Submicroscopic Plasmodium falciparum infections during pregnancy, in an area of Sudan with a low intensity of malaria transmission
Abstract
There are few published studies on the burden of malaria during pregnancy from areas of sub-Saharan Africa where the intensity of malarial transmission is low, and few on submicroscopic malarial infections in pregnant women. The present study was conducted in New Halfa, an area of low-intensity transmission in eastern Sudan, between August 2003 and July 2004. The main aims were to assess the prevalences of submicroscopic and multiple Plasmodium falciparum infections in pregnant women (using the P. falciparum merozoite surface protein-2 as a polymorphic marker in PCR-based assays) and to determine the effects of such infections on anaemia during pregnancy. Of the 142 pregnant women who were recruited, only 17 (11.9%) were found smear-positive for P. falciparum by microscopy. The results of the PCR-based assays revealed, however, that 40 (32%) of the 125 smear-negative women had submicroscopic P. falciparum infections. Blood samples from 32 (80%) of those with submicroscopic infections showed only the FC 27 allele (of merozoite surface protein-2), six (15%) showed only the ICI allele, and two (5%) showed both of these alleles. Although the age, parity, gestational age and haemoglobin concentrations of the women with submicroscopic P. falciparum infections were not significantly different from those of the women who were smear- and PCR-negative, such infections may have a significant impact on materno-foetal health.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Whether applied to peripheral blood or placental blood samples, PCR methods yield positivity rates 20% or more above those of blood smear microscopy.
“Whether applied to peripheral blood or placental blood samples, PCR methods yield positivity rates 20% or more above those of BS microscopy (Tables 3 & 4) [10,14–16,38–46].”
From Diagnosing malaria in pregnancy: An update (2012) · cites this paper as [39]
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
The burden of malaria in pregnancy in malaria-endemic areas
Steketee, R., Nahlen, B., Parise, M., & Menendez, C. (2001) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2001.64.28 · Cited by 1,063 · see citing works
Plowe, C. V., DJIMDÉ, A. A., Bouaré, M., Doumbo, O. K., & Wellems, T. E. (1995) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1995.52.565 · Cited by 675 · see citing works
Epidemiology, Malaria and Pregnancy
McGregor, I. A. (1984) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1984.33.517 · Cited by 452 · cited 1× · see citing works
“In contrast, those women who live in areas of stable and intense transmission enjoy considerable immunity and generally experience few symptoms during episodes of malarial infection, although some may develop severe anaemia (McGregor, 1984; Brabin, 1993; Newman et al., 2003; Okoko et al., 2003).”
BackgroundRoper, C., Elhassan, I. M., Hviid, L., Giha, H. A., Richardson, W. A., Babiker, H. A., Satti, G. M. H., Theander, T. G., & Arnot, D. E. (1996) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1996.54.325 · Cited by 188 · see citing works
Robert, F., Ntoumi, F., Angel, G., Candito, D., Rogier, C., Fandeur, T., Sarthou, J. L., & Mercereau‐Puijalon, O. (1996) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/s0035-9203(96)90446-0 · Cited by 173 · see citing works
Newman, R. D., Hailemariam, A. T., Jima, D., Degifie, A., Kebede, D., Rietveld, A. E. C., Nahlen, B. L., Barnwell, J. W., Steketee, R. W., & Parise, M. E. (2003) · The Journal of Infectious Diseases · doi:10.1086/374878 · Cited by 140 · see citing works
Färnert, A., Rooth, I., Svensson, Å., Snounou, G., & Björkman, A. (1999) · The Journal of Infectious Diseases · doi:10.1086/314652 · Cited by 139 · see citing works
Submicroscopic <i>Plasmodium falciparum</i> infections in pregnancy in Ghana
Mockenhaupt, F. P., Rong, B., Till, H., Eggelte, T. A., Beck, S., Gyasi‐Sarpong, C., Thompson, W. N. A., & Bienzle, U. (2000) · Tropical Medicine & International Health · doi:10.1046/j.1365-3156.2000.00532.x · Cited by 105 · see citing works
The epidemiology and consequences of maternal malaria: a review of immunological basis
Okoko, B. J., Enwere, G., & Ota, M. O. C. (2003) · Acta Tropica · doi:10.1016/s0001-706x(03)00097-4 · Cited by 98 · 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
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
Hoffmann, L. (2001) · Annals of Tropical Medicine and Parasitology · doi:10.1080/00034980120045833 · Cited by 61 · see citing works
Malaria and Low Birth Weight in Central Sudan
Taha, T. E., Gray, R. H., & Mohamedani, A. A. (1993) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a116861 · Cited by 59 · 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
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
Maternal mortality in a teaching hospital in Sudan
Dafallah, S. E., El-Agib, F. H., & Bushra, G. O. (2003) · Saudi Medical Journal · doi:10.15537/1658-3175.2012 · Cited by 41 · see citing works
Quinine therapy in severe Plasmodium falciparum malaria during pregnancy in Sudan
Adam, I., Mirghani, O. A., Saed, O. K., Ahmed, S. M., Mohamadani, A. A., Ahmed, H. M. S., Mackenzie, C. D., Homeida, M. M. A., & Bashir, M. I. E. (2004) · Eastern Mediterranean Health Journal · doi:10.26719/2004.10.1-2.159 · Cited by 25 · see citing works
Self-citationA study of the consequences of malarial infection in pregnant women and their infants.
Brabin, B. J., Maxwell, S. L., Chimsuku, L., Verhoeff, F. H., Hj, V. D. K., Broadhead, R., Kazembe, P., & Thomas, A. (1993) · PubMed · Cited by 24 · see citing works
Severe malaria in west African children
Kurtzhals, J. A. L., Helleberg, M., Goka, B. Q., & Akanmori, B. D. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13068-1 · Cited by 11 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Barcus, M. J., Basri, H., Picarima, H., Manyakori, C., Sekartuti, Elyazar, I., Bangs, M. J., Maguire, J. D., & Baird, J. K. (2007) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2007.77.984 · Cited by 195 · 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
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
Mayor, 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
Adam, I., Ibrahim, Y., & Elhardello, O. (2018) · BMC Hematology · doi:10.1186/s12878-018-0124-1 · Cited by 104 · see citing works
“The minimum sample size was 125 participants in a study conducted in New Halfa [22].”
BackgroundSelf-citationDynamics of Anti‐VAR2CSA Immunoglobulin G Response in a Cohort of Senegalese Pregnant Women
Tuikue Ndam, N. G., Salanti, A., Le‐Hesran, J. ‐., Cottrell, G., Fievet, N., Turner, L., Sow, S., Dangou, J. ‐., Theander, T., & Deloron, P. (2006) · The Journal of Infectious Diseases · doi:10.1086/500146 · Cited by 89 · see citing works
Detection 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
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 · 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
Mohammed, A. H., Salih, M. M., Elhassan, E. M., Mohmmed, A. A., Elzaki, S. E., El-Sayed, B. B., & Adam, I. (2013) · Malaria Journal · doi:10.1186/1475-2875-12-172 · Cited by 59 · see citing works
Self-citationAdam, I., Elhassan, E. M., Haggaz, A. E. D., Ali, A. A. A., & Adam, G. K. (2010) · The Journal of Infection in Developing Countries · doi:10.3855/jidc.1282 · Cited by 54 · see citing works
Self-citationUneke, C. J. (2008) · Parasitology Research · doi:10.1007/s00436-007-0782-6 · Cited by 53 · see citing works
Adam, I., Babiker, S., Mohmmed, A. A., Salih, M. M., Prins, M. H., & Zaki, Z. M. (2007) · Malaria Journal · doi:10.1186/1475-2875-6-110 · Cited by 43 · 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
Arango, E., Maestre, A., & Carmona-Fonseca, J. (2010) · Revista Brasileira de Epidemiologia · doi:10.1590/s1415-790x2010000300002 · Cited by 33 · 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
Maestre, A., & Carmona‐Fonseca, J. (2014) · The Journal of Infection in Developing Countries · doi:10.3855/jidc.3777 · Cited by 27 · see citing works
Fluorescence microscope (Cyscope®) for malaria diagnosis in pregnant women in Medani Hospital, Sudan
Hassan, S. E.-D., Haggaz, A. E. D., Mohammed-Elhassan, E. B., Malik, E. M., & Adam, I. (2011) · Diagnostic Pathology · doi:10.1186/1746-1596-6-88 · Cited by 26 · see citing works
Self-citationAdam, I., Adam, G. K., Mohmmed, A. A., Salih, M. M., Ibrahuim, S. A., & Ryan, C. A. (2009) · Journal of Parasitology · doi:10.1645/ge-1912.1 · Cited by 24 · see citing works
Self-citationEpidemiology and aetiology of maternal parasitic infections in low- and middle-income countries.
Roberts, T., Gravett, C. A., Velu, P. P., Τheodoratou, E., Wagner, T. A., Zhang, J. S. F., Campbell, H. J., Rubens, C. E., Gravett, M. G., & Rudan, I. (2011) · PubMed Central · 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
Pregnant women carrying female fetuses are at higher risk of placental malaria infection
Adam, I., Salih, M. M., Mohmmed, A. A., Rayis, D. A., & Elbashir, M. I. (2017) · PLoS ONE · doi:10.1371/journal.pone.0182394 · Cited by 19 · see citing works
Self-citationOmer, S. A., Noureldein, A. N., Eisa, H., Abdelrahim, M., Idress, H. E., Abdelrazig, A. M., & Adam, I. (2019) · Journal of Tropical Medicine · doi:10.1155/2019/3162378 · Cited by 15 · see citing works
Self-citationTagelsir, N., Ibrahim, Z., Medani, A.-R., Salih, O., Hamad, A., Giha, H. A., Elagib, A. A., Khan, B., Saeed, N., & Ibrahim, M. E. (2005) · Acta Tropica · doi:10.1016/j.actatropica.2005.07.030 · Cited by 14 · see citing works
Elbashir, H. M., Salih, M. M., Elhassan, E. M., Mohmmed, A. A., Elbashir, M. I., & Adam, I. (2011) · Diagnostic Pathology · doi:10.1186/1746-1596-6-128 · Cited by 12 · see citing works
Self-citationEpidemiology and Seasonal Pattern of Malaria in an Irrigated Area of Eastern Sudan
Himeidan, Y. E., Malik, E. M., & Adam, I. (2005) · American Journal of Infectious Diseases · doi:10.3844/ajidsp.2005.75.78 · Cited by 11 · see citing works
Self-citationAdam, I., Elmardi, K. A., & Malik, E. M. (2008) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/j.trstmh.2008.07.005 · Cited by 7 · see citing works
Self-citationFadlelseed, O. E., Osman, M. E., Shamseldin, N. M., Elhussein, A. B., & Adam, I. (2017) · Heliyon · doi:10.1016/j.heliyon.2017.e00326 · Cited by 6 · see citing works
Self-citationOsman, A. A., Osman, Y. E., Ibrahim, Y., Mussa, A., Mohamed, Z., Suppain, R., & Hajissa, K. (2022) · SN Comprehensive Clinical Medicine · doi:10.1007/s42399-022-01160-x · Cited by 4 · see citing works
Odio, B. N., Ajah, L. O., Ibekwe, P. C., Ajah, M. I., Ugwu, G., Nwankwo, T. O., & Anikwe, C. C. (2020) · Global Journal of Health Science · doi:10.5539/gjhs.v12n8p52 · Cited by 1 · see citing works
Elsheikh, H., Adam, I., Elhassan, E. M., Mohammed, A. A., Khamis, A. H., & Elbashir, M. I. (2017) · F1000Research · doi:10.12688/f1000research.10641.1
Self-citationDeresinski, S. C. (2006) · Clinical Infectious Diseases · doi:10.1086/500024
- Authors
- Adam, I., A-Elbasit, I. E., Salih, I., & Elbashir, M. I.
- Affiliations
- New Halfa Teaching HospitalP.O. Box 61, New Halfa, Sudan
- University of Khartoum (SD)
- ORCID
- Adam, I.
- Venue
- Annals of Tropical Medicine & Parasitology
- Publisher
- Informa UK Limited
- Published
- 2005-06
- Volume
- 99
- Issue
- 4
- Pages
- 339-344
- ISSN
- 0003-4983 (ISSN-L)
- 1364-8594
- OpenAlex
- W2087744036
- Cited by
- 34
- References
- 20
- Citations by year
- 2022: 1 · 2020: 1 · 2019: 1 · 2018: 1 · 2017: 3 · 2014: 2 · 2013: 2 · 2012: 3
- FWCI
- 3.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annals of Tropical Medicine and Parasitology (publishedVersion)
- PubMed (publishedVersion)
- 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, merozoite surface protein 2
- MeSH terms
- Adult, Anemia, Animals, Female, Hemoglobins, Humans, Parity, Plasmodium falciparum, Pregnancy, Sudan, Pregnancy Complications, Parasitic, Prevalence, DNA, Protozoan, Polymerase Chain Reaction, Malaria, Falciparum
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