Respiratory Viruses and Bacteria among Pilgrims during the 2013 Hajj - Volume 20, Number 11—November 2014 - Emerging Infectious Disease journal - CDC

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Respiratory Viruses and Bacteria among Pilgrims during the 2013 Hajj - Volume 20, Number 11—November 2014 - Emerging Infectious Disease journal - CDC

Volume 20, Number 11—November 2014

Research

Respiratory Viruses and Bacteria among Pilgrims during the 2013 Hajj

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• Discussion
• Suggested Citation

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• Figure 2

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Samir Benkouiten, Rémi Charrel, Khadidja Belhouchat, Tassadit Drali, Antoine Nougairede, Nicolas Salez, Ziad A. Memish, Malak al Masri, Pierre-Edouard Fournier, Didier Raoult, Philippe Brouqui, Philippe Parola, and Philippe Gautret 

Author affiliations: Aix Marseille Université, Marseille, France (S. Benkouiten, R. Charrel, K. Belhouchat, T. Drali, A. Nougairede, N. Salez, P.-E. Fournier, D. Raoult, P. Brouqui, P. Parola, P. Gautret); Institut Hospitalo-Universitaire Méditerranée, Marseille (S. Benkouiten, R. Charrel, A. Nougairede, N. Salez, P.-E. Fournier, D. Raoult, P. Brouqui, P. Parola, P. Gautret); Saudi Ministry of Health, Riyadh, Saudi Arabia (Z.A. Memish, M. al Masri); Alfaisal University College of Medicine, Riyadh (Z.A. Memish)

Suggested citation for this article

Abstract

Pilgrims returning from the Hajj might contribute to international spreading of respiratory pathogens. Nasal and throat swab specimens were obtained from 129 pilgrims in 2013 before they departed from France and before they left Saudi Arabia, and tested by PCR for respiratory viruses and bacteria. Overall, 21.5% and 38.8% of pre-Hajj and post-Hajj specimens, respectively, were positive for ≥1 virus (p = 0.003). One third (29.8%) of the participants acquired ≥1 virus, particularly rhinovirus (14.0%), coronavirus E229 (12.4%), and influenza A(H3N2) virus (6.2%) while in Saudi Arabia. None of the participants were positive for the Middle East respiratory syndrome coronavirus. In addition, 50.0% and 62.0% of pre-Hajj and post-Hajj specimens, respectively, were positive for Streptococcus pneumoniae (p = 0.053). One third (36.3%) of the participants had acquired S. pneumoniae during their stay. Our results confirm high acquisition rates of rhinovirus and S. pneumoniae in pilgrims and highlight the acquisition of coronavirus E229.

More than 2 million Muslims gather annually in Saudi Arabia for a pilgrimage to the holy places of Islam known as the Hajj. The Hajj presents major public health and infection control challenges. Inevitable overcrowding within a confined area with persons from >180 countries in close contact with others, particularly during the circumambulation of the Kaaba (Tawaf) inside the Grand Mosque in Mecca, leads to a high risk pilgrims to acquire and spread infectious diseases during their time in Saudi Arabia (1), particularly respiratory diseases (2). Respiratory diseases are a major cause of consultation in primary health care facilities in Mina, Saudi Arabia, during the Hajj (3). Pneumonia is a leading cause of hospitalization in intensive care units (4).

Numerous studies have shown a high prevalence of respiratory symptoms among pilgrims (5–7). Respiratory viruses, especially influenza virus, are the most common cause of acute respiratory infections among pilgrims (8–11). We recently reported the acquisition of rhinovirus (5) and Streptococcus pneumoniae infections (12) by French pilgrims during the 2012 Hajj season and highlighted the potential for spread of these infections to home countries of pilgrims upon their return. However, none of the French pilgrims were positive for Middle East respiratory syndrome coronavirus (MERS-CoV) in 2012 (13) and 2013 (14).

In this study, we collected paired nasal and throat swab specimens from adult pilgrims departing from Marseille, France to Mecca, Saudi Arabia, for the 2013 Hajj season. The primary objective was to determine the prevalence of the most common respiratory viruses and bacteria upon return of pilgrims from the Hajj. The secondary objective was to evaluate the potential yearly variation of the acquisition of these respiratory pathogens by comparing results from the 2012 and 2013 Hajj seasons.

Dr Benkouiten is a researcher at the Institut Hospitalo–Universitaire Méditerranée Infection, Marseille, France. His research interests focus on the epidemiology of respiratory infections in the context of mass gatherings.

Acknowledgment

This study was supported by The Marseille Public Hospitals Authority.

References

1. Ahmed QA, Arabi YM, Memish ZA. Health risks at the Hajj. Lancet. 2006;367:1008–15. DOIPubMed
2. Alzeer AH. Respiratory tract infection during Hajj. Ann Thorac Med. 2009;4:50–3. DOIPubMed
3. Alzahrani AG, Choudhry AJ, Al Mazroa MA, Turkistani AH, Nouman GS, Memish ZA. Pattern of diseases among visitors to Mina health centers during the Hajj season, 1429 H (2008 G). J Infect Public Health. 2012;5:22–34. DOIPubMed
4. Mandourah Y, Al-Radi A, Ocheltree AH, Ocheltree SR, Fowler RA. Clinical and temporal patterns of severe pneumonia causing critical illness during Hajj. BMC Infect Dis. 2012;12:117. DOIPubMed
5. Benkouiten S, Charrel R, Belhouchat K, Drali T, Salez N, Nougairede A, Circulation of respiratory viruses among pilgrims during the 2012 Hajj pilgrimage. Clin Infect Dis. 2013;57:992–1000. DOIPubMed
6. Meysamie A, Ardakani HZ, Razavi SM, Doroodi T. Comparison of mortality and morbidity rates among Iranian pilgrims in Hajj 2004 and 2005. Saudi Med J. 2006;27:1049–53 .PubMed
7. Deris ZZ, Hasan H, Sulaiman SA, Wahab MS, Naing NN, Othman NH. The prevalence of acute respiratory symptoms and role of protective measures among Malaysian hajj pilgrims. J Travel Med. 2010;17:82–8. DOIPubMed
8. Balkhy HH, Memish ZA, Bafaqeer S, Almuneef MA. Influenza a common viral infection among Hajj pilgrims: time for routine surveillance and vaccination. J Travel Med. 2004;11:82–6. DOIPubMed
9. Rashid H, Shafi S, Booy R, El Bashir H, Ali K, Zambon M, Influenza and respiratory syncytial virus infections in British Hajj pilgrims. Emerg Health Threats J. 2008;1:e2.
10. Moattari A, Emami A, Moghadami M, Honarvar B. Influenza viral infections among the Iranian Hajj pilgrims returning to Shiraz, Fars province, Iran. Influenza Other Respir Viruses. 2012;6:e77–9.
11. Memish ZA, Assiri AM, Hussain R, Alomar I, Stephens G. Detection of respiratory viruses among pilgrims in Saudi Arabia during the time of a declared influenza A(H1N1) pandemic. J Travel Med. 2012;19:15–21. DOIPubMed
12. Benkouiten S, Gautret P, Belhouchat K, Drali T, Salez N, Memish ZA, Acquisition of Streptococcus pneumoniae carriage in pilgrims during the 2012 Hajj pilgrimage. Clin Infect Dis. 2014;58:e106–9. DOIPubMed
13. Gautret P, Charrel R, Belhouchat K, Drali T, Benkouiten S, Nougairede A, Lack of nasal carriage of novel corona virus (HCoV-EMC) in French Hajj pilgrims returning from the Hajj 2012, despite a high rate of respiratory symptoms. Clin Microbiol Infect. 2013;19:E315–7. DOIPubMed
14. Gautret P, Charrel R, Benkouiten S, Belhouchat K, Nougairede A, Drali T, Lack of MERS coronavirus but prevalence of influenza virus in French pilgrims after 2013 Hajj. Emerg Infect Dis. 2014;20:728–30. DOIPubMed
15. Rashid H, Shafi S, El Bashir H, Haworth E, Memish ZA, Ali KA, Influenza and the Hajj: defining influenza-like illness clinically. Int J Infect Dis.2008;12:102–3. DOIPubMed
16. van Elden LJ, Nijhuis M, Schipper P, Schuurman R, van Loon AM. Simultaneous detection of influenza viruses A and B using real-time quantitative PCR. J Clin Microbiol. 2001;39:196–200. DOIPubMed
17. Faux C. Influenza type C. PCR methodology. In: Schuller M, Sloots TP, James GS, Halliday CL, Carter IW, editors. PCR for clinical microbiology: an Australian and international perspective. London: Springer; 2010. p. 311–2.
18. Duchamp MB, Casalegno JS, Gillet Y, Frobert E, Bernard E, Escuret V, Pandemic A(H1N1)2009 influenza virus detection by real time RT-PCR: is viral quantification useful? Clin Microbiol Infect. 2010;16:317–21. DOIPubMed
19. Heim A, Ebnet C, Harste G, Pring-Akerblom P. Rapid and quantitative detection of human adenovirus DNA by real-time PCR. J Med Virol.2003;70:228–39. DOIPubMed
20. Lu X, Chittaganpitch M, Olsen SJ, Mackay IM, Sloots TP, Fry AM, Real-time PCR assays for detection of bocavirus in human specimens. J Clin Microbiol. 2006;44:3231–5. DOIPubMed
21. Griscelli F, Barrois M, Chauvin S, Lastere S, Bellet D, Bourhis JH. Quantification of human cytomegalovirus DNA in bone marrow transplant recipients by real-time PCR. J Clin Microbiol. 2001;39:4362–9. DOIPubMed
22. Tan CY, Ninove L, Gaudart J, Nougairede A, Zandotti C, Thirion-Perrier L, A retrospective overview of enterovirus infection diagnosis and molecular epidemiology in the public hospitals of Marseille, France (1985–2005). PLoS ONE. 2011;6:e18022. DOIPubMed
23. Maertzdorf J, Wang CK, Brown JB, Quinto JD, Chu M, de Graaf M, Real-time reverse transcriptase PCR assay for detection of human metapneumoviruses from all known genetic lineages. J Clin Microbiol. 2004;42:981–6. DOIPubMed
24. Bennett S, Harvala H, Witteveldt J, McWilliam Leitch EC, McLeish N, Templeton K, Rapid simultaneous detection of enterovirus and parechovirus RNAs in clinical samples by one-step real-time reverse transcription-PCR assay. J Clin Microbiol. 2011;49:2620–4 and. DOIPubMed
25. van Elden LJ, van Loon AM, van der Beek A, Hendriksen KA, Hoepelman AI, van Kraaij MG, Applicability of a real-time quantitative PCR assay for diagnosis of respiratory syncytial virus infection in immunocompromised adults. J Clin Microbiol. 2003;41:4378–81. DOIPubMed
26. Lu X, Holloway B, Dare RK, Kuypers J, Yagi S, Williams JV, Real-time reverse transcription-PCR assay for comprehensive detection of human rhinoviruses. J Clin Microbiol. 2008;46:533–9. DOIPubMed
27. Pillet S, Lardeux M, Dina J, Grattard F, Verhoeven P, Le Goff J, Comparative evaluation of six commercialized multiplex PCR kits for the diagnosis of respiratory infections. PLoS ONE. 2013;8:e72174. DOIPubMed
28. Cohen-Bacrie S, Ninove L, Nougairède A, Charrel R, Richet H, Minodier P, Revolutionizing clinical microbiology laboratory organization in hospitals with in situ point-of-care. PLoS ONE. 2011;6:e22403. DOIPubMed
29. Memish ZA, Assiri A, Almasri M, Alhakeem RF, Turkestani A, Al Rabeeah AA, Prevalence of MERS-CoV nasal carriage and compliance with the Saudi health recommendations among pilgrims attending the 2013 Hajj. J Infect Dis. 2014. In press and. DOIPubMed
30. Jacobs SE, Lamson DM, St George K, Walsh TJ. Human rhinoviruses. Clin Microbiol Rev. 2013;26:135–62. DOIPubMed
31. Graham RL, Donaldson EF, Baric RS. A decade after SARS: strategies for controlling emerging coronaviruses. Nat Rev Microbiol. 2013;11:836–48.DOIPubMed

Figures

• Figure 1. Patterns of respiratory viruses detected among 64 pilgrims who were positive for viruses during the study period before departing from France and before leaving Saudi Arabia, 2013 Hajj. FLUA,...
• Figure 2. Detection of Streptococcus pneumoniae among 92 pilgrims who were positive for viruses during the study period before departing from France and before leaving Saudi Arabia, 2013 Hajj.

Tables

• Table 1. Demographic and baseline characteristics of pilgrims during the 2012 and 2013 Hajj
• Table 2. Prevalence of respiratory viruses and bacteria among participants before departing from France and before leaving Saudi Arabia, 2012 and 2013 Hajj

Suggested citation for this article: Benkouiten S, Charrel R, Belhouchat K, Drali T, Nougairede A, Salez N, et al. Respiratory viruses and bacteria among pilgrims during the 2013 Hajj. Emerg Infect Dis [Internet]. 2011 Nov [date cited]. http://dx.doi.org/10.3201/eid2011.140600

DOI: 10.3201/eid2011.140600