Use of qPCR and Genomic Sequencing to Diagnose Plasmodium ovale wallikeri Malaria in a Returned Soldier in the Setting of a Negative Rapid Diagnostic Assay

Robert Cohen Infectious Disease Service, Walter Reed National Military Medical Center, Bethesda, Maryland; Parasitology Section, Department of Pathology, Walter Reed National Military Medical Center, Bethesda, Maryland; Malaria Vaccine Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Headquarters, Walter Reed Army Institute of Research, Silver Spring, Maryland

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Karla Feghali Infectious Disease Service, Walter Reed National Military Medical Center, Bethesda, Maryland; Parasitology Section, Department of Pathology, Walter Reed National Military Medical Center, Bethesda, Maryland; Malaria Vaccine Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Headquarters, Walter Reed Army Institute of Research, Silver Spring, Maryland

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Saba Alemayehu Infectious Disease Service, Walter Reed National Military Medical Center, Bethesda, Maryland; Parasitology Section, Department of Pathology, Walter Reed National Military Medical Center, Bethesda, Maryland; Malaria Vaccine Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Headquarters, Walter Reed Army Institute of Research, Silver Spring, Maryland

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Jack Komisar Infectious Disease Service, Walter Reed National Military Medical Center, Bethesda, Maryland; Parasitology Section, Department of Pathology, Walter Reed National Military Medical Center, Bethesda, Maryland; Malaria Vaccine Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Headquarters, Walter Reed Army Institute of Research, Silver Spring, Maryland

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Jun Hang Infectious Disease Service, Walter Reed National Military Medical Center, Bethesda, Maryland; Parasitology Section, Department of Pathology, Walter Reed National Military Medical Center, Bethesda, Maryland; Malaria Vaccine Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Headquarters, Walter Reed Army Institute of Research, Silver Spring, Maryland

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Peter J. Weina Infectious Disease Service, Walter Reed National Military Medical Center, Bethesda, Maryland; Parasitology Section, Department of Pathology, Walter Reed National Military Medical Center, Bethesda, Maryland; Malaria Vaccine Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Headquarters, Walter Reed Army Institute of Research, Silver Spring, Maryland

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Patricia Coggeshall Infectious Disease Service, Walter Reed National Military Medical Center, Bethesda, Maryland; Parasitology Section, Department of Pathology, Walter Reed National Military Medical Center, Bethesda, Maryland; Malaria Vaccine Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Headquarters, Walter Reed Army Institute of Research, Silver Spring, Maryland

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Edwin Kamau Infectious Disease Service, Walter Reed National Military Medical Center, Bethesda, Maryland; Parasitology Section, Department of Pathology, Walter Reed National Military Medical Center, Bethesda, Maryland; Malaria Vaccine Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Headquarters, Walter Reed Army Institute of Research, Silver Spring, Maryland

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Michael Zapor Infectious Disease Service, Walter Reed National Military Medical Center, Bethesda, Maryland; Parasitology Section, Department of Pathology, Walter Reed National Military Medical Center, Bethesda, Maryland; Malaria Vaccine Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Viral Diseases Branch, Walter Reed Army Institute of Research, Silver Spring, Maryland; Headquarters, Walter Reed Army Institute of Research, Silver Spring, Maryland

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Plasmodium ovale is one of several clinically relevant malaria species known to cause disease in humans. However, in contrast to Plasmodium falciparum and Plasmodium vivax, which are responsible for most cases of human malaria, P. ovale has a wide distribution but low prevalence in tropical regions. Here, we report the case of a soldier returning from Liberia with P. ovale wallikeri malaria. This case highlights the limitations of both microscopy and the malaria rapid diagnostic test for diagnosing infection with P. ovale and for distinguishing P. ovale wallikeri from P. ovale curtisi. To our knowledge, this is the first case report in which quantitative real-time polymerase chain reaction amplification using the Cytochrome B gene, coupled with genomic sequencing of the potra locus, was used for definitive diagnosis of P. ovale wallikeri malaria.

Author Notes

* Address correspondence to Michael Zapor, 8901 Wisconsin Avenue, Bethesda, MD 20889. E-mail: Michael.J.Zapor.mil@health.mil

Authors' addresses: Robert Cohen, Walter Reed National Military Medical Center - Infectious Disease Service, Bethesda, MD, E-mail: cohen.robbie@gmail.com. Karla Feghali, Saba Alemayehu, and Jack Komisar, Walter Reed Army Institute of Research - Malaria Vaccine Branch, Silver Spring, MD, E-mails: Karla.C.Feghali.ctr@us.army.mil, Saba.Alemayehu.ctr@us.army.mil, and Jack.Komisar@us.army.mil. Jun Hang, Walter Reed Army Institute of Research - Viral Diseases Branch, Silver Spring, MD, E-mail: Jun.Hang.ctr@us.army.mil. Peter J. Weina, Walter Reed Army Institute of Research - Headquarters, Silver Spring, MD, E-mail: peter.weina@us.army.mil. Patricia Coggeshall, Walter Reed National Military Medical Center - Parasitology Section, Department of Pathology, Bethesda, MD, E-mail: Patricia.A.Coggeshall.civ@health.mil. Edwin Kamau, Walter Reed Army Institute of Research - Malaria Vaccine Development, Silver Spring, MD, E-mail: edwin.kamau@us.army.mil. Michael Zapor, Infectious Disease Service, Department of Medicine, Walter Reed National Military Medical Center, Bethesda, MD, E-mail: Michael.J.Zapor.mil@health.mil.

  • 1.

    WHO, Malaria rapid diagnostic test performance. Results of WHO product testing of malaria RDTs: round 2. Geneva: World Health Organization. Available at: http://www.who.int/malaria/publications/atoz/9789241599467/en/index.html. Accessed November 10, 2012.

    • Search Google Scholar
    • Export Citation
  • 2.

    Kawamoto F, Liu Q, Ferreira MU, Tantular IS, 1999. How prevalent are Plasmodium ovale and P. malariae in East Asia? Parasitol Today 15: 422–426.

    • Search Google Scholar
    • Export Citation
  • 3.

    Mueller I, Zimmerman PA, Reeder JC, 2007. Plasmodium malariae and Plasmodium ovale-the ā€˜bashful’ malaria parasites. Trends Parasitol 23: 278–283.

    • Search Google Scholar
    • Export Citation
  • 4.

    Faye FB, Spiegel A, Tall A, Sokhna C, Fontenille D, Rogier C, Trape JF, 2002. Diagnostic criteria and risk factors for Plasmodium ovale malaria. J Infect Dis 186: 690–695.

    • Search Google Scholar
    • Export Citation
  • 5.

    Sutherland CJ, Tanomsing N, Nolder D, Oguike M, Jennison C, Pukrittayakamee S, Dolecek C, Hien TT, do RosĆ”rio VE, Arez AP, Pinto J, Michon P, Escalante AA, Nosten F, Burke M, Lee R, Blaze M, Otto TD, Barnwell JW, Pain A, Williams J, White NJ, Day NP, Snounou G, Lockhart PJ, Chiodini PL, Imwong M, Polley SD, 2010. Two nonrecombining sympatric forms of the human malaria parasite Plasmodium ovale occur globally. J Infect Dis 201: 1544–1550.

    • Search Google Scholar
    • Export Citation
  • 6.

    Oguike MC, Betson M, Burke M, Nolder D, Stothard JR, Kleinschmidt I, Proietti C, Bousema T, Ndounga M, Tanabe K, Ntege E, Culleton R, Sutherland CJ, 2011. Plasmodium ovale curtisi and Plasmodium ovale wallikeri circulate simultaneously in African communities. Int J Parasitol 41: 677–683.

    • Search Google Scholar
    • Export Citation
  • 7.

    Kamau E, Tolbert LS, Kortpeter L, Pratt M, Nyakoe N, Muringo L, Ogutu B, Waitumbi JN, Ockenhouse CF, 2011. Development of a highly sensitive genus-specific quantitative reverse transcriptase real-time PCR assay for detection and quantitation of Plasmodium by amplifying RNA and DNA of the 18S rRNA genes. J Clin Microbiol 49: 2946–2953.

    • Search Google Scholar
    • Export Citation
  • 8.

    CDC DPDX (Centers for Disease Control and Prevention, Division of Parasitic Diseases), 2012. Comparison of Plasmodium species which cause malaria in humans. Available at: http://www.dpd.cdc.gov/DPDx/HTML/malaria.htm. Accessed October 10, 2012.

    • Search Google Scholar
    • Export Citation
  • 9.

    Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ, 1990. Basic local alignment search tool. J Mol Biol 215: 403–410.

  • 10.

    Drummond AJ, Ashton B, Buxton S, Cheung M, 2011. Geneious v5.6. Available at: http://www.geneious.com. Accessed October 9, 2012.

  • 11.

    Centers for Disease Control and Prevention, 2012. Malaria Information by Country. Available at: http://www.cdc.gov/malaria/travelers/country_table/a.html. Accessed November 10, 2012.

    • Search Google Scholar
    • Export Citation
  • 12.

    Ohrt C, Obare P, Nanakorn A, Adhiambo C, Awuondo K, O'Meara WP, Remich S, Martin K, Cook E, Chretien J-P, Lucas C, Osoga J, McEvoy P, Owaga ML, Odera JS, Ogutu B, 2007. Establishing a malaria diagnostics centre of excellence in Kisumu, Kenya. Malar J 6: 79.

    • Search Google Scholar
    • Export Citation
  • 13.

    Perandin F, Manca N, Calderaro A, Piccolo G, Galati L, Ricci L, Medici MC, Arcangeletti MC, Snounou G, Dettori G, Chezzi C, 2004. Development of a real-time PCR assay for detection of Plasmodium falciparum, Plasmodium vivax, and Plasmodium ovale for routine clinical diagnosis. J Clin Microbiol 42: 1214–1219.

    • Search Google Scholar
    • Export Citation
  • 14.

    Veron V, Simon S, Carme B, 2009. Multiplex real-time PCR detection of P. falciparum, P. vivax and P. malariae in human blood samples. Exp Parasitol 121: 346–351.

    • Search Google Scholar
    • Export Citation
  • 15.

    Shute GT, 1988. The microscopic diagnosis of malaria. Wernsdorfer WH, McGregor I, eds. Malaria: Principles and Practice of Malariology. New York: Churchill Livingstone, 781–814.

    • Search Google Scholar
    • Export Citation
  • 16.

    Ash LR, Orihel TC, 2007. Ash & Orihel's Atlas of Human Parasitology. Fifth edition. Chicago, IL: American Society for Clinical Pathology Press.

    • Search Google Scholar
    • Export Citation
  • 17.

    WHO, 2009. Bench Aids for Malaria Microscopy. Geneva: World Health Organization.

  • 18.

    Garnham PC, 1988. Malaria parasites of man: life-cycles and morphology (excluding ultrastructure). Wernsdorfer WH, McGregor I, eds. Malaria: Principles and Practice of Malariology. New York: Churchill Livingstone, 61–96.

    • Search Google Scholar
    • Export Citation
  • 19.

    Swierczynski G, Gobbo M, 2007. Atlas of Human Malaria. Sirmione, Italy: Az Color SRL.

  • 20.

    CDC, WHO, 2010. CD-ROM entitled ā€œThe Microscopic Diagnosis of Malaria.ā€ Furnished along with the book Basic Malaria Microscopy. Part I. Learner's Guide. Second edition. Geneva: World Health Organization.

    • Search Google Scholar
    • Export Citation
  • 21.

    Heutmekers M, Gillet P, Maltha J, Scheirlinck A, Cnops L, Bottieau E, Van Esbroeck M, Jacobs J, 2012. Evaluation of the rapid diagnostic test CareStart pLDH Malaria (Pf-pLDH/pan-pLDH) for the diagnosis of malaria in a reference setting. Malar J 11: 204.

    • Search Google Scholar
    • Export Citation
  • 22.

    HouzƩe S, Hubert V, Cohen DP, Rivetz B, Le Bras J, 2011. Evaluation of the Clearview Malaria pLDH Malaria Rapid Diagnostic Test in a non-endemic setting. Malar J 10: 284.

    • Search Google Scholar
    • Export Citation
  • 23.

    van Dijk DP, Gillet P, Vlieghe E, Cnops L, Van Esbroeck M, Jacobs J, 2010. Evaluation of the Immunoquick+4 malaria rapid diagnostic test in a non-endemic setting. Eur J Clin Microbiol Infect Dis 29: 577–583.

    • Search Google Scholar
    • Export Citation
  • 24.

    Global Malaria Programme WHO, 2012. Information note on recommended selection criteria for procurement of malaria rapid diagnostic tests (RDTs). Available at: http://www.finddiagnostics.org/programs/malaria/find_activities/product_testing/malaria-rdtproduct-testing. Accessed July 30, 2012.

    • Search Google Scholar
    • Export Citation
  • 25.

    Farcas GA, Zhong KJY, Lovegrove FE, Graham CM, Kain KC, 2003. Evaluation of the Binax NOW ICT test versus polymerase chain reaction and microscopy for the detection of malaria in returned travelers. Am J Trop Med Hyg 69: 589–592.

    • Search Google Scholar
    • Export Citation
  • 26.

    Bigaillon C, Fontan E, Cavallo J-D, Hernandez E, Spiegel A, 2005. Ineffectiveness of the Binax NOW malaria test for diagnosis of Plasmodium ovale malaria. J Clin Microbiol 43: 1011.

    • Search Google Scholar
    • Export Citation
  • 27.

    Mens PF, Moers AP, de Bes LM, Flint J, Sak JR, Keereecharoen L, van Overmeir C, Verweij JJ, Hallett RL, Wihokhoen B, Proux S, Schallig HD, van Amerongen A, 2012. Development, validation and evaluation of a rapid PCR-nucleic acid lateral flow immuno-assay for the detection of Plasmodium and the differentiation between Plasmodium falciparum and Plasmodium vivax. Malar J 11: 279.

    • Search Google Scholar
    • Export Citation
  • 28.

    Rodriguez-Morales AJ, SĆ”nchez E, Vargas M, Piccolo C, Colina R, Arria M, Franco-Paredes C, 2005. Occurrence of thrombocytopenia in Plasmodium vivax malaria. Clin Infect Dis 41: 130–131.

    • Search Google Scholar
    • Export Citation
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