Development of a TaqMan array card for acute-febrile-illness outbreak investigation and surveillance of emerging pathogens, including ebola virus

Journal of Clinical Microbiology

Volumn 54, Issue 1, 2016, Pages 49-58

  Liu, Jie ^a   Ochieng, Caroline ^b   Wiersma, Steve ^c   Ströher, Ute ^d   Towner, Jonathan S ^d   Whitmer, Shannon ^d   Nichol, Stuart T ^d   Moore, Christopher C ^a   Kersh, Gilbert J ^d   Kato, Cecilia ^d   Sexton, Christopher ^d   Petersen, Jeannine ^d   Massung, Robert ^d   Hercik, Christine ^e   Crump, John A ^f,g   Kibiki, Gibson ^h   Maro, Athanasia ^h   Mujaga, Buliga ^h   Gratz, Jean ^h   Jacob, Shevin T ⁱ   Banura, Patrick ^j   Scheld, W Michael ^a   Juma, Bonventure ^c   Onyango, Clayton O ^c   Montgomery, Joel M ^c   Houpt, Eric ^a   Fields, Barry ^c   more..

^a UNIVERSITY OF VIRGINIA   (United States)

^b KENYA MEDICAL RESEARCH INSTITUTE   (Kenya)

^c CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^d NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

^e GEORGETOWN UNIVERSITY   (United States)

^f DUKE UNIVERSITY   (United States)

^g UNIVERSITY OF OTAGO   (New Zealand)

^h KILIMANJARO CLINICAL RESEARCH INSTITUTE   (Tanzania)

ⁱ UNIVERSITY OF WASHINGTON   (United States)

^j Masaka Regional Referral Hospital   (Uganda)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ASSAY; BARTONELLA; BRUCELLA; BUNDIBUGYO VIRUS; CHIKUNGUNYA VIRUS; CONTROLLED STUDY; COXIELLA BURNETII; CRIMEAN-CONGO HEMORRHAGIC FEVER VIRUS; DENGUE VIRUS; EBOLAVIRUS; ENTEROBACTERIA PHAGE MS2; FALSE NEGATIVE RESULT; FALSE POSITIVE RESULT; HANTAAN VIRUS; HEPATITIS E VIRUS; HERPES SIMPLEX VIRUS 1; HUMAN; LEISHMANIA; LEPTOSPIRA; MARBURGVIRUS; NIPAH VIRUS; NONHUMAN; O NYONG NYONG VIRUS; PHOCINE HERPESVIRUS 1; PLASMODIUM; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RICKETTSIA; RIFT VALLEY FEVER VIRUS; SALMONELLA ENTERICA; SALMONELLA ENTERICA SEROVAR TYPHI; SENSITIVITY AND SPECIFICITY; SUDAN VIRUS; TAQMAN ARRAY CARD; TRYPANOSOMA BRUCEI; VALIDATION PROCESS; VIRUS; WEST NILE VIRUS; YELLOW FEVER VIRUS; YERSINIA PESTIS; ADULT; COMMUNICABLE DISEASES; EPIDEMIC; EPIDEMIOLOGICAL MONITORING; EVALUATION STUDY; FEVER OF UNKNOWN ORIGIN; MOLECULAR DIAGNOSIS; PROCEDURES; STANDARD; STANDARDS; TIME FACTOR;

ADULT; COMMUNICABLE DISEASES; DISEASE OUTBREAKS; EPIDEMIOLOGICAL MONITORING; FEVER OF UNKNOWN ORIGIN; HUMANS; MOLECULAR DIAGNOSTIC TECHNIQUES; REAL-TIME POLYMERASE CHAIN REACTION; REFERENCE STANDARDS; SENSITIVITY AND SPECIFICITY; TIME FACTORS;

EID: 84954312429     PISSN: 00951137     EISSN: 1098660X     Source Type: Journal    
DOI: 10.1128/JCM.02257-15     Document Type: Article

References (52)

1. Hammitt LL, Kazungu S, Morpeth SC, Gibson DG, Mvera B, Brent AJ, Mwarumba S, Onyango CO, Bett A, Akech DO, Murdoch DR, Nokes DJ, Scott JA. 2012. A preliminary study of pneumonia etiology among hospitalized children in Kenya. Clin Infect Dis 54(Suppl):S190-S199. http://dx.doi.org/10.1093/cid/cir1071.
2. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Pan-chalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acacio S, Biswas K, O'Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM. 2013. Burden and aetiologyofdiarrhoeal diseaseininfants and young childrenin developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 382:209-222. http://dx.doi.org/10.1016/S0140-6736(13)60844-2.
3. Prasad N, Sharples KJ, Murdoch DR, Crump JA. 2015. Community prevalence of fever and relationship with malaria among infants and children in low-resource areas. Am J Trop Med Hyg 93:178-180. http://dx.doi.org/10.4269/ajtmh.14-0646.
4. World Health Organization. 2010. Guidelines for the treatment of malaria, 2nd ed. World Health Organization, Geneva, Switzerland.
5. Kariuki S. 2008. Typhoid fever in sub-Saharan Africa: challenges of diagnosis and management of infections. J Infect Dev Ctries 2:443-447.
6. Ochieng C, Lutomiah J, Makio A, Koka H, Chepkorir E, Yalwala S, Mutisya J, Musila L, Khamadi S, Richardson J, Bast J, Schnabel D, Wurapa E, Sang R. 2013. Mosquito-borne arbovirus surveillance at selected sitesin diverse ecological zones ofKenya; 2007-2012. Virol J 10:140. http://dx.doi.org/10.1186/1743-422X-10-140.
7. Brent AJ, Ahmed I, Ndiritu M, Lewa P, Ngetsa C, Lowe B, Bauni E, English M, Berkley JA, Scott JA. 2006. Incidence of clinically significant bacteraemia in children who present to hospital in Kenya: community-based observational study. Lancet 367:482-488. http://dx.doi.org/10.1016/S0140-6736(06)68180-4.
8. D'Acremont V, Kilowoko M, Kyungu E, Philipina S, Sangu W, Ka-hama-Maro J, Lengeler C, Cherpillod P, Kaiser L, Genton B. 2014. Beyond malaria-causes of fever in outpatient Tanzanian children. N Engl J Med 370:809-817. http://dx.doi.org/10.1056/NEJMoa1214482.
9. Baize S, Pannetier D, Oestereich L, Rieger T, Koivogui L, Magassouba N, Soropogui B, Sow MS, Keita S, De Clerck H, Tiffany A, Dominguez G, Loua M, Traore A, Kolie M, Malano ER, Heleze E, Bocquin A, Mely S, Raoul H, Caro V, Cadar D, Gabriel M, Pahlmann M, Tappe D, Schmidt-Chanasit J, Impouma B, Diallo AK, Formenty P, Van Herp M, Gunther S. 2014. Emergence of Zaire Ebola virus disease in Guinea. N Engl J Med 371:1418-1425. http://dx.doi.org/10.1056/NEJMoa1404505.
10. Crump JA, Morrissey AB, Nicholson WL, Massung RF, Stoddard RA, Galloway RL, Ooi EE, Maro VP, Saganda W, Kinabo GD, Muiruri C, Bartlett JA. 2013. Etiology of severe non-malaria febrile illness in Northern Tanzania: a prospective cohort study. PLoS Negl Trop Dis 7:e2324. http://dx.doi.org/10.1371/journal.pntd.0002324.
11. Prasad N, Murdoch DR, Reyburn H, Crump JA. 2015. Etiology of severe febrile illness in low-and middle-income countries: a systematic review. PLoS One 10:e0127962. http://dx.doi.org/10.1371/journal.pone.0127962.
12. Towner JS, Pourrut X, Albarino CG, Nkogue CN, Bird BH, Grard G, Ksiazek TG, Gonzalez JP, Nichol ST, Leroy EM. 2007. Marburg virus infection detected in a common African bat. PLoS One 2:e764. http://dx.doi.org/10.1371/journal.pone.0000764.
13. Towner JS, Sealy TK, Khristova ML, Albarino CG, Conlan S, Reeder SA, Quan PL, Lipkin WI, Downing R, Tappero JW, Okware S, Lutwama J, Bakamutumaho B, Kayiwa J, Comer JA, Rollin PE, Ksiazek TG, Nichol ST. 2008. Newly discovered Ebola virus associated with hemor-rhagic fever outbreak in Uganda. PLoS Pathog 4:e1000212. http://dx.doi.org/10.1371/journal.ppat.1000212.
14. Diaz MH, Waller JL, Napoliello RA, Islam MS, Wolff BJ, Burken DJ, Holden RL, Srinivasan V, Arvay M, McGee L, Oberste MS, Whitney CG, Schrag SJ, Winchell JM, Saha SK. 2013. Optimization of multiple pathogen detection using the TaqMan array card: application for a population-based study of neonatal infection. PLoS One 8:e66183. http://dx.doi.org/10.1371/journal.pone.0066183.
15. Kodani M, Yang G, Conklin LM, Travis TC, Whitney CG, Anderson LJ, Schrag SJ, Taylor TH, Jr, Beall BW, Breiman RF, Feikin DR, Njenga MK, Mayer LW, Oberste MS, Tondella ML, Winchell JM, Lindstrom SL, Erdman DD, Fields BS. 2011. Application of TaqMan low-density arrays for simultaneous detectionofmultiple respiratory pathogens.J Clin Microbiol 49:2175-2182. http://dx.doi.org/10.1128/JCM.02270-10.
16. Liu J, Gratz J, Amour C, Kibiki G, Becker S, Janaki L, Verweij JJ, Taniuchi M, Sobuz SU, Haque R, Haverstick DM, Houpt ER. 2013. A laboratory-developed TaqMan array card for simultaneous detection of 19 enteropathogens. J Clin Microbiol 51:472-480. http://dx.doi.org/10.1128/JCM.02658-12.
17. Liu J, Kabir F, Manneh J, Lertsethtakarn P, Begum S, Gratz J, Becker SM, Operario DJ, Taniuchi M, Janaki L, Platts-Mills JA, Haverstick DM, Kabir M, Sobuz SU, Nakjarung K, Sakpaisal P, Silapong S, Bod-hidatta L, Qureshi S, Kalam A, Saidi Q, Swai N, Mujaga B, Maro A, Kwambana B, Dione M, Antonio M, Kibiki G, Mason CJ, Haque R, Iqbal N, Zaidi AK, Houpt ER. 2014. Development and assessment of molecular diagnostic tests for 15 enteropathogens causing childhood diarrhoea: a multicentre study. Lancet Infect Dis 14:716-724. http://dx.doi.org/10.1016/S1473-3099(14)70808-4.
18. Summers A, Nyenswah TG, Montgomery JM, Neatherlin J, Tappero, Centers for Disease Control and Prevention. 2014. Challenges in responding to the Ebola epidemic-four rural counties, Liberia, August-November 2014. MMWR Morb Mortal Wkly Rep 63:1202-1204.
19. Kodani M, Winchell JM. 2012. Engineered combined-positive-control template for real-time reverse transcription-PCR in multiple-pathogen-detection assays. J Clin Microbiol 50:1057-1060. http://dx.doi.org/10.1128/JCM.05987-11.
20. Towner JS, Khristova ML, Sealy TK, Vincent MJ, Erickson BR, Bawiec DA, Hartman AL, Comer JA, Zaki SR, Stroher U, Gomes Da Silva F, del Castillo F, Rollin PE, Ksiazek TG, Nichol ST. 2006. Marburgvirus genomics and association with a large hemorrhagic fever outbreak in Angola. J Virol 80:6497-6516. http://dx.doi.org/10.1128/JVI.00069-06.
21. Imwong M, Woodrow CJ, Hendriksen IC, Veenemans J, Verhoef H, Faiz MA, Mohanty S, Mishra S, Mtove G, Gesase S, Seni A, Chhaganlal KD, Day NP, Dondorp AM, White NJ. 2015. Plasma concentration of parasite DNA as a measure of disease severity in falciparum malaria. J Infect Dis 211:1128-1133. http://dx.doi.org/10.1093/infdis/jiu590.
22. Reddy V, Mani RS, Desai A, Ravi V. 2014. Correlation of plasma viral loads and presence of Chikungunya IgM antibodies with cytokine/chemokine levels during acute Chikungunya virus infection. J Med Virol 86:1393-1401. http://dx.doi.org/10.1002/jmv.23875.
23. Towner JS, Rollin PE, Bausch DG, Sanchez A, Crary SM, Vincent M, Lee WF, Spiropoulou CF, Ksiazek TG, Lukwiya M, Kaducu F, Downing R, Nichol ST. 2004. Rapid diagnosis ofEbola hemorrhagic fever byreverse transcription-PCR in an outbreak setting and assessment of patient viral load as a predictor of outcome. J Virol 78:4330-4341. http://dx.doi.org/10.1128/JVI.78.8.4330-4341.2004.
24. Wang WK, Chen HL, Yang CF, Hsieh SC, Juan CC, Chang SM, Yu CC, Lin LH, Huang JH, King CC. 2006. Slower rates of clearance of viral load and virus-containing immune complexes in patients with dengue hemor-rhagic fever. Clin Infect Dis 43:1023-1030. http://dx.doi.org/10.1086/507635.
25. de Oliveira Poersch C, Pavoni DP, Queiroz MH, de Borba L, Golden-berg S, dos Santos CN, Krieger MA. 2005. Dengue virus infections: comparison of methods for diagnosing the acute disease. J Clin Virol 32: 272-277. http://dx.doi.org/10.1016/j.jcv.2004.08.008.
26. Gyarmati P, Mohammed N, Norder H, Blomberg J, Belak S, Widen F. 2007. Universal detection of hepatitis E virus by two real-time PCR assays: TaqMan and primer-probe energy transfer. JVirol Methods 146:226-235. http://dx.doi.org/10.1016/j.jviromet.2007.07.014.
27. Vasoo S, Pritt BS. 2013. Molecular diagnostics and parasitic disease. Clin Lab Med 33:461-503. http://dx.doi.org/10.1016/j.cll.2013.03.008.
28. Towner JS, Sealy TK, Ksiazek TG, Nichol ST. 2007. High-throughput molecular detection of hemorrhagic fever virus threats with applications for outbreak settings. J Infect Dis 196(Suppl):S205-S212. http://dx.doi.org/10.1086/520601.
29. Chang SS, Hsieh WH, Liu TS, Lee SH, Wang CH, Chou HC, Yeo YH, Tseng CP, Lee CC. 2013. Multiplex PCR system for rapid detection of pathogens in patients with presumed sepsis-a systemic review and meta-analysis. PLoS One 8:e62323. http://dx.doi.org/10.1371/journal.pone.0062323.
30. Gordon MA, Kankwatira AM, Mwafulirwa G, Walsh AL, Hopkins MJ, Parry CM, Faragher EB, Zijlstra EE, Heyderman RS, Molyneux ME. 2010. Invasive non-typhoid salmonellae establish systemic intracellular infection in HIV-infected adults: an emerging disease pathogenesis. Clin Infect Dis 50:953-962. http://dx.doi.org/10.1086/651080.
31. Wain J, Pham VB, Ha V, Nguyen NM, To SD, Walsh AL, Parry CM, Hasserjian RP, HoHo VA, Tran TH, Farrar J, White NJ, Day NP. 2001. Quantitationofbacteriainbone marrow from patients with typhoid fever: relationship between counts and clinical features. J Clin Microbiol 39: 1571-1576. http://dx.doi.org/10.1128/JCM.39.4.1571-1576.2001.
32. Baker S, Favorov M, Dougan G. 2010. Searching for the elusive typhoid diagnostic. BMC Infect Dis 10:45. http://dx.doi.org/10.1186/1471-2334-10-45.
33. Schotthoefer AM, Meece JK, Ivacic LC, Bertz PD, Zhang K, Weiler T, Uphoff TS, Fritsche TR. 2013. Comparison of a real-time PCR method with serology and blood smear analysis for diagnosis of human anaplas-mosis: importance of infection time course for optimal test utilization. J Clin Microbiol 51:2147-2153. http://dx.doi.org/10.1128/JCM.00347-13.
34. Lanciotti RS, Kosoy OL, Laven JJ, Panella AJ, Velez JO, Lambert AJ, Campbell GL. 2007. Chikungunya virus in US travelers returning from India, 2006. Emerg Infect Dis 13:764-767. http://dx.doi.org/10.3201/eid1305.070015.
35. Drosten C, Gottig S, Schilling S, Asper M, Panning M, Schmitz H, Gunther S. 2002. Rapid detection and quantification of RNA of Ebola and Marburg viruses, Lassa virus, Crimean-Congo hemorrhagic fever virus, Rift Valley fever virus, dengue virus, and yellow fever virus by real-time reverse transcription-PCR. J Clin Microbiol 40:2323-2330. http://dx.doi.org/10.1128/JCM.40.7.2323-2330.2002.
36. Kramski M, Meisel H, Klempa B, Kruger DH, Pauli G, Nitsche A. 2007. Detection and typing of human pathogenic hantaviruses by real-time reverse transcription-PCR and pyrosequencing. Clin Chem 53:1899-1905. http://dx.doi.org/10.1373/clinchem.2007.093245.
37. Jothikumar N, Cromeans TL, Robertson BH, Meng XJ, Hill VR. 2006. A broadly reactive one-step real-time RT-PCR assay for rapid and sensitive detection of hepatitis E virus. J Virol Methods 131:65-71. http://dx.doi.org/10.1016/j.jviromet.2005.07.004.
38. Lo MK, Lowe L, Hummel KB, Sazzad HM, Gurley ES, Hossain MJ, Luby SP, Miller DM, Comer JA, Rollin PE, Bellini WJ, Rota PA. 2012. Characterization of Nipah virus from outbreaks in Bangladesh, 2008-2010. Emerg Infect Dis 18:248-255. http://dx.doi.org/10.3201/eid1802.111492.
39. Saxton-Shaw KD, Ledermann JP, Borland EM, Stovall JL, Mossel EC, Singh AJ, Wilusz J, Powers AM. 2013. O'nyong nyong virus molecular determinants of unique vector specificity reside in non-structural protein 3. PLoS Negl Trop Dis 7:e1931. http://dx.doi.org/10.1371/journal.pntd.0001931.
40. Bird BH, Bawiec DA, Ksiazek TG, Shoemaker TR, Nichol ST. 2007. Highly sensitive and broadly reactive quantitative reverse transcription-PCR assay for high-throughput detection of Rift Valley fever virus. J Clin Microbiol 45:3506-3513. http://dx.doi.org/10.1128/JCM.00936-07.
41. Lanciotti RS, Kerst AJ, Nasci RS, Godsey MS, Mitchell CJ, Savage HM, Komar N, Panella NA, Allen BC, Volpe KE, Davis BS, Roehrig JT. 2000. Rapid detection of West Nile virus from human clinical specimens, field-collected mosquitoes, and avian samples by a TaqMan reverse transcrip-tase-PCR assay. J Clin Microbiol 38:4066-4071.
42. Chao DY, Davis BS, Chang GJ. 2007. Development of multiplex realtime reverse transcriptase PCR assays for detecting eight medically important flaviviruses in mosquitoes. J Clin Microbiol 45:584-589. http://dx.doi.org/10.1128/JCM.00842-06.
43. Diaz MH, Bai Y, Malania L, Winchell JM, Kosoy MY. 2012. Development of a novel genus-specific real-time PCR assay for detection and differentiation of Bartonella species and genotypes. J Clin Microbiol 50: 1645-1649. http://dx.doi.org/10.1128/JCM.06621-11.
44. Hinic V, Brodard I, Thomann A, Cvetnic Z, Makaya PV, Frey J, Abril C. 2008. Novel identification and differentiation of Brucella melitensis, B. abortus, B. suis, B. ovis, B. canis, and B. neotomae suitable for both conventional and real-time PCR systems. J Microbiol Methods 75:375-378. http://dx.doi.org/10.1016/j.mimet.2008.07.002.
45. Loftis AD, Reeves WK, Szumlas DE, Abbassy MM, Helmy IM, Mori-arity JR, Dasch GA. 2006. Surveillance of Egyptian fleas for agents of public health significance: Anaplasma, Bartonella, Coxiella, Ehrlichia, Rickettsia, and Yersinia pestis. Am J Trop Med Hyg 75:41-48.
46. Stoddard RA, Gee JE, Wilkins PP, McCaustland K, Hoffmaster AR. 2009. Detection of pathogenic Leptospira spp. through TaqMan polymer-ase chain reaction targeting the LipL32 gene. Diagn Microbiol Infect Dis 64:247-255. http://dx.doi.org/10.1016/j.diagmicrobio.2009.03.014.
47. Kato CY, Chung IH, Robinson LK, Austin AL, Dasch GA, Massung RF. 2013. Assessment of real-time PCR assay for detection of Rickettsia spp. and Rickettsia rickettsii in banked clinical samples. J Clin Microbiol 51: 314-317. http://dx.doi.org/10.1128/JCM.01723-12.
48. Malorny B, Cook N, D'Agostino M, De Medici D, Croci L, Abdulmaw-jood A, Fach P, Karpiskova R, Aymerich T, Kwaitek K, Hoorfar J, Malorny B. 2004. Multicenter validation of PCR-based method for detection of Salmonella in chicken and pig samples. J AOAC Int 87:861-866.
49. Nga TV, Karkey A, Dongol S, Thuy HN, Dunstan S, Holt K, Tu le TP, Campbell JI, Chau TT, Chau NV, Arjyal A, Koirala S, Basnyat B, Dolecek C, Farrar J, Baker S. 2010. The sensitivity of real-time PCR amplification targeting invasive Salmonella serovars in biological specimens. BMC Infect Dis 10:125. http://dx.doi.org/10.1186/1471-2334-10-125.
50. Wortmann G, Sweeney C, Houng HS, Aronson N, Stiteler J, Jackson J, Ockenhouse C. 2001. Rapid diagnosis of leishmaniasis by fluorogenic polymerase chain reaction. Am J Trop Med Hyg 65:583-587.
51. Kamau E, Tolbert LS, Kortepeter 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. http://dx.doi.org/10.1128/JCM.00276-11.
52. Deborggraeve S, Claes F, Laurent T, Mertens P, Leclipteux T, Dujardin JC, Herdewijn P, Buscher P. 2006. Molecular dipstick test for diagnosis of sleeping sickness. J Clin Microbiol 44:2884-2889. http://dx.doi.org/10.1128/JCM.02594-05.