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Intermittent Preventive Treatment of Malaria in Pregnancy: at the Crossroads of Public Health Policy

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Intermittent Preventive Treatment of Malaria in Pregnancy: at the Crossroads of Public Health Policy Tropical Medicine and International Health doi:10.1111/j.1365-3156.2011.02765.x volume 00 no 00 Systematic Review Intermittent preventive treatment of malaria in pregnancy: at the crossroads of public health policy R. Matthew Chico and Daniel Chandramohan Department of Disease Control, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, UK Summary The intermittent preventive treatment of malaria in pregnancy (IPTp) with sulphadoxine-pyrimethamine (SP) has been a key component of the focused antenatal care package for nearly a decade, reducing the burden of low birthweight attributable to malaria in sub-Saharan Africa. However, SP has lost parasite sensitivity in many sub-Saharan locations during the same period, rendering its beneficial effect in IPTp debatable. Malaria transmission has also declined in some epidemiological settings. There is no evidence to suggest, however, that the risk of malaria in pregnancy without preventive measures has declined in the same locations. Thus, the urgency to identify efficacious drugs and ⁄ or new strategies to prevent malaria in pregnancy remains as great as ever. We summarise the results of recently published SP-IPTp studies from areas of high drug resistance and ⁄ or low malaria transmission. We also present the evidence for mefloquine and azithromycin-based combinations (ABCs), two leading drug options to replace SP in IPTp. We discuss optimal dosing for ABCs and their likely protection against several sexually transmitted and reproductive tract infections. We also summarise data from a diagnosis-based alternative to IPTp known as the intermittent screening and treatment (IST) for malaria. Clinical and operational research is urgently needed to compare birth outcomes achieved by IPTp with ABCs vs. IST using an efficacious antimalarial therapy. keywords pregnancy, malaria, sexually transmitted infections, Africa south of the Sahara, antenatal care, intermittent preventive treatment of malaria in pregnancy worldwide, of which 33 are in sub-Saharan Africa (WHO Introduction 2009). The unique burden of malaria in pregnancy was first The objective of SP-IPTp is to reduce the incidence of described 75 years ago (Wickaramsuriya 1937). Several poor pregnancy outcomes. Of particular importance is chemoprophylaxes in pregnancy have been used in the protecting against low birthweight (<2.5 kg) attributable decades since. The intermittent preventive treatment of to malaria. Mortality rates rise sharply among infants born malaria in pregnancy (IPTp) was first tested in 1995 as a <2.5 kg (Kramer 1987), and malaria placental infection is single, observed, therapeutic course of sulphadoxine and a key risk factor for low birthweight that is preventable by pyrimethamine (SP; 500-mg sulphadoxine and 25-mg SP-IPTp (Steketee et al. 2001). Low birthweight babies pyrimethamine per tablet; three tablets total) provided as who survive infancy have more episodes of diarrhoeal part of antenatal consultations (Shulman et al. 1999). disease and respiratory infection than children born above WHO now recommends that pregnant women in areas of the 2.5 kg threshold (Mccormick 1985; Ashworth 1998). stable transmission receive 2–3 courses of SP-IPTp after the They are also more likely to have micro-vascular condi- onset of foetal movement with each course at least tions later in life (Godfrey & Barker 2000; Osmond & 1 month apart (WHO 2009). SP-IPTp was readily incor- Barker 2000; Eriksson et al. 2001; Barker 2004) and porated into the focused antenatal care package as women are at greater risk, when adults, of developing recommended by WHO (WHO Antenatal Care Trial pre-eclampsia and delivering low birthweight infants Research Group 2002) and is now policy in 37 countries themselves (Sibai et al. 2005). Thus, increasing birthweight ª 2011 Blackwell Publishing Ltd 1 Tropical Medicine and International Health volume 00 no 00 R. M. Chico & D. Chandramohan Intermittent preventive treatment of malaria in pregnancy has public health implications that are lifelong and inter- (Table 1) suggests that SP-IPTp protection is limited where generational. However, recent evidence suggests that the the risk of personal exposure has been reduced by sleeping protective effect of SP-IPTp against low birthweight has under insecticide-treated nets (ITNs). declined substantially in areas of high SP drug resistance. Two doses of SP-IPTp had no protective effect against Alternative drugs for IPTp and ⁄ or different strategies all low birthweight [relative risk (RR), 0.99; 95% CI: 0.70– together are urgently needed. 1.39] or placental infection (RR = 1.0; 95% CI: 0.88–1.13; Despite reductions in malaria transmission in some P = 0.964) in a randomised controlled trial in Mozam- locales of sub-Saharan Africa (O’meara et al. 2010), there bique. The trial was conducted 2003–2005 among 1030 is no evidence the risk of malaria in pregnancy has also women of all gravidae, 90% of whom used ITNs. SP-IPTp fallen without preventive measures in the same areas. did, however, confer some important benefits. Women Plasmodium falciparum is the most common form of given SP had 40% fewer clinical malaria cases (95% CI: malaria in the sub-Saharan region and is uniquely respon- 7.40–61.20; P = 0.020) and half the prevalence of periph- sible for placental infection. Primigravidae are most at risk eral parasitaemia (7.10% vs. 15.15%; P = 0.001). SP-IPTp because of their lack of anti-adhesion antibodies that provided greater protection than ITNs alone against prevent parasites from binding to placental chondroitin malaria parasitaemia (RR = 0.52; 95% CI: 0.27–0.99; sulphate A with semi-immunity acquired following P. fal- P = 0.044) in the first 8 weeks post-partum (Menendez ciparum infection in each successive pregnancy (Fried et al. 2008). Secondary analysis showed that SP-IPTp 1998). Thus, at the population level, it is possible that the reduced early neonatal mortality by 61.3% (95% CI: 7.4– risk of adverse events associated with P. falciparum 83.8; P = 0.024; 20 deaths overall; 15 placebo vs. exposure will remain constant (and potentially increase) 5 SP-IPTp; P = 0.039; Menendez et al. 2010). for an unknown period of time while malaria control and Another placebo-controlled trial of 1035 pregnant elimination measures are scaled up and multigravidae fail multigravidae conducted 2002–2004 in The Gambia to acquire immunity through exposure in prior pregnan- reported that SP-IPTp offers no greater protection against cies. low birthweight than ITNs alone (effect difference = 28 g; We summarise results of recently published SP-IPTp 95% CI: 11–67; P = 0.16; Mbaye et al. 2006). Self- studies from areas of high SP resistance and ⁄ or low reported ITN use was 78% in both groups, although nets malaria transmission and present efficacy and safety data were not study-issued. for mefloquine and azithromycin-based combinations A lack of protective effect of SP-IPTp was observed in an (ABCs), two leading drug options to replace SP in IPTp. un-blinded randomised trial carried out from 2004 to 2007 We discuss optimal dosing for ABCs and the secondary among 5775 women of all gravidae in a low transmission benefits they would offer: clearing and ⁄ or preventing area of Uganda. No difference in the percentage of low several sexually transmitted and reproductive tract infec- birthweight infants was seen across the three intervention tions (STI ⁄ RTIs) in pregnancy. We present evidence from a groups: SP-IPTp alone (6.48%), ITNs alone (6.28%) and diagnosis-based alternative to IPTp that relies on inter- SP-IPTp plus ITNs (6.85%); P = 0.80 (Ndyomugyenyi mittent screening and treatment (IST) for malaria delivered et al. 2010). within a focused antenatal care package. Finally, we Alarming evidence comes from another cross-sectional discuss current coverage rates of antenatal care, the study in Tanzania with data from 2002 to 2005. Placental growing use of point-of-care diagnostic tools for HIV and parasitaemia was significantly higher in women given any syphilis, and the implications of incorporating a rapid dose of SP-IPTp than in women who received none [84% malaria tests alongside them as part of IST of malaria. (87 of 104) vs. 16% (17 of 104); P = 0.03]. Bed-net use was lowest among those who received no SP-IPTp doses (23.5%) in contrast to women given treatment early in IPTp with sulphadoxine-pyrimethamine pregnancy (36%) or shortly before delivery (30%) (Har- Meta-analysis has shown that two courses of SP-IPTp rington et al. 2009). The increase in placental parasitaemia administered in areas of high malaria transmission where among women given SP-IPTp was likely the result of parasites are sensitive to the drug combination increases extreme drug resistance. A study conducted in a nearby the mean birthweight of children born to paucigravidae by area reported a day-28 SP treatment failure rate of 82% 121 g [95% confidence interval (CI): 61–180] (Garner & among children under 5 years of age with a parasite Gulmezoglu 2006). SP-IPTp has less effect on the neonatal population that exhibited near saturation of the dhfr ⁄ dhps birthweight of multigravidae because they are better able quintuple mutation and mutation along dhps gene at codon to manage parasite densities (Rogerson et al. 2007). 581 (Gesase et al. 2009). Parasites resistant to pyrimeth- However, evidence from recently published studies amine may also be able to repopulate a human host more 2 ª 2011 Blackwell Publishing Ltd ª Table 1 Low birthweight and parasitaemia (peripheral and placental)
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