No Serologic Evidence of Middle East Respiratory Syndrome Coronavirus Infection Among Camel Farmers Exposed to Highly Seropositive Camel Herds: A Household Linked Study, Kenya, 2013

Peninah Munyua Global Disease Detection Program, Division of Global Health Protection, U.S. Centers for Disease Control and Prevention, Nairobi, Kenya.

Search for other papers by Peninah Munyua in
Current site
Google Scholar
PubMed Close
,
Victor Max Corman Institute of Virology, University of Bonn Medical Centre, Bonn, Germany.
German Centre for Infection Research, Partner Site Bonn-Cologne, Bonn, Germany.

Search for other papers by Victor Max Corman in
Current site
Google Scholar
PubMed Close
,
Austine Bitek State Department of Veterinary Services; Ministry of Agriculture Livestock and Fisheries, Nairobi, Kenya.

Search for other papers by Austine Bitek in
Current site
Google Scholar
PubMed Close
,
Eric Osoro Department of Preventive and Promotive Health, Ministry of Health, Nairobi, Kenya.

Search for other papers by Eric Osoro in
Current site
Google Scholar
PubMed Close
,
Benjamin Meyer Institute of Virology, University of Bonn Medical Centre, Bonn, Germany.

Search for other papers by Benjamin Meyer in
Current site
Google Scholar
PubMed Close
,
Marcel A. Müller Institute of Virology, University of Bonn Medical Centre, Bonn, Germany.

Search for other papers by Marcel A. Müller in
Current site
Google Scholar
PubMed Close
,
Erik Lattwein EUROIMMUN AG, Lübeck, Germany.

Search for other papers by Erik Lattwein in
Current site
Google Scholar
PubMed Close
,
S. M. Thumbi Center for Global Health Research, Kenya Medical Research Institute, Nairobi, Kenya.
Paul G. Allen School for Global Animal Health, Washington State University, Pullman, Washington.

Search for other papers by S. M. Thumbi in
Current site
Google Scholar
PubMed Close
,
Rees Murithi State Department of Veterinary Services; Ministry of Agriculture Livestock and Fisheries, Nairobi, Kenya.

Search for other papers by Rees Murithi in
Current site
Google Scholar
PubMed Close
,
Marc-Alain Widdowson Global Disease Detection Program, Division of Global Health Protection, U.S. Centers for Disease Control and Prevention, Nairobi, Kenya.

Search for other papers by Marc-Alain Widdowson in
Current site
Google Scholar
PubMed Close
,
Christian Drosten Institute of Virology, University of Bonn Medical Centre, Bonn, Germany.
German Centre for Infection Research, Partner Site Bonn-Cologne, Bonn, Germany.

Search for other papers by Christian Drosten in
Current site
Google Scholar
PubMed Close
, and
M. Kariuki Njenga Center for Global Health Research, Kenya Medical Research Institute, Nairobi, Kenya.
Paul G. Allen School for Global Animal Health, Washington State University, Pullman, Washington.

Search for other papers by M. Kariuki Njenga in
Current site
Google Scholar
PubMed Close
DOI:
https://doi.org/10.4269/ajtmh.16-0880
Volume/Issue:
Volume 96: Issue 6
Page(s):
1318–1324
Restricted access
Get Permissions

High seroprevalence of Middle East respiratory syndrome coronavirus (MERS-CoV) among camels has been reported in Kenya and other countries in Africa. To date, the only report of MERS-CoV seropositivity among humans in Kenya is of two livestock keepers with no known contact with camels. We assessed whether persons exposed to seropositive camels at household level had serological evidence of infection. In 2013, 760 human and 879 camel sera were collected from 275 and 85 households respectively in Marsabit County. Data on human and animal demographics and type of contact with camels were collected. Human and camel sera were tested for anti-MERS-CoV IgG using a commercial enzyme-linked immunosorbent assay (ELISA) test. Human samples were confirmed by plaque reduction neutralization test (PRNT). Logistic regression was used to identify factors associated with seropositivity. The median age of persons sampled was 30 years (range: 5–90) and 50% were males. A quarter (197/760) of the participants reported having had contact with camels defined as milking, feeding, watering, slaughtering, or herding. Of the human sera, 18 (2.4%) were positive on ELISA but negative by PRNT. Of the camel sera, 791 (90%) were positive on ELISA. On univariate analysis, higher prevalence was observed in female and older camels over 4 years of age (P < 0.05). On multivariate analysis, only age remained significantly associated with increased odds of seropositivity. Despite high seroprevalence among camels, there was no serological confirmation of MERS-CoV infection among camel pastoralists in Marsabit County. The high seropositivity suggests that MERS-CoV or other closely related virus continues to circulate in camels and highlights ongoing potential for animal-to-human transmission.

Author Notes

* Address correspondence to Peninah Munyua, Global Disease Detection Program, Division of Global Health Protection, U.S. Centers for Disease Control and Prevention, P.O. Box 606-00627, Nairobi, Kenya. E-mail: ikg2@cdc.gov
† These authors contributed equally to this work.

Financial support: Financial support for the field work was provided by the U.S. Department of Defense's Defense Threat Reduction Agency and U.S. Centers for Disease Control and Prevention. All the laboratory testing was supported by the German Research Foundation (DFG grant DR772/12-1 to CD), the European Commission project PREPARE (contract number 602525) and the ZAPI project; IMI grant agreement n°115760, with the assistance and financial support of IMI and the European Commission, in kind contributions from EFPIA partners.

Authors' addresses: Peninah Munyua and Marc-Alain Widdowson, Global Disease Detection Program, Division of Global Health Protection, U.S. Centers for Disease Control and Prevention, Nairobi, Kenya, E-mails: ikg2@cdc.gov and zux5@cdc.gov. Victor Max Corman and Christian Drosten, Institute of Virology, University of Bonn Medical Centre, Bonn, Germany, and German Centre for Infection Research, Partner Site Bonn-Cologne, Bonn, Germany, E-mails: corman@virology-bonn.de and drosten@virology-bonn.de. Austine Bitek and Rees Murithi, State Department of Veterinary Services, Ministry of Agriculture Livestock and Fisheries, Nairobi, Kenya, E-mails: bitekorinde@gmail.com and murithi.mbabu@gmail.com. Eric Osoro, Department of Preventive and Promotive Health, Ministry of Health, Nairobi, Kenya, E-mail: osoroe@gmail.com. Benjamin Meyer and Marcel A. Müller, Institute of Virology, University of Bonn Medical Centre, Bonn, Germany, E-mails: meyer@virology-bonn.de and muller@virology-bonn.de. Erik Lattwein, EUROIMMUN AG, Lübeck, Germany, E-mail: e.lattwein@euroimmun.de. S. M. Thumbi and M. Kariuki Njenga, Center for Global Health Research, Kenya Medical Research Institute, Nairobi, Kenya, and Paul G. Allen School for Global Animal Health, Washington State University, Pullman, WA, E-mails: thumbi.mwangi@wsu.edu and knjenga@vetmed.wsu.edu.

Copyright:
© The American Society of Tropical Medicine and Hygiene 2017
Received:
08 Nov 2016
|
Accepted:
30 Jan 2017
|
Published Online:
07 Jun 2017
Cover The American Journal of Tropical Medicine and Hygiene
The American Journal of Tropical Medicine and Hygiene
Print ISSN:
0002-9637
Online ISSN:
1476-1645
  • 1.

    World Health Organization (WHO), 2016. Middle East Respiratory Syndrome Coronavirus. Available at: http://www.who.int/emergencies/mers-cov/en/. Accessed June 22, 2016.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Alsahafi AJ, Cheng AC, 2016. The epidemiology of Middle East respiratory syndrome coronavirus in the Kingdom of Saudi Arabia, 2012–2015. Int J Infect Dis 45: 1–4.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3.

    Hunter JC, Nguyen D, Aden B, Al Bandar Z, Al Dhaheri W, Abu Elkheir K, Khudair A, Al Mulla M, El Saleh F, Imambaccus H, Al Kaabi N, Sheikh FA, Sasse J, Turner A, Abdel Wareth L, Weber S, Al Ameri A, Abu Amer W, Alami NN, Bunga S, Haynes LM, Hall AJ, Kallen AJ, Kuhar D, Pham H, Pringle K, Tong S, Whitaker BL, Gerber SI, Al Hosani FI, 2016. Transmission of Middle East respiratory syndrome coronavirus infections in healthcare settings, Abu Dhabi. Emerg Infect Dis 22: 647–656.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Liu S, Chan TC, Chu YT, Wu JT, Geng X, Zhao N, Cheng W, Chen E, King CC, 2016. Comparative epidemiology of human infections with Middle East respiratory syndrome and severe acute respiratory syndrome coronaviruses among healthcare personnel. PLoS One 11: e0149988.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    Haagmans BL, Al Dhahiry SH, Reusken CB, Raj VS, Galiano M, Myers R, Godeke GJ, Jonges M, Farag E, Diab A, Ghobashy H, Alhajri F, Al-Thani M, Al-Marri SA, Al Romaihi HE, Al Khal A, Bermingham A, Osterhaus AD, AlHajri MM, Koopmans MP, 2014. Middle East respiratory syndrome coronavirus in dromedary camels: an outbreak investigation. Lancet Infect Dis 14: 140–145.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6.

    Memish ZA, Cotten M, Meyer B, Watson SJ, Alsahafi AJ, Al Rabeeah AA, Corman VM, Sieberg A, Makhdoom HQ, Assiri A, Al Masri M, Aldabbagh S, Bosch BJ, Beer M, Muller MA, Kellam P, Drosten C, 2014. Human infection with MERS coronavirus after exposure to infected camels, Saudi Arabia, 2013. Emerg Infect Dis 20: 1012–1015.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Nowotny N, Kolodziejek J, 2014. Middle East respiratory syndrome coronavirus (MERS-CoV) in dromedary camels, Oman, 2013. Euro Surveill 19: 20781.

  • 8.

    Corman VM, Jores J, Meyer B, Younan M, Liljander A, Said MY, Gluecks I, Lattwein E, Bosch BJ, Drexler JF, Bornstein S, Drosten C, Muller MA, 2014. Antibodies against MERS coronavirus in dromedary camels, Kenya, 1992–2013. Emerg Infect Dis 20: 1319–1322.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Deem SL, Fevre EM, Kinnaird M, Browne AS, Muloi D, Godeke GJ, Koopmans M, Reusken CB, 2015. Serological evidence of MERS-CoV antibodies in dromedary camels (Camelus dromedaries) in Laikipia County, Kenya. PLoS One 10: e0140125.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Meyer B, Muller MA, Corman VM, Reusken CB, Ritz D, Godeke GJ, Lattwein E, Kallies S, Siemens A, van Beek J, Drexler JF, Muth D, Bosch BJ, Wernery U, Koopmans MP, Wernery R, Drosten C, 2014. Antibodies against MERS coronavirus in dromedary camels, United Arab Emirates, 2003 and 2013. Emerg Infect Dis 20: 552–559.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11.

    Muller MA, Corman VM, Jores J, Meyer B, Younan M, Liljander A, Bosch BJ, Lattwein E, Hilali M, Musa BE, Bornstein S, Drosten C, 2014. MERS coronavirus neutralizing antibodies in camels, eastern Africa, 1983–1997. Emerg Infect Dis 20: 2093–2095.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Chu DK, Oladipo JO, Perera RA, Kuranga SA, Chan SM, Poon LL, Peiris M, 2015. Middle East respiratory syndrome coronavirus (MERS-CoV) in dromedary camels in Nigeria, 2015. Euro Surveill 20: 11–17.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Gutierrez C, Tejedor-Junco MT, Gonzalez M, Lattwein E, Renneker S, 2015. Presence of antibodies but no evidence for circulation of MERS-CoV in dromedaries on the Canary Islands, 2015. Euro Surveill 20: 31–34.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Hemida MG, Chu DK, Poon LL, Perera RA, Alhammadi MA, Ng HY, Siu LY, Guan Y, Alnaeem A, Peiris M, 2014. MERS coronavirus in dromedary camel herd, Saudi Arabia. Emerg Infect Dis 20: 1231–1234.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Crameri G, Durr PA, Barr J, Yu M, Graham K, Williams OJ, Kayali G, Smith D, Peiris M, Mackenzie JS, Wang L-F, 2015. Absence of MERS-CoV antibodies in feral camels in Australia: implications for the pathogen's origin and spread. One Health 1: 76–82.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Hemida MG, Perera RA, Al Jassim RA, Kayali G, Siu LY, Wang P, Chu KW, Perlman S, Ali MA, Alnaeem A, Guan Y, Poon LL, Saif L, Peiris M, 2014. Seroepidemiology of Middle East respiratory syndrome (MERS) coronavirus in Saudi Arabia (1993) and Australia (2014) and characterisation of assay specificity. Euro Surveill 19: 2–7.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17.

    Muller MA, Meyer B, Corman VM, Al-Masri M, Turkestani A, Ritz D, Sieberg A, Aldabbagh S, Bosch BJ, Lattwein E, Alhakeem RF, Assiri AM, Albarrak AM, Al-Shangiti AM, Al-Tawfiq JA, Wikramaratna P, Alrabeeah AA, Drosten C, Memish ZA, 2015. Presence of Middle East respiratory syndrome coronavirus antibodies in Saudi Arabia: a nationwide, cross-sectional, serological study. Lancet Infect Dis 15: 629.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Food and Agriculture Organization (FAO), 2001. FAOSTAT Database, 2001. FAO, ed. Available at: http://www.fao.org/faostat/en/data/QA/visualize. Accessed January 1, 2016.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Abroug F, Slim A, Ouanes-Besbes L, Hadj Kacem MA, Dachraoui F, Ouanes I, Lu X, Tao Y, Paden C, Caidi H, Miao C, Al-Hajri MM, Zorraga M, Ghaouar W, BenSalah A, Gerber SI; World Health Organization Global Outbreak Alert and Response Network Middle East Respiratory Syndrome Coronavirus International Investigation Team, 2014. Family cluster of Middle East respiratory syndrome coronavirus infections, Tunisia, 2013. Emerg Infect Dis 20: 1527–1530.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Liljander A, Meyer B, Jores J, Muller MA, Lattwein E, Njeru I, Bett B, Drosten C, Corman VM, 2016. MERS-CoV antibodies in humans, Africa, 2013–2014. Emerg Infect Dis 22: 1086–1089.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Osoro EM, Munyua P, Omulo S, Ogola E, Ade F, Mbatha P, Mbabu M, Ng'ang'a Z, Kairu S, Maritim M, Thumbi SM, Bitek A, Gaichugi S, Rubin C, Njenga K, Guerra M, 2015. Strong association between human and animal Brucella seropositivity in a linked study in Kenya, 2012–2013. Am J Trop Med Hyg 93: 224–231.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    World Health Organization (WHO), 2015. Laboratory Testing for Middle East Respiratory Syndrome Coronavirus (MERS-CoV) Interim Guidance. Available at: http://apps.who.int/iris/bitstream/10665/176982/1/WHO_MERS_LAB_15.1_eng.pdf?ua=1. Accessed June 22, 2016.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Muller MA, Meyer B, Corman VM, Al-Masri M, Turkestani A, Ritz D, Sieberg A, Aldabbagh S, Bosch BJ, Lattwein E, Alhakeem RF, Assiri AM, Albarrak AM, Al-Shangiti AM, Al-Tawfiq JA, Wikramaratna P, Alrabeeah AA, Drosten C, Memish ZA, 2015. Presence of Middle East respiratory syndrome coronavirus antibodies in Saudi Arabia: a nationwide, cross-sectional, serological study. Lancet Infect Dis 15: 559–564.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24.

    Park SW, Perera RA, Choe PG, Lau EH, Choi SJ, Chun JY, Oh HS, Song KH, Bang JH, Kim ES, Kim HB, Park WB, Kim NJ, Poon LL, Peiris M, Oh MD, 2015. Comparison of serological assays in human Middle East respiratory syndrome (MERS)-coronavirus infection. Euro Surveill 20: 13–17.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25.

    Reusken CB, Farag EA, Jonges M, Godeke GJ, El-Sayed AM, Pas SD, Raj VS, Mohran KA, Moussa HA, Ghobashy H, Alhajri F, Ibrahim AK, Bosch BJ, Pasha SK, Al-Romaihi HE, Al-Thani M, Al-Marri SA, AlHajri MM, Haagmans BL, Koopmans MP, 2014. Middle East respiratory syndrome coronavirus (MERS-CoV) RNA and neutralising antibodies in milk collected according to local customs from dromedary camels, Qatar, April 2014. Euro Surveill 19: 8–12.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Al Hammadi ZM, Chu DK, Eltahir YM, Al Hosani F, Al Mulla M, Tarnini W, Hall AJ, Perera RA, Abdelkhalek MM, Peiris JS, Al Muhairi SS, Poon LL, 2015. Asymptomatic MERS-CoV infection in humans possibly linked to infected dromedaries imported from Oman to United Arab Emirates, May 2015. Emerg Infect Dis 21: 2197–2200.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Alshukairi AN, Khalid I, Ahmed WA, Dada AM, Bayumi DT, Malic LS, Althawadi S, Ignacio K, Alsalmi HS, Al-Abdely HM, Wali GY, Qushmaq IA, Alraddadi BM, Perlman S, 2016. Antibody response and disease severity in healthcare worker MERS survivors. Emerg Infect Dis 22: 1113–1115.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Gossner C, Danielson N, Gervelmeyer A, Berthe F, Faye B, Kaasik Aaslav K, Adlhoch C, Zeller H, Penttinen P, Coulombier D, 2016. Human-dromedary camel interactions and the risk of acquiring zoonotic Middle East respiratory syndrome coronavirus infection. Zoonoses Public Health 63: 1–9.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Reeves T, Samy AM, Peterson AT, 2015. MERS-CoV geography and ecology in the Middle East: analyses of reported camel exposures and a preliminary risk map. BMC Res Notes 8: 801.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Faye B, 2013. Camel farming sustainability: the challenges of the camel farming system in the XXIth century. J Sustain Dev 6: 74–82.

Past two years Past Year Past 30 Days
Abstract Views 2174 1885 66
Full Text Views 513 18 0
PDF Downloads 342 19 0
 

 

 

 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save