Studies on prevalence of malaria and its adverse fetal outcomes in Federal Medical Centre (FMC), Owerri, IMO State, Nigeria

Main Article Content

Iwuchukwu IC*
Vincent CN

Abstract

Despite a massive increase in private and public efforts over the last years, malaria remains one of the most salient global health concerns. The study adopted cross sectional and descriptive survey design to assess the prevalence of maternal malaria and its adverse fetal outcomes in Federal Medical Centre (FMC), Owerri, Imo State, Nigeria from September, 2020 to March, 2021. The study population were 814 consented pregnant women in their reproductive ages (16 - 55years) who attended ante natal clinic or delivered of their babies at FMCO during the time of study. Data collection involved administration of closed ended questionnaire to illicit information on biographic data. Clinical assessments/examinations (laboratory investigations) of maternal peripheral blood, and fetal birth weight were utilized. Shortly before child birth maternal peripheral blood was obtained from each participant into sterile container for laboratory analysis. Statistical analysis of generated data was carried out using descriptive analysis and of percentages and presented using tables. Statistical comparisons and test of significance between positive and negative groups were calculated using the non-parametric Chi-square test. Differences were considered significant at P< 0.05. The study revealed that 65.6% had malaria during pregnancy. Malaria prevalence is significantly associated with maternal age bracket ( x2= 16.27; P < 0.05), gravidity (x2 = 14.9; P < 0.05) and level of education (x2= 24.69; P < 0.05). There is significant relationship between maternal malaria and perinatal mortality (x2 = 23.14; P < 0.05). There is significant effect of maternal malaria on perinatal mortality based on maternal age (x2= 40.11; P < 0.05) and gravidity (x2= 48.67; P < 0.05). An overall prevalence of preterm deliveries were 19.7%. There is significant relationship between maternal malaria and preterm delivery (x2 = 27.58; P < 0.05). There is significant effect of maternal malaria on preterm delivery based on maternal age (x2 = 49.2; P < 0.05) and gravidity (x2= 56.94; P < 0.05). An overall prevalence of low birth weight were 23.6%. There is significant relationship between maternal malaria and fetal birth weight (x2 = 34.06; P < 0.05). There is significant effect of maternal malaria on fetal birth weight based on maternal age (x2 = 53.82; P < 0.05) and gravidity (x2= 65.94; P < 0.05). The study suggests effective therapy since perinatal mortality due to maternal malaria was recorded in this study. Preterm deliveries and low fetal birth weight based on gravidity and maternal age groups associated with maternal malaria as identified is a call for program managers to make haste and implement new strategies for malaria control.

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IC, I., & CN , V. (2021). Studies on prevalence of malaria and its adverse fetal outcomes in Federal Medical Centre (FMC), Owerri, IMO State, Nigeria. Archives of Community Medicine and Public Health, 7(2), 151–163. https://doi.org/10.17352/2455-5479.000156
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Copyright (c) 2021 Iwuchukwu IC, et al.

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Yartey JE (2016) Malaria in pregnancy: Access to effective interventions in Africa. International Journal of Gynecology and Obstetrics 94: 364–373. Link: https://bit.ly/2VBDPGS

Taylor DW, Zhou A, Marsillio LE, Thuita LW, Leke EB, et al. (2014) “Antibodies That Inhibit Binding of Plasmodium falciparum-Infected Erythrocytes to Chondroitin Sulfate A and to the C Terminus of Merozoite Surface Protein 1 Correlate with Reduced Placental Malaria in Cameroonian Women. Infect Immun 72: 1603–1607. Link: https://bit.ly/2U2EmRS

World Health Organization (2017) World malaria report 2016. Link: https://bit.ly/3AjYM8u

World Health Organization (2018) “Implementing malaria in pregnancy programs in the context of World Health Organization recommendations on antenatal care for a positive pregnancy experience,” Link: https://bit.ly/3xp61di

World Health Organization (2007) Gender, health and malaria. Health Policy (New York) 52: 267–292. Link:

Marchesini P, Crawley J (2014) Reducing the burden of malaria in pregnancy. MERA IV, supporting agency–Roll Back Malaria.

Malaria consortium (2016) Malaria control Nigeria: State fact sheets. Link: https://bit.ly/3fG8B8K

Tako EA, Zhou A, Lohoue J, Leke R, Taylor DW, et al. (2008) Risk factors for placental malaria and its effect on pregnancy outcome in Yaoundé, Cameroon. Journal of Tropical Medical Hygiene 72: 236–242.

Heggenhougen HK, Hackethal V, Vivek P (2003) The behavioural and social aspects of malaria control: An introduction and annotated bibliography. WHO on behalf of the Special Programme for Research and Training in Tropical Diseases 3. Link: https://bit.ly/37ofCGP

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. Link: https://bit.ly/3AnesYj

Morgan HG (2014) Placental malaria and low birthweight neonates in urban Sierra Leone. Trop Med Parasitol 88: 575–580.

Guyatt HL, Snow RW (2001) The epidemiology and burden of Plasmodium falciparum-related anemia among pregnant in sub-Saharan Africa. Journal of Tropical Medical Hygiene 64: 36–44. Link: https://bit.ly/3CqDs2P

Guyatt HL, Snow RW (2014) Impact of malaria in Africa. Clinical Microbiology Review 17: 760-769. Link:

Ohalete CN, Dozie INS, Nwachukwu MI, Obiukwu CE (2011) Epidemiology and Economic consequences of malaria in pregnant womenin Imo State, Nigeria. African Journal of Microbiology Research 5: 3895-3900. Link: https://bit.ly/3iq2x66

Steketee RW (2006) Malaria prevention in pregnancy: the effects of treatment and chemoprophylaxis on placental malaria infection, low birth weight, and fetal, infant, and child survival. Mangochi Malaria Research Project. Washington, D.C.: United States Agency for International Development.

Menendez C, Ordi J, Ismail MR (2000) The impact of placental malaria on gestational age and birth weight. J Infect Dis 181: 1740–1745. Link: https://bit.ly/3yvEtV0

Shulman CE, Dorman EK (2007) Reducing childhood mortality in poor countries ― Importance and prevention of malaria in pregnancy. Journal of Tropical Medical Hygiene 7: 30–35.

Akanbi OL (2013) Effect of malaria infection on oxidative stress and lipid profile in pregnant women. Journal of Medical Sciences 4: 128-133. Link: https://bit.ly/37sPz0Z

Fleming AF (2009) The aetiology of severe malaria in pregnancy in Ndola, Zambia. Ann Trop Med Parasitol 83: 37–49. Link: https://bit.ly/2VwQLxM

Onyeneke EN, Amadi JC, Anyanwu HO, Ekeogu EC, Enyoh CE (2020) Food, Health Habits and Anthropometric Indices of Under-Five Aged Children in Imo State, Nigeria. Journal of Food Nutrition and Metabolism 3: 1-9. Link: https://bit.ly/3lH2uoj

Amal HM, Magdi MS, Elhassan ME, Ahmed AM, Salah EE, et al. (2013) Submicroscopic Plasmodium Falciparum Malaria and low birth weight in Central Sudan. Malaria Journal 12: 172–178. Link: https://bit.ly/3itI2W7

Aguilar R, Machevo S, Menéndez C, Bardají A, Nhabomba A, et al. (2012) Comparison of placental blood microscopy and the ICT HRP2 rapid diagnostic test to detect placental malaria. Trans R Soc Trop Med Hyg 106: 573-575. Link: https://bit.ly/3fI3Ifl

Uneke CJ (2008) Diagnosis of Plasmodium falciparum variant surface antigens in protective immunity and vaccine development. Human Vaccine 6: 84- 89.

Bulmer JN, Rasheed FN, Francis N, Morrison L, Greenwood BM (2003) Placental malaria I: Pathological classification. Histopathology 22: 211–218. Link: https://bit.ly/3rYfUxv

Salafia CM, Charles AK, Mass EM (2006) Placenta and fetal growth restriction. Clin obstet Gynecol 49: 236–256. Link: https://bit.ly/3xuRrAU

Mayor A, Moro L, Aguilar R, Bardají A, Cisteró P, et al. (2012) How hidden can malaria be in pregnant women? Diagnosis by microscopy, placental histology, polymerease chain reaction and detection of histidine-rich protein 2 in plasma. Clin Infect Dis 54: 1561–1568. Link: https://bit.ly/3iumiJS

Murray CK, Grasser RA, Magill AJ, Miller RS (2008) Update on rapid diagnostic testing for malaria. Clin Microbiol Rev 21: 97–100. Link: https://bit.ly/3rZ3fKE

Adefioye OA, Adeyeba OA, Hassan WO, Oyeniran OA (2007) Prevalence of Malaria Parasite Infection among Pregnant Women in Osogbo, Southwest, Nigeria. American-Eurasian Journal of Scientific Research 2: 43-45. Link: https://bit.ly/3s3H463

Uko EK, Emeribe AO, Ejezie GC (1998) Malaria Infection of the Placenta and Neonatal Low Birth Weight in Calabar. Journal of Medical Laboratory Sciences 7: 7-10.

Riley EM, Schneider G, Sambou I, Greenwood BM (2008) Suppression of cell-mediated immune responses to malaria antigens in pregnant Gambian women. Am J Trop Med Hyg 40: 141–144. Link: https://bit.ly/3AnfK5B

Nyirjesy P, Kavasya T, Axelrod P, Fischer PR (2013) Malaria during pregnancy: neonatal morbidity and mortality and the efficacy of chloroquine chemoprophylaxis. Clin Infect Dis 16: 127–132. Link: https://bit.ly/2U2FwwI

Brabin BJ, Agbaje SOF, Ahmed Y, Briggs ND (2009) A birthweight nomogram for Africa, as a malaria-control indicator. Ann Trop Med Parasitol 111: 77-83. Link: https://bit.ly/3An5M4a

Centers for Disease Control and Prevention (2015) Intermittent Preventive Treatment of Malaria for Pregnant Women (IPTp)

Rogerson SJ, Van den Broek NR, Chaluluka E, Qongwane C, Mhango CG, et al. (2000) Malaria and anemia in antenatal women in Blantyre, Malawi: a twelve-month survey. Am J Trop Med Hyg 62: 335–340. Link: https://bit.ly/3jyyUio

Bardaji A, Sigaugue B, Sanz S, Maixenchs M, Ordi J, et al. (2011) Impact of malaria at the end of pregnancy on infant mortality and morbidity. J Infect Dis 203: 691-699. Link: https://bit.ly/3iuLqA5

Greenwood BM, Greenwood AM, Snow RW, Byass P, Bennett S, et al. (2018) The effects of malaria chemoprophylaxis given by traditional birth attendants on the course and outcome of pregnancy. Tropical Medicine and Hygiene 83: 589–594.

Romagosa C, Ordi J, Saute F, Quintó L, Machungo F, et al. (2017) Seasonal variations in maternal mortality in Maputo, Mozambique: the role of malaria. Trop Med Int Health 12: 62-67. Link: https://bit.ly/2TYLv5x

Brahmbhatt H, Sullivan D, Kigozi G, Askin F, Wabwire-Mangenm F, et al. (2018) Association of HIV and malaria with mother-to-child transmission, birth outcomes, and child mortality. J Acquir Immune Defic Syndr 47: 472–476. Link: https://bit.ly/3itW36j

Haghdoost AA, Alexander N, Smith T (2007) Malaria during pregnancy and infant mortality rate: critical literature review and a new analytical approach. J Vector Borne Dis 44: 98–104. Link: https://bit.ly/3rXQm3F

van Eijk AM, Ayisi JG, Ter Kuile FO, Slutsker L, Shi YP, et al. (2007) HIV, malaria, and infant anemia as risk factors for postneonatal infant mortality among HIV-seropositive women in Kisumu, Kenya. Journal of Infectious Diseases 196: 30–37. Link: https://bit.ly/3lGEfHa

Achidi EA, Kuoh AJ, Minang JT, Ngum B, Achimbom BM, et al. (2005) Malaria infection in pregnancy and its effects on haemoglobin levels in women from a malaria endemic area of Fako Division, South West Province, Cameroon. J Obstet Gynaecol 25: 235–240. Link: https://bit.ly/3AoXbyd

Anagnos D, Lanoie LO, Palmieri JR, Ziefer A, Connor DH (2005) Effects of placental malaria on mothers and neonates from Zaire. Z Parasitenkd 72: 57–64. Link: https://bit.ly/3AiDhor

Antelman G, Msamanga GI, Spiegelman D, Urassa EJ, Narh R, et al. (2000) Nutritional factors and infectious disease contribute to anemia among pregnant women with human immunodeficiency virus in Tanzania. J Nutr 130: 1950–1957. Link: https://bit.ly/3An6Jtg

Asmelash D, Ambachew S, Eshetie S, Addisu A, Zeleke AJ (2019) The prevalence of malaria among pregnant women in Ethiopia: A systematic Review and Meta-analysis. Journal of Parasitology 2019: 8396091. Link: https://bit.ly/3lH48Gv

Bloland PB, Wirima JJ, Steketee RW, Chilima B, Hightower A, et al. (2005) Maternal HIV infection and infant mortality in Malawi: evidence for increased mortality due to placental malaria infection. AIDS 9: 721–726. Link: https://bit.ly/3jwM92X

Bouyou-Akotet MK, Ionete-Collard DE, Mabika-Manfoumbi M, Kendjo E, Matsiegui PB, et al. (2003) Prevalence of Plasmodium falciparum infection in pregnant women in Gabon. Malar J 2: 18. Link: https://bit.ly/3fHpHTH

Brabin BJ (2004) The risks and severity of malaria in pregnant women. Geneva: WHO; 2003.

Brabin BJ (1983) An analysis of malaria in pregnancy in Africa. Bull World Health Organ 61: 1005–1016. Link: https://bit.ly/3CqFQqb

Brabin BJ, Verhoeff F (2006) The contribution of malaria. In: Mac-Lean AB, Neilson JP, editors. Maternal Morbidity and Mortality. London: RCOG Press 65–78. Link:

Bugvi SM, Ahmed N (2015) Congenital malaria: A rare entity. J Coll Physicians Surg Pak 25: 841-842. Link: https://bit.ly/2VA8SD9

De Beaudrap P, Turyakira E, White LJ, Nabasumba C, Tumwebaze B, et al. (2013) Impact of malaria during pregnancy on pregnancy outcomes in a Ugandan prospectivecohort with intensive malaria screening and prompt treatment. Malar J 12: 139. Link: https://bit.ly/37r1Kf2

Dicko A, Mantel C, Aly-Thera M, Doumbia S, Diallo M, et al. (2003) Risk factors for malaria infection and anemia for pregnant women in the Sahel area of Bandiagara, Mali. ActaTrop 89: 17-23. Link: https://bit.ly/3AeHAky

Fondjo LA, Addai Mensah O, Annani-Akollor ME, Quarshie JT, Boateng AA, et al. (2020) A multicenter study of the prevalence and risk factors of malaria and anemia among pregnant women at first antenatal care visit in Ghana. Plos One 15: e0238077. Link: https://bit.ly/3yxr5Q6

Fried M, Duffy PE (2017) Malaria during Pregnancy. Cold Spring Harb Perspect Med 7: a025551. Link: https://bit.ly/3yvp47h

Getachew M, Yewhalaw D, Tafess K, Getachew Y, Zeynudin A, et al. (2012) Anaemia and associated risk factors among pregnant women in Gilgel Gibe dam area, Southwest Ethiopia. Parasit Vectors 5: 296. Link: https://bit.ly/3jCV4QG

Githeko AK, Mbogo CNM, Curtis CF, Lines J, Lengeler C (2011) Entomological monitoring of large-scale vector control interventions. Parasitology Today 44: 101-107. Link: https://bit.ly/3lG7V6Y

Hack M, Klein N, Taylor HG (2013) Long-term developmental outcomes of low-birth weight infants. Future Child 25: 333-339.

Hahn S, Williamson PR, Hutton JL, Garner P, Garner P (2000) Assessing the potential for bias in meta-analysis due to selective reporting of subgroup analyses within studies. Stat Med 19: 3325-3336. Link: https://bit.ly/3jA9noQ

Hanscheid T (2009) Diagnosis of malaria: a review of alternatives to conventional microscopy. Clin Lab Haematol 28: 186–209.

Hoestermann CF, Ogbaselassie G, Wacker J, Bastert G (2004) Maternal mortality in the main referral hospital in The Gambia, West Africa. Trop Med Int Health 1: 710-717. Link: https://bit.ly/3xsSi5m

Institute of Medicine (1985) Preventing low birthweight. National Academy Press, Washington, D.C. Link: https://bit.ly/3lF6DsZ

Ismail MR, Ordi J, Menendez C, Ventura PJ, Aponte JJ, et al. (2010) Placental pathology in malaria: a histological, immunohistochemical, and quantitative study. Hum Pathol 31: 85–93. Link: https://bit.ly/3jpBIy0

Johnson AH, Leke RG, Mendell NR, Shon D, Suh YJ, et al. (2009) HLA class II alleles influence levels of antibodies to the Plasmodium falciparum asexual-stage apical membrane antigen 1 but not to merozoite surface antigen 2 and merozoite surface protein 1. Infect Immun 72: 2762–2771. Link: https://bit.ly/3lFBd5R

Le Hesran JY, Cot M, Personne P, Fievet N, Dubois B, et al. (1997) Maternal placental infection with Plasmodium falciparum and malaria morbidity during the first 2 years of life. Am J Epidemiol 146: 826-831. Link: https://bit.ly/3iqY4jE

Levine RJ, Maynard SE, Qian C, Lim KH, England LJ, et al. (2004) Circulating angiogenic factors and the risk of preeclampsia. N Engl J Med 350: 672-683. Link: https://bit.ly/2VvvwfL

Malhotra I, Dent A, Mungai P, Wamachi A, Ouma JH, et al. (2009) Can prenatal malaria exposure produce an immune tolerant phenotype? A prospective birth cohort study in Kenya. PLoS Med 6: e1000116. Link: https://bit.ly/3jtVA3f

Mangochi Malaria Research Project (1993) Malaria prevention in pregnancy: the effects of treatment and chemoprophylaxis on placental malaria infection, low birth weight, and fetal, infant, and child survival. U.S. Agency for International Development in conjunction with Centers for Disease Control and Prevention, Atlanta, Ga.

Matteelli A, Donato F, Shein A, Muchi JA, Leopardi O, et al. (2010) Malaria and anemia in pregnant women in urban Zanzibar, Tanzania. Tropical Medical Parasitology 88: 475-483.

Maubert B, Fievet N, Tami G, Cot M, Boudin C, et al. (2009) Development of antibodies against chondroitin sulfate A-adherent Plasmodium falciparum in pregnant women. Infect Immun 107: 869-875.

Maynard SE, Min JY, Merchan J, Lim KH, Li J, et al. (2003) Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest 111: 649–658. Link: https://bit.ly/3CqK2Gz

McCormick MC (2015) The contribution of low birth weight to infant mortality and childhood mortality. N Engl J Med 443: 91-99.

McCormick MC, Brooks-Gunn J, Workman-Daniels K, Turner J, Peckham GJ (1992) The health and developmental status of very low-birth-weight children at school age. JAMA 267: 2204-2208. Link: https://bit.ly/3xqag8l

McGregor IA (2005) Epidemiology, malaria, and pregnancy. Journal of Tropical Medical Hygiene 33: 517–525.

McGregor IA, Wilson ME, Billewicz WZ (2004) Malaria infection of the placenta in the Gambia, West Africa: its incidence and relationship of stillbirth, birthweight, and placental weight. Journal of Tropical Medical Hygiene 77: 232–244.

Muehlenbachs A, Mutabingwa TK, Edmonds S, Fried M, Duffy PE (2006) Hypertension and maternal–fetal conflict during placental malaria. Journal of Tropical Medical Hygiene 79: 398-446.

Mutabingwa TK (2015) Artemisinin-based combination therapies (ACTs): best hope for malaria treatment but inaccessible to the needy! Acta Trop 95: 305-315. Link: https://bit.ly/3yvRi1D

Newman RD, Steketee RW, Parise ME (2013) Burden of malaria during pregnancy in areas of stable and unstable transmission in Ethiopia during a nonepidemic year. J Infect Dis 210: 1882-1886.

Nokes C, van den Bosch C, Bundy DAP (2008) The effects of iron deficiency and anemia on mental and motor performance, educational achievement and behaviour in children: an annotated bibliography. Washington, D.C.: International Nutritional Anemia Consultative Group.

Oeuvray C, Theisen M, Rogier C, Trape JF, Jepsen S, et al. (2006) Cytophilic immunoglobulin responses to Plasmodium falciparum glutamate-rich protein are correlated with protection against clinical malaria in Dielmo, Senegal. Infect Immun 68: 2617-2620.

Okoko BJ, Ota MO, Yamuah LK, Idiong D, Mkpanam SN, et al. (2002) Influence of placental malaria infection on foetal outcome in the Gambia: twenty years after Ian McGregor. J Hlth Pop Nutr 20: 4-11. Link: https://bit.ly/37ocVFh

Parise ME, Sambo C (2006) The burden of malaria in pregnancy in malaria-endemic areas. Journal of Tropical Medical Hygiene 64: 28-35.

Pertet AM (1990) The effect of weekly chloroquine prophylaxis given to pregnant mothers and their respective infants on birthweight and physical growth during infancy in a rural area of Kenya. Ph.D. thesis. University of Nairobi, Nairobi, Kenya.

Rogerson SJ, Desai M, Mayor A, Sicuri E, Taylor SM, et al. (2018) Burden, pathology, and costs of malaria in pregnancy: new developments for an old problem. Lancet Infect Dis 18: 5-9. Link: https://bit.ly/3xxuiho

Salihu HM, Tchuinguem G, Ratard R (2012) Effect of chloroquine prophylaxis on birthweight and malaria parasite load among pregnant women delivering in a regional hospital in Cameroon. West Indian Med J 99: 238-244.

Scherf A, Pouvelle B, Buffet PA, Gysin J (2007) Molecular mechanisms of Plasmodium falciparum placental adhesion. Journal of Tropical Medical Hygiene 3: 125.

Schwarz NG, Adegnika AA, Breitling LP, Gabor J, Agnandji ST, et al. (2008) Placental malaria increases malaria risk in the first 30 months of life. Clin Infect Dis 47: 1017-1025. Link: https://bit.ly/3lIVlE2

Seal SL, Mukhopadhay S, Ganguly RP (2010) Malaria in pregnancy. J Indian Med Assoc 108: 487-490. Link: https://bit.ly/3fJBvF3

Shi YP, Sayed U, Qari SH, Roberts JM, Udhayakumar V, et al. (2004) Natural immune response to the C-terminal 19-kilodalton domain of Plasmodium falciparum merozoite surface protein Journal of Tropical Medical Hygiene 64: 2716–2723.

Staalsoe T, Megnekou R, Fievet N, Ricke CH, Zornig HD, et al. (2009) Acquisition and decay of antibodies to pregnancy-associated variant antigens on the surface of Plasmodium falciparum-infected erythrocytes that protect against placental parasitemia. J Infect Dis 184: 618-626. Link: https://bit.ly/2VFWAcx

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. Link: https://bit.ly/3CrKhkJ

Sule-Odu AO, Ogunledun A, Olatunji AO (2012) Impact of asymptomatic malaria parasitaemia at parturition on perinatal outcome. J Obstet Gynaecol 44: 55-59.

Takem EN, D'Alessandro U (2013) Malaria in pregnancy. Mediterr J Hematol Infect Dis 5: e2013010. Link: https://bit.ly/3jEXz4C

Teplin SW, Burchinal M, Johnson-Martin N, Humphrey R, Kraybill E (1991) Neurodevelopmental, health and growth status at age 6 years of children with birth weights less than 1001 grams. Journal of Pediatrics 118: 768-777. Link: https://bit.ly/3fL0Mi6

Ter Kuile FO, Terlouw DJ, Phillips-Howard PA, Hawley WA, Nahlen BL, 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. Link: https://bit.ly/3fJrTdx

Tyagi P, Roy A, Malhotra MS (2005) Knowledge, awareness and practices towards malaria in communities of rural, semi-rural and bordering areas of east Delhi (India). J Vect Borne Dis 42: 30-35. Link: https://bit.ly/3jAw1NW

Verhoeff FH, Le Cessie S, Kalanda BF, Kazembe PN, Broadhead RL, et al. (2014) Post-neonatal infant mortality in Malawi: the importance of maternal health. Ann Trop Paediatr 24: 161-169. Link: https://bit.ly/2U3cVHv

Walraven GEL, Dolmans MV (2011) The aetiology of low birthweight in a rural area of Tanzania. Tropical Medicine 28: 558-567.

World Health Organization (2010) Insecticide-treated mosquito nets: a WHO position statement. Geneva: WHO.