Sensitive and specific detection of low-level antibody responses in mild Middle East respiratory syndrome coronavirus infections

Emerging Infectious Diseases

Volumn 25, Issue 10, 2019, Pages 1868-1877

  Okba, Nisreen M A ^d   Stalin Raj, V ^d   Widjaja, Ivy ^a   GeurtsvanKessel, Corine H ^d   De Bruin, Erwin ^d   Chandler, Felicity D ^d   Park, Wan Beom ^b   Kim, Nam Joong ^b   Farag, Elmoubasher A B A ^c   Al Hajri, Mohammed ^c   Bosch, Berend Jan ^a   Oh, Myoung Don ^b   Koopmans, Marion P G ^d   Reusken, Chantal B E M ^d   Haagmans, Bart L ^d  

^a UTRECHT UNIVERSITY   (Netherlands)

^b Seoul National University   (South Korea)

^c Ministry of Health   (Qatar)

^d ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

NEUTRALIZING ANTIBODY; VIRUS ANTIBODY;

ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; AUTOIMMUNE DISEASE IMMUNOFLUORESCENCE ASSAY; CAMEL; COHORT ANALYSIS; CONTROLLED STUDY; CROSS REACTION; DIAGNOSTIC TEST ACCURACY STUDY; DISEASE SEVERITY; DISEASE SURVEILLANCE; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CORONAVIRUS OC43; HUMAN METAPNEUMOVIRUS; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNE RESPONSE; IMMUNOPRECIPITATION; LONGITUDINAL STUDY; LUCIFERASE IMMUNOPRECIPITATION ASSAY; MIDDLE EAST RESPIRATORY SYNDROME; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; NONHUMAN; NORMAL HUMAN; PLAQUE REDUCTION NEUTRALIZATION ASSAY; PREDICTIVE VALUE; PROTEIN DENATURATION; PROTEIN MICROARRAY; REAL TIME REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RECEIVER OPERATING CHARACTERISTIC; SENSITIVITY AND SPECIFICITY; SEROCONVERSION; SEROPREVALENCE; VALIDATION PROCESS; VIRUS DETECTION; VIRUS NEUTRALIZATION; VIRUS NUCLEOCAPSID; WESTERN BLOTTING; BLOOD; CORONAVIRUS INFECTION; HUMORAL IMMUNITY; IMMUNOLOGY; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEVERITY OF ILLNESS INDEX; TIME FACTOR; VIROLOGY;

ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CORONAVIRUS INFECTIONS; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; IMMUNITY, HUMORAL; MIDDLE EAST RESPIRATORY SYNDROME CORONAVIRUS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; SEVERITY OF ILLNESS INDEX; TIME FACTORS;

EID: 85072354827     PISSN: 10806040     EISSN: 10806059     Source Type: Journal    
DOI: 10.3201/eid2510.190051     Document Type: Article

References (40)

1. Zaki AM, van Boheemen S, Bestebroer TM, Osterhaus AD, Fouchier RA. Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med. 2012;367:1814-20. https://doi.org/10.1056/NEJMoa1211721
2. World Health Organization. Middle East respiratory syndrome coronavirus (MERS-CoV) [cited 2017 Jul 16]. http://www.who.int/emergencies/mers-cov
3. Puzelli S, Azzi A, Santini MG, Di Martino A, Facchini M, Castrucci MR, et al. Investigation of an imported case of Middle East respiratory syndrome coronavirus (MERS-CoV) infection in Florence, Italy, May to June 2013. Euro Surveill. 2013;18:20564. https://doi.org/10.2807/1560-7917.ES2013.18.34.20564
4. Al Hammadi ZM, Chu DK, Eltahir YM, Al Hosani F, Al Mulla M, Tarnini W, et al. Asymptomatic MERS-CoV infection in humans possibly linked to infected dromedaries imported from Oman to United Arab Emirates, May 2015. Emerg Infect Dis. 2015;21:2197-200. https://doi.org/10.3201/eid2112.151132
5. Alshukairi AN, Khalid I, Ahmed WA, Dada AM, Bayumi DT, Malic LS, et al. Antibody response and disease severity in healthcare worker MERS survivors. Emerg Infect Dis. 2016;22. https://doi.org/10.3201/eid2206.160010
6. Reusken CB, Haagmans BL, Müller MA, Gutierrez C, Godeke GJ, Meyer B, et al. Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study. Lancet Infect Dis. 2013;13:859-66. https://doi.org/10.1016/S1473-3099(13)70164-6
7. Haagmans BL, Al Dhahiry SH, Reusken CB, Raj VS, Galiano M, Myers R, et al. Middle East respiratory syndrome coronavirus in dromedary camels: an outbreak investigation. Lancet Infect Dis. 2014;14:140-5. https://doi.org/10.1016/S1473-3099(13)70690-X
8. Reusken CB, Farag EA, Haagmans BL, Mohran KA, Godeke GJ V, Raj S, et al. Occupational exposure to dromedaries and risk for MERS-CoV infection, Qatar, 2013-2014. Emerg Infect Dis. 2015;21:1422-5. https://doi.org/10.3201/eid2108.150481
9. Müller MA, Meyer B, Corman VM, Al-Masri M, Turkestani A, Ritz D, et al. Presence of Middle East respiratory syndrome coronavirus antibodies in Saudi Arabia: a nationwide, cross-sectional, serological study. Lancet Infect Dis. 2015;15:559-64. https://doi.org/10.1016/S1473-3099(15)70090-3
10. Kayali G, Peiris M. A more detailed picture of the epidemiology of Middle East respiratory syndrome coronavirus. Lancet Infect Dis. 2015;15:495-7. https://doi.org/10.1016/S1473-3099(15)70128-3
11. Assiri AM, Biggs HM, Abedi GR, Lu X, Bin Saeed A, Abdalla O, et al. Increase in Middle East respiratory syndrome-coronavirus cases in Saudi Arabia linked to hospital outbreak with continued circulation of recombinant virus, July 1-August 31, 2015. Open Forum Infect Dis. 2016;3:ofw165. https://doi.org/10.1093/ofid/ ofw165
12. Park JW, Lee KJ, Lee KH, Lee SH, Cho JR, Mo JW, et al. Hospital outbreaks of Middle East respiratory syndrome, Daejeon, South Korea, 2015. Emerg Infect Dis. 2017;23:898-905. https://doi.org/10.3201/eid2306.160120
13. Memish ZA, Zumla AI, Al-Hakeem RF, Al-Rabeeah AA, Stephens GM. Family cluster of Middle East respiratory syndrome coronavirus infections. N Engl J Med. 2013;368:2487-94. https://doi.org/10.1056/NEJMoa1303729
14. Assiri A, McGeer A, Perl TM, Price CS, Al Rabeeah AA, Cummings DA, et al.; KSA MERS-CoV Investigation Team. Hospital outbreak of Middle East respiratory syndrome coronavirus. N Engl J Med. 2013;369:407-16. https://doi.org/10.1056/NEJMoa1306742
15. Drosten C, Meyer B, Müller MA, Corman VM, Al-Masri M, Hossain R, et al. Transmission of MERS-coronavirus in household contacts. N Engl J Med. 2014;371:828-35. https://doi.org/10.1056/ NEJMoa1405858
16. Aleanizy FS, Mohmed N, Alqahtani FY, El Hadi Mohamed RA. Outbreak of Middle East respiratory syndrome coronavirus in Saudi Arabia: a retrospective study. BMC Infect Dis. 2017;17:23. https://doi.org/10.1186/s12879-016-2137-3
17. Choe PG, Perera RAPM, Park WB, Song KH, Bang JH, Kim ES, et al. MERS-CoV antibody responses 1 year after symptom onset, South Korea, 2015. Emerg Infect Dis. 2017;23:1079-84. https://doi.org/10.3201/eid2307.170310
18. Corman VM, Eckerle I, Bleicker T, Zaki A, Landt O, Eschbach-Bludau M, et al. Detection of a novel human coronavirus by real-time reverse-transcription polymerase chain reaction. Euro Surveill. 2012;17:20285. https://doi.org/10.2807/ese.17.39.20285-en
19. Corman VM, Müller MA, Costabel U, Timm J, Binger T, Meyer B, et al. Assays for laboratory confirmation of novel human coronavirus (hCoV-EMC) infections. Euro Surveill. 2012;17:20334. https://doi.org/10.2807/ese.17.49.20334-en
20. Furuse Y, Okamoto M, Oshitani H. Conservation of nucleotide sequences for molecular diagnosis of Middle East respiratory syndrome coronavirus, 2015. Int J Infect Dis. 2015;40:25-7. https://doi.org/10.1016/j.ijid.2015.09.018
21. Park SW, Perera RA, Choe PG, Lau EH, Choi SJ, Chun JY, et al. Comparison of serological assays in human Middle East respiratory syndrome (MERS)-coronavirus infection. Euro Surveill. 2015;20:30042. https://doi.org/10.2807/1560-7917.ES.2015.20.41.30042
22. Al-Abdallat MM, Payne DC, Alqasrawi S, Rha B, Tohme RA, Abedi GR, et al.; Jordan MERS-CoV Investigation Team. Hospital-associated outbreak of Middle East respiratory syndrome coronavirus: a serologic, epidemiologic, and clinical description. Clin Infect Dis. 2014;59:1225-33. https://doi.org/10.1093/cid/ ciu359
23. Reusken C, Mou H, Godeke GJ, van der Hoek L, Meyer B, Müller MA, et al. Specific serology for emerging human coronaviruses by protein microarray. Euro Surveill. 2013;18:20441. https://doi.org/10.2807/1560-7917.ES2013.18.14.20441
24. Alagaili AN, Briese T, Mishra N, Kapoor V, Sameroff SC, Burbelo PD, et al. Middle East respiratory syndrome coronavirus infection in dromedary camels in Saudi Arabia. MBio. 2014;5:e01002-14. https://doi.org/10.1128/mBio.01002-14
25. Perera RA, Wang P, Gomaa MR, El-Shesheny R, Kandeil A, Bagato O, et al. Seroepidemiology for MERS coronavirus using microneutralisation and pseudoparticle virus neutralisation assays reveal a high prevalence of antibody in dromedary camels in Egypt, June 2013. Euro Surveill. 2013;18:20574. https://doi.org/ 10.2807/1560-7917.ES2013.18.36.20574
26. Meyer B, Müller MA, Corman VM, Reusken CB, Ritz D, Godeke GJ, et al. Antibodies against MERS coronavirus in dromedary camels, United Arab Emirates, 2003 and 2013. Emerg Infect Dis. 2014;20:552-9. https://doi.org/10.3201/eid2004.131746
27. Meyer B, Drosten C, Müller MA. Serological assays for emerging coronaviruses: challenges and pitfalls. Virus Res. 2014;194:175-83. https://doi.org/10.1016/j.virusres.2014.03.018
28. Payne DC, Iblan I, Rha B, Alqasrawi S, Haddadin A, Al Nsour M, et al. Persistence of antibodies against Middle East respiratory syndrome coronavirus. Emerg Infect Dis. 2016;22:1824-6. https://doi.org/10.3201/eid2210.160706
29. Fanoy EB, van der Sande MA, Kraaij-Dirkzwager M, Dirksen K, Jonges M, van der Hoek W, et al. Travel-related MERS-CoV cases: an assessment of exposures and risk factors in a group of Dutch travelers returning from the Kingdom of Saudi Arabia, May 2014. Emerg Themes Epidemiol. 2014;11:16. https://doi.org/10.1186/1742-7622-11-16
30. Ko JH, Muller MA, Seok H, Park GE, Lee JY, Cho SY, et al. Suggested new breakpoints of anti-MERS-CoV antibody ELISA titers: performance analysis of serologic tests. Eur J Clin Microbiol Infect Dis. 2017;36:2179-86.
31. Ko JH, Müller MA, Seok H, Park GE, Lee JY, Cho SY, et al. Serologic responses of 42 MERS-coronavirus-infected patients according to the disease severity. Diagn Microbiol Infect Dis. 2017;89:106-11. https://doi.org/10.1016/j.diagmicrobio.2017.07.006
32. Chan KH, Chan JF, Tse H, Chen H, Lau CC, Cai JP, et al. Cross-reactive antibodies in convalescent SARS patients' sera against the emerging novel human coronavirus EMC (2012) by both immunofluorescent and neutralizing antibody tests. J Infect. 2013;67:130-40. https://doi.org/10.1016/j.jinf.2013.03.015
33. Liljander A, Meyer B, Jores J, Müller MA, Lattwein E, Njeru I, et al. MERS-CoV antibodies in humans, Africa, 2013-2014. Emerg Infect Dis. 2016;22:1086-9. https://doi.org/10.3201/eid2206.160064
34. Oh MD, Park WB, Choe PG, Choi SJ, Kim JI, Chae J, et al. Viral load kinetics of MERS coronavirus infection. N Engl J Med. 2016;375:1303-5. https://doi.org/10.1056/NEJMc1511695
35. Hangartner L, Zinkernagel RM, Hengartner H. Antiviral antibody responses: the two extremes of a wide spectrum. Nat Rev Immunol. 2006;6:231-43. https://doi.org/10.1038/nri1783
36. Sakurai H, Williamson RA, Crowe JE, Beeler JA, Poignard P, Bastidas RB, et al. Human antibody responses to mature and immature forms of viral envelope in respiratory syncytial virus infection: significance for subunit vaccines. J Virol. 1999;73:2956-62.
37. World Health Organization. Laboratory testing for Middle East respiratory syndrome coronavirus, interim guidance (WHO/MERS/ LAB/15.1/Rev1/2018). Geneva: The Organization; 2018.
38. Zhao J, Alshukairi AN, Baharoon SA, Ahmed WA, Bokhari AA, Nehdi AM, et al. Recovery from the Middle East respiratory syndrome is associated with antibody and T-cell responses. Sci Immunol. 2017;2:eaan5393. https://doi.org/10.1126/sciimmunol.aan5393
39. Buchholz U, Müller MA, Nitsche A, Sanewski A, Wevering N, Bauer-Balci T, et al. Contact investigation of a case of human novel coronavirus infection treated in a German hospital, October-November 2012. Euro Surveill. 2013;18:20406.
40. Patel DA, Patel AC, Nolan WC, Zhang Y, Holtzman MJ. High throughput screening for small molecule enhancers of the interferon signaling pathway to drive next-generation antiviral drug discovery. PLoS One. 2012;7:e36594. https://doi.org/10.1371/journal.pone.0036594