• 1.

    Duffy P, Fried M, 2005. Malaria in the pregnant woman. Curr Top Microbiol Immunol 295: 169200.

  • 2.

    Falade C, Tongo O, Ogunkunle O, Orimadegun A, 2010. Effects of malaria in pregnancy on newborn anthropometry. J Infect Dev Ctries 4: 448453.

  • 3.

    Nosten F, McGready R, Simpson J, Thwai K, Balkan S, Cho T, Hkirijaroen L, Looareesuwan S, White N, 1999. Effects of Plasmodium vivax malaria in pregnancy. Lancet 354: 546549.

    • Search Google Scholar
    • Export Citation
  • 4.

    Beeson J, Rogerson S, Cooke B, Reeder J, Chai W, Lawson A, Molyneux M, Brown G, 2000. Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria. Nat Med 6: 8689.

    • Search Google Scholar
    • Export Citation
  • 5.

    Beeson J, Rogerson S, Elliott S, Duffy M, 2005. Targets of protective antibodies to malaria during dregnancy. JID 192: 16471660.

  • 6.

    Okoko BJ, Enwere G, Ota MO, 2003. The epidemiology and consequences of maternal malaria: a review of immunological basis. Acta Trop 87: 193205.

    • Search Google Scholar
    • Export Citation
  • 7.

    Rogerson S, Hviid L, Duffy P, Leke R, Taylor D, 2007. Malaria in pregnancy: pathogenesis and immunity. Lancet 7: 105117.

  • 8.

    Rogerson S, Mwapasa V, Meshnick S, 2007. Malaria in pregnancy: linking immunity and pathogenesis to prevention. Am J Trop Med Hyg 77: 1422.

  • 9.

    Castejón O, Molinaro M, de Zamora G, 2001. The hairiness placental in the event of infected primigesta for Plasmodium vivax and tried with cloroquine. Gac Med Caracas 109: 345351.

    • Search Google Scholar
    • Export Citation
  • 10.

    Davison B, Cogswell F, Baskin G, Falkenstein K, Henson E, Tarantal A, Krogstad D, 1998. Plasmodium coatneyi in the rhesus monkey (Macaca mulata) as a model of malaria in pregnancy. Am J Trop Med Hyg 59: 189201.

    • Search Google Scholar
    • Export Citation
  • 11.

    Ismail M, Ordi J, Menendez C, Ventura PA, Kahigwa E, Hirt R, Cardesa A, Alonso PL, 2000. Placental pathology in malaria: an histological, immunohistochemical and quantitative study. Hum Pathol 31: 8593.

    • Search Google Scholar
    • Export Citation
  • 12.

    Singh N, Shukla M, Sharma V, 1999. Epidemiology of malaria in pregnancy in central India. Bull World Health Organ 77: 567572.

  • 13.

    Khunrae P, Higgins M, 2010. Structural insights into chondroitin sulfate binding in pregnancy-associated malaria. Biochem Soc Trans 38: 13371341.

    • Search Google Scholar
    • Export Citation
  • 14.

    Fried M, Hixson K, Anderson L, Ogata Y, Mutabingwa T, Duffy P, 2007. The distinct proteome of placental malaria parasites. Mol Biochem Parasitol 155: 5765.

    • Search Google Scholar
    • Export Citation
  • 15.

    Flick K, Scholander C, Chen Q, Fernandez V, Pouvelle B, Gysin J, Wahlgren M, 2001. Role of nonimmune IgG bound to PfEMP1 in placental malaria. Science 293: 20982100.

    • Search Google Scholar
    • Export Citation
  • 16.

    Rasti N, Namusoke F, Chêne A, Chen Q, Staalsoe T, Klinkert MQ, Mirembe F, Kironde F, Wahlgren M, 2006. Nonimmune immunoglobulin binding and multiple adhesion characterize Plasmodium falciparum-infected erythrocytes of placental origin. Proc Natl Acad Sci USA 103: 1379513800.

    • Search Google Scholar
    • Export Citation
  • 17.

    Carvalho B, Lopes S, Nogueira P, Orlandi P, Bargieri D, Blanco Y, Mamoni R, Leite J, Rodrigues M, Soares I, Oliveira T, Wunderlich G, Lacerda M, del Portillo H, Araújo M, Russell B, Suwanarusk R, Snounou G, Rénia L, Costa F, 2010. On the cytoadhesion of Plasmodium vivax-infected erythrocytes. J Infect Dis 202: 638647.

    • Search Google Scholar
    • Export Citation
  • 18.

    Galbraith R, Fox H, Hsi B, Galbraith G, Bray R, Faulk W, 1980. The human materno-foetal relationship in malaria: II. Histological, ultras structural and inmunopatological studies of the placenta. Trans R Soc Trop Med Hyg 74: 6171.

    • Search Google Scholar
    • Export Citation
  • 19.

    Philippe E, Walter P, 1985. Placental lesions in malaria. Arch Fr Pediatr 42: 921923.

  • 20.

    Walter P, Garin Y, Blot P, 1982. Placental pathologic changes in malaria. A histologic and ultrastructural study. Am J Pathol 109: 330342.

  • 21.

    Bulmer JN, Rasheed FN, Francis N, Morrison L, Greenwoods BM, 1993. Placental malaria. I. Pathological classification. Histopathology 22: 211218.

  • 22.

    Bulmer JN, Rasheed FN, Morrison L, Francis N, Greenwood BM, 1993. Placental malaria. II. A semi-quantitative investigation of the pathological features. Histopathology 22: 219225.

    • Search Google Scholar
    • Export Citation
  • 23.

    Leopardi O, Naughten W, Salvia L, Colecchia M, Matteelli A, Zucchi A, Shein A, Muchi J, Carosi G, Ghione M, 1996. Malaric placentas. A quantitative study and clinico-pathological correlations. Pathol Res Pract 192: 892898.

    • Search Google Scholar
    • Export Citation
  • 24.

    McGready R, Davison B, Stepniewska K, Cho T, Shee H, Brockman A, Udomsangpetch R, Looareesuwan S, White N, Meshnick S, Nosten F, 2004. The effects of Plasmodium falciparum and P. vivax infections on placental histopathology in an area of low malaria transmission. Am J Trop Med Hyg 70: 398407.

    • Search Google Scholar
    • Export Citation
  • 25.

    Muehlenbachs A, Fried M, McGready R, Harrington W, Mutabingwa T, Nosten F, Duffy P, 2010. A novel histological grading scheme for placental malaria applied in areas of high and low malaria transmission. J Infect Dis 202: 16061616.

    • Search Google Scholar
    • Export Citation
  • 26.

    Rogerson S, Mkundika P, Kanjala M, 2003. Diagnosis of Plasmodium falciparum malaria at delivery: comparison of blood film preparation methods and of blood films with histology. J Clin Microbiol 41: 13701374.

    • Search Google Scholar
    • Export Citation
  • 27.

    Watkinson M, Rushton D, 1983. Plasmodial pigmentation of placenta and outcome of pregnancy in west African mothers. BMJ 287: 251254.

  • 28.

    Boström S, Ibitokou S, Oesterholt M, Schmiegelow C, Persson JO, Minja D, Lusingu J, Lemnge M, Fievet N, Deloron P, Luty AJ, Troye-Blomberg M, 2012. Biomarkers of Plasmodium falciparum infection during pregnancy in women living in northeastern Tanzania. PLoS ONE 7: e48763.

    • Search Google Scholar
    • Export Citation
  • 29.

    Campos I, Uribe M, Cuesta C, Franco-Gallego A, Carmona-Fonseca J, Maestre A, 2011. Diagnosis of gestational, congenital, and placental malaria in Colombia: comparison of the efficacy of microscopy, nested polymerase chain reaction, and histopathology. Am J Trop Med Hyg 84: 929935.

    • Search Google Scholar
    • Export Citation
  • 30.

    Carmona-Fonseca J, Maestre A, 2009. Incidence of gestational, congenital and placental malaria in Urabá (Antioquia, Colombia), 2005–2007. Rev Colomb Obstet Ginecol 60: 1226.

    • Search Google Scholar
    • Export Citation
  • 31.

    Almeida L, Barbosa M, Martinez-Espinosa F, 2010. Malaria among women aged 10 to 49 years, according to SIVEP-Malaria, Manaus, State of Amazonas, 2003–2006. Rev Soc Bras Med Trop 43: 304308.

    • Search Google Scholar
    • Export Citation
  • 32.

    Chagas E, do Nascimento C, de Santana Filho F, Bôtto-Menezes C, Martinez-Espinosa F, 2009. Impact of malaria during pregnancy in the Amazon region. Rev Panam Salud Publica 26: 203208.

    • Search Google Scholar
    • Export Citation
  • 33.

    Martínez-Espinosa F, Daniel-Ribeiro C, Alecrim W, 2004. Malaria during pregnancy in a reference centre from the Brazilian Amazon: unexpected increase in the frequency of Plasmodium falciparum infections. Mem Inst Oswaldo Cruz 99: 921.

    • Search Google Scholar
    • Export Citation
  • 34.

    Gómez E, López E, Ache A, 2009. Malaria and pregnancy. San Isidro Parish, Municipality Sifontes, state of Bolívar, Venezuela, 2005–2006 [in Spanish]. Invest Clin 50: 455464.

    • Search Google Scholar
    • Export Citation
  • 35.

    Rodriguez-Morales A, Sanchez E, Vargas M, Piccolo C, Colina R, Arria M, Franco-Paredes C, 2006. Pregnancy outcomes associated with Plasmodium vivax malaria in northeastern Venezuela. Am J Trop Med Hyg 75: 755757.

    • Search Google Scholar
    • Export Citation
  • 36.

    Parekh F, Davison B, Gamboa D, Hernandez J, Branch O, 2010. Placental histopathologic changes associated with subclinical malaria infection and its impact on the fetal environment. Am J Trop Med Hyg 83: 973980.

    • Search Google Scholar
    • Export Citation
  • 37.

    Parekh F, Hernandez J, Krogstad D, Casapia W, Branch O, 2007. Prevalence and risk of Plasmodium falciparum and P. vivax malaria among pregnant women living in the hypoendemic communities of the Peruvian Amazon. Am J Trop Med Hyg 77: 451457.

    • Search Google Scholar
    • Export Citation
  • 38.

    Espinoza E, Hidalgo L, Chedraui P, 2005. The effect of malarial infection on maternal-fetal outcome in Ecuador. J Matern Fetal Neonatal Med 18: 101105.

    • Search Google Scholar
    • Export Citation
  • 39.

    Carles G, Bousquet F, Raynal P, Peneau C, Mignot V, Arbeille P, 1998. Pregnancy and malaria. Study of 143 cases in French Guiana [in French]. J Gynecol Obstet Biol Reprod (Paris) 27: 798805.

    • Search Google Scholar
    • Export Citation
  • 40.

    Carmona-Fonseca J, 2003. Malaria in the Colombian regions of Uraba and Bajo cauca, province of Antioquia: an overwiew to interpret the antimalarial therapeutic failure. Part 1. Iatreia 16: 299318.

    • Search Google Scholar
    • Export Citation
  • 41.

    Carmona-Fonseca J, 2004. Malaria in the Colombian regions of Uraba and Bajo cauca, province of Antioquia: an overwiew to interpret the antimalarial therapeutic failure. Part 2. Iatreia 17: 3453.

    • Search Google Scholar
    • Export Citation
  • 42.

    Carmona-Fonseca J, Arias M, Correa A, Lemos M, 2011. Gestational malaria and living conditions in Turbo, Colombia. Social Medicine 6: 7382.

  • 43.

    Carmona-Fonseca J, 2011. Food and nutritional status among children of endemic malaria zones of Antioquia (Colombia). MedUNAB 14: 94102.

    • Search Google Scholar
    • Export Citation
  • 44.

    Galbraith R, Faulk W, Galbraith G, Holbrook T, Bray R, 19800. The human materno-foetal relationship in malaria: I. Identification of pigment and parasites in placenta. Trans R Soc Trop Med Hyg 74: 5260.

    • Search Google Scholar
    • Export Citation
  • 45.

    Ordi J, Ismail M, Ventura P, Kahigwa E, Hirt R, Cardesa A, Alonso P, Menendez C, 1998. Massive chronic intervillositis of the placenta associated with malaria infection. Am J Surg Pathol Res Pract 22: 10061011.

    • Search Google Scholar
    • Export Citation
  • 46.

    Abrams E, Brown H, Chensue S, Turner G, Tadesse E, Lema V, Molyneux M, Rochford R, Meshnick S, Rogerson S, 2003. Host response to malaria during pregnancy: placental monocyte recruitment is associated with elevated beta chemokine expression. J Immunol 170: 27592764.

    • Search Google Scholar
    • Export Citation
  • 47.

    Ordi J, Menendez C, Ismail M, Ventura P, Palacín A, Kahigwa E, Ferrer B, Cardesa A, Alonso P, 2001. Placental malaria is associated with cell-mediated inflammatory responses with selective absence of natural killer cells. J Infect Dis 183: 11001107.

    • Search Google Scholar
    • Export Citation
  • 48.

    Carmona-Fonseca J, Arango E, 2012. Mixed malaria: prevalence in Colombia and Latin America. Iatreia 25: 334346.

  • 49.

    Silvera A, Manjarrez C, Peñuela M, Villalba D, Correa E, Díaz V, Salazar S, 2005. Anatomic and histopathological characterization of the placenta and clinical correlation in the hypertensive disease in patients of Barranquilla (Colombia). Salud Uninorte. Barranquilla (Col) 21: 4154.

    • Search Google Scholar
    • Export Citation
  • 50.

    Pathak S, Lees CC, Hackett G, Jessop F, Sebire NJ, 2011. Frequency and clinical significance of placental histological lesions in an unselected population at or near term. Virchows Arch 459: 565572.

    • Search Google Scholar
    • Export Citation
  • 51.

    Diouf I, Fievet N, Doucouré S, Ngom M, Andrieu M, Mathieu J, Gaye A, Thiaw O, Deloron P, 2007. IL-12 producing monocytes and IFN-gamma and TNF-alpha producing T-lymphocytes are increased in placentas infected by Plasmodium falciparum. J Reprod Immunol 74: 152162.

    • Search Google Scholar
    • Export Citation
  • 52.

    Diouf I, Fievet N, Doucouré S, Ngom M, Gaye A, Dumont A, Ndao C, Le Hesran J, Chaouat G, Deloron P, 2004. Monocyte activation and T cell inhibition in Plasmodium falciparum-infected placenta. J Infect Dis 189: 22352242.

    • Search Google Scholar
    • Export Citation
  • 53.

    Ordi J, Bardaj A, Castillo P, Ismail M, Menéndez C, 2011. Grading schemes for placental malaria. J Infect Dis 203: 16941695.

  • 54.

    Blair S, Carmona-Fonseca J, Piñeros J, Ríos A, Álvarez T, Álvarez G, Tobón A, 2006. Therapeutic efficacy test for falciparum malaria in Antioquia, Colombia. Malar J 5: 14.

    • Search Google Scholar
    • Export Citation
  • 55.

    Carmona-Fonseca J, Álvarez G, Blair S, 2006. Plasmodium vivax malaria: treatment of primary attacks with primaquine, in three different doses, and a fixed dose of chloroquine, Antioquia, Colombia, 2003–2004. Biomedica 26: 353365.

    • Search Google Scholar
    • Export Citation
  • 56.

    McGready R, Brockman A, Cho T, Levesque M, Tkachuk A, Meshnick S, Nosten F, 2002. Haemozoin as a marker of placental parasitization. Trans R Soc Trop Med Hyg 96: 644646.

    • Search Google Scholar
    • Export Citation
  • 57.

    Arango E, Maestre A, Carmona-Fonseca J, 2010. Effect of submicroscopic or polyclonal Plasmodium falciparum infection on mother and gestation product. Systematic review. Rev Bras Epidemiol 13: 373386.

    • Search Google Scholar
    • Export Citation
  • 58.

    Avery J, Smith G, Owino S, Sarr D, Nagy T, Mwalimu S, Matthias J, Kelly L, Poovassery J, Middii J, Abramowsky C, Moore J, 2012. Maternal malaria induces a procoagulant and antifibrinolytic state that is embryotoxic but responsive to anticoagulant therapy. PLoS ONE 7: e31090.

    • Search Google Scholar
    • Export Citation
  • 59.

    Conroy A, Liles W, Molyneux M, Rogerson S, Kain K, 2011. Performance characteristics of combinations of host biomarkers to identify women with occult placental malaria: a case-control study from Malawi. PLoS ONE 6: e28540.

    • Search Google Scholar
    • Export Citation
 
 
 

 

 
 
 

 

 

 

 

 

 

Placental Malaria in Colombia: Histopathologic Findings in Plasmodium vivax and P. falciparum Infections

View More View Less
  • Grupo Salud y Comunidad-César Uribe Piedrahíta, Universidad de Antioquia, Medellín, Colombia

Studies on gestational malaria and placental malaria have been scarce in malaria-endemic areas of the Western Hemisphere. To describe the histopathology of placental malaria in Colombia, a longitudinal descriptive study was conducted. In this study, 179 placentas were studied by histologic analysis (112 with gestational malaria and 67 negative for malaria). Placental malaria was confirmed in 22.35%, 50.0% had previous infections, and 47.5% had acute infections. Typical malaria-associated changes were observed in 37%. The most common changes were villitis, intervillitis, deciduitis, increased fibrin deposition, increased syncytial knots, mononuclear (monocytes/macrophages and lymphocytes), polymorphonuclear cell infiltration, and trophozoites in fetal erythrocytes. No association was found between type of placental changes observed and histopathologic classification of placental malaria. The findings are consistent with those reported for placental malaria in other regions. Plasmodium vivax was the main parasite responsible for placental and gestational malaria, but its role in the pathogenesis of placental malaria was not conclusive.

Author Notes

* Address correspondence to Amanda Maestre, Grupo Salud y Comunidad, Universidad de Antioquia, Carrera 51D, No. 62–29, Medellín, Colombia. E-mail: aemaestre@gmail.com

Financial support: This study was supported by Instituto Colombiano para el Desarollo de la Ciencia y la Tecnologia (code 11150417041, contract RC-316-2004; code 111540820495, contract RC 238-2007 and code 111549326134 contract RC-611-2009); Dirección Seccional de Salud de Antioquia; CODI-Estrategia de Sostenibilidad 2013-2014; CODI-REGIONALIZACION code 2557; and Universidad de Antioquia Colombia.

Authors' addresses: Jaime Carmona-Fonseca, Eliana Arango, and Amanda Maestre, Grupo Salud y Comunidad, Universidad de Antioquia, Carrera 51D, No. 62–29, Medellín, Colombia, E-mails: jaimecarmonaf@hotmail.com, amarango@gmail.com, and aemaestre@gmail.com.

Save