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Published in: Malaria Journal 1/2008

Open Access 01-12-2008 | Research

Enhanced detection of gametocytes by magnetic deposition microscopy predicts higher potential for Plasmodium falciparum transmission

Authors: Stephan Karl, Makindi David, Lee Moore, Brian T Grimberg, Pascal Michon, Ivo Mueller, Maciej Zborowski, Peter A Zimmerman

Published in: Malaria Journal | Issue 1/2008

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Abstract

Background

Aggregated haemozoin crystals within malaria-infected erythrocytes confer susceptibility of parasitized cells to a magnetic field. Here the utility of this method for diagnosis of human malaria is evaluated in a malaria-endemic region of Papua New Guinea (PNG).

Methods and findings

Individuals with Plasmodium falciparum malaria symptoms (n = 55) provided samples for conventional blood smear (CBS) and magnetic deposition microscopy (MDM) diagnosis. Standard Giemsa staining and light microscopy was performed to evaluate all preparations. Plasmodium falciparum parasitaemia observed on MDM slides was consistently higher than parasitaemia observed by (CBS) for ring (CBS = 2.6 vs. MDM = 3.4%; t-test P-value = 0.13), trophozoite (CBS = 0.5 vs. MDM = 1.6%; t-test P-value = 0.01), schizont (CBS = 0.003 vs. MDM = 0.1%; t-test P-value = 0.08) and gametocyte (CBS = 0.001 vs. MDM = 0.4%; t-test P-value = 0.0002) parasitaemias. Gametocyte prevalence determined by CBS compared to MDM increased from 7.3% to 45%, respectively.

Conclusion

MDM increased detection sensitivity of P. falciparum-infected, haemozoin-containing erythrocytes from infected humans while maintaining detection of ring-stage parasites. Gametocyte prevalence five-fold higher than observed by CBS suggests higher malaria transmission potential in PNG endemic sites compared to previous estimates.
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Literature
1.
go back to reference Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI: The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature. 2005, 434: 214-7. 10.1038/nature03342.PubMedCentralCrossRefPubMed Snow RW, Guerra CA, Noor AM, Myint HY, Hay SI: The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature. 2005, 434: 214-7. 10.1038/nature03342.PubMedCentralCrossRefPubMed
2.
go back to reference Zimmerman PA, Mehlotra RK, Kasehagen LJ, Kazura JW: Why do we need to know more about mixed Plasmodium species infections in humans?. Trends in Parasitology. 2004, 20: 440-447. 10.1016/j.pt.2004.07.004.PubMedCentralCrossRefPubMed Zimmerman PA, Mehlotra RK, Kasehagen LJ, Kazura JW: Why do we need to know more about mixed Plasmodium species infections in humans?. Trends in Parasitology. 2004, 20: 440-447. 10.1016/j.pt.2004.07.004.PubMedCentralCrossRefPubMed
3.
go back to reference Zimmerman PA, Thomson JM, Fujioka H, Collins WE, Zborowski M: Diagnosis Of Malaria By Magnetic Deposition Microscopy. Am J Trop Med Hyg. 2006, 74: 568-572.PubMedCentralPubMed Zimmerman PA, Thomson JM, Fujioka H, Collins WE, Zborowski M: Diagnosis Of Malaria By Magnetic Deposition Microscopy. Am J Trop Med Hyg. 2006, 74: 568-572.PubMedCentralPubMed
4.
go back to reference Noland GS, Briones N, Sullivan DJ: The shape and size of hemozoin crystals distinguishes diverse Plasmodium species. Mol Biochem Parasitol. 2003, 130: 91-9. 10.1016/S0166-6851(03)00163-4.CrossRefPubMed Noland GS, Briones N, Sullivan DJ: The shape and size of hemozoin crystals distinguishes diverse Plasmodium species. Mol Biochem Parasitol. 2003, 130: 91-9. 10.1016/S0166-6851(03)00163-4.CrossRefPubMed
5.
go back to reference Mehlotra RK, Lorry K, Kastens W, Miller SM, Alpers MP, Bockarie M, Kazura JW, Zimmerman PA: Random distribution of mixed species malaria infections in Papua New Guinea. Am J Trop Med Hyg. 2000, 62: 225-31.PubMed Mehlotra RK, Lorry K, Kastens W, Miller SM, Alpers MP, Bockarie M, Kazura JW, Zimmerman PA: Random distribution of mixed species malaria infections in Papua New Guinea. Am J Trop Med Hyg. 2000, 62: 225-31.PubMed
6.
go back to reference Genton B, al-Yaman F, Beck HP, Hii J, Mellor S, Narara A, Gibson N, Smith T, Alpers MP: The epidemiology of malaria in the Wosera area, East Sepik Province, Papua New Guinea, in preparation for vaccine trials. I. Malariometric indices and immunity. Ann Trop Med Parasitol. 1995, 89: 359-76.PubMed Genton B, al-Yaman F, Beck HP, Hii J, Mellor S, Narara A, Gibson N, Smith T, Alpers MP: The epidemiology of malaria in the Wosera area, East Sepik Province, Papua New Guinea, in preparation for vaccine trials. I. Malariometric indices and immunity. Ann Trop Med Parasitol. 1995, 89: 359-76.PubMed
7.
go back to reference Kasehagen LJ, Mueller I, McNamara DT, Bockarie MJ, Kiniboro B, Rare L, Lorry K, Kastens W, Reeder JC, Kazura JW, Zimmerman PA: Changing patterns of Plasmodium blood-stage infections in the Wosera region of Papua New Guinea monitored by light microscopy and high throughput PCR diagnosis. Am J Trop Med Hyg. 2006, 75: 588-96.PubMedCentralPubMed Kasehagen LJ, Mueller I, McNamara DT, Bockarie MJ, Kiniboro B, Rare L, Lorry K, Kastens W, Reeder JC, Kazura JW, Zimmerman PA: Changing patterns of Plasmodium blood-stage infections in the Wosera region of Papua New Guinea monitored by light microscopy and high throughput PCR diagnosis. Am J Trop Med Hyg. 2006, 75: 588-96.PubMedCentralPubMed
8.
go back to reference McNamara DT, Kasehagen LJ, Grimberg BT, Cole-Tobian J, Collins WE, Zimmerman PA: Diagnosing infection levels of four human malaria parasite species by a polymerase chain reaction/ligase detection reaction fluorescent microsphere-based assay. Am J Trop Med Hyg. 2006, 74: 413-21.PubMedCentralPubMed McNamara DT, Kasehagen LJ, Grimberg BT, Cole-Tobian J, Collins WE, Zimmerman PA: Diagnosing infection levels of four human malaria parasite species by a polymerase chain reaction/ligase detection reaction fluorescent microsphere-based assay. Am J Trop Med Hyg. 2006, 74: 413-21.PubMedCentralPubMed
9.
go back to reference Mehlotra RK, Kasehagen LJ, Baisor M, Lorry K, Kazura JW, Bockarie MJ, Zimmerman PA: Malaria infections are randomly distributed in diverse holoendemic areas of Papua New Guinea. Am J Trop Med Hyg. 2002, 67: 555-62.PubMedCentralPubMed Mehlotra RK, Kasehagen LJ, Baisor M, Lorry K, Kazura JW, Bockarie MJ, Zimmerman PA: Malaria infections are randomly distributed in diverse holoendemic areas of Papua New Guinea. Am J Trop Med Hyg. 2002, 67: 555-62.PubMedCentralPubMed
10.
go back to reference Mehlotra RK, Lorry K, Kastens W, Miller SM, Alpers MP, Bockarie M, Kazura JW, Zimmerman PA: Random distribution of mixed species malaria infections in Papua New Guinea. Am J Trop Med Hyg. 2000, 62: 225-31.PubMed Mehlotra RK, Lorry K, Kastens W, Miller SM, Alpers MP, Bockarie M, Kazura JW, Zimmerman PA: Random distribution of mixed species malaria infections in Papua New Guinea. Am J Trop Med Hyg. 2000, 62: 225-31.PubMed
11.
go back to reference Abdel-Wahab A, Abdel-Muhsin AM, Ali E, Suleiman S, Ahmed S, Walliker D, Babiker HA: Dynamics of gametocytes among Plasmodium falciparum clones in natural infections in an area of highly seasonal transmission. J Infect Dis. 2002, 185: 1838-42. 10.1086/340638.CrossRefPubMed Abdel-Wahab A, Abdel-Muhsin AM, Ali E, Suleiman S, Ahmed S, Walliker D, Babiker HA: Dynamics of gametocytes among Plasmodium falciparum clones in natural infections in an area of highly seasonal transmission. J Infect Dis. 2002, 185: 1838-42. 10.1086/340638.CrossRefPubMed
12.
go back to reference Babiker HA, Abdel-Muhsin AM, Ranford-Cartwright LC, Satti G, Walliker D: Characteristics of Plasmodium falciparum parasites that survive the lengthy dry season in eastern Sudan where malaria transmission is markedly seasonal. Am J Trop Med Hyg. 1998, 59: 582-90.PubMed Babiker HA, Abdel-Muhsin AM, Ranford-Cartwright LC, Satti G, Walliker D: Characteristics of Plasmodium falciparum parasites that survive the lengthy dry season in eastern Sudan where malaria transmission is markedly seasonal. Am J Trop Med Hyg. 1998, 59: 582-90.PubMed
13.
go back to reference Bousema JT, Schneider P, Gouagna LC, Drakeley CJ, Tostmann A, Houben R, Githure JI, Ord R, Sutherland CJ, Omar SA, Sauerwein RW: Moderate Effect of Artemisinin-Based Combination Therapy on Transmission of Plasmodium falciparum. J Infect Dis. 2006, 193: 1151-9. 10.1086/503051.CrossRefPubMed Bousema JT, Schneider P, Gouagna LC, Drakeley CJ, Tostmann A, Houben R, Githure JI, Ord R, Sutherland CJ, Omar SA, Sauerwein RW: Moderate Effect of Artemisinin-Based Combination Therapy on Transmission of Plasmodium falciparum. J Infect Dis. 2006, 193: 1151-9. 10.1086/503051.CrossRefPubMed
14.
go back to reference Coleman RE, Kumpitak C, Ponlawat A, Maneechai N, Phunkitchar V, Rachapaew N, Zollner G, Sattabongkot J: Infectivity of asymptomatic Plasmodium-infected human populations to Anopheles dirus mosquitoes in western Thailand. J Med Entomol. 2004, 41: 201-8.CrossRefPubMed Coleman RE, Kumpitak C, Ponlawat A, Maneechai N, Phunkitchar V, Rachapaew N, Zollner G, Sattabongkot J: Infectivity of asymptomatic Plasmodium-infected human populations to Anopheles dirus mosquitoes in western Thailand. J Med Entomol. 2004, 41: 201-8.CrossRefPubMed
15.
go back to reference Nassir E, Abdel-Muhsin AM, Suliaman S, Kenyon F, Kheir A, Geha H, Ferguson HM, Walliker D, Babiker HA: Impact of genetic complexity on longevity and gametocytogenesis of Plasmodium falciparum during the dry and transmission-free season of eastern Sudan. Int J Parasitol. 2005, 35: 49-55. 10.1016/j.ijpara.2004.10.014.CrossRefPubMed Nassir E, Abdel-Muhsin AM, Suliaman S, Kenyon F, Kheir A, Geha H, Ferguson HM, Walliker D, Babiker HA: Impact of genetic complexity on longevity and gametocytogenesis of Plasmodium falciparum during the dry and transmission-free season of eastern Sudan. Int J Parasitol. 2005, 35: 49-55. 10.1016/j.ijpara.2004.10.014.CrossRefPubMed
16.
go back to reference Nwakanma D, Kheir A, Sowa M, Dunyo S, Jawara M, Pinder M, Milligan P, Walliker D, Babiker HA: High gametocyte complexity and mosquito infectivity of Plasmodium falciparum in the Gambia. Int J Parasitol. 2007 Nwakanma D, Kheir A, Sowa M, Dunyo S, Jawara M, Pinder M, Milligan P, Walliker D, Babiker HA: High gametocyte complexity and mosquito infectivity of Plasmodium falciparum in the Gambia. Int J Parasitol. 2007
17.
go back to reference Schneider P, Bousema JT, Gouagna LC, Otieno S, van deVegte-Bolmer M, Omar SA, Sauerwein RW: Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007, 76: 470-4.PubMed Schneider P, Bousema JT, Gouagna LC, Otieno S, van deVegte-Bolmer M, Omar SA, Sauerwein RW: Submicroscopic Plasmodium falciparum gametocyte densities frequently result in mosquito infection. Am J Trop Med Hyg. 2007, 76: 470-4.PubMed
18.
go back to reference Shekalaghe SA, Bousema JT, Kunei KK, Lushino P, Masokoto A, Wolters LR, Mwakalinga S, Mosha FW, Sauerwein RW, Drakeley CJ: Submicroscopic Plasmodium falciparum gametocyte carriage is common in an area of low and seasonal transmission in Tanzania. Trop Med Int Health. 2007, 12: 547-53.CrossRefPubMed Shekalaghe SA, Bousema JT, Kunei KK, Lushino P, Masokoto A, Wolters LR, Mwakalinga S, Mosha FW, Sauerwein RW, Drakeley CJ: Submicroscopic Plasmodium falciparum gametocyte carriage is common in an area of low and seasonal transmission in Tanzania. Trop Med Int Health. 2007, 12: 547-53.CrossRefPubMed
19.
go back to reference Drakeley C, Sutherland C, Bousema JT, Sauerwein RW, Targett GA: The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol. 2006, 22: 424-30. 10.1016/j.pt.2006.07.001.CrossRefPubMed Drakeley C, Sutherland C, Bousema JT, Sauerwein RW, Targett GA: The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion. Trends Parasitol. 2006, 22: 424-30. 10.1016/j.pt.2006.07.001.CrossRefPubMed
20.
go back to reference Schneider P, Schoone G, Schallig H, Verhage D, Telgt D, Eling W, Sauerwein R: Quantification of Plasmodium falciparum gametocytes in differential stages of development by quantitative nucleic acid sequence-based amplification. Mol Biochem Parasitol. 2004, 137: 35-41. 10.1016/j.molbiopara.2004.03.018.CrossRefPubMed Schneider P, Schoone G, Schallig H, Verhage D, Telgt D, Eling W, Sauerwein R: Quantification of Plasmodium falciparum gametocytes in differential stages of development by quantitative nucleic acid sequence-based amplification. Mol Biochem Parasitol. 2004, 137: 35-41. 10.1016/j.molbiopara.2004.03.018.CrossRefPubMed
21.
go back to reference Cattani JA, Tulloch JL, Vrbova H, Jolley D, Gibson FD, Moir JS, Heywood PF, Alpers MP, Stevenson A, Clancy R: The epidemiology of malaria in a population surrounding Madang, Papua New Guinea. Am J Trop Med Hyg. 1986, 35: 3-15.PubMed Cattani JA, Tulloch JL, Vrbova H, Jolley D, Gibson FD, Moir JS, Heywood PF, Alpers MP, Stevenson A, Clancy R: The epidemiology of malaria in a population surrounding Madang, Papua New Guinea. Am J Trop Med Hyg. 1986, 35: 3-15.PubMed
22.
go back to reference Graves PM, Burkot TR, Carter R, Cattani JA, Lagog M, Parker J, Brabin BJ, Gibson FD, Bradley DJ, Alpers MP: Measurement of malarial infectivity of human populations to mosquitoes in the Madang area, Papua, New Guinea. Parasitology. 1988, 96: 251-63.CrossRefPubMed Graves PM, Burkot TR, Carter R, Cattani JA, Lagog M, Parker J, Brabin BJ, Gibson FD, Bradley DJ, Alpers MP: Measurement of malarial infectivity of human populations to mosquitoes in the Madang area, Papua, New Guinea. Parasitology. 1988, 96: 251-63.CrossRefPubMed
23.
go back to reference Adedeji AA, Fehintola FA, Fateye BA, Happi TC, Amoo AO, Gbotosho GO, Sowunmi A: Plasmodium falciparum malaria in Nigerian children during high and low transmission seasons: gametocyte carriage and response to oral chloroquine. J Trop Pediatr. 2005, 51: 288-94. 10.1093/tropej/fmi016.CrossRefPubMed Adedeji AA, Fehintola FA, Fateye BA, Happi TC, Amoo AO, Gbotosho GO, Sowunmi A: Plasmodium falciparum malaria in Nigerian children during high and low transmission seasons: gametocyte carriage and response to oral chloroquine. J Trop Pediatr. 2005, 51: 288-94. 10.1093/tropej/fmi016.CrossRefPubMed
24.
go back to reference John CC, McHugh MM, Moormann AM, Sumba PO, Ofulla AV: Low prevalence of Plasmodium falciparum infection among asymptomatic individuals in a highland area of Kenya. Trans R Soc Trop Med Hyg. 2005, 99: 780-6.CrossRefPubMed John CC, McHugh MM, Moormann AM, Sumba PO, Ofulla AV: Low prevalence of Plasmodium falciparum infection among asymptomatic individuals in a highland area of Kenya. Trans R Soc Trop Med Hyg. 2005, 99: 780-6.CrossRefPubMed
25.
go back to reference Nacher M, Carrara VI, Ashley E, McGready R, Hutagalung R, Nguen JV, Thwai KL, Looareesuwan S, Nosten F: Seasonal variation in hyperparasitaemia and gametocyte carriage in patients with Plasmodium falciparum malaria on the Thai-Burmese border. Trans R Soc Trop Med Hyg. 2004, 98: 322-8. 10.1016/j.trstmh.2003.10.005.CrossRefPubMed Nacher M, Carrara VI, Ashley E, McGready R, Hutagalung R, Nguen JV, Thwai KL, Looareesuwan S, Nosten F: Seasonal variation in hyperparasitaemia and gametocyte carriage in patients with Plasmodium falciparum malaria on the Thai-Burmese border. Trans R Soc Trop Med Hyg. 2004, 98: 322-8. 10.1016/j.trstmh.2003.10.005.CrossRefPubMed
26.
go back to reference Boudin C, Olivier M, Molez JF, Chiron JP, Ambroise-Thomas P: High human malarial infectivity to laboratory-bred Anopheles gambiae in a village in Burkina Faso. Am J Trop Med Hyg. 1993, 48: 700-6.PubMed Boudin C, Olivier M, Molez JF, Chiron JP, Ambroise-Thomas P: High human malarial infectivity to laboratory-bred Anopheles gambiae in a village in Burkina Faso. Am J Trop Med Hyg. 1993, 48: 700-6.PubMed
27.
go back to reference Bell D, Wongsrichanalai C, Barnwell JW: Ensuring quality and access for malaria diagnosis: how can it be achieved?. Nat Rev Microbiol. 2006, 4: S7-20. 10.1038/nrmicro1525.CrossRefPubMed Bell D, Wongsrichanalai C, Barnwell JW: Ensuring quality and access for malaria diagnosis: how can it be achieved?. Nat Rev Microbiol. 2006, 4: S7-20. 10.1038/nrmicro1525.CrossRefPubMed
Metadata
Title
Enhanced detection of gametocytes by magnetic deposition microscopy predicts higher potential for Plasmodium falciparum transmission
Authors
Stephan Karl
Makindi David
Lee Moore
Brian T Grimberg
Pascal Michon
Ivo Mueller
Maciej Zborowski
Peter A Zimmerman
Publication date
01-12-2008
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2008
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-7-66

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