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Epidemiology, Malaria and Pregnancy
Abstract
It is a great honor for me to be invited to give this Soper Lecture. I met Fred Soper only once—at the 6th International Congresses of Tropical Medicine and Malaria at Lisbon in 1958. I had, of course, known of him for a number of years beforehand, and had read with the greatest interest his account of how Anopheles gambiae was halted in its invasion of Brazil and finally expelled from an area of some 18,000 square miles. In his lifetime, Soper was associated with many significant achievements in diverse fields of public health, but to me as a malariologist none compares with his eradication of Anopheles gambiae from Brazil. More than 40 years later, this episode still stands as one of the most significant victories that man has scored over malaria and epitomizes Soper's administrative genius and technological competence.
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“In areas of stable malaria transmission, primigravidae are at highest risk of P. falciparum pregnancy malaria and women develop resistance over 1–2 pregnancies that controls infection and prevents severe sequelae [6, 7].”
In the citing paper
“Susceptibility diminishes with successive pregnancies, and this pattern is most prominent in high transmission areas where primigravidae are significantly more susceptible to Plasmodium falciparum infection and disease than multigravidae [3,4].”
From Diagnosing malaria in pregnancy: An update (2012) · cites this paper as [3]
In the citing paper
“In malaria endemic areas, pregnant women are more susceptible to malaria infection than their nonpregnant counterparts[3,4].”
From Diagnosing malaria in pregnancy: An update (2012) · cites this paper as [3]
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“Pregnant women are at increased risk of malaria infection because the parasite is able to adhere to the trophoblastic villous epithelium (1) and sequester in the placenta (2, 3).”
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“This results in a lowering of malaria prevalence in subsequent pregnancies with the development of parity-specific immunity (McGregor 1984; Brabin & Brabin 1992), i.”
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Clinical Features and Outcome of Severe Malaria in Gambian Children
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“Since malaria is more common in first pregnancies (19, 20), it is not surprising that malaria-infected women were more likely to be primigravid (t 4.”
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“In areas where malaria is endemic, infection with I? falciparwn in pregnancy is greatest in primigravidae, with the prevalence and intensity of parasitaemia decreasing with increasing gravidity (MCGREGOR & SMITH, 1952; MCGREGOR, 1984; STEKETEE & BREMA~, 1988; GREENWOOD et aZ., 1989).”
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Poespoprodjo, J. R., Fobia, W., Kenangalem, E., Lampah, D. A., Hasanuddin, A., Warikar, N., Sugiarto, P., Tjitra, E., Anstey, N., & Price, R. N. (2009) · Clinical Infectious Diseases · doi:10.1086/599041 · Cited by 164
“In sub-Saharan Africa, infants younger than 3–4 months of age who are infected with Plasmodium falciparum are less susceptible to clinical symptoms and severe disease, compared with older infected children [1, 2].”
BackgroundBed nets for the prevention of malaria and anaemia in pregnancy
Dolan, G., ter Kuile, F. O., Jacoutot, V., White, N. J., Luxemburger, C., Maelankirri, L., Chongsuphajaisiddhi, T., & Nosten, F. H. (1993) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(93)90262-o · Cited by 155
Increased Susceptibility to Malaria during the Early Postpartum Period
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“Symptoms tend to be severe in the relatively nonimmune people who contract malaria during epidemics [108, 109].”
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Flick, K., Scholander, C., Chen, Q., Fernandez, V., Pouvelle, B., Gysin, J., & Wahlgren, M. (2001) · Science · doi:10.1126/science.1062891 · Cited by 152
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“HIV infection thus seems to alter the wellestablished parity-specific pattern of malaria susceptibility in areas of stable malaria transmission, where in the absence of HIV, primigravidae and, to a lesser extent, secundigravidae are more affected than are other parities [1,3].”
BackgroundPrevalence of Plasmodium falciparum infection in pregnant women in Gabon
Bouyou-Akotet, M. K., Ionete-Collard, D. E., Mabika-Manfoumbi, M., Kendjo, E., Matsiegui, P.-B., Mavoungou, E., & Kombila, M. (2003) · Malaria Journal · doi:10.1186/1475-2875-2-18 · Cited by 149
“Discussion The susceptibility of pregnant women to malaria is wellestablished [1,20].”
Poespoprodjo, J. R., Fobia, W., Kenangalem, E., Lampah, D. A., Warikar, N., Seal, A., McGready, R., Sugiarto, P., Tjitra, E., Anstey, N. M., et al. (2008) · Clinical Infectious Diseases · doi:10.1086/586743 · Cited by 148
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TAKO, E. A., ZHOU, A., LOHOUE, J., LEKE, R., TAYLOR, D. W., & LEKE, R. F. G. (2005) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2005.72.236 · Cited by 138
“are more common in pregnant women than in non-pregnant women.(1,2) A number of factors influence the prevalence of malaria in pregnant women, including maternal age, gravidity, use of prophylaxis, nutrition, host genetics, level of antiparasite immunity, as well as parasite genetics and transmission rates.”
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Brabin, L., & Brabin, B. J. (1992) · Advances in Parasitology/Advances in parasitology · doi:10.1016/s0065-308x(08)60020-2 · Cited by 137
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“In malaria-endemic areas, the prevalence of clinical and asymptomatic malaria is highest in young women and those in their first and second pregnancies.(1,3) With successive pregnancies, women acquire a gravidity-dependent form of immunity, resulting in a decrease in both prevalence and severity of infection.”
BackgroundTropical obstetrics and gynaecology. 1. Anaemia in pregnancy in tropical Africa
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Short-range attractiveness of pregnant women to Anopheles gambiae mosquitoes
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Epidemiology of malaria in pregnancy in central India.
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The effects of maternal helminth and malaria infections on mother-to-child HIV transmission
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“Since primigravid or secundagravid women are more likely to be infected with malaria and have placental malaria during gestation [20], this serves as a surrogate for increased risk for malaria throughout pregnancy.”
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“Together with maternal malaria induced anemia [5,6], parasite sequestration in the placenta are thought to trigger a pathological process that contributes to decrease fetal viability and leads to infant Low Birth Weight (LBW) [7,8], due to both preterm delivery and/or Intrauterine Growth Retardation (IUGR) [9,10].”
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“Primagravida are at particular risk for malarial infection (38, 39).”
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“As a result, high numbers of trophozoite and schizont stage parasites may be found in the placenta (4, 13).”
BackgroundMaternal malaria and parasite adhesion
Fried, M., & Duffy, P. E. (1998) · Journal of Molecular Medicine · doi:10.1007/s001090050205 · Cited by 117
“Clinical consequences of maternal malaria In 1934 Wickramasuriya observed the devastating outcome of a malaria epidemic on pregnant women in Sri Lanka [4], and subsequent reports throughout the tropics have documented the high susceptibility of pregnant women to malaria infection [4–7].”
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Congenital malaria: The least known consequence of malaria in pregnancy
Menéndez, C., & Mayor, A. G. (2007) · Seminars in Fetal and Neonatal Medicine · doi:10.1016/j.siny.2007.01.018 · Cited by 111
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Malaria and anemia in antenatal women in Blantyre, Malawi: a twelve-month survey.
Rogerson, S. J., van den Broek, N. R., Chaluluka, E., Qongwane, C., Mhango, C., & Molyneux, M. E. (2000) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2000.62.335 · Cited by 107
Acquired Immune Responses to Plasmodium falciparum Merozoite Surface Protein-1 in the Human Fetus
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“Pregnancy is associated with an increased risk of maternal Plasmodium falciparum malaria and predisposes the developing fetus to stunted growth (1).”
BackgroundEconomic Analysis of Malaria Control in Sub-Saharan Africa
MILLS, A. J., Goodman, C. A., & Coleman, P. G. (2000) · Cited by 106
Chaiyaroj, S. C., Rutta, A. S. M., Muenthaisong, K., Watkins, P., Ubol, M. N., & Looareesuwan, S. (2003) · Acta Tropica · doi:10.1016/j.actatropica.2003.10.010 · Cited by 105
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“This increased IL-10 production in primiparae, the group most sensitive to malaria [1], may be of importance to help buffer the increased potential Th1 stimulus of the parasite.”
BackgroundThe epidemiology and consequences of maternal malaria: a review of immunological basis
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The Consequences of Iron Deficiency and Anemia in Pregnancy
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“Malaria infection is more common in primigravidae (45).”
BackgroundThe Immunology and Pathogenesis of Malaria During Pregnancy
Beeson, J. G., & Duffy, P. E. (2005) · Current topics in microbiology and immunology · doi:10.1007/3-540-29967-x_6 · Cited by 95
Maubert, B., Fiévet, N., Tami, G., Cot, M., Boudin, C., & Deloron, P. (1999) · Infection and Immunity · doi:10.1128/iai.67.10.5367-5371.1999 · Cited by 98
“Interestingly, among pregnant women, primiparae are more susceptible to malaria than multiparae (16).”
BackgroundAnaemia in pregnancy in developing countries
van den Broek, N. R. (1998) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1998.tb10120.x · Cited by 95
Cottrell, G., Mary, J., Barro, D., & Cot, M. (2007) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2007.76.849 · Cited by 93
“which usually affects 10%–15% of births in malaria-endemic areas.(3,4) The mean decrease in birth weight related to placental infection ranges from 55 g to 348 g (all parities).”
BackgroundAnaemia in pregnant Ghanaian women: importance of malaria, iron deficiency, and haemoglobinopathies
Mockenhaupt, F. P., Rong, B., Günther, M., Beck, S., Till, H., KOHNE, E., Thompson, W. N. A., & Bienzle, U. (2000) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/s0035-9203(00)90057-9 · Cited by 93
Malaria and anaemia in pregnant women in urban Zanzibar, Tanzania
Matteelli, A., Donato, F., Shein, A., Muchi, J. A., Leopardi, O., Astori, L., & Carosi, G. (1994) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.1994.11812894 · Cited by 91
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“(41), we assessed the relationship between parity and CBL cytokine responses.”
BackgroundPrevalence and risk factors for Plasmodium falciparum malaria in pregnant women of eastern Sudan
Adam, I., Khamis, A. H., & Elbashir, M. I. (2005) · Malaria Journal · doi:10.1186/1475-2875-4-18 · Cited by 89
“Dafallah SE, EL-Agib FH, Bushra GO: Maternal mortality in a teaching hospital in Sudan.”
BackgroundInfluentialMalaria chemoprophylaxis, birth weight and child survival
Greenwood, A. M., ARMSTRONG, J. R. M., Byass, P., Snow, R. W., & Greenwood, B. M. (1992) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(92)90078-q · Cited by 88
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Plasmodiumin the placenta: parasites, parity, protection, prevention and possibly preeclampsia
Duffy, P. E. (2007) · Parasitology · doi:10.1017/s0031182007000170 · Cited by 84
“To explain parity-related resistance, MacGregor speculated that local uteroplacental immune responses were required for protection, and that these might develop over successive pregnancies (McGregor, 1984).”
BackgroundAzithromycin-chloroquine and the intermittent preventive treatment of malaria in pregnancy
Chico, R. M., Pittrof, R., Greenwood, B. M., & Chandramohan, D. (2008) · Malaria Journal · doi:10.1186/1475-2875-7-255 · Cited by 83
“LBW is a strong predictor of infant mortality in sub-Saharan Africa; death within the first year of life is three-times higher for LBW newborns compared to neonates of normal birth-weight [7].”
BackgroundInfluentialThe role of chemokines in severe malaria: more than meets the eye
Ioannidis, L. J., Nie, C. Q., & Hansen, D. S. (2013) · Parasitology · doi:10.1017/s0031182013001984 · Cited by 84
“…serious complication has been found to be associated with adverse pregnancy outcomes including premature labour, intrauterine growth retardation and low birth weight delivery, and is responsible for more than 75000 infant deaths each year (McGregor, 1984; Steketee et al. 2001; Desai et al. 2007).”
BackgroundMaubert, B., Guilbert, L. J., & Deloron, P. (1997) · Infection and Immunity · doi:10.1128/iai.65.4.1251-1257.1997 · Cited by 84
“Three observations suggest that IRBCs are sequestered in the intravillous spaces of the placenta: at delivery IRBCs are more frequently found in the placenta than in the peripheral blood (25); parasite densities are often much higher in the placenta than in the peripheral blood (4, 16); and lastly, most of the P.”
BackgroundDeterminants of Anemia among Pregnant Women in Mali
Ayoya, M. A., Spiekermann‐Brouwer, G. M., Traoré, A. K., Stoltzfus, R. J., & Garza, C. (2006) · Food and Nutrition Bulletin · doi:10.1177/156482650602700101 · Cited by 83
Shulman, Shulman, Dorman, Dorman, Talisuna, Lowe, Lowe, Nevill, Nevill, Snow, et al. (1998) · Tropical Medicine & International Health · doi:10.1046/j.1365-3156.1998.00214.x · Cited by 83
“It has long been recognized that malaria parasitaemia is more prevalent, with higher parasite burdens, in pregnant women than in nonpregnant women (McGregor 1984; Brabin 1983) and that the increase in prevalence and density of parasitaemia is greatest in primigravidae and decreases as gravidity…”
BackgroundWeather and Infant Mortality in Africa
Kudamatsu, M., Persson, T., & Strömberg, D. (2012) · Cited by 103
Malaria-related maternal mortality in urban Mozambique
Granja, A. C. L., Machungo, F., Gomes, A., Bergström, S., & Brabin, B. J. (1998) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.1998.11813288 · Cited by 82
Diagnosing malaria in pregnancy: An update
Fried, M., Muehlenbachs, A., & Duffy, P. E. (2012) · Expert Review of Anti-infective Therapy · doi:10.1586/eri.12.98 · Cited by 80
Mefloquine antimalarial prophylaxis in pregnancy: dose finding and pharmacokinetic study.
Nosten, F. H., Karbwang, J., White, N. J., Honeymoon, Bangchang, K. N., BUNNAG, D., & Harinasuta, T. (1990) · British Journal of Clinical Pharmacology · doi:10.1111/j.1365-2125.1990.tb03746.x · Cited by 79
Matteelli, A., Caligaris, S., Castelli, F., & Carosi, G. (1997) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034989760563 · Cited by 87
Njagi, J. K., Magnussen, P., Estambale, B., Ouma, J., & Mugo, B. (2003) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/s0035-9203(03)90141-6 · Cited by 78
Hviid, L. (2010) · Human Vaccines · doi:10.4161/hv.6.1.9602 · Cited by 75
“falciparum malaria than their non-pregnant peers, this susceptibility is highly parity-dependent (decreases with increasing parity).(12) The finding that levels of VSA PAM /VAR2CSA-specific antibodies are also highly dependent on parity (increase with increasing parity) suggest that the two phenomena are related.”
BackgroundMahende, C., Ngasala, B., Lusingu, J., Yong, T., Lushino, P., Lemnge, M., Mmbando, B. P., & Premji, Z. (2016) · Malaria Journal · doi:10.1186/s12936-016-1450-z · Cited by 75
“Infants appear to be relatively protected from malaria (and other infections) for the first 6 months of life, mainly due to acquiring maternal antibodies and the presence of foetal haemoglobin [22–24].”
BackgroundMalhotra, I. J., Dent, A. E., Mungai, P., Muchiri, E. M., & King, C. L. (2005) · Journal of Clinical Microbiology · doi:10.1128/jcm.43.8.3630-3635.2005 · Cited by 74
“falciparum parasites, develop episodes of symptomatic malaria, and have involvement of the placenta than are multiparous women based on BS analysis (3, 16, 21).”
BackgroundSaute, F., Menendez, C., Mayor, A., Aponte, J., Gomez‐Olive, X., Dgedge, M., & Alonso, P. (2002) · Tropical Medicine & International Health · doi:10.1046/j.1365-3156.2002.00831.x · Cited by 74
“As previously reported (McGregor 1984; Diagne et al. 2000), malaria parasitaemia was more frequent during the second trimester, suggesting that this is the time of maximum risk for malaria infection during gestation.”
BackgroundThe Status of Malaria among Pregnant Women: A Study in Lagos, Nigeria
Okwa, O. (2003) · African Journal of Reproductive Health · doi:10.2307/3583292 · Cited by 74
Kalilani, L., Mofolo, I., Chaponda, M., Rogerson, S. J., & Meshnick, S. R. (2010) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/j.trstmh.2010.01.013 · Cited by 74
“In high transmission areas, women of reproductive age have acquired partial immunity to malaria [4].”
BackgroundNeonatal Infections: A Global Perspective
Stoll, B. J. (2006) · Elsevier eBooks · doi:10.1016/b0-72-160537-0/50004-9 · Cited by 73
SUGUITAN, A. L., CADIGAN, T. J., NGUYEN, T. A., ZHOU, A., LEKE, R. J. I., METENOU, S., THUITA, L., MEGNEKOU, R., FOGAKO, J., LEKE, R. G. F., et al. (2003) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2003.69.574 · Cited by 72
“Their malariometric profile, however, is similar to that reported for pregnant women in other African countries.(1,2) The influence of other diseases on the results is difficult to assess, including infection with human immunodeficiency virus, which infects an estimated 4.”
ResultOkoko, B. J., Ota, M. O. C., Yamuah, L. K., Idiong, D., Mkpanam, S. N., Avieka, A., BANYA, W. A. S., & Osinusi, K. (2002) · PubMed · Cited by 72
Micronutrient malnutrition and the pathogenesis of malarial anemia
Nussenblatt, V. R., & Semba, R. D. (2002) · Acta Tropica · doi:10.1016/s0001-706x(02)00049-9 · Cited by 72
Relationships between maternal malaria and malarial immune responses in mothers and neonates
Rasheed, F. N., Bulmer, J. N., de Francisco, A., Jawla, M., Jakobsen, P., Jepson, A., & Greenwood, B. M. (1995) · Parasite Immunology · doi:10.1111/j.1365-3024.1995.tb00960.x · Cited by 72
“In hyperendemic areas, malarial parasites often concentrate in the intervillous spaces of placentas (McGregor 1984).”
BackgroundInfluentialCongenital Malaria in the United States: Report of a Case and Review
Hulbert, T. V. (1992) · Clinical Infectious Diseases · doi:10.1093/clinids/14.4.922 · Cited by 72
“Infants of mothers who have had malaria in the past are probably less severely affected because maternal IgG transfer; however, they are not completely protected [27, 29, 32].”
BackgroundInfluentialvan Eijk, A. M., Ayisi, J., ter Kuile, F. O., Misore, A. O., Otieno, J. A., KOLCZAK, M. S., Kager, P. A., Steketee, R. W., & Nahlen, B. L. (2001) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2001.65.623 · Cited by 71
Metadata
- Authors
- McGregor, I. A.
- Corresponding author
- McGregor, Ian A.
- Venue
- The American Journal of Tropical Medicine and Hygiene
- Published
- 1984-07
- Volume
- 33
- Issue
- 4
- Pages
- 517-525
- ISSN
- 0002-9637 (ISSN-L)
- OpenAlex
- W74585451
- Cited by
- 452
- References
- 0
- Citations by year
- 2024: 7 · 2023: 4 · 2022: 1 · 2021: 8 · 2020: 5 · 2019: 5 · 2018: 8 · 2017: 9 · 2016: 7 · 2015: 10 · 2014: 11 · 2013: 14 · 2012: 14
- FWCI
- 2.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Tropical Medicine and Hygiene (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
- Social Sciences › Arts and Humanities › History › History of Medicine and Tropical Health
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Mosquito-borne diseases and control
- Keywords
- malaria in pregnancy, malaria epidemiology, mosquito control
- MeSH terms
- Adolescent, Adult, Africa, Birth Weight, Disease Susceptibility, Female, Fetal Blood, Fetal Death, Hemoglobins, Humans, Immunity, Active, Immunity, Maternally-Acquired, Immunoglobulins, Infant, Newborn, Malaria, Male, Maternal-Fetal Exchange, Middle Aged, Parity, Placenta Diseases, Plasmodium, Pregnancy, Pregnancy Complications, Infectious, Seasons, Uterus
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