Hajj: infectious disease surveillance and control.

Religious festivals attract a large number of pilgrims from worldwide and are a potential risk for the transmission of infectious diseases between pilgrims, and to the indigenous population. The gathering of a large number of pilgrims could compromise the health system of the host country. The threat to global health security posed by infectious diseases with epidemic potential shows the importance of advanced planning of public health surveillance and response at these religious events. Saudi Arabia has extensive experience of providing health care at mass gatherings acquired through decades of managing millions of pilgrims at the Hajj. In this report, we describe the extensive public health planning, surveillance systems used to monitor public health risks, and health services provided and accessed during Hajj 2012 and Hajj 2013 that together attracted more than 5 million pilgrims from 184 countries. We also describe the recent establishment of the Global Center for Mass Gathering Medicine, a Saudi Government partnership with the WHO Collaborating Centre for Mass Gatherings Medicine, Gulf Co-operation Council states, UK universities, and public health institutions globally.

Prevalence of MERS-CoV nasal carriage and compliance with the Saudi health recommendations among pilgrims attending the 2013 Hajj.

BACKGROUND: Annually, Saudi Arabia is the host of the Hajj mass gathering. We aimed to determine the Middle East respiratory syndrome coronavirus (MERS-CoV) nasal carriage rate among pilgrims performing the 2013 Hajj and to describe the compliance with the Saudi Ministry of Health vaccine recommendations. METHOD: Nasopharyngeal samples were collected from 5235 adult pilgrims from 22 countries and screened for MERS-CoV using reverse transcriptase-polymerase chain reaction. Information regarding the participants' age, gender, country of origin, medical conditions, and vaccination history were obtained. RESULTS: The mean age of the screened population was 51.8 years (range, 18-93 years) with a male/female ratio of 1.17:1. MERS-CoV was not detected in any of the samples tested (3210 pre-Hajj and 2025 post-Hajj screening). According to the vaccination documents, all participants had received meningococcal vaccination and the majority of those from at-risk countries were vaccinated against yellow fever and polio. Only 22% of the pilgrims (17.5% of those ≥65 years and 36.3% of diabetics) had flu vaccination, and 4.4% had pneumococcal vaccination. CONCLUSION: There was no evidence of MERS-CoV nasal carriage among Hajj pilgrims. While rates of compulsory vaccinations uptake were high, uptake of pneumococcal and flu seasonal vaccinations were low, including among the high-risk population.

Hajj abattoirs in Makkah: risk of zoonotic infections among occupational workers.

At completion of Hajj, the Islamic pilgrimage to Makkah, pilgrims give thanks for the blessing, and acceptance, of Hajj, marking the end of the pilgrimage by sacrificing an animal and distributing the sacrificial meat to the poor. With over two million Muslims making Hajj, each Hajj, more than 1.2 million heads of cattle: sheep, goats and camels are slaughtered. Over 16 000 abattoir workers work around the clock to sacrifice and process the cattle in keeping with Islamic law and public health guidelines. Because of their proximity to high densities of cattle and cattle meat, Makkah's abattoir workers are at risk of zoonosis. This was a longitudinal study aimed at determining the risk of some zoonotic diseases among male permanent abattoir workers during Hajj. Specifically, seroprevalence of antigens for Brucella, Crimean-Congo haemorrhagic fever (CCHF), Alkhurma haemorrhagic fever (AHF) and Rift Valley Fever (RVF) were determined, among the study participants. An enrolment questionnaire, and a follow-up questionnaire, with provision of 10 mL blood for testing 2 days before intense Hajj animal exposure, up to 20 days after intense animal exposure and between 30 and 42 days after Hajj butchering exposures. While working with livestock, study participants were interrogated on hand hygiene and personal protection. Eighty male permanent abattoir workers participated in the study. Majority, 96.25% (n = 77) declared washing their hands with soap and water, most 98.75% (n = 79) never used eye protection, few occupational workers dressed in personal protective clothing or footwear. All workers tested negative for CCHF and RVF, one was positive for AHF and six for Brucella. The risk of some zoonotic infections like Brucella and AHF is low among permanent occupational workers in the slaughtering house in Makkah during Hajj 2013. No serological evidence for CCHF and RVF viruses, even though workers showed low compliance with use of personnel protective equipment.

Strengthening health security at the Hajj mass gatherings: characteristics of the infectious diseases surveillance systems operational during the 2015 Hajj.

BACKGROUND: Hajj is one of the largest and the most ethnically and culturally diverse mass gatherings worldwide. The use of appropriate surveillance systems ensures timely information management for effective planning and response to infectious diseases threats during the pilgrimage. The literature describes infectious diseases prevention and control strategies for Hajj but with limited information on the operations and characteristics of the existing Hajj infectious diseases surveillance systems. METHOD: We reviewed documents, including guidelines and reports from the Saudi Ministry of Health's database, to describe the characteristics of the infectious diseases surveillance systems that were operational during the 2015 Hajj, highlighting best practices and gaps and proposing strategies for strengthening and improvement. Using Pubmed and Embase online search engines and a combination of search terms including, 'mass gatherings' 'Olympics' 'surveillance' 'Hajj' 'health security', we explored the existing literature and highlighted some lessons learnt from other international mass gatherings. RESULTS: A regular indicator-based infectious disease surveillance system generates routine reports from health facilities within the Kingdom to the regional and central public health directorates all year round. During Hajj, enhanced indicator-based notifiable diseases surveillance systems complement the existing surveillance tool to ensure timely reporting of event information for appropriate action by public health officials. CONCLUSION: There is need to integrate the existing Hajj surveillance data management systems and to implement syndromic surveillance as an early warning system for infectious disease control during Hajj. International engagement is important to strengthen Hajj infectious diseases surveillance and to prevent disease transmission and globalization of infectious agents which could undermine global health security.

A cohort study of the impact and acquisition of naspharyngeal carriage of Streptococcus pneumoniae during the Hajj.

BACKGROUND: The annual Muslim pilgrimage attracts over two million pilgrims who gather in a limited time and space. The pilgrimage carries the potential risk of increase risk of the acquisition of Streptococcus pneumonia. In this cohort study, we evaluate the effect of the Hajj on the prevalence of pneumococcal serotype nasopharyngeal carriage in the Hajj pilgrim population. The secondary objective is to evaluate the effects of the mass gathering on carriage of invasive pneumococcal serotypes. METHODS: This is a prospective cohort study with two data collection periods: at the beginning and at the end of the Hajj. Nasopharyngeal samples were taken via a standardized swabbing method. RESULTS: A total of 1175 pilgrims were enrolled at the beginning of the study and 1155 (98.3%) were included at the second part of the study. The pre-Hajj samples were obtained at a mean of 0 days and the post-Hajj sampling occurred at a mean of 15 days after arrival to Saudi Arabia. The overall carriage rate of Streptococcus pneumoniae in the pre- and post-Hajj was 1.8% and 7.1% (P = 0.0016). The potential coverage of the 7-valent pneumococcal conjugate vaccine (PCV7), PCV10 and PCV13 were 15.5%, 19.1%; and 35.5%, respectively. The coverage for the 23-valent pneumococcal polysaccharide vaccine (PPV23) was 40%. CONCLUSION: Although there was an increase in the acquisition of S. pneumoniae, its magnitude is low which does not support public health recommendations for general pneumococcal vaccination of pilgrims except those at risk.

Presence of Middle East respiratory syndrome coronavirus antibodies in Saudi Arabia: a nationwide, cross-sectional, serological study.

BACKGROUND: Scientific evidence suggests that dromedary camels are the intermediary host for the Middle East respiratory syndrome coronavirus (MERS-CoV). However, the actual number of infections in people who have had contact with camels is unknown and most index patients cannot recall any such contact. We aimed to do a nationwide serosurvey in Saudi Arabia to establish the prevalence of MERS-CoV antibodies, both in the general population and in populations of individuals who have maximum exposure to camels. METHODS: In the cross-sectional serosurvey, we tested human serum samples obtained from healthy individuals older than 15 years who attended primary health-care centres or participated in a national burden-of-disease study in all 13 provinces of Saudi Arabia. Additionally, we tested serum samples from shepherds and abattoir workers with occupational exposure to camels. Samples were screened by recombinant ELISA and MERS-CoV seropositivity was confirmed by recombinant immunofluorescence and plaque reduction neutralisation tests. We used two-tailed Mann Whitney U exact tests, χ(2), and Fisher's exact tests to analyse the data. FINDINGS: Between Dec 1, 2012, and Dec 1, 2013, we obtained individual serum samples from 10,009 individuals. Anti-MERS-CoV antibodies were confirmed in 15 (0·15%; 95% CI 0·09-0·24) of 10,009 people in six of the 13 provinces. The mean age of seropositive individuals was significantly younger than that of patients with reported, laboratory-confirmed, primary Middle Eastern respiratory syndrome (43·5 years [SD 17·3] vs 53·8 years [17·5]; p=0·008). Men had a higher antibody prevalence than did women (11 [0·25%] of 4341 vs two [0·05%] of 4378; p=0·028) and antibody prevalence was significantly higher in central versus coastal provinces (14 [0·26%] of 5479 vs one [0·02%] of 4529; p=0·003). Compared with the general population, seroprevalence of MERS-CoV antibodies was significantly increased by 15 times in shepherds (two [2·3%] of 87, p=0·0004) and by 23 times in slaughterhouse workers (five [3·6%] of 140; p<0·0001). INTERPRETATION: Seroprevalence of MERS-CoV antibodies was significantly higher in camel-exposed individuals than in the general population. By simple multiplication, a projected 44,951 (95% CI 26,971-71,922) individuals older than 15 years might be seropositive for MERS-CoV in Saudi Arabia. These individuals might be the source of infection for patients with confirmed MERS who had no previous exposure to camels. FUNDING: European Union, German Centre for Infection Research, Federal Ministry of Education and Research, German Research Council, and Ministry of Health of Saudi Arabia.

Etiology of severe community-acquired pneumonia during the 2013 Hajj-part of the MERS-CoV surveillance program.

BACKGROUND: Pneumonia is the leading cause of hospital admission during the annual Islamic pilgrimage (Hajj). The etiology of severe pneumonia is complex and includes the newly emerged Middle East respiratory syndrome coronavirus (MERS-CoV). Since 2012, the Saudi Ministry of Health (MoH) has required screening for MERS-CoV for all cases of severe pneumonia requiring hospitalization. We aimed to screen Hajj pilgrims admitted to healthcare facilities in 2013 with severe community-acquired pneumonia (CAP) for MERS-CoV and to determine other etiologies. METHODS: Sputum samples were collected from all pilgrims admitted to 15 healthcare facilities in the cities of Makkah and Medina, Saudi Arabia, who were diagnosed with severe CAP on admission, presenting with bilateral pneumonia. The medical records were reviewed to collect information on age, gender, nationality, and patient outcome. Samples were screened for MERS-CoV by PCR, and a respiratory multiplex array was used to detect up to 22 other viral and bacterial respiratory pathogens. RESULTS: Thirty-eight patients met the inclusion criteria; they were predominantly elderly (mean age 58.6 years, range 25-83 years) and male (68.4%), and all were from developing countries. Fourteen of the 38 patients died (36.8%). MERS-CoV was not detected in any of the samples. Other respiratory pathogens were detected in 26 (68.4%) samples. Of these, bacterial pathogens were detected in 84.6% (22/26) and viruses in 80.7% (21/26). Twenty-one (80.7%) samples were positive for more than one respiratory pathogen and 17 (65.3%) were positive for both bacteria and viruses. The most common respiratory virus was human rhinovirus, detected in 57.7% of the positive samples, followed by influenza A virus (23.1%) and human coronaviruses (19.2%). Haemophilus influenzae and Streptococcus pneumoniae were the predominant bacteria, detected in 57.7% and 53.8%, respectively, of the positive samples, followed by Moraxella catarrhalis (36.4%). CONCLUSIONS: MERS-CoV was not the cause of severe CAP in any of the hospitalized pilgrims investigated. However we identified a variety of other respiratory pathogens in the sputum of this small number of patients. This indicates that the etiology of severe CAP in Hajj is complex with implications regarding its management.

Meningococcal serogroup A, C, W, and Y serum bactericidal antibody profiles in Hajj pilgrims.

BACKGROUND: The religious seasons of Hajj and Umra in the Kingdom of Saudi Arabia (KSA) have historically been associated with epidemics of meningococcal disease. Due to the effective preventive measures taken in recent years, including vaccination, no meningococcal outbreaks have been reported during Hajj or were Hajj-associated. However, little is known about the immunological profile of pilgrims. The aim of this study was to assess the immunological profile of pilgrims on arrival in KSA against the four meningococcal serogroups, A, C, W, and Y, contained within the quadrivalent vaccine. METHODS: Following consent, socio-demographic factors and health-related information was collected from pilgrims arriving at King Abdul Aziz International Airport and a blood sample taken. Antibodies were quantified by serum bactericidal antibody assay using baby rabbit complement (rSBA) against the four meningococcal serogroups, A, C, W, and Y. RESULTS: Serum samples were collected from 796 pilgrims; rSBA results were obtained for all four serogroups for 741 of these samples. A total of 48 (6.5%) Hajjis had previously attended Hajj, ranging from 1 to 14 times (median 2 times); 98.2% had received meningococcal quadrivalent vaccine in the last 3 years. Of the 13 who had not, all originated from Bangladesh, with four reporting no previous meningococcal vaccination and nine reporting having received the vaccination more than 3 years ago. For serogroup A, only one pilgrim from Indonesia had an rSBA titre <8. For serogroups C, W, and Y, the percentages of pilgrims with rSBA titres <8 were 9.9%, 17.4%, and 9.4%, respectively. Of note was the high prevalence of non-complement-mediated lysis in pilgrims originating from Nigeria (28/47; 59.6%) and Afghanistan (21/47; 44.7%), but not the other countries. This may be a reflection of the type and pattern of antibiotic usage among these communities. CONCLUSION: The vast majority of pilgrims are vaccinated and protected against meningococcal serogroups A, C, W, and Y.

Demographic distribution and transmission potential of influenza A and 2009 pandemic influenza A H1N1 in pilgrims.

INTRODUCTION: The World Health Organization's persistent reporting of global outbreaks of influenza A viruses, including the 2009 pandemic swine A H1N1 strain (H1N1pdm09), justified the targeted surveillance of pilgrims during their annual congregation that pools more than two million people from around 165 nations in a confined area of Makkah city in the Kingdom of Saudi Arabia (KSA). METHODOLOGY: A total of 1,600 pilgrims were included in the targeted surveillance of influenza A and the 2009 pandemic swine H1N1 strain in the Hajj (pilgrimage) season of 2010. Each pilgrim responded to a demographic and health questionnaire. Collected oropharyngeal swabs were analyzed by real-time PCR for influenza A viruses, and positive samples were further analyzed for the presence of H1N1pdm09. Fisher's exact test was applied in the analysis of the significance of the distribution of influenza-positive pilgrims according to demographic characters. RESULTS: A total of 120 pilgrims (7.5%) tested positive for influenza A viruses by real-time PCR. Nine out of the 120 influenza-A-positive pilgrims (7.5%) were positive for H1N1pdm09. Demographics played a significant role in those pilgrims who tested positive for influenza A. CONCLUSIONS: The detection of H1N1pdm09 in pilgrims at their port of entry to the KSA was alarming, due to the high potential of trans-boundary transmission. This situation necessitates the implementation of specific prevention and control programs to limit infection by influenza A viruses.