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Supplementary appendixThis appendix formed part of the original submission and has been peer reviewed. We post it as supplied by the authors.
Supplement to: 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; published online Sept 26. http://dx.doi.org/10.1016/S2214-109X(17)30340-6.
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Webappendix for ‘Quantification of the association between malaria in pregnancy and
stillbirth: a systematic review and meta‐analysis’
Table of contents
1. PRISMA Checklist .......................................................................................................................................... 2
2. Search strategy .............................................................................................................................................. 3
3. Proforma ....................................................................................................................................................... 4
4. Risk of bias assessment ................................................................................................................................. 5
5. Reasons for study exclusion .......................................................................................................................... 7
6. The association between falciparum malaria in pregnancy and perinatal death ......................................... 8
7. Meta‐analyses of the association between falciparum malaria and stillbirth according to the method of malaria detection.................................................................................................................................................. 10
8. Stillbirth proportions in women with no malaria ........................................................................................ 14
9. Funnel plots ................................................................................................................................................. 15
10. Subgroups for meta‐analysis of falciparum malaria detected during pregnancy by the gestational age at detection. ......................................................................................................................................................... 16
11. Meta‐regression ..................................................................................................................................... 17
12. Population attributable fractions ........................................................................................................... 19
13. The association between symptomatic falciparum malaria detected during pregnancy and stillbirth . 21
14. Odds ratio for the association between vivax or falciparum malaria and stillbirth ............................... 22
15. Further acknowledgements ................................................................................................................... 22
References ............................................................................................................................................................ 23
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1. PRISMA Checklist
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2. Search strategy
We searched Scopus, PubMed, and Web of Science for studies published in any language up to and including 28 February 2016, that assessed the association between malaria in pregnancy and birth outcomes, and reported on stillbirth or perinatal death. We searched all fields for stillbirth or perinatal mortality (search terms: stillb*, ‘still b*’, ‘perinatal death*’, ‘perinatal mortality’, ‘f(o)etal loss’, ‘f(o)etal death’) and titles and abstracts for malaria in pregnancy (search terms: pregnan*, malaria, plasmodium]), birth outcomes (search terms: small, birthweight, ‘birth weight’, preterm, prematur*, death*, mortality, growth, miscarr*, abortion, stillb*, ‘still b*’, ‘perinatal death*’, ‘perinatal mortality’, ‘f(o)etal loss’, ‘f(o)etal death’, ‘birth outcome*’) and terms of association or occurrence in population studies (search terms: incidence, prevalence, proportion, risk, rate, association, ratio). Full search strategies for each database are given in Table 1. Table S1. Search strategy
Database Search
Scopus
(TITLE-ABS-KEY(pregnan*) AND TITLE-ABS-KEY(malaria OR plasmodium) AND TITLE-ABS-KEY(small OR birthweight OR "birth weight" OR preterm OR prematur* OR growth OR death* OR mortality OR abortion OR miscarri* OR stillbirth* OR "still birth*" OR stillborn* OR “still born*” OR “birth outcome*” OR "f(o)etal loss" OR "f(o)etal death") AND TITLE-ABS-KEY(incidence OR prevalence OR proportion OR risk OR rate OR associat* OR ratio)) AND ALL(stillbirth* OR "still birth*" OR stillborn* OR “still born*” OR "perinatal death" OR "perinatal mortality" OR "f(o)etal loss" OR "f(o)etal death")
PubMed
((((((stillbirth* OR "still birth*" OR "perinatal death*" OR "perinatal mortality" OR "f(o)etal loss" OR "f(o)etal death" OR stillborn* OR “still born*”)) AND pregnan*[Title/Abstract]) AND (malaria[Title/Abstract] OR plasmodium[Title/Abstract])) AND (small[Title/Abstract] OR birthweight[Title/Abstract] OR "birth weight"[Title/Abstract] OR preterm[Title/Abstract] OR prematur*[Title/Abstract] OR death*[Title/Abstract] OR mortality[Title/Abstract] OR growth[Title/Abstract] OR miscarr*[Title/Abstract] OR abortion[Title/Abstract] OR stillbirth[Title/Abstract] OR "still birth"[Title/Abstract] OR "perinatal death*"[Title/Abstract] OR "perinatal mortality"[Title/Abstract] OR "f(o)etal loss"[Title/Abstract] OR "f(o)etal death"[Title/Abstract] OR stillborn*[Title/Abstract] OR “still born*”[Title/Abstract] OR “birth outcome*”[Title/Abstract])) AND (incidence[Title/Abstract] OR prevalence[Title/Abstract] OR proportion[Title/Abstract] OR risk[Title/Abstract] OR rate[Title/Abstract] OR associat*[Title/Abstract] OR ratio[Title/Abstract]))
African Index Medicus
small OR birthweight OR “birth weight” OR preterm OR premature* OR death* OR mortality OR growth OR miscarr* OR abortion OR stillbirth OR “still birth” OR stillborn OR “still born” OR “birth outcome” [Key Word] AND malaria OR plasmodium [Key Word] AND pregnan* [Key Word]
Web of Science
TI=(pregnan*) AND TI=(malaria OR plasmodium) AND TS=(small OR birthweight OR birth weight OR preterm OR premature* OR death* OR mortality OR growth OR miscarr* OR abortion OR stillbirth OR "still birth" OR stillborn* OR “still born*” OR “birth outcome*” OR "f(o)etal loss" OR "f(o)etal death") AND TS=(incidence OR prevalence OR proportion OR risk OR rate OR associat* OR ratio)
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3. Proforma
OPTION 1: Fill out 2x2 tables
2X2 TABLE (repeat this table for each definition of malaria used in your study)
Definition of malaria*
Species (circle one): falciparum / vivax / either Blood sample (circle one): peripheral / placental / either Method of detection (circle one): PCR / microscopy / RDT / histology / any Time of test/detection (circle one): during pregnancy / at delivery / either Tested (circle one): all women / symptomatic women only / asymptomatic women only
Fill in 2x2 cells with N, not %
Stillborn
Liveborn
TOTAL
Malaria
No malaria
TOTAL *One definition of malaria = any unique combination of species, blood sample, detection method, time of test,
and population tested. A separate 2x2 table should be filled out for each definition of malaria used in the study.
OPTION 2: reanalyse your data and provide estimates for the association between malaria and stillbirth
(preferably odds ratios)
ESTIMATES (repeat this table for each definition of malaria used in your study)
Definition of malaria*
Species (circle one): falciparum / vivax / either Blood sample (circle one): peripheral / placental / either Method of detection (circle one): PCR / microscopy / RDT / histology / any Time of test/detection (circle one): during pregnancy / at delivery / either Tested (circle one): all women / symptomatic women only / asymptomatic women only
Measure of association (e.g. odds ratio): Adjusted variables (if applicable):
Unadj. (95% CI):
Adj. (95% CI): *One definition of malaria = any unique combination of species, blood sample, detection method, time of test,
and population tested. Separate estimates should be provided for each definition of malaria used in the study.
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4. Risk of bias assessment
Risk of bias was assessed for each study by one independent reviewer using the Risk of Bias In Non-randomized Studies – of Interventions (ROBINS-I) assessment tool.1 A second independent reviewer assessed 10 randomly selected studies for inter-reviewer agreement, which was >95%. This tool enables assessment of bias within seven domains: 1) confounding; 2) selection of participants; 3) classification of ‘interventions’ (i.e. exposures); 4) departures from intended ‘interventions’; 5) missing data; 6) measurement of outcomes; 7) and selection of reported results (Additional file 3). Our risk of bias assessment pertains to the malaria-stillbirth association derived from the study, rather than the study itself. Table S2. Risk of bias assessments ‐ minimum criteria for 'Low' risk
Domain Minimum criteria for ‘Low’ risk Comment Confounding Adjusted for relevant confounders and did not adjust for
collinear variables or variables on the causal pathway Many studies were classified as having a ‘serious’ risk of bias due to confounding for reasons that were usually not related to the quality of the study, including:
Inclusion of studies where the primary research question was not related to the association between malaria in pregnancy and stillbirth
Too few stillbirth cases for a formal analysis to be performed
Authors responding to our request for cross-tabulated (i.e. unadjusted) data for malaria in pregnancy and stillbirth.
Selection of participants into the study
Selection of participants into the study that was not based on factors on the causal pathway between malaria in pregnancy and stillbirth, and prospective follow-up of participants from some time before delivery.
Classification of interventions
Confirmation of malaria in pregnancy by PCR, microscopy, RDT, or histology.
All studies were classified as having ‘low’ risk of bias due to classification of the ‘intervention’ (i.e. the exposure, malaria)
Departures from intended interventions
A priori co-interventions (HIV) were balanced across malaria groups, adjusted for in a formal analysis, at a prevalence of <10%, or study enrollment was before 1980.
A ‘co-intervention’ is the equivalent to a potential effect modifier of the association of interest. We identified HIV as an a priori co-intervention for our risk of bias assessments.
Missing data Proportion of missing data was equivalent across malaria groups, multiple imputation was used to account for missing data, or percentage of missing data was <10%.
Measurement of outcomes
Stated a gestational age and/or birthweight threshold that differentiated stillbirths from miscarriages.
Selection of the reported result
Have a single definition/measurement of stillbirth, absence of selective reporting of the association between malaria in pregnancy and stillbirth due to multiple analyses or sub-group analyses.
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Figure S1. Risk of bias assessment. Black – critical risk; red – serious risk; orange – moderate risk; green – low risk; hollow circle – no information.
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5. Reasons for study exclusion
Titles and abstracts of studies identified in searches were screened for relevance. Full texts were then examined for compliance with the inclusion and exclusion criteria. After excluding studies based on titles and abstracts only, full texts of 455 studies were considered for inclusion. 332 records did not meet the inclusion criteria: Studies Reason 154 Did not mention key terms related to stillbirth or perinatal mortality (of the current pregnancy) in either the methods or results
sections 2–155 44 Data already captured by our review from another publication 156–199 43 Did not confirm malaria using either PCR, microscopy, RDT, or placental histology 200–242 36 Only included women with an underlying condition (e.g. fever) (excluding HIV) 243–277 12 Only included women with malaria 278–289 10 Not original research articles (e.g. reviews, commentaries, letters to the editor) 290–299 8 Case-control studies of a pregnancy outcome that was not stillbirth 300–307 6 RCT of non-malaria interventions 308–313 5 Considered only a sub-set of stillbirths, e.g. intrapartum deaths 314–319 3 Could not locate the full text 320–322 2 Did not report birth outcomes 323,324 2 Not conducted in malaria-endemic regions 325,326 1 Only included stillborns 327 1 Stillbirth was within a composite variable for ‘adverse perinatal outcome’ which included other adverse outcomes 328 1 Did not differentiate miscarriage from stillbirth 329 1 Case-control study of stillbirth, but controls were liveborn newborns, >2500g, and alive at 28 days 330 1 Used aggregate rather than individual-level data 331 1 Only mentioned stillbirth in a quote from focus group discussions on the benefits of IPTp 332 1 Selected women into the study so that there would be an equal number of stillbirths in the malaria and no malaria groups 333
Studies that potentially met inclusion criteria and were excluded after author contact:
8 studies excluded after failure to obtain author contact information334–341 13 studies excluded after authors did not respond after three email attempts342–354 3 studies did not meet inclusion criteria following clarification with authors355–357 22 studies excluded because authors informed us that they could not provide data358–379 13 studies excluded because authors did not meet deadline for providing data380–392
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6. The association between falciparum malaria in pregnancy and perinatal death
Table S3. Study characteristics (perinatal death)
Study ID [data source*] Country
Study Design
Perinatal death definition**
% falciparum MiP****
Total N*****
Deaths******
Adam et al. 2007393 [1] Sudan
X‐sectional 28; 7
[Includes PCR detection] 578 46
D'Alessandro et al. 1996394 [4]
The Gambia RCT DNS; 7 241 515 38
El Ghazali et al. 2003395 [2] Sudan Cohort 28; 7
[Only symptomatic
tested] 209 4
McDermott et al. 1996396 [1] Malawi Cohort 28; 7 213 2586 111
N'Dao et al. 2006397 [1] Senegal
X‐sectional DNS; DNS 93 8273 DNS
Nyirjesy et al. 1993398 [2] Zaire
X‐sectional DNS; 2 282 302 6
Valea et al. 2010399 [1]
Burkina Faso RCT 28; DNS 171 1296 19
Weiner et al. 2003400 [1] Kenya
X‐sectional DNS; 7 473 910 108
DNS – Did not state. 1Data sources: 1: measure of association reported in publication (all odds ratios); 2: cross‐
tabulation of malaria and perinatal death reported in publication; 3: measure of association provided by
author (all odds ratios); 4: cross‐tabulation of malaria and stillbirth/perinatal death provided by author; cross‐
tabulation or odds ratio of malaria and perinatal death provided by key author. RCT: randomised controlled
trial; X‐sectional: cross‐sectional. 2Weeks’ gestation used to differentiate a stillbirth from a miscarriage; and
days of life to define the perinatal period. 3P. falciparum endemicity categorised as low, intermediate, or high
using information in the published papers or using the Malaria Atlas Project Data Explorer if insufficient
information was given in papers and enrolment started after 2005 (see Methods for more information on
classification). 4Proportion of women with falciparum MiP (malaria in pregnancy) detected by light microscopy,
rapid diagnostic test, or placental histology: subscript 1 – during pregnancy; subscript 2 – at delivery
(peripheral sample); subscript 3 – at delivery (placental sample). 5Total number of pregnant women enrolled,
including women with missing exposure or outcome data. 6Total number of perinatal deaths recorded. “Fresh
stillbirths and deaths in the delivery room.”
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Figure S2. Odds ratios (95% CI) for the association between falciparum malaria and perinatal death. Pooled
odds ratios are calculated for malaria detected during pregnancy or at delivery. Method of detection: All light
microscopy (LM) except for Weiner 2003 (histology), Adam 2007 (LM or histology), and McDermott 1996 (LM
or histology). D’Alessandro 1996 also provided an estimate for malaria detected at delivery in peripheral blood
(OR: 0.96; 95% CI: 0.21, 4.28), and was omitted from the meta‐analysis because detection in placental samples
was the most common method within this analysis. It should be noted that heterogeneity across studies for
malaria detected at delivery was very high.
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7. Meta‐analyses of the association between falciparum malaria and stillbirth according to the method of malaria detection
Figure S3. Odds ratios (95% CI) for the association between peripheral falciparum malaria during pregnancy
and stillbirth. n = stillbirths. N = total births. MiP: malaria in pregnancy. *Cross‐tabulation unknown. PCR:
polymerase chain reaction. De Beaudrap 2013: parasites detected by PCR, light microscopy, or rapid diagnostic
test. Kalilani‐Phiri 2013 provided two estimates for 1) malaria detected by light microscopy, and 2) malaria
detected by PCR. Klement 2014 contributed two cohorts: 1) HIV positive women receiving intermittent
preventative therapy in pregnancy – sulphadoxine‐pyrimethamine (IPTp‐SP) and 2) HIV positive women
receiving co‐trimoxazole (CMX). Luntamo 2010 contributed two cohorts: 1) HIV positive women receiving IPTp‐
SP and 2) HIV negative women receiving IPTp‐SP. Huynh 2011: Plasmodium species was not specified, but
assumed to be P. falciparum because the study was conducted in an area of unstable P. vivax transmission and
high Duffy negativity. De Beaudrap 2013: Estimates were not species‐specific, however only 4.5% of all
Plasmodium spp. infections in the cohort were not P. falciparum. Klement 2014 and Singh 1998: malaria
exposure may have also been at delivery (included in this meta‐analysis because separate estimates were not
provided for malaria during pregnancy and malaria at delivery, and the studies were designed to detect
malaria during pregnancy). Klement 2014 used rapid diagnostic tests if light microscopy was not available.
Briand 2009 provided estimates for malaria detected at enrolment (~22 weeks) (OR: 0.82 [95% CI: 0.048,
13.99]), and malaria detected at the second IPTp administration visit (~31 weeks) (OR: 3.03 [95% CI: 0.37,
24.48]), which we pooled to obtain a single odds ratio.
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Figure S4. Odds ratios (95% CI) for the association between falciparum malaria at delivery in peripheral
blood and stillbirth. n = stillbirths. N = total births. MiP: malaria in pregnancy. *Cross‐tabulation unknown.
Studies contributing estimates to more than one meta‐analysis provided separate estimates for malaria
detected by more than one diagnostic method. De Beaudrap 2013: parasites detected by PCR, light
microscopy, or rapid diagnostic test. McGregor 1983 contributed two cohorts: 1) women living in rural areas
and 2) women living in urban areas. Arinaitwe 2013, De Beaudrap 2013, Huynh 2011, Watson‐Jones 2007,
Sule‐Odu 2002, Axemo 1995, Lamikanra 1993: Plasmodium species was not specified, but assumed to be P.
falciparum because the study was conducted in an area of unstable P. vivax transmission and high Duffy
negativity. All studies included all women, regardless of the presence of symptoms, except for Mbonye 2008
(asymptomatic women only).
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Figure S5. Odds ratios (95% CI) for the association between falciparum malaria at delivery detected in
placental samples and stillbirth. n = stillbirths. N = total births. MiP: malaria in pregnancy. *Cross‐tabulation
unknown. Studies contributing estimates to more than one meta‐analysis provided separate estimates for
malaria detected by more than one diagnostic method. McGregor 1983 contributed two cohorts: 1) women
living in rural areas and 2) women living in urban areas. Arinaitwe 2013, Huynh 2011, Watson‐Jones 2007,
Lamikanra 1993: Plasmodium species was not specified, but assumed to be P. falciparum because the study
was conducted in an area of unstable P. vivax transmission and high Duffy negativity. Ahmed 2014 and
McGregor 1983: Estimates were not species‐specific, however only 5% and <1% of all Plasmodium spp.
infections in the cohort were not P. falciparum, respectively. Watson‐Jones 2007 reported odds ratios for
active (OR: 7.74 [95% CI: 1.80, 32.70]), active chronic (OR: 1.92 [95% CI: 0.50, 6.90]), and past chronic placental
infection (OR: 1.84 [95% CI: 0.60, 5.20]), which we pooled to obtain a single odds ratio. Hamer 2007 provided
odds ratios for acute/active (OR: 2.09 [95% CI: 0.46, 9.53]), and past infection (OR: 0.19 [95% CI: 0.01, 3.38]),
which we pooled to obtain a single odds ratio. Mace 2015 provided odds ratios for Class 1‐3 [parasites
present] (OR: 2.67 [95% CI: 0.52, 13.59]), and Class 4 [past infection] (OR: 0.98 [95% CI: 0.20, 4.95]), which we
pooled to obtain a single odds ratio. Gutman 2013: estimate is for acute/chronic placental malaria. All studies
13
included all women, regardless of the presence of symptoms, except for Mbonye 2015 (asymptomatic women
only).
14
8. Stillbirth proportions in women with no malaria
Figure 6. Stillbirth proportions in women with no malaria in pregnancy. A pooled proportion was not
calculated because of high between‐study heterogeneity (I2 = 90%). PCR: polymerase chain reaction; RDT:
rapid diagnostic test; LM: light microscopy. *“No malaria” was defined according to the most sensitive
diagnostic method available for each study. Most to least sensitive diagnostic method: PCR; placental
histology; RDT, light microscopy. No malaria at delivery was used, unless samples were only taken during
pregnancy. For each diagnostic method, placental samples were prioritised over peripheral samples.
Africa
Asia
The Americas
Author, Year [Ref No.]
Ako‐Nai 2013 [14]Anagnos 1986 [16]Arinaitwe 2013 [17]Asundep 2014 [18]Ayisi 2003 [20]Braun 2015 [21]Briand 2009 [22]De Beaudrap 2013 [26]Desai 2015 [27]Diallo 2007 [28]Fouelifack 2015 [29]Geidam 2011 [30]Gutman 2013 [31]Gutman 2015 [32]Hamer 2007 [33]Huynh 2011 [35]Kakuru 2016 [36]Kalanda 2006 [37]Kalilani‐Phiri 2013 [38]Kasumba 2000 [39]Kayentao 2005 [40]Kayentao 2007 [41]Klement 2014 [42]Klement 2014 [42]Lamikanra 1993 [43]Luntamo 2010 [44]Mace 2015 [45]Maiga 2011 [46]Mbonye 2008 [47]Mbonye 2015 [48]McGregor 1983 [49]McGregor 1983 [49]Natureeba 2014 [51]Newman 2003 [52]Obieche 2015 [53]Okoko 2002 [54]Olliaro 2008 [55]Osman 2001 [56]Rulisa 2012 [58]Sule‐Odu 2002 [63]Tagbor 2015 [64]Ticconi 2003 [66]Valente 2011 [67]Van Spronsen 2012 [68]Watson‐Jones 2007 [69]Wort 2006 [70]Wort 2007 [71]
Ahmed 2014 [13]Das 2000 [25]Hamer 2009 [34]Moore 2017 [50]Poespoprodjo 2015 [57]Singh 1998 [59]Singh 2001 [60]Singh 2014 [61]Singh 2015 [62]
Carles 1998 [23]Carmona‐Fonseca 2009 [24]
No malaria defini; on*
LM during pregnancyPlacental histologyPCR at deliveryRDT at deliveryLM at deliveryPCR at deliveryLM at deliveryPCR at deliveryPCR at deliveryLM at deliveryLM during pregnancyLM during pregnancyPCR at deliveryPCR at deliveryPlacental histologyLM at deliveryPlacental histologyLM at deliveryPCR at deliveryLM at deliveryLM at deliveryLM at deliveryPlacental histologyPlacental histologyLM at deliveryPCR at deliveryPlacental histologyLM at deliveryLM at deliveryPCR at deliveryPlacental histologyPlacental histologyPCR at deliveryLM at deliveryRDT at deliveryPlacental histologyLM during pregnancyLM at deliveryLM during pregnancyLM at deliveryLM at deliveryLM at deliveryPCR at deliveryLM at deliveryPlacental histologyLM at deliveryLM at delivery
Placental histologyLM during pregnancyRDT at deliveryLM during pregnancyLM at deliveryLM during pregnancyLM during pregnancyLM during pregnancyRDT at delivery
LM during pregnancyLM at delivery
Prevalence [95% CI]
5.00 [0.52, 34.45]8.33 [2.87, 21.83]1.72 [0.84, 3.52]0.00 [0.00, 0.67]1.09 [0.72, 1.66][No 2x2 data]1.28 [0.65, 2.50]2.92 [1.93, 4.38]3.58 [2.10, 6.03]0.20 [0.02, 1.85]3.15 [1.72, 5.71][No 2x2 data]0.62 [0.11, 3.43]0.41 [0.16, 1.04]1.55 [0.60, 3.92]0.47 [0.16, 1.39]2.08 [0.37, 10.90]0.00 [0.00, 0.32]2.05 [0.88, 4.71]3.59 [2.28, 5.61]4.89 [2.88, 8.18]4.55 [2.73, 7.48]0.93 [0.10, 8.27]4.29 [1.47, 11.86]6.12 [2.84, 12.72]3.06 [1.05, 8.62]1.57 [0.72, 3.38]1.66 [0.88, 3.13]1.94 [1.12, 3.37]0.93 [0.53, 1.61]7.60 [6.64, 8.70]4.50 [3.77, 5.38]2.17 [1.00, 4.66]2.71 [1.80, 4.07]1.00 [0.27, 3.57]6.54 [3.59, 11.61]3.68 [2.40, 5.62][No 2x2 data]1.25 [0.13, 10.91]2.59 [1.45, 4.59]4.08 [2.96, 5.60]1.14 [0.60, 2.15]3.88 [2.47, 6.05]1.00 [0.10, 8.89][No 2x2 data]4.72 [3.72, 5.98]1.58 [0.86, 2.89]
3.86 [2.46, 6.02]2.29 [0.78, 6.52]4.08 [2.84, 5.84]0.89 [0.81, 0.98]2.62 [2.22, 3.10]0.44 [0.08, 2.45]0.35 [0.04, 3.28]3.05 [1.19, 7.59]2.35 [1.56, 3.54]
1.19 [0.89, 1.59]5.88 [2.88, 11.65]
0 1 2 3 4 5 6 7 8Prevalence (%) [95% CI]
15
9. Funnel plots
Figure S7. Funnel plot of the studies included in the meta‐analysis of the association between falciparum
malaria detected during pregnancy and stillbirth. The x‐axis is on a log scale. Continuous vertical line: no
effect; dashed line: upper and lower 95% confidence limits; orange line: regression line of effect estimates on
their standard errors. P‐values are from Egger’s test for asymmetry. Bias due to small‐study effects was only
assessed for meta‐analyses with low between‐study variance more than 10 contributing estimates.
Figure S8. Funnel plot of the studies included in the meta‐analysis of the association between falciparum
malaria detected in peripheral blood or placental samples at delivery and stillbirth. The x‐axis is on a log
scale. Continuous vertical line: no effect; dashed line: upper and lower 95% confidence limits; orange line:
regression line of effect estimates on their standard errors. P‐values are from Egger’s test for asymmetry. Bias
due to small‐study effects was only assessed for meta‐analyses with low between‐study variance more than 10
contributing estimates.
p = 0.763
0.5
11.5
2Standard error o
f log(odds ra9o)
.1 1 10 100Odds ra9o
p = 0.3190
0.5
11.5
2Standard error o
f log(odds ra8o)
.1 1 10 100Odds ra8o
Peripheral
p = 0.0490
0.5
11.5
2Standard error o
f log(odds ra8o)
.1 1 10 100Odds ra8o
Placental
16
10. Subgroups for meta‐analysis of falciparum malaria detected during pregnancy by the gestational age at detection.
Estimates included in subgroup for malaria detected and treated before 30 weeks’ gestation
Gestational age range of malaria detection
Briand 2009* 16‐28 weeks
Luntamo (HIV+) 14‐26 weeks
Luntamo (HIV‐) 14‐26 weeks
Moore 2017† <28 weeks
Osman 2001 <21 weeks
Tagbor 2015 (Burkina Faso) 16‐30 weeks
Tagbor 2015 (Ghana) 16‐30 weeks
Tagbor 2015 (Mali) 16‐30 weeks
Tagbor 2015 (The Gambia) 16‐30 weeks
Estimates included in subgroup for malaria detected and treated at any time, or an unspecified time‡, during pregnancy
Ako‐Nai 2013
Briand 2009*
Carles 1998
De Beaudrap 2013
Huynh 2011
Kalanda 2006
Kalilani‐Phiri 2013
Klement 2014 (CMX)
Klement 2014 (IPTp‐SP)
Moore 2017†
Singh 1998
Singh 2001 *Pooled odds ratio combining estimates for malaria detected at enrolment (16‐28 weeks) and malaria detected
at 2nd IPTp administration (~31 weeks) was included in the primary analysis of falciparum malaria during
pregnancy, and in the subgroup of 12 estimates for malaria detected at any time or an unspecified time during
pregnancy. †Unstratified estimate for malaria detected at any time during pregnancy was included in the
primary analysis of falciparum malaria during pregnancy, and in the subgroup of 12 estimates for malaria
detected at any time or an unspecified time during pregnancy. ‡These studies may have information on when
during pregnancy malaria was detected, however this information was not available to us in relation to
stillbirth.
17
11. Meta‐regression Table S4. Meta‐regression of the association between falciparum malaria in pregnancy and stillbirth
Covariate No. of ORs
I2, %* τ2 OR (95% CI; p-value) Univariable Ratio of ORs
(95% CI); p-value Exposure: falciparum malaria detected in peripheral blood during pregnancy [Figure 2]; I2 = 23.5% No covariates 19 23.4 0.064 1.47 (1.10, 1.96); 0.012 P. falciparum endemicity† 6.5 0.013
High 10 1.16 (0.83, 1.62); 0.365 Referent Low-to-intermediate 9 1.88 (1.35, 2.62); 0.001 1.62 (1.02, 2.60); 0.044
Stillbirth definition‡ 22.7 0.091 No definition provided 9 1.17 (0.72, 1.92); 0.496 Referent 20-24 weeks 4 1.79 (0.90, 3.58); 0.092 1.53 (0.65, 3.56); 0.305 28 weeks 6 1.65 (1.03, 2.65); 0.040 1.40 (0.71, 2.78); 0.307
Ultrasound§ 21.6 0.054 No 12 1.30 (0.86, 1.94); 0.195 Referent Yes 7 1.67 (1.11, 2.51); 0.018 1.29 (0.72, 2.29); 0.371
Maximum enrolment GA¶ 14.8 0.024 <28 weeks 4 1.19 (0.57, 2.47); 0.629 Referent 28 weeks 14 1.42 (1.07, 1.89); 0.018 1.20 (0.55, 2.63); 0.631 At delivery 1 3.64 (1.30, 10.20); 0.017 3.07 (0.87, 10.87); 0.078
Study design 12.9 0.019 Cohort 9 1.48 (1.07, 2.05); 0.021 Referent RCT 9 1.25 (0.82, 1.91); 0.279 0.84 (0.49, 1.44); 0.511 Retrospective cohort 1 3.64 (1.31, 10.11); 0.016 2.46 (0.84, 7.17); 0.094
Enrolment start year|| 18 13.2 0.061 1.47 (1.10, 1.96); 0.013 0.97 (0.95, 1.00); 0.071 Exposure: falciparum malaria detected in peripheral blood at delivery [Figure 3]; I2 = 26.1% No covariates 34 26.4 0.101 1.81 (1.41, 2.32); <0.001 P. falciparum endemicity† 0.0 0.000
High 19 1.32 (1.04, 1.68); 0.027 Referent Low-to-intermediate 11 2.59 (1.92, 3.50); <0.001 1.96 (1.34, 2.89); 0.001
Stillbirth definition‡ 10.7 0.062 No definition provided 16 1.47 (1.04, 2.06); 0.028 Referent 20-24 weeks 8 1.66 (1.06, 2.59); 0.027 1.13 (0.65, 1.98); 0.658 28 weeks 10 2.70 (1.74, 4.20); <0.001 1.84 (1.05, 3.21); 0.033
Ultrasound§ 27.9 0.105 No 27 1.75 (1.34, 2.30); <0.001 Referent Yes 7 2.15 (1.13, 4.12); 0.022 1.23 (0.61, 2.48); 0.555
Maximum enrolment GA¶ 26.0 0.099 <28 weeks 6 1.68 (0.81, 3.49); 0.156 Referent 28 weeks 14 1.61 (1.03, 2.52); 0.036 0.96 (0.41, 2.25); 0.923 At delivery 14 1.95 (1.40, 2.71); <0.001 1.16 (0.52, 2.58); 0.708
Study design 18.0 0.070 Cohort 7 1.53 (0.90, 2.61); 0.109 Referent Cross-sectional 12 1.71 (1.17, 2.49); 0.007 1.11 (0.58, 2.13); 0.741 RCT 13 1.66 (0.99, 2.80); 0.056 1.08 (0.51, 2.27); 0.831 Retrospective cohort 2 2.62 (1.50, 4.60); 0.001 1.71 (0.79, 3.70); 0.166
Enrolment start year|| 32 25.1 0.096 1.75 (1.34, 2.28); <0.001 1.02 (0.98, 1.05); 0.321 Exposure: falciparum malaria detected in placental samples at delivery [Figure 3]; I2 = 33.6% No covariates 31 34.6 0.147 1.96 (1.47, 2.62); <0.001 P. falciparum endemicity† 15.6 0.039
High 18 1.49 (1.12, 1.98); 0.008 Referent Low-to-intermediate 10 3.11 (1.83, 5.30); <0.001 2.09 (1.14, 3.82); 0.019
Stillbirth definition‡ 0.0 0.019 No definition provided 17 1.38 (1.06, 1.78); 0.017 Referent 20-24 weeks 8 2.34 (1.60, 3.43); <0.001 1.70 (1.07, 2.70); 0.026 28 weeks 6 7.16 (2.94, 17.44); <0.001 5.20 (2.06, 13.14); 0.001
Ultrasound§ 26.1 0.126 No 26 1.80 (1.33, 2.44); <0.001 Referent Yes 5 3.22 (1.50, 6.90); 0.004 1.79 (0.79, 4.06); 0.157
Maximum enrolment GA¶ 33.3 0.167 <28 weeks 5 1.51 (0.55, 4.17); 0.409 Referent 28 weeks 9 2.22 (1.22, 4.03); 0.011 1.46 (0.45, 4.75); 0.511 At delivery 17 1.96 (1.36, 2.83); 0.001 1.29 (0.44, 3.80); 0.628
Study design 34.1 0.179 Cohort 6 2.18 (1.13, 4.19); 0.022 Referent Cross-sectional 17 1.97 (1.35, 2.86); 0.001 0.90 (0.43, 1.92); 0.786 RCT 8 1.75 (0.74, 4.12); 0.194 0.80 (0.27, 2.36); 0.679
Enrolment start year|| 28 10.1 0.050 2.21 (1.63, 2.99); <0.001 1.03 (0.98, 1.07); 0.257
18
OR: odds ratio. GA: gestational age. RCT: randomised controlled trail. To give an indication of how much
variation each covariate explains, the between‐study variance (τ2) from a meta‐regression model with no
covariates was compared to τ2 from univariable meta‐regression models. *Discrepancies between I2 from
meta‐analyses and I2 from meta‐regressions due to slight differences in estimators. †P. falciparum endemicity
categorised as low, intermediate, or high using information in the published papers (N = 42) or the Malaria
Atlas Project Data Explorer if insufficient information was given in papers and enrolment started after 2005 (N
= 9) (see Methods for more information); low and intermediate endemicity were grouped together because
too few studies were in areas of low endemicity; endemicity could not be determined in 8 of 59 studies with
enrolment starting before or during 2005. Of the 9 studies classified using the Malaria Atlas Project Data
Explorer (which uses 2010 estimates), enrolment start year (number of studies) was: 2006 (1), 2007 (2), 2009
(1), 2010 (1), 2011 (2), 2012 (1), 2014 (1). ‡Weeks’ gestation used to differentiate a fetal death as a miscarriage
or stillbirth. §Ultrasound used to estimate GA; referent group is studies that estimated GA using fundal height,
last menstrual period, Ballard or Dubowitz assessments, or did not specify a method. ¶Maximum GA at
enrolment as per study inclusion criteria. ||Years since 2000; OR is for the estimated association for studies
starting enrolment in 2000; ratio of OR is for the estimated change in the association per year increase in
enrolment start year.
19
12. Population attributable fractions
A. Assuming all malaria in pregnancy (MiP) goes unresolved prior to delivery This calculation uses the population prevalence of malaria detected in peripheral blood, and the pooled odds ratio (OR) for the association between falciparum MiP detected in peripheral blood at delivery and stillbirth. Because the association for MiP at delivery is used, this assumes that no MiP is resolved through antimalarial treatment prior to delivery. PAFs were calculated using the formula: [prevalence x (OR – 1)]/ [prevalence x (OR – 1) + 1]. 95% confidence intervals (CIs) were calculated using the 95% CIs of the OR. For low-to-intermediate P. falciparum endemicity settings (prevalence <50%) the OR is 2.59 [95% CI: 1.92, 3.50]. For high P. falciparum endemicity settings (prevalence 50%) the OR is 1.32 [95% CI: 1.04, 1.68]. ORs were derived from meta-regression (Appendix 11).
Figure S9. The proportion of stillbirths attributed to falciparum malaria at varying population prevalence of
falciparum malaria, assuming all malaria in pregnancy goes unresolved prior to delivery. PAF: population
attributable fractions. CI: confidence interval. Calculated using the pooled odds ratio for the association
between falciparum malaria in pregnancy detected in peripheral blood at delivery and stillbirth in either low‐
to‐intermediate (prevalence <50%) or high endemicity (prevalence 50%) settings. PAF range in Africa was
calculated using the lower and upper CI limits for OR and prevalence estimates in malaria‐endemic Africa
(overall prevalence 16.20% [95% CI: 14.24, 19.02]).
020
4060
Pop
ulat
ion
Att
ribu
tabl
e F
ract
ion
(%)
0 20 40 60 80 100Population prevalence (%)
PAF, low-to-intermediate endemcity PAF, high endemcity
PAF range in Africa 95% CI
20
B. Assuming all malaria in pregnancy (MiP) is treated during pregnancy, regardless of the presence of symptoms
This calculation uses the population prevalence of malaria detected in peripheral blood, and the odds ratio (OR) for the association between falciparum MiP detected in peripheral blood and treated during pregnancy and stillbirth. Because the association for MiP during pregnancy is used, this assumes that all MiP is detected and treated during pregnancy, regardless of the presence of symptoms. PAFs were calculated using the formula: [prevalence x (OR – 1)]/ [prevalence x (OR – 1) + 1]. 95% confidence intervals (CIs) were calculated using the 95% CIs of the OR. For low-to-intermediate P. falciparum endemicity settings (prevalence <50%) the OR is 1.88 [95% CI: 1.35, 2.62]. For high P. falciparum endemicity
settings (prevalence 50%) the OR is 1.16 [95% CI: 0.83, 1.62]. ORs were derived from meta-regression (Appendix 11).
Figure S10. The proportion of stillbirths attributed to falciparum malaria at varying population prevalence of
falciparum malaria, assuming all malaria in pregnancy is treated during pregnancy. PAF: population
attributable fractions. CI: confidence interval. Calculated using the pooled odds ratio for the association
between falciparum malaria in pregnancy detected in peripheral blood during pregnancy and stillbirth in either
low‐to‐intermediate (prevalence <50%) or high endemicity (prevalence 50%) settings. PAF range in Africa was
calculated using the lower and upper CI limits for OR and prevalence estimates in malaria‐endemic Africa
(overall prevalence 16.20% [95% CI: 14.24, 19.02]).
020
40
60
Popula+on A/ributable
Frac+on (%
)
0 20 40 60 80 100Popula+on prevalence (%)
PAF, low‐to‐intermediate endemcity PAF, high endemcity
PAF range in Africa 95% CI
21
13. The association between symptomatic falciparum malaria detected during pregnancy and stillbirth
Figure S11. Odds ratios (95% CI) for the association between peripheral symptomatic falciparum malaria
during pregnancy and stillbirth. Detection methods: all light microscopy (LM), except for Desai 2015 – LM or
rapid diagnostic test. Olliaro 2008 contributed two cohorts – pre‐ and post‐ introduction of intermittent
preventative therapy in pregnancy – sulphadoxine‐pyrimethamine (IPTp‐SP). Huynh 2011: Plasmodium species
was not specified, but assumed to be P. falciparum because the study was conducted in an area of unstable P.
vivax transmission and high Duffy negativity. Fouelifack 2015: malaria exposure may have also been at delivery
(included in this meta‐analysis because separate estimates were not provided for malaria during pregnancy
and malaria at delivery, and the studies were designed to detect malaria during pregnancy).
Tes$ng symptoma$c women
Falciparum malaria during pregnancy
Author, Year (Ref No.)
Desai 2015 [27]
Fouelifack 2015 [29]
Geidam 2011 [30]
Huynh 2011 (SymptomaBc) [35]
Moore 2017 (SymptomaBc) [50]
Olliaro 2008 (post‐IPTp‐SP) [55]
Olliaro 2008 (pre‐IPTp‐SP) [55]
Rulisa 2012 [58]
Subtotal (I²=19.3%, p = 0.28)
1/55
2/145
*
4/110
*
0/5
1/8
1/39
16/401
10/317
*
28/758
*
12/379
20/543
0/39
OR (95% CI)
0.45 (0.06, 3.43)
0.43 (0.09, 1.99)
0.77 (0.23, 13.60)
0.98 (0.34, 2.86)
2.16 (1.51, 3.09)
2.67 (0.14, 51.04)
3.74 (0.44, 31.83)
3.08 (0.12, 77.91)
1.43 (0.84, 2.42)
0.2 0.5 1.0 2.0 4.0 8.0 16.0Odds Ra$o
22
14. Odds ratio for the association between vivax or falciparum malaria and stillbirth
Figure S12. Odds ratio (95% CI) for the association between vivax or falciparum malaria and stillbirth. Pooled
odds ratios are calculated for malaria detected in peripheral and placental blood. Detection methods: All
light microscopy (LM) except for Hamer 2009 and Singh 2015: LM or RDT. Amoa 1998 only tested symptomatic
women for malaria, rather than all women. Proportion of Plasmodium spp. infections that were P. vivax:
Hamer 2009 – 47%; Newman 2003 – 46%; Das 2000 – 30%; Singh 2015 – 36%; Amoa 1998 – not specified. All
estimates are for malaria detected at at delivery except for Das 2000 (during pregnancy).
15. Further acknowledgements
In addition to those listed in the Acknowledgements section of the main paper, we also thank the following
authors for their email correspondence and provision of data: Leo Lanoie, Don Connor, Anthonia O Obieche,
Babalola Adeyemi, Harry Tagbor, James Berkley, Marianne Munene, Daniel Chandramohan, Elise Klement,
Ghislain K. Koura, Bianor Valente, Jaime Carmona-Fonseca, Jeanne McDermott, Julie Gutman, Laurent Brutus,
Pisake Lumbiganon, Neeru Singh, David Mwakazanga, Piero Luigi Olliaro, Raquel González, Richard Steketee,
Robert Newman, Theonest Mutabingwa, and Umberto D'Alessandro.
Peripheral
Placental
Vivax or falciparum malaria during pregnancy or at deliveryAuthor, Year (Ref No.)
Amoa 1998 [15]Das 2000 [25]
Subtotal (I²=0.0%, p = 0.51)
Hamer 2009 [34]Newman 2003 [52]Singh 2015 [62]
Subtotal (I²=23.7%, p = 0.27)
MiP (n/N)
46/60
3/66
2/174/21
1/31
No MiP (n/N)
268/569
3/131
28/68622/812
22/935
OR (95% CI)
3.69 (1.92, 7.21)2.03 (0.40, 10.35)
3.39 (1.83, 6.26)
3.13 (0.68, 14.37)8.45 (2.63, 27.19)1.38 (0.18, 10.60)
4.24 (1.56, 11.47)
0.5 1.0 2.0 4.0 8.0 16.0Odds RaQo
23
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