Malaria, malnutrition, and birthweight: A meta-analysis using individual participant data

Jordan E. Cates; Holger W. Unger; Valerie Briand; Nadine Fievet; Innocent Valea; Halidou Tinto; Umberto D’Alessandro; Sarah H. Landis; Seth Adu-Afarwuah; Kathryn G. Dewey; Feiko O. ter Kuile; Meghna Desai; Stephanie Dellicour; Peter Ouma; Julie Gutman; Martina Oneko; Laurence Slutsker; Dianne J. Terlouw; Simon Kariuki; John Ayisi; Mwayiwawo Madanitsa; Victor Mwapasa; Per Ashorn; Kenneth Maleta; Ivo Mueller; Danielle Stanisic; Christentze Schmiegelow; John P.A. Lusingu; Anna Maria van Eijk; Melissa Bauserman; Linda Adair; Stephen R. Cole; Daniel Westreich; Steven Meshnick; Stephen Rogerson

doi:10.1371/journal.pmed.1002373

Malaria, malnutrition, and birthweight: A meta-analysis using individual participant data

Jordan E. Cates^*, Holger W. Unger, Valerie Briand, Nadine Fievet, Innocent Valea, Halidou Tinto, Umberto D’Alessandro, Sarah H. Landis, Seth Adu-Afarwuah, Kathryn G. Dewey, Feiko O. ter Kuile, Meghna Desai, Stephanie Dellicour, Peter Ouma, Julie Gutman, Martina Oneko, Laurence Slutsker, Dianne J. Terlouw, Simon Kariuki, John AyisiMwayiwawo Madanitsa, Victor Mwapasa, Per Ashorn, Kenneth Maleta, Ivo Mueller, Danielle Stanisic, Christentze Schmiegelow, John P.A. Lusingu, Anna Maria van Eijk, Melissa Bauserman, Linda Adair, Stephen R. Cole, Daniel Westreich, Steven Meshnick, Stephen Rogerson

^*Corresponding author for this work

16 Citations (Scopus)

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Abstract

Background: Four studies previously indicated that the effect of malaria infection during pregnancy on the risk of low birthweight (LBW; <2,500 g) may depend upon maternal nutritional status. We investigated this dependence further using a large, diverse study population.

Methods and findings: We evaluated the interaction between maternal malaria infection and maternal anthropometric status on the risk of LBW using pooled data from 14,633 pregnancies from 13 studies (6 cohort studies and 7 randomized controlled trials) conducted in Africa and the Western Pacific from 1996–2015. Studies were identified by the Maternal Malaria and Malnutrition (M3) initiative using a convenience sampling approach and were eligible for pooling given adequate ethical approval and availability of essential variables. Study-specific adjusted effect estimates were calculated using inverse probability of treatment-weighted linear and log-binomial regression models and pooled using a random-effects model. The adjusted risk of delivering a baby with LBW was 8.8% among women with malaria infection at antenatal enrollment compared to 7.7% among uninfected women (adjusted risk ratio [aRR] 1.14 [95% confidence interval (CI): 0.91, 1.42]; N = 13,613), 10.5% among women with malaria infection at delivery compared to 7.9% among uninfected women (aRR 1.32 [95% CI: 1.08, 1.62]; N = 11,826), and 15.3% among women with low mid-upper arm circumference (MUAC <23 cm) at enrollment compared to 9.5% among women with MUAC ≥ 23 cm (aRR 1.60 [95% CI: 1.36, 1.87]; N = 9,008). The risk of delivering a baby with LBW was 17.8% among women with both malaria infection and low MUAC at enrollment compared to 8.4% among uninfected women with MUAC ≥ 23 cm (joint aRR 2.13 [95% CI: 1.21, 3.73]; N = 8,152). There was no evidence of synergism (i.e., excess risk due to interaction) between malaria infection and MUAC on the multiplicative (p = 0.5) or additive scale (p = 0.9). Results were similar using body mass index (BMI) as an anthropometric indicator of nutritional status. Meta-regression results indicated that there may be multiplicative interaction between malaria infection at enrollment and low MUAC within studies conducted in Africa; however, this finding was not consistent on the additive scale, when accounting for multiple comparisons, or when using other definitions of malaria and malnutrition. The major limitations of the study included availability of only 2 cross-sectional measurements of malaria and the limited availability of ultrasound-based pregnancy dating to assess impacts on preterm birth and fetal growth in all studies.

Conclusions: Pregnant women with malnutrition and malaria infection are at increased risk of LBW compared to women with only 1 risk factor or none, but malaria and malnutrition do not act synergistically.

Original language	English
Article number	e1002373
Journal	PLOS Medicine
Volume	14
Issue number	8
Number of pages	20
ISSN	1549-1277
DOIs	https://doi.org/10.1371/journal.pmed.1002373
Publication status	Published - 2017

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Cates, J. E., Unger, H. W., Briand, V., Fievet, N., Valea, I., Tinto, H., D’Alessandro, U., Landis, S. H., Adu-Afarwuah, S., Dewey, K. G., ter Kuile, F. O., Desai, M., Dellicour, S., Ouma, P., Gutman, J., Oneko, M., Slutsker, L., Terlouw, D. J., Kariuki, S., ... Rogerson, S. (2017). Malaria, malnutrition, and birthweight: A meta-analysis using individual participant data. PLOS Medicine, 14(8), [e1002373]. https://doi.org/10.1371/journal.pmed.1002373

Cates, JE, Unger, HW, Briand, V, Fievet, N, Valea, I, Tinto, H, D’Alessandro, U, Landis, SH, Adu-Afarwuah, S, Dewey, KG, ter Kuile, FO, Desai, M, Dellicour, S, Ouma, P, Gutman, J, Oneko, M, Slutsker, L, Terlouw, DJ, Kariuki, S, Ayisi, J, Madanitsa, M, Mwapasa, V, Ashorn, P, Maleta, K, Mueller, I, Stanisic, D, Schmiegelow, C, Lusingu, JPA, van Eijk, AM, Bauserman, M, Adair, L, Cole, SR, Westreich, D, Meshnick, S & Rogerson, S 2017, 'Malaria, malnutrition, and birthweight: A meta-analysis using individual participant data', PLOS Medicine, vol. 14, no. 8, e1002373. https://doi.org/10.1371/journal.pmed.1002373

@article{c3c440a65bb148b0907fbe2a403c2e78,

title = "Malaria, malnutrition, and birthweight: A meta-analysis using individual participant data",

abstract = "Background: Four studies previously indicated that the effect of malaria infection during pregnancy on the risk of low birthweight (LBW; <2,500 g) may depend upon maternal nutritional status. We investigated this dependence further using a large, diverse study population. Methods and findings: We evaluated the interaction between maternal malaria infection and maternal anthropometric status on the risk of LBW using pooled data from 14,633 pregnancies from 13 studies (6 cohort studies and 7 randomized controlled trials) conducted in Africa and the Western Pacific from 1996–2015. Studies were identified by the Maternal Malaria and Malnutrition (M3) initiative using a convenience sampling approach and were eligible for pooling given adequate ethical approval and availability of essential variables. Study-specific adjusted effect estimates were calculated using inverse probability of treatment-weighted linear and log-binomial regression models and pooled using a random-effects model. The adjusted risk of delivering a baby with LBW was 8.8% among women with malaria infection at antenatal enrollment compared to 7.7% among uninfected women (adjusted risk ratio [aRR] 1.14 [95% confidence interval (CI): 0.91, 1.42]; N = 13,613), 10.5% among women with malaria infection at delivery compared to 7.9% among uninfected women (aRR 1.32 [95% CI: 1.08, 1.62]; N = 11,826), and 15.3% among women with low mid-upper arm circumference (MUAC <23 cm) at enrollment compared to 9.5% among women with MUAC ≥ 23 cm (aRR 1.60 [95% CI: 1.36, 1.87]; N = 9,008). The risk of delivering a baby with LBW was 17.8% among women with both malaria infection and low MUAC at enrollment compared to 8.4% among uninfected women with MUAC ≥ 23 cm (joint aRR 2.13 [95% CI: 1.21, 3.73]; N = 8,152). There was no evidence of synergism (i.e., excess risk due to interaction) between malaria infection and MUAC on the multiplicative (p = 0.5) or additive scale (p = 0.9). Results were similar using body mass index (BMI) as an anthropometric indicator of nutritional status. Meta-regression results indicated that there may be multiplicative interaction between malaria infection at enrollment and low MUAC within studies conducted in Africa; however, this finding was not consistent on the additive scale, when accounting for multiple comparisons, or when using other definitions of malaria and malnutrition. The major limitations of the study included availability of only 2 cross-sectional measurements of malaria and the limited availability of ultrasound-based pregnancy dating to assess impacts on preterm birth and fetal growth in all studies. Conclusions: Pregnant women with malnutrition and malaria infection are at increased risk of LBW compared to women with only 1 risk factor or none, but malaria and malnutrition do not act synergistically.",

author = "Cates, {Jordan E.} and Unger, {Holger W.} and Valerie Briand and Nadine Fievet and Innocent Valea and Halidou Tinto and Umberto D{\textquoteright}Alessandro and Landis, {Sarah H.} and Seth Adu-Afarwuah and Dewey, {Kathryn G.} and {ter Kuile}, {Feiko O.} and Meghna Desai and Stephanie Dellicour and Peter Ouma and Julie Gutman and Martina Oneko and Laurence Slutsker and Terlouw, {Dianne J.} and Simon Kariuki and John Ayisi and Mwayiwawo Madanitsa and Victor Mwapasa and Per Ashorn and Kenneth Maleta and Ivo Mueller and Danielle Stanisic and Christentze Schmiegelow and Lusingu, {John P.A.} and {van Eijk}, {Anna Maria} and Melissa Bauserman and Linda Adair and Cole, {Stephen R.} and Daniel Westreich and Steven Meshnick and Stephen Rogerson",

year = "2017",

doi = "10.1371/journal.pmed.1002373",

language = "English",

volume = "14",

journal = "P L o S Medicine (Online)",

issn = "1549-1277",

publisher = "Public Library of Science",

number = "8",

}

TY - JOUR

T1 - Malaria, malnutrition, and birthweight

T2 - A meta-analysis using individual participant data

AU - Cates, Jordan E.

AU - Unger, Holger W.

AU - Briand, Valerie

AU - Fievet, Nadine

AU - Valea, Innocent

AU - Tinto, Halidou

AU - D’Alessandro, Umberto

AU - Landis, Sarah H.

AU - Adu-Afarwuah, Seth

AU - Dewey, Kathryn G.

AU - ter Kuile, Feiko O.

AU - Desai, Meghna

AU - Dellicour, Stephanie

AU - Ouma, Peter

AU - Gutman, Julie

AU - Oneko, Martina

AU - Slutsker, Laurence

AU - Terlouw, Dianne J.

AU - Kariuki, Simon

AU - Ayisi, John

AU - Madanitsa, Mwayiwawo

AU - Mwapasa, Victor

AU - Ashorn, Per

AU - Maleta, Kenneth

AU - Mueller, Ivo

AU - Stanisic, Danielle

AU - Schmiegelow, Christentze

AU - Lusingu, John P.A.

AU - van Eijk, Anna Maria

AU - Bauserman, Melissa

AU - Adair, Linda

AU - Cole, Stephen R.

AU - Westreich, Daniel

AU - Meshnick, Steven

AU - Rogerson, Stephen

PY - 2017

Y1 - 2017

N2 - Background: Four studies previously indicated that the effect of malaria infection during pregnancy on the risk of low birthweight (LBW; <2,500 g) may depend upon maternal nutritional status. We investigated this dependence further using a large, diverse study population. Methods and findings: We evaluated the interaction between maternal malaria infection and maternal anthropometric status on the risk of LBW using pooled data from 14,633 pregnancies from 13 studies (6 cohort studies and 7 randomized controlled trials) conducted in Africa and the Western Pacific from 1996–2015. Studies were identified by the Maternal Malaria and Malnutrition (M3) initiative using a convenience sampling approach and were eligible for pooling given adequate ethical approval and availability of essential variables. Study-specific adjusted effect estimates were calculated using inverse probability of treatment-weighted linear and log-binomial regression models and pooled using a random-effects model. The adjusted risk of delivering a baby with LBW was 8.8% among women with malaria infection at antenatal enrollment compared to 7.7% among uninfected women (adjusted risk ratio [aRR] 1.14 [95% confidence interval (CI): 0.91, 1.42]; N = 13,613), 10.5% among women with malaria infection at delivery compared to 7.9% among uninfected women (aRR 1.32 [95% CI: 1.08, 1.62]; N = 11,826), and 15.3% among women with low mid-upper arm circumference (MUAC <23 cm) at enrollment compared to 9.5% among women with MUAC ≥ 23 cm (aRR 1.60 [95% CI: 1.36, 1.87]; N = 9,008). The risk of delivering a baby with LBW was 17.8% among women with both malaria infection and low MUAC at enrollment compared to 8.4% among uninfected women with MUAC ≥ 23 cm (joint aRR 2.13 [95% CI: 1.21, 3.73]; N = 8,152). There was no evidence of synergism (i.e., excess risk due to interaction) between malaria infection and MUAC on the multiplicative (p = 0.5) or additive scale (p = 0.9). Results were similar using body mass index (BMI) as an anthropometric indicator of nutritional status. Meta-regression results indicated that there may be multiplicative interaction between malaria infection at enrollment and low MUAC within studies conducted in Africa; however, this finding was not consistent on the additive scale, when accounting for multiple comparisons, or when using other definitions of malaria and malnutrition. The major limitations of the study included availability of only 2 cross-sectional measurements of malaria and the limited availability of ultrasound-based pregnancy dating to assess impacts on preterm birth and fetal growth in all studies. Conclusions: Pregnant women with malnutrition and malaria infection are at increased risk of LBW compared to women with only 1 risk factor or none, but malaria and malnutrition do not act synergistically.

AB - Background: Four studies previously indicated that the effect of malaria infection during pregnancy on the risk of low birthweight (LBW; <2,500 g) may depend upon maternal nutritional status. We investigated this dependence further using a large, diverse study population. Methods and findings: We evaluated the interaction between maternal malaria infection and maternal anthropometric status on the risk of LBW using pooled data from 14,633 pregnancies from 13 studies (6 cohort studies and 7 randomized controlled trials) conducted in Africa and the Western Pacific from 1996–2015. Studies were identified by the Maternal Malaria and Malnutrition (M3) initiative using a convenience sampling approach and were eligible for pooling given adequate ethical approval and availability of essential variables. Study-specific adjusted effect estimates were calculated using inverse probability of treatment-weighted linear and log-binomial regression models and pooled using a random-effects model. The adjusted risk of delivering a baby with LBW was 8.8% among women with malaria infection at antenatal enrollment compared to 7.7% among uninfected women (adjusted risk ratio [aRR] 1.14 [95% confidence interval (CI): 0.91, 1.42]; N = 13,613), 10.5% among women with malaria infection at delivery compared to 7.9% among uninfected women (aRR 1.32 [95% CI: 1.08, 1.62]; N = 11,826), and 15.3% among women with low mid-upper arm circumference (MUAC <23 cm) at enrollment compared to 9.5% among women with MUAC ≥ 23 cm (aRR 1.60 [95% CI: 1.36, 1.87]; N = 9,008). The risk of delivering a baby with LBW was 17.8% among women with both malaria infection and low MUAC at enrollment compared to 8.4% among uninfected women with MUAC ≥ 23 cm (joint aRR 2.13 [95% CI: 1.21, 3.73]; N = 8,152). There was no evidence of synergism (i.e., excess risk due to interaction) between malaria infection and MUAC on the multiplicative (p = 0.5) or additive scale (p = 0.9). Results were similar using body mass index (BMI) as an anthropometric indicator of nutritional status. Meta-regression results indicated that there may be multiplicative interaction between malaria infection at enrollment and low MUAC within studies conducted in Africa; however, this finding was not consistent on the additive scale, when accounting for multiple comparisons, or when using other definitions of malaria and malnutrition. The major limitations of the study included availability of only 2 cross-sectional measurements of malaria and the limited availability of ultrasound-based pregnancy dating to assess impacts on preterm birth and fetal growth in all studies. Conclusions: Pregnant women with malnutrition and malaria infection are at increased risk of LBW compared to women with only 1 risk factor or none, but malaria and malnutrition do not act synergistically.

U2 - 10.1371/journal.pmed.1002373

DO - 10.1371/journal.pmed.1002373

M3 - Journal article

C2 - 28792500

AN - SCOPUS:85028551217

SN - 1549-1277

VL - 14

JO - P L o S Medicine (Online)

JF - P L o S Medicine (Online)

IS - 8

M1 - e1002373

ER -

Malaria, malnutrition, and birthweight: A meta-analysis using individual participant data

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