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Published in: BMC Medicine 1/2017

Open Access 01-12-2017 | Research article

Influence of the number and timing of malaria episodes during pregnancy on prematurity and small-for-gestational-age in an area of low transmission

Authors: Kerryn A. Moore, Julie A. Simpson, Jacher Wiladphaingern, Aung Myat Min, Mupawjay Pimanpanarak, Moo Kho Paw, Jathee Raksuansak, Sasithon Pukrittayakamee, Freya J. I. Fowkes, Nicholas J. White, François Nosten, Rose McGready

Published in: BMC Medicine | Issue 1/2017

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Abstract

Background

Most evidence on the association between malaria in pregnancy and adverse pregnancy outcomes focuses on falciparum malaria detected at birth. We assessed the association between the number and timing of falciparum and vivax malaria episodes during pregnancy on small-for-gestational-age (SGA) and preterm birth.

Methods

We analysed observational data collected from antenatal clinics on the Thailand-Myanmar border (1986–2015). We assessed the effects of the total number of malaria episodes in pregnancy on SGA and the effects of malaria in pregnancy on SGA, very preterm birth, and late preterm birth, by the gestational age at malaria detection and treatment using logistic regression models with time-dependent malaria variables (monthly intervals). World Health Organisation definitions of very preterm birth (≥28 and <32 weeks) and late preterm birth (≥32 and <37 weeks) and international SGA standards were used.

Results

Of 50,060 pregnant women followed, 8221 (16%) had malaria during their pregnancy. Of the 50,060 newborns, 10,005 (21%) were SGA, 540 (1%) were very preterm, and 4331 (9%) were late preterm. The rates of falciparum and vivax malaria were highest at 6 and 5 weeks’ gestation, respectively. The odds of SGA increased linearly by 1.13-fold (95% confidence interval: 1.09, 1.17) and 1.27-fold (1.21, 1.33) per episode of falciparum and vivax malaria, respectively. Falciparum malaria at any gestation period after 12–16 weeks and vivax malaria after 20–24 weeks were associated with SGA (falciparum odds ratio, OR range: 1.15–1.63 [p range: <0.001–0.094]; vivax OR range: 1.12–1.54 [p range: <0.001–0.138]). Falciparum malaria at any gestation period after 24–28 weeks was associated with either very or late preterm birth (OR range: 1.44–2.53; p range: <0.001–0.001). Vivax malaria at 24–28 weeks was associated with very preterm birth (OR: 1.79 [1.11, 2.90]), and vivax malaria at 28–32 weeks was associated with late preterm birth (OR: 1.23 [1.01, 1.50]). Many of these associations held for asymptomatic malaria.

Conclusions

Protection against malaria should be started as early as possible in pregnancy. Malaria control and elimination efforts in the general population can avert the adverse consequences associated with treated asymptomatic malaria in pregnancy.
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Literature
2.
3.
go back to reference Matangila JR, Lufuluabo J, Ibalanky AL, da Luz RA I, Lutumba P, Van Geertruyden J-P. Asymptomatic Plasmodium falciparum infection is associated with anaemia in pregnancy and can be more cost-effectively detected by rapid diagnostic test than by microscopy in Kinshasa, Democratic Republic of the Congo. Malar J. 2014;13:132.CrossRefPubMedPubMedCentral Matangila JR, Lufuluabo J, Ibalanky AL, da Luz RA I, Lutumba P, Van Geertruyden J-P. Asymptomatic Plasmodium falciparum infection is associated with anaemia in pregnancy and can be more cost-effectively detected by rapid diagnostic test than by microscopy in Kinshasa, Democratic Republic of the Congo. Malar J. 2014;13:132.CrossRefPubMedPubMedCentral
4.
go back to reference Douamba Z, Bisseye C, Djigma FW, Compaoré TR, Bazie VJT, Pietra V, et al. Asymptomatic malaria correlates with anaemia in pregnant women at Ouagadougou, Burkina Faso. J Biomed Biotechnol. 2012;2012(October 2010):198317.PubMedPubMedCentral Douamba Z, Bisseye C, Djigma FW, Compaoré TR, Bazie VJT, Pietra V, et al. Asymptomatic malaria correlates with anaemia in pregnant women at Ouagadougou, Burkina Faso. J Biomed Biotechnol. 2012;2012(October 2010):198317.PubMedPubMedCentral
5.
go back to reference Rijken MJ, Papageorghiou AT, Thiptharakun S, Kiricharoen S, Dwell SLM, Wiladphaingern J, et al. Ultrasound evidence of early fetal growth restriction after maternal malaria infection. PLoS One. 2012;7(2):e31411. doi:10.1371/journal.pone.0031411. Rijken MJ, Papageorghiou AT, Thiptharakun S, Kiricharoen S, Dwell SLM, Wiladphaingern J, et al. Ultrasound evidence of early fetal growth restriction after maternal malaria infection. PLoS One. 2012;7(2):e31411. doi:10.​1371/​journal.​pone.​0031411.
6.
go back to reference Dorman EK, Shulman CE, Kingdom J, Bulmer JN, Mwendwa J, Peshu N, et al. Impaired uteroplacental blood flow in pregnancies complicated by falciparum malaria. Ultrasound Obs Gynecol. 2002;19:165–70.CrossRef Dorman EK, Shulman CE, Kingdom J, Bulmer JN, Mwendwa J, Peshu N, et al. Impaired uteroplacental blood flow in pregnancies complicated by falciparum malaria. Ultrasound Obs Gynecol. 2002;19:165–70.CrossRef
7.
go back to reference McGready R, Lee SJ, Wiladphaingern J, Ashley EA, Rijken MJ, Boel M, et al. Adverse effects of falciparum and vivax malaria and the safety of antimalarial treatment in early pregnancy: a population-based study. Lancet Infect Dis. 2012;12:388–96.CrossRefPubMedPubMedCentral McGready R, Lee SJ, Wiladphaingern J, Ashley EA, Rijken MJ, Boel M, et al. Adverse effects of falciparum and vivax malaria and the safety of antimalarial treatment in early pregnancy: a population-based study. Lancet Infect Dis. 2012;12:388–96.CrossRefPubMedPubMedCentral
8.
go back to reference Nosten F, McGready R, Simpson JA, Thwai KL, Balkan S, Cho T, et al. Effects of Plasmodium vivax malaria in pregnancy. Lancet. 1999;354:546–9.CrossRefPubMed Nosten F, McGready R, Simpson JA, Thwai KL, Balkan S, Cho T, et al. Effects of Plasmodium vivax malaria in pregnancy. Lancet. 1999;354:546–9.CrossRefPubMed
9.
go back to reference Katz J, Lee ACC, Kozuki N, Lawn JE, Cousens S, Blencowe H, et al. Mortality risk in preterm and small-for-gestational-age infants in low-income and middle-income countries: a pooled country analysis. Lancet. 2013;382:417–25.CrossRefPubMedPubMedCentral Katz J, Lee ACC, Kozuki N, Lawn JE, Cousens S, Blencowe H, et al. Mortality risk in preterm and small-for-gestational-age infants in low-income and middle-income countries: a pooled country analysis. Lancet. 2013;382:417–25.CrossRefPubMedPubMedCentral
10.
go back to reference Lawn JE, Blencowe H, Oza S, You D, Lee ACC, Waiswa P, et al. Every newborn: progress, priorities, and potential beyond survival. Lancet. 2014;384:189–205.CrossRefPubMed Lawn JE, Blencowe H, Oza S, You D, Lee ACC, Waiswa P, et al. Every newborn: progress, priorities, and potential beyond survival. Lancet. 2014;384:189–205.CrossRefPubMed
11.
go back to reference Kalilani L, Mofolo I, Chaponda M, Rogerson SJ, Meshnick SR. The effect of timing and frequency of Plasmodium falciparum infection during pregnancy on the risk of low birth weight and maternal anemia. Trans R Soc Trop Med Hyg. 2010;104:416–22.CrossRefPubMedPubMedCentral Kalilani L, Mofolo I, Chaponda M, Rogerson SJ, Meshnick SR. The effect of timing and frequency of Plasmodium falciparum infection during pregnancy on the risk of low birth weight and maternal anemia. Trans R Soc Trop Med Hyg. 2010;104:416–22.CrossRefPubMedPubMedCentral
12.
go back to reference Verhoeff FH, Brabin BJ, van Buuren S, Chimsuku L, Kazembe P, Wit JM, et al. An analysis of intra-uterine growth retardation in rural Malawi. Eur J Clin Nutr. 2001;55:682–9.CrossRefPubMed Verhoeff FH, Brabin BJ, van Buuren S, Chimsuku L, Kazembe P, Wit JM, et al. An analysis of intra-uterine growth retardation in rural Malawi. Eur J Clin Nutr. 2001;55:682–9.CrossRefPubMed
13.
go back to reference Kalilani-Phiri L, Thesing PC, Nyirenda OM, Mawindo P, Madanitsa M, Membe G, et al. Timing of malaria infection during pregnancy has characteristic maternal, infant and placental outcomes. PLoS One. 2013;8:e74643.CrossRefPubMedPubMedCentral Kalilani-Phiri L, Thesing PC, Nyirenda OM, Mawindo P, Madanitsa M, Membe G, et al. Timing of malaria infection during pregnancy has characteristic maternal, infant and placental outcomes. PLoS One. 2013;8:e74643.CrossRefPubMedPubMedCentral
14.
go back to reference Cottrell G, Mary J-Y, Barro D, Cot M. The importance of the period of malarial infection during pregnancy on birth weight in tropical Africa. Am J Trop Med Hyg. 2007;76:849–54.PubMed Cottrell G, Mary J-Y, Barro D, Cot M. The importance of the period of malarial infection during pregnancy on birth weight in tropical Africa. Am J Trop Med Hyg. 2007;76:849–54.PubMed
15.
go back to reference Huynh B-T, Fievet N, Gbaguidi G, Dechavanne S, Borgella S, Guézo-Mévo B, et al. Influence of the timing of malaria infection during pregnancy on birth weight and on maternal anemia in Benin. Am J Trop Med Hyg. 2011;85:214–20.CrossRefPubMedPubMedCentral Huynh B-T, Fievet N, Gbaguidi G, Dechavanne S, Borgella S, Guézo-Mévo B, et al. Influence of the timing of malaria infection during pregnancy on birth weight and on maternal anemia in Benin. Am J Trop Med Hyg. 2011;85:214–20.CrossRefPubMedPubMedCentral
16.
go back to reference Valea I, Tinto H, Drabo MK, Huybregts L, Sorgho H, Ouedraogo J-B, et al. An analysis of timing and frequency of malaria infection during pregnancy in relation to the risk of low birth weight, anaemia and perinatal mortality in Burkina Faso. Malar J. 2012;11:71.CrossRefPubMedPubMedCentral Valea I, Tinto H, Drabo MK, Huybregts L, Sorgho H, Ouedraogo J-B, et al. An analysis of timing and frequency of malaria infection during pregnancy in relation to the risk of low birth weight, anaemia and perinatal mortality in Burkina Faso. Malar J. 2012;11:71.CrossRefPubMedPubMedCentral
17.
go back to reference Sullivan AD, Nyirenda T, Cullinan T, Taylor T, Harlow SD, James SA, et al. Malaria infection during pregnancy: intrauterine growth retardation and preterm delivery in Malawi. J Infect Dis. 1999;179:1580–3.CrossRefPubMed Sullivan AD, Nyirenda T, Cullinan T, Taylor T, Harlow SD, James SA, et al. Malaria infection during pregnancy: intrauterine growth retardation and preterm delivery in Malawi. J Infect Dis. 1999;179:1580–3.CrossRefPubMed
18.
go back to reference McClure EM, Meshnick SR, Lazebnik N, Mungai P, King CL, Hudgens M, et al. A cohort study of Plasmodium falciparum malaria in pregnancy and associations with uteroplacental blood flow and fetal anthropometrics in Kenya. Int J Gynecol Obstet. 2014;126:78–82.CrossRef McClure EM, Meshnick SR, Lazebnik N, Mungai P, King CL, Hudgens M, et al. A cohort study of Plasmodium falciparum malaria in pregnancy and associations with uteroplacental blood flow and fetal anthropometrics in Kenya. Int J Gynecol Obstet. 2014;126:78–82.CrossRef
19.
go back to reference Griffin JB, Lokomba V, Landis SH, Thorp JM, Herring AH, Tshefu AK, et al. Plasmodium falciparum parasitaemia in the first half of pregnancy, uterine and umbilical artery blood flow, and foetal growth: a longitudinal Doppler ultrasound study. Malar J. 2012;11:319.CrossRefPubMedPubMedCentral Griffin JB, Lokomba V, Landis SH, Thorp JM, Herring AH, Tshefu AK, et al. Plasmodium falciparum parasitaemia in the first half of pregnancy, uterine and umbilical artery blood flow, and foetal growth: a longitudinal Doppler ultrasound study. Malar J. 2012;11:319.CrossRefPubMedPubMedCentral
20.
go back to reference Machado Filho AC, Da Costa EP, Da Costa EP, Reis IS, Fernandes EAC, Paim BV, et al. Effects of vivax malaria acquired before 20 weeks of pregnancy on subsequent changes in fetal growth. Am J Trop Med Hyg. 2014;90:371–6.CrossRefPubMedPubMedCentral Machado Filho AC, Da Costa EP, Da Costa EP, Reis IS, Fernandes EAC, Paim BV, et al. Effects of vivax malaria acquired before 20 weeks of pregnancy on subsequent changes in fetal growth. Am J Trop Med Hyg. 2014;90:371–6.CrossRefPubMedPubMedCentral
21.
go back to reference McGready R, Thwai K, Cho T, Samuel, Looareesuwan S, White N, et al. The effects of quinine and chloroquine antimalarial treatments in the first trimester of pregnancy. Trans R Soc Trop Med Hyg. 2002;96:180–4.CrossRefPubMed McGready R, Thwai K, Cho T, Samuel, Looareesuwan S, White N, et al. The effects of quinine and chloroquine antimalarial treatments in the first trimester of pregnancy. Trans R Soc Trop Med Hyg. 2002;96:180–4.CrossRefPubMed
22.
go back to reference Briand V, Saal J, Ghafari C, Huynh B, Fievet N, Schmiegelow C, et al. Fetal growth restriction is associated with malaria in pregnancy: a prospective longitudinal study in Benin. J Infect Dis. 2016;214:417–25.CrossRefPubMed Briand V, Saal J, Ghafari C, Huynh B, Fievet N, Schmiegelow C, et al. Fetal growth restriction is associated with malaria in pregnancy: a prospective longitudinal study in Benin. J Infect Dis. 2016;214:417–25.CrossRefPubMed
23.
go back to reference Landis SH, Lokomba V, Ananth CV, Atibu J, Ryder RW, Hartmann KE, et al. Impact of maternal malaria and under-nutrition on intrauterine growth restriction: a prospective ultrasound study in Democratic Republic of Congo. Epidemiol Infect. 2009;137:294–304.CrossRefPubMed Landis SH, Lokomba V, Ananth CV, Atibu J, Ryder RW, Hartmann KE, et al. Impact of maternal malaria and under-nutrition on intrauterine growth restriction: a prospective ultrasound study in Democratic Republic of Congo. Epidemiol Infect. 2009;137:294–304.CrossRefPubMed
24.
go back to reference De Beaudrap P, Turyakira E, White LJ, Nabasumba C, Tumwebaze B, Muehlenbachs A, et al. Impact of malaria during pregnancy on pregnancy outcomes in a Ugandan prospective cohort with intensive malaria screening and prompt treatment. Malar J. 2013;12:139.CrossRefPubMedPubMedCentral De Beaudrap P, Turyakira E, White LJ, Nabasumba C, Tumwebaze B, Muehlenbachs A, et al. Impact of malaria during pregnancy on pregnancy outcomes in a Ugandan prospective cohort with intensive malaria screening and prompt treatment. Malar J. 2013;12:139.CrossRefPubMedPubMedCentral
25.
go back to reference Nosten F, ter Kuile F, Maelankirri L, Decludt B, White NJ. Malaria during pregnancy in an area of unstable endemicity. Trans R Soc Trop Med Hyg. 1991;85:424–9.CrossRefPubMed Nosten F, ter Kuile F, Maelankirri L, Decludt B, White NJ. Malaria during pregnancy in an area of unstable endemicity. Trans R Soc Trop Med Hyg. 1991;85:424–9.CrossRefPubMed
26.
go back to reference McGready R, Boel M, Rijken MJ, Ashley EA, Cho T, Moo O, et al. Effect of early detection and treatment on malaria related maternal mortality on the north-western border of Thailand 1986–2010. PLoS One. 2012;7(7):e40244. doi:10.1371/journal.pone.0040244. McGready R, Boel M, Rijken MJ, Ashley EA, Cho T, Moo O, et al. Effect of early detection and treatment on malaria related maternal mortality on the north-western border of Thailand 1986–2010. PLoS One. 2012;7(7):e40244. doi:10.​1371/​journal.​pone.​0040244.
27.
go back to reference McGready R, Kang J, Watts I, Tyrosvoutis MEG, Torchinsky MB, Htut AM, et al. Audit of antenatal screening for syphilis and HIV in migrant and refugee women on the Thai-Myanmar border: a descriptive study. F1000Res. 2014;3:123.PubMed McGready R, Kang J, Watts I, Tyrosvoutis MEG, Torchinsky MB, Htut AM, et al. Audit of antenatal screening for syphilis and HIV in migrant and refugee women on the Thai-Myanmar border: a descriptive study. F1000Res. 2014;3:123.PubMed
28.
go back to reference Laochan N, Zaloumis S, Imwong M, Lek-Uthai U, Brockman A, Sriprawat K, et al. Intervals to Plasmodium falciparum recurrence after anti-malarial treatment in pregnancy: a longitudinal prospective cohort. Malar J. 2015;14:221.CrossRefPubMedPubMedCentral Laochan N, Zaloumis S, Imwong M, Lek-Uthai U, Brockman A, Sriprawat K, et al. Intervals to Plasmodium falciparum recurrence after anti-malarial treatment in pregnancy: a longitudinal prospective cohort. Malar J. 2015;14:221.CrossRefPubMedPubMedCentral
29.
go back to reference Moore KA, Simpson JA, Thomas KH, Rijken MJ, White LJ, Dwell SLM, et al. Estimating gestational age in late presenters to antenatal care in a resource-limited setting on the Thai-Myanmar border. PLoS One. 2015;10:e0131025.CrossRefPubMedPubMedCentral Moore KA, Simpson JA, Thomas KH, Rijken MJ, White LJ, Dwell SLM, et al. Estimating gestational age in late presenters to antenatal care in a resource-limited setting on the Thai-Myanmar border. PLoS One. 2015;10:e0131025.CrossRefPubMedPubMedCentral
30.
go back to reference Villar J, Ismail LC, Victora CG, Ohuma EO, Bertino E, Altman DG, et al. International standards for newborn weight, length, and head circumference by gestational age and sex: the Newborn Cross-Sectional Study of the INTERGROWTH-21st Project. Lancet. 2014;384:857–68.CrossRefPubMed Villar J, Ismail LC, Victora CG, Ohuma EO, Bertino E, Altman DG, et al. International standards for newborn weight, length, and head circumference by gestational age and sex: the Newborn Cross-Sectional Study of the INTERGROWTH-21st Project. Lancet. 2014;384:857–68.CrossRefPubMed
31.
go back to reference Moore KA, Simpson JA, Paw MK, Pimanpanarak M, Wiladphaingern J, Rijken MJ, et al. Safety of artemisinins in first trimester of prospectively followed pregnancies: an observational study. Lancet Infect Dis. 2016;16:576–83.CrossRefPubMedPubMedCentral Moore KA, Simpson JA, Paw MK, Pimanpanarak M, Wiladphaingern J, Rijken MJ, et al. Safety of artemisinins in first trimester of prospectively followed pregnancies: an observational study. Lancet Infect Dis. 2016;16:576–83.CrossRefPubMedPubMedCentral
32.
go back to reference Brabin BJ. An analysis of malaria in pregnancy in Africa. Bull World Heal Organ. 1983;61:1005–16. Brabin BJ. An analysis of malaria in pregnancy in Africa. Bull World Heal Organ. 1983;61:1005–16.
33.
go back to reference Das L. Malaria during pregnancy and its effects on foetus in a tribal area of Koraput District, Orissa. Indian J Malariol. 2000;37:11–7.PubMed Das L. Malaria during pregnancy and its effects on foetus in a tribal area of Koraput District, Orissa. Indian J Malariol. 2000;37:11–7.PubMed
34.
go back to reference Coulibaly SO, Gies S, D’Alessandro U. Malaria burden among pregnant women living in the rural district of Boromo, Burkina Faso. Am J Trop Med Hyg. 2007;77(6 Suppl):56–60.PubMed Coulibaly SO, Gies S, D’Alessandro U. Malaria burden among pregnant women living in the rural district of Boromo, Burkina Faso. Am J Trop Med Hyg. 2007;77(6 Suppl):56–60.PubMed
35.
go back to reference Singh N, Mehra RK, Srivastava N. Malaria during pregnancy and infancy, in an area of intense malaria transmission in central India. Ann Trop Med Parasitol. 2001;95:19–29.CrossRefPubMed Singh N, Mehra RK, Srivastava N. Malaria during pregnancy and infancy, in an area of intense malaria transmission in central India. Ann Trop Med Parasitol. 2001;95:19–29.CrossRefPubMed
36.
go back to reference Imwong M, Nguyen TN, Tripura R, Peto TJ, Lee SJ, Lwin KM, et al. The epidemiology of subclinical malaria infections in South-East Asia: findings from cross-sectional surveys in Thailand–Myanmar border areas, Cambodia, and Vietnam. Malar J. 2015;14:381.CrossRefPubMedPubMedCentral Imwong M, Nguyen TN, Tripura R, Peto TJ, Lee SJ, Lwin KM, et al. The epidemiology of subclinical malaria infections in South-East Asia: findings from cross-sectional surveys in Thailand–Myanmar border areas, Cambodia, and Vietnam. Malar J. 2015;14:381.CrossRefPubMedPubMedCentral
37.
go back to reference Umbers AJ, Aitken EH, Rogerson SJ. Malaria in pregnancy: small babies, big problem. Trends Parasitol. 2011;27:168–75.CrossRefPubMed Umbers AJ, Aitken EH, Rogerson SJ. Malaria in pregnancy: small babies, big problem. Trends Parasitol. 2011;27:168–75.CrossRefPubMed
38.
go back to reference Umbers AJ, Stanisic DI, Ome M, Wangnapi R, Hanieh S, Unger HW, et al. Does malaria affect placental development? Evidence from in vitro models. PLoS One. 2013;8:e55269.CrossRefPubMedPubMedCentral Umbers AJ, Stanisic DI, Ome M, Wangnapi R, Hanieh S, Unger HW, et al. Does malaria affect placental development? Evidence from in vitro models. PLoS One. 2013;8:e55269.CrossRefPubMedPubMedCentral
39.
go back to reference Walker PGT, Griffin JT, Cairns M, Rogerson SJ, Eijk AMV, Kuile F, et al. A model of parity-dependent immunity to placental malaria. Nat Commun. 2013;4:1609.CrossRefPubMedPubMedCentral Walker PGT, Griffin JT, Cairns M, Rogerson SJ, Eijk AMV, Kuile F, et al. A model of parity-dependent immunity to placental malaria. Nat Commun. 2013;4:1609.CrossRefPubMedPubMedCentral
40.
go back to reference Fried M, Muga RO, Misore AO, Duffy PE. Malaria elicits type 1 cytokines in the human placenta: IFN-gamma and TNF-alpha associated with pregnancy outcomes. J Immunol. 1998;160:2523–30.PubMed Fried M, Muga RO, Misore AO, Duffy PE. Malaria elicits type 1 cytokines in the human placenta: IFN-gamma and TNF-alpha associated with pregnancy outcomes. J Immunol. 1998;160:2523–30.PubMed
41.
go back to reference Rogerson SJ, Hviid L, Duff PE, Leke RFG, Taylor DW. Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis. 2007;7:105–17.CrossRefPubMed Rogerson SJ, Hviid L, Duff PE, Leke RFG, Taylor DW. Malaria in pregnancy: pathogenesis and immunity. Lancet Infect Dis. 2007;7:105–17.CrossRefPubMed
42.
go back to reference Umbers AJ, Boeuf P, Clapham C, Stanisic DI, Baiwog F, Mueller I, et al. Placental malaria-associated inflammation disturbs the insulin-like growth factor axis of fetal growth regulation. J Infect Dis. 2011;203:561–9.CrossRefPubMedPubMedCentral Umbers AJ, Boeuf P, Clapham C, Stanisic DI, Baiwog F, Mueller I, et al. Placental malaria-associated inflammation disturbs the insulin-like growth factor axis of fetal growth regulation. J Infect Dis. 2011;203:561–9.CrossRefPubMedPubMedCentral
43.
go back to reference McGready R, Davison B, Stepniewska K, Cho T, Shee H, Brockman A, et al. The effects of Plasmodium falciparum and P. vivax infections on placental histopathology in an area of low malaria transmission. Am J Trop Med Hyg. 2004;70:398–407.PubMed McGready R, Davison B, Stepniewska K, Cho T, Shee H, Brockman A, et al. The effects of Plasmodium falciparum and P. vivax infections on placental histopathology in an area of low malaria transmission. Am J Trop Med Hyg. 2004;70:398–407.PubMed
44.
45.
go back to reference Bishop EH. Pelvic scoring for elective induction. Obstet Gynecol. 1964;24:266–8.PubMed Bishop EH. Pelvic scoring for elective induction. Obstet Gynecol. 1964;24:266–8.PubMed
46.
go back to reference Iams JD, Goldenberg RL, Mercer BM, Moawad AH, Meis PJ, Das AF, et al. The Preterm Prediction Study: can low-risk women destined for spontaneous preterm birth be identified? Am J Obstet Gynecol. 2001;184:652–5.CrossRefPubMed Iams JD, Goldenberg RL, Mercer BM, Moawad AH, Meis PJ, Das AF, et al. The Preterm Prediction Study: can low-risk women destined for spontaneous preterm birth be identified? Am J Obstet Gynecol. 2001;184:652–5.CrossRefPubMed
47.
go back to reference van Zijl MD, Koullali B, Mol BW, Pajkrt E, Oudijk MA. Prevention of preterm delivery: current challenges and future prospects. Int J Womens Health. 2016;8:633–45.CrossRefPubMedPubMedCentral van Zijl MD, Koullali B, Mol BW, Pajkrt E, Oudijk MA. Prevention of preterm delivery: current challenges and future prospects. Int J Womens Health. 2016;8:633–45.CrossRefPubMedPubMedCentral
48.
go back to reference Ahmed R, Levy EI, Maratina SS, de Jong JJ, Asih PBS, Rozi IE, et al. 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. doi:10.1186/s12936-015-0943-5.CrossRefPubMedPubMedCentral Ahmed R, Levy EI, Maratina SS, de Jong JJ, Asih PBS, Rozi IE, et al. 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. doi:10.​1186/​s12936-015-0943-5.CrossRefPubMedPubMedCentral
49.
go back to reference Chico RM, Chandramohan D. Intermittent preventive treatment of malaria in pregnancy: at the crossroads of public health policy. Trop Med Int Health. 2011;16:774–85.CrossRefPubMed Chico RM, Chandramohan D. Intermittent preventive treatment of malaria in pregnancy: at the crossroads of public health policy. Trop Med Int Health. 2011;16:774–85.CrossRefPubMed
50.
go back to reference Williams JE, Cairns M, Njie F, Laryea Quaye S, Awine T, Oduro A, 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;62:837–44.CrossRefPubMed Williams JE, Cairns M, Njie F, Laryea Quaye S, Awine T, Oduro A, 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;62:837–44.CrossRefPubMed
51.
go back to reference Nosten F, van Vugt M, Price R, Luxemburger C, Thway K, Brockman A, et al. Effects of artesunate-mefloquine combination on incidence of Plasmodium falciparum malaria and mefloquine resistance in western Thailand: a prospective study. Lancet. 2000;356:297–302.CrossRefPubMed Nosten F, van Vugt M, Price R, Luxemburger C, Thway K, Brockman A, et al. Effects of artesunate-mefloquine combination on incidence of Plasmodium falciparum malaria and mefloquine resistance in western Thailand: a prospective study. Lancet. 2000;356:297–302.CrossRefPubMed
52.
go back to reference Carrara VI, Sirilak S, Thonglairuam J, Rojanawatsirivet C, Proux S, Gilbos V, et al. Deployment of early diagnosis and mefloquine-artesunate treatment of falciparum malaria in Thailand: The Tak Malaria Initiative. PLoS Med. 2006;3:e183.CrossRefPubMedPubMedCentral Carrara VI, Sirilak S, Thonglairuam J, Rojanawatsirivet C, Proux S, Gilbos V, et al. Deployment of early diagnosis and mefloquine-artesunate treatment of falciparum malaria in Thailand: The Tak Malaria Initiative. PLoS Med. 2006;3:e183.CrossRefPubMedPubMedCentral
53.
go back to reference McGready R, Paw MK, Wiladphaingern J, Myat AM, Carrara V, Moore KA, et al. Miscarriage, stillbirth and neonatal mortality in the extreme preterm birth window of gestation in a limited-resource setting on the Thailand- Myanmar border: a population cohort study [version 1; referees: 2 approved with reservations]. Wellcome Open Res. 2016;1:32. doi:10.12688/wellcomeopenres.10352.1. McGready R, Paw MK, Wiladphaingern J, Myat AM, Carrara V, Moore KA, et al. Miscarriage, stillbirth and neonatal mortality in the extreme preterm birth window of gestation in a limited-resource setting on the Thailand- Myanmar border: a population cohort study [version 1; referees: 2 approved with reservations]. Wellcome Open Res. 2016;1:32. doi:10.​12688/​wellcomeopenres.​10352.​1.
Metadata
Title
Influence of the number and timing of malaria episodes during pregnancy on prematurity and small-for-gestational-age in an area of low transmission
Authors
Kerryn A. Moore
Julie A. Simpson
Jacher Wiladphaingern
Aung Myat Min
Mupawjay Pimanpanarak
Moo Kho Paw
Jathee Raksuansak
Sasithon Pukrittayakamee
Freya J. I. Fowkes
Nicholas J. White
François Nosten
Rose McGready
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Medicine / Issue 1/2017
Electronic ISSN: 1741-7015
DOI
https://doi.org/10.1186/s12916-017-0877-6

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