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Cited by 18Malaria Research and ControlVector-borne infectious diseasesHemoglobinopathies and Related Disorders

Reliability of rapid diagnostic test for diagnosing peripheral and placental malaria in an area of unstable malaria transmission in Eastern Sudan

Open access
Kashif, Awadalla H, Adam, Gamal K, Mohmmed, Ahmed A, Elzaki, Salah E, AbdelHalim, Ahmed M, Adam, Ishag·2013·Diagnostic Pathology
DOI 10.1186/1746-1596-8-59PMC PMC3640898
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Abstract

Background: Diagnosing Plasmodium falciparum malaria during pregnancy is a great challenge for clinicians because of the low density of parasites in the peripheral blood and parasite sequestration in the placenta. Nevertheless, few data on the use of malaria rapid diagnostic test (RDT) during pregnancy have been published. Methods: P. falciparum infections were assessed in 156 febrile pregnant women by microscopic examination of their blood smears and by RDT and polymerase chain reactions (PCR). In addition, 150 women were assessed at the time of delivery by microscopy, RDT, PCR and placental histology investigations. The study was conducted at the Gadarif Hospital, Eastern Sudan. The SD Bioline P. f / P. v (Bio Standard Diagnostics, Gurgaon, Korea) RDT kit was evaluated in this study. Results: Among the febrile pregnant women, 17 (11.0%), 26 (16.7%) and 18 (11.5%) positive cases of P. falciparum were detected by microscopy, RDT, and PCR, respectively. The sensitivity and specificity of the microscopy was 94.4% and 100%, respectively. The corresponding values for RDT evaluation were 83.3% and 92.0%, as compared with PCR as the gold standard. While there were no detected cases of malaria by microscopic examination of blood smears, 27 (18.0%), 21(14.0%) and 46 (30.7%) out of the 150 placentae investigated had P. falciparum as determined by RDT, PCR, and histology, respectively. The sensitivity and specificity for RDT was 17.4% and 81.7%, respectively. The corresponding values for PCR were 6.5% and 82.7%, where histology was used as the gold standard. Conclusions: The RDT kit used in this study has poor performance for peripheral and placental P. falciparum malaria detection in this setting. Virtual slides: The virtual slide(s) for this article can be found here: http://www.diagnosticpathology.diagnomx.eu/vs/1092363465928479

AI snapshot

Written from the paper’s full text.

TL;DR

In febrile pregnant women in Eastern Sudan, the SD Bioline P.f/P.v rapid diagnostic test had moderate sensitivity (83.3%) and acceptable specificity (92.0%) for peripheral P. falciparum malaria compared with PCR, but poor sensitivity (17.4%) and specificity (81.7%) for placental malaria compared with placental histology. The authors conclude the RDT kit has poor performance for peripheral and placental P. falciparum malaria detection in this setting.

Key findings

  • Among 156 febrile pregnant women, P. falciparum positivity was 17 (11.0%) by microscopy, 26 (16.7%) by RDT, and 18 (11.5%) by PCR. Against PCR, microscopy had sensitivity 94.4% and specificity 100%; RDT had sensitivity 83.3%, specificity 92.0%, PPV 57.7%, and NPV 97.7%.
  • Among 150 placentae at delivery, no malaria cases were detected by microscopy, while RDT detected 27 (18.0%), PCR detected 21 (14.0%), and histology detected 46 (30.7%). Against histology, RDT had sensitivity 17.4%, specificity 81.7%, PPV 29.6%, and NPV 69.6% in the text (table reports 69.1%); PCR had sensitivity 6.5% and specificity 82.7%.
  • Against PCR for placental malaria, RDT had sensitivity 14.3%, specificity 81.4%, PPV 11.1%, and NPV 85.4%.
  • The authors conclude that the RDT kit used has poor performance for peripheral and placental P. falciparum malaria detection in this setting.

Methods

  • Cross-sectional studies were conducted at Gadarif Hospital, Eastern Sudan, from September through December 2011, in an area of unstable malaria transmission where P. falciparum is the sole malaria species.
  • The first study recruited 156 febrile pregnant women (temperature ≥ 37.5°C) and compared RDT and microscopy with PCR as the reference standard for peripheral parasitaemia. The second study assessed 150 women at delivery by microscopy, RDT, PCR, and placental histology, using histology as the reference standard for placental malaria.
  • The RDT evaluated was SD Bioline P.f/P.v (Bio Standard Diagnostics, Gurgaon, Korea). Sensitivity, specificity, PPV, and NPV were calculated using SPSS version 19.0; sample sizes were calculated with Epi Info using 80% power and 95% confidence intervals.

Limitations

  • The paper does not include a formal limitations section (not stated in the paper).
  • Evident from the text: the study was hospital-based and conducted at a single site in an area of unstable transmission with P. falciparum only, so findings may not generalize to other transmission settings or species.
  • Evident from the text: no placental malaria cases were detected by microscopy, limiting direct comparison of microscopy with histology/PCR for placental infection; the authors also discuss possible false-positive RDT results due to persistent HRP-2 antigenaemia.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1186/1746-1596-8-59

Cites

37 of 37 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 31 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    RDT had a specificity of 81.7% compared with histology for detecting placental malaria.

    “The sensitivity, specificity, PPV and NPV for the RDT kit were 17.4%, 81.7%, 29.6% and 69.6%, respectively.”
    Quote in the paperSubstantial claim
  • Findingown data

    PCR had a sensitivity of 6.5% compared with histology for detecting placental malaria.

    “The corresponding values for PCR were 6.5%, 82.7%, 14.3% and 66.7%, where histology was used as the gold standard, Table 3, Figure 2 and Figure 3.”
    Quote in the paperSubstantial claim
  • Findingown data

    RDT had a positive predictive value of 29.6% compared with histology for detecting placental malaria.

    “The sensitivity, specificity, PPV and NPV for the RDT kit were 17.4%, 81.7%, 29.6% and 69.6%, respectively.”
    Quote in the paperSubstantial claim
  • Findingown data

    RDT had a specificity of 81.4% compared with PCR for detecting placental malaria.

    “Likewise, the sensitivity, specificity, PPV and NPV for the RDT kit were low (14.3%, 81.4%, 11.1% and 85.43%, respectively), where PCR was used as the gold standard, Table 4.”
    Quote in the paperSubstantial claim
  • Findingown data

    PCR had a negative predictive value of 66.7% compared with histology for detecting placental malaria.

    “The corresponding values for PCR were 6.5%, 82.7%, 14.3% and 66.7%, where histology was used as the gold standard, Table 3, Figure 2 and Figure 3.”
    Quote in the paperNot a substantial claim
  • Classified as probably not a substantial claim. 17
  • May combine two claims. 11

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    RDT had high sensitivity (96.8%) and specificity (73.5%) for diagnosis of P. falciparum malaria among febrile pregnant women in a hyper-endemic region in Uganda, compared with microscopy as the gold standard.

    “Nevertheless, it has been observed that RDT had high sensitivity (96.8%) and specificity (73.5%) for the diagnosis of P. falciparum malaria among febrile pregnant women in a hyper-endemic region in Uganda, when compared with microscopy as the gold standard [15].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [15] Kyabayinze DJ, Tibenderana JK, Nassali M, Tumwine LK, Riches C, Montague M, Counihan H, Hamade P, Van Geertruyden JP, Meek S: Placental Plasmodium falciparum malaria infection: operational accuracy of HRP2 rapid diagnostic tests in a malaria endemic setting. Malar J. 2011, 10: 306-10.1186/1475-2875-10-306. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Among 122 women PCR-positive for P. falciparum, 87 (71.3%) and 74 (60.7%) were not considered positive by peripheral microscopy and HRP2 RDT, respectively.

    “Furthermore, Mayor et al., [16] have recently shown that among the 122 women that were PCR-positive for P. falciparum (as judged by peripheral and/or placental blood sampling) 87 (71.3%) and 74 (60.7%) were not considered positive by peripheral microscopy and the HRP2 RDT, respectively.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [16] Mayor A, Moro L, Aguilar R, Bardají A, Cisteró P, Serra-Casas E, Sigaúque B, Alonso PL, Ordi J, Menéndez C: How hidden can malaria be in pregnant women? Diagnosis by microscopy, placental histology, polymerase chain reaction and detection of histidine-rich protein 2 in plasma. Clin Infect Dis. 2012, 54 (11): 1561-1568. 10.1093/cid/cis236. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    RDT kits used during pregnancy in Uganda had low sensitivity (31.8%) but full specificity (100%) when PCR was used as the gold standard.

    “Recently low sensitivity (31.8%) but full specificity (100%) was reported for RDT kits used during pregnancy in Uganda, where PCR was used as the gold standard [13].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [13] Dhorda M, Piola P, Nyehangane D, Tumwebaze B, Nalusaji A, Nabasumba C, Turyakira E, McGready R, Ashley E, Guerin PJ, Snounou G: Performance of a histidine-rich protein 2 rapid diagnostic test, Paracheck Pf®, for detection of malaria infections in Ugandan pregnant women. Am J Trop Med Hyg. 2012, 86 (1): 93-95. 10.4269/ajtmh.2012.10-0631. source

      Not checked in the free run.

  • Classified as probably not a substantial claim. May combine two claims.

    Premisecitation

    The prevalence of placental infection determined by microscopy and RDT was 5.1% and 5.0%, respectively, with highly significant agreement (82.9%); discordances were observed between the two methods at low level parasitaemias.

    “Recently, the prevalence of placental infection, as determined by microscopy and RDT, was 5.1% and 5.0%, respectively, with highly significant agreement (82.9%); however discordances were observed between the two methods at low level parasitaemias [12].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [12] Aguilar R, Machevo S, Menéndez C, Bardají A, Nhabomba A, Alonso PL, Mayor A: Comparison of placental blood microscopy and the ICT HRP2 rapid diagnostic test to detect placental malaria. Trans R Soc Trop Med Hyg. 2012, 106 (9): 573-575. 10.1016/j.trstmh.2012.05.001. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    HRP2-based RDT positivity among pregnant women can persist for up to 28 days after antimalarial drug treatment, especially among women with low gravidity and those with a higher parasite density at enrolment.

    “It should be mentioned that HRP2 based RDT positivity among pregnant women can persist for up to 28 days after antimalarial drug treatment, especially among women with low gravidity and those with a higher parasite density at enrolment [14].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [14] Kattenberg JH, Tahita CM, Versteeg IA, Tinto H, Traoré-Coulibaly M, Schallig HD, Mens PF: Antigen persistence of rapid diagnostic tests in pregnant women in Nanoro, Burkina Faso, and the implications for the diagnosis of malaria in pregnancy. Trop Med Int Health. 2012, 17 (5): 550-557. 10.1111/j.1365-3156.2012.02975.x. source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    The World Health Organization now recommends a parasite-based diagnosis of malaria infection.

    “The World Health Organization (WHO) now recommends a parasite-based diagnosis of malaria infection [6].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [6] World Health Organization (WHO) Guidelines for the treatment of malaria: Geneva. 2010, Switzerland: WHO, 9241546948

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Previous studies conducted at the time of birth have shown that RDT detecting P. falciparum HRP2 are more sensitive than blood smears, and appear to be reliable predictors of adverse outcomes of malaria in pregnancy.

    “Previous studies conducted at the time of birth have shown that RDT detecting P. falciparum HRP2 are more sensitive than blood smears, and appear to be reliable predictors of adverse outcomes of malaria in pregnancy [30-32].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [30] Mockenhaupt FP, Bedu-Addo G, von Gaertner C, Boye R, Fricke K, Hannibal I, Karakaya F, Schaller M, Ulmen U, Acquah PA, Dietz E, Eggelte TA, Bienzle U: Detection and clinical manifestation of placental malaria in southern Ghana. Malar J. 2006, 5: 119-10.1186/1475-2875-5-119. source

      Not checked in the free run.

    • cites [31] Mockenhaupt FP, Ulmen U, von Gaertner C, Bedu-Addo G, Bienzle U: Diagnosis of placental malaria. J Clin Microbiol. 2002, 40: 306-308. 10.1128/JCM.40.1.306-308.2002. source

      Not checked in the free run.

    • cites [32] Singer LM, Newman RD, Diarra A, Moran AC, Huber CS, Stennies G, Sirima SB, Konate A, Yameogo M, Sawadogo R, Barnwell JW, Parise ME: Evaluation of a malaria rapid diagnostic test for assessing the burden of malaria during pregnancy. Am J Trop Med Hyg. 2004, 70: 481-485. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    Blood film microscopy is time-consuming and needs significant technical skills, good-quality reagents, and clean slides; its accuracy is of highly variable quality in sub-Saharan African hospitals.

    “However, blood film microscopy is time-consuming and needs significant technical skills, good-quality reagents, and clean slides; thus, its accuracy is of highly variable quality in sub-Saharan African hospitals [7-10].”
    Quote in the paperSubstantial claim0 of 4 sources checked
    • cites [7] Moerman F, Lengeler C, Chimumbwa J, Talisuna A, Erhart A, Coosemans M, D’Alessandro U: The contribution of the health-care service to a sound and sustainable malaria-control policy. Lancet Infect Dis. 2003, 3: 99-102. 10.1016/S1473-3099(03)00518-8. source

      Not checked in the free run.

    • cites [8] Nkrumah B, Acquah SEK, Ibrahim L, May J, Brattig N, Tannich E, Nguah SB, Adu-Sarkodie Y, Huenger F: Comparative evaluation of two rapid field tests for malaria diagnosis: partec rapid malaria test and binax now malaria rapid diagnostic test. BMC Infect Dis. 2011, 11: 143-170. 10.1186/1471-2334-11-143. source

      Not checked in the free run.

    • cites [9] Nankabirwa J, Zurovac D, Njogu JN, Rwakimari JB, Counihan H, Snow RW, Tibenderana JK: Malaria misdiagnosis in Uganda–implications for policy change. Malar J. 2009, 8: 66-10.1186/1475-2875-8-66. source

      Not checked in the free run.

    • cites [10] McMorrow ML, Masanja MI, Abdulla SM, Kahigwa E, Kachur SP: Challenges in routine implementation and quality control of rapid diagnostic tests for malaria–Rufiji District, Tanzania. Am J Trop Med Hyg. 2008, 79: 385-390. source

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Prescription of any drug during pregnancy poses a risk to the unborn child.

    “This goal is of fundamental importance because prescription of any drug during pregnancy poses a risk to the unborn child [5].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [5] Bánhidy F, Lowry RB, Czeizel AE: Risk and benefit of drug use during pregnancy. Int J Med Sci. 2005, 2: 100-106. source

      Not checked in the free run.

  • May combine two claims.

    Premisecitation

    RDT is easy to use, heat stable, and has the ability to detect low parasitaemias.

    “It has been shown that RDT is easy to use, are heat stable and have the ability to detect low parasitaemias [11].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [11] World Health Organization: Results of WHO product testing of malaria rapid diagnostic tests. Malaria Rapid Diagnostic Test Peformance. Round 1 (2008). 2012, Geneva: World Health Organization

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Placental histology smears were examined by a senior pathologist, blindly.

    “Placental histology smears were examined by a senior pathologist, blindly (AAM).”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Pregnant Sudanese women are at risk of malaria regardless of their age or parity, and malaria is associated with adverse maternal and perinatal outcomes.

    “Pregnant Sudanese women are at risk of malaria regardless of their age or parity and malaria is associated with adverse maternal and perinatal outcomes [18].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [18] Adam I, Elhassan EM, Haggaz AE, Ali AA, Adam GK: A perspective of the epidemiology of malaria and anaemia and their impact on maternal and perinatal outcomes in Sudan. J Infect Dev Ctries. 2011, 5 (2): 83-87. source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    A negative control sample containing no template DNA and an internal positive control were used for quality control purposes.

    “A negative control sample containing no template DNA and an internal positive control were used for quality control purposes.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Blood smears were examined by two independent laboratory technologists who were blinded to each other's results.

    “Blood smears were stained with 10% Giemsa and examined under the X100 oil immersion objective lens of a light microscope by two independent laboratory technologists that were blinded to each other's results.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    The slide and RDT results were read by two individuals blinded to each other's results.

    “The slide and RDT results were read by two individuals blinded to each other's results.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The sample sizes were calculated based on 2-sided hypothesis tests using Epi Info with 80% power and a 95% confidence interval.

    “The sample sizes were calculated based on 2-sided hypothesis tests using Epi Info with 80% power and a confidence interval of 95%.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductnone given

    All of the study research team were trained and had continuous supervision by the pathologist and site supervisor.

    “All of the study research team were trained and had continuous supervision by the pathologist and site supervisor.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The manufacturer's storage temperature specifications (4-30°C) were adhered to by monitoring the air temperature during transportation and storage.

    “The manufacturer's storage temperature specifications (4-30°C) were adhered to by monitoring the air temperature during transportation and storage.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    PCR was performed by the research team who were blind to the microscopy, RDT, and histology results.

    “Likewise, the PCR was performed by the research team (AH and SA) who were blind to the microscopy, RDT, and histology results.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    The manufacturer's instructions were strictly followed.

    “Although the manufacturer’s (Bio Standard Diagnostics, Gurgaon, Korea) instructions were strictly followed, the poor performance this RDT kit in the current study is disappointing, and perhaps somewhat difficult to explain.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Premisecitation

    The study area is characterized by unstable malaria transmission and P. falciparum is the sole malaria species present.

    “The area is characterized by unstable malaria transmission and P. falciparum is the sole malaria species present [22].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [22] Malik EM, Atta HY, Weis M, Lang A, Puta C, Lettenmaier C:Sudan RBM Country Consultative Mission Final Report. Sudan Roll Back Malaria Consultative Mission: Essential Actions to Support the Attainment of the Abuja Targets. 2004, Geneva: Roll Back Malaria Partnership,

      Not checked in the free run.

21 of 21

  • The paper relies on this without support.

    RDT has not yet been implemented as standard methods for diagnosing malaria during pregnancy in Sudan.

    “RDT has not yet been implemented as standard methods for diagnosing malaria during pregnancy in Sudan.”
1 of 1

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

Each contradiction between two passages listed here was confirmed by an independent check.

  • Placental RDT estimate falls outside its reported confidence interval

    Minor

    Table 3 reports a negative predictive value of 69.1%, but its stated 95% confidence interval ends at 67.8%.

  • Discussion names the wrong reference standard for placental RDT results

    Minor

    The 17.4% sensitivity and 81.7% specificity are calculated against histology in Table 3, not PCR. Table 4 reports 14.3% and 81.4% when PCR is the reference standard.

  • Discussion attributes PCR's predictive value to the RDT

    Minor

    In its discussion of the RDT, the paper calls its PPV 14.3%. Table 3 reports 29.6% for the RDT; 14.3% is the PPV for PCR against histology.

3 of 3

Cites

Flagged first, then by citations

1 of the 38 references couldn’t be matched to a known paper.

Research works printed but not linked: 2

  1. World Health Organization (WHO) Guidelines for the treatment of malaria: Geneva. 2010, Switzerland: WHO, 9241546948
  2. World Health Organization: Results of WHO product testing of malaria rapid diagnostic tests. Malaria Rapid Diagnostic Test Peformance. Round 1 (2008). 2012, Geneva: World Health Organization

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Authors
Kashif, A. H., Adam, G. K., Mohmmed, A. A., Elzaki, S. E., AbdelHalim, A. M., & Adam, I.
Affiliations
  • University of Khartoum (SD)
  • Gadarif University (SD)
  • National Ribat University (SD)
  • National Centre for Research (Sudan) (SD)
Corresponding author
Adam, Ishag
ORCID
Adam, Ishag
Venue
Diagnostic Pathology
Publisher
Springer Science and Business Media LLC
Published
2013-04-15
Volume
8
Issue
1
Pages
59-59
ISSN
1746-1596 (ISSN-L)
DOI
10.1186/1746-1596-8-59
PMC
PMC3640898
OpenAlex
W2137220788
Cited by
18
References
38
Citations by year
2025: 2 · 2023: 1 · 2022: 3 · 2021: 1 · 2020: 1 · 2018: 2 · 2017: 2 · 2016: 1 · 2015: 1 · 2014: 3 · 2013: 1
FWCI
2.04
Type
journal article
Language
en
Open access
Licence
Locations
  • Diagnostic Pathology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Greater South Information System
Topics
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Malaria Research and Control
  • Life Sciences › Immunology and Microbiology › Parasitology › Vector-borne infectious diseases
  • Health Sciences › Medicine › Genetics › Hemoglobinopathies and Related Disorders
Keywords
Plasmodium falciparum, malaria in pregnancy, placental malaria, rapid diagnostic tests, diagnostic accuracy, placental histology, PCR, microscopy, unstable malaria transmission, Eastern Sudan
MeSH terms
Adult, Cross-Sectional Studies, Female, Humans, Microscopy, Parasitology, Placenta, Plasmodium falciparum, Predictive Value of Tests, Pregnancy, Quality Control, Reagent Kits, Diagnostic, Sensitivity and Specificity, Sudan, Reproducibility of Results, Pregnancy Complications, Parasitic, DNA, Protozoan, Polymerase Chain Reaction, Malaria, Falciparum, Young Adult

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