Seroprevalence and Associated Risk Factors for Toxoplasma gondii Infections Among Urban Poor Communities in Peninsular Malaysia

Acta Parasitologica (2020)Cite this article

Abstract

Purpose

Toxoplasmosis is a zoonotic infection linked to compromised hygiene and sanitation via the handling of infected cat faeces, eating undercooked contaminated meat or transplacental transmission. We conducted a study to determine seroprevalence and risk factors associated with toxoplasmosis among the urban poor communities in Malaysia.

Methods

The demographic profiles for each participant were obtained through a questionnaire survey prior to blood collection. A total of 389 participants were recruited and blood samples screened for the presence of anti-Toxoplasma IgG and IgM antibody using an ELISA commercial kit, SERION ELISA classic Toxoplasma gondii IgG and IgM.

Results

The overall T. gondii seroprevalence was 69.6% with 56.8% seropositive for anti-Toxoplasma IgG, 7.7% seropositive for anti-Toxoplasma IgM and 5.1% seropositive for both IgG and IgM antibodies. The presence of both antibody classes in blood samples indicated high avidity, suggesting latent infection. Univariate analysis revealed significant associations that included; age, ethnicity, location and employment status while, significant lifestyle factors included source of drinking water and eating style. A multifactorial statistical model that incorporated all the significant effects from the first-stage univariate analyses listed above revealed that age and ethnicity were the two dominant and independent effects on IgG seroprevalence. For seroprevalence of IgM, the multifactorial model revealed a significant interaction between work and accommodation. IgM seroprevalence was higher among the unemployed inhabitants of PPR (Program Perumahan Rakyat) than those living in non-PPR accommodation, and higher than among the employed irrespective of their accommodation.

Conclusion

High seroprevalence of Toxoplasmosis in the community calls for increased awareness of disease transmission and improvements in hygiene and sanitation.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2

References

  1. 1.

    Abu Bakar A, Khairul Anuar A, Ludin M, Rahmah N (1992) Survey of meat samples for Toxoplasma gondii in Northern Peninsular Malaysia. Diagnosa 6:700–704

    Google Scholar 

  2. 2.

    Brandon-Mong GJ, Seri CM, Anati NA, Sharma RS, Andiappan H, Tan TC, Lim YA, Nissapatorn V (2015) Seroepidemiology of toxoplasmosis among people having close contact with animals. Front Immunol 6:143. https://doi.org/10.3389/fimmu.2015.00143

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Department of Statistics Malaysia, 2018. The source Malaysia's Official Statistics. Department of Statistics Malaysia Official Portal. https://www.statistics.gov.my/index.php?r=column/ctheme&menu_id=L0pheU43NWJwRWVSZklWdzQ4TlhUUT09&bul_id=MDMxdHZjWTk1SjFzTzNkRXYzcVZjdz09/. Accessed 5 Mar 2017

  4. 4.

    Dubey JP (2008) The history of Toxoplasma gondii—the first 100 years. J Eukaryot Microbiol 55(6):467–475. https://doi.org/10.1111/j.1550-7408.2008.00345.x

    Article  PubMed  Google Scholar 

  5. 5.

    Dubey JP (2010) Toxoplasmosis of animals and humans. CRC Press, Boca Raton, p 313. https://doi.org/10.1186/1756-3305-3-112

    Google Scholar 

  6. 6.

    Elhadary YA, Samat N (2012) Political economy and urban poverty in developing countries: lesson learned from Sudan and Malaysia. J Geogr Geol 4(1):212–223. https://doi.org/10.5539/jgg.v4n1p212

    Article  Google Scholar 

  7. 7.

    Flegr J, Klapilová K, Kaňková Š (2014) Toxoplasmosis can be a sexually transmitted infection with serious clinical consequences. Not all routes of infection are created equal. Med Hypotheses 83(3):286–289. https://doi.org/10.1016/j.mehy.2014.05.019

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Flegr J, Prandota J, Sovičková M, Israili ZH (2014) Toxoplasmosis—a global threat correlation of latent toxoplasmosis with specific disease burden in a set of 88 countries. PLoS ONE 9(3):e90203. https://doi.org/10.1371/journal.pone.0090203

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    Gandahusada S (1991) Study on the prevalence of toxoplasmosis in Indonesia: a review. Southeast Asian J Trop Med Public Health 22:93–98

    PubMed  Google Scholar 

  10. 10.

    Hotez PJ, Bottazzi ME, Strych U, Chang LY, Lim YA, Goodenow MM, AbuBakar S (2015) Neglected tropical diseases among the Association of Southeast Asian Nations (ASEAN): overview and update. PLoS Negl Trop Dis 9(4):e0003575. https://doi.org/10.1371/journal.pntd.0003575

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Husni OM, Bowman DD, Khairul Anuar A, Rahmah N (1994) Evaluation of strategies to reduce the risk of congenital toxoplasmosis. J Eukaryot Microbiol 41:155

    Article  Google Scholar 

  12. 12.

    Innes EA (2010) A brief history and overview of Toxoplasma gondii. Zoonoses Public Health 57(1):1–7. https://doi.org/10.1111/j.1863-2378.2009.01276.x

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Jones JL, Dargelas V, Roberts J, Press C, Remington JS, Montoya JG (2009) Risk factors for Toxoplasma gondii infection in the United States. Clinx Infect Dis 49(6):878–884. https://doi.org/10.1086/605433

    Article  Google Scholar 

  14. 14.

    Juanah LY, Jalaludin J, Osman M, Osman ZJ (2013) Seroprevalence of Toxoplasma gondii among Schizophrenics in Hospital Kajang. Am J Infect Dis 9(1):11. https://doi.org/10.3844/ajidsp.2013.11.16

    Article  Google Scholar 

  15. 15.

    Kaňková Š, Hlaváčová J, Flegr J (2020) Oral sex: a new, and possibly the most dangerous, route of toxoplasmosis transmission. Med Hypotheses. https://doi.org/10.1016/j.mehy.2020.109725

    Article  PubMed  Google Scholar 

  16. 16.

    Khairul Anuar A, Afifi A, Dighe V, Rosiani A (1991) Toxoplasma antibody in pregnant women in Northern peninsular Malaysia. Diagnosis 5:18–23.

    Google Scholar 

  17. 17.

    Kolbekova P, Kourbatova E, Novotna M, Kodym P, Flegr J (2007) New and old risk-factors for Toxoplasma gondii infection: prospective cross-sectional study among military personnel in the Czech Republic. Clin Microbiol Infect 13:1012–1017. https://doi.org/10.1111/j.1469-0691.2007.01771.x

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Mohamed Z, Hajissa K (2016) Seroprevalence of Toxoplasma gondii infection among patients in Hospital Universiti Sains Malaysia. Trop Biomed 33(1):78–83. https://www.researchgate.net/publication/305702155

    Google Scholar 

  19. 19.

    Mok TY, Gan C, Sanyal A (2007) The determinants of urban household poverty in Malaysia. J Soc Sci 3(4):190–196. https://doi.org/10.3844/jssp.2007.190.196

    Article  Google Scholar 

  20. 20.

    Montoya J, Liesenfeld O (2004) Toxoplasmosis. Lancet 363(9425):1965–1976. https://doi.org/10.1016/S0140-6736(04)16412-X

    CAS  Article  PubMed  Google Scholar 

  21. 21.

    Munoz-Zanzi C, Campbell C, Berg S (2016) Seroepidemiology of toxoplasmosis in rural and urban communities from Los Rios Region, Chile. Infect Ecol Epidemiol 6(1):30597. https://doi.org/10.3402/iee.v6.30597

    Article  PubMed  Google Scholar 

  22. 22.

    Ngui R, Lim YA, Amir NF, Nissapatorn V, Mahmud R (2011) Seroprevalence and sources of toxoplasmosis among Orang Asli (indigenous) communities in Peninsular Malaysia. Am J Trop Med Hyg 85(4):660–666. https://doi.org/10.4269/ajtmh.2011.11-0058

    Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Nissapatorn V (2007) Toxoplasmosis: A silent threat in Southeast Asia. Res J Parasitol 2(1):1–12.https://doi.org/10.3923/jp.2007.1.12

    Article  Google Scholar 

  24. 24.

    Nissapatorn V, Abdullah KA (2004) Review on human toxoplasmosis in Malaysia: the past, present and prospective future. Southeast Asian J Trop Med Public Health 35:24–30

    PubMed  Google Scholar 

  25. 25.

    Nissapatorn V, Kamarulzaman A, Init I, Tan LH, Rohela M, Norliza A, Chan LL, Latt HM, Anuar AK, Quek KF (2002) Seroepidemiology of toxoplasmosis among HIV-infected patients and healthy blood donors. Med J Malaysia 57(3):304–310

    CAS  PubMed  Google Scholar 

  26. 26.

    Nissapatorn V, Lee C, Quek KF, Khairul AA (2003) AIDS-related opportunistic infections in Hospital Kuala Lumpur. Jpn J Infect Dis 56(5/6):187–192

    PubMed  Google Scholar 

  27. 27.

    Nissapatorn V, Lee CK, Cho SM, Rohela M, Anuar AK, Quek KF, Latt HM (2003) Toxoplasmosis in HIV/AIDS patients in Malaysia. Southeast Asian J Trop Med Public Health 57(2):18–19

    Google Scholar 

  28. 28.

    Nissapatorn V, Lee CK, Khairul AA (2003) Seroprevalence of toxoplasmosis among AIDS patients in Hospital Kuala Lumpur. Singap Med J 44:194–196

    CAS  Google Scholar 

  29. 29.

    Petersen E, Vesco G, Villari S, Buffolano W (2010) What do we know about risk factors for infection in humans with Toxoplasma gondii and how can we prevent infections? Zoonoses Public Health 57:8–17. https://doi.org/10.1111/j.1863-2378.2009.01278.x

    CAS  Article  PubMed  Google Scholar 

  30. 30.

    Ravichandran J, Rahmah N, Kamaruzzaman A, Khairul Anuar A (1998) Toxoplasma gondii antibodies among Malaysian pregnant women: a hospital-based study. Biomed Res 1:25–28

    Google Scholar 

  31. 31.

    Rohlf FJ, Sokal RR (1995) Statistical tables. Freeman W.H. and Company, San Francisco

    Google Scholar 

  32. 32.

    Sahimin N, Lim YA, Ariffin F, Behnke JM, Basáñez MG, Walker M, Lewis JW, Noordin R, Abdullah KA, Mohd Zain SN (2017) Socio-demographic determinants of Toxoplasma gondii seroprevalence in migrant workers of Peninsular Malaysia. Parasites Vectors 10(1):238. https://doi.org/10.1186/s13071-017-2167-8

    Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Sherina MS, Rampal L, Hejar AR, Rozali A, Mohd Yunus A (2011) Prevalence of urban poor and its health related factors in the state of Selangor, Malaysia. Malays J Med Health Sci 7(1):17–26. http://psasir.upm.edu.my/24406/

    Google Scholar 

  34. 34.

    Silva MG, Camara JT, Vinaud MC, Castro AM (2014) Epidemiological factors Associated with Seropositivity for Toxoplasmosis in Pregnant Women from Gurupi, State of Tocantins, Brazil. Rev Soc Bras Med Trop 47(4):469–475

    Article  Google Scholar 

  35. 35.

    Sinniah B, Thomas V, Yap PL (1984) Toxoplasmosis in West Malaysian population. Trop Biomed 1:81

    Google Scholar 

  36. 36.

    Siwar C, Ahmed F, Bashawir A, Mia MS (2016) Urbanization and urban poverty in Malaysia: consequences and vulnerability. J Appl Sci 16(4):154–160. https://doi.org/10.3923/jas.2016.154.160

    Article  Google Scholar 

  37. 37.

    Sukthana Y (2006) Toxoplasmosis: beyond animals to humans. Trends Parasitol 22(3):137–142. https://doi.org/10.1016/j.pt.2006.01.007

    Article  PubMed  Google Scholar 

  38. 38.

    Tan DS, Mak JW (1985) The role of toxoplasmosis in congenital disease in Malaysia. Southeast Asian J Trop Med Public Health 16(1):88–92

    CAS  PubMed  Google Scholar 

  39. 39.

    Tenter AM, Heckeroth AR, Weiss LM (2000) Erratum—Toxoplasma gondii: from animals to humans. Int J Parasitol 31(2):217–220

    Article  Google Scholar 

  40. 40.

    Thomas V, Sinniah B, Yap PL (1980) Prevalence of antibodies including IgM to Toxoplasma gondii in Malaysians. Southeast Asian J Trop Med Public Health 11(1):119–125

    CAS  PubMed  Google Scholar 

  41. 41.

    UNICEF, 2018. Children without: a study of child poverty and deprivation in low cost flats. https://sustainabledevelopment.un.org/post2015/transformingourworld . Accessed 23 May 2018

  42. 42.

    United Nations, 2015. Transforming our World: the 2030 agenda for sustainable development. https://sustainabledevelopment.un.org/post2015/transformingourworld . Accessed 23 May 2018

  43. 43.

    Wong A, Tan KH, Tee CS, Yeo GSH (2000) Seroprevalence of cytomegalovirus, Toxoplasma and parvovirus in pregnancy. Singap Med J 41(4):151–155

    CAS  Google Scholar 

  44. 44.

    Wreghitt T, Joynson D (2001) Toxoplasma infection in immunosuppressed (HIV-negative) patients. Toxoplasmosis, a comprehensive clinical guide. Cambridge University Press, New York, pp 178–192

    Google Scholar 

  45. 45.

    Yahaya N (1991) Review of toxoplasmosis in Malaysia. Southeast Asian J Trop Med Public Health 22:102–106

    PubMed  Google Scholar 

Download references

Acknowledgements

The authors are very grateful to the Ministry of Health, Malaysia and all participants for their support to this study. Special mention also goes to medical staff from University of Malaya Medical Centre (UMMC) and UC Bioscience, Kuala Lumpur for their technical assistance. OR Software was provided by Gilbert, FS and Behnke JM. This research work was funded by University of Malaya, Faculty Grant GPF 012B-2018, Fundamental Research Grant Scheme (FRGS) from Ministry of Higher Education, FP015-2014B and Ministry of Education, Malaysia for niche area research under the Higher Institution Centre of Excellence (HICoE) program (Project MO002-2019) (Vector—Cat).

Author information

Affiliations

  1. Tropical Infectious Diseases Research and Education Centre (TIDREC), Universiti Malaya, 50603, Kuala Lumpur, Malaysia

    Norhidayu Sahimin

  2. Institute of Biological Sciences, Faculty of Science, Universiti Malaya, 50603, Kuala Lumpur, Malaysia

    Izzah Ruzana Mohd Hanapi, Zarin Amalina Nurikhan & Siti Nursheena Mohd Zain

  3. School of Life Sciences, University of Nottingham, University Park, Nottingham, NG7 2RD, UK

    Jerzy M. Behnke

Authors
  1. Norhidayu Sahimin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Izzah Ruzana Mohd Hanapi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zarin Amalina Nurikhan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jerzy M. Behnke
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Siti Nursheena Mohd Zain
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Siti Nursheena Mohd Zain.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sahimin, N., Mohd Hanapi, I.R., Nurikhan, Z.A. et al. Seroprevalence and Associated Risk Factors for Toxoplasma gondii Infections Among Urban Poor Communities in Peninsular Malaysia. Acta Parasit. (2020). https://doi.org/10.1007/s11686-020-00304-0

Download citation

Keywords

  • Toxoplasmosis
  • Toxoplasma gondii
  • Seroprevalence
  • Urban poor communities
  • Malaysia