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Review |

Prevalence of Malaria and Sexually Transmitted and Reproductive Tract Infections in Pregnancy in Sub-Saharan Africa:  A Systematic Review FREE

R. Matthew Chico, MPH; Philippe Mayaud, MD; Cono Ariti, MSc; David Mabey, MD; Carine Ronsmans, MD; Daniel Chandramohan, PhD
[+] Author Affiliations

Author Affiliations: Departments of Disease Control (Mr Chico and Dr Chandramohan), Clinical Research (Drs Mayaud and Mabey), Medical Statistics (Mr Ariti), and Infectious Disease Epidemiology (Dr Ronsmans) and the Malaria Centre (Mr Chico and Drs Mabey and Chandramohan), London School of Hygiene and Tropical Medicine, London, England.


JAMA. 2012;307(19):2079-2086. doi:10.1001/jama.2012.3428.
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Published online

Context Malaria and sexually transmitted infections/reproductive tract infections (STIs/RTIs) in pregnancy are direct and indirect causes of stillbirth, prematurity, low birth weight, and maternal and neonatal morbidity and mortality.

Objective To conduct a systematic review and meta-analysis of malaria and STI/RTI prevalence estimates among pregnant women attending antenatal care facilities in sub-Saharan Africa.

Data Sources PubMed, MEDLINE, EMBASE, the World Health Organization International Clinical Trials Registry, and reference lists were searched for studies reporting malaria, syphilis, Neisseria gonorrhoeae, Chlamydia trachomatis, Trichomonas vaginalis, or bacterial vaginosis among pregnant women attending antenatal care facilities in sub-Saharan Africa.

Study Selection Included studies were conducted in 1990-2011 with open enrollment. Studies from South Africa, where malaria is no longer endemic, were excluded.

Data Extraction Point prevalence estimates were corrected for diagnostic precision. A random-effects model meta-analysis was applied to produce pooled prevalence estimates.

Results A total of 171 studies met inclusion criteria, providing 307 point prevalence estimates for malaria or STIs/RTIs and including a total of 340 904 women. The pooled prevalence estimates (with 95% CIs and number of women with positive diagnosis) among studies in 1990-2011 in East and Southern Africa were as follows: syphilis, 4.5% (3.9%-5.1%; n = 8346 positive diagnoses), N gonorrhoeae, 3.7% (2.8%-4.6%; n = 626), C trachomatis, 6.9% (5.1%-8.6%; n = 350), T vaginalis, 29.1% (20.9%-37.2%; n = 5502), bacterial vaginosis, 50.8% (43.3%-58.4%; n = 4280), peripheral malaria, 32.0% (25.9%-38.0%; n = 11 688), and placental malaria, 25.8% (19.7%-31.9%; n = 1388). West and Central Africa prevalence estimates were as follows: syphilis, 3.5% (1.8%-5.2%; n = 851), N gonorrhoeae, 2.7% (1.7%-3.7%; n = 73), C trachomatis, 6.1% (4.0%-8.3%; n = 357), T vaginalis, 17.8% (12.4%-23.1%; n = 822), bacterial vaginosis, 37.6% (18.0%-57.2%; n = 1208), peripheral malaria, 38.2% (32.3%-44.1%; n = 12 242), and placental malaria, 39.9% (34.2%-45.7%; n = 4658).

Conclusion The dual prevalence of malaria and STIs/RTIs in pregnancy among women who attend antenatal care facilities in sub-Saharan Africa is considerable, with the combined prevalence of curable STIs/RTIs being equal to, if not greater than, malaria.

Figures in this Article

Quiz Ref IDThere are 880 000 stillbirths1 and 1.2 million neonatal deaths2 each year in sub-Saharan Africa. Low birth weight (<2.5 kg), attributable to intrauterine growth retardation, preterm delivery, or both, is the leading risk factor for neonatal mortality.3 Intrauterine infection is implicated in stillbirth4 and is associated with 25% to 40% of preterm births.5 Sexually transmitted infections and reproductive tract infections (STIs/RTIs)6 and malaria7 are associated with adverse birth outcomes, but both may be mitigated with preventive or presumptive treatment or by repeated screening and treatment throughout the antenatal period. The extent to which either approach may be beneficial depends on the underlying prevalence of STIs/RTIs and malaria in pregnancy. This systematic review and meta-analysis provide estimates for the dual prevalence of STIs/RTIs and malaria in pregnancy among women attending antenatal care facilities in sub-Saharan Africa.

We searched 3 databases, PubMed, MEDLINE, and EMBASE, in November 2011 using Medical Subject Headings and free text terms, respectively; the World Health Organization (WHO) International Clinical Trials Registry; and relevant reference lists to identify studies conducted between 1990-2011 that reported point prevalence estimates for STIs/RTIs, malaria, or both among pregnant women attending antenatal care facilities in sub-Saharan Africa (eAppendix 1). If 2 or more prevalence estimates were reported—whether the result of a comparative diagnostic study, use of the same diagnostic method on multiple occasions, or subsequent use of a more sensitive assay—we used the higher/highest measurement in our analysis.

Quiz Ref IDOur aim was to establish the dual prevalence of these infections in pregnancy among women receiving antenatal care without inflating estimates by including studies that selectively enrolled women from high-risk groups. Thus, studies that enrolled subsets of women from the antenatal care population were excluded (eg, only pregnant women with human immunodeficiency virus [HIV]). Studies of commercial sex workers, women seeking treatment at STI facilities or family planning facilities, or nonpregnant women tested in community-based surveys were also excluded. Multiyear studies that included pre-1990 data were excluded, as were studies from South Africa, where malaria is no longer endemic.

Records retrieved were all in English, although several abstracts had been translated from Chinese, Danish, Dutch, French, German, Italian, Portuguese, and Swedish. One author (R.M.C.) conducted the data retrieval. Data abstraction was not blinded to author or publication but was performed independently and in duplicate by R.M.C. and a research assistant, reviewing records against inclusion/exclusion criteria to identify 3618 records of interest. Any discrepancies were resolved by D.C. Two authors (P.M. and D.M.) and another researcher assisted R.M.C. in the identification and classification of STI/RTI diagnostic methods; D.C. did the same with R.M.C. for malaria studies. No evidence of publication bias was found using funnel-plot assessment as described by Sterne et al.8 Given that data for this review have been drawn from studies reporting point prevalence estimates without intervention, the potential for publication bias should be minimal.

Point prevalences and 95% confidence intervals were calculated for each study. We then applied a standard method9 for correcting errors of magnitude with the known sensitivity and specificity of individual assays (eAppendix 2 and eAppendix 3) to increase the precision of each point prevalence estimate. Corrected point prevalence data were then used to generate pooled prevalence estimates and corresponding 95% confidence intervals. We stratified results by subregion (East and Southern Africa vs West and Central Africa) because of underlying differences in epidemiology, particularly the extent to which HIV modulates the transmission of malaria and STIs/RTIs.

We conducted the meta-analysis with random-effects models,10 accounting for the possibility of heterogeneity between studies, and assessed our results with the Q statistic. Separate sensitivity analyses were performed for studies conducted before and after the year 2000 to examine temporal changes in prevalence. Using Stata/IC version 12 software11 to generate the random-effects meta-analysis model, we produced forest plots to display the point prevalence and 95% confidence intervals of individual studies as well as the pooled estimates and 95% confidence intervals for all strata.

A total of 171 studies met inclusion criteria, providing 307 point prevalence estimates and including a total of 340 904 women. Search results are summarized in Figure 1. The Table summarizes the pooled mean prevalence estimates of 1990-2011 with subanalyses for 1990-1999 and 2000-2011. Results for the period 1990-2011 are presented in Figure 2, plotted by subregion along with the lowest and highest point estimates reported. Detailed analyses by infection type and subregion are available online (eTable 1 and eFigure 1 [syphilis], eTable 2 and eFigure 2 [Neisseria gonorrhoeae ], eTable 3 and eFigure 3 [Chlamydia trachomatis ], eTable 4 and eFigure 4 [Trichomonas vaginalis ], eTable 5 and eFigure 5 [bacterial vaginosis], eTable 6 and eFigure 6 [peripheral malaria], and eTable 7 and eFigure 7 [placental malaria]), with key findings reported herein. In all instances, prevalence estimates have been corrected to account for diagnostic errors as previously described.

Place holder to copy figure label and caption
Figure 1. Identification, Screening, and Eligibility of Studies in the Meta-analysis
Graphic Jump Location

aData believed to have appeared in more than 1 article were reviewed in full text and therefore do not appear under records excluded.

Table Graphic Jump LocationTable. Pooled Mean Prevalence Estimates Among Pregnant Women Attending Antenatal Care Facilities in Sub-Saharan Africa
Place holder to copy figure label and caption
Figure 2. Curable STI/RTI and Malaria Infection Among Pregnant Women Attending Antenatal Facilities in Africa by Subregion
Graphic Jump Location

Diamonds indicate pooled mean prevalence estimates; the extremes of the diamonds indicate 95% CIs. Horizontal bars indicate lowest to highest point prevalence estimates. STI/RTI indicates sexually transmitted infection/reproductive tract infection.
aPlacental malaria is measured at delivery.

Syphilis

The pooled mean prevalence of syphilis in East and Southern Africa was 4.5% (95% CI, 3.9%-5.1%), with the highest estimate, 13.7% (95% CI, 9.0%-18.5%), in Vilanculos, Mozambique, based on rapid plasma reagin (RPR) testing and Treponema pallidum hemagglutination confirmation.12 In West and Central Africa, the pooled mean prevalence of serological syphilis was 3.5% (95% CI, 1.8%-5.2%). Yaoundé, Cameroon, reported the highest point estimate of 16.3% (95% CI, 15.2%-17.4%) using a T pallidum hemagglutination assay that confirms syphilis infection, although not necessarily active cases.13

Neisseria gonorrhoeae

In East and Southern Africa, the pooled prevalence was 3.7% (95% CI, 2.8%-4.6%), with the highest point estimate of 23.3% (95% CI, 16.4%-30.2%) observed in Manhiça, Mozambique.12 The pooled mean prevalence of N gonorrhoeae in West and Central Africa was 2.7% (95% CI, 1.7%-3.7%); the highest individual estimate, 4.6% (95% CI, 2.8%-6.3%), came from a study in Abidjan, Côte d’Ivoire, that used culture diagnostic methods.14

Chlamydia trachomatis

The pooled prevalence of C trachomatis infection in East and Southern Africa was 6.9% (95% CI, 5.1%-8.6%), with Khartoum, Sudan, reporting the highest prevalence estimate of 23.2% (95% CI, 16.5%-29.9%) as detected by an enzyme immunoassay.15 In West and Central Africa, the pooled mean prevalence was 6.1% (95% CI, 4.0%-8.3%). The highest prevalence, 16.4% (95% CI, 12.6%-20.1%) based on culture or enzyme immunoassay, was observed in Pikine, Senegal.16

Trichomonas vaginalis

The pooled prevalence of T vaginalis infection was 29.1% (95% CI, 20.9%-37.2%) among women in East and Southern Africa, compared with 17.8% (95% CI, 12.4%-23.1%) in West and Central Africa. The highest point estimate in East and Southern Africa was 51.7% (95% CI, 41.9%-61.5%), reported in a refugee camp of Rwandans in Tanzania,17 as diagnosed by wet-mount microscopy. The highest prevalence estimate in West and Central Africa, 52.0% (95% CI, 47.6%-56.4%), was in Jos, Nigeria, where T vaginalis was identified by the same method.18

Bacterial Vaginosis

The burden of bacterial vaginosis was higher than any other STI/RTI in both subregions. In East and Southern Africa, the pooled prevalence estimate was 50.8% (95% CI, 43.4%-58.4%). The highest point estimate was 85.5% (95% CI, 82.8%-88.1%) in Blantyre, Malawi, where Amsel criteria were used for diagnosis.17 In West and Central Africa, the pooled prevalence estimate was 37.6% (95% CI, 18.0%-57.2%), with the highest point estimate at 74.5% (95% CI, 70.0%-79.1%) in Praia, Cape Verde, based on clue cell count.19

Malaria

Peripheral Malaria. The pooled prevalence of peripheral malaria in East and Southern Africa was 32.0% (95% CI, 25.9%-38.0%). The highest subregional prevalence, 87.9% (95% CI, 85.7%-90.1%), was reported from Hoima, Uganda, where diagnosis was made by microscopy.20 In West and Central Africa, the pooled prevalence of peripheral malaria parasitemia was 38.2% (95% CI, 32.3%-44.1%). The highest point estimate was 94.9% (95% CI, 88.0%-102.0%) in Ngali II, Cameroon, as identified by polymerase chain reaction (PCR) diagnosis.21

Placental Malaria. For placental malaria, measurable only after delivery, the pooled prevalence in East and Southern Africa was 25.8% (95% CI, 19.7%-31.9%); the highest point estimate, 74.7% (95% CI, 65.5%-84.0%), was based on histological diagnosis in Kisumu, Kenya.22 In West and Central Africa, the pooled prevalence was 39.9% (95% CI, 34.2%-45.7%), and the highest point prevalence was 91.6% (95% CI, 84.8%-94.4%) as diagnosed by placental histology, impression, and smears with microscopy in Ebolowa, Cameroon.23

Dual Prevalence of STIs/RTIs and Malaria

Only 5 publications reported the prevalence of syphilis and malaria,2428 and no single article reported coinfection of malaria and STIs/RTIs. Subanalysis in a prospective cohort study of pregnant women in Tanzania provided some of the only published data on coinfection: 48.3% of RPR-positive women also had placental parasitemia and 35.0% of RPR-negative women had malaria-infected placentas (P < .001).29

This systematic review of STIs/RTIs and malaria prevalence estimates over a 20-year period suggests that a considerable burden of malaria and STIs/RTIs exists at the population level among pregnant women attending antenatal facilities in sub-Saharan Africa. However, the absence of reports on coinfection makes it impossible to describe the prevalence of malaria only, curable STIs/RTIs only, or coinfection in pregnancy.

The GRADE approach to data quality assessment30 was considered inappropriate for this particular meta-analysis. It is a useful and transparent tool for the analysis of treatment outcomes following contrasting interventions produced by different study designs. However, because we included studies that had open enrollment in the antenatal care setting and we were not investigating the effect of medical intervention, we did not expect the population prevalence of STIs/RTIs and malaria in pregnancy to vary across study designs. In addition, the GRADE system requires ranking of evidence by outcomes of interest, scored as high, intermediate, low, or very low. In this review, we could have assigned quality scores to point prevalence estimates, but that would have introduced a limited but unavoidable level of subjectivity. Thus, we chose instead to improve the precision of each point estimate with a standard method9 for correcting errors of known magnitude before incorporating data into the random-effects models. This same approach has been used with prevalence data from Tanzania to compare STI/RTI estimates derived by disparate diagnostic tests.31 We present corrected and uncorrected point prevalence estimates by study in eTable 1 through eTable 7.

Diagnostic methods and tools have changed for many pathogens during the period covered in this review. The advent of molecular tests such as PCR and ligase chain reaction has allowed researchers in recent years to detect infection where older diagnostic methods may have failed to do so. Although our statistical correction for diagnostic errors can make data more comparable, the pooled mean prevalence of STIs/RTIs and malaria is still probably an underestimate of the true burden of disease. Among 59 studies providing estimates for syphilis prevalence, 45 used the nontreponemal RPR or venereal disease research laboratory tests confirmed by a Treponema -specific test, reflecting wide acceptance of the diagnostic gold standard. Because biological false-positive nontreponemal test results can be produced by malaria and other infections, the burden of syphilis in studies that did not use treponemal confirmatory testing may be overstated.

A variety of diagnostic methods were used for identifying N gonorrhoeae and C trachomatis infections, whereas wet-mount microscopy was used in all but 2 studies reporting trichomoniasis prevalence, a method notoriously lacking sensitivity compared with culture or molecular tests.32,33 Bacterial vaginosis was diagnosed using 4 methods: Nugent score, Spiegel criteria, Amsel criteria, and clue cell prevalence estimates. The Nugent score34 is the preferred objective method and was used in studies reporting the 7 highest rates of infection from East and Southern Africa. Thus, the pooled mean prevalence would likely have been higher had the Nugent score been used in all studies.

Peripheral parasitemia may be underrepresented for 2 reasons. Infection tends to be highest between gestational weeks 9 through 16, declining until term.35,36 No studies appeared to have measured peripheral parasitemia during this peak period. Another important source of underestimated disease burden is that most malaria diagnoses were based on microscopy without molecular test correction. A study in Blantyre, Malawi, illustrates the extent to which underdiagnosis may occur with conventional microscopy; the prevalence of peripheral parasitemia of 51.9% (95% CI, 43.4%-60.3%) was found by PCR, while microscopy detected infection only in 14.9% (95% CI, 11.8%-18.0%) of pregnant women.37

The dual prevalence of STIs/RTIs and malaria varied in the subregions we analyzed. Overall, East and Southern Africa has a greater burden of STIs/RTIs compared with West and Central Africa. Several factors that are linked to exposure may contribute to this difference, including higher prevalence of STIs/RTIs circulating at the community level, patterns of male circumcision as well as sexual behavior related to age of sexual debut, age at first marriage, premarital sex, and number of total partners and concurrent sex partners. The prevalence of HIV, for example, remains substantially higher in East and Southern Africa compared with the West and Central subregion. According to the Joint United Nations Programme on HIV/AIDS, 34% of the world's HIV-positive population was living in 10 countries of Southern Africa in 2010.38 The epidemic in East Africa has declined over the past decade, but HIV prevalence remains higher than in West and Central Africa.

Quiz Ref IDPeripheral and placental malaria is slightly higher in West and Central Africa compared with the East and Southern subregion. This may be due to greater seasonal variation in transmission within West and Central Africa. Recent declines in malaria transmission within selected locales of Africa will likely translate into fewer pregnant women acquiring immunity from one pregnancy to the next. Thus, all women in their reproductive years (rather than just those in their first or second pregnancies) may remain vulnerable to malaria in the years ahead until the absolute risk of exposure is negligible.

Quiz Ref IDHuman immunodeficiency virus and malaria interact to increase parasitic infection of the placenta and incidence of low birth weight.39Plasmodium falciparum infection also increases viral load among HIV-positive pregnancy women.40 New evidence suggests that malaria parasites are more likely to develop wild-type mutations following exposure to sulfadoxine-pyrimethamine as intermittent preventive treatment during pregnancy (IPTp) when administered to HIV-positive women.41 The interaction between STIs/RTIs and HIV has been well established, although providing presumptive treatment for STIs/RTIs to pregnant women in Rakai, Uganda, has not shown protective effect against maternal to child transmission of HIV.42 However, malaria chemoprophylaxis was not provided in this study; therefore, the potential modulating effect of malaria on maternal to child transmission in the presence of STIs/RTIs remains unknown.

Our study has several limitations. An unavoidable but important limitation is the inherent delay between gathering evidence at the clinic level and public dissemination. This is important in our study because HIV prevention campaigns, including STI/RTI screening and treatment programs, have made inroads in reducing transmission in many settings. To capture these reductions with greater precision, more recent data are needed. Another limitation is that even after stratifying by geography and age of study, heterogeneity among studies persisted. The random-effects models, in turn, produced wide 95% confidence intervals in some instances. In addition, because we relied on evidence from English-language sources and abstracts that had been translated into English, we may have identified fewer studies from researchers who publish in other languages.

There is a major risk of adverse birth outcomes associated with malaria and STIs/RTIs in pregnancy. More than 30 million pregnant women are at risk of infection each year in sub-Saharan Africa.43 Malaria is associated with intrauterine growth retardation, preterm delivery, low birth weight,44,45 stillbirth,44 early neonatal death,44 and maternal anemia.45 In Tanzania, T pallidum is associated with 51% of stillbirths and 24% of preterm live births.46Neisseria gonorrhoeae is associated with a 2-fold increase in the risk of preterm delivery,47 whereas the risk of early preterm delivery in the presence of C trachomatis infection is 4 times higher.48 Untreated C trachomatis infects the eyes of 50% of newborns at delivery, and pneumonia will develop in 10% to 20% of these infants.49,50Neisseria gonorrhoeae and C trachomatis are common causes of ophthalmia neonatorum and may lead to corneal scarring and blindness if untreated. Trichomonas vaginalis infection is associated with a 2-fold increase in preterm delivery,51 as is bacterial vaginosis, the odds of which are 7 times higher when the condition manifests prior to 16 weeks' gestation.52 Bacterial vaginosis is also significantly associated with the risk of spontaneous abortion.52 Within this context, progress toward the maternal and child health targets of Millennium Development Goals may be possible by improving malaria and STI/RTI control measures within the antenatal care package.

Quiz Ref IDSeveral current infection control strategies are included in the antenatal care package. In areas of stable malaria transmission, WHO recommends that pregnant women sleep under insecticide-treated mosquito bed nets and receive 2 to 3 treatment courses of SP-IPTp during antenatal consultations. Drug resistance to SP has compromised the protective effect of SP-IPTp in recent years, prompting a need to identify efficacious drugs and new strategies to prevent malaria in pregnancy.53

WHO recommends syphilis screening and treatment for pregnant women at their first antenatal visit. For other curable STIs/RTIs, WHO suggests using syndrome-based algorithms to guide diagnosis and treatment. However, the vast majority of gonococcal (80%) and chlamydial (70%-75%) infections in women are asymptomatic54 and therefore never diagnosed. Consequently, the algorithm based on vaginal discharge syndrome has a low sensitivity (30%-80%) and specificity (40%-80%) for N gonorrhoeae and C trachomatis among pregnant women.5557 Syndromic management has slightly higher sensitivity for T vaginalis (54%-83%) and bacterial vaginosis (51%-69%), with moderate specificity (40%-54% for T vaginalis and 40%-58% for bacterial vaginosis).58

In addition, potential new directions for the antenatal care package have been suggested, including use of novel drugs and rapid diagnostic tests. Several trials of azithromycin-based combination therapies are under investigation for use in IPTp. Azithromycin has modest antimalarial properties but needs a partner antimalarial drug against P falciparum.59 Despite concerns about drug resistance,60 a 2-g dose of azithromycin has resulted in cure rates of 97.7% (95% CI, 94.0%-99.4%) of syphilis cases in a study in Tanzania.61 A single 2-g dose of azithromycin was 98.9% (95% CI, 97.9%-100%) efficacious against N gonorrhoeae in the United States,62 while meta-analysis showed that 1 g cures 96.5% (95% CI, 95.3%-97.7%) of C trachomatis infections.63 A trial in Malawi using 1 g of azithromycin administered twice with SP-IPTp reduced the risk of T vaginalis 35% (P = .02).64 Azithromycin-based combinations could protect against bacterial vaginosis if administered early in pregnancy; a meta-analysis of antibiotic therapy for the treatment of bacterial vaginosis in pregnancy prior to gestational week 20 is associated with a significant reduction in the risk of preterm birth.65

Novel use of rapid diagnostic tests may replace IPTp with sulfadoxine-pyrimethamine altogether if used for intermittent screening and treatment for malaria during antenatal visits. Intermittent screening and treatment with artesunate-amodiaquine was noninferior to IPTp with sulfadoxine-pyrimethamine in Ghana in an area where sulfadoxine-pyrimethamine resistance was low; the incidence of low birth weight was similar between the IPTp with sulfadoxine-pyrimethamine and intermittent screening and treatment groups among multigravid mothers (11.3% vs 11.3%) and among primigravid mothers (16.1% vs 17.2%).66 Rapid point-of-care tests for HIV have revolutionized the uptake and performance of voluntary counseling and testing67 and are used in some antenatal settings in Africa. Point-of-care tests for syphilis are increasingly available, making possible same-day results and prompt treatment.68,69

Mitigating the dual prevalence of malaria and STIs/RTIs will require improvements in the Safe Motherhood package.70 Bacterial vaginosis requires particular attention given its high prevalence. Clinical trials are needed to investigate the protective effect of presumptive treatment of bacterial vaginosis with metronidazole at time points that are biologically optimal and operationally feasible. It is less clear whether pregnancy outcomes would be improved more with point-of-care tests and treatment for HIV, syphilis, and malaria, while syndromic management is provided for the remaining curable STIs/RTIs—or if maternal, fetal, and newborn health will be better if women are given point-of-care tests for HIV and syphilis along with azithromycin-based combination therapy in IPTp. Rigorously conducted clinical trials are urgently needed.

The dual prevalence of malaria and STIs/RTIs is evident among pregnant women who attend antenatal facilities in sub-Saharan Africa. As malaria control and elimination efforts are brought to scale, the relative contribution of STIs/RTIs to adverse birth outcomes most likely will increase proportionately. Coinfection prevalence estimates for malaria and STIs/RTIs need to be established and routinely reported. Rigorous studies using molecular diagnostic methods are needed to characterize more accurately the prevalence of these infections and their clinical consequences. Clinical trials are needed to compare birth outcomes, operational feasibility/acceptability, and cost-effectiveness of IPTp with azithromycin-based combination therapy against an approach of integrated screening and treatment for malaria and STIs/RTIs.

Corresponding Author: R. Matthew Chico, MPH, London School of Hygiene and Tropical Medicine, Keppel Street, Room 445, London WC1E 7HT, England (matthew.chico@lshtm.ac.uk).

Author Contributions: Mr Chico and Dr Chandramohan had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Study concept and design: Chandramohan.

Acquisition of data: Chico.

Analysis and interpretation of data: Chico, Mayaud, Mabey, Ariti, Ronsmans, Chandramohan.

Drafting of the manuscript: Chico.

Critical revision of the manuscript for important intellectual content: Chico, Mayaud, Mabey, Ariti, Ronsmans, Chandramohan.

Statistical analysis: Chico, Ariti.

Administrative, technical, or material support: Chico, Mayaud, Mabey, Ariti, Ronsmans, Chandramohan.

Study supervision: Chandramohan.

Conflict of Interest Disclosures: All authors have completed and submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Mr Chico reports having previously received funding as part of 2 studies co-financed by Pfizer and the Medicines for Malaria Venture that are investigating the use of azithromycin plus chloroquine in IPTp. No other disclosures were reported.

Additional Contributions: We are grateful to Rosanna Peeling, PhD, London School of Hygiene and Tropical Medicine, for reviewing the data and assisting in the classification of methods by quality, and Mythili Ramakrishna, BDS, MSc, London School of Hygiene and Tropical Medicine, for screening studies against inclusion/exclusion criteria separately from Mr Chico. Dr Ramakrishna was compensated for her contribution. No other compensation was received.

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PubMed
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PubMed
Wessel HF, Herrmann B, Dupret A, Moniz F, Brito C, Bergström S. Genital infections among antenatal care attendees in Cape Verde.  Afr J Reprod Health. 1998;2(1):32-40
PubMed
Ndyomugyenyi R, Magnussen P. Anaemia in pregnancy: Plasmodium falciparum infection is an important cause in primigravidae in Hoima district, western Uganda.  Ann Trop Med Parasitol. 1999;93(5):457-465
PubMed   |  Link to Article
Leke RF, Bioga JD, Zhou J,  et al.  Longitudinal studies of Plasmodium falciparum malaria in pregnant women living in a rural Cameroonian village with high perennial transmission.  Am J Trop Med Hyg. 2010;83(5):996-1004
PubMed   |  Link to Article
Kassam SN, Nesbitt S, Hunt LP, Oster N, Soothill P, Sergi C. Pregnancy outcomes in women with or without placental malaria infection.  Int J Gynaecol Obstet. 2006;93(3):225-232
PubMed   |  Link to Article
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 Cameroon.  Am J Trop Med Hyg. 1995;53(6):581-585
PubMed
Ayisi JG, van Eijk AM, ter Kuile FO,  et al.  Risk factors for HIV infection among asymptomatic pregnant women attending an antenatal clinic in western Kenya.  Int J STD AIDS. 2000;11(6):393-401
PubMed   |  Link to Article
Luján J, de Oñate WA, Delva W,  et al.  Prevalence of sexually transmitted infections in women attending antenatal care in Tete province, Mozambique.  S Afr Med J. 2008;98(1):49-51
PubMed
Menéndez C, Castellsagué X, Renom M,  et al.  Prevalence and risk factors of sexually transmitted infections and cervical neoplasia in women from a rural area of southern Mozambique.  Infect Dis Obstet Gynecol. 2010;2010:609315Link to Article
PubMed   |  Link to Article
Montoya PJ, Lukehart SA, Brentlinger PE,  et al.  Comparison of the diagnostic accuracy of a rapid immunochromatographic test and the rapid plasma reagin test for antenatal syphilis screening in Mozambique.  Bull World Health Organ. 2006;84(2):97-104
PubMed   |  Link to Article
van den Broek NR, White SA, Goodall M,  et al.  The APPLE study: a randomized, community-based, placebo-controlled trial of azithromycin for the prevention of preterm birth, with meta-analysis.  PLoS Med. 2009;6(12):e1000191
PubMed   |  Link to Article
Watson-Jones D, Weiss HA, Changalucha JM,  et al.  Adverse birth outcomes in United Republic of Tanzania—impact and prevention of maternal risk factors.  Bull World Health Organ. 2007;85(1):9-18
PubMed   |  Link to Article
Guyatt GH, Oxman AD, Vist GE,  et al; GRADE Working Group.  GRADE: an emerging consensus on rating quality of evidence and strength of recommendations.  BMJ. 2008;336(7650):924-926
PubMed   |  Link to Article
Orroth KK, Korenromp EL, White RG,  et al.  Comparison of STD prevalences in the Mwanza, Rakai, and Masaka trial populations: the role of selection bias and diagnostic errors.  Sex Transm Infect. 2003;79(2):98-105
PubMed   |  Link to Article
Fouts AC, Kraus SJ. Trichomonas vaginalis: reevaluation of its clinical presentation and laboratory diagnosis.  J Infect Dis. 1980;141(2):137-143
PubMed   |  Link to Article
van Der Schee C, van Belkum A, Zwijgers L,  et al.  Improved diagnosis of Trichomonas vaginalis infection by PCR using vaginal swabs and urine specimens compared to diagnosis by wet mount microscopy, culture, and fluorescent staining.  J Clin Microbiol. 1999;37(12):4127-4130
PubMed
Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of Gram stain interpretation.  J Clin Microbiol. 1991;29(2):297-301
PubMed
Brabin BJ. An analysis of malaria in pregnancy in Africa.  Bull World Health Organ. 1983;61(6):1005-1016
PubMed
Brabin B. The Risks and Severity of Malaria in Pregnant Women: Applied Field Research in Malaria Reports. Geneva, Switzerland: Special Programme for Research and Training in Tropical Diseases, World Health Organization; 1991
Mankhambo L, Kanjala M, Rudman S, Lema VM, Rogerson SJ. Evaluation of the OptiMAL rapid antigen test and species-specific PCR to detect placental Plasmodium falciparum infection at delivery.  J Clin Microbiol. 2002;40(1):155-158
PubMed   |  Link to Article
Joint United Nations Programme on HIV/AIDS.  Report on the Global AIDS Epidemic 2010. Geneva, Switzerland: Joint United Nations Programme on HIV/AIDS; 2010
Ayisi JG, van Eijk AM, ter Kuile FO,  et al.  The effect of dual infection with HIV and malaria on pregnancy outcome in western Kenya.  AIDS. 2003;17(4):585-594
PubMed   |  Link to Article
Ayisi JG, van Eijk AM, Newman RD,  et al.  Maternal malaria and perinatal HIV transmission, western Kenya.  Emerg Infect Dis. 2004;10(4):643-652
PubMed   |  Link to Article
Menéndez C, Serra-Casas E, Scahill MD,  et al.  HIV and placental infection modulate the appearance of drug-resistant Plasmodium falciparum in pregnant women who receive intermittent preventive treatment.  Clin Infect Dis. 2011;52(1):41-48
PubMed   |  Link to Article
Gray RH, Wabwire-Mangen F, Kigozi G,  et al.  Randomized trial of presumptive sexually transmitted disease therapy during pregnancy in Rakai, Uganda.  Am J Obstet Gynecol. 2001;185(5):1209-1217
PubMed   |  Link to Article
Dellicour S, Tatem AJ, Guerra CA, Snow RW, ter Kuile FO. Quantifying the number of pregnancies at risk of malaria in 2007: a demographic study.  PLoS Med. 2010;7(1):e1000221
PubMed   |  Link to Article
van Geertruyden JP, Thomas F, Erhart A, D’Alessandro U. The contribution of malaria in pregnancy to perinatal mortality.  Am J Trop Med Hyg. 2004;71(2):(suppl)  35-40
PubMed
Kalilani L, Mofolo I, Chaponda M, Rogerson S, Meshnick S. The effect of timing and frequency of malaria infection during pregnancy on low birth weight and maternal anemia.  Am J Trop Med Hyg. 2006;75(5):414
Watson-Jones D, Changalucha J, Gumodoka B,  et al.  Syphilis in pregnancy in Tanzania, I: impact of maternal syphilis on outcome of pregnancy.  J Infect Dis. 2002;186(7):940-947
PubMed   |  Link to Article
Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth.  Lancet. 2008;371(9606):75-84
PubMed   |  Link to Article
Rours GI, Duijts L, Moll HA,  et al.  Chlamydia trachomatis infection during pregnancy associated with preterm delivery: a population-based prospective cohort study.  Eur J Epidemiol. 2011;26(6):493-502
PubMed   |  Link to Article
Schachter J, Grossman M, Sweet RL, Holt J, Jordan C, Bishop E. Prospective study of perinatal transmission of Chlamydia trachomatis JAMA. 1986;255(24):3374-3377
PubMed   |  Link to Article
Hammerschlag MR. Chlamydial and gonococcal infections in infants and children.  Clin Infect Dis. 2011;53:(suppl 3)  S99-S102
PubMed   |  Link to Article
French JI, McGregor JA, Parker R. Readily treatable reproductive tract infections and preterm birth among black women.  Am J Obstet Gynecol. 2006;194(6):1717-1726
PubMed   |  Link to Article
Leitich H, Bodner-Adler B, Brunbauer M, Kaider A, Egarter C, Husslein P. Bacterial vaginosis as a risk factor for preterm delivery: a meta-analysis.  Am J Obstet Gynecol. 2003;189(1):139-147
PubMed   |  Link to Article
Chico RM, Chandramohan D. Intermittent preventive treatment of malaria in pregnancy: at the crossroads of public health policy.  Trop Med Int Health. 2011;16(7):774-785
PubMed   |  Link to Article
World Health Organization.  Global Prevalence and Incidence of Selected Curable Sexually Transmitted Infections: Overview and EstimatesGeneva, Switzerland: World Health Organization; 2001
Mayaud P, ka-Gina G, Cornelissen J,  et al.  Validation of a WHO algorithm with risk assessment for the clinical management of vaginal discharge in Mwanza, Tanzania.  Sex Transm Infect. 1998;74:(suppl 1)  S77-S84
PubMed
Vuylsteke B, Laga M, Alary M,  et al.  Clinical algorithms for the screening of women for gonococcal and chlamydial infection: evaluation of pregnant women and prostitutes in Zaire.  Clin Infect Dis. 1993;17(1):82-88
PubMed   |  Link to Article
Costello Daly C, Wangel AM, Hoffman IF,  et al.  Validation of the WHO diagnostic algorithm and development of an alternative scoring system for the management of women presenting with vaginal discharge in Malawi.  Sex Transm Infect. 1998;74:(suppl 1)  S50-S58
PubMed   |  Link to Article
Tann CJ, Mpairwe H, Morison L,  et al.  Lack of effectiveness of syndromic management in targeting vaginal infections in pregnancy in Entebbe, Uganda.  Sex Transm Infect. 2006;82(4):285-289
PubMed   |  Link to Article
Chico RM, Pittrof R, Greenwood B, Chandramohan D. Azithromycin-chloroquine and the intermittent preventive treatment of malaria in pregnancy.  Malar J. 2008;7(1):255
PubMed   |  Link to Article
Mabey D. Azithromycin resistance in Treponema pallidum Sex Transm Dis. 2009;36(12):777-778
PubMed   |  Link to Article
Riedner G, Rusizoka M, Todd J,  et al.  Single-dose azithromycin vs penicillin G benzathine for the treatment of early syphilis.  N Engl J Med. 2005;353(12):1236-1244
PubMed   |  Link to Article
Handsfield HH, Dalu ZA, Martin DH, Douglas JM Jr, McCarty JM, Schlossberg D.Azithromycin Gonorrhea Study Group.  Multicenter trial of single-dose azithromycin vs ceftriaxone in the treatment of uncomplicated gonorrhea.  Sex Transm Dis. 1994;21(2):107-111
PubMed   |  Link to Article
Lau CY, Qureshi AK. Azithromycin vs doxycycline for genital chlamydial infections: a meta-analysis of randomized clinical trials.  Sex Transm Dis. 2002;29(9):497-502
PubMed   |  Link to Article
Luntamo M, Kulmala T, Mbewe B, Cheung YB, Maleta K, Ashorn P. Effect of repeated treatment of pregnant women with sulfadoxine-pyrimethamine and azithromycin on preterm delivery in Malawi: a randomized controlled trial.  Am J Trop Med Hyg. 2010;83(6):1212-1220
PubMed   |  Link to Article
McDonald HM, Brocklehurst P, Gordon A. Antibiotics for treating bacterial vaginosis in pregnancy.  Cochrane Database Syst Rev. 2007;(1):CD000262
PubMed
Tagbor H, Bruce J, Agbo M, Greenwood B, Chandramohan D. Intermittent screening and treatment vs intermittent preventive treatment of malaria in pregnancy: a randomised controlled non-inferiority trial.  PLoS One. 2010;5(12):e14425
PubMed   |  Link to Article
Dewsnap CH, Mcowan A. A review of HIV point-of-care tests.  Int J STD AIDS. 2006;17(6):357-359
PubMed   |  Link to Article
Peeling R. The Sexually Transmitted Diseases Diagnostics Initiative: Laboratory Based Evaluation of Rapid Syphilis Diagnostics. Geneva, Switzerland: World Health Organization; 2003
Peeling RW, Ye H. Diagnostic tools for preventing and managing maternal and congenital syphilis: an overview.  Bull World Health Organ. 2004;82(6):439-446
PubMed
Mahler H. The Safe Motherhood initiative: a call to action.  Lancet. 1987;1(8534):668-670
PubMed   |  Link to Article

Figures

Place holder to copy figure label and caption
Figure 1. Identification, Screening, and Eligibility of Studies in the Meta-analysis
Graphic Jump Location

aData believed to have appeared in more than 1 article were reviewed in full text and therefore do not appear under records excluded.

Place holder to copy figure label and caption
Figure 2. Curable STI/RTI and Malaria Infection Among Pregnant Women Attending Antenatal Facilities in Africa by Subregion
Graphic Jump Location

Diamonds indicate pooled mean prevalence estimates; the extremes of the diamonds indicate 95% CIs. Horizontal bars indicate lowest to highest point prevalence estimates. STI/RTI indicates sexually transmitted infection/reproductive tract infection.
aPlacental malaria is measured at delivery.

Tables

Table Graphic Jump LocationTable. Pooled Mean Prevalence Estimates Among Pregnant Women Attending Antenatal Care Facilities in Sub-Saharan Africa

References

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Mbopi Kéou FX, Mbu R, Mauclère P,  et al.  Antenatal HIV prevalence in Yaounde, Cameroon.  Int J STD AIDS. 1998;9(7):400-402
PubMed   |  Link to Article
Diallo MO, Ettiègne-Traoré V, Maran M,  et al.  Sexually transmitted diseases and human immunodeficiency virus infections in women attending an antenatal clinic in Abidjan, Côte d’Ivoire.  Int J STD AIDS. 1997;8(10):636-638
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Ortashi OM, El Khidir I, Herieka E. Prevalence of HIV, syphilis, Chlamydia trachomatis, Neisseria gonorrhoeae, Trichomonas vaginalis and candidiasis among pregnant women attending an antenatal clinic in Khartoum, Sudan.  J Obstet Gynaecol. 2004;24(5):513-515
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Van Dyck E, Samb N, Sarr AD,  et al.  Accuracy of 2 enzyme immunoassays and cell culture in the detection of Chlamydia trachomatis in low and high risk populations in Senegal.  Eur J Clin Microbiol Infect Dis. 1992;11(6):527-534
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Mayaud P, Msuya W, Todd J,  et al.  STD rapid assessment in Rwandan refugee camps in Tanzania.  Genitourin Med. 1997;73(1):33-38
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Ogbonna CI, Ogbonna IB, Ogbonna AA, Anosike JC. Studies on the incidence of Trichomonas vaginalis amongst pregnant women in Jos area of Plateau State, Nigeria.  Angew Parasitol. 1991;32(4):198-204
PubMed
Wessel HF, Herrmann B, Dupret A, Moniz F, Brito C, Bergström S. Genital infections among antenatal care attendees in Cape Verde.  Afr J Reprod Health. 1998;2(1):32-40
PubMed
Ndyomugyenyi R, Magnussen P. Anaemia in pregnancy: Plasmodium falciparum infection is an important cause in primigravidae in Hoima district, western Uganda.  Ann Trop Med Parasitol. 1999;93(5):457-465
PubMed   |  Link to Article
Leke RF, Bioga JD, Zhou J,  et al.  Longitudinal studies of Plasmodium falciparum malaria in pregnant women living in a rural Cameroonian village with high perennial transmission.  Am J Trop Med Hyg. 2010;83(5):996-1004
PubMed   |  Link to Article
Kassam SN, Nesbitt S, Hunt LP, Oster N, Soothill P, Sergi C. Pregnancy outcomes in women with or without placental malaria infection.  Int J Gynaecol Obstet. 2006;93(3):225-232
PubMed   |  Link to Article
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 Cameroon.  Am J Trop Med Hyg. 1995;53(6):581-585
PubMed
Ayisi JG, van Eijk AM, ter Kuile FO,  et al.  Risk factors for HIV infection among asymptomatic pregnant women attending an antenatal clinic in western Kenya.  Int J STD AIDS. 2000;11(6):393-401
PubMed   |  Link to Article
Luján J, de Oñate WA, Delva W,  et al.  Prevalence of sexually transmitted infections in women attending antenatal care in Tete province, Mozambique.  S Afr Med J. 2008;98(1):49-51
PubMed
Menéndez C, Castellsagué X, Renom M,  et al.  Prevalence and risk factors of sexually transmitted infections and cervical neoplasia in women from a rural area of southern Mozambique.  Infect Dis Obstet Gynecol. 2010;2010:609315Link to Article
PubMed   |  Link to Article
Montoya PJ, Lukehart SA, Brentlinger PE,  et al.  Comparison of the diagnostic accuracy of a rapid immunochromatographic test and the rapid plasma reagin test for antenatal syphilis screening in Mozambique.  Bull World Health Organ. 2006;84(2):97-104
PubMed   |  Link to Article
van den Broek NR, White SA, Goodall M,  et al.  The APPLE study: a randomized, community-based, placebo-controlled trial of azithromycin for the prevention of preterm birth, with meta-analysis.  PLoS Med. 2009;6(12):e1000191
PubMed   |  Link to Article
Watson-Jones D, Weiss HA, Changalucha JM,  et al.  Adverse birth outcomes in United Republic of Tanzania—impact and prevention of maternal risk factors.  Bull World Health Organ. 2007;85(1):9-18
PubMed   |  Link to Article
Guyatt GH, Oxman AD, Vist GE,  et al; GRADE Working Group.  GRADE: an emerging consensus on rating quality of evidence and strength of recommendations.  BMJ. 2008;336(7650):924-926
PubMed   |  Link to Article
Orroth KK, Korenromp EL, White RG,  et al.  Comparison of STD prevalences in the Mwanza, Rakai, and Masaka trial populations: the role of selection bias and diagnostic errors.  Sex Transm Infect. 2003;79(2):98-105
PubMed   |  Link to Article
Fouts AC, Kraus SJ. Trichomonas vaginalis: reevaluation of its clinical presentation and laboratory diagnosis.  J Infect Dis. 1980;141(2):137-143
PubMed   |  Link to Article
van Der Schee C, van Belkum A, Zwijgers L,  et al.  Improved diagnosis of Trichomonas vaginalis infection by PCR using vaginal swabs and urine specimens compared to diagnosis by wet mount microscopy, culture, and fluorescent staining.  J Clin Microbiol. 1999;37(12):4127-4130
PubMed
Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of Gram stain interpretation.  J Clin Microbiol. 1991;29(2):297-301
PubMed
Brabin BJ. An analysis of malaria in pregnancy in Africa.  Bull World Health Organ. 1983;61(6):1005-1016
PubMed
Brabin B. The Risks and Severity of Malaria in Pregnant Women: Applied Field Research in Malaria Reports. Geneva, Switzerland: Special Programme for Research and Training in Tropical Diseases, World Health Organization; 1991
Mankhambo L, Kanjala M, Rudman S, Lema VM, Rogerson SJ. Evaluation of the OptiMAL rapid antigen test and species-specific PCR to detect placental Plasmodium falciparum infection at delivery.  J Clin Microbiol. 2002;40(1):155-158
PubMed   |  Link to Article
Joint United Nations Programme on HIV/AIDS.  Report on the Global AIDS Epidemic 2010. Geneva, Switzerland: Joint United Nations Programme on HIV/AIDS; 2010
Ayisi JG, van Eijk AM, ter Kuile FO,  et al.  The effect of dual infection with HIV and malaria on pregnancy outcome in western Kenya.  AIDS. 2003;17(4):585-594
PubMed   |  Link to Article
Ayisi JG, van Eijk AM, Newman RD,  et al.  Maternal malaria and perinatal HIV transmission, western Kenya.  Emerg Infect Dis. 2004;10(4):643-652
PubMed   |  Link to Article
Menéndez C, Serra-Casas E, Scahill MD,  et al.  HIV and placental infection modulate the appearance of drug-resistant Plasmodium falciparum in pregnant women who receive intermittent preventive treatment.  Clin Infect Dis. 2011;52(1):41-48
PubMed   |  Link to Article
Gray RH, Wabwire-Mangen F, Kigozi G,  et al.  Randomized trial of presumptive sexually transmitted disease therapy during pregnancy in Rakai, Uganda.  Am J Obstet Gynecol. 2001;185(5):1209-1217
PubMed   |  Link to Article
Dellicour S, Tatem AJ, Guerra CA, Snow RW, ter Kuile FO. Quantifying the number of pregnancies at risk of malaria in 2007: a demographic study.  PLoS Med. 2010;7(1):e1000221
PubMed   |  Link to Article
van Geertruyden JP, Thomas F, Erhart A, D’Alessandro U. The contribution of malaria in pregnancy to perinatal mortality.  Am J Trop Med Hyg. 2004;71(2):(suppl)  35-40
PubMed
Kalilani L, Mofolo I, Chaponda M, Rogerson S, Meshnick S. The effect of timing and frequency of malaria infection during pregnancy on low birth weight and maternal anemia.  Am J Trop Med Hyg. 2006;75(5):414
Watson-Jones D, Changalucha J, Gumodoka B,  et al.  Syphilis in pregnancy in Tanzania, I: impact of maternal syphilis on outcome of pregnancy.  J Infect Dis. 2002;186(7):940-947
PubMed   |  Link to Article
Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth.  Lancet. 2008;371(9606):75-84
PubMed   |  Link to Article
Rours GI, Duijts L, Moll HA,  et al.  Chlamydia trachomatis infection during pregnancy associated with preterm delivery: a population-based prospective cohort study.  Eur J Epidemiol. 2011;26(6):493-502
PubMed   |  Link to Article
Schachter J, Grossman M, Sweet RL, Holt J, Jordan C, Bishop E. Prospective study of perinatal transmission of Chlamydia trachomatis JAMA. 1986;255(24):3374-3377
PubMed   |  Link to Article
Hammerschlag MR. Chlamydial and gonococcal infections in infants and children.  Clin Infect Dis. 2011;53:(suppl 3)  S99-S102
PubMed   |  Link to Article
French JI, McGregor JA, Parker R. Readily treatable reproductive tract infections and preterm birth among black women.  Am J Obstet Gynecol. 2006;194(6):1717-1726
PubMed   |  Link to Article
Leitich H, Bodner-Adler B, Brunbauer M, Kaider A, Egarter C, Husslein P. Bacterial vaginosis as a risk factor for preterm delivery: a meta-analysis.  Am J Obstet Gynecol. 2003;189(1):139-147
PubMed   |  Link to Article
Chico RM, Chandramohan D. Intermittent preventive treatment of malaria in pregnancy: at the crossroads of public health policy.  Trop Med Int Health. 2011;16(7):774-785
PubMed   |  Link to Article
World Health Organization.  Global Prevalence and Incidence of Selected Curable Sexually Transmitted Infections: Overview and EstimatesGeneva, Switzerland: World Health Organization; 2001
Mayaud P, ka-Gina G, Cornelissen J,  et al.  Validation of a WHO algorithm with risk assessment for the clinical management of vaginal discharge in Mwanza, Tanzania.  Sex Transm Infect. 1998;74:(suppl 1)  S77-S84
PubMed
Vuylsteke B, Laga M, Alary M,  et al.  Clinical algorithms for the screening of women for gonococcal and chlamydial infection: evaluation of pregnant women and prostitutes in Zaire.  Clin Infect Dis. 1993;17(1):82-88
PubMed   |  Link to Article
Costello Daly C, Wangel AM, Hoffman IF,  et al.  Validation of the WHO diagnostic algorithm and development of an alternative scoring system for the management of women presenting with vaginal discharge in Malawi.  Sex Transm Infect. 1998;74:(suppl 1)  S50-S58
PubMed   |  Link to Article
Tann CJ, Mpairwe H, Morison L,  et al.  Lack of effectiveness of syndromic management in targeting vaginal infections in pregnancy in Entebbe, Uganda.  Sex Transm Infect. 2006;82(4):285-289
PubMed   |  Link to Article
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Chico RM, Mayaud P, Ariti C, Mabey D, Ronsmans C, Chandramohan D. Prevalence of malaria and sexually transmitted and reproductive tract infections in pregnancy in sub-Saharan Africa: a systematic review. JAMA. 2012;307(19):10.1001/jama.2012.3428.

eFigure 1a. Syphilis: East and Southern Africa: Pooled mean prevalence estimate among pregnant women at antenatal care facilities

eFigure 1b. Syphilis: West and Central Africa: Pooled mean prevalence estimate among pregnant women at antenatal care facilities

eFigure 2a. Neisseria gonorrhoeae: East and Southern Africa: Pooled mean prevalence estimate among pregnant women at antenatal care facilities

eFigure 2b. Neisseria gonorrhoeae: West and Central Africa Pooled mean prevalence estimate among pregnant women at antenatal care facilities

eFigure 3a. Chlamydia trachomatis: East and Southern Africa: Pooled mean prevalence estimate among pregnant women at antenatal care facilities

eFigure 3b. Chlamydia trachomatis: West and Central Africa: Pooled mean prevalence estimate among pregnant women at antenatal care facilities

eFigure 4a. Trichomonas vaginalis: East and Southern Africa: Pooled mean prevalence estimate among pregnant women at antenatal care facilities

eFigure 4b. Trichomonas vaginalis: West and Central Africa: Pooled mean prevalence estimate among pregnant women at antenatal care facilities

eFigure 5a. Bacterial vaginosis: East and Southern Africa: Pooled mean prevalence estimate among pregnant women at antenatal care facilities

eFigure 5b. Bacterial vaginosis: West and Central Africa: Pooled mean prevalence estimate among pregnant women at antenatal care facilities

eFigure 6a. Peripheral malaria: East and Southern Africa: Pooled mean prevalence estimate among pregnant women at antenatal care facilities

eFigure 6b. Peripheral malaria: West and Central Africa: Pooled mean prevalence estimate among pregnant women at antenatal care facilities

eFigure 7a. Placental malaria: East and Southern Africa: Pooled mean prevalence estimate among pregnant women at delivery

eFigure 7b. Placental malaria: West and Central Africa: Pooled mean prevalence estimate among pregnant women at delivery

eTable 1. Syphilis Point Prevalence Estimates Among Pregnant Women at Antenatal Care Facilities in Sub-Saharan Africa

eTable 2. Neisseria gonorrhoeae Point Prevalence Estimates Among Pregnant Women at Antenatal Care Facilities in Sub-Saharan Africa

eTable 3. Chlamydia trachomatis Point Prevalence Estimates Among Pregnant Women at Antenatal Care Facilities in Sub-Saharan Africa

eTable 4. Trichomonas vaginalis Point Prevalence Estimates Among Pregnant Women at Antenatal Care Facilities in Sub-Saharan Africa

eTable 5. Bacterial Vaginosis Point Prevalence Estimates Among Pregnant Women at Antenatal Care Facilities in Sub-Saharan Africa

eTable 6. Peripheral Malaria Point Prevalence Estimates Among Pregnant Women at Antenatal Care Facilities in Sub-Saharan Africa

eTable 7. Placental Malaria Point Prevalence Estimates Among Pregnant Women at Antenatal Care Facilities in Sub-Saharan Africa

eAppendix 1. Search Terms

eAppendix 2. Published Sensitivity and Specificity Measures for Diagnostic Methods Used

eAppendix 3. References for Studies Used in Meta-analysis and eAppendix 2

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