Skip to main content
Top
Published in: BMC Pregnancy and Childbirth 1/2020

01-12-2020 | Plasmodium Falciparum | Research article

Evaluation of highly sensitive diagnostic tools for the detection of P. falciparum in pregnant women attending antenatal care visits in Colombia

Authors: A. M. Vásquez, G. Vélez, A. Medina, E. Serra-Casas, A. Campillo, I. J. Gonzalez, S. C. Murphy, A. M. Seilie, X. C. Ding, A. Tobón Castaño

Published in: BMC Pregnancy and Childbirth | Issue 1/2020

Login to get access

Abstract

Background

In low transmission settings early diagnosis is the main strategy to reduce adverse outcomes of malaria in pregnancy; however, microscopy and rapid diagnostic tests (RDTs) are inadequate for detecting low-density infections. We studied the performance of the highly sensitive-RDT (hsRDT) and the loop mediated isothermal DNA amplification (LAMP) for the detection of P. falciparum in pregnant women.

Methods

A cross-sectional study was conducted in two malaria-endemic municipalities in Colombia. We screened pregnant women in the context of an antenatal care program in health facilities and evaluated five tests (microscopy, conventional RDT, hsRDT, LAMP and nested polymerase chain reaction-PCR) for the detection of P. falciparum in peripheral blood, using a quantitative reverse transcription PCR (qRT-PCR) as the reference standard. Diagnostic performance of hsRDT and LAMP were compared with routine testing.

Results

The prevalence of P. falciparum was 4.5% by qRT-PCR, half of those infections were subpatent. The sensitivity of the hsRDT (64.1%) was slightly better compared to microscopy and cRDT (59 and 53.8% respectively). LAMP had the highest sensitivity (89.7%) for detecting P. falciparum and the ability to detect very low-density infections (minimum parasite density detected 0.08 p/μL).

Conclusions

There is an underestimation of Plasmodium spp. infections by tests routinely used in pregnant women attending antenatal care visits. LAMP methodology can be successfully implemented at local hospitals in malaria-endemic areas. The relevance of detecting and treating this sub-patent P. falciparum infections in pregnant women should be evaluated.

Trial registration

ClinicalTrials.gov, Identifier: NCT03172221, Date of registration: May 29, 2017.
Appendix
Available only for authorised users
Literature
1.
go back to reference Bardají A, Martínez-Espinosa FE, Arévalo-Herrera M, Padilla N, Kochar S, Ome-Kaius M, Bôtto-Menezes C, Castellanos ME, Kochar DK, Kochar SK, et al. Burden and impact of Plasmodium vivax in pregnancy: a multi-Centre prospective observational study. PLoS Negl Trop Dis. 2017;11(6):e0005606.PubMedPubMedCentral Bardají A, Martínez-Espinosa FE, Arévalo-Herrera M, Padilla N, Kochar S, Ome-Kaius M, Bôtto-Menezes C, Castellanos ME, Kochar DK, Kochar SK, et al. Burden and impact of Plasmodium vivax in pregnancy: a multi-Centre prospective observational study. PLoS Negl Trop Dis. 2017;11(6):e0005606.PubMedPubMedCentral
2.
go back to reference Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, Newman RD. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis. 2007;7(2):93–104.PubMed Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, Brabin B, Newman RD. Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis. 2007;7(2):93–104.PubMed
3.
go back to reference Moore KA, Simpson JA, Scoullar MJL, McGready R, Fowkes FJI. Quantification of the association between malaria in pregnancy and stillbirth: a systematic review and meta-analysis. Lancet Glob Health. 2017;5(11):e1101–12.PubMed Moore KA, Simpson JA, Scoullar MJL, McGready R, Fowkes FJI. Quantification of the association between malaria in pregnancy and stillbirth: a systematic review and meta-analysis. Lancet Glob Health. 2017;5(11):e1101–12.PubMed
4.
go back to reference Rogerson SJ, Desai M, Mayor A, Sicuri E, Taylor SM, van Eijk AM. Burden, pathology, and costs of malaria in pregnancy: new developments for an old problem. Lancet Infect Dis. 2018;18(4):e107–18.PubMed Rogerson SJ, Desai M, Mayor A, Sicuri E, Taylor SM, van Eijk AM. Burden, pathology, and costs of malaria in pregnancy: new developments for an old problem. Lancet Infect Dis. 2018;18(4):e107–18.PubMed
5.
go back to reference Dellicour S, Tatem AJ, Guerra CA, Snow RW, ter Kuile FO. Quantifying the number of pregnancies at risk of malaria in 2007: a demographic study. PLoS Med. 2010;7(1):e1000221.PubMedPubMedCentral Dellicour S, Tatem AJ, Guerra CA, Snow RW, ter Kuile FO. Quantifying the number of pregnancies at risk of malaria in 2007: a demographic study. PLoS Med. 2010;7(1):e1000221.PubMedPubMedCentral
6.
go back to reference Padilla J, Montoya R. Guía de Atención Clínica de Malaria. Infectio. 2011;15(4):215–323. Padilla J, Montoya R. Guía de Atención Clínica de Malaria. Infectio. 2011;15(4):215–323.
7.
go back to reference Yanow SK, Gavina K, Gnidehou S, Maestre A. Impact of malaria in pregnancy as Latin America approaches elimination. Trends Parasitol. 2016;32(5):416–27.PubMed Yanow SK, Gavina K, Gnidehou S, Maestre A. Impact of malaria in pregnancy as Latin America approaches elimination. Trends Parasitol. 2016;32(5):416–27.PubMed
8.
go back to reference Kattenberg JH, Ochodo EA, Boer KR, Schallig HD, Mens PF, Leeflang MM. Systematic review and meta-analysis: rapid diagnostic tests versus placental histology, microscopy and PCR for malaria in pregnant women. Malar J. 2011;10:321.PubMedPubMedCentral Kattenberg JH, Ochodo EA, Boer KR, Schallig HD, Mens PF, Leeflang MM. Systematic review and meta-analysis: rapid diagnostic tests versus placental histology, microscopy and PCR for malaria in pregnant women. Malar J. 2011;10:321.PubMedPubMedCentral
9.
go back to reference Uneke CJ. Diagnosis of Plasmodium falciparum malaria in pregnancy in sub-Saharan Africa: the challenges and public health implications. Parasitol Res. 2008;102(3):333–42.PubMed Uneke CJ. Diagnosis of Plasmodium falciparum malaria in pregnancy in sub-Saharan Africa: the challenges and public health implications. Parasitol Res. 2008;102(3):333–42.PubMed
10.
go back to reference Campos IM, Uribe ML, Cuesta C, Franco-Gallego A, Carmona-Fonseca J, Maestre A. 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. 2011;84(6):929–35.PubMedPubMedCentral Campos IM, Uribe ML, Cuesta C, Franco-Gallego A, Carmona-Fonseca J, Maestre A. 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. 2011;84(6):929–35.PubMedPubMedCentral
11.
go back to reference Agudelo O, Arango E, Maestre A, Carmona-Fonseca J. Prevalence of gestational, placental and congenital malaria in north-West Colombia. Malar J. 2013;12:341.PubMedPubMedCentral Agudelo O, Arango E, Maestre A, Carmona-Fonseca J. Prevalence of gestational, placental and congenital malaria in north-West Colombia. Malar J. 2013;12:341.PubMedPubMedCentral
12.
go back to reference Arango EM, Samuel R, Agudelo OM, Carmona-Fonseca J, Maestre A, Yanow SK. 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. 2013;89(1):178–83.PubMedPubMedCentral Arango EM, Samuel R, Agudelo OM, Carmona-Fonseca J, Maestre A, Yanow SK. 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. 2013;89(1):178–83.PubMedPubMedCentral
13.
go back to reference Gavina K, Gnidehou S, Arango E, Hamel-Martineau C, Mitran C, Agudelo O, Lopez C, Karidio A, Banman S, Carmona-Fonseca J, et al. Clinical Outcomes of Submicroscopic Infections and Correlates of Protection of VAR2CSA Antibodies in a Longitudinal Study of Pregnant Women in Colombia. Infect Immun. 2018;86(4):e00797–17.PubMedPubMedCentral Gavina K, Gnidehou S, Arango E, Hamel-Martineau C, Mitran C, Agudelo O, Lopez C, Karidio A, Banman S, Carmona-Fonseca J, et al. Clinical Outcomes of Submicroscopic Infections and Correlates of Protection of VAR2CSA Antibodies in a Longitudinal Study of Pregnant Women in Colombia. Infect Immun. 2018;86(4):e00797–17.PubMedPubMedCentral
14.
go back to reference Vásquez AM, Zuluaga L, Tobón A, Posada M, Vélez G, González IJ, Campillo A, Ding X. Diagnostic accuracy of loop-mediated isothermal amplification (LAMP) for screening malaria in peripheral and placental blood samples from pregnant women in Colombia. Malar J. 2018;17(1):262.PubMedPubMedCentral Vásquez AM, Zuluaga L, Tobón A, Posada M, Vélez G, González IJ, Campillo A, Ding X. Diagnostic accuracy of loop-mediated isothermal amplification (LAMP) for screening malaria in peripheral and placental blood samples from pregnant women in Colombia. Malar J. 2018;17(1):262.PubMedPubMedCentral
15.
go back to reference Vásquez AM, Medina AC, Tobón-Castaño A, Posada M, Vélez GJ, Campillo A, González IJ, Ding X. Performance of a highly sensitive rapid diagnostic test (HS-RDT) for detecting malaria in peripheral and placental blood samples from pregnant women in Colombia. PLoS One. 2018;13(8):e0201769.PubMedPubMedCentral Vásquez AM, Medina AC, Tobón-Castaño A, Posada M, Vélez GJ, Campillo A, González IJ, Ding X. Performance of a highly sensitive rapid diagnostic test (HS-RDT) for detecting malaria in peripheral and placental blood samples from pregnant women in Colombia. PLoS One. 2018;13(8):e0201769.PubMedPubMedCentral
16.
go back to reference Fried M, Muehlenbachs A, Duffy PE. Diagnosing malaria in pregnancy: an update. Expert Rev Anti-Infect Ther. 2012;10(10):1177–87.PubMedPubMedCentral Fried M, Muehlenbachs A, Duffy PE. Diagnosing malaria in pregnancy: an update. Expert Rev Anti-Infect Ther. 2012;10(10):1177–87.PubMedPubMedCentral
17.
go back to reference Ahmed R, Levy EI, Maratina SS, de Jong JJ, Asih PB, Rozi IE, Hawley W, Syafruddin D, ter Kuile F. Performance of four HRP-2/pLDH combination rapid diagnostic tests and field microscopy as screening tests for malaria in pregnancy in Indonesia: a cross-sectional study. Malar J. 2015;14:420.PubMedPubMedCentral Ahmed R, Levy EI, Maratina SS, de Jong JJ, Asih PB, Rozi IE, Hawley W, Syafruddin D, ter Kuile F. Performance of four HRP-2/pLDH combination rapid diagnostic tests and field microscopy as screening tests for malaria in pregnancy in Indonesia: a cross-sectional study. Malar J. 2015;14:420.PubMedPubMedCentral
18.
go back to reference Umbers AJ, Unger HW, Rosanas-Urgell A, Wangnapi RA, Kattenberg JH, Jally S, Silim S, Lufele E, Karl S, Ome-Kaius M, et al. Accuracy of an HRP-2/panLDH rapid diagnostic test to detect peripheral and placental Plasmodium falciparum infection in Papua new Guinean women with anaemia or suspected malaria. Malar J. 2015;14:412.PubMedPubMedCentral Umbers AJ, Unger HW, Rosanas-Urgell A, Wangnapi RA, Kattenberg JH, Jally S, Silim S, Lufele E, Karl S, Ome-Kaius M, et al. Accuracy of an HRP-2/panLDH rapid diagnostic test to detect peripheral and placental Plasmodium falciparum infection in Papua new Guinean women with anaemia or suspected malaria. Malar J. 2015;14:412.PubMedPubMedCentral
19.
go back to reference Kyabayinze DJ, Zongo I, Cunningham J, Gatton M, Angutoko P, Ategeka J, Compaoré YD, Muehlenbachs A, Mulondo J, Nakalembe M, et al. HRP2 and pLDH-based rapid diagnostic tests, expert microscopy, and PCR for detection of malaria infection during pregnancy and at delivery in areas of varied transmission: a prospective cohort study in Burkina Faso and Uganda. PLoS One. 2016;11(7):e0156954.PubMedPubMedCentral Kyabayinze DJ, Zongo I, Cunningham J, Gatton M, Angutoko P, Ategeka J, Compaoré YD, Muehlenbachs A, Mulondo J, Nakalembe M, et al. HRP2 and pLDH-based rapid diagnostic tests, expert microscopy, and PCR for detection of malaria infection during pregnancy and at delivery in areas of varied transmission: a prospective cohort study in Burkina Faso and Uganda. PLoS One. 2016;11(7):e0156954.PubMedPubMedCentral
20.
go back to reference Williams JE, Cairns M, Njie F, Laryea Quaye S, Awine T, Oduro A, Tagbor H, Bojang K, Magnussen P, Ter Kuile FO, et al. The performance of a rapid diagnostic test in detecting malaria infection in pregnant women and the impact of missed infections. Clin Infect Dis. 2016;62(7):837–44.PubMed Williams JE, Cairns M, Njie F, Laryea Quaye S, Awine T, Oduro A, Tagbor H, Bojang K, Magnussen P, Ter Kuile FO, et al. The performance of a rapid diagnostic test in detecting malaria infection in pregnant women and the impact of missed infections. Clin Infect Dis. 2016;62(7):837–44.PubMed
21.
go back to reference Britton S, Cheng Q, McCarthy JS. Novel molecular diagnostic tools for malaria elimination: a review of options from the point of view of high-throughput and applicability in resource limited settings. Malar J. 2016;15:88.PubMedPubMedCentral Britton S, Cheng Q, McCarthy JS. Novel molecular diagnostic tools for malaria elimination: a review of options from the point of view of high-throughput and applicability in resource limited settings. Malar J. 2016;15:88.PubMedPubMedCentral
22.
go back to reference Lucchi NW, Ndiaye D, Britton S, Udhayakumar V. Expanding the malaria molecular diagnostic options: opportunities and challenges for loop-mediated isothermal amplification tests for malaria control and elimination. Expert Rev Mol Diagn. 2018;18(2):195–203.PubMed Lucchi NW, Ndiaye D, Britton S, Udhayakumar V. Expanding the malaria molecular diagnostic options: opportunities and challenges for loop-mediated isothermal amplification tests for malaria control and elimination. Expert Rev Mol Diagn. 2018;18(2):195–203.PubMed
23.
go back to reference Tegegne B, Getie S, Lemma W, Mohon AN, Pillai DR. Performance of loop-mediated isothermal amplification (LAMP) for the diagnosis of malaria among malaria suspected pregnant women in Northwest Ethiopia. Malar J. 2017;16(1):34.PubMedPubMedCentral Tegegne B, Getie S, Lemma W, Mohon AN, Pillai DR. Performance of loop-mediated isothermal amplification (LAMP) for the diagnosis of malaria among malaria suspected pregnant women in Northwest Ethiopia. Malar J. 2017;16(1):34.PubMedPubMedCentral
24.
go back to reference Das S, Jang IK, Barney B, Peck R, Rek JC, Arinaitwe E, Adrama H, Murphy M, Imwong M, Ling CL, et al. Performance of a high-sensitivity rapid diagnostic test for Plasmodium falciparum malaria in asymptomatic individuals from Uganda and Myanmar and naive human challenge infections. Am J Trop Med Hyg. 2017;97(5):1540–50.PubMedPubMedCentral Das S, Jang IK, Barney B, Peck R, Rek JC, Arinaitwe E, Adrama H, Murphy M, Imwong M, Ling CL, et al. Performance of a high-sensitivity rapid diagnostic test for Plasmodium falciparum malaria in asymptomatic individuals from Uganda and Myanmar and naive human challenge infections. Am J Trop Med Hyg. 2017;97(5):1540–50.PubMedPubMedCentral
25.
go back to reference Landier J, Haohankhunnatham W, Das S, Konghahong K, Christensen P, Raksuansak J, Phattharakokoedbun P, Kajeechiwa L, Thwin MM, Jang IK, et al. Operational Performance of a Plasmodium falciparum Ultrasensitive Rapid Diagnostic Test for Detection of Asymptomatic Infections in Eastern Myanmar. J Clin Microbiol. 2018;56(8):e00565–18.PubMedPubMedCentral Landier J, Haohankhunnatham W, Das S, Konghahong K, Christensen P, Raksuansak J, Phattharakokoedbun P, Kajeechiwa L, Thwin MM, Jang IK, et al. Operational Performance of a Plasmodium falciparum Ultrasensitive Rapid Diagnostic Test for Detection of Asymptomatic Infections in Eastern Myanmar. J Clin Microbiol. 2018;56(8):e00565–18.PubMedPubMedCentral
26.
go back to reference Girma S, Cheaveau J, Mohon AN, Marasinghe D, Legese R, Balasingam N, Abera A, Feleke SM, Golassa L, Pillai DR. Prevalence and epidemiological characteristics of asymptomatic malaria based on ultrasensitive diagnostics: a cross-sectional study. Clin Infect Dis. 2019;9(6):1003-10. Girma S, Cheaveau J, Mohon AN, Marasinghe D, Legese R, Balasingam N, Abera A, Feleke SM, Golassa L, Pillai DR. Prevalence and epidemiological characteristics of asymptomatic malaria based on ultrasensitive diagnostics: a cross-sectional study. Clin Infect Dis. 2019;9(6):1003-10.
28.
go back to reference Departamento Administrativo Nacional de Estadística (DANE). Series de población 1985–2020. Colombia. In: Proyecciones de población a nivel nacional y departamental por sexo y edades simples hasta 80 años y más. [https://www.dane.gov.co/]. Accesed Sept 2018. Departamento Administrativo Nacional de Estadística (DANE). Series de población 1985–2020. Colombia. In: Proyecciones de población a nivel nacional y departamental por sexo y edades simples hasta 80 años y más. [https://​www.​dane.​gov.​co/​]. Accesed Sept 2018.
29.
go back to reference Dorado EJ, Okoth SA, Montenegro LM, Diaz G, Barnwell JW, Udhayakumar V, Murillo Solano C. Genetic characterisation of Plasmodium falciparum isolates with deletion of the pfhrp2 and/or pfhrp3 genes in Colombia: the Amazon region, a challenge for malaria diagnosis and control. PLoS One. 2016;11(9):e0163137.PubMedPubMedCentral Dorado EJ, Okoth SA, Montenegro LM, Diaz G, Barnwell JW, Udhayakumar V, Murillo Solano C. Genetic characterisation of Plasmodium falciparum isolates with deletion of the pfhrp2 and/or pfhrp3 genes in Colombia: the Amazon region, a challenge for malaria diagnosis and control. PLoS One. 2016;11(9):e0163137.PubMedPubMedCentral
30.
go back to reference Buderer NM. Statistical methodology: I. incorporating the prevalence of disease into the sample size calculation for sensitivity and specificity. Acad Emerg Med. 1996;3(9):895–900.PubMed Buderer NM. Statistical methodology: I. incorporating the prevalence of disease into the sample size calculation for sensitivity and specificity. Acad Emerg Med. 1996;3(9):895–900.PubMed
31.
go back to reference World Health Organization (WHO). Microscopy for the detection, identification and quantification of malaria parasites on stained thick and thin blood films in research settings (version 1.0): procedure: methods manual. 1st ed; 2015. World Health Organization (WHO). Microscopy for the detection, identification and quantification of malaria parasites on stained thick and thin blood films in research settings (version 1.0): procedure: methods manual. 1st ed; 2015.
33.
go back to reference Hopkins H, González IJ, Polley SD, Angutoko P, Ategeka J, Asiimwe C, Agaba B, Kyabayinze DJ, Sutherland CJ, Perkins MD, et al. Highly sensitive detection of malaria parasitemia in a malaria-endemic setting: performance of a new loop-mediated isothermal amplification kit in a remote clinic in Uganda. J Infect Dis. 2013;208(4):645–52.PubMedPubMedCentral Hopkins H, González IJ, Polley SD, Angutoko P, Ategeka J, Asiimwe C, Agaba B, Kyabayinze DJ, Sutherland CJ, Perkins MD, et al. Highly sensitive detection of malaria parasitemia in a malaria-endemic setting: performance of a new loop-mediated isothermal amplification kit in a remote clinic in Uganda. J Infect Dis. 2013;208(4):645–52.PubMedPubMedCentral
34.
go back to reference Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah MS, Rahman HA. A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg. 1999;60(4):687–92.PubMed Singh B, Bobogare A, Cox-Singh J, Snounou G, Abdullah MS, Rahman HA. A genus- and species-specific nested polymerase chain reaction malaria detection assay for epidemiologic studies. Am J Trop Med Hyg. 1999;60(4):687–92.PubMed
35.
go back to reference Murphy SC, Daza G, Chang M, Coombs R. Laser cutting eliminates nucleic acid cross-contamination in dried-blood-spot processing. J Clin Microbiol. 2012;50(12):4128–30.PubMedPubMedCentral Murphy SC, Daza G, Chang M, Coombs R. Laser cutting eliminates nucleic acid cross-contamination in dried-blood-spot processing. J Clin Microbiol. 2012;50(12):4128–30.PubMedPubMedCentral
36.
go back to reference Seilie AM, Chang M, Hanron AE, Billman ZP, Stone BC, Zhou K, Olsen TM, Daza G, Ortega J, Cruz KR, et al. Beyond blood smears: qualification of. Am J Trop Med Hyg. 2019;100(6):1466–76.PubMedPubMedCentral Seilie AM, Chang M, Hanron AE, Billman ZP, Stone BC, Zhou K, Olsen TM, Daza G, Ortega J, Cruz KR, et al. Beyond blood smears: qualification of. Am J Trop Med Hyg. 2019;100(6):1466–76.PubMedPubMedCentral
37.
go back to reference Heberle H, Meirelles GV, da Silva FR, Telles GP, Minghim R. InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinformatics. 2015;16:169.PubMedPubMedCentral Heberle H, Meirelles GV, da Silva FR, Telles GP, Minghim R. InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinformatics. 2015;16:169.PubMedPubMedCentral
38.
go back to reference Kattenberg JH, Tahita CM, Versteeg IA, Tinto H, Traoré Coulibaly M, D'Alessandro U, Schallig HD, Mens PF. Evaluation of antigen detection tests, microscopy, and polymerase chain reaction for diagnosis of malaria in peripheral blood in asymptomatic pregnant women in Nanoro, Burkina Faso. Am J Trop Med Hyg. 2012;87(2):251–6.PubMedPubMedCentral Kattenberg JH, Tahita CM, Versteeg IA, Tinto H, Traoré Coulibaly M, D'Alessandro U, Schallig HD, Mens PF. Evaluation of antigen detection tests, microscopy, and polymerase chain reaction for diagnosis of malaria in peripheral blood in asymptomatic pregnant women in Nanoro, Burkina Faso. Am J Trop Med Hyg. 2012;87(2):251–6.PubMedPubMedCentral
39.
go back to reference Hofmann NE, Antunes Moniz C, Holzschuh A, Keitel K, Boillat-Blanco N, Kagoro F, Samaka J, Mbarack Z, Ding XC, González IJ, et al. Diagnostic performance of conventional and ultrasensitive rapid diagnostic tests for malaria in febrile outpatients in Tanzania. J Infect Dis. 2019;219(9):1490–8.PubMed Hofmann NE, Antunes Moniz C, Holzschuh A, Keitel K, Boillat-Blanco N, Kagoro F, Samaka J, Mbarack Z, Ding XC, González IJ, et al. Diagnostic performance of conventional and ultrasensitive rapid diagnostic tests for malaria in febrile outpatients in Tanzania. J Infect Dis. 2019;219(9):1490–8.PubMed
40.
go back to reference Rogerson SJ, Meshnick S. Malaria in pregnancy: late consequences of early infections. J Infect Dis. 2019;220(9):1396–8. Rogerson SJ, Meshnick S. Malaria in pregnancy: late consequences of early infections. J Infect Dis. 2019;220(9):1396–8.
41.
go back to reference Cohee LM, Kalilani-Phiri L, Boudova S, Joshi S, Mukadam R, Seydel KB, Mawindo P, Thesing P, Kamiza S, Makwakwa K, et al. Submicroscopic malaria infection during pregnancy and the impact of intermittent preventive treatment. Malar J. 2014;13:274.PubMedPubMedCentral Cohee LM, Kalilani-Phiri L, Boudova S, Joshi S, Mukadam R, Seydel KB, Mawindo P, Thesing P, Kamiza S, Makwakwa K, et al. Submicroscopic malaria infection during pregnancy and the impact of intermittent preventive treatment. Malar J. 2014;13:274.PubMedPubMedCentral
42.
go back to reference Cottrell G, Moussiliou A, Luty AJ, Cot M, Fievet N, Massougbodji A, Deloron P, Tuikue Ndam N. Submicroscopic Plasmodium falciparum infections are associated with maternal Anemia, premature births, and low birth weight. Clin Infect Dis. 2015;60(10):1481–8.PubMed Cottrell G, Moussiliou A, Luty AJ, Cot M, Fievet N, Massougbodji A, Deloron P, Tuikue Ndam N. Submicroscopic Plasmodium falciparum infections are associated with maternal Anemia, premature births, and low birth weight. Clin Infect Dis. 2015;60(10):1481–8.PubMed
Metadata
Title
Evaluation of highly sensitive diagnostic tools for the detection of P. falciparum in pregnant women attending antenatal care visits in Colombia
Authors
A. M. Vásquez
G. Vélez
A. Medina
E. Serra-Casas
A. Campillo
I. J. Gonzalez
S. C. Murphy
A. M. Seilie
X. C. Ding
A. Tobón Castaño
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Pregnancy and Childbirth / Issue 1/2020
Electronic ISSN: 1471-2393
DOI
https://doi.org/10.1186/s12884-020-03114-4

Other articles of this Issue 1/2020

BMC Pregnancy and Childbirth 1/2020 Go to the issue