- ABSTRACT.
- INTRODUCTION
- METHODS
- Study site.
- Study design and sample selection.
- Inclusion and exclusion criteria.
- Data and specimen collection.
- Diagnosis of infection by Plasmodium.
- Expression analysis of immune mediators in placental tissue.
- Quantification of IgG against tetanus toxoid.
- ELISA for measuring rotavirus specific IgG in serum.
- Histologic study of the placental tissue.
- Statistical analysis.
- Ethics.
- RESULTS
- General characteristics of pregnant women and newborns.
- Anti-TT and anti-RV IgG levels in peripheral maternal and umbilical cord blood.
- Effect of malaria in pregnancy on the expression of immune mediators in placental tissue.
- Placental histological findings.
- Significant correlations between anti-RV and anti-TT IgG in umbilical cord with anti-RV and anti-TT IgG in maternal blood and placental histological findings.
- Significant correlations between CMR of anti-RV and CMR of anti-TT in umbilical cord with the expression of immune mediators and placental histological findings.
- DISCUSSION
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Swamy GK , Garcia-Putnam R , 2013. Vaccine-preventable diseases in pregnancy. Am J Perinatol 30: 89–97.
-
2.
van den Berg JP , Westerbeek EA , van der Klis FR , Berbers GA , van Elburg RM , 2011. Transplacental transport of IgG antibodies to preterm infants: a review of the literature. Early Hum Dev 87: 67–72.
-
3.
Basha S , Surendran N , Pichichero M , 2014. Immune responses in neonates. Expert Rev Clin Immunol 10: 1171–1184.
-
4.
Faucette AN , Pawlitz MD , Pei B , Yao F , Chen K , 2015. Immunization of pregnant women: Future of early infant protection. Hum Vaccin Immunother 11: 2549–2555.
-
5.
Aboud S , Matre R , Lyamuya EF , Kristoffersen EK , 2001. Antibodies to tetanus toxoid in women of childbearing age in Dar es Salaam and Bagamoyo, Tanzania. Trop Med Int Health 6: 119–125.
-
6.
Schofield FD , Tucker VM , Westbrook GR , 1961. Neonatal tetanus in New Guinea. Effect of active immunization in pregnancy. BMJ 2: 785–789.
-
7.
Lanata CF , Fischer-Walker CL , Olascoaga AC , Torres CX , Aryee MJ , Black RE , 2013. Global causes of diarrheal disease mortality in children <5 years of age: a systematic review. PLoS One 8: e72788.
-
8.
Bryce J , Boschi-Pinto C , Shibuya K , Black RE , Group WCHER , 2005. WHO estimates of the causes of death in children. Lancet 365: 1147–1152.
-
9.
Linhares AC et al., 2011. Burden and typing of rotavirus group A in Latin America and the Caribbean: systematic review and meta-analysis. Rev Med Virol 21: 89–109.
-
10.
Mwila K , Chilengi R , Simuyandi M , Permar SR , Becker-Dreps S , 2017. Contribution of maternal immunity to decreased rotavirus vaccine performance in low–and middle-income countries. Clin Vaccine Immunol 24: e00405–e00416.
-
11.
Appaiahgari MB , Glass R , Singh S , Taneja S , Rongsen-Chandola T , Bhandari N , Mishra S , Vrati S , 2014. Transplacental rotavirus IgG interferes with immune response to live oral rotavirus vaccine ORV-116E in Indian infants. Vaccine 32: 651–656.
-
12.
Scott S , 2005. Neonatal measles immunity in rural Kenya: the influence of HIV and placental malaria infections on placental transfer of antibodies and levels of antibody in maternal and cord serum samples. J Infect Dis 191: 1854–1860.
-
13.
Jauniaux E , Jurkovic D , Gulbis B , Liesnard C , Lees C , Campbell S , 1995. Materno-fetal immunoglobulin transfer and passive immunity during the first trimester of human pregnancy. Hum Reprod 10: 3297–3300.
-
14.
Malek A , Sager R , Kuhn P , Nicolaides KH , Schneider H , 1996. Evolution of maternofetal transport of immunoglobulins during human pregnancy. Am J Reprod Immunol 36: 248–255.
-
15.
Okoko BJ , Wesumperuma LH , Ota MO , Pinder M , Banya W , Gomez SF , McAdam KP , Hartet AC , 2001. The influence of placental malaria infection and maternal hypergammaglobulinemia on transplacental transfer of antibodies and IgG subclasses in a rural West African population. J Infect Dis 184: 627–632.
-
16.
Okoko BJ , Wesuperuma LH , Ota MO , Banya WA , Pinder M , Gomez FS , Osinusi K , Hart AC , 2001. Influence of placental malaria infection and maternal hypergammaglobulinaemia on materno-foetal transfer of measles and tetanus antibodies in a rural west African population. J Health Popul Nutr 19: 59–65.
-
17.
Cavalcante RS , Kopelman BI , Costa-Carvalho BT , 2008. Placental transfer of Haemophilus influenzae type b antibodies in malnourished pregnant women. Braz J Infect Dis 12: 47–51.
-
18.
de Souza EG , Hara CC , Fagundes DL , de Queiroz AA , Morceli G , Calderon IM , França EL , Honorio-França AC , 2016. Maternal-foetal diabetes modifies neonatal fc receptor expression on human leucocytes. Scand J Immunol 84: 237–244.
-
19.
Atwell JE et al., 2016. Impact of placental malaria and hypergammaglobulinemia on transplacental transfer of respiratory syncytial virus antibody in Papua New Guinea. J Infect Dis 213: 423–431.
-
20.
Brair ME , Brabin BJ , Milligan P , Maxwell S , Hart CA , 1994. Reduced transfer of tetanus antibodies with placental malaria. Lancet 343: 208–209.
-
21.
Cumberland P , Shulman CE , Maple PA , Bulmer JN , Dorman EK , Kawuondo K , Marsh K , Cutts FT , 2007. Maternal HIV infection and placental malaria reduce transplacental antibody transfer and tetanus antibody levels in newborns in Kenya. J Infect Dis 196: 550–557.
-
22.
de Moraes-Pinto MI , Verhoeff F , Chimsuku L , Milligan PJ , Wesumperuma L , Broadhead RL , Brabin BJ , Johnson PM , Hart CA , 1998. Placental antibody transfer: influence of maternal HIV infection and placental malaria. Arch Dis Child Fetal Neonatal 79: 202–205.
-
23.
Fu C , Lu L , Wu H , Shaman J , Cao Y , Fang F , Yang Q , He Q , Yang Z , Wang M , 2016. Placental antibody transfer efficiency and maternal levels: specific for measles, coxsackievirus A16, enterovirus 71, poliomyelitis I-III and HIV-1 antibodies. Sci Rep 6: 38874.
-
24.
Khan WA et al., 2014. Asymptomatic Plasmodium falciparum malaria in pregnant women in the Chittagong Hill Districts of Bangladesh. PLoS One 9: e98442.
-
25.
Arango EM , Samuel R , Agudelo OM , Carmona-Fonseca J , Maestre A , Yanow SK , 2013. Molecular detection of malaria at delivery reveals a high frequency of submicroscopic infections and associated placental damage in pregnant women from northwest Colombia. Am J Trop Med Hyg 89: 178–183.
-
26.
Agudelo OM , Aristizabal BH , Yanow SK , Arango E , Carmona-Fonseca J , Maestre A , 2014. Submicroscopic infection of placenta by Plasmodium produces Th1/Th2 cytokine imbalance, inflammation and hypoxia in women from north-west Colombia. Malar J 13: 122.
-
27.
Ibitokou SA et al., 2014. Submicroscopic infections with Plasmodium falciparum during pregnancy and their association with circulating cytokine, chemokine, and cellular profiles. Clin Vaccine Immunol 21: 859–866.
-
28.
Carmona-Fonseca J , Arango E , Maestre A , 2013. Placental malaria in Colombia: histopathologic findings in Plasmodium vivax and P. falciparum infections. Am J Trop Med Hyg 88: 1093–1101.
-
29.
Muehlenbachs A , Fried M , McGready R , Harrington WE , Mutabingwa TK , Nosten F , Duffy PE , 2010. A novel histological grading scheme for placental malaria applied in areas of high and low malaria transmission. J Infect Dis 202: 1608–1616.
-
30.
Carmona-Fonseca J , Maestre A , 2009. Incidencia de la malaria gestacional, congénita y placentaria en Urabá (Antioquia, Colombia), 2005–2007. Rev Colomb Obstet Ginecol 60: 15.
-
31.
Agudelo OM , Arango EM , Maestre A , Carmona-Fonseca J , 2013. Prevalence of gestational, placental and congenital malaria in north-west Colombia. Malar J 12: 341.
-
32.
Plowe CV , Djimde A , Bouare M , Doumbo O , Wellems TE , 1995. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg 52: 565–568.
-
33.
Shokoples SE , Ndao M , Kowalewska-Grochowska K , Yanow SK , 2009. Multiplexed real-time PCR assay for discrimination of Plasmodium species with improved sensitivity for mixed infections. J Clin Microbiol 47: 975–980.
-
34.
Pfaffl MW , 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
-
35.
Rojas OL , Narváez CF , Greenberg HB , Angel J , Franco MA , 2008. Characterization of rotavirus specific B cells and their relation with serological memory. Virology 380: 234–242.
-
36.
Gnidehou S , Doritchamou J , Arango EM , Cabrera A , Arroyo MI , Kain KC , Ndam NT , Maestre A , Yanow SK , 2014. Functional antibodies against VAR2CSA in nonpregnant populations from colombia exposed to Plasmodium falciparum and Plasmodium vivax. Infect Immun 82: 2565–2573.
-
37.
Thomann M , Schlothauer T , Dashivets T , Malik S , Avenal C , Bulau P , Rüger P , Reusch D , 2015. In vitro glycoengineering of IgG1 and its effect on Fc receptor binding and ADCC activity. PLoS One 10: e0134949.
-
38.
Bondt A , Rombouts Y , Selman MH , Hensbergen PJ , Reiding KR , Hazes JM , Dolhain RJ , Wuhrer M , 2014. Immunoglobulin G (IgG) Fab glycosylation analysis using a new mass spectrometric high-throughput profiling method reveals pregnancy-associated changes. Mol Cell Proteomics 11: 3029–3039.
-
39.
Huhn C , Selman MH , Ruhaak LR , Deelder AM , Wuhrer M , 2009. IgG glycosylation analysis. Proteomics 9: 882–913.
-
40.
Liu X , Ye L , Bai Y , Mojidi H , Simister NE , Zhu X , 2008. Activation of the JAK/STAT-1 signaling pathway by IFN-gamma can down-regulate functional expression of the MHC class I-related neonatal Fc receptor for IgG. J Immunol 181: 449–463.
-
41.
Goyal JP , Makwana AM , 2014. Comparison of clinical profile between P. vivax and P. falciparum malaria in children: a tertiary care centre perspective from India. Malar Res Treat 2014: 132672.
-
42.
Karunaweera ND , Wijesekera SK , Wanasekera D , Mendis KN , Carter R , 2003. The paroxysm of Plasmodium vivax malaria. Trends Parasitol 19: 188–193.
-
43.
King T , Lamb T , 2015. Interferon-γ: the Jekyll and Hyde of malaria. PLoS Pathog 11: e1005118.
-
44.
Rudin W , Favre N , Bordmann G , Ryffel B , 1997. Interferon-γ is essential for the development of cerebral malaria. Eur J Immunol 27: 810–815.
-
45.
Agudelo García OM. Malaria placentaria submicroscópica por Plasmodium vivax o Plasmodium falciparum: histopatología, células inmunitarias y expresión de genes asociados a hipoxia, apoptosis e inflamación. Medellín, Colombia: Universidad de Antioquia; 2018.
-
46.
López-Guzman C , Carmona-Fonseca J , 2020. Malaria placentaria submicroscópica: histopatología y expresión de mediadores de procesos fisiológicos. Rev Peru Med Exp Salud Publica 37: 220.
-
47.
Abu-Raya B , Smolen KK , Willems F , Kollmann TR , Marchant A , 2016. Transfer of maternal antimicrobial immunity to HIV-exposed uninfected newborns. Front Immunol 7: 338.
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Effect of Plasmodium Infection during Pregnancy on Passive Neonatal Immunity against Tetanus Toxoid and Rotavirus
Catalina Álvarez-Larrotta
Catalina Álvarez-Larrotta
Grupo Salud y Comunidad, Facultad de Medicina, Universidad de Antioquia, Medellín, Colombia,
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Olga M. Agudelo
Olga M. Agudelo
Grupo Salud y Comunidad, Facultad de Medicina, Universidad de Antioquia, Medellín, Colombia,
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Kenneth Gavina
Kenneth Gavina
Department of Medical Microbiology and Immunology, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada;
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Stephanie K. Yanow
Stephanie K. Yanow
Department of Medical Microbiology and Immunology, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada;
School of Public Health, University of Alberta, Edmonton, Canada
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School of Public Health, University of Alberta, Edmonton, Canada
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Jaime Carmona-Fonseca
Jaime Carmona-Fonseca
Grupo Salud y Comunidad, Facultad de Medicina, Universidad de Antioquia, Medellín, Colombia,
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E. Arango
E. Arango
Grupo Salud y Comunidad, Facultad de Medicina, Universidad de Antioquia, Medellín, Colombia,
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ABSTRACT.
Passive immunity acquired through transplacental IgG transport is essential to protect infants against pathogens as childhood vaccination programs begins. Diarrhea caused by rotavirus and neonatal tetanus are common and potentially fatal childhood infections that can be prevented by transplacental IgG. However, it is not known whether maternal infections in pregnancy can reduce the transfer of these antibodies to the fetus. This study evaluated the effect of submicroscopic Plasmodium infection during pregnancy on the transfer of maternal IgG antibodies against rotavirus (anti-RV) and tetanus toxoid (anti-TT) to newborns of pregnant women residing in Puerto Libertador and Tierralta, Colombia. Expression of different immune mediators and levels of IgG against rotavirus and tetanus toxoid were quantified in pregnant women with and without Plasmodium infection during pregnancy. Submicroscopic infection at the time of delivery was associated with a cord-to-maternal ratio (CMR) > 1 for anti-RV and < 1 for anti-TT IgG, as well as with an increase in the expression of immune mediators of inflammation (IFN-γ), anti-inflammation (IL-10, TGF-β), and regulation (FoxP3, CTLA-4). When compared by species, these findings (CMR > 1 for anti-RV and < 1 for anti-TT IgG) were conserved in submicroscopic Plasmodium vivax infections at delivery. The impact of Plasmodium infections on neonatal susceptibility to other infections warrants further exploration.
Author Notes
Financial support: This work was supported by the Departamento Administrativo de Ciencia, Tecnología e Inovación Colciencias (Project Code 111574454975).
Authors’ addresses: Catalina Alvarez-Larrotta, Jaime Carmona-Fonseca, Olga M. Agudelo-García and Eliana M. Arango, Grupo Salud y Comunidad-César Uribe Piedrahíta, Facultad de Medicina, Universidad de Antioquia, Medellín, Colombia, E-mail: catalinaalvarezl95@gmail.com, jaimecarmonaf@hotmail.com, momag204@gmail.com and emarango@gmail.com. Kenneth Gavina, Department of Medical Microbiology and Immunology, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada, E-mail: gavinakc@gmail.com. Stephanie Yanow, School of Public Health, University of Alberta, Edmonton, Canada, Department of Medical Microbiology and Immunology, Faculty of Medicine and Dentistry, University of Alberta, Edmonton, Canada E-mail: yanow@ualberta.ca.
- ABSTRACT.
- INTRODUCTION
- METHODS
- Study site.
- Study design and sample selection.
- Inclusion and exclusion criteria.
- Data and specimen collection.
- Diagnosis of infection by Plasmodium.
- Expression analysis of immune mediators in placental tissue.
- Quantification of IgG against tetanus toxoid.
- ELISA for measuring rotavirus specific IgG in serum.
- Histologic study of the placental tissue.
- Statistical analysis.
- Ethics.
- RESULTS
- General characteristics of pregnant women and newborns.
- Anti-TT and anti-RV IgG levels in peripheral maternal and umbilical cord blood.
- Effect of malaria in pregnancy on the expression of immune mediators in placental tissue.
- Placental histological findings.
- Significant correlations between anti-RV and anti-TT IgG in umbilical cord with anti-RV and anti-TT IgG in maternal blood and placental histological findings.
- Significant correlations between CMR of anti-RV and CMR of anti-TT in umbilical cord with the expression of immune mediators and placental histological findings.
- DISCUSSION
- ACKNOWLEDGMENTS
- REFERENCES
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Swamy GK , Garcia-Putnam R , 2013. Vaccine-preventable diseases in pregnancy. Am J Perinatol 30: 89–97.
-
2.
van den Berg JP , Westerbeek EA , van der Klis FR , Berbers GA , van Elburg RM , 2011. Transplacental transport of IgG antibodies to preterm infants: a review of the literature. Early Hum Dev 87: 67–72.
-
3.
Basha S , Surendran N , Pichichero M , 2014. Immune responses in neonates. Expert Rev Clin Immunol 10: 1171–1184.
-
4.
Faucette AN , Pawlitz MD , Pei B , Yao F , Chen K , 2015. Immunization of pregnant women: Future of early infant protection. Hum Vaccin Immunother 11: 2549–2555.
-
5.
Aboud S , Matre R , Lyamuya EF , Kristoffersen EK , 2001. Antibodies to tetanus toxoid in women of childbearing age in Dar es Salaam and Bagamoyo, Tanzania. Trop Med Int Health 6: 119–125.
-
6.
Schofield FD , Tucker VM , Westbrook GR , 1961. Neonatal tetanus in New Guinea. Effect of active immunization in pregnancy. BMJ 2: 785–789.
-
7.
Lanata CF , Fischer-Walker CL , Olascoaga AC , Torres CX , Aryee MJ , Black RE , 2013. Global causes of diarrheal disease mortality in children <5 years of age: a systematic review. PLoS One 8: e72788.
-
8.
Bryce J , Boschi-Pinto C , Shibuya K , Black RE , Group WCHER , 2005. WHO estimates of the causes of death in children. Lancet 365: 1147–1152.
-
9.
Linhares AC et al., 2011. Burden and typing of rotavirus group A in Latin America and the Caribbean: systematic review and meta-analysis. Rev Med Virol 21: 89–109.
-
10.
Mwila K , Chilengi R , Simuyandi M , Permar SR , Becker-Dreps S , 2017. Contribution of maternal immunity to decreased rotavirus vaccine performance in low–and middle-income countries. Clin Vaccine Immunol 24: e00405–e00416.
-
11.
Appaiahgari MB , Glass R , Singh S , Taneja S , Rongsen-Chandola T , Bhandari N , Mishra S , Vrati S , 2014. Transplacental rotavirus IgG interferes with immune response to live oral rotavirus vaccine ORV-116E in Indian infants. Vaccine 32: 651–656.
-
12.
Scott S , 2005. Neonatal measles immunity in rural Kenya: the influence of HIV and placental malaria infections on placental transfer of antibodies and levels of antibody in maternal and cord serum samples. J Infect Dis 191: 1854–1860.
-
13.
Jauniaux E , Jurkovic D , Gulbis B , Liesnard C , Lees C , Campbell S , 1995. Materno-fetal immunoglobulin transfer and passive immunity during the first trimester of human pregnancy. Hum Reprod 10: 3297–3300.
-
14.
Malek A , Sager R , Kuhn P , Nicolaides KH , Schneider H , 1996. Evolution of maternofetal transport of immunoglobulins during human pregnancy. Am J Reprod Immunol 36: 248–255.
-
15.
Okoko BJ , Wesumperuma LH , Ota MO , Pinder M , Banya W , Gomez SF , McAdam KP , Hartet AC , 2001. The influence of placental malaria infection and maternal hypergammaglobulinemia on transplacental transfer of antibodies and IgG subclasses in a rural West African population. J Infect Dis 184: 627–632.
-
16.
Okoko BJ , Wesuperuma LH , Ota MO , Banya WA , Pinder M , Gomez FS , Osinusi K , Hart AC , 2001. Influence of placental malaria infection and maternal hypergammaglobulinaemia on materno-foetal transfer of measles and tetanus antibodies in a rural west African population. J Health Popul Nutr 19: 59–65.
-
17.
Cavalcante RS , Kopelman BI , Costa-Carvalho BT , 2008. Placental transfer of Haemophilus influenzae type b antibodies in malnourished pregnant women. Braz J Infect Dis 12: 47–51.
-
18.
de Souza EG , Hara CC , Fagundes DL , de Queiroz AA , Morceli G , Calderon IM , França EL , Honorio-França AC , 2016. Maternal-foetal diabetes modifies neonatal fc receptor expression on human leucocytes. Scand J Immunol 84: 237–244.
-
19.
Atwell JE et al., 2016. Impact of placental malaria and hypergammaglobulinemia on transplacental transfer of respiratory syncytial virus antibody in Papua New Guinea. J Infect Dis 213: 423–431.
-
20.
Brair ME , Brabin BJ , Milligan P , Maxwell S , Hart CA , 1994. Reduced transfer of tetanus antibodies with placental malaria. Lancet 343: 208–209.
-
21.
Cumberland P , Shulman CE , Maple PA , Bulmer JN , Dorman EK , Kawuondo K , Marsh K , Cutts FT , 2007. Maternal HIV infection and placental malaria reduce transplacental antibody transfer and tetanus antibody levels in newborns in Kenya. J Infect Dis 196: 550–557.
-
22.
de Moraes-Pinto MI , Verhoeff F , Chimsuku L , Milligan PJ , Wesumperuma L , Broadhead RL , Brabin BJ , Johnson PM , Hart CA , 1998. Placental antibody transfer: influence of maternal HIV infection and placental malaria. Arch Dis Child Fetal Neonatal 79: 202–205.
-
23.
Fu C , Lu L , Wu H , Shaman J , Cao Y , Fang F , Yang Q , He Q , Yang Z , Wang M , 2016. Placental antibody transfer efficiency and maternal levels: specific for measles, coxsackievirus A16, enterovirus 71, poliomyelitis I-III and HIV-1 antibodies. Sci Rep 6: 38874.
-
24.
Khan WA et al., 2014. Asymptomatic Plasmodium falciparum malaria in pregnant women in the Chittagong Hill Districts of Bangladesh. PLoS One 9: e98442.
-
25.
Arango EM , Samuel R , Agudelo OM , Carmona-Fonseca J , Maestre A , Yanow SK , 2013. Molecular detection of malaria at delivery reveals a high frequency of submicroscopic infections and associated placental damage in pregnant women from northwest Colombia. Am J Trop Med Hyg 89: 178–183.
-
26.
Agudelo OM , Aristizabal BH , Yanow SK , Arango E , Carmona-Fonseca J , Maestre A , 2014. Submicroscopic infection of placenta by Plasmodium produces Th1/Th2 cytokine imbalance, inflammation and hypoxia in women from north-west Colombia. Malar J 13: 122.
-
27.
Ibitokou SA et al., 2014. Submicroscopic infections with Plasmodium falciparum during pregnancy and their association with circulating cytokine, chemokine, and cellular profiles. Clin Vaccine Immunol 21: 859–866.
-
28.
Carmona-Fonseca J , Arango E , Maestre A , 2013. Placental malaria in Colombia: histopathologic findings in Plasmodium vivax and P. falciparum infections. Am J Trop Med Hyg 88: 1093–1101.
-
29.
Muehlenbachs A , Fried M , McGready R , Harrington WE , Mutabingwa TK , Nosten F , Duffy PE , 2010. A novel histological grading scheme for placental malaria applied in areas of high and low malaria transmission. J Infect Dis 202: 1608–1616.
-
30.
Carmona-Fonseca J , Maestre A , 2009. Incidencia de la malaria gestacional, congénita y placentaria en Urabá (Antioquia, Colombia), 2005–2007. Rev Colomb Obstet Ginecol 60: 15.
-
31.
Agudelo OM , Arango EM , Maestre A , Carmona-Fonseca J , 2013. Prevalence of gestational, placental and congenital malaria in north-west Colombia. Malar J 12: 341.
-
32.
Plowe CV , Djimde A , Bouare M , Doumbo O , Wellems TE , 1995. Pyrimethamine and proguanil resistance-conferring mutations in Plasmodium falciparum dihydrofolate reductase: polymerase chain reaction methods for surveillance in Africa. Am J Trop Med Hyg 52: 565–568.
-
33.
Shokoples SE , Ndao M , Kowalewska-Grochowska K , Yanow SK , 2009. Multiplexed real-time PCR assay for discrimination of Plasmodium species with improved sensitivity for mixed infections. J Clin Microbiol 47: 975–980.
-
34.
Pfaffl MW , 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
-
35.
Rojas OL , Narváez CF , Greenberg HB , Angel J , Franco MA , 2008. Characterization of rotavirus specific B cells and their relation with serological memory. Virology 380: 234–242.
-
36.
Gnidehou S , Doritchamou J , Arango EM , Cabrera A , Arroyo MI , Kain KC , Ndam NT , Maestre A , Yanow SK , 2014. Functional antibodies against VAR2CSA in nonpregnant populations from colombia exposed to Plasmodium falciparum and Plasmodium vivax. Infect Immun 82: 2565–2573.
-
37.
Thomann M , Schlothauer T , Dashivets T , Malik S , Avenal C , Bulau P , Rüger P , Reusch D , 2015. In vitro glycoengineering of IgG1 and its effect on Fc receptor binding and ADCC activity. PLoS One 10: e0134949.
-
38.
Bondt A , Rombouts Y , Selman MH , Hensbergen PJ , Reiding KR , Hazes JM , Dolhain RJ , Wuhrer M , 2014. Immunoglobulin G (IgG) Fab glycosylation analysis using a new mass spectrometric high-throughput profiling method reveals pregnancy-associated changes. Mol Cell Proteomics 11: 3029–3039.
-
39.
Huhn C , Selman MH , Ruhaak LR , Deelder AM , Wuhrer M , 2009. IgG glycosylation analysis. Proteomics 9: 882–913.
-
40.
Liu X , Ye L , Bai Y , Mojidi H , Simister NE , Zhu X , 2008. Activation of the JAK/STAT-1 signaling pathway by IFN-gamma can down-regulate functional expression of the MHC class I-related neonatal Fc receptor for IgG. J Immunol 181: 449–463.
-
41.
Goyal JP , Makwana AM , 2014. Comparison of clinical profile between P. vivax and P. falciparum malaria in children: a tertiary care centre perspective from India. Malar Res Treat 2014: 132672.
-
42.
Karunaweera ND , Wijesekera SK , Wanasekera D , Mendis KN , Carter R , 2003. The paroxysm of Plasmodium vivax malaria. Trends Parasitol 19: 188–193.
-
43.
King T , Lamb T , 2015. Interferon-γ: the Jekyll and Hyde of malaria. PLoS Pathog 11: e1005118.
-
44.
Rudin W , Favre N , Bordmann G , Ryffel B , 1997. Interferon-γ is essential for the development of cerebral malaria. Eur J Immunol 27: 810–815.
-
45.
Agudelo García OM. Malaria placentaria submicroscópica por Plasmodium vivax o Plasmodium falciparum: histopatología, células inmunitarias y expresión de genes asociados a hipoxia, apoptosis e inflamación. Medellín, Colombia: Universidad de Antioquia; 2018.
-
46.
López-Guzman C , Carmona-Fonseca J , 2020. Malaria placentaria submicroscópica: histopatología y expresión de mediadores de procesos fisiológicos. Rev Peru Med Exp Salud Publica 37: 220.
-
47.
Abu-Raya B , Smolen KK , Willems F , Kollmann TR , Marchant A , 2016. Transfer of maternal antimicrobial immunity to HIV-exposed uninfected newborns. Front Immunol 7: 338.
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