Submicroscopic Plasmodium falciparum infections in pregnancy in Ghana
Open accessAbstract
Malarial parasitaemia below the threshold of microscopy but detectable by polymerase chain reaction (PCR) assays is common in endemic regions. This study was conducted to examine prevalence, predictors, and effects of submicroscopic Plasmodium falciparum infections in pregnancy. In a cross-sectional study among 530 pregnant women in Ghana, plasmodial infections were assessed by microscopy and PCR assays. Concentrations of haemoglobin and C-reactive protein (CRP) were measured and antimalarial drugs (chloroquine, pyrimethamine) in urine were demonstrated by ELISA dipsticks. By microscopy, 32% of the women were found to harbour malaria parasites. This rate increased to 63% adding the results of the parasite-specific PCR. P. falciparum was present in all but one infection. With increasing gravidity, infection rates and parasite densities decreased and the proportions of submicroscopic parasitaemia among infected women grew. Correspondingly, anaemia, fever and evidence of inflammation (CRP > 0.6 mg/dl) were more frequent in primigravidae than in multigravidae. Antimalarial drugs were detected in 65% of the women and were associated with a reduced prevalence of P. falciparum infections and a raised proportion of submicroscopic parasitaemia. Both gravidity and antimalarial drug use were independent predictors of submicroscopic P. falciparum infections. These infections caused a slight reduction of Hb levels and considerably increased serum concentrations of CRP. Conventional microscopy underestimates the actual extent of malarial infections in pregnancy in endemic regions. Submicroscopic P. falciparum infections are frequent and may contribute to mild anaemia and inflammation in seemingly aparasitaemic pregnant women.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Pregnant women may become asymptomatic reservoirs with low density infections and remain unidentified during routine passive surveillance because P. falciparum sequestration in the placenta hinders detection by RDT or microscopy.
“Pregnant women may become asymptomatic reservoirs with low density infections; remain unidentified during routine passive surveillance since P. falciparum sequestration in the placenta hinders their detection by RDT or microscopy”
From Intermittent preventive treatment with Sulphadoxine-Pyrimethamine (IPTp-SP) is associated with protection against sub-microscopic P. falciparum infection in pregnant women during the low transmission dry season in southwestern Cameroon: A Semi - longitudinal study (2022) · cites this paper as [31]
The proportion of submicroscopic parasitaemia among infected women decreased with increasing gravidity.
“and the proportion of submicroscopic parasitaemia among infected women decreased with increasing gravidity [31].”
From Intermittent preventive treatment with Sulphadoxine-Pyrimethamine (IPTp-SP) is associated with protection against sub-microscopic P. falciparum infection in pregnant women during the low transmission dry season in southwestern Cameroon: A Semi - longitudinal study (2022) · cites this paper as [31]
SMIs are frequently detected in pregnant women in sub-Saharan Africa and were associated with adverse outcomes in several cross-sectional and longitudinal studies.
“SMIs are also frequently detected in pregnant women in sub-Saharan Africa and were associated with adverse outcomes in several cross-sectional (21)(22)(23)(24) and longitudinal studies (25,26).”
From Clinical outcomes of submicroscopic infections and correlates of protection of VAR2CSA antibodies in a longitudinal study of pregnant women in Colombia (2018) · cites this paper as [23]
An earlier study reported higher rates of submicroscopic infection with increasing parity, whereas other studies reported similar rates among women of different parities.
“An earlier study also reported higher rates of submicroscopic infection with increasing parity [47], whereas other studies have reported similar rates of sub microscopic infections among women of different parities [16,38,40].”
From Diagnosing malaria in pregnancy: An update (2012) · cites this paper as [47]
The association of maternal anemia to submicroscopic infection is inconsistent, with some studies finding a relationship and other studies not.
“However, the association of maternal anemia to submicroscopic infection (defined by PCR, qPCR or HRP2 methods) is inconsistent, with some studies finding a relationship [16,47,53] while other studies did not [38,40,47].”
From Diagnosing malaria in pregnancy: An update (2012) · cites this paper as [47]
Studies in Africa have consistently shown that conventional microscopy vastly underestimates infection compared to PCR in both peripheral and placental blood samples.
“These studies have consistently shown that conventional microscopy vastly underestimates infection compared to PCR in both peripheral and placental blood samples. 12-22”
From What is the burden of submicroscopic malaria in pregnancy in central India? (2015) · cites this paper as [12]
Submicroscopic infections were linked with maternal anemia in some studies but not all.
“Submicroscopic infections were linked with maternal anemia in some 17,18,20,23 but not all 12,13,15,21 studies.”
From What is the burden of submicroscopic malaria in pregnancy in central India? (2015) · cites this paper as [12]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Snounou, G., Viriyakosol, S., Zhu, X. P., Jarra, W., Pinheiro, L., do Rosario, V. E., Thaithong, S., & Brown, K. N. (1993) · Molecular and Biochemical Parasitology · doi:10.1016/0166-6851(93)90077-b · Cited by 1,591 · see citing works
Adherence of <i>Plasmodium falciparum</i> to Chondroitin Sulfate A in the Human Placenta
Fried, M., & Duffy, P. E. (1996) · Science · doi:10.1126/science.272.5267.1502 · Cited by 1,108 · see citing works
Maternal antibodies block malaria
Fried, M., Nosten, F., Brockman, A., Brabin, B. J., & Duffy, P. E. (1998) · Nature · doi:10.1038/27570 · Cited by 659 · see citing works
Bull, P. C., Lowe, B. S., Kortok, M., Molyneux, C. S., Newbold, C. I., & Marsh, K. (1998) · Nature Medicine · doi:10.1038/nm0398-358 · Cited by 645 · see citing works
Mortality and morbidity from malaria among children in a rural area of The Gambia, West Africa
Greenwood, B. M., Bradley, A. K., Greenwood, A. M., Byass, P., Jammeh, K., Marsh, K., Tulloch, S., Oldfield, F. S. J., & Hayes, R. (1987) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(87)90170-2 · Cited by 622 · see citing works
Beeson, J. G., Brown, G. V., Molyneux, M. E., Mhango, C., Dzinjalamala, F., & Rogerson, S. J. (1999) · The Journal of Infectious Diseases · doi:10.1086/314899 · Cited by 266 · see citing works
Massive chronic intervillositis of the placenta associated with malaria infection
Ordi, J., Ismail, M. R., Ventura, P. J., Kahigwa, E., Hirt, R., Cardesa, A., Alonso, P. L., & Menendez, C. (1998) · The American Journal of Surgical Pathology · doi:10.1097/00000478-199808000-00011 · Cited by 265 · see citing works
Reeder, J. C., Cowman, A. F., Davern, K. M., Beeson, J. G., Thompson, J. K., Rogerson, S. J., & Brown, G. V. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.9.5198 · Cited by 252 · see citing works
Dati, F., Schumann, G., Thomas, L., Aguzzi, F., BAUDNER, S., Bienvenu, J., Blaabjerg, O., Blirup-Jensen, S., Carlström, A., Petersen, P. H., et al. (1996) · PubMed · Cited by 195 · see citing works
Bottius, E., Guanzirolli, A., Trape, J.-F., Rogier, C., Konate, L., & Druilhe, P. (1996) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/s0035-9203(96)90463-0 · Cited by 190 · see citing works
Malaria Infection during Pregnancy: Intrauterine Growth Retardation and Preterm Delivery in Malawi
Sullivan, A. D., Nyirenda, T. E., Cullinan, T. R., Taylor, T. E., Harlow, S. D., James, S. A., & Meshnick, S. (1999) · The Journal of Infectious Diseases · doi:10.1086/314752 · Cited by 136 · see citing works
Leke, R. F. G., Djokam, R. R., Mbu, R., Leke, R. J., Fogako, J., Megnekou, R., Metenou, S., Sama, G., Zhou, Y., Cadigan, T., et al. (1999) · Journal of Clinical Microbiology · doi:10.1128/jcm.37.9.2992-2996.1999 · Cited by 118 · see citing works
Wagner, G., Koram, K., McGuinness, D., Bennett, S., Nkrumah, F., & Riley, E. (1998) · The American journal of tropical medicine and hygiene · doi:10.4269/ajtmh.1998.59.115 · Cited by 93 · see citing works
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 · see citing works
Maubert, B., Guilbert, L. J., & Deloron, P. (1997) · Infection and Immunity · doi:10.1128/iai.65.4.1251-1257.1997 · Cited by 84 · see citing works
High rate of mixed and subpatent malarial infections in southwest Nigeria.
May, J., Mockenhaupt, F. P., Ademowo, O. G., Falusi, A. G., Olumese, P. E., Bienzle, U., & Meyer, C. G. (1999) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1999.61.339 · Cited by 84 · see citing works
Self-citationMalaria-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 · see citing works
Steketee, R. W., Wirima, J. J., Breman, J. G., Slutsker, L., & Heymann, D. L. (1996) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1996.55.17 · Cited by 81 · see citing works
Gestational Malaria: Assessment of its Consequences on Fetal Growth
Meuris, S., Piko, B. B., Eerens, P., Vanbellinghen, A.-M., Dramaix, M., & Hennart, P. (1993) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1993.48.603 · Cited by 71 · cited 1× · see citing works
“Malaria results in intrauterine growth retardation, low birthweight and preterm delivery (Meuris et al. 1993; Ordi et al. 1998; Sullivan et al. 1999).”
BackgroundJarra, W., & Snounou, G. (1998) · Infection and Immunity · doi:10.1128/iai.66.8.3783-3787.1998 · Cited by 71 · see citing works
Incidence of clinical malaria in pregnant women exposed to intense perennial transmission
Diagne, N., Rogier, C., Cissé, B., & Trape, J. (1997) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/s0035-9203(97)90209-1 · Cited by 66 · see citing works
C-reactive protein and haptoglobin in the evaluation of a community-based malaria control programme.
McGuire, W., D'Alessandro, U., Olaleye, B., Thomson, M. C., Langerock, P., Greenwood, B., & Kwiatkowski, D. P. (1996) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/s0035-9203(96)90461-7 · Cited by 55 · see citing works
Desowitz, R. S., & Alpers, M. P. (1992) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034983.1992.11812638 · Cited by 40 · see citing works
Landgraf, B., Kollaritsch, H., Wiedermann, G., & Wernsdorfer, W. H. (1994) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(94)90424-3 · Cited by 36 · see citing works
Can malaria chemoprophylaxis be restricted to first pregnancies?
Greenwood, A. M., Menéndez, C., Alonso, P. L., Jaffar, S. S., Langerock, P., Lulat, S., Todd, J., M'Boge, B., Francis, N. A., & Greenwood, B. M. (1994) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(94)90228-3 · Cited by 30 · see citing works
Sensitive ELISA dipstick test for the detection of chloroquine in urine under field conditions
Schwick, P., Eggelte, T. A., Hess, F., Tueumuna, T. T., Payne, D. J., Nothdurft, H. D., von Sonnenburg, F., & Löscher, T. (1998) · Tropical Medicine & International Health · doi:10.1046/j.1365-3156.1998.00307.x · Cited by 24 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- Eggelte TA, Sondji S & Gussenhove G (1992) Simple dipstick tests for the determination of antimalarials in body fluids. Proceedings XIIIth International Congress for Tropical Medicine and Malaria, Pattaya, Thailand November 29 -December 4 (1992), 2, pp. 242.
Cited by
Sorted by citations
Malaria in pregnancy: pathogenesis and immunity
Rogerson, S. J., Hviid, L., Duffy, P. E., Leke, R. F., & Taylor, D. W. (2007) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(07)70022-1 · Cited by 628 · see citing works
TER KUILE, F. O., TERLOUW, D. J., PHILLIPS-HOWARD, P. A., HAWLEY, W. A., FRIEDMAN, J. F., KARIUKI, S. K., SHI, Y. P., KOLCZAK, M. S., LAL, A. A., VULULE, J. M., et al. (2003) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2003.68.50 · Cited by 204 · see citing works
Asymptomatic Carriage of Plasmodium in Urban Dakar: The Risk of Malaria Should Not Be Underestimated
Diallo, A., Ndam, N. T., Moussiliou, A., Dos Santos, S., Ndonky, A., Borderon, M., Oliveau, S., Lalou, R., & Le Hesran, J.-Y. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031100 · Cited by 154 · see citing works
Cottrell, G., Moussiliou, A., Luty, A. J. F., Cot, M., Fievet, N., Massougbodji, A., Deloron, P., & Tuikue Ndam, N. (2015) · Clinical Infectious Diseases · doi:10.1093/cid/civ122 · Cited by 151 · see citing works
Prevalence 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 · see citing works
High-Throughput Pooling and Real-Time PCR-Based Strategy for Malaria Detection
Taylor, S. M., Juliano, J. J., Trottman, P. A., Griffin, J., Landis, S., Kitsa, P., Tshefu, A. K., & Meshnick, S. R. (2009) · Journal of Clinical Microbiology · doi:10.1128/jcm.01800-09 · Cited by 147 · see citing works
Kattenberg, J. H., Ochodo, E. A., Boer, K. R., Schallig, H. D., Mens, P. F., & Leeflang, M. M. (2011) · Malaria Journal · doi:10.1186/1475-2875-10-321 · Cited by 138 · see citing works
WALKER-ABBEY, A., DJOKAM, R. R. T., ENO, A., LEKE, R. F. G., TITANJI, V. P. K., FOGAKO, J., SAMA, G., THUITA, L. H., BEARDSLEE, E., SNOUNOU, G., et al. (2005) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2005.72.229 · Cited by 132 · see citing works
Comparison of real-time PCR and microscopy for malaria parasite detection in Malawian pregnant women
Rantala, A.-M., Taylor, S. M., Trottman, P. A., Luntamo, M., Mbewe, B., Maleta, K., Kulmala, T., Ashorn, P., & Meshnick, S. R. (2010) · Malaria Journal · doi:10.1186/1475-2875-9-269 · Cited by 110 · see citing works
Diagnosis of Placental Malaria
Mockenhaupt, F. P., Ulmen, U., von Gaertner, C., Bedu-Addo, G., & Bienzle, U. (2002) · Journal of Clinical Microbiology · doi:10.1128/jcm.40.1.306-308.2002 · Cited by 108 · see citing works
Self-citationMayor, A., Serra-Casas, E., Bardají, A., Sanz, S., Puyol, L., Cisteró, P., Sigauque, B., Mandomando, I., Aponte, J. J., Alonso, P. L., et al. (2009) · Malaria Journal · doi:10.1186/1475-2875-8-9 · Cited by 105 · see citing works
Mayor, A., Moro, L., Aguilar, R., Bardají, A., Cisteró, P., Serra-Casas, E., Sigaúque, B., Alonso, P. L., Ordi, J., & Menéndez, C. (2012) · Clinical Infectious Diseases · doi:10.1093/cid/cis236 · Cited by 92 · see citing works
Anaemia 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 · see citing works
Self-citationUneke, C. J. (2007) · PubMed Central · Cited by 92 · see citing works
Hommerich, L., von Oertzen, C., Bedu‐Addo, G., Holmberg, V., Acquah, P. A., Eggelte, T. A., Bienzle, U., & Mockenhaupt, F. P. (2007) · Malaria Journal · doi:10.1186/1475-2875-6-144 · Cited by 83 · see citing works
Self-citationDetection and clinical manifestation of placental malaria in southern Ghana
Mockenhaupt, F. P., Bedu-Addo, G., von Gaertner, C., Boyé, R., Fricke, K., Hannibal, I., Karakaya, F., Schaller, M., Ulmen, U., Acquah, P. A., et al. (2006) · Malaria Journal · doi:10.1186/1475-2875-5-119 · Cited by 81 · see citing works
Self-citationDiagnosing 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 · see citing works
EVALUATION OF A MALARIA RAPID DIAGNOSTIC TEST FOR ASSESSING THE BURDEN OF MALARIA DURING PREGNANCY
SINGER, L. M., NEWMAN, R. D., DIARRA, A., MORAN, A. C., HUBER, C. S., STENNIES, G., SIRIMA, S. B., KONATE, A., YAMEOGO, M., SAWADOGO, R., et al. (2004) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2004.70.481 · Cited by 77 · see citing works
Cohee, L. M., Kalilani-Phiri, L., Boudova, S., Joshi, S., Mukadam, R., Seydel, K. B., Mawindo, P., Thesing, P., Kamiza, S., Makwakwa, K., et al. (2014) · Malaria Journal · doi:10.1186/1475-2875-13-274 · Cited by 75 · see citing works
Saute, 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 · see citing works
Elphinstone, R. E., Weckman, A. M., McDonald, C. R., Tran, V., Zhong, K., Madanitsa, M., Kalilani‐Phiri, L., Khairallah, C., Taylor, S. M., Meshnick, S. R., et al. (2019) · PLoS Medicine · doi:10.1371/journal.pmed.1002914 · Cited by 67 · see citing works
Mankhambo, L., Kanjala, M., Rudman, S., Lema, V. M., & Rogerson, S. J. (2002) · Journal of Clinical Microbiology · doi:10.1128/jcm.40.1.155-158.2002 · Cited by 65 · see citing works
Anchang-Kimbi, J. K., Achidi, E. A., Nkegoum, B., Sverremark-Ekström, E., & Troye-Blomberg, M. (2009) · Malaria Journal · doi:10.1186/1475-2875-8-126 · Cited by 65 · see citing works
Hawadak, J., Nana, R. R. D., & Singh, V. (2021) · Parasites & Vectors · doi:10.1186/s13071-021-04797-0 · Cited by 64 · see citing works
Malaria Diagnostics in Clinical Trials
Murphy, S. C., Shott, J. P., Parikh, S., Etter, P., Prescott, W. R., & Stewart, V. A. (2013) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.12-0675 · Cited by 64 · see citing works
Kalilani‐Phiri, L., Thesing, P. C., Nyirenda, O. M., Mawindo, P., Madanitsa, M., Gadama, G. M., Wylie, B. J., Masonbrink, A. R., Makwakwa, K., Kamiza, S., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074643 · Cited by 62 · see citing works
Kamwendo, D., Dzinjalamala, F. K., Snounou, G., Kanjala, M. K., Mhango, C. G., Molyneux, M. E., & Rogerson, S. J. (2002) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/s0035-9203(02)90284-1 · Cited by 62 · see citing works
Leke, R. F. G., Bioga, J. D., Zhou, J., Fouda, G. G., LEKE, R. J. I., Tchinda, V. H. M., Megnekou, R., Fogako, J., Sama, G., Gwanmesia, P., et al. (2010) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2010.10-0249 · Cited by 60 · see citing works
Ray, S., Renu, D., Srivastava, R., Gollapalli, K., Taur, S. R., Jhaveri, T. A., Dhali, S., Chennareddy, S., Potla, A., Dikshit, J. B., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041751 · Cited by 55 · see citing works
The Effect of Malaria and Intestinal Helminth Coinfection on Birth Outcomes in Kumasi, Ghana
Yatich, N., Jolly, P. E., Funkhouser, E. M., Agbenyega, T., Rayner, J. C., Ehiri, J. E., Turpin, A., Stiles, J. K., Ellis, W. O., Jiang, Y., et al. (2010) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2010.09-0165 · Cited by 55 · see citing works
Muñóz, J., Rojo-Marcos, G., Ramírez‐Olivencia, G., Salas-Coronas, J., Treviño, B., Pérez-Arellano, J.-L., Torrús, D., Vilches, M. J. M., Ramos, J. M., Alegría, I., et al. (2014) · Enfermedades Infecciosas y Microbiología Clínica · doi:10.1016/j.eimc.2013.12.014 · Cited by 54 · see citing works
Uneke, C. J. (2008) · Parasitology Research · doi:10.1007/s00436-007-0782-6 · Cited by 53 · see citing works
Point-of-care diagnostics to improve maternal and neonatal health in low-resource settings
Majors, C. E., Smith, C. A., Natoli, M. E., Kundrod, K. A., & Richards-Kortum, R. R. (2017) · Lab on a Chip · doi:10.1039/c7lc00374a · Cited by 52 · see citing works
Mayengue, P. I., Rieth, H., Khattab, A., Issifou, S., Kremsner, P. G., Klinkert, M., & Ntoumi, F. (2004) · Tropical Medicine & International Health · doi:10.1111/j.1365-3156.2004.01294.x · Cited by 50 · see citing works
Conroy, A. L., Liles, W. C., Molyneux, M. E., Rogerson, S. J., & Kain, K. C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028540 · Cited by 46 · see citing works
Multiplicity of Plasmodium falciparum infection in pregnancy.
Beck, S., Mockenhaupt, F. P., Bienzle, U., Eggelte, T. A., Thompson, W. N. A., & Stark, K. (2001) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2001.65.631 · Cited by 46 · see citing works
Self-citationKyabayinze, D. J., Tibenderana, J. K., Nassali, M., Tumwine, L. K., Riches, C., Montague, M., Counihan, H., Hamade, P., Van Geertruyden, J.-P., & Meek, S. (2011) · Malaria Journal · doi:10.1186/1475-2875-10-306 · Cited by 42 · see citing works
Taylor, S. M., van Eijk, A. M., Hand, C. C., Mwandagalirwa, K., Messina, J. P., Tshefu, A. K., Atua, B., Emch, M., Muwonga, J. M., Meshnick, S. R., et al. (2011) · The Journal of Infectious Diseases · doi:10.1093/infdis/jir625 · Cited by 41 · see citing works
Determinants of anaemia in pregnancy in sekyere west district, ghana.
Glover‐Amengor, M., Owusu, W. B., & Akanmori, B. D. (2005) · PubMed Central · Cited by 41 · see citing works
Use of a highly-sensitive rapid diagnostic test to screen for malaria in pregnancy in Indonesia
Unwin, V. T., Ahmed, R., Noviyanti, R., Puspitasari, A. M., Utami, R. A. S., Trianty, L., Lukito, T., Syafruddin, D., Poespoprodjo, J. R., Santana-Morales, M. A., et al. (2020) · Malaria Journal · doi:10.1186/s12936-020-3110-6 · Cited by 40 · see citing works
Minja, D. T., Schmiegelow, C., Oesterholt, M., Magistrado, P. A., Boström, S., John, D., Pehrson, C., Andersen, D., Deloron, P., Salanti, A., et al. (2012) · Malaria Journal · doi:10.1186/1475-2875-11-211 · Cited by 37 · see citing works
Ofori, M. F., Staalsoe, T., Bam, V., Lundquist, M., David, K. P., Browne, E. N. L., Akanmori, B. D., & Hviid, L. (2003) · Infection and Immunity · doi:10.1128/iai.71.3.1584-1586.2003 · Cited by 37 · see citing works
Luntamo, M., Rantala, A.-M., Meshnick, S. R., Cheung, Y. B., Kulmala, T., Maleta, K. M., & Ashorn, P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0041123 · Cited by 36 · see citing works
Helegbe, G. K., Aryee, P. A., Mohammed, B. S., Wemakor, A., Kolbila, D. Z., Abubakari, A.-W., Askanda, S., Alhassan, R., Barnie, C., Donkoh, A. A., et al. (2018) · Canadian Journal of Infectious Diseases and Medical Microbiology · doi:10.1155/2018/5610981 · Cited by 35 · see citing works
Unger, H. W., Rosanas-Urgell, A., Robinson, L. J., Ome-Kaius, M., Jally, S., Umbers, A. J., Pomat, W., Mueller, I., Kattenberg, E., & Rogerson, S. J. (2019) · Malaria Journal · doi:10.1186/s12936-019-2931-7 · Cited by 35 · see citing works
Williams, J. E., Cairns, M. E., Njie, F., Quaye, S. L., Awine, T., Oduro, A. R., Tagbor, H. K., Bojang, K., Magnussen, P., ter Kuile, F. O., et al. (2015) · Clinical Infectious Diseases · doi:10.1093/cid/civ1198 · Cited by 36 · see citing works
Adam, I., A-Elbasit, I. E., Salih, I., & Elbashir, M. I. (2005) · Annals of Tropical Medicine & Parasitology · doi:10.1179/136485905x36244 · Cited by 34 · see citing works
Arango, E., Maestre, A., & Carmona-Fonseca, J. (2010) · Revista Brasileira de Epidemiologia · doi:10.1590/s1415-790x2010000300002 · Cited by 33 · see citing works
Trends of malaria infection in pregnancy in Ghana over the past two decades: a review
Osarfo, J., Ampofo, G. D., & Tagbor, H. K. (2022) · Malaria Journal · doi:10.1186/s12936-021-04031-3 · Cited by 34 · see citing works
van Eijk, A. M., Stepniewska, K., Hill, J., Taylor, S. M., Rogerson, S. J., Cottrell, G., Chico, R. M., Gutman, J., Tinto, H., Unger, H. W., et al. (2023) · The Lancet Global Health · doi:10.1016/s2214-109x(23)00194-8 · Cited by 31 · see citing works
Self-citationAkanbi, O., Odaibo, A. B., Afolabi, K., & Ademowo, O. G. (2004) · Medical Principles and Practice · doi:10.1159/000081915 · Cited by 28 · see citing works
Malaria in pregnancy: diagnosing infection and identifying fetal risk
Conroy, A. L., McDonald, C. R., & Kain, K. C. (2012) · Expert Review of Anti-infective Therapy · doi:10.1586/eri.12.123 · Cited by 27 · see citing works
MiRNA-146a polymorphism increases the odds of malaria in pregnancy
van Loon, W., Gai, P. P., Hamann, L., Bedu‐Addo, G., & Mockenhaupt, F. P. (2019) · Malaria Journal · doi:10.1186/s12936-019-2643-z · Cited by 27 · see citing works
Self-citationGavina, K., Gnidehou, S., Arango, E., Hamel-Martineau, C., Mitran, C., Agudelo, O., Lopez, C., Karidio, A., Banman, S., Carmona-Fonseca, J., et al. (2018) · Infection and Immunity · doi:10.1128/iai.00797-17 · Cited by 26 · see citing works
Zhou, Z., Mitchell, R. M., Gutman, J., Wiegand, R. E., Mwandama, D. A., Mathanga, D. P., Skarbinski, J., & Shi, Y. P. (2014) · Malaria Journal · doi:10.1186/1475-2875-13-509 · Cited by 26 · see citing works
What is the burden of submicroscopic malaria in pregnancy in central India?
Singh, N., Bharti, P. K., Singh, M. P., Singh, R., Yeboah-Antwi, K., Desai, M., Udhayakumar, V., Muniyandi, M., Hamer, D. H., & Wylie, B. J. (2015) · Pathogens and Global Health · doi:10.1179/2047773215y.0000000002 · Cited by 25 · see citing works
Maternal anaemia as an indicator for monitoring malaria control in pregnancy in sub‐Saharan Africa
Savage, E., Msyamboza, K. P., Gies, S., D’Alessandro, U., & Brabin, B. J. (2007) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2007.01420.x · Cited by 25 · see citing works
Wogu, M. D. (2014) · International Journal of TROPICAL DISEASE & Health · doi:10.9734/ijtdh/2013/2738 · Cited by 25 · see citing works
Tagbor, H. (2008) · Therapeutics and Clinical Risk Management · doi:10.2147/tcrm.s2809 · Cited by 24 · see citing works
Dhorda, M., Piola, P., Nyehangane, D., Tumwebaze, B., Nalusaji, A., Nabasumba, C., Turyakira, E., McGready, R., Ashley, E., Guerin, P. J., et al. (2012) · The American Society of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2012.10-0631 · Cited by 23 · see citing works
Mockenhaupt, F. P., Eggelte, T. A., Till, H., & Bienzle, U. (2001) · Tropical Medicine & International Health · doi:10.1046/j.1365-3156.2001.00792.x · Cited by 23 · see citing works
Self-citationEffect of antimalarial drugs and malaria infection on oxidative stress in pregnant women.
Akanbi, O., Odaibo, A. B., & Ademowo, O. G. (2010) · PubMed · Cited by 22 · see citing works
Ntoumi, F., Bakoua, D., Anna, F., Kombo, M., Christevy, V. J., & Koukouikila-Koussounda, F. (2015) · Acta Tropica · doi:10.1016/j.actatropica.2015.10.009 · Cited by 21 · see citing works
Factors influencing urban malaria: a comparative study of two communities in the Accra Metropolis
Brenyah, R., Osakunor, D., & Ephraim, R. (2014) · African Health Sciences · doi:10.4314/ahs.v13i4.19 · Cited by 20 · see citing works
Hounkonnou, C., Briand, V., Fiévet, N., Accrombessi, M., Yovo, E., Mama, A., Sossou, D., Vianou, B., Massougbodji, A., Ndam, N. T., et al. (2019) · Clinical Infectious Diseases · doi:10.1093/cid/ciz748 · Cited by 20 · see citing works
Submicroscopic and multiple plasmodium falciparum infections in pregnant Sudanese women
Omer, S., Khalil, E., Ali, H., & Sharief, A. (2011) · North American Journal of Medical Sciences · doi:10.4297/najms.2011.3137 · Cited by 19 · see citing works
Imported submicroscopic malaria in Madrid
Ramírez‐Olivencia, G., Rubio, J. M., Rivas, P., Subirats, M., Herrero, M. D., Lago, M., & Puente, S. (2012) · Malaria Journal · doi:10.1186/1475-2875-11-324 · Cited by 19 · see citing works
Nwaefuna, E. K., Afoakwah, R., Orish, V. N., Egyir-Yawson, A., & Boampong, J. N. (2015) · Journal of Parasitology Research · doi:10.1155/2015/959427 · Cited by 17 · see citing works
Mbouamboua, Y., Koukouikila-Koussounda, F., Ntoumi, F., Adukpo, S., Kombo, M., Vouvoungui, J. C., van Helden, J., & Kobawila, S. C. (2019) · Acta Tropica · doi:10.1016/j.actatropica.2019.03.001 · Cited by 17 · see citing works
Mockenhaupt, F. P., Eggelte, T. A., Böhme, T., Thompson, W. N. A., & Bienzle, U. (2001) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2001.65.21 · Cited by 17 · see citing works
Self-citationResisting and tolerating P. falciparum in pregnancy under different malaria transmission intensities
Ndam, N. T., Mbuba, E., González, R., Cisteró, P., Kariuki, S., Sevene, E., Rupérez, M., Fonseca, A. M., Valá, A., Maculuve, S. A., et al. (2017) · BMC Medicine · doi:10.1186/s12916-017-0893-6 · Cited by 16 · see citing works
Ajonina, M. U., Ajonina-Ekoti, I. U., Ngulefac, J., Ade, N., Awambeng, D. N., Nfor, C. K., Ayim, M., & Apinjoh, T. O. (2024) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-024-06769-5 · Cited by 16 · see citing works
Persistence of Plasmodium falciparum Parasites in Infected Pregnant Mozambican Women after Delivery
Serra‐Casas, E., Menéndez, C., Dobaño, C., Bardají, A., Quintó, L., Ordï, J., Sigaúque, B., Cisteró, P., Mandomando, I., Alonso, P. L., et al. (2010) · Infection and Immunity · doi:10.1128/iai.00814-10 · Cited by 14 · see citing works
Coulibaly, S. O., NEZIEN, D., Traoré, S., Koné, B., & Magnussen, P. (2006) · Malaria Journal · doi:10.1186/1475-2875-5-49 · Cited by 14 · see citing works
Apinjoh, T. O., Ntui, V. N., Chi, H. F., Moyeh, M. N., Toussi, C. T., Mayaba, J. M., Tangi, L. N., Kwi, P. N., Anchang-Kimbi, J. K., Dionne-Odom, J., et al. (2022) · PLOS ONE · doi:10.1371/journal.pone.0275370 · Cited by 13 · see citing works
Peripheral and Placental Biomarkers in Women With Placental Malaria: A Systematic Review
Ruizendaal, E., van Leeuwen, E., & Mens, P. F. (2015) · Biomarkers in Medicine · doi:10.2217/bmm.14.117 · Cited by 11 · see citing works
Bouaziz, O., Courtin, D., Cottrell, G., Milet, J., Nuel, G., & Garcia, A. (2017) · Clinical Infectious Diseases · doi:10.1093/cid/cix899 · Cited by 10 · see citing works
Ampofo, G. D., Osarfo, J., Okyere, D. D., Kouevidjin, E., Aberese-Ako, M., & Tagbor, H. K. (2025) · BMC Pregnancy and Childbirth · doi:10.1186/s12884-025-07735-5 · Cited by 9 · see citing works
Malaria parasitemia during delivery
Ahmed, S. M., Mohamedani, A. A., Habour, A., & Sadek, A. (2002) · Saudi Medical Journal · doi:10.15537/1658-3175.1731 · Cited by 9 · see citing works
Role of malaria induced oxidative stress on anaemia in pregnancy
Akanbi, O., Odaibo, A., Olatoregun, R., & Ademowo, A. (2010) · Asian Pacific Journal of Tropical Medicine · doi:10.1016/s1995-7645(10)60011-9 · Cited by 8 · see citing works
Mbacham, H. F., Mosume, D. M., Apinjoh, T. O., Ntui, V. N., Moyeh, M. N., Kalaji, L. N., Wepnje, G. B., Ghogomu, S. M., Dionne, J. A., Tita, A., et al. (2023) · Malaria Journal · doi:10.1186/s12936-023-04485-7 · Cited by 5 · see citing works
Seth, M. D., Mdetele, D., Phillips, S. T., Buza, J., & African, M. (2015) · Cited by 7 · see citing works
Zablon, K. N., Kakilla, C., Lykina, T., Minakova, V., Chibago, A., & Bochkaeva, Z. (2015) · Malaria Research and Treatment · doi:10.1155/2015/473203 · Cited by 5 · see citing works
Hopkins, H., & Cunningham, J. A. (2019) · Wiley eBooks · doi:10.1002/9781119282686.ch7 · Cited by 5 · see citing works
Diagnostic Tools of Malaria During Pregnancy
Mayor, A. G., & Meshnick, S. R. (2015) · Springer eBooks · doi:10.1007/978-1-4614-8326-7_68 · Cited by 4 · see citing works
Tarimo, D. S. (2016) · Asian Pacific Journal of Tropical Disease · doi:10.12980/apjtd.7.2017d6-360 · Cited by 3 · see citing works
Madanitsa, M. (2016) · University of Liverpool · doi:10.17638/02003527 · Cited by 1 · see citing works
Ajonina, M. U., Ajonina-Ekoti, I. U., Ngulefac, J., Ade, N., Awambeng, D. N., Nfor, C. K., Ayim, M., & Apinjoh, T. O. (2024) · medRxiv · doi:10.1101/2024.05.29.24308147 · Cited by 1 · see citing works
Estudio del metabolismo del hierro en lactantes de una alta y perenne transmisión de malaria.
Giménez, N. (2003) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas)
Ansar, W., & Ghosh, S. (2016) · Springer eBooks · doi:10.1007/978-81-322-2680-2_11
Gavina, K. (2018) · ERA: Education and Research Archive (University of Alberta) · doi:10.7939/r3w08wz46
Bashir, N., Ashraf, S., Rashid, N., Naqvi, S. T. R., Majeed, S., Murtaza, G., Ashiq, M. N., & Haq, M. N. U. (2021) · Springer eBooks · doi:10.1007/978-3-030-76320-6_21
Anato, A., Laillou, A., Nanama, S., Ntambi, J., Seyoum, Y., & Baye, K. (2025) · Nutrition reviews · doi:10.1093/nutrit/nuaf219
Hawadak, J., Nana, R. R. D., & Singh, V. (2021) · Figshare · doi:10.6084/m9.figshare.14728580
Mbacham, H. F., Mosume, D. M., Apinjoh, T. O., Ntui, V. N., Moyeh, M. N., Kalaji, L. N., Wepnje, G. B., Ghogomu, S. M., Dionne, J. A., Tita, A. T. N., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22615097
Hawadak, J., Nana, R. R. D., & Singh, V. (2021) · Figshare · doi:10.6084/m9.figshare.14728577
Hawadak, J., Nana, R. R. D., & Singh, V. (2021) · Figshare · doi:10.6084/m9.figshare.14728568
Mbacham, H. F., Mosume, D. M., Apinjoh, T. O., Ntui, V. N., Moyeh, M. N., Kalaji, L. N., Wepnje, G. B., Ghogomu, S. M., Dionne, J. A., Tita, A. T. N., et al. (2023) · Figshare · doi:10.6084/m9.figshare.22615088
- Authors
- Mockenhaupt, F. P., Rong, B., Till, H., Eggelte, T. A., Beck, S., Gyasi‐Sarpong, C., Thompson, W. N. A., & Bienzle, U.
- Affiliations
- Humboldt-Universität zu Berlin (DE)
- Amsterdam UMC Location University of Amsterdam (NL)
- Venue
- Tropical Medicine & International Health
- Publisher
- Wiley
- Published
- 2000-03
- Volume
- 5
- Issue
- 3
- Pages
- 167-173
- ISSN
- 1360-2276 (ISSN-L)
- 1365-3156
- OpenAlex
- W2033480254
- Cited by
- 105
- References
- 26
- Citations by year
- 2025: 2 · 2024: 2 · 2023: 5 · 2022: 2 · 2021: 8 · 2020: 1 · 2019: 7 · 2018: 3 · 2017: 3 · 2016: 3 · 2015: 9 · 2014: 6 · 2013: 2 · 2012: 9
- FWCI
- 5.14
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Tropical Medicine & International Health (publishedVersion)
- PubMed (publishedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- Royal Society
- Royal Society of Tropical Medicine and Hygiene
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
- Health Sciences › Medicine › Genetics › Hemoglobinopathies and Related Disorders
- Life Sciences › Immunology and Microbiology › Parasitology › Bird parasitology and diseases
- Keywords
- Plasmodium falciparum, submicroscopic malaria infection, malaria in pregnancy, gravidity, antimalarial drug use, chloroquine, pyrimethamine, C-reactive protein, anemia, malaria prevalence, Ghana
- MeSH terms
- Adult, Anemia, Animals, Antimalarials, Cross-Sectional Studies, Female, Fever, Ghana, Humans, Inflammation, Plasmodium falciparum, Pregnancy, Pregnancy Trimesters, Pregnancy Complications, Parasitic, Prevalence, Malaria, Falciparum, Parasitemia, Gravidity
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review