Submicroscopic and multiple plasmodium falciparum infections in pregnant Sudanese women

Omer, Samia; Khalil, Eltahir; Ali, Hashim; Sharief, Abdalla

doi:10.4297/najms.2011.3137

Cited by 19Malaria Research and ControlBird parasitology and diseasesHemoglobinopathies and Related Disorders

Submicroscopic and multiple plasmodium falciparum infections in pregnant Sudanese women

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Omer, Samia, Khalil, Eltahir, Ali, Hashim, Sharief, Abdalla·2011·North American Journal of Medical Sciences

DOI 10.4297/najms.2011.3137PMC PMC3336900

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Abstract

BACKGROUND: Control of malaria during pregnancy remains a major public health challenge in developing countries. Microscopic parasite detection represents a pivotal step in malaria control, while modern molecular techniques are deemed to improve detection rates markedly. AIMS: This study aimed to investigate the frequency of submicroscopic and multiple Plasmodium falciparum (P. falciparum) infections during pregnancy, using the P. falciparum merozoite surface protein1 (MSP-1) gene as a polymorphic marker. MATERIALS AND METHODS: The study was a cross-sectional, analytical study that was conducted at Omdurman Maternity Hospital, Sudan, between July 2003 and December 2004. Following informed consent, 836 pregnant women between the ages of 16-47 years with different gestational ages were enrolled in the study. Thin and thick blood films were stained with Giemsa and examined by experienced microscopists. Parasite DNA was extracted using Chelex method. Nested polymerase chain reaction (PCR) assays specific for P. falciparum were carried out to detect infections below the threshold of microscopy and to genotype different strains in the samples using merozoite surface protein-1. RESULTS: More than a quarter of the study participants (219/836; 26.2%) were smear-positive for malaria infection. The results of the PCR-based assays showed that 41.8 % (257/617) of the smear-negative women were PCR positive and therefore had submicroscopic infections. The mean number of genetically different P. falciparum parasites detected was 2.7 (range 1-9). The multiplicity of infection identified by at least two alleles of MSP-1 was significantly higher among paucigravidae (45.6%) compared to multigravidae (28.9%), with mean number of alleles of 2.4 and 1.9, respectively (p=0.009). This likely indicates the gradual acquisition of immunity. CONCLUSION: Conventional microscopy underestimates the actual extent of malaria infections during pregnancy in endemic regions. Multiplicity of infection may be an important factor in the gradual acquisition of strain-specific immunity.

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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 [19]

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An analysis of malaria in pregnancy in Africa.
Brabin, B. J. (1983) · PubMed · Cited by 785 · see citing works
Pyrimethamine and Proguanil Resistance-Conferring Mutations in Plasmodium falciparum Dihydrofolate Reductase: Polymerase Chain Reaction Methods for Surveillance in Africa
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
“falciparum) infection as opposed to their non-pregnant counterparts [1-4].”
Background
Malaria during pregnancy: A priority area of malaria research and control
Menéndez, C. (1995) · Parasitology Today · doi:10.1016/0169-4758(95)80151-0 · Cited by 322 · see citing works
Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria
Beeson, J. G., Rogerson, S. J., Cooke, B. M., Reeder, J. C., Chai, W., Lawson, A. M., Molyneux, M. E., & Brown, G. V. (2000) · Nature Medicine · doi:10.1038/71582 · Cited by 310 · see citing works
Malaria: even more chronic in nature than previously thought; evidence for subpatent parasitaemia detectable by the polymerase chain reaction
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
THE EFFECTS OF PLASMODIUM FALCIPARUM AND P. VIVAX INFECTIONS ON PLACENTAL HISTOPATHOLOGY IN AN AREA OF LOW MALARIA TRANSMISSION
McGREADY, R., DAVISON, B. B., STEPNIEWSKA, K., CHO, T., SHEE, H., BROCKMAN, A., UDOMSANGPETCH, R., LOOAREESUWAN, S., WHITE, N. J., MESHNICK, S. R., et al. (2004) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2004.70.398 · Cited by 170 · see citing works
4. Age dependence of the multiplicity of Plasmodium falciparum infections and of other malariological indices in an area of high endemicity
Smith, T. A., Beck, H., Kitua, A. Y., Mwankusye, S., Felger, I., Fraser‐Hurt, N., Irion, A. R., Alonso, P. L., Teuscher, T. M., & Tanner, M. (1999) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/s0035-9203(99)90322-x · Cited by 149 · 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
No influence of age on infection complexity and allelic distribution in Plasmodium falciparum infections in Ndiop, a Senegalese village with seasonal, mesoendemic malaria.
Zwetyenga, J. S. L. G., Rogier, C., Tall, A., Fontenille, D., Snounou, G., Trape, J., & Mercereau‐Puijalon, O. (1998) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1998.59.726 · Cited by 132 · see citing works
MALARIA IN PREGNANT CAMEROONIAN WOMEN: THE EFFECT OF AGE AND GRAVIDITY ON SUBMICROSCOPIC AND MIXED-SPECIES INFECTIONS AND MULTIPLE PARASITE GENOTYPES
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
Malaria and pregnancy.
Bruce-Chwatt, L. J. (1983) · BMJ · doi:10.1136/bmj.286.6376.1457 · Cited by 129 · see citing works
MICROSCOPIC AND SUB-MICROSCOPIC PLASMODIUM FALCIPARUM INFECTION, BUT NOT INFLAMMATION CAUSED BY INFECTION, IS ASSOCIATED WITH LOW BIRTH WEIGHT
ADEGNIKA, A. A., VERWEIJ, J. J., AGNANDJI, S. T., CHAI, S. K., BREITLING, L. P., RAMHARTER, M., FROLICH, M., ISSIFOU, S., KREMSNER, P. G., & YAZDANBAKHSH, M. (2006) · The American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2006.75.798 · Cited by 113 · see citing works
Sub-microscopic infections and long-term recrudescence of Plasmodium falciparum in Mozambican pregnant women
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
Submicroscopic Plasmodium falciparum 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
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
Risk factors for malaria infection and anemia for pregnant women in the Sahel area of Bandiagara, Mali
Dicko, A., Mantel, C. F., Thera, M. A., Doumbia, S., Diallo, M., Diakité, M., Sagara, I., & Doumbo, O. K. (2003) · Acta Tropica · doi:10.1016/j.actatropica.2003.07.001 · Cited by 77 · see citing works
Malaria in pregnancy in rural Mozambique: the role of parity, submicroscopic and multiple Plasmodium falciparum infections
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
Plasmodium falciparum: PCR detection and genotyping of isolates from peripheral, placenta), and cord blood of pregnant Malawian women and their infants
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
Submicroscopic Plasmodium falciparum infections and multiplicity of infection in matched peripheral, placental and umbilical cord blood samples from Gabonese women
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
PCR typing of Plasmodium falciparum in matched peripheral, placental and umbilical cord blood
Kassberger, F., Birkenmaier, A., Khattab, A., Kremsner, P. G., & Klinkert, M. (2002) · Parasitology Research · doi:10.1007/s00436-002-0715-3 · Cited by 43 · see citing works
Submicroscopic Plasmodium falciparum infections during pregnancy, in an area of Sudan with a low intensity of malaria transmission
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
Increased multiplicity of Plasmodium falciparum infections and skewed distribution of individual msp1 and msp2 alleles during pregnancy in Ndiop, a Senegalese village with seasonal, mesoendemic malaria.
Schleiermacher, D., Rogier, C., Spiegel, A., Tall, A., Trape, J., & Mercereau‐Puijalon, O. (2001) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2001.64.303 · Cited by 34 · see citing works
Plasmodium falciparummalaria in pregnancy: Prevalence of peripheral parasitaemia, anaemia and malaria care-seeking behaviour among pregnant women attending two antenatal clinics in Edo State, Nigeria
Enato, E. F. O., Mens, P. F., Okhamafe, A. O., Okpere, E. E., Pogoson, E., & Schallig, H. D. F. H. (2009) · Journal of Obstetrics and Gynaecology · doi:10.1080/01443610902883320 · Cited by 22 · see citing works

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Authors: Omer, S., Khalil, E., Ali, H., & Sharief, A.
Affiliations: National Centre for Research (Sudan) (SD)
University of Khartoum (SD)
Corresponding author: Omer, Samia
ORCID: Omer, Samia
Khalil, Eltahir
Venue: North American Journal of Medical Sciences
Publisher: Medknow
Published: 2011
Volume: 3
Issue: 3
Pages: 137-141
ISSN: 1947-2714 (ISSN-L)
DOI: 10.4297/najms.2011.3137
PMC: PMC3336900
OpenAlex: W2153542611
Cited by: 19
References: 25
Citations by year: 2025: 1 · 2022: 1 · 2021: 1 · 2020: 2 · 2019: 3 · 2018: 3 · 2017: 2 · 2015: 2 · 2014: 1 · 2013: 2
FWCI: 1.26
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
Locations: North American Journal of Medical Sciences (publishedVersion, cc-by-nc-sa)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion, cc-by-nc-sa)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
Life Sciences › Immunology and Microbiology › Parasitology › Bird parasitology and diseases
Health Sciences › Medicine › Genetics › Hemoglobinopathies and Related Disorders
Keywords: Plasmodium falciparum, malaria in pregnancy, submicroscopic malaria infection, multiplicity of infection, merozoite surface protein 1, strain-specific immunity, multigravidae, malaria parasite detection, Sudan

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Submicroscopic and multiple plasmodium falciparum infections in pregnant Sudanese women

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