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. 2013 Oct;57(7):992-1000.
doi: 10.1093/cid/cit446. Epub 2013 Jul 9.

Circulation of respiratory viruses among pilgrims during the 2012 Hajj pilgrimage

Samir Benkouiten  1 , Rémi Charrel, Khadidja Belhouchat, Tassadit Drali, Nicolas Salez, Antoine Nougairede, Christine Zandotti, Ziad A Memish, Malak al Masri, Catherine Gaillard, Philippe Parola, Philippe Brouqui, Philippe Gautret
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Circulation of respiratory viruses among pilgrims during the 2012 Hajj pilgrimage

Samir Benkouiten et al. Clin Infect Dis. .
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Abstract

Background: The Hajj is the oldest and largest annual mass gathering in the world and may increase the risk of spread of respiratory viruses.

Methods: We performed a prospective survey among a cohort of pilgrims departing from Marseille, France, to Mecca in the Kingdom of Saudi Arabia (KSA) for the 2012 Hajj season. Nasal swabs were collected from participants and tested for 11 respiratory viruses by real-time reverse transcription polymerase chain reaction.

Results: Of 165 participants sampled before departing to the KSA, 8 (4.8%) were positive for at least 1 virus (5 rhinovirus, 1 influenza C, 1 adenovirus, and 1 enterovirus). Seventy symptomatic pilgrims underwent additional nasal swabs during their pilgrimage in the KSA, of which 27 (38.6%) were positive for at least 1 virus (19 rhinovirus, 6 influenza A, 1 influenza C, 1 respiratory syncytial virus B, 1 metapneumovirus, 1 adenovirus, and 1 enterovirus). This was significantly higher than the 4.8% who were positive before departing for the KSA (P < .001). Of 154 pilgrims sampled before leaving the KSA, 17 (11%) were positive for at least 1 virus (13 rhinovirus, 3 adenovirus, 2 influenza B, and 1 enterovirus), which was also significantly higher than the percentage of positive pilgrims (4.8%), before departing for the KSA (P = .040).

Conclusions: This study suggests a rapid acquisition of respiratory viruses among pilgrims during their stay in the KSA, most notably rhinovirus, and highlights the potential of spreading these infections in the pilgrims' home countries upon their return.

Keywords: Hajj; cohort study; epidemiology; respiratory tract infections; viruses.

Figures

Figure 1.
Overview of the Hajj pilgrimage route. 1: Circumambulating the Kaaba (first Tawaf) at the Great Mosque, in Mecca. 2: Staying at the Mina tent encampment. 3: Standing prayer in the valley of Arafat. 4: Gathering stones at Muzdalifah. 5: Stoning the Devil at the Jamaraat pillars in Mina. 6: Circumambulating the Kaaba again (second Tawaf) in Mecca. 7: Visiting the Mosque of the Prophet at Medina.
Figure 2.
Patterns of respiratory viruses detected before departing to the Kingdom of Saudi Arabia (KSA). A, Numbers of pilgrims sampled before departing to the KSA with detection rate of total respiratory viruses. B, Daily numbers of cases of respiratory viruses detected before departing to the KSA. Mean time of storage at 20°C was 13 days (range, 5–37 days) for the 146 pre-Hajj samples (88.5%) collected in the month before departing from France. The 19 pre-Hajj samples (11.5%) collected on the day of departure from France (at the airport) were stored at 20°C for 30 days after the collection date. Abbreviations: FLUC, influenza C virus; HAdV, human adenovirus; HEV, human enterovirus; HRV, human rhinovirus.
Figure 3.
Patterns of reported respiratory symptoms and respiratory viruses detected during the stay in the Kingdom of Saudi Arabia (KSA). A, The respiratory symptoms reported by pilgrims during the stay in the KSA. B, Numbers of pilgrims sampled during the stay in the KSA with detection rate of total respiratory viruses. C, Daily numbers of cases of respiratory viruses detected during the stay in the KSA. Mean time of storage at 20°C was 22 days (range, 10–27 days) for samples collected in ill pilgrims during the pilgrimage in the KSA, and 6 days (range, 5–8 days) for post-Hajj samples collected just before leaving the KSA. 1: Arrival at Jeddah airport (afternoon) then Mecca (night). 2: Mecca. 3: Mecca then Mina (afternoon). 4: Arafat (morning) then Muzdalifah (night). 5: Muzdalifah then Mina (morning). 6: Mina, Mecca (morning) then Mina. 7: Mina. 8: Mina. 9: Medina (morning). 10: Departure from Jeddah airport. Abbreviations: FLUA, influenza A virus; FLUB, influenza B virus; FLUC, influenza C virus; HAdV, human adenovirus; HEV, human enterovirus; HMPV, human metapneumovirus; HRV, human rhinovirus; KSA, Kingdom of Saudi Arabia; RSVB, human respiratory syncytial virus B.
Figure 4.
The respiratory viruses detected among the Hajj pilgrims who tested positive during the study period. Abbreviations: FLUA, influenza A virus; FLUB, influenza B virus; FLUC, influenza C virus; H1N1, influenza A/2009/H1N1 virus; HAdV, human adenovirus; HEV, human enterovirus; HMPV, human metapneumovirus; HRV, human rhinovirus; KSA, Kingdom of Saudi Arabia; MS2, MS2 bacteriophage; RSVA, human respiratory syncytial virus A; RSVB, human respiratory syncytial virus B.
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