined. The largest proportion (60.8%) of seropositive study participants had CD4+ lymphocyte count of ≥350 cells/mm3. Risk of development of toxoplasmic encephalitis for AIDS patients who were seropositive for T. gondii  is higher within two years after the onset of AIDS, while toxoplasmic encephalitis occurs rarely in AIDS patients who were seronegative for the parasite during pre-AIDS stage [18]. In this study, rapid slide agglutination test was used to detect anti-Toxoplasma antibody, hence it is the limitation of the study.

5. Conclusion

The seroprevalence of T. gondii among people living with HIV was high. Cautious followup of HIV-positive individuals is needed to prevent development of toxoplasmic encephalitis and other related complications as studies confirmed that T. gondii infection was high among people living with HIV.

Conflict of Interests

The authors declare that they have no conflict of interests.

Acknowledgments

The authors acknowledge the technical support provided by University of Gondar. Their special thanks and appreciation go to all the study participants who voluntarily participated in this study. We also thank Gondar University hospital ART laboratory personnel for their support during data collection.

References

  1. R. Fayer, J. P. Dubey, and D. S. Lindsay, “Zoonotic protozoa: from land to sea,” Trends in Parasitology, vol. 20, no. 11, pp. 531–536, 2004. View at: Publisher Site | Google Scholar
  2. B. G. Gellin and R. Soave, “Coccidian infections in AIDS: toxoplasmosis, cryptosporidiosis, and isosporiasis,” Medical Clinics of North America, vol. 76, no. 1, pp. 205–234, 1992. View at: Google Scholar
  3. C. Contini, “Clinical and diagnostic management of toxoplasmosis in the immunocompromised patient,” Parassitologia, vol. 50, no. 1-2, pp. 45–50, 2008. View at: Google Scholar
  4. J. E. Vidal, A. V. Hernandez, A. C. Penalva de Oliveira, R. F. Dauar, S. P. Barbosa Jr., and R. Focaccia, “Cerebral toxoplasmosis in HIV-positive patients in Brazil: clinical features and predictors of treatment response in the HAART era,” AIDS Patient Care and STDs, vol. 19, no. 10, pp. 626–634, 2005. View at: Publisher Site | Google Scholar
  5. P. A. Conrad, M. A. Miller, C. Kreuder et al., “Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment,” International Journal for Parasitology, vol. 35, no. 11-12, pp. 1155–1168, 2005. View at: Publisher Site | Google Scholar
  6. B. T. E. Chan, R. N. Amal, M. I. Noor Hayati et al., “Seroprevalence of toxoplasmosis among migrant workers from different Asian countries working in Malaysia,” Southeast Asian Journal of Tropical Medicine and Public Health, vol. 39, no. 1, pp. 9–13, 2008. View at: Google Scholar
  7. J. Zufferey, A. Sugar, P. Rudaz, J. Bille, M. P. Glauser, and J. P. Chave, “Prevalence of latent toxoplasmosis and serological diagnosis of active infection in HIV-Positive patients,” European Journal of Clinical Microbiology and Infectious Diseases, vol. 12, no. 8, pp. 591–595, 1993. View at: Google Scholar
  8. B. J. Luft and J. S. Remington, “Toxoplasmic encephalitis,” Journal of Infectious Diseases, vol. 157, no. 1, pp. 1–6, 1988. View at: Google Scholar
  9. T. Shimelis, M. Tebeje, E. Tadesse, B. Tegbaru, and A. Terefe, “Sero-prevalence of latent Toxoplasma gondii infection among HIV-infected and HIV-uninfected people in Addis Ababa, Ethiopia: a comparative cross-sectional study,” BMC Research Notes, vol. 2, article 213, 2009. View at: Publisher Site | Google Scholar
  10. V. Nissapatorn, “Toxoplasmosis in HIV/AIDS: a living legacy,” Southeast Asian Journal of Tropical Medicine and Public Health, vol. 40, no. 6, pp. 1158–1178, 2009. View at: Google Scholar
  11. B. J. Luft, R. Hafner, A. H. Korzun et al., “Toxoplasmic encephalitis in patients with the acquired immunodeficiency syndrome. Members of the ACTG 077p/ANRS 009 Study Team,” The New England Journal of Medicine, vol. 329, pp. 995–1000, 1993. View at: Google Scholar
  12. E. F. Torrey and R. H. Yolken, “Toxoplasma gondii and Schizophrenia,” Emerging Infectious Diseases, vol. 9, no. 11, pp. 1375–1380, 2003. View at: Google Scholar
  13. “BD FACS Count System User's Guide for Use with BD FACS Count CD4 Reagents,” 2008, http://www.bdbiosciences.com/external_files/pm/doc/manuals/live/web_enabled/339011. View at: Google Scholar
  14. R. Shafiei, Z. Riazi, M. Sarvghad, M. G. Sharifdini, A. Mahmoodzadeh, and M. Hajia, “Prevalence of IgG and IgM anti-Toxoplasma gondii antibodies in HIV positive patients in northeast of Iran,” Iranian Journal of Pathology, vol. 6, no. 2, pp. 68–72, 2011. View at: Google Scholar
  15. V. Nissapatorn, C. Lee, K. F. Quek, C. L. Leong, R. Mahmud, and K. A. Abdullah, “Toxoplasmosis in HIV/AIDS patients: a current situation,” Japanese Journal of Infectious Diseases, vol. 57, no. 4, pp. 160–165, 2004. View at: Google Scholar
  16. P. O. Bessong and L. M. Mathomu, “Seroprevalence of HTLV1/2, HSV1/2 and Toxoplasma gondii among chronic HIV-1 infected individuals in rural northeastern South Africa,” African Journal of Microbiology Research, vol. 4, no. 23, pp. 2587–2591, 2010. View at: Google Scholar
  17. A. Pauwels, M. C. Meyohas, M. Eliaszewicz, C. Legendre, G. Mougeot, and J. Frottier, “Toxoplasma colitis in the acquired immunodeficiency syndrome,” American Journal of Gastroenterology, vol. 87, no. 4, pp. 518–519, 1992. View at: Google Scholar
  18. M. A. Abu-Madi, N. Al-Molawi, and J. M. Behnke, “Seroprevalence and epidemiological correlates of Toxoplasma gondii infections among patients referred for hospital-based serological testing in Doha, Qatar,” Parasites and Vectors, vol. 1, no. 1, article 39, 2008. View at: Publisher Site | Google Scholar

Copyright © 2013 Dagnachew Muluye et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


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