Maternal schistosomiasis japonica is associated with maternal, placental, and fetal inflammation

Infection and Immunity

Volumn 79, Issue 3, 2011, Pages 1254-1261

  Kurtis, Jonathan D ^a   Higashi, Ashley ^a   Wu, Hai Wei ^a   Gundogan, Fusun ^a   McDonald, Emily A ^a   Sharma, Surrendra ^a   PondTor, Sunthorn ^a   Jarilla, Blanca ^b   Sagliba, Marriane Joy ^b   Gonzal, Analisa ^b   Olveda, Remigio ^b   Acosta, Luz ^a,b   Friedman, Jennifer F ^a  

^a BROWN UNIVERSITY   (United States)

^b RESEARCH INSTITUTE FOR TROPICAL MEDICINE   (Philippines)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA RECEPTOR; TUMOR NECROSIS FACTOR ALPHA RECEPTOR 2; UNCLASSIFIED DRUG;

ACUTE SUBCHORIONITIS; ADULT; ARTICLE; BIRTH WEIGHT; CHRONIC DECIDUITIS; CHRONIC INFLAMMATION; CHRONIC VILLITIS; CYTOKINE PRODUCTION; FEMALE; FETAL INFLAMMATION; GESTATIONAL AGE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MAJOR CLINICAL STUDY; MATERNAL BLOOD; PHILIPPINES; PREGNANCY; PREGNANT WOMAN; PRIORITY JOURNAL; SCHISTOSOMA JAPONICUM; SCHISTOSOMIASIS JAPONICA; SPECIES ENDEMICITY; TROPHOBLAST;

ADULT; ANIMALS; BIRTH WEIGHT; FEMALE; FETAL DISEASES; FETUS; HUMANS; INFLAMMATION; PHILIPPINES; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS, PARASITIC; SCHISTOSOMA JAPONICUM; SCHISTOSOMIASIS JAPONICA;

EID: 79952286964     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01072-10     Document Type: Article

References (57)

1. Abdel-Aaty, H. E., M. M. Selim, and H. A. Abdel-Rehim. 1999. Study of gamma-interferon in schistosomiasis mansoni, autoimmune diseases and schistosomal arthropathy. J. Egypt Soc. Parasitol. 29:721-734.
2. Abdel Azim, A., H. A. Sedky, M. A. el-Tahawy, A. A. Fikry, and H. Mostafa. 1995. Serum levels of tumor necrosis factor in different stages of schistosomal infection. J. Egypt Soc. Parasitol. 25:279-287.
3. Amano, T., G. L. Freeman, Jr., and D. G. Colley. 1990. Reduced reproductive efficiency in mice with schistosomiasis mansoni and in uninfected pregnant mice injected with antibodies against Schistosoma mansoni soluble egg antigens. Am. J. Trop. Med. Hyg. 43:180-185.
4. Attallah, A. M., G. E. Ghanem, H. Ismail, and A. M. El Waseef. 2003. Placental and oral delivery of Schistosoma mansoni antigen from infected mothers to their newborns and children. Am. J. Trop. Med. Hyg. 68:647-651.
5. Ballard, J. L., K. K. Novak, and M. Driver. 1979. A simplified score for assessment of fetal maturation of newly born infants. J. Pediatr. 95:769-774. (Pubitemid 10228542)
6. Benyo, D. F., A. Smarason, C. W. Redman, C. Sims, and K. P. Conrad. 2001. Expression of inflammatory cytokines in placentas from women with preeclampsia. J. Clin. Endocrinol. Metab. 86:2505-2512.
7. Bittencourt, A. L., M. A. Cardoso de Almeida, M. A. Iunes, and L. D. Casulari da Motta. 1980. Placental involvement in schistosomiasis mansoni. Report of four cases. Am. J. Trop. Med. Hyg. 29:571-575.
8. Cannon, J. G., J. L. Nerad, D. D. Poutsiaka, and C. A. Dinarello. 1993. Measuring circulating cytokines. J. Appl. Physiol. 75:1897-1902.
9. Carlier, Y., H. Nzeyimana, D. Bout, and A. Capron. 1980. Evaluation of circulating antigens by a sandwich radioimmunoassay, and of antibodies and immune complexes, in Schistosoma mansoni-infected African parturients and their newborn children. Am. J. Trop. Med. Hyg. 29:74-81.
10. Chaouat, G., et al. 1990. Control of fetal survival in CBA x DBA/2 mice by lymphokine therapy. J. Reprod. Fertil. 89:447-458.
11. Coutinho, H. M., et al. 2006. Pro-inflammatory cytokines and C-reactive protein are associated with undernutrition in the context of Schistosoma japonicum infection. Am. J. Trop. Med. Hyg. 75:720-726.
12. Coutinho, H. M., et al. 2005. Nutritional status and serum cytokine profiles in children, adolescents, and young adults with Schistosoma japonicum-associated hepatic fibrosis, in Leyte, Philippines. J. Infect. Dis. 192:528-536.
13. Crocker, I. P., S. Cooper, S. C. Ong, and P. N. Baker. 2003. Differences in apoptotic susceptibility of cytotrophoblasts and syncytiotrophoblasts in normal pregnancy to those complicated with preeclampsia and intrauterine growth restriction. Am. J. Pathol. 162:637-643.
14. de Jesus, A. R., et al. 2002. Clinical and immunologic evaluation of 31 patients with acute schistosomiasis mansoni. J. Infect. Dis. 185:98-105.
15. Døllner, H., L. Vatten, J. Halgunset, S. Rahimipoor, and R. Austgulen. 2002. Histologic chorioamnionitis and umbilical serum levels of pro-inflammatory cytokines and cytokine inhibitors. BJOG 109:534-539. (Pubitemid 37337994)
16. Ekerfelt, C., et al. 2002. Spontaneous secretion of interleukin-4, interleukin-10 and interferon-gamma by first trimester decidual mononuclear cells. Am. J. Reprod. Immunol. 47:159-166.
17. el-Nahal, H. M., et al. 1998. Mutual effect of Schistosoma mansoni infection and pregnancy in experimental C57 BL/6 black mice. J. Egypt Soc. Parasitol. 28:277-292.
18. Fried, M., R. O. Muga, A. O. Misore, and P. E. Duffy. 1998. Malaria elicits type 1 cytokines in the human placenta: IFN-gamma and TNF-alpha associated with pregnancy outcomes. J. Immunol. 160:2523-2530.
19. Friedman, J. F., et al. 2005. Relationship between Schistosoma japonicum and nutritional status among children and young adults in Leyte, the Philippines. Am. J. Trop. Med. Hyg. 72:527-533.
20. Friedman, J. F., P. Mital, H. K. Kanzaria, G. R. Olds, and J. D. Kurtis. 2007. Schistosomiasis and pregnancy. Trends Parasitol. 23:159-164.
21. Hagberg, H., U. B. Wennerholm, and K. Savman. 2002. Sequelae of chorioamnionitis. Curr. Opin. Infect. Dis. 15:301-306.
22. Hahn-Zoric, M., et al. 2002. Aberrations in placental cytokine mRNA related to intrauterine growth retardation. Pediatr. Res. 51:201-206.
23. Hanna, N., et al. 2000. Gestational age-dependent expression of IL-10 and its receptor in human placental tissues and isolated cytotrophoblasts. J. Immunol. 164:5721-5728. (Pubitemid 30389814)
24. Hassan, M. M., et al. 1997. Transmission of circulating schistosomal antigens from infected mothers to their newborns. J. Egypt Soc. Parasitol. 27:773-780.
25. Hennessy, A., H. L. Pilmore, L. A. Simmons, and D. M. Painter. 1999. A deficiency of placental IL-10 in preeclampsia. J. Immunol. 163:3491-3495.
26. Holcberg, G., et al. 2001. Increased production of tumor necrosis factor-alpha (TNF-alpha) by IUGR human placentae. Eur. J. Obstet. Gynecol. Reprod. Biol. 94:69-72.
27. Khalil, H. M., et al. 1995. Serum levels of tumour necrosis factor-alpha in schistosomiasis mansoni and their analogous changes in collagen diseases and schistosomal arthropathy. J. Egypt Soc. Parasitol. 25:427-436.
28. King, C. L., et al. 1998. B cell sensitization to helminthic infection develops in utero in humans. J. Immunol. 160:3578-3584. (Pubitemid 28164754)
29. Krishnan, L., L. J. Guilbert, T. G. Wegmann, M. Belosevic, and T. R. Mosmann. 1996. T helper 1 response against Leishmania major in pregnant C57BL/6 mice increases implantation failure and fetal resorptions. Correlation with increased IFN-gamma and TNF and reduced IL-10 production by placental cells. J. Immunol. 156:653-662.
30. Leenstra, T., et al. 2006. Schistosomiasis japonica, anemia, and iron status in children, adolescents, and young adults in Leyte, Philippines. Am. J. Clin. Nutr. 83:371-379.
31. Malhotra, I., et al. 1997. In utero exposure to helminth and mycobacterial antigens generates cytokine responses similar to that observed in adults. J. Clin. Invest. 99:1759-1766.
32. Marzi, M., et al. 1996. Characterization of type 1 and type 2 cytokine production profile in physiologic and pathologic human pregnancy. Clin. Exp. Immunol. 106:127-133.
33. Meyer, O. 2004. Making pregnancy safer for patients with lupus. Joint Bone Spine 71:178-182. (Pubitemid 38739126)
34. Moormann, A. M., et al. 1999. Malaria and pregnancy: placental cytokine expression and its relationship to intrauterine growth retardation. J. Infect. Dis. 180:1987-1993.
35. Mott, K. E. 1996. Global health statistics. A compendium of incidence, prevalence and mortality estimates for over 200 conditions, vol. 11. World Health Organization, Boston, MA.
36. Mwatha, J. K., et al. 1998. High levels of TNF, soluble TNF receptors, soluble ICAM-1, and IFN-gamma, but low levels of IL-5, are associated with hepatosplenic disease in human schistosomiasis mansoni. J. Immunol. 160: 1992-1999. (Pubitemid 28106490)
37. Ndibazza, J., et al. 2010. Effects of deworming during pregnancy on maternal and perinatal outcomes in Entebbe, Uganda: a randomized controlled trial. Clin. Infect. Dis. 50:531-540.
38. Novato-Silva, E., G. Gazzinelli, and D. G. Colley. 1992. Immune responses during human schistosomiasis mansoni. XVIII. Immunologic status of pregnant women and their neonates. Scand. J. Immunol. 35:429-437.
39. Okoko, B. J., et al. 2002. Influence of placental malaria infection on foetal outcome in the Gambia: twenty years after Ian McGregor. J. Health Popul. Nutr. 20:4-11.
40. Othoro, C., et al. 2006. Evaluation of various methods of maternal placental blood collection for immunology studies. Clin. Vaccine Immunol. 13:568-574.
41. Qunhua, L., et al. 2000. Investigation of association between female genital tract diseases and Schistosomiasis japonica infection. Acta Trop. 77:179-183.
42. Redline, R. W. 2006. Inflammatory responses in the placenta and umbilical cord. Semin. Fetal Neonatal Med. 11:296-301.
43. Redline, R. W., et al. 2003. Amniotic infection syndrome: nosology and reproducibility of placental reaction patterns. Pediatr. Dev. Pathol. 6:435-448.
44. Renaud, R., P. Brettes, C. Castanier, and R. Loubiere. 1972. Placental bilharziasis. Int. J. Gynaecol. Obstet. 10:24-30.
45. Rogerson, S. J., et al. 2003. Placental tumor necrosis factor alpha but not gamma interferon is associated with placental malaria and low birth weight in Malawian women. Infect. Immun. 71:267-270.
46. Romia, S. A., A. E. Handoussa, S. A. Youseff, and M. M. el Zayat. 1992. Transplacental transfer of schistosomal antigens and antibodies. J. Egypt Soc. Parasitol. 22:575-582.
47. Siegrist, D., and P. Siegrist-Obimpeh. 1992. Schistosoma haematobium infection in pregnancy. Acta Trop. 50:317-321.
48. Steketee, R. W., et al. 1996. The effect of malaria and malaria prevention in pregnancy on offspring birthweight, prematurity, and intrauterine growth retardation in rural Malawi. Am. J. Trop. Med. Hyg. 55:33-41.
49. Tachon, P., and R. Borojevic. 1978. Mother-child relation in human schistosomiasis mansoni: skin test and cord blood reactivity to schistosomal antigens. Trans. R. Soc. Trop. Med. Hyg. 72:605-609.
50. Vassiliadis, S., D. Tsoukatos, and I. Athanassakis. 1994. Interferon-induced class II expression at the spongiotrophoblastic zone of the murine placenta is linked to fetal rejection and developmental abnormalities. Acta Physiol. Scand. 151:485-495.
51. Vince, G. S., P. M. Starkey, R. Austgulen, D. Kwiatkowski, and C. W. Redman. 1995. Interleukin-6, tumour necrosis factor and soluble tumour necrosis factor receptors in women with pre-eclampsia. Br. J. Obstet. Gynaecol. 102:20-25.
52. Wang, X., N. Athayde, and B. Trudinger. 2003. A proinflammatory cytokine response is present in the fetal placental vasculature in placental insufficiency. Am. J. Obstet. Gynecol. 189:1445-1451.
53. Wang, Y., and S. W. Walsh. 1996. TNF alpha concentrations and mRNA expression are increased in preeclamptic placentas. J. Reprod. Immunol. 32:157-169.
54. WHO. 1987. Prevention and control of intestinal parasitic infections. Report of a WHO expert committee. World Health Organ. Tech. Rep. Ser. 749:1-86.
55. Wolfberg, A. J., A. Lee-Parritz, A. J. Peller, and E. S. Lieberman. 2004. Association of rheumatologic disease with preeclampsia. Obstet. Gynecol. 103:1190-1193.
56. Zhang, J. M., F. T. Kraus, and T. I. Aquino. 1985. Chorioamnionitis: a comparative histologic, bacteriologic, and clinical study. Int. J. Gynecol Pathol. 4:1-10.
57. Zwingenberger, K., E. Irschick, J. G. Vergetti Siqueira, A. R. Correia Dacal, and H. Feldmeier. 1990. Tumour necrosis factor in hepatosplenic schistosomiasis. Scand. J. Immunol. 31:205-211.