Pregnancy-associated malaria is a major global health concern. To assess the Plasmodium falciparum burden in pregnancy we conducted a cross-sectional study at Mulago Hospital in Kampala, Uganda. Malaria prevalence by each of three measures—peripheral smear, placental smear, and placental histology was 9% (35/391), 11.3% (44/389), and 13.9% (53/382) respectively. Together, smear and histology data yielded an infection rate of 15.5% (59/380) of active infections and 4.5% (17/380) of past infections; hence 20% had been or were infected when giving birth. A crude parity dependency was observed with main burden being concentrated in gravidae 1 through gravidae 3. Twenty-two percent were afflicted by anaemia and 12.2% delivered low birthweight babies. Active placental infection and anaemia showed strong association ( ) whereas parity and placental infection had an interactive effect on mean birthweight ( ). Primigravidae with active infection and multigravidae with past infection delivered on average lighter babies. Use of bednet protected significantly against infection ( ) whilst increased haemoglobin level protected against low birthweight ( ) irrespective of infection status. Albeit a high attendance at antenatal clinics (96.8%), there was a poor coverage of insecticide-treated nets (32%) and intermittent preventive antimalarial treatment (41.5%). 1. Introduction Malaria is a major public health problem affecting between 300–500 million people annually. Plasmodium falciparum is responsible for the main disease burden afflicting primarily sub-Saharan Africa. In areas with stable malaria transmission, due to protracted exposure to infectious bites, partial protective immunity to clinical malaria is gradually acquired with increasing age. Severe P. falciparum malaria is thus predominantly a childhood disease. There is however one exception to this general rule: pregnancy-associated malaria (PAM). Despite their semi-immune status, women become more susceptible to malaria upon pregnancy. In endemic areas, approximately 25 million pregnancies are at risk of P. falciparum infection every year, and 25% of these women have evidence of placental infection at the time of delivery [1–3]. Clinical features of infection during pregnancy vary with the degree of preexisting immunity and thus the epidemiological setting. In high-transmission areas, maternal anaemia and low birthweight (LBW), as a result of prematurity and/or intrauterine growth restriction (IUGR), are the main adverse outcomes of placental infection and tend to be more severe in first pregnancies and in
References
[1]
B. J. Brabin, “An analysis of malaria in pregnancy in Africa,” Bulletin of the World Health Organization, vol. 61, no. 6, pp. 1005–1016, 1983.
[2]
H. L. Guyatt and R. W. Snow, “Impact of malaria during pregnancy on low birth weight in sub-Saharan Africa,” Clinical Microbiology Reviews, vol. 17, no. 4, pp. 760–769, 2004.
[3]
R. W. Steketee, B. L. Nahlen, M. E. Parise, and C. Menendez, “The burden of malaria in pregnancy in malaria-endemic areas,” American Journal of Tropical Medicine and Hygiene, vol. 64, no. 1-2, pp. 28–35, 2001.
[4]
H. L. Guyatt and R. W. Snow, “The epidemiology and burden of Plasmodium Falciparum-related anemia among pregnant women in sub-Saharan Africa,” American Journal of Tropical Medicine and Hygiene, vol. 64, no. 1-2, pp. 36–44, 2001.
[5]
T. Leenstra, P. A. Phillips-Howard, S. K. Kariuki et al., “Permethrin-treated bed nets in the prevention of malaria and anemia in adolescent schoolgirls in Western Kenya,” American Journal of Tropical Medicine and Hygiene, vol. 68, no. 4, pp. 86–93, 2003.
[6]
C. Menendez, J. Ordi, M. R. Ismail et al., “The impact of placental malaria on gestational age and birth weight,” Journal of Infectious Diseases, vol. 181, no. 5, pp. 1740–1745, 2000.
[7]
S. J. Rogerson, N. R. Van den Broek, E. Chaluluka, C. Qongwane, C. G. Mhango, and M. E. Molyneux, “Malaria and anemia in antenatal women in Blantyre, Malawi: a twelve-month survey,” American Journal of Tropical Medicine and Hygiene, vol. 62, no. 3, pp. 335–340, 2000.
[8]
A. Walker-Abbey, R. R. T. Djokam, A. Eno et al., “Malaria in pregnant Cameroonian women: the effect of age and gravidity on submicroscopic and mixed-species infections and multiple parasite genotypes,” American Journal of Tropical Medicine and Hygiene, vol. 72, no. 3, pp. 229–235, 2005.
[9]
F. Nosten, F. ter Kuile, L. Maelankirri, B. Decludt, and N. J. White, “Malaria during pregnancy in an area of unstable endemicity,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 85, no. 4, pp. 424–429, 1991.
[10]
H. L. Guyatt and R. W. Snow, “Malaria in pregnancy as an indirect cause of infant mortality in sub-Saharan Africa,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 95, no. 6, pp. 569–576, 2001.
[11]
S. C. Murphy and J. G. Breman, “GAPS in the childhood malaria burden in Africa: cerebral malaria, neurological sequelae, anemia, respiratory distress, hypoglycemia, and complications of pregnancy,” American Journal of Tropical Medicine and Hygiene, vol. 64, no. 1-2, pp. 57–67, 2001.
[12]
M. C. Nunes and A. Scherf, “Plasmodium falciparum during pregnancy: a puzzling parasite tissue adhesion tropism,” Parasitology, vol. 134, no. 13, pp. 1863–1869, 2007.
[13]
M. R. Ismail, J. Ordi, C. Menendez et al., “Placental pathology in malaria: a histological, immunohistochemical, and quantitative study,” Human Pathology, vol. 31, no. 1, pp. 85–93, 2000.
[14]
F. H. Verhoeff, B. J. Brabin, S. Van Buuren et al., “An analysis of intra-uterine growth retardation in rural Malawi,” European Journal of Clinical Nutrition, vol. 55, no. 8, pp. 682–689, 2001.
[15]
A. Yeka, K. Banek, N. Bakyaita et al., “Artemisinin versus nonartemisinin combination therapy for uncomplicated malaria: randomized clinical trials from four sites in Uganda,” PLoS Medicine, vol. 2, no. 7, article e190, 2005.
[16]
J. N. Bulmer, F. N. Rasheed, N. Francis, L. Morrison, and B. M. Greenwood, “Placental malaria. I. Pathological classification,” Histopathology, vol. 22, no. 3, pp. 211–218, 1993.
[17]
J. N. Bulmer, F. N. Rasheed, L. Morrison, N. Francis, and B. M. Greenwood, “Placental malaria. II. A semi-quantitative investigation of the pathological features,” Histopathology, vol. 22, no. 3, pp. 219–225, 1993.
[18]
S. J. Rogerson, P. Mkundika, and M. K. Kanjalal, “Diagnosis of Plasmodium falciparum malaria at delivery: comparison of blood film preparation methods and of blood films with histology,” Journal of Clinical Microbiology, vol. 41, no. 4, pp. 1370–1374, 2003.
[19]
M. Fried, F. Nosten, A. Brockman, B. J. Brabin, and P. E. Duffy, “Maternal antibodies block malaria,” Nature, vol. 395, no. 6705, pp. 851–850, 1998.
[20]
C. H. Ricke, T. Staalsoe, K. Koram et al., “Plasma antibodies from malaria-exposed pregnant women recognize variant surface antigens on Plasmodium falciparum-infected erythrocytes in a parity-dependent manner and block parasite adhesion to chondroitin sulfate A,” Journal of Immunology, vol. 165, no. 6, pp. 3309–3316, 2000.
[21]
J. G. Beeson, G. V. Brown, M. E. Molyneux, C. Mhango, F. Dzinjalamala, and S. J. Rogerson, “Plasmodium falciparum isolates from infected pregnant women and children are associated with distinct adhesive and antigenic properties,” Journal of Infectious Diseases, vol. 180, no. 2, pp. 464–472, 1999.
[22]
M. Fried and P. E. Duffy, “Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta,” Science, vol. 272, no. 5267, pp. 1502–1504, 1996.
[23]
N. Rasti, F. Namusoke, A. Chêne et al., “Nonimmune immunoglobulin binding and multiple adhesion characterize Plasmodium falciparum-infected erythrocytes of placental origin,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 37, pp. 13795–13800, 2006.
[24]
M. Desai, F. O. ter Kuile, F. Nosten et al., “Epidemiology and burden of malaria in pregnancy,” Lancet Infectious Diseases, vol. 7, no. 2, pp. 93–104, 2007.
[25]
R. W. Steketee, J. J. Wirima, L. Slutsker et al., “Malaria parasite infection during pregnancy and at delivery in mother, placenta, and newborn: efficacy of chloroquine and mefloquine in Rural Malawi,” American Journal of Tropical Medicine and Hygiene, vol. 55, no. 1, pp. 24–32, 1996.
[26]
F. H. Verhoeff, B. J. Brabin, C. A. Hart, L. Chimsuku, P. Kazembe, and R. L. Broadhead, “Increased prevalence of malaria in HIV-infected pregnant women and its implications for malaria control,” Tropical Medicine and International Health, vol. 4, no. 1, pp. 5–12, 1999.
[27]
R. Ndyomugyenyi, N. Kabatereine, A. Olsen, and P. Magnussen, “Malaria and hookworm infections in relation to haemoglobin and serum ferritin levels in pregnancy in Masindi district, western Uganda,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 102, no. 2, pp. 130–136, 2008.
[28]
B. J. Brabin, C. Romagosa, S. Abdelgalil et al., “The sick placenta—the role of malaria,” Placenta, vol. 25, no. 5, pp. 359–378, 2004.
[29]
C. E. Shulman, T. Marshall, E. K. Dorman et al., “Malaria in pregnancy: adverse effects on haemoglobin levels and birthweight in primigravidae and multigravidae,” Tropical Medicine and International Health, vol. 6, no. 10, pp. 770–778, 2001.
[30]
L. Kalilani, I. Mofolo, M. Chaponda, S. J. Rogerson, and S. R. Meshnick, “The effect of timing and frequency of Plasmodium falciparum infection during pregnancy on the risk of low birth weight and maternal anemia,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 104, no. 6, pp. 416–422, 2010.
[31]
C. Gamble, J. P. Ekwaru, and F. O. ter Kuile, “Insecticide-treated nets for preventing malaria in pregnancy,” Cochrane Database of Systematic Reviews, no. 2, Article ID CD003755, 2006.