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Research Article

Identification of a New Cyclovirus in Cerebrospinal Fluid of Patients with Acute Central Nervous System Infections

Le Van Tan, H. Rogier van Doorn, Ho Dang Trung Nghia, Tran Thi Hong Chau, Le Thi Phuong Tu, Michel de Vries, Marta Canuti, Martin Deijs, Maarten F. Jebbink, Stephen Baker, Juliet E. Bryant, Nguyen Thi Tham, Nguyen Thi Thuy Chinh BKrong, Maciej F. Boni, Tran Quoc Loi, Le Thi Phuong, Joost T. P. Verhoeven, Martin Crusat, Rienk E. Jeeninga, Constance Schultsz, Nguyen Van Vinh Chau, Tran Tinh Hien, Lia van der Hoek, Jeremy Farrar, Menno D. de Jong
Amit Kapoor, Invited Editor, W. Ian Lipkin, Editor
Le Van Tan
Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme, South East Asia Infectious Diseases Clinical Research Network, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnama
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H. Rogier van Doorn
Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme, South East Asia Infectious Diseases Clinical Research Network, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnama
Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Centre for Clinical Vaccinology and Tropical Medicine, Oxford, United Kingdomb
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Ho Dang Trung Nghia
Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme, South East Asia Infectious Diseases Clinical Research Network, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnama
Pham Ngoc Thach University of Medicine, Ho Chi Minh City, Vietnamc
Hospital for Tropical Diseases, Ho Chi Minh City, Vietnamd
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Tran Thi Hong Chau
Hospital for Tropical Diseases, Ho Chi Minh City, Vietnamd
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Le Thi Phuong Tu
Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme, South East Asia Infectious Diseases Clinical Research Network, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnama
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Michel de Vries
Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlandse
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Marta Canuti
Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlandse
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Martin Deijs
Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlandse
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Maarten F. Jebbink
Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlandse
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Stephen Baker
Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme, South East Asia Infectious Diseases Clinical Research Network, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnama
Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Centre for Clinical Vaccinology and Tropical Medicine, Oxford, United Kingdomb
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Juliet E. Bryant
Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme, South East Asia Infectious Diseases Clinical Research Network, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnama
Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Centre for Clinical Vaccinology and Tropical Medicine, Oxford, United Kingdomb
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Nguyen Thi Tham
Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme, South East Asia Infectious Diseases Clinical Research Network, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnama
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Nguyen Thi Thuy Chinh BKrong
Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme, South East Asia Infectious Diseases Clinical Research Network, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnama
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Maciej F. Boni
Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme, South East Asia Infectious Diseases Clinical Research Network, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnama
Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Centre for Clinical Vaccinology and Tropical Medicine, Oxford, United Kingdomb
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Tran Quoc Loi
Dong Thap Provincial Hospital, Dong Thap, Vietnamf
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Le Thi Phuong
Dong Thap Provincial Hospital, Dong Thap, Vietnamf
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Joost T. P. Verhoeven
Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlandse
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Martin Crusat
Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlandse
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Rienk E. Jeeninga
Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlandse
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Constance Schultsz
Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme, South East Asia Infectious Diseases Clinical Research Network, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnama
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Nguyen Van Vinh Chau
Hospital for Tropical Diseases, Ho Chi Minh City, Vietnamd
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Tran Tinh Hien
Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme, South East Asia Infectious Diseases Clinical Research Network, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnama
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Lia van der Hoek
Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlandse
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Jeremy Farrar
Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme, South East Asia Infectious Diseases Clinical Research Network, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnama
Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, University of Oxford, Centre for Clinical Vaccinology and Tropical Medicine, Oxford, United Kingdomb
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Menno D. de Jong
Oxford University Clinical Research Unit, Wellcome Trust Major Overseas Programme, South East Asia Infectious Diseases Clinical Research Network, Hospital for Tropical Diseases, Ho Chi Minh City, Vietnama
Department of Medical Microbiology, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlandse
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Amit Kapoor
Columbia University
Roles: Invited Editor
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W. Ian Lipkin
Columbia University
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DOI: 10.1128/mBio.00231-13
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  • FIG 1
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    FIG 1

    Gel electrophoresis of PCR products. (A) Cyclovirus-like sequence PCR; (B) inverse PCR of cyclovirus. Lanes 1 and 8, 100-bp and 1-kb ladders, respectively; lanes 2 to 6, 9, and 10, patient samples; lanes 7 and 11, negative controls. Arrows indicate products of expected sizes. The thin black line indicates the spliced margin where the two unrelated lanes between lanes 10 and 11 were removed from the original gel picture.

  • FIG 2
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    FIG 2

    (A)Predicted genome organization of CyCV-VN; (B) stem-loop structure of CyCV-VN, with nonamer sequence in red.

  • FIG 3
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    FIG 3

    Reconstructed phylogeny trees of cycloviruses. (A) Tree based on complete genome sequences of 7 strains of CyCV-VN (red), 16 cycloviruses, 12 circoviruses, and a gyrovirus as an outlier. (B) Tree based on partial amino acid sequences of Rep proteins of 28 reported CyCV species and 27 CyCV-VN strains, indicated by the compressed branch. Trees were built by means of neighbor joining (MEGA 4.1); bootstrap tests of the reconstructed trees were done with 1,000 replicates. Sequence accession numbers are in brackets. CV, circovirus.

Tables

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  • TABLE 1 

    Oligonucleotide sequences of primers and a probe used in this study

    PrimersOligonucleotide sequence (5′–3′) Source
    CyCV31_53FGAGCGCACATTGAAAGAGCTAAANewly designed
    CyCV178-153RTCTCCTCCTTCAATGACAGAAACAACNewly designed
    CyCV65-96Probe*FAM-CGADAATAAGGMATACTGCTCTAAAGSTGGCG-BHQ1Newly designed
    CVF1GGIAYICCICAYYTICARGG3
    CVR1AWCCAICCRTARAARTCRTC3
    CVF2GGIAYICCI CAYYTICARGGITT3
    CVR2TGYTGYTCRTAICCRTCCCACCA3
    CyCV31_53F-rcTTTAGCTCTTTCAATGTGCGCTCNewly designed
    CyCV178-153R-rcGTTGTTTCTGTCATTGAAGGAGGAGANewly designed
    CyCV_FL1ACTTATTTCTAATTCATATTGCCGGGTANewly designed
    CyCV_FL2TCAGCGTCCAGCAGAATCTACNewly designed
    CyCV_FL3AAGCTCATCGTATTTGATCCATCCNewly designed
    CyCV_FL4CCTCACTGAGCTATGTAAATTTGCTNewly designed
  • TABLE 2

    Characteristics and clinical outcome of patients with CNS infections and positive for CyCV-VN by PCR

    Group
    and
    patient
    (n)a
    Other
    confirmed
    diagnosisb
    Sample
    date
    No. (%) of males
    in group or sex
    of patientc,d
    Age
    (yr)d
    Length of
    hospital
    stay
    (days)d
    Illness
    day  
    No. of patients withd:CSF white
    blood cell
    count
    % of
    lympho-
    cytes
    in CSF
    CSF/blood
    glucose
    ratio
    Out-
    comef
    Sequelae
    at
    discharge
    FeverConvul-
    sions
    Neck
    stiff-
    ness
    Limb
    weak-
    ness
    Head-
    ache
    Vom-
    iting
    GCS
    scoree
    Group 1
    (12)
    9
    (75)
    19.5
    (<1–50)
    8
    (2–41)
    5
    (2–20)
    11
    (92)
    4
    (33)
    7
    (58)
    2
    (18)
    6
    (86)
    8
    (89)
    40
    (1–464)
     1NoneJan. 5, 2004F<175YNNYNANA2 (BCS)10.881None
     2NoneJun. 8, 2004M<187YNNNNANA3 (BCS)30.531None
     3NoneFeb. 7, 2004M1283YNNNNANA626900.961None
     4NoneOct. 18, 1999M2757YNYNANAY1554680.551None
     5NoneJun. 12, 2008M3122YYNNYY15100.543Unknown
     6NoneNov. 25, 2009F<292YYNNNAY5 (BCS)10600.561Unknown
     7NoneNov. 29, 2008M204120YYYYYY7160300.731Unknown
     8NoneSep. 4, 2009M15159YNYNYY1578200.621Unknown
     9NoneSep. 7, 2009F50157YNYNYY15105220.441Unknown
     10NoneNov. 18, 2009M1955YYYNYN1114360.551Unknown
     11NoneMar. 31, 2008M4335NNYNYY978200.573Unknown
     12NoneApr. 16, 2008M24174YNYNNY15464200.511Unknown
    Group 2
    (4)
    3
    (75)
    14
    (2–19)
    14
    (4–38)
    5.5
    (2–7)
    2
    (50)
    3
    (100)
    2
    (50)
    1
    (25)
    2
    (100)
    2
    (100)
    50 (0–110)
     1JEVJan. 30 2004M242NNNNNANA1300.981None
     2JEVAug. 12 2004M1155YNYNNANA1122650.811None
     3DENVOct. 24 2008M19387NNAYYYY979210.411Unknown
     4JEVMay 05 2008F17236YNNNYY15110250.711Unknown
    Group 3
    (7)
    6
    (85)
    5
    (<1–61)
    19
    (1–34)
    2
    (1–3)
    6
    (85)
    2
    (28)
    5
    (71)
    1
    (14)
    4
    (100)
    4
    (57)
    1,439
    (2–9,160)
     1S. suisAug. 31, 2008M29211NNYNYY153,5000.041Unknown
     2S. pneumoniaeNov. 17, 2008M25162YNYNYY155,513200.231Unknown
     3H. influenzaeJan. 20, 2009M<1191YNYNNAN5 (BCS)9,16090.361Unknown
     4S. pneumoniaeJan. 27, 2009M511YYNYYY830110.182
     5S. suisMar. 16, 2009F61343YNYNNAN111,439280.191Unknown
     6S. pneumoniaeApr. 17, 2009M242YYNNNAN0 (BCS)20.651Unknown
     7S. pneumoniaeDec. 23, 2009M3202YNYNyY1180330.951Unknown
    Group 4
    (5)
    1
    (20)
    32
    (29–68)
    4
    (2–10)
    5
    (3–7)
    4
    (80)
    04
    (80)
    0NANA296
    (100–950)
     1187M. tuberculosisAug. 4, 2009F3047YNYNNANA13296NA0.183Unknown
     1847NoneFeb. 16, 2009M32103YNYNNANA15100200.131Unknown
     1854NoneJul. 24, 2009F2923YNNNNANA15603200.341Unknown
     2117M. tuberculosisFeb. 9, 2010F55NA7NUnknownYNNANA795060NA3Unknown
     2460NoneNov. 13, 2008F68NA5YNYNNANA15296NA0.723Unknown
    • ↵a Group 1, patients with CNS infections of unknown etiology; group 2, patients with laboratory-confirmed CNS infections; group 3, bacterial meningitis patients; group 4, PCR confirmed/clinically suspected tuberculosis meningitis patients. Names of provinces from which the patients were originated are intentionally not shown; patients 5 and 6 were the index cases in whose samples the CyCV-like sequence was detected by VIDISCA-454.

    • ↵b For M. tuberculosis, denominators may vary. JEV, Japanese encephalitis virus; DENV, dengue virus.

    • ↵c M, male; F, female.

    • ↵d Data are numbers (percentages) of patients; continuous variables are presented as medians (ranges). NA, not available; Y, yes; N, no.

    • ↵e Scores are on the Glasgow coma scale (GCS) unless the Blantyre coma scale (BCS) is indicated.

    • ↵f 1, recovery; 2, death; 3, unknown.

  • TABLE 3

    Nonamer sequences of CyCV-VN and 15 different CyCV species and lengths of the stems

    CyCV speciesNonamer sequenceaLoop length
    VNTAATACTAT11
    PK 5006TAATACTAT13
    PK 5034TAATACTAT13
    PK 5222TAATACTAT13
    PK 5510TAATACTAT12
    Chimp 11TAATACTAT13
    NG12TAATACTAT13
    NG 14TAATACTAT11
    TN 18TAATACTAT12
    NG chicken 8TAATACTAA12
    PK goat 11TAATACTAT12
    PK goat 21TAATACTAG13
    TB bat USATAATACTAT12
    Bat GF-4cTAATACTAT11
    NG 13TAGTATTAC9
    DfCyCV-A1TAATACTAT13
    FWCasCyV-GS140TAGTATTAC11
    • ↵a Underlined nucleotides are those that differ from the consensus sequence.

  • TABLE 4

    Degree of sequence identities between CyCV-VN and other cyclovirusesa

    CyCV species% identity of:Host
    Complete genome (nt level)Cap protein (aa level)Rep protein (aa level)
    USAbat-TB/2009462251Bats
    BatGF-4c452250Bats
    Chimp12432446Chimpanzees
    NG12442651Humans
    NG13401443Humans
    NG14442250Humans
    NGchicken15/2009452349Chickens
    PK5006462248Humans
    PK5034442351Humans
    PK5222443049Humans
    PK5510462851Humans
    PKgoat11/2009442549Sheep
    PKgoat21/2009675070Sheep
    TN18704874Humans
    DfCyCV-A1503047Dragonflies
    FWCasCyV-GS140452333Cockroaches
    NG23NANA50Humans
    Chimp13NANA51Chimpanzees
    PK5192NANA40Humans
    PKgoat24NANA30Sheep
    Pkbeef25NANA76Bovines
    TN12NANA46Humans
    TN9NANA46Humans
    TN26NANA49Humans
    NG6NANA46Humans
    NG15NANA46Humans
    Chimp73NANA45Chimpanzees
    TN6NANA46Humans
    Chimp53NANA48Chimpanzees
    • ↵a NA, not available. Sequence accession numbers are shown in Fig. 3.

  • TABLE 5

    Samples for PCR screening of CyCV-VN

    Samplea Disease/syndromeNo.Collection periodHospitalbHospital location
    CSFcCNS6421999-2009—aSouthern and central Vietnam
    CSFdNoninfectious condition1221997-2011Hospital for Tropical Diseases and Cho Ray HospitalHo Chi Minh City, southern Vietnam
    BloodeUnknown902009-2010Hue Central Hospital Hue City, central Vietnam
    Human fecesHealthy children1882011NASouthern Vietnam
    Animal fecesfNA652011NADong Thap Province, southern Vietnam
    • ↵a  Prior to PCR screening, nucleic acid was isolated from clinical samples with use of the easyMAG (bioMérieux, Marcy l’Étoile, France) or the MagNA pure96 system (Roche), following the manufacturer’s instructions.

    • ↵b  The hospitals from which the noninfectious CSF and blood samples were collected are referral hospitals for southern and central provinces in Vietnam. NA, not applicable.

    • ↵c  From children and adult patients enrolled in the BMD, PVE, or 01SS study (see Materials and Methods for study details).

    • ↵d  Indications for lumbar puncture included headache/migraine (n = 17), trauma (n = 16), postoperative CSF leakage (n = 2), tumors (n = 13), benign intracranial hypertension (n = 1), epilepsy/convulsion (n = 15), encephalopathy (n = 5), external ventricular draining (n = 4), hemorrhage/stroke (n = 29), Guillain-Barré syndrome (n = 3), cranial nerve palsies (n = 6), and others (n = 11). The patients included both children and adults [age median (range): 36 (1 to 91) years; 67% male], and they were from 26 provinces in central or southern Vietnam.

    • ↵e  Anonymized residual blood samples from an influenza sero-surveillance study.

    • ↵f  Including samples collected from individual animals and boot swabs—from pigs (n = 20), chickens (n = 12), and ducks (n = 33).

Supplemental Material

  • Figures
  • Tables
  • Additional Files
  • Figure S1

    Nucleotide sequence alignment showing sequence identity between primers/probe of CyCV-VN PCR used and CyCV-VN and CyCV-20 (including CyCV-TN8, -TN15, -TN16, -TN18, -TN22, and -TN25) sequences. Degenerate nucleotides: D = A, G, or T; M = A or C; S = G or C. Download Figure S1, TIF file, 1.2 MB.

    Copyright © 2013 Tan et al.

    This is an open-access article distributed under the terms of the Creative Commons Attribution 3.0 Unported license.

Additional Files

  • Figures
  • Tables
  • Supplemental Material
  • Supplementary Data

    Files in this Data Supplement:

    • Figure sf01, TIF - Figure sf01, TIF
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Identification of a New Cyclovirus in Cerebrospinal Fluid of Patients with Acute Central Nervous System Infections
Le Van Tan, H. Rogier van Doorn, Ho Dang Trung Nghia, Tran Thi Hong Chau, Le Thi Phuong Tu, Michel de Vries, Marta Canuti, Martin Deijs, Maarten F. Jebbink, Stephen Baker, Juliet E. Bryant, Nguyen Thi Tham, Nguyen Thi Thuy Chinh BKrong, Maciej F. Boni, Tran Quoc Loi, Le Thi Phuong, Joost T. P. Verhoeven, Martin Crusat, Rienk E. Jeeninga, Constance Schultsz, Nguyen Van Vinh Chau, Tran Tinh Hien, Lia van der Hoek, Jeremy Farrar, Menno D. de Jong
mBio Jun 2013, 4 (3) e00231-13; DOI: 10.1128/mBio.00231-13

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Identification of a New Cyclovirus in Cerebrospinal Fluid of Patients with Acute Central Nervous System Infections
Le Van Tan, H. Rogier van Doorn, Ho Dang Trung Nghia, Tran Thi Hong Chau, Le Thi Phuong Tu, Michel de Vries, Marta Canuti, Martin Deijs, Maarten F. Jebbink, Stephen Baker, Juliet E. Bryant, Nguyen Thi Tham, Nguyen Thi Thuy Chinh BKrong, Maciej F. Boni, Tran Quoc Loi, Le Thi Phuong, Joost T. P. Verhoeven, Martin Crusat, Rienk E. Jeeninga, Constance Schultsz, Nguyen Van Vinh Chau, Tran Tinh Hien, Lia van der Hoek, Jeremy Farrar, Menno D. de Jong
mBio Jun 2013, 4 (3) e00231-13; DOI: 10.1128/mBio.00231-13
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    • ABSTRACT
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