Citation: Hill J, Hoyt J, van Eijk AM, ter Kuile FO, Webster J, Steketee RW (2014) Prioritizing Pregnant Women for Long-Lasting Insecticide Treated Nets through Antenatal Care Clinics. PLoS Med 11(9): e1001717. https://doi.org/10.1371/journal.pmed.1001717
Published: September 9, 2014
Copyright: © 2014 Hill et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This article was made possible by the generous support of the American people through the United States Agency for International Development (USAID) under the terms of USAID/JHU Cooperative Agreement No. GHS-A-00-09-00014-00 for the NetWorks Project. The contents are the responsibility of the authors and do not necessarily reflect the views of USAID or the United States Government. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: ANC, antenatal care; CI, confidence interval; CrI, credible interval; EPI, expanded programme on immunisation; IPTp, intermittent preventive treatment in pregnancy; ITN, insecticide treated net; LBW, low birth weight; LLIN, long-lasting insecticide treated net; MPAC, Malaria Policy Advisory Committee; PMTCT, prevention of mother to child transmission of HIV; RBM, Roll Back Malaria
Provenance: Not commissioned; externally peer reviewed
- Long-lasting insecticide treated nets (LLINs) are a powerful public health tool and, when used by pregnant women, contribute to improving maternal, neonatal, and infant health, with lasting benefits to the developing child.
- Use of LLINs among pregnant women is well below national and international targets; the median use of an insecticide treated net (ITN) the previous night among pregnant women across 37 countries for 2009–2011 was 35.3% (range, 5.2%–75.5%); ITN use was higher in areas with both a high disbursement of funds for malaria control and a lower per-head gross domestic product.
- Routine antenatal care (ANC) services constitute an important delivery channel that ensures pregnant women who attend an ANC clinic at least once (77% in sub-Saharan Africa) are covered with a LLIN from their first ANC visit in each pregnancy and plays an important role in maintaining population-level coverage between campaigns, particularly for women who become pregnant between campaigns and for infants born outside of campaign years.
- The majority of LLINs delivered from 2010–2012 in sub-Saharan Africa were through mass campaigns as countries sought to reach the 80% coverage target, and some of the LLINs used in these campaigns were re-allocated from routine ANC delivery.
- Going forward, national malaria programmes and donors alike will have to make difficult decisions to balance costs with the benefits and impact of investments in LLINs. Where choices must be made, high-risk groups (pregnant women and children under 5 years of age) should be prioritized for the same reason these groups were targeted under the pre-universal coverage WHO strategy.
The use of insecticide treated nets (ITNs), and subsequently the new generation of long-lasting insecticide treated nets (LLINs), has been a core malaria prevention strategy for more than two decades , and until 2010, distribution of LLINs targeted biologically vulnerable groups such as pregnant women and children aged less than 5 years ,. In 2008, due largely to increased funding for malaria control leading to impressive gains in LLIN coverage, the Roll Back Malaria (RBM) Partnership set a more ambitious target of universal coverage of LLINs, defined as universal access to, and use of, LLINs ,.
The strategy for achieving and maintaining universal coverage outlined by the RBM Partnership involves a combination of strategies based on mass campaigns, either target-specific or population-wide, to rapidly scale up coverage (“catch up”), complemented by continuous distribution through routine health services, including antenatal clinics, child health clinics, and expanded programme on immunisation (EPI) services (“keep up”) . The choice of the combination is generally based on existing coverage and status of available distribution mechanisms in a given country. It is well recognised that, individually, each mechanism is suboptimal to maintain universal coverage and will leave some gaps.
Use of ITNs among pregnant women is well below national and international targets; a recent meta-analysis of national survey data in 37 countries for the years 2009–2011 estimated the median use of an ITN the previous night among pregnant women was 35.3% (range 5.2%–75.5%) . ITN use was higher in areas with both a high disbursement of funds for malaria control and a lower per-head gross domestic product. Younger or adolescent, unmarried, and less educated women are significantly less likely to use ITNs, which may be related to lower affordability and in-household access among these women .
Public Health Rationale for Net Distribution to Pregnant Women
LLINs are a powerful public health tool and, when used by pregnant women, contribute to improving maternal, neonatal, and infant health, with long-lasting benefits to the developing child. Worldwide, an estimated 125 million pregnancies are at risk from malaria each year . Pregnant women are 1.5 times more susceptible to malaria infection than non-pregnant women  and malaria infection can have devastating consequences on maternal, newborn, infant, and child health. In Africa, 10,000 women , and between 75,000 and 200,000 infants , are estimated to die annually as a result of malaria infection during pregnancy, and approximately 11% (100,000) of neonatal deaths are due to low birth weight (LBW) resulting from Plasmodium falciparum infections in pregnancy . In the absence of malaria control in pregnancy, it is estimated that 11.4 million (95% credible interval [CrI], 10.7–12.1) pregnancies would have experienced P. falciparum placental infection at some stage of pregnancy, accounting for 41% of the estimated 27.6 million live births in sub-Saharan Africa in 2010 . Combined with estimates of the relationship between placental infection and the risk of LBW, 900,000 (95% CrI, 530,000–1,240,000) LBW deliveries per year were estimated to be caused by placental malaria. The end of the first trimester is a key period during which 65% (95% CrI, 61%–70%) of the potentially infected pregnancies first experience infection, and primigravidae experience a high proportion 39% (95% CrI, 33%–46%) of the total potential malaria-attributable LBW burden.
LLINs have been proven in clinical trials and in field programs to substantially reduce the adverse consequences of malaria in pregnancy, reducing maternal anaemia, severe anaemia, peripheral and placental malaria, and low birth weight –, and LLINs are highly cost effective . As a consequence, LLINs, along with intermittent preventive treatment in pregnancy (IPTp) ,,, together with effective case management of malaria, are recommended by WHO in malaria endemic settings in Africa. At 2012 coverage levels across 32 countries in sub-Saharan Africa, LLIN or IPTp use among women in their first or second pregnancies was significantly associated with a decreased risk of neonatal mortality (incidence rate ratio 0·82; 95% confidence interval (CI), 0·698–0·96) and reduced odds of low birth weight (adjusted odds ratio 0·79; 95% CI 0·73–0·86), compared with newborn babies of mothers with no protection, after controlling for potential confounding factors .
Routine Distribution through Antenatal Care Clinics—An Important “Keep Up” Strategy
The delivery of free or subsidized LLINs (or vouchers) to pregnant women through ANC services is a key strategy for controlling malaria and increases coverage and use by both pregnant women – and their infants ,. As infants in most malaria-endemic settings sleep with their mother during the first year of life (or longer), the protective effect of an LLIN delivered to a pregnant woman is therefore extended through the infant's first year of life.
Routine ANC services constitute an important delivery channel that ensures pregnant women who attend ANC at least once (77% in sub-Saharan Africa)  are covered with an LLIN from their first ANC visit and in subsequent pregnancies and plays an important role in maintaining population-level coverage between campaigns, particularly for women who become pregnant between campaigns and for infants born outside of campaign years ,. Whilst mass campaigns can rapidly scale up coverage, by as much as 30%–80% , universal coverage will not be maintained without the continuous distribution of LLINs, and ANC routine services have proven effective for reaching pregnant women ,–.
In addition, campaign delivery of LLINs to households with pregnant women , households with children under 5 years of age , or households with low socioeconomic status  has shown limited impact on increasing coverage among pregnant women , supporting the need for routine ANC services. Notwithstanding important limitations of modelling studies, which in the absence of evidence use some assumptions (costs, efficiencies of scale, data from a limited number of countries, etc.), modelling has demonstrated that a combination of an ANC- and school-based distribution would sustain the high coverage achieved in recent years by the mass campaigns . Modelling also predicts that supplementing mass distribution campaigns with ANC delivery could achieve a 1.4 times greater reduction in child mortality than mass distribution alone, as children born between campaign years would be covered during the most vulnerable time . Delivery of LLINs through ANC to pregnant women is an effective, sustainable strategy for continuous distribution ; greater effort is needed to encourage women to initiate ANC attendance early in the first trimester, and promoting the availability of a free ITN at early ANC booking may encourage women to initiate ANC earlier .
In short, the distribution of LLINs through routine services, ANC services included, is an important strategy and will require a sustained commitment to health systems strengthening; and neglecting this strategy will impede a country's ability to maintain universal coverage over the longer term. Delivery of LLINs through ANC has been observed to increase pregnant women's attendance at ANC clinics , which is an important platform through which women receive other essential antenatal care services, such as prevention of mother to child transmission of HIV (PMTCT); management of anaemia, syphilis, and other conditions; birth planning; etc. In addition, ANC clinics provide an opportunity to educate, inform, and encourage women to use ITNs.
Recent Policy and Funding for LLINs among Key Donors and Partners
The policy shift towards universal coverage reflects huge progress in malaria control and is a laudable goal that has injected enthusiasm into the global malaria community and has attracted calls for elimination. Notwithstanding, funding for malaria control peaked at $US2 billion in 2011  and has begun to decline, ushering in an era of limited resources. Amidst the push to achieve universal coverage and dwindling resources, there is the potential danger whereby “keep-up” strategies lose resources and funding to its more attractive “catch-up” counterpart.
Despite recent encouraging statistics on funding for continuous delivery systems, including ANC, increasing from 22% in 2008–2010 of all funding commitments to 42% for the 2012–2016 funding interval , the funding gap has meant that the routine systems are the first to be left unfunded. One estimate for 2013–2016 suggests current funding commitments meet just over half of countries' needs, leaving a funding gap of approximately 374 million LLINs , and in a funding review of the Global Fund to fight AIDS, Tuberculosis, and Malaria and other major donors the authors report that 70% of as-yet-unfunded LLINs are for continuous delivery systems . The majority of LLINs delivered from 2010–2012 in sub-Saharan Africa were through mass campaigns as countries sought to reach the 80% coverage target ,. Some of the LLINs used in these campaigns were re-allocated by national planners from routine ANC delivery to fill gaps in campaigns, as reported in Angola (2013), Cote d'Ivoire (2008), Cameroon (2011), Democratic Republic of Congo (2012, 2013), Kenya (2011), Malawi (2011), Nigeria (2014), Togo (2011), and Uganda (2012, 2014) (Matthew Lynch, Johns Hopkins University, personal communication, June 2014).
These trends prompted a policy recommendation from the WHO Vector Control Technical Expert Group to the Malaria Policy Advisory Committee (MPAC) noting that, although universal coverage was still the priority, LLINs distributed through routine channels such as ANC and EPI should continue regardless of mass campaign timing, and that nets for routine distribution should not be diverted to campaigns. This recommendation has been approved by MPAC  and a policy recommendation published .
The shortfall in funding for malaria, generally, and for LLINs, in particular, calls for endemic country programs, malaria donors, implementing agencies, and partners to adopt the most cost-effective strategies to deliver this life-saving intervention. The challenge will be to ensure that population-wide coverage does not fall while maintaining highest priority for pregnant women and children. The arguments for maintaining the ANC distribution mechanism are strong. This mechanism reaches the highest risk population of mothers and their newborns, takes advantage of the fact that most pregnant women visit ANC clinics, is the only antenatal malaria prevention intervention that provides protection in the first trimester of pregnancy, and adds an important benefit to the focused ANC delivery system as it serves to encourage ANC attendance.
Going forward, national malaria programmes and donors alike will have to make difficult decisions to balance costs with the benefits and impact of investments in LLINs. WHO's MPAC has recommended that routine LLIN distribution (through ANC and the EPI) continue “before, during, and after” campaigns, and that recommendation needs to be adopted by Ministries of Health and donors ,. For routine distribution to continue, unaffected by campaigns, donors need to make their funding commitments for LLIN procurement for both routine and campaign delivery explicit and well in advance (2 years minimum), to allow governments to plan ahead for both catch-up and keep-up. Governments will need to track both stock of LLINs and their coverage and ensure that there are sufficient commodities for delivery through both routine and campaign strategies, requiring quality data on ANC delivery of LLINs, both through strengthened Health Management Information System reporting of LLIN distribution and through national surveys. Where choices must be made, high-risk groups (pregnant women and children under 5 years of age) should be prioritized for the same reason these groups were targeted under the pre-universal coverage WHO strategy. Receiving a net as an integral part of antenatal care sends a powerful message to a pregnant woman that this tool is important to protect herself and her child. Ministries of Health need to maximise ANC opportunities, for example, to use LLINs delivery at ANC clinics to promote earlier and increased demand for ANC, and vice versa.
We are grateful to the President's Malaria Initiative's Malaria in Pregnancy working group for their input and direction on this topic and for their comments.
Conceived and designed the experiments: JHi. Performed the experiments: JHi JHo. Analyzed the data: JHi JHo AMvE FOtK JW RWS. Wrote the first draft of the manuscript: JHi. Contributed to the writing of the manuscript: JHi JHo. ICMJE criteria for authorship read and met: JHi JHo AMvE FOtK JW RWS. Agree with manuscript results and conclusions: JHi JHo AMvE FOtK JW RWS.
- 1. World Health Organization (1993) Implementation of the global malaria control strategy: report of a WHO study group on the implementation of the global plan of action for malaria control 1993–2000 [meeting held in Geneva from 8 to 12 February 1993]. WHO Study Group on the Implementation of the Global Plan of Action for Malaria Control. WHO Technical Report Series 839.
- 2. World Health Organization (2002) Scaling-Up Insecticide Treated Netting Programmes in Africa: A Strategic Framework for Coordinated National Action. WHO/CDS/RBM/2002.43. Available: http://www.unicef.org/programme/cimci/assets/ITN%20Strategic%20Framework.pdf. Accessed 5 August 2014.
- 3. World Health Organization (2004) A strategic framework for malaria prevention and control during pregnancy in the African region. Brazzaville: WHO Regional Office for Africa. Available: http://whqlibdoc.who.int/afro/2004/AFR_MAL_04.01.pdf Accessed 13 July 2014.
- 4. Roll Back Malaria Partnership (2008) The Global Malaria Action Plan. Available: http://www.rbm.who.int/gmap/gmap.pdf Accessed 27 October 2011.
- 5. World Health Organization, Global Malaria Programme (2014) WHO recommendations for achieving universal coverage with long-lasting insecticidal nets in malaria control. Available: http://www.who.int/malaria/publications/atoz/who_recommendations_universal_coverage_llins.pdf?ua=1. Accessed 10 April 2014.
- 6. World Health Organization (2013) World Malaria Report 2013. Available: http://www.who.int/malaria/publications/world_malaria_report_2013/en/ Accessed 13 July 2014.
- 7. van Eijk AM, Hill J, Larsen DA, Webster J, Steketee RW, et al. (2013) Coverage of intermittent preventive treatment and insecticide-treated nets for the control of malaria during pregnancy in sub-Saharan Africa: a synthesis and meta-analysis of national survey data, 2009–11. Lancet Infect Dis 13: 1029–1042.
- 8. Hill J, Hoyt J, van Eijk AM, D'Mello-Guyett L, Ter Kuile FO, et al. (2013) Factors affecting the delivery, access, and use of interventions to prevent malaria in pregnancy in sub-Saharan Africa: a systematic review and meta-analysis. PLoS Med 10: e1001488.
- 9. Dellicour S, Tatem AJ, Guerra CA, Snow RW, ter Kuile FO (2010) Quantifying the number of pregnancies at risk of malaria in 2007: a demographic study. PLoS Med 7: e1000221.
- 10. Taylor SM, van Eijk AM, Hand CC, Mwandagalirwa K, Messina JP, et al. (2011) Quantification of the burden and consequences of pregnancy-associated malaria in the Democratic Republic of the Congo. J Infect Dis 204: 1762–1771.
- 11. Guyatt HL, Snow RW (2001) The epidemiology and burden of Plasmodium falciparum-related anemia among pregnant women in sub-Saharan Africa. Am J Trop Med Hyg 64: 36–44.
- 12. Menendez C, Romagosa C, Ismail MR, Carrilho C, Saute F, et al. (2008) An autopsy study of maternal mortality in Mozambique: the contribution of infectious diseases. PLoS Med 5: e44.
- 13. Steketee RW, Nahlen BL, Parise ME, Menendez C (2001) The burden of malaria in pregnancy in malaria-endemic areas. Am J Trop Med Hyg 64: 28–35.
- 14. Murphy SC, Breman JG (2001) Gaps in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy. Am J Trop Med Hyg 64: 57–67.
- 15. Desai M, ter Kuile FO, Nosten F, McGready R, Asamoa K, et al. (2007) Epidemiology and burden of malaria in pregnancy. Lancet Infect Dis 7: 93–104.
- 16. Walker PGT, ter Kuile FO, Garske T, Menendez C, Ghani AC (2014) Estimates of the risk of placental infection and burden of low birthweight attributable to P. falciparum malaria in Africa in 2010. Lancet Glob Health 2: 460–467.
- 17. Menendez C, D'Alessandro U, ter Kuile FO (2007) Reducing the burden of malaria in pregnancy by preventive strategies. Lancet Infect Dis 7: 126–135.
- 18. Gamble C, Ekwaru PJ, Garner P, ter Kuile FO (2007) Insecticide-treated nets for the prevention of malaria in pregnancy: a systematic review of randomised controlled trials. PLoS Med 4: e107.
- 19. ter Kuile FO, Terlouw DJ, Phillips-Howard PA, Hawley WA, Friedman JF, et al. (2003) Reduction of malaria during pregnancy by permethrin-treated bed nets in an area of intense perennial malaria transmission in western Kenya. Am J Trop Med Hyg 68: 50–60.
- 20. Worrall E, Morel C, Yeung S, Borghi J, Webster J, et al. (2007) The economics of malaria in pregnancy–a review of the evidence and research priorities. Lancet Infect Dis 7: 156–168.
- 21. Kayentao K, Garner P, van Eijk AM, Naidoo I, Roper C, et al. (2013) Intermittent preventive therapy for malaria during pregnancy using 2 vs 3 or more doses of sulfadoxine-pyrimethamine and risk of low birth weight in Africa: systematic review and meta-analysis. JAMA 309: 594–604.
- 22. ter Kuile FO, van Eijk AM, Filler SJ (2007) Effect of sulfadoxine-pyrimethamine resistance on the efficacy of intermittent preventive therapy for malaria control during pregnancy: a systematic review. JAMA 297: 2603–2616.
- 23. Eisele TP, Larsen DA, Anglewicz PA, Keating J, Yukich J, et al. (2012) Malaria prevention in pregnancy, birthweight, and neonatal mortality: a meta-analysis of 32 national cross-sectional datasets in Africa. Lancet Infect Dis 12: 942–949.
- 24. Pettifor A, Taylor E, Nku D, Duvall S, Tabala M, et al. (2009) Free distribution of insecticide treated bed nets to pregnant women in Kinshasa: an effective way to achieve 80% use by women and their newborns. Trop Med Int Health 14: 20–28.
- 25. Guyatt H, Ochola S (2003) Use of bednets given free to pregnant women in Kenya. The Lancet 362: 1549–1550.
- 26. Marchant T, Hanson K, Nathan R, Mponda H, Bruce J, et al. (2011) Timing of delivery of malaria preventive interventions in pregnancy: results from the Tanzania national voucher programme. J Epidemiol Community Health 65: 78–82.
- 27. Hanson K, Marchant T, Nathan R, Mponda H, Jones C, et al. (2009) Household ownership and use of insecticide treated nets among target groups after implementation of a national voucher programme in the United Republic of Tanzania: plausibility study using three annual cross sectional household surveys. BMJ 339: b2434.
- 28. UNICEF (2011) Childinfo: Multiple Indicators Cluster Surveys - Round 4. Available: http://www.childinfo.org/mics4.html. Accessed 28 March 2014.
- 29. Kulkarni MA, Vanden Eng J, Desrochers RE, Cotte AH, Goodson JL, et al. (2010) Contribution of integrated campaign distribution of long-lasting insecticidal nets to coverage of target groups and total populations in malaria-endemic areas in Madagascar. Am J Trop Med Hyg 82: 420–425.
- 30. Grabowsky M, Nobiya T, Selanikio J (2007) Sustained high coverage of insecticide-treated bednets through combined Catch-up and Keep-up strategies. Trop Med Int Health 12: 815–822.
- 31. Kilian A, Wijayanandana N, Ssekitoleeko J (2010) Review of delivery strategies for insecticide treated mosquito nets - are we ready for the next phase of malaria control efforts? TropIKAnet Journal 1. ISSN 2078–8606.
- 32. West PA, Protopopoff N, Rowland MW, Kirby MJ, Oxborough RM, et al. (2012) Evaluation of a national universal coverage campaign of long-lasting insecticidal nets in a rural district in north-west Tanzania. Malar J 11: 273.
- 33. Bennett A, Juana Smith S, Yambasu S, Jambai A, Alemu W, et al. (2012) Household possession and use of insecticide-treated mosquito nets in Sierra Leone 6 months after a national mass-distribution campaign. PLoS ONE 7: e37927.
- 34. Ye Y, Patton E, Kilian A, Dovey S, Eckert E (2012) Can universal insecticide-treated net campaigns achieve equity in coverage and use? the case of northern Nigeria. Malar J 11: 32.
- 35. Hightower A, Kiptui R, Manya A, Wolkon A, Vanden Eng JL, et al. (2010) Bed net ownership in Kenya: the impact of 3.4 million free bed nets. Malar J 9: 183.
- 36. Okeibunor JC, Orji BC, Brieger W, Ishola G, Otolorin E, et al. (2011) Preventing malaria in pregnancy through community-directed interventions: evidence from Akwa Ibom State, Nigeria. Malar J 10: 227.
- 37. Khatib RA, Killeen GF, Abdulla SM, Kahigwa E, McElroy PD, et al. (2008) Markets, voucher subsidies and free nets combine to achieve high bed net coverage in rural Tanzania. Malar J 7: 98.
- 38. Ahmed SM, Zerihun A (2010) Possession and usage of insecticidal bed nets among the people of Uganda: is BRAC Uganda Health Programme pursuing a pro-poor path? PLoS ONE 5: e12660.
- 39. Koenker HM, Yukich JO, Mkindi A, Mandike R, Brown N, et al. (2013) Analysing and recommending options for maintaining universal coverage with long-lasting insecticidal nets: the case of Tanzania in 2011. Malar J 12: 150.
- 40. Okell LC, Paintain LS, Webster J, Hanson K, Lines J (2012) From intervention to impact: modelling the potential mortality impact achievable by different long-lasting, insecticide-treated net delivery strategies. Malar J 11: 327.
- 41. Sexton AR (2011) Best practices for an insecticide-treated bed net distribution programme in sub-Saharan eastern Africa. Malar J 10: 157.
- 42. Beiersmann C, De AM, Tiendrebeogo J, Ye M, Jahn A, et al. (2010) Different delivery mechanisms for insecticide-treated nets in rural Burkina Faso: a provider's perspective. Malar J 9: 352.
- 43. Paintain LS, Kolaczinski J, Renshaw M, Filler S, Kilian A, et al. (2013) Sustaining fragile gains: the need to maintain coverage with long-lasting insecticidal nets for malaria control and likely implications of not doing so. PLoS ONE 8: e83816.
- 44. Paintain L (2011) LLINs for Continuous and Campaign Distribution in Sub-Saharan Africa: A Collation of Global Funding Commitments for 2011–2016. Available: http://www.allianceformalariaprevention.com/resources/R10-2_LLINs_for_Cont_and_Campaign_Dist_GF_Commitments.pdf. Accessed 13 July 2014.
- 45. WHO Malaria Policy Advisory Committee and Secretariat (2013) Malaria Policy Advisory Committee to the WHO: conclusions and recommendations of September 2013 meeting. Malar J 12: 456.