Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study

Chantal B E M Reusken; Bart L Haagmans; Marcel A Müller; Carlos Gutierrez; Gert-Jan Godeke; Benjamin Meyer; Doreen Muth; V Stalin Raj; Laura Smits-De Vries; Victor M Corman; Jan-Felix Drexler; Saskia L Smits; Yasmin E El Tahir; Rita De Sousa; Janko van Beek; Norbert Nowotny; Kees van Maanen; Ezequiel Hidalgo-Hermoso; Berend-Jan Bosch; Peter Rottier; Albert Osterhaus; Christian Gortázar-Schmidt; Christian Drosten; Marion P G Koopmans

doi:10.1016/S1473-3099(13)70164-6

Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study

Chantal B E M Reusken^*
, Bart L Haagmans
, Marcel A Müller
, Carlos Gutierrez
, Gert-Jan Godeke
, Benjamin Meyer
, Doreen Muth
, V Stalin Raj
, Laura Smits-De Vries
, Victor M Corman
, Jan-Felix Drexler
, Saskia L Smits
, Yasmin E El Tahir
, Rita De Sousa
, Janko van Beek
, Norbert Nowotny
, Kees van Maanen
, Ezequiel Hidalgo-Hermoso
, Berend-Jan Bosch
, Peter Rottier

Albert Osterhaus, Christian Gortázar-Schmidt, Christian Drosten, Marion P G Koopmans

^*Corresponding author for this work

Virology

National Institute of Public Health and the Environment
University of Bonn Medical Centre
Utrecht University

Research output: Contribution to journal › Article › Academic › peer-review

630 Citations (Scopus)

Abstract

BACKGROUND: A new betacoronavirus-Middle East respiratory syndrome coronavirus (MERS-CoV)-has been identified in patients with severe acute respiratory infection. Although related viruses infect bats, molecular clock analyses have been unable to identify direct ancestors of MERS-CoV. Anecdotal exposure histories suggest that patients had been in contact with dromedary camels or goats. We investigated possible animal reservoirs of MERS-CoV by assessing specific serum antibodies in livestock.

METHODS: We took sera from animals in the Middle East (Oman) and from elsewhere (Spain, Netherlands, Chile). Cattle (n=80), sheep (n=40), goats (n=40), dromedary camels (n=155), and various other camelid species (n=34) were tested for specific serum IgG by protein microarray using the receptor-binding S1 subunits of spike proteins of MERS-CoV, severe acute respiratory syndrome coronavirus, and human coronavirus OC43. Results were confirmed by virus neutralisation tests for MERS-CoV and bovine coronavirus.

FINDINGS: 50 of 50 (100%) sera from Omani camels and 15 of 105 (14%) from Spanish camels had protein-specific antibodies against MERS-CoV spike. Sera from European sheep, goats, cattle, and other camelids had no such antibodies. MERS-CoV neutralising antibody titres varied between 1/320 and 1/2560 for the Omani camel sera and between 1/20 and 1/320 for the Spanish camel sera. There was no evidence for cross-neutralisation by bovine coronavirus antibodies.

INTERPRETATION: MERS-CoV or a related virus has infected camel populations. Both titres and seroprevalences in sera from different locations in Oman suggest widespread infection.

FUNDING: European Union, European Centre For Disease Prevention and Control, Deutsche Forschungsgemeinschaft.

Original language	English
Pages (from-to)	859-866
Number of pages	8
Journal	Lancet Infectious Diseases
Volume	13
Issue number	10
DOIs	https://doi.org/10.1016/S1473-3099(13)70164-6
Publication status	Published - Oct 2013

Bibliographical note

Funding:
European Union, European Centre For Disease Prevention and Control, Deutsche Forschungsgemeinschaft.

Role of the funding source:
The sponsors had no role in study design, data collection,
data analysis, data interpretation, or writing of the report.
The corresponding author had full access to all the data
in the study and had fi nal responsibility for the decision
to submit for publication

Copyright © 2013 Elsevier Ltd. All rights reserved.

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

Research programs

EMC MM-04-27-01

Access to Document

10.1016/S1473-3099(13)70164-6

http://hdl.handle.net/1765/41567

Cite this

Reusken, C. B. E. M., Haagmans, B. L., Müller, M. A., Gutierrez, C., Godeke, G.-J., Meyer, B., Muth, D., Raj, V. S., Smits-De Vries, L., Corman, V. M., Drexler, J.-F., Smits, S. L., El Tahir, Y. E., De Sousa, R., van Beek, J., Nowotny, N., van Maanen, K., Hidalgo-Hermoso, E., Bosch, B.-J., ... Koopmans, M. P. G. (2013). Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study. Lancet Infectious Diseases, 13(10), 859-866. https://doi.org/10.1016/S1473-3099(13)70164-6

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title = "Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study",

abstract = "BACKGROUND: A new betacoronavirus-Middle East respiratory syndrome coronavirus (MERS-CoV)-has been identified in patients with severe acute respiratory infection. Although related viruses infect bats, molecular clock analyses have been unable to identify direct ancestors of MERS-CoV. Anecdotal exposure histories suggest that patients had been in contact with dromedary camels or goats. We investigated possible animal reservoirs of MERS-CoV by assessing specific serum antibodies in livestock.METHODS: We took sera from animals in the Middle East (Oman) and from elsewhere (Spain, Netherlands, Chile). Cattle (n=80), sheep (n=40), goats (n=40), dromedary camels (n=155), and various other camelid species (n=34) were tested for specific serum IgG by protein microarray using the receptor-binding S1 subunits of spike proteins of MERS-CoV, severe acute respiratory syndrome coronavirus, and human coronavirus OC43. Results were confirmed by virus neutralisation tests for MERS-CoV and bovine coronavirus.FINDINGS: 50 of 50 (100\%) sera from Omani camels and 15 of 105 (14\%) from Spanish camels had protein-specific antibodies against MERS-CoV spike. Sera from European sheep, goats, cattle, and other camelids had no such antibodies. MERS-CoV neutralising antibody titres varied between 1/320 and 1/2560 for the Omani camel sera and between 1/20 and 1/320 for the Spanish camel sera. There was no evidence for cross-neutralisation by bovine coronavirus antibodies.INTERPRETATION: MERS-CoV or a related virus has infected camel populations. Both titres and seroprevalences in sera from different locations in Oman suggest widespread infection.FUNDING: European Union, European Centre For Disease Prevention and Control, Deutsche Forschungsgemeinschaft.",

author = "Reusken, \{Chantal B E M\} and Haagmans, \{Bart L\} and M{\"u}ller, \{Marcel A\} and Carlos Gutierrez and Gert-Jan Godeke and Benjamin Meyer and Doreen Muth and Raj, \{V Stalin\} and \{Smits-De Vries\}, Laura and Corman, \{Victor M\} and Jan-Felix Drexler and Smits, \{Saskia L\} and \{El Tahir\}, \{Yasmin E\} and \{De Sousa\}, Rita and \{van Beek\}, Janko and Norbert Nowotny and \{van Maanen\}, Kees and Ezequiel Hidalgo-Hermoso and Berend-Jan Bosch and Peter Rottier and Albert Osterhaus and Christian Gort{\'a}zar-Schmidt and Christian Drosten and Koopmans, \{Marion P G\}",

note = "Funding: European Union, European Centre For Disease Prevention and Control, Deutsche Forschungsgemeinschaft. Role of the funding source: The sponsors had no role in study design, data collection, data analysis, data interpretation, or writing of the report. The corresponding author had full access to all the data in the study and had fi nal responsibility for the decision to submit for publication Copyright {\textcopyright} 2013 Elsevier Ltd. All rights reserved.",

year = "2013",

month = oct,

doi = "10.1016/S1473-3099(13)70164-6",

language = "English",

volume = "13",

pages = "859--866",

journal = "Lancet Infectious Diseases",

issn = "1473-3099",

publisher = "Elsevier Ltd.",

number = "10",

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Reusken, CBEM, Haagmans, BL, Müller, MA, Gutierrez, C, Godeke, G-J, Meyer, B, Muth, D, Raj, VS, Smits-De Vries, L, Corman, VM, Drexler, J-F, Smits, SL, El Tahir, YE, De Sousa, R, van Beek, J, Nowotny, N, van Maanen, K, Hidalgo-Hermoso, E, Bosch, B-J, Rottier, P, Osterhaus, A, Gortázar-Schmidt, C, Drosten, C & Koopmans, MPG 2013, 'Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study', Lancet Infectious Diseases, vol. 13, no. 10, pp. 859-866. https://doi.org/10.1016/S1473-3099(13)70164-6

TY - JOUR

T1 - Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels

T2 - a comparative serological study

AU - Reusken, Chantal B E M

AU - Haagmans, Bart L

AU - Müller, Marcel A

AU - Gutierrez, Carlos

AU - Godeke, Gert-Jan

AU - Meyer, Benjamin

AU - Muth, Doreen

AU - Raj, V Stalin

AU - Smits-De Vries, Laura

AU - Corman, Victor M

AU - Drexler, Jan-Felix

AU - Smits, Saskia L

AU - El Tahir, Yasmin E

AU - De Sousa, Rita

AU - van Beek, Janko

AU - Nowotny, Norbert

AU - van Maanen, Kees

AU - Hidalgo-Hermoso, Ezequiel

AU - Bosch, Berend-Jan

AU - Rottier, Peter

AU - Osterhaus, Albert

AU - Gortázar-Schmidt, Christian

AU - Drosten, Christian

AU - Koopmans, Marion P G

N1 - Funding: European Union, European Centre For Disease Prevention and Control, Deutsche Forschungsgemeinschaft. Role of the funding source: The sponsors had no role in study design, data collection, data analysis, data interpretation, or writing of the report. The corresponding author had full access to all the data in the study and had fi nal responsibility for the decision to submit for publication Copyright © 2013 Elsevier Ltd. All rights reserved.

PY - 2013/10

Y1 - 2013/10

N2 - BACKGROUND: A new betacoronavirus-Middle East respiratory syndrome coronavirus (MERS-CoV)-has been identified in patients with severe acute respiratory infection. Although related viruses infect bats, molecular clock analyses have been unable to identify direct ancestors of MERS-CoV. Anecdotal exposure histories suggest that patients had been in contact with dromedary camels or goats. We investigated possible animal reservoirs of MERS-CoV by assessing specific serum antibodies in livestock.METHODS: We took sera from animals in the Middle East (Oman) and from elsewhere (Spain, Netherlands, Chile). Cattle (n=80), sheep (n=40), goats (n=40), dromedary camels (n=155), and various other camelid species (n=34) were tested for specific serum IgG by protein microarray using the receptor-binding S1 subunits of spike proteins of MERS-CoV, severe acute respiratory syndrome coronavirus, and human coronavirus OC43. Results were confirmed by virus neutralisation tests for MERS-CoV and bovine coronavirus.FINDINGS: 50 of 50 (100%) sera from Omani camels and 15 of 105 (14%) from Spanish camels had protein-specific antibodies against MERS-CoV spike. Sera from European sheep, goats, cattle, and other camelids had no such antibodies. MERS-CoV neutralising antibody titres varied between 1/320 and 1/2560 for the Omani camel sera and between 1/20 and 1/320 for the Spanish camel sera. There was no evidence for cross-neutralisation by bovine coronavirus antibodies.INTERPRETATION: MERS-CoV or a related virus has infected camel populations. Both titres and seroprevalences in sera from different locations in Oman suggest widespread infection.FUNDING: European Union, European Centre For Disease Prevention and Control, Deutsche Forschungsgemeinschaft.

AB - BACKGROUND: A new betacoronavirus-Middle East respiratory syndrome coronavirus (MERS-CoV)-has been identified in patients with severe acute respiratory infection. Although related viruses infect bats, molecular clock analyses have been unable to identify direct ancestors of MERS-CoV. Anecdotal exposure histories suggest that patients had been in contact with dromedary camels or goats. We investigated possible animal reservoirs of MERS-CoV by assessing specific serum antibodies in livestock.METHODS: We took sera from animals in the Middle East (Oman) and from elsewhere (Spain, Netherlands, Chile). Cattle (n=80), sheep (n=40), goats (n=40), dromedary camels (n=155), and various other camelid species (n=34) were tested for specific serum IgG by protein microarray using the receptor-binding S1 subunits of spike proteins of MERS-CoV, severe acute respiratory syndrome coronavirus, and human coronavirus OC43. Results were confirmed by virus neutralisation tests for MERS-CoV and bovine coronavirus.FINDINGS: 50 of 50 (100%) sera from Omani camels and 15 of 105 (14%) from Spanish camels had protein-specific antibodies against MERS-CoV spike. Sera from European sheep, goats, cattle, and other camelids had no such antibodies. MERS-CoV neutralising antibody titres varied between 1/320 and 1/2560 for the Omani camel sera and between 1/20 and 1/320 for the Spanish camel sera. There was no evidence for cross-neutralisation by bovine coronavirus antibodies.INTERPRETATION: MERS-CoV or a related virus has infected camel populations. Both titres and seroprevalences in sera from different locations in Oman suggest widespread infection.FUNDING: European Union, European Centre For Disease Prevention and Control, Deutsche Forschungsgemeinschaft.

U2 - 10.1016/S1473-3099(13)70164-6

DO - 10.1016/S1473-3099(13)70164-6

M3 - Article

C2 - 23933067

SN - 1473-3099

VL - 13

SP - 859

EP - 866

JO - Lancet Infectious Diseases

JF - Lancet Infectious Diseases

IS - 10

ER -

Middle East respiratory syndrome coronavirus neutralising serum antibodies in dromedary camels: a comparative serological study

Abstract

Bibliographical note

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