Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-23T03:49:22.489Z Has data issue: false hasContentIssue false
  • English
  • Français

Maternal filarial infection: association of anti-sheath antibody responses with plasma levels of IFN-γ and IL-10

Published online by Cambridge University Press:  24 January 2013

K. G. ACHARY ,
N. N. MANDAL ,
S. MISHRA ,
S. S. SARANGI ,
S. K. KAR ,
A. K. SATAPATHY  and
M. S. BAL
K. G. ACHARY
Affiliation:
Division of Immunology, Regional Medical Research Centre (Indian Council of Medical Research), Chandrasekharpur, Bhubaneswar 751023, Odisha, India
N. N. MANDAL
Affiliation:
Division of Immunology, Regional Medical Research Centre (Indian Council of Medical Research), Chandrasekharpur, Bhubaneswar 751023, Odisha, India
S. MISHRA
Affiliation:
Division of Immunology, Regional Medical Research Centre (Indian Council of Medical Research), Chandrasekharpur, Bhubaneswar 751023, Odisha, India
S. S. SARANGI
Affiliation:
Department of Obsterics and Gynaecology, District Hospital, Khurda, Odisha, India
S. K. KAR
Affiliation:
Division of Immunology, Regional Medical Research Centre (Indian Council of Medical Research), Chandrasekharpur, Bhubaneswar 751023, Odisha, India
A. K. SATAPATHY
Affiliation:
Division of Immunology, Regional Medical Research Centre (Indian Council of Medical Research), Chandrasekharpur, Bhubaneswar 751023, Odisha, India
M. S. BAL*
Affiliation:
Division of Immunology, Regional Medical Research Centre (Indian Council of Medical Research), Chandrasekharpur, Bhubaneswar 751023, Odisha, India
*
*Corresponding author: Division of Immunology, Regional Medical Research Centre (Indian council of Medical Research), Chandrasekharpur, Bhubaneswar 751023, India. Tel: +91 674 301413. Fax: +91 674 2301351. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Maternal filarial infection influences the risk of acquiring infection and development of immunity in children. Here we have analysed the blood samples of 60 mothers (24 infected and 36 uninfected) and their corresponding cord bloods to assess the impact of maternal infection on the anti-sheath antibodies and cytokine production in neonates born from them. About 69·4% of non-infected mothers and their cord bloods showed the presence of anti-sheath antibodies, while only 16·6% of the cord bloods from infected mothers were positive for it. The IL-10 level was significantly high in cord bloods of infected mothers compared with non-infected mothers. At the same time the IL-10 level was also observed to be remarkably high in cord bloods of both infected and non-infected mothers negative for anti-sheath antibody. In contrast, IFN-γ levels were significantly high in cord bloods of non-infected mothers compared with infected mothers and the increment was prominent in cord bloods of both infected and non-infected mothers positive for anti-sheath antibody. The study reveals that the presence or absence of anti-sheath antibodies in association with cytokines skews the filarial specific immunity to either Th1 or Th2 responses in neonates. This may affect the natural history of filarial infection in early childhood.

Keywords

filariasisanti-sheath antibodiescytokinesmaternal filarial infection
Type
Research Article
Information
Parasitology , Volume 140 , Issue 5 , April 2013 , pp. 598 - 603
Copyright
Copyright © Cambridge University Press 2013

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alexander, N. D., Kazura, J. W., Bockarie, M. J., Perry, R. T., Dimber, Z. B., Grenfell, B. T. and Alpers, M. P. (1998). Prenatal infection confounded with local infection intensity as risk factors for childhood microfilaraemia in bancroftian filariasis. Transaction of the Royal Society of Tropical Medicine and Hygiene 92, 23–24.Google Scholar
Bal, M. S., Manadal, N. N., Das, M. K., Kar, S. K., Sarangi, S. S. and Beuria, M. K. (2010). Transplacental transfer of filarial antigens from Wuchereria bancrofti infected mothers to their offsprings. Parasitology 137, 669–673.Google Scholar
Beuria, M. K., Bal, M. S., Mandal, N .N. and Das, M. K. (2003). Age-dependent prevalence of asymptomatic amicrofilaraemic individuals in a Wuchereria bancrofti endemic region of India. Transaction of the Royal Society of Tropical Medicine and Hygiene 97, 297–298.Google Scholar
Carlier, Y. and Truyens, C. (1995). Influence of maternal infection on offspring resistance towards parasites. Parasitology Today 11, 94–99.Google Scholar
Freedman, D. O. (1998). Immune dynamics in the pathogenesis of human lymphatic filariasis. Parasitology Today 14, 229–234.Google Scholar
Guadalupe, I., Mitre, E., Benitez, S., Chico, M. E., Nutman, T. B. and Cooper, P. J. (2009). Evidence for in utero sensitization to Ascaris lumbricoides in newborns with ascariasis. Journal of Infectious Diseases 199, 1846–1850.CrossRefGoogle ScholarPubMed
Holt, P. G. (1995). Environmental factors and primary T-cell sensitization to inhalant allergen in infancy: reappraisal of the role of infections and air pollution. Pediatric Allergy and Immunology 6, 1–10.Google Scholar
King, C. L., Kumarswami, V., Poindexter, R. W., Kumari, S., Jayaraman, K., Alling, D. W., Ottesen, E. A. and Nutman, T. B. (1992). Immunologic tolerance in lymphatic filariasis. Diminished parasite specific T and B lymphocyte. Precursor frequency in the microfilaraemic state. Journal of Clinical Investigation 89, 1403–1410.Google Scholar
King, C. L., Mohanty, S., Kumarwsami, V., Abrams, J. S., Reghunathan, J., Jayaraman, K., Ottesen, E. A. and Nutman, T. B. (1993). Cytokine control of parasite specific anergy in human lymphatic filariasis. Preferential induction of a regulatory T helper type 2 lymphocyte subset. Journal of Clinical Investigation 92, 1667–1673.Google Scholar
Kohler, C., Adegnika, A. A., Linden, R. V. D., Agnandji, S. T., Chai, S. K., Luty, A. J. F., Szepfalusi, Z., Kremsner, P. G. and Yazdanbaksh, M. (2008). Comparision of immunological status of African and European cord blood mononuclear cells. Pediatric Research 64, 631–636.Google Scholar
Lammie, P. J. (2002). In utero exposure to filarial antigens and its influence on infection outcomes. In The Filaria (ed. Klei, T. R. and Rajan, T. V.), 5, 97–107. Kluwer Academic Publishers, the Netherlands.Google Scholar
Lammie, P. J., Hitch, W. L., Walker Allen, E. M., Hightower, W. and Eberhard, M. L. (1991). Maternal filarial infection is a risk factor for infection in children. Lancet 27, 1005–1006.CrossRefGoogle Scholar
Maizels, R. M., Bundy, D. A. P., Selkirk, M. E., Smith, D. F. and Anderson, R. M. (1993). Immunological modulation and evasion by helminth parasites in human populations. Nature 365, 797–804.Google Scholar
Malhotra, I., Mungai, P., Wamachi, A., Kioko, J. H., Kazura, J. W. and King, C. L. (1999). Helminth and Bacillus Calmette-Guerin induced immunity in children sensitized in utero to filariasis and schistosomiasis. Journal of Immunology 162, 6843–6848.Google Scholar
Malhotra, I., Mungia, P. L., Wamachi, A. N., Tisch, D. J., Kioko, J. M., Ouma, J. H., Muchiri, E., Kazura, J. W. and King, C. L. (2006). Prenatal T-cell immunity to Wuchereria bancrofti and its effect on filarial immunity and infection susceptibility during childhood. Journal of Infectious Diseases 193, 1005–1013.CrossRefGoogle ScholarPubMed
Malhotra, I., Ouma, J. and Wamachi, A. (1997). In utero exposure to helminth and mycobacterial antigens generates cytokine responses similar to that observed in adults. Journal of Clinical Investigation 99, 1759–1766.Google Scholar
Malhotra, I., Ouma, J., Wamachi, A., Kioko, J., Mungai, P., Njzovu, M., Kazura, J. W. and King, C. L. (2003). Influence of maternal filariasis on childhood infection and immunity to Wuchereria bancrofti in Kenya. Infection and Immunity 71, 5231–5237.Google Scholar
Pit, D. S. S., Polderman, A. M., Schulz-key, H. and Soboslay, P. T. (2000). Prenatal immune priming with helminth infections: parasite-specific cellular reactivity and Th1 and Th2 cytokines responses in neonates. Allergy 55, 732–739.Google Scholar
Prescott, S. L., Macaubas, C., Holt, B. J., Smallacombe, T. B., Loh, R., Sly, P. D. and Holt, P. G. (1998). Transplacental priming of the human immune system to environmental allergens: universal skewing of the initial T-cell response towards the Th2 cytokine profile. Journal of Immunology 160, 4730–4737.CrossRefGoogle Scholar
Rajan, T. V. (2007). Neonatal tolerance and patent filarial infection. Trends in Parasitology 23, 459–462.Google Scholar
Ravindran, B., Satapathy, A. K., Das, M. K., Pattnaik, N. M. and Subramanyam, V. R. (1990). Antibodies to microfilarial sheath in bancroftian filariasis – prevalence and characterization. Annals of Tropical Medicine and Parasitology 84, 607–613.Google Scholar
Ravindran, B., Satapathy, A. K., Sahoo, P. K. and Babu Geddam, J. J. (2000). Protective immunity in human bancroftian filariasis: inverse relationship between antibodies to microfilarial sheath and circulating filarial antigens. Parasite Immunology 22, 633–637.Google Scholar
Sepulveda, W., Be, C., Youlton, R., Gutierrez, J. and Carstens, E. (1999). Accuracy of the hemoglobin denaturation test for detecting maternal blood contamination of foetal blood samples for parental karyotyping. Prenatal Diagnosis 19, 927–929.Google Scholar
Simonsen, P. E. and Meyrowitsch, D. W. (1998). Bancroftian filariasis in Tanzania: specific antibody responses in relation to long-term observations on microfilaraemia. American Journal of Tropical Medicine and Hygiene 59, 667–672.CrossRefGoogle Scholar
Simonsen, P. E., Meyrowitsch, D. W., Jaoko, W. G., Malecela, M. N. and Michael, E. (2008). Immunoepidemiology of Wuchereria bancrofti infection in two east African communities: antibodies to microfilarial sheath and their role in regulating microfilaraemia. Acta Tropica 106, 200–206.Google Scholar
Simonsen, P. E., Meyrowitsch, D. W., Jaoko, W. G., Malecela, M. N., Mukoko, D., Pedersen, E. M., Ouma, J. H., Rwegoshora, R. T., Masese, N., Magnussen, P., Estambale, B. B. A. and Michale, E. (2002). Bancroftian filariasis infection, disease and specific antibody response patterns in a high and low endemicity community in East Africa. American Journal of Tropical Medicine and Hygiene 66, 550–559.Google Scholar
Steel, C., Guinea, A., McCartily, J. and Ottesen, E. A. (1994). Long-term effect of prenatal exposure to maternal microfilaraemia on immune responsiveness to filarial parasite antigen. Lancet 343, 890–893.Google Scholar