The coexistence of the Hajj pilgrimage and the swine flu pandemic influenza A (H1N1) in late 2009 inspired an expert conference in Jeddah to predict the potential for an amplification of the virus and an epidemic number of cases during such a mass gathering and to set up a plan to mitigate the transmission of the virus at the Hajj.1 Significant numbers of H1N1 cases had been reported in Saudi Arabia since June 2009, including 15,850 cases with 124 deaths [case fatality rate (CFR) of 0.8%] as of December 30, 2009.2–4 Paradoxically, only 26 cases of H1N1 and no related deaths were reported among Umrah pilgrims in the month of Ramadan (August 22 to September 22, 2009).5 Even more surprisingly, only 73 additional cases of H1N1, including five deaths (CFR 4.9%), were identified during the Hajj among an estimated 2.5 million pilgrims.5 These extremely low numbers, together with a high observed CFR, led Haworth and colleagues to propose that there were many more undetected surviving cases.6 We hypothesized that the low number of H1N1 cases reported during the Hajj of 2009 may have resulted from the effective use of preventive measures against influenza rather than the lack of detection, leading to a reduction in the number of acute respiratory infections due to the H1N1 virus and other etiological agents.
Among a cohort of 274 French pilgrims participating in the 2009 Hajj, 77.4% used hand disinfectant, 89.8% used disposable handkerchiefs, and 79.6% used face masks; 97.4% were vaccinated against seasonal flu, 5.8% against H1N1, and 31.4% against pneumococcus. Influenza vaccine and face mask use did not significantly reduce respiratory symptoms.
Materials and Methods
To test this hypothesis, we conducted an observational study that covered geographically defined French pilgrims participating in the Hajj in 2009. We included 405 individuals departing for Hajj and presenting at the travel clinic of the hospital to receive the compulsory vaccination against meningococcal meningitis between October 7 and November 6, 2009. All pilgrims were administered a pre-travel questionnaire at enrollment that addressed demographics, risk factors for complications from H1N1 virus infection and vaccination status. A total of 274 (response rate of 67.7%) pilgrims were administered a post-travel questionnaire by telephone that addressed compliance with preventive measures against respiratory infections and the occurrence of disease during their 4-week stay in Saudi Arabia and participation in the Hajj ritual. Questionnaires were administered by a French/Arabic-speaking medical doctor. In this study, 131 pilgrims did not participate in the follow-up. Data were captured anonymously in EpiData 3.1 (The EpiData Association; http://www.epidata.dk) and analyzed by Stata 9.2 software (StataCorp LP; http://www.stata.com) using univariate statistics. Risk ratios (RR), according to risk factors and compliance with preventive measures by symptoms, were estimated by logistic regression analysis. The p values were calculated by the Fisher's exact test. A p value ≤0.05 was considered significant.
The majority of the 274 pilgrims originated from North Africa (90.1%) and had not previously visited Saudi Arabia (70.8%). The mean age was 58 years (range 23–83 y), with a male-to-female sex ratio of 1.1. Overall, 49.3% of the pilgrims presented at least one risk factor for complications from H1N1 virus infection, including age over 65 years (26.3%), diabetes mellitus (23.7%), chronic respiratory disease (5.5%), chronic cardiac disease (3.3%), other chronic conditions (2.2%), and pregnancy (0.4%). The vast majority of the pilgrims were vaccinated against seasonal influenza, while only 6% were vaccinated against the H1N1 pandemic influenza; this was likely due to the lack of availability of the H1N1 vaccine in France at that time. These characteristics were similar to that of the whole population of Hajj pilgrims seen for pre-travel advice in our clinic.7 Pre-travel characteristics of the nonresponders did not significantly differ from those of responders.
Most pilgrims reported having used surgical face masks and disposable handkerchiefs, and they practiced good hand hygiene (Table 1). A total of 165 (60.2%) individuals presented with at least one health problem during their stay in Saudi Arabia, including cough (48.5% of all pilgrims), sore throat (36.1%), rhinorrhea (23.7%), sputum (13.5%), shortness of breath (2.9%), voice failure (2.9%), subjective fever (10.9%), myalgia (9.5%), gastrointestinal symptoms (9.5%), and conjunctivitis (0.4%). Influenza-like illness, as defined by the triad of cough, sore throat, and fever, was reported by 22 individuals (8.0%). The onset of respiratory symptoms peaked between November 20 and 26, 2009 (data available in 143 of 161 patients, 88%), just prior to the 5-day Hajj period. Therefore, the majority of individuals had respiratory symptoms during the Hajj. We found that 38 pilgrims with respiratory symptoms were still symptomatic upon returning to France (27%). Five individuals (1.8%) were hospitalized; of these, two had a respiratory tract infection, one had an acute myocardial infarction, one an acute asthma attack, and one individual was hospitalized due to trauma.
|Preventive measure||Number (%)|
|Seasonal flu||267 (97.4%)|
|Pandemic H1N1 influenza||16 (5.8%)|
|Wearing a surgical face mask|
|As usual||83 (30.3%)|
|More frequently than usual||191 (69.7%)|
|Hand disinfectant||212 (77.4%)|
|Disposable handkerchief||246 (89.8%)|
None of the risk factors for complications from H1N1 infection significantly affected the occurrence of respiratory symptoms and fever. None of the preventive measures significantly affected the occurrence of cough, sore throat, rhinorrhea, voice failure, shortness of breath, and gastrointestinal symptoms. Sputum was less frequently reported in individuals using hand disinfectant [9.4% vs 27.4%; RR = 0.28, 95% confidence interval (CI) = 0.13–0.57, p < 0.001] and disposable handkerchiefs (11.0% vs 35.7%; RR = 0.22, 95% CI = 0.09–0.53, p < 0.001); myalgia was less frequently reported in those using hand disinfectant (6.1% vs 20.1%; RR = 0.25, 95% CI = 0.11–0.56, p < 0.001), and fever was less frequently reported in those vaccinated against pneumococcal infections (8.3% vs 14.6%; RR = 0.22, 95% CI = 0.06–0.73, p = 0.007).
Discussions and Conclusion
Of the Jeddah recommendations, the most challenging was that the population groups considered at high risk for complications from influenza should voluntarily refrain from the Hajj of 2009.1 Although our results cannot be extrapolated to all Hajj pilgrims, they clearly indicated that European pilgrims departing from southern France were unlikely to have heeded the recommendations from the expert conference.7 This was mainly due to the effect of the high proportion of older Hajjis with underlying chronic conditions. Several limitations of our study must be acknowledged. Reported symptoms were not specific and may be due to non-influenza respiratory infections. Only testing for influenza at or after Hajj would acquire more accurate data. The reliability of reported symptoms and preventive measures taken by telephone interviews may be questionable, and a significant proportion of the enrolled pilgrims were lost prior follow-up. Nevertheless, our results showed that French pilgrims had significant adherence to individual preventive measures during the Hajj of 2009. While the proportion of French pilgrims who suffered a cough during their stay in Saudi Arabia in 2009 (48.5%) was slightly less than that observed in those participating in the Hajj of 2006 (60.6%) and 2007 (61.1%), when no specific preventive measure was proposed with the exception of the influenza vaccination,8,9 our results suggest that vaccination against influenza and the use of surgical face masks were not efficient against respiratory infections in the context of the 2009 Hajj pilgrimage. Similar results were observed in Malaysian pilgrims during the Hajj of 2007.10 Therefore, these preventive measures probably did not account for the low number of H1N1 cases reported during the Hajj of 2009. Further investigation, including large-scale prospective testing of the effectiveness of preventive measures, particularly surgical face masks and N95 mask use, should be of interest to identify the preventive measures that should be recommended during the pre-travel consultation with future Hajj pilgrims.
The highest percentages of H1N1 cases observed in Saudi Arabia before the Hajj were in individuals under the age of 30, and individuals over the age of 50 were less susceptible to infection by the virus but were more severely affected when infected.2–4 Therefore, the large proportion of older individuals in the Hajj population may have been responsible for the low number of H1N1 cases recorded during the pilgrimage. Finally, as proposed by other authors, it is possible that the low numbers were also due to underreporting.6
We are grateful to Dr C. Gaillard and our medical students for their help in conducting this study. We thank Dr Vanessa Field for her critical review of the manuscript. This document (B508-99E0-D313-5715-2DE3) was edited by American Journal Experts (firstname.lastname@example.org).
Declaration of Interests
The authors state that they have no conflicts of interest to declare.