|Malaria in pregnancy: the difficulties in measuring birthweight.|
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|PMID: 21332632 Owner: NLM Status: MEDLINE|
|Recommendations for interventions to control malaria in pregnancy are often based on studies using birthweight as the primary endpoint. Differences in birthweight may be attributable partly to methodological difficulties. We performed a structured search of the literature using 'malaria', 'pregnancy' and 'birth weight' as search terms. Of the clinical trials reporting birthweight, only 33% (14/43) gave information about the timing of the measurement and details on the scales used. Seventy seven per cent explained how gestational age was estimated. We propose a standardised method for the measurement and reporting of birthweight in future studies.|
|M J Rijken; J A Rijken; A T Papageorghiou; S H Kennedy; G H A Visser; F Nosten; R McGready|
|Type: Journal Article; Research Support, Non-U.S. Gov't; Review Date: 2011-02-18|
|Title: BJOG : an international journal of obstetrics and gynaecology Volume: 118 ISSN: 1471-0528 ISO Abbreviation: BJOG Publication Date: 2011 May|
|Created Date: 2011-04-12 Completed Date: 2011-09-13 Revised Date: 2013-06-30|
Medline Journal Info:
|Nlm Unique ID: 100935741 Medline TA: BJOG Country: England|
|Languages: eng Pagination: 671-8 Citation Subset: AIM; IM|
|© 2011 The Authors BJOG An International Journal of Obstetrics and Gynaecology © 2011 RCOG.|
|Shoklo Malaria Research Unit, Mae Sot, Tak, Thailand. email@example.com|
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Confounding Factors (Epidemiology)
Malaria / physiopathology*
Pregnancy Complications, Parasitic / physiopathology*
Journal ID (nlm-ta): BJOG
Journal ID (publisher-id): bjo
Publisher: Blackwell Publishing Ltd
BJOG An International Journal of Obstetrics and Gynaecology © 2011 RCOG
Accepted Day: 02 Month: 12 Year: 2010
Print publication date: Month: 5 Year: 2011
Electronic publication date: Day: 18 Month: 2 Year: 2011
Volume: 118 Issue: 6
First Page: 671 Last Page: 678
PubMed Id: 21332632
|Malaria in pregnancy: the difficulties in measuring birthweight|
aShoklo Malaria Research UnitMae Sot, Tak, Thailand
bDepartment of Obstetrics, University Medical Centre Utrecht Utrechtthe Netherlands
cNuffield Department of Obstetrics and Gynaecology, John Radcliffe HospitalOxford, UK
dCentre for Clinical Vaccinology and Tropical Medicine, Nuffield Department of Clinical Medicine, John Radcliffe Hospital, University of OxfordOxford, UK
eFaculty of Tropical Medicine, Mahidol University BangkokThailand
|Correspondence: Dr MJ Rijken, Shoklo Malaria Research Unit, PO Box 46, Mae Sot, Tak 63110, Thailand. Email firstname.lastname@example.org
Re-use of this article is permitted in accordance with the Terms and Conditions set out at http://wileyonlinelibrary.com/onlineopen#OnlineOpen_Terms
Malaria in pregnancy has a major impact on the health of the mother and fetus. In endemic areas, malaria is estimated to be responsible for 20% of low-birthweight (LBW) infants, the greatest single risk factor for infant mortality.1–3 However, malaria can cause both intrauterine growth restriction (IUGR), related to the sequestration of malaria parasites in the placenta, and preterm labour (PTL), which is associated with symptomatic maternal illness in the third trimester. IUGR and PTL can be distinguished only if the gestational age is known with some accuracy.4–6 This can be difficult in resource-poor settings. Many published clinical trials on maternal malaria have recruited women at the time of delivery, and birthweight (but not IUGR or PTL) has been the major endpoint. Different types of intervention may have different impacts on IUGR and PTL.
In this article, we review the methods used to obtain and report birthweight in studies of malaria during pregnancy. We also propose a systematic method for the reporting of birth outcomes, with an emphasis on studies in resource-poor settings.
A Medline (PubMed) search was performed with the search terms ‘malaria’ AND ‘pregnancy’ AND ‘birth weight’ using a combination of MeSH headings and keywords. The search was not designed to identify all studies on malaria in pregnancy, but to analyse those that included birthweight and malaria as outcomes. Only trials that specifically used birthweight as the main outcome were included.
The search was limited to humans, clinical trials, randomised controlled trials (RCTs), case reports and English language articles from 1 January 1966 to 23 July 2009. Full articles of all citations resulting from this search were obtained. We scrutinised all articles for details of the methodology used to obtain birthweight. Two investigators independently performed eligibility assessment and, if disagreements were not resolved by consensus, a decision was made by a third author. Data from the included studies were extracted and entered onto an Excel spreadsheet for collation and analysis. Information on the type of scales, precision of scales, scale calibration, day of weight, inclusion criteria for birthweight analysis, proportion of pregnant women enrolled, proportion of infants weighed and studies reporting significant difference in birthweight were extracted. When available, the method of gestational age estimation and the potential confounders of birthweight measurements were also extracted.
Sixty-three publications were identified. Three of these reports were excluded because one was a review article7 and two did not report birthweight.8,9 There were 43 different trials and three case reports described in the remaining articles. The case reports did not contain sufficient details on the methodology used to measure birthweight and were excluded.10–12 Forty-three studies described in 59 publications were reviewed (Table S1, see Supporting information).13–72 Most (56%, 24/43) were studies on the prevention of malaria by intermittent preventive treatment (IPTp) or chemoprophylaxis in the African subcontinent (Table S1).
Different types of weighing scales were described, varying from spring scales used in field situations to very precise digital scales in referral hospitals. Only 44% (19/43) of the articles reported the type of scale (Table S2, see Supporting information). Calibration of scales with standard weights was reported in three studies.46,55,68 Scale precision varied from 1 to 100 g (Table S2).
In resource-limited, tropical, humid or dusty field conditions, electronic scales can break56 or trained midwives can be too busy to measure all babies;15 however, only two research teams reported such events. One study in Kenya confirmed birthweight measurement by a double reading, and used the mean value for data analysis.68
Table S2 shows the variation in the printed format of birthweight. Most articles provided the mean ± standard deviation (SD) birthweight in grams; those that reported a significant difference between groups (44% [19/43]) are highlighted in bold in the table. One study reported a significant difference of 80 g between two groups, although ‘birthweight at the two hospitals was recorded to the nearest 100 g’.59 Three articles only reported the proportions of LBW, but not the actual mean birthweight.26,55,66 The average percentage of newborns that were included for birthweight analysis was 71% (range, 33–100%). In 58% (11/19) of the studies that reported a significant difference in birthweight, the result was based on the analysis of <80% of the participants.
Delay in the weighing of the infant has an effect on the reported result.73,74 Seventy per cent (30/43) of the publications reported the time interval between the delivery and measurement of birthweight, and 35% (15/43) included babies weighed within 24 hours of birth (Table S2). The percentage of babies that were included for birthweight analysis is shown in Table S2. Some studies had a low proportion (14%53 or 15%68) of infants weighed within 24 hours. Eight publications adjusted for the day of weight using one of two formulae.35,75 However, the actual formulae were not provided, and different articles derived different percentage adjustments despite referencing the same formula. For example, some authors adjusted the weights by 1% for weight measured on day 4,33 and others, using the same formula,75 used a 3% correction,15 whereas a 5% adjustment was made using the formula described by Greenwood et al.35
Most of the included studies confined their analysis of birthweight to liveborn singletons (Table S2). Three publications included multiple deliveries (twins or triplets).54,59,70 Three teams specifically reported that twins and congenital abnormalities were excluded from further analysis.41,43,72 The remaining publications did not mention whether twins, stillborn infants or those with congenital abnormalities were included in the analysis. Congenital abnormalities were reported in 15 publications.13,14,17,22,23,29,43,45,46,50,54,60–62,72 Eight studies (18%) reported the length of the infant at birth and, of these, four reported IUGR.41,50,64,72
Gestational age is defined as the time elapsed from the first day of the last menstrual period (LMP), if known, to the day of delivery.76 Gestational age can then be divided into blocks depending largely on neonatal viability (see Figure 1). The World Health Organization (WHO) uses a 22-week threshold to define miscarriage, but different definitions continue to be used. In the articles reviewed, the method of estimating gestational age was described in 77% (33/43) of the publications. Table 1 shows that the symphysis–fundal height (SFH) was the most commonly used method.
This measurement enables the gestational age to be calculated, but the formulae differ between populations.72,77,78 Several publications report SFH to be inaccurate34,43,68; however, it was the most common single method used to describe gestational age in this review (Table 1).24,28,32,34,40,45,51,52,54–56,60,61,72
The use of LMP was reported to be inaccurate in studies in which another method of gestational age estimation was available.26,41,43,64,65 Examples of such inaccuracies were because the women could not recall their LMP,26,50 or there was no menstruation between two consecutive pregnancies.43 One study reported 22% of pregnancies in which the ultrasound measurement of fetal size was more than two SDs above or below the mean for gestation calculated from the menstrual history.26 In another study, estimation of gestational age was based on the identification of ‘quickening’, which was interpreted as an indication that the gestational age was more than 18 weeks.42 A combination of LMP and SFH was used to estimate gestational age in six studies.15,38,41,46,63,67 One study that compared postnatal tests and LMP/SFH reported, ‘an unacceptably high number of women had pregnancies of more than 44 weeks, which makes the usefulness of LMP for assessment of gestational age doubtful’ and ‘gestational age derived from SFH is not reliable, with a range of 20–50 weeks’.43
The number of physical and neuromuscular maturity criteria examined in standardised neonatal scoring systems is critical to the accuracy of the test.79 However, a number of modifications to the methods of Ballard43 and Dubowitz80,81 have been used in resource-poor settings. Newborn tests have been reported to be less accurate when performed after 12–20 hours of age,22 and to be time consuming.56
Several factors were reported to have an impact on birthweight, including maternal smoking (n = 2),66,72 high blood pressure or pre-eclampsia (n = 9),17,23,26,32,60–62,66,72 maternal infections (e.g. chorioamnionitis) as risk factors for premature labour (n = 3),29,45,61 parity, height and nutritional status of the mother, number of antenatal clinic visits, rainy season and sex of the baby.17,23,24,29,45,61,63–66,72 The sex of the newborn was reported in 40% (17/43) of studies. A few authors make reference to the problem of ‘infants that were not weighed’, attributed to highly mobile rural populations and large numbers of home deliveries resulting in missing delivery information.34,55,69 These missing data may introduce bias, and one study showed that the loss of contact with subjects during follow-up was more prevalent in the control group than in the treated group.20
Considerable effort by researchers and the pregnant women themselves has been devoted to determine the impact of antimalarial interventions on birthweight, often under difficult conditions. Important information regarding the methodology and reporting of birth outcome data is often missing or inaccurately reported. Journal space restrictions may not allow authors to describe completely what they actually did and this is a potential limitation of our review. This article does not question the association between malaria and birthweight reduction, but highlights that the conclusions drawn about the effects of interventions based on differences in birthweight could partly be explained by inaccuracy in measurement methods.
When designing and conducting perinatal research studies, careful selection of the method of gestational age estimation is necessary, as findings can differ considerably according to the method.82 When differences in birthweight are found, a bias caused by the selection of a particular method must be considered as an alternative explanation for any association found.82
An error in gestational age estimation of even 1 week has major implications on birthweight. The weight gain of a fetus in the late third trimester can be as much as 250 g per week:83 this value is similar to the reduction in weight attributable to malaria.1–3 Ideally, gestational age should be estimated by fetal crown–rump length (CRL) or early second-trimester ultrasound, which is the standard in resource-rich countries84–86 and is becoming available in developing countries.87 When no reliable LMP, SFH or ultrasound measurements are available, postnatal examination of the newborn, with clinical scoring for external and/or neurological characteristics, can be used. These methods can be performed by locally trained paramedical health workers or nurses.43,88 The Dubowitz80 examination for the estimation of gestational age is recommended from 6 to 72 hours of life, which can make it difficult to include home births.
All that is needed to measure newborn weight is a scale. As a result, birthweight is frequently used as the only item to describe birth outcome. To describe the type of growth restriction caused by malaria, additional parameters, such as gestational age, newborn length and/or head circumference measurements, are required.
The accuracy of the equipment used to measure birthweight is paramount.89 It is preferable to use scales that have been registered for medical use, and the name, model and accuracy should be reported, especially if newborns are weighed at home. In the articles included here, none compared birthweight of home- and hospital-delivered babies, but this has the potential for large differences in measurements. Although some studies reported weight to the nearest gram,29,31,54,64 the reported accuracy by the manufacturer is usually of the order of 10 g, even though some digital scales may provide readouts to the nearest gram.
Research teams should be adequately trained in obtaining and reporting measurements. Ideally, research measurements should be taken by two different trained observers who are blind to the results obtained by the other, with measurements repeated that exceed preset maximum allowable differences.90 A standard method of calibrating scales should also take place at least once a week. With a sufficient sample size of newborns, birthweight is a normally distributed continuous variable, so that the presentation of such data would be expected to include the mean ± SD, as well as the minimum and maximum (range).
Normal birthweight reduction can be as much as 10% by day 3,73,74 and, in a 3000-g baby, this would result in a weight reduction of 300 g; this is within the order of magnitude of the effect described for malaria in pregnancy. Consequently, the day the newborn is weighed has important implications for research, particularly as a large proportion of women in resource-poor settings deliver at home, and delays in the recording of birthweight are expected. Ideally, birthweight should be obtained within 24 hours of birth or, if taken after 24 hours, a correction formula could be applied. However, blanket correction factors do not account for the differences in postnatal weight loss as a result of birthweight categories,91 gravidity/parity,92 race, asphyxia92 and age at the initiation of breastfeeding.92 In the context of RCTs, the proportion of infants weighed on different days should not be significantly different between the groups.
The inclusion of multiple pregnancies, stillbirths or infants with congenital abnormalities will have an impact on birthweight analysis. Although such pregnancies need to be reported, they should not be included in any analysis of birthweight. Whether minor congenital abnormalities have an impact on birthweight is debatable but, for the sake of consistency, they should probably be excluded from any birthweight analysis in the context of clinical trials. Nevertheless, it is important to highlight that congenital abnormalities will not be reliably reported without an adequate examination of the newborn by a trained observer and a standardised method of classifying abnormalities. WHO has established a pregnancy registry (http://apps.who.int/tdr/svc/grants/calls/call-contributions) that will include the prevalence of birth defects in Asia, Africa and Latin-America, and classification using International Classification of Diseases (ICD10).
Most potential factors confounding birthweight can be detected by adequate antenatal and intrapartum care. Inclusion of gender in the analysis could be used as an internal validity check, as female newborns are lighter than males.93,94 Although clinical trials often exclude women with known medical or obstetric problems, some could arise after inclusion and should be controlled for, for example, hypertension (eclampsia, pre-eclampsia, pregnancy-induced hypertension), infections (pyelonephritis, sexually transmitted infections, local area-specific infections, e.g. typhoid, scrub typhus), obstetric problems, such as preterm labour, and whether there is a recognised trigger, for example, symptomatic malaria or pyelonephritis. RCTs could minimise the effect of potential confounders, but they should be included in any (multivariate) analysis.
Birthweight may not necessarily be the best method to evaluate the efficacy of interventions against malaria in pregnancy. The study of IUGR and the type of growth restriction (symmetrical or asymmetrical) requires additional parameters, including gestational age, newborn length and/or head circumference measurements.
Differences in birthweight are often used to compare the efficacy of interventions aimed to reduce the impact of malaria during pregnancy.95–98 Such differences can clearly be affected by inaccuracies in measurement methods, and confounders such as those affecting gestational age or time of weighing. The reporting of birthweight and gestational age in maternal malaria studies can be improved. Simple methodological guidelines for reporting birth outcome, with an emphasis on studies of malaria in pregnancy, are provided (Table 2).
The authors would like to thank Ishag Adam, Machteld Boel, Piet Kager, Nattapan Kanjanawatti, Jeanne Packer, Georges Snounou and Adrienne White for their help in finding full texts of the articles.
All authors declare that they have no conflict of interest.
MJR and JAR performed the literature searches required for this review. MJR and JAR reviewed all abstracts and full text articles, and wrote and edited the manuscript. RM decided when MJR and JAR could not agree. MJR, JAR, ATP, FN and RM formulated the protocol and database. All authors participated in the writing and editing of the manuscript. All authors read and approved the final manuscript.
This is a review of previously published data and, as such, does not require ethics approval.
Mahidol-Oxford Tropical Medicine Research Unit is funded by the Wellcome Trust of Great Britain. ATP is supported by the Oxford Partnership Comprehensive Biomedical Research Centre with funding from the Department of Health NIHR Biomedical Research Centres funding scheme.
|1.||Luxemburger C,McGready R,Kham A,Morison L,Cho T,Chongsuphajaisiddhi T,et al. Effects of malaria during pregnancy on infant mortality in an area of low malaria transmissionAm J EpidemiolYear: 20011544596511532788|
|2.||Steketee RW,Nahlen BL,Parise ME,Menendez C. The burden of malaria in pregnancy in malaria-endemic areasAm J Trop Med HygYear: 2001641–2 Suppl283511425175|
|3.||Guyatt HL,Snow RW. Impact of malaria during pregnancy on low birth weight in sub-Saharan AfricaClin Microbiol RevYear: 2004177609 table of contents. 15489346|
|4.||Tambyraja RL,Ratnam SS. The small fetus: growth-retarded and pretermClin Obstet GynaecolYear: 19829517376756748|
|5.||Salomon LJ. Early fetal growth: concepts and pitfallsUltrasound Obstet GynecolYear: 201035385920373482|
|6.||Brabin B,Rogerson SJ. Duffy PE,Fried MThe epidemiology and outcomes of maternal malariaMalaria in Pregnancy: Deadly Parasite, Susceptible HostYear: 2001LondonTaylor and Francis2752|
|7.||Dellicour S,Hall S,Chandramohan D,Greenwood B. The safety of artemisinins during pregnancy: a pressing questionMalaria JYear: 2007615|
|8.||Lindsay S,Ansell J,Selman C,Cox V,Hamilton K,Walraven G. Effect of pregnancy on exposure to malaria mosquitoesLancetYear: 2000355197210859048|
|9.||Nahlen BL,Akintunde A,Alakija T,Nguyen-Dinh P,Ogunbode O,Edungbola LD,et al. Lack of efficacy of pyrimethamine prophylaxis in pregnant Nigerian womenLancetYear: 1989283042571759|
|10.||Ahmed A,Cerilli LA,Sanchez PJ. Congenital malaria in a preterm neonate: case report and review of the literatureAm J PerinatolYear: 19981519229475682|
|11.||Hewson MP,Simmer K,Blackmore T. Congenital malaria in a preterm infantJ Paediatr Child HealthYear: 200339713514629507|
|12.||Rolfe M. Multiple drug resistant Plasmodium falciparum malaria in a pregnant indigenous Zambian womanTrans R Soc Trop Med HygYear: 19888255473076712|
|13.||Adam I,Ali DA,Alwaseila A,Kheir MM,Elbashir MI. Mefloquine in the treatment of falciparum malaria during pregnancy in Eastern SudanSaudi Med JYear: 2004251400215494810|
|14.||Bounyasong S. Randomized trial of artesunate and mefloquine in comparison with quinine sulfate to treat P. falciparum malaria pregnant womenJ Med Assoc Thail [Chotmaihet thangphaet]Year: 200184128999|
|15.||Browne EN,Maude GH,Binka FN. The impact of insecticide-treated bednets on malaria and anaemia in pregnancy in Kassena-Nankana district, Ghana: a randomized controlled trialTrop Med Int HealthYear: 200166677611555433|
|16.||Challis K,Osman NB,Cotiro M,Nordahl G,Dgedge M,Bergstrom S. Impact of a double dose of sulphadoxine-pyrimethamine to reduce prevalence of pregnancy malaria in southern MozambiqueTrop Med Int HealthYear: 2004910667315482398|
|17.||Clerk CA,Bruce J,Affipunguh PK,Mensah N,Hodgson A,Greenwood B,et al. A randomized, controlled trial of intermittent preventive treatment with sulfadoxine–pyrimethamine, amodiaquine, or the combination in pregnant women in GhanaJ Infect DisYear: 200819812021118752443|
|18.||Cot M,le Hesran JY,Miailhes P,Roisin A,Fievet N,Barro D,et al. Effect of chloroquine prophylaxis during pregnancy on maternal haematocritAnn Trop Med ParasitolYear: 19989237439614452|
|19.||Cot M,Le Hesran JY,Miailhes P,Esveld M,Etya'ale D,Breart G. Increase of birth weight following chloroquine chemoprophylaxis during the first pregnancy: results of a randomized trial in CameroonAm J Trop Med HygYear: 19955358158561257|
|20.||Cot M,Roisin A,Barro D,Yada A,Verhave JP,Carnevale P,et al. Effect of chloroquine chemoprophylaxis during pregnancy on birth weight: results of a randomized trialAm J Trop Med HygYear: 1992462171536379|
|21.||Cottrell G,Mary JY,Barro D,Cot M. The importance of the period of malarial infection during pregnancy on birth weight in tropical AfricaAm J Trop Med HygYear: 2007768495417488903|
|22.||Deen JL,von Seidlein L,Pinder M,Walraven GE,Greenwood BM. The safety of the combination artesunate and pyrimethamine–sulfadoxine given during pregnancyTrans R Soc Trop Med HygYear: 200195424811579889|
|23.||Denoeud L,Fievet N,Aubouy A,Ayemonna P,Kiniffo R,Massougbodji A,et al. Is chloroquine chemoprophylaxis still effective to prevent low birth weight? Results of a study in BeninMalaria JYear: 2007627|
|24.||Dolan G,ter Kuile FO,Jacoutot V,White NJ,Luxemburger C,Malankirii L,et al. Bed nets for the prevention of malaria and anaemia in pregnancyTrans R Soc Trop Med HygYear: 19938762068296357|
|25.||Shulman CE,Dorman EK,Cutts F,Kawuondo K,Bulmer JN,Peshu N,et al. Intermittent sulphadoxine-pyrimethamine to prevent severe anaemia secondary to malaria in pregnancy: a randomised placebo-controlled trialLancetYear: 1999353632610030329|
|26.||Dorman EK,Shulman CE,Kingdom J,Bulmer JN,Mwendwa J,Peshu N,et al. Impaired uteroplacental blood flow in pregnancies complicated by falciparum malariaUltrasound Obstet GynecolYear: 2002191657011876809|
|27.||Egwunyenga OA,Ajayi JA,Duhlinska-Popova DD. Transplacental passage of Plasmodium falciparum and seroevaluation of newborns in northern NigeriaJ Commun DisYear: 19952777837499776|
|28.||Ekejindu IM,Udigwe GO,Chijioke IR. Malaria and anaemia in pregnancy in Enugu, south east NigeriaAfr J Med Med SciYear: 2006351317209319|
|29.||Falade CO,Yusuf BO,Fadero FF,Mokuolu OA,Hamer DH,Salako LA. Intermittent preventive treatment with sulphadoxine-pyrimethamine is effective in preventing maternal and placental malaria in Ibadan, south-western NigeriaMalaria JYear: 2007688|
|30.||Falade C,Mokuolu O,Okafor H,Orogade A,Falade A,Adedoyin O,et al. Epidemiology of congenital malaria in Nigeria: a multi-centre studyTrop Med Int HealthYear: 20071212798717956542|
|31.||Filler SJ,Kazembe P,Thigpen M,Macheso A,Parise ME,Newman RD,et al. Randomized trial of 2-dose versus monthly sulfadoxine–pyrimethamine intermittent preventive treatment for malaria in HIV-positive and HIV-negative pregnant women in MalawiJ Infect DisYear: 20061942869316826475|
|32.||Fleming AF,Ghatoura GB,Harrison KA,Briggs ND,Dunn DT. The prevention of anaemia in pregnancy in primigravidae in the guinea savanna of NigeriaAnn Trop Med ParasitolYear: 198680211333530158|
|33.||Gies S,Coulibaly SO,Ouattara FT,D'Alessandro U. Individual efficacy of intermittent preventive treatment with sulfadoxine–pyrimethamine in primi- and secundigravidae in rural Burkina Faso: impact on parasitaemia, anaemia and birth weightTrop Med Int HealthYear: 2009141748219171009|
|34.||Gies S,Coulibaly SO,Ouattara FT,Ky C,Brabin BJ,D'Alessandro U. A community effectiveness trial of strategies promoting intermittent preventive treatment with sulphadoxine-pyrimethamine in pregnant women in rural Burkina FasoMalaria JYear: 20087180|
|35.||Greenwood BM,Greenwood AM,Snow RW,Byass P,Bennett S,Hatib-N'Jie AB. The effects of malaria chemoprophylaxis given by traditional birth attendants on the course and outcome of pregnancyTrans R Soc Trop Med HygYear: 198983589942617619|
|36.||Greenwood AM,Menendez C,Todd J,Greenwood BM. The distribution of birth weights in Gambian women who received malaria chemoprophylaxis during their first pregnancy and in control womenTrans R Soc Trop Med HygYear: 19948831127974672|
|37.||Greenwood AM,Armstrong JR,Byass P,Snow RW,Greenwood BM. Malaria chemoprophylaxis, birth weight and child survivalTrans R Soc Trop Med HygYear: 19928648351475810|
|38.||Hamer DH,Mwanakasale V,Macleod WB,Chalwe V,Mukwamataba D,Champo D,et al. Two-dose versus monthly intermittent preventive treatment of malaria with sulfadoxine–pyrimethamine in HIV-seropositive pregnant Zambian womenJ Infect DisYear: 200719615859418008241|
|39.||Gill CJ,Macleod WB,Mwanakasale V,Chalwe V,Mwananyanda L,Champo D,et al. Inferiority of single-dose sulfadoxine–pyrimethamine intermittent preventive therapy for malaria during pregnancy among HIV-positive Zambian womenJ Infect DisYear: 200719615778418008240|
|40.||Hamilton PJ,Gebbie DA,Wilks NE,Lothe F. The role of malaria, folic acid deficiency and haemoglobin AS in pregnancy at Mulago hospitalTrans R Soc Trop Med HygYear: 1972665946025071088|
|41.||Kalanda BF,van Buuren S,Verhoeff FH,Brabin BJ. Anthropometry of fetal growth in rural Malawi in relation to maternal malaria and HIV statusArch Dis ChildYear: 200590F1615|
|42.||le Cessie S,Verhoeff FH,Mengistie G,Kazembe P,Broadhead R,Brabin BJ. Changes in haemoglobin levels in infants in Malawi: effect of low birth weight and fetal anaemiaArch Dis ChildYear: 200286F1827|
|43.||Verhoeff FH,Milligan P,Brabin BJ,Mlanga S,Nakoma V. Gestational age assessment by nurses in a developing country using the Ballard method, external criteria onlyAnn Trop PaediatrYear: 199717333429578793|
|44.||Verhoeff FH,Le Cessie S,Kalanda BF,Kazembe PN,Broadhead RL,Brabin BJ. Post-neonatal infant mortality in Malawi: the importance of maternal healthAnn Trop PaediatrYear: 200424161915186545|
|45.||Kayentao K,Kodio M,Newman RD,Maiga H,Doumtabe D,Ongoiba A,et al. Comparison of intermittent preventive treatment with chemoprophylaxis for the prevention of malaria during pregnancy in MaliJ Infect DisYear: 20051911091615593011|
|46.||Larocque R,Casapia M,Gotuzzo E,MacLean JD,Soto JC,Rahme E,et al. A double-blind randomized controlled trial of antenatal mebendazole to reduce low birthweight in a hookworm-endemic area of PeruTrop Med Int HealthYear: 20061114859517002722|
|47.||Mbaye A,Richardson K,Balajo B,Dunyo S,Shulman C,Milligan P,et al. A randomized, placebo-controlled trial of intermittent preventive treatment with sulphadoxine-pyrimethamine in Gambian multigravidaeTrop Med Int HealthYear: 200611992100216827700|
|48.||Mbonye AK,Bygbjerg IC,Magnussen P. Intermittent preventive treatment of malaria in pregnancy: a new delivery system and its effect on maternal health and pregnancy outcomes in UgandaBull World Health OrganYear: 2008869310018297163|
|49.||Mbonye AK,Bygbjerg I,Magnussen P. Intermittent preventive treatment of malaria in pregnancy: a community-based delivery system and its effect on parasitemia, anemia and low birth weight in UgandaInt J Infect DisYear: 20081222917526422|
|50.||McGready R,Ashley EA,Moo E,Cho T,Barends M,Hutagalung R,et al. A randomized comparison of artesunate–atovaquone–proguanil versus quinine in treatment for uncomplicated falciparum malaria during pregnancyJ Infect DisYear: 20051928465316088834|
|51.||Menendez C,Todd J,Alonso PL,Lulat S,Francis N,Greenwood BM. Malaria chemoprophylaxis, infection of the placenta and birth weight in Gambian primigravidaeJ Trop Med HygYear: 19949724488064949|
|52.||Menendez C,Todd J,Alonso PL,Francis N,Lulat S,Ceesay S,et al. The response to iron supplementation of pregnant women with the haemoglobin genotype AA or ASTrans R Soc Trop Med HygYear: 199589289927660438|
|53.||Menendez C,Todd J,Alonso PL,Francis N,Lulat S,Ceesay S,et al. The effects of iron supplementation during pregnancy, given by traditional birth attendants, on the prevalence of anaemia and malariaTrans R Soc Trop Med HygYear: 19948859037992349|
|54.||Menendez C,Bardaji A,Sigauque B,Romagosa C,Sanz S,Serra-Casas E,et al. A randomized placebo-controlled trial of intermittent preventive treatment in pregnant women in the context of insecticide treated nets delivered through the antenatal clinicPLoS ONEYear: 20083e193418398460|
|55.||Msyamboza KP,Savage EJ,Kazembe PN,Gies S,Kalanda G,D'Alessandro U,et al. Community-based distribution of sulfadoxine–pyrimethamine for intermittent preventive treatment of malaria during pregnancy improved coverage but reduced antenatal attendance in southern MalawiTrop Med Int HealthYear: 200914183919207178|
|56.||Mutabingwa TK,Malle LN,de Geus A,Oosting J. Malaria chemosuppression in pregnancy. II. Its effect on maternal haemoglobin levels, placental malaria and birth weightTrop Geog MedYear: 1993454955|
|57.||Mutabingwa TK,Malle LN,de Geus A,Oosting J. Malaria chemosuppression in pregnancy. I. The effect of chemosuppressive drugs on maternal parasitaemiaTrop Geog MedYear: 199345614|
|58.||Ndyomugyenyi R,Magnussen P. Chloroquine prophylaxis, iron/folic-acid supplementation or case management of malaria attacks in primigravidae in western Uganda: effects on congenital malaria and infant haemoglobin concentrationsAnn Trop Med ParasitolYear: 20009475968 discussion 69–70. 11214094|
|59.||Ndyomugyenyi R,Magnussen P. Malaria morbidity, mortality and pregnancy outcome in areas with different levels of malaria transmission in Uganda: a hospital record-based studyTrans R Soc Trop Med HygYear: 200195463811706650|
|60.||Nosten F,Karbwang J,White NJ,Honeymoon,Na Bangchang K,Bunnag D,et al. Mefloquine antimalarial prophylaxis in pregnancy: dose finding and pharmacokinetic studyBr J Clin PharmacolYear: 19903079852390434|
|61.||Nosten F,ter Kuile F,Maelankiri L,Chongsuphajaisiddhi T,Nopdonrattakoon L,Tangkitchot S,et al. Mefloquine prophylaxis prevents malaria during pregnancy: a double-blind, placebo-controlled studyJ Infect DisYear: 19941695956038158032|
|62.||Rahimy MC,Gangbo A,Adjou R,Deguenon C,Goussanou S,Alihonou E. Effect of active prenatal management on pregnancy outcome in sickle cell disease in an African settingBloodYear: 2000961685910961864|
|63.||Shulman CE,Dorman EK,Talisuna AO,Lowe BS,Nevill C,Snow RW,et al. A community randomized controlled trial of insecticide-treated bednets for the prevention of malaria and anaemia among primigravid women on the Kenyan coastTrop Med Int HealthYear: 199831972049593358|
|64.||Steketee RW,Wirima JJ,Slutsker WL,Khoromana CO,Breman JG,Heymann DL. Objectives and methodology in a study of malaria treatment and prevention in pregnancy in rural Malawi: The Mangochi Malaria Research ProjectAm J Trop Med HygYear: 19961Suppl8168702043|
|65.||Steketee RW,Wirima JJ,Hightower AW,Slutsker L,Heymann DL,Breman JG. The effect of malaria and malaria prevention in pregnancy on offspring birthweight, prematurity, and intrauterine growth retardation in rural MalawiAm J Trop Med HygYear: 19961Suppl33418702035|
|66.||Taha Tel T,Gray RH,Abdelwahab MM,Abdelhafeez A. Distribution and determinants of low birthweight in central SudanPaediatr Perinatal EpidemiolYear: 19959185200|
|67.||ter Kuile FO,Terlouw DJ,Kariuki SK,Phillips-Howard PA,Mirel LB,Hawley WA,et al. Impact of permethrin-treated bed nets on malaria, anemia, and growth in infants in an area of intense perennial malaria transmission in western KenyaAm J Trop Med HygYear: 20034Suppl687712749488|
|68.||ter Kuile FO,Terlouw DJ,Phillips-Howard PA,Hawley WA,Friedman JF,Kariuki SK,et al. Reduction of malaria during pregnancy by permethrin-treated bed nets in an area of intense perennial malaria transmission in western KenyaAm J Trop Med HygYear: 20034Suppl506012749486|
|69.||Tukur IU,Thacher TD,Sagay AS,Madaki JK. A comparison of sulfadoxine–pyrimethamine with chloroquine and pyrimethamine for prevention of malaria in pregnant Nigerian womenAm J Trop Med HygYear: 20077610192317556604|
|70.||Villamor E,Msamanga G,Aboud S,Urassa W,Hunter DJ,Fawzi WW. Adverse perinatal outcomes of HIV-1-infected women in relation to malaria parasitemia in maternal and umbilical cord bloodAm J Trop Med HygYear: 200573694716222011|
|71.||Fawzi WW,Villamor E,Msamanga GI,Antelman G,Aboud S,Urassa W,et al. Trial of zinc supplements in relation to pregnancy outcomes, hematologic indicators, and T cell counts among HIV-1-infected women in TanzaniaAm J Clin NutrYear: 200581161715640476|
|72.||Villegas L,McGready R,Htway M,Paw MK,Pimanpanarak M,Arunjerdja R,et al. Chloroquine prophylaxis against vivax malaria in pregnancy: a randomized, double-blind, placebo-controlled trialTrop Med Int HealthYear: 2007122091817300627|
|73.||Wright CM,Parkinson KN. Postnatal weight loss in term infants: what is normal and do growth charts allow for it?Arch Dis ChildYear: 200489F2547|
|74.||Macdonald PD,Ross SR,Grant L,Young D. Neonatal weight loss in breast and formula fed infantsArch Dis ChildYear: 200388F4726|
|75.||D'Alessandro U,Langerock P,Bennett S,Francis N,Cham K,Greenwood BM. The impact of a national impregnated bed net programme on the outcome of pregnancy in primigravidae in The GambiaTrans R Soc Trop Med HygYear: 199690487928944251|
|76.||Engle WA. Age terminology during the perinatal periodPediatricsYear: 20041141362415520122|
|77.||Buhmann L,Elder WG,Hendricks B,Rahn K. A comparison of Caucasian and Southeast Asian Hmong uterine fundal height during pregnancyActa Obstet Gynecol ScandYear: 19987752169654174|
|78.||Nosten F,McGready R,Simpson JA,Thwai KL,Balkan S,Cho T,et al. Effects of Plasmodium vivax malaria in pregnancyLancetYear: 1999354546910470698|
|79.||Nicolopoulos D,Perakis A,Papadakis M,Alexiou D,Aravantinos D. Estimation of gestational age in the neonate: a comparison of clinical methodsAm J Dis ChildYear: 1976130477801274897|
|80.||Dubowitz LM,Dubowitz V,Goldberg C. Clinical assessment of gestational age in the newborn infantJ PediatrYear: 1970771105430794|
|81.||Eregie CO. Assessment of gestational age: modification of a simplified methodDev Med Child NeurolYear: 1991335966001879623|
|82.||Lynch CD,Zhang J. The research implications of the selection of a gestational age estimation methodPaediatr Perinatal EpidemiolYear: 200721Suppl 28696|
|83.||Doubilet PM,Benson CB,Nadel AS,Ringer SA. Improved birth weight table for neonates developed from gestations dated by early ultrasonographyJ Ultrasound MedYear: 19971624199315150|
|84.||Hadlock FP,Harrist RB,Martinez-Poyer J. How accurate is second trimester fetal dating?J Ultrasound MedYear: 199110557611942221|
|85.||Chervenak FA,Skupski DW,Romero R,Myers MK,Smith-Levitin M,Rosenwaks Z,et al. How accurate is fetal biometry in the assessment of fetal age?Am J Obstet GynecolYear: 1998178678879579429|
|86.||Taipale P,Hiilesmaa V. Predicting delivery date by ultrasound and last menstrual period in early gestationObstet GynecolYear: 2001971899411165580|
|87.||Rijken MJ,Lee SJ,Boel ME,Papageorghiou AT,Visser GH,Dwell SL,et al. Obstetric ultrasound scanning by local health workers in a refugee camp on the Thai–Burmese borderUltrasound Obstet GynecolYear: 20093439540319790099|
|88.||McGready R,Simpson J,Panyavudhikrai S,Loo S,Mercuri E,Haataja L,et al. Neonatal neurological testing in resource-poor settingsAnn Trop PaediatrYear: 2000203233611219171|
|89.||Mullany LC,Darmstadt GL,Katz J,Khatry SK,Tielsch JM. Effect of instrument precision on estimation of low birth weight prevalenceJ PerinatolYear: 20052511315496868|
|90.||Onis Md,Onyango AW,Van den Broeck J,Chumlea WC,Martorell R. Measurement and standardization protocols for anthropometry used in the construction of a new international growth referenceFood Nutr BullYear: 2004251 Suppl 1S273615069917|
|91.||Smith SL,Kirchhoff KT,Chan GM,Squire SJ. Patterns of postnatal weight changes in infants with very low and extremely low birth weightsHeart LungYear: 199423439457852058|
|92.||Enzunga A,Fischer PR. Neonatal weight loss in rural ZaireAnn Trop PaediatrYear: 199010159631699479|
|93.||Gibson JR,Mc KT. Observations on all births (23,970) in Birmingham, 1947. VI. Birth weight, duration of gestation, and survival related to sexBr J Soc MedYear: 19526152814935162|
|94.||Naeye RL,Burt LS,Wright DL,Blanc WA,Tatter D. Neonatal mortality, the male disadvantagePediatricsYear: 19714890265129451|
|95.||Macgregor JD,Avery JG. Malaria transmission and fetal growthBr Med JYear: 1974343364606777|
|96.||Rulisa S,Mens PF,Karema C,Schallig HD,Kaligirwa N,Vyankandondera J,et al. Malaria has no effect on birth weight in RwandaMalaria JYear: 20098194|
|97.||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 anemiaTrans R Soc Trop Med HygYear: 20101044162220207387|
|98.||Tiono AB,Ouedraogo A,Bougouma EC,Diarra A,Konate AT,Nebie IO,et al. Placental malaria and low birth weight in pregnant women living in a rural area of Burkina Faso following the use of three preventive treatment regimensMalaria JYear: 20098224|
The following supplementary materials are available for this article:
Table S1. Included studies.Click here for additional data file (bjo0118-0671-SD1.doc)
Table S2. Reporting of weight measurements.Click here for additional data file (bjo0118-0671-SD2.doc)
Additional Supporting Information may be found in the online version of this article.
Please note: Wiley-Blackwell are not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing material) should be directed to the corresponding author.
[Figure ID: fig01]
Definitions of pregnancy partitions. Maternal mortality can occur whilst pregnant or up to 42 days after termination of pregnancy.
Reporting of estimation of gestational age during pregnancy or in the postpartum period
|Postnatal dating method||Pregnancy dating||Total|
|No postnatal test||1019,20,23,27,35,47,49,58,59,69||316,22,70||828,32,33,40,51,53,55,60||315,46,63||4*, 13,14,26,62||28|
LMP, last menstrual period; SFH, symphysis–fundal height; US, ultrasound.
*Ultrasound-derived gestational age assessment was used when menstrual dates were unknown (31%) or when the measurement of fetal size was more than two standard deviations above or below the mean for gestation calculated from the menstrual history (22%).26 Only women who could afford to pay had an ultrasound dating scan in Benin.62
**If the discrepancy between the LMP- and Dubowitz-derived gestational age was more than 14 days, the Dubowitz score was used.38
***The gestational age was determined using the Ballard score. Anthropometric parameters and gestational age were used to classify the babies using a Lubchenko chart as preterm, term and postdate.29,30
****Midwives and Mother and Child Health aids recorded newborns as being full term or premature using personal experiences and based on the indicators for rapid assessment of maturity.56
|•Measure birthweight on all newborns (alive or stillborn) as soon as possible after birth, preferably before 24 hours|
|•Only liveborn singletons without congenital abnormalities should be included in birthweight analysis|
|•Report the actual number of newborn babies included in the birthweight analysis|
|•Report the time interval (in days) between birth and the measurement of birthweight|
|•Certified medical scales should be used|
|•Report the name, model and accuracy of the weight scale and state whether the scale was sufficiently sensitive to detect any difference identified. Scales should be calibrated on a weekly basis|
|•Head circumference and length of the newborn should be measured|
|•Regular standardisation sessions and quality control checks of the measurers are required90|
|•The sex of the baby should be recorded|
|Gestational age assessment|
|•Report the method of estimating gestational age|
|•A suggested algorithm to obtain the best estimate for the woman is, in order of priority: (1) ultrasound at <24 weeks by measuring, preferably, the crown–rump length (8–14 weeks) or head circumference (15–24 weeks); (2) if ultrasound not available, validated newborn gestational age assessment; (3) if (1) and (2) not available, the date of the last menstrual period or the symphysis–fundal height|
|•Analysis using birthweight or low birthweight should be controlled for gestational age|
|•Methods used to estimate gestational age should have regular (yearly) standardisation sessions and ongoing quality control (http://www.medscinet.net/intergrowth/protocol.aspx)|
|•Bias caused by the selection of a particular dating method—or no dating method—should always be considered as an alternative explanation for any identified associations65|
|•Potential confounders should be diagnosed and included in the birthweight analysis|
Keywords: Birthweight, gestational age, malaria, pregnancy.
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