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Travel epidemiology: the Saudi perspective
International Journal of Antimicrobial Agents 21 (2003) 96 /101 www.isochem.org
Travel epidemiology: the Saudi perspective Ziad A. Memish a,b,*, S. Venkatesh c, Qanta A. Ahmed d a
Department of Medicine, King Abdulaziz Medical City, King Fahad National Guard Hospital, P.O. Box 22490, Riyadh 11426, Saudi Arabia Department of Infection Prevention and Control, King Abdulaziz Medical City, King Fahad National Guard Hospital, P.O. Box 22490, Riyadh 11426, Saudi Arabia c Department of Medical Affairs, King Abdulaziz Medical City, King Fahad National Guard Hospital, P.O. Box 22490, Riyadh 11426, Saudi Arabia d Respiratory Medicine, Royal Berkshire and Battle Hospitals, Reading, UK
b
Abstract The Kingdom of Saudi Arabia occupies four-fifths of the Arabian Peninsula, with a land area of 2 million square kilometres. Saudi Arabia holds a unique position in the Islamic world, as the custodian of the two holiest places of Islam, in Mecca and Medina. Annually, some 2 million Muslims from over 140 countries embark on Hajj. This extraordinary en masse migration is a unique forum for the study of travel epidemiology since the Hajj carries various health risks, both communicable and non-communicable, often on a colossal scale. Non-communicable hazards of the Hajj include stampede and motor vehicle trauma, fire-related burn injuries and accidental hand injury during animal slaughter. Communicable hazards in the form of outbreaks of multiple infectious diseases have been reported repeatedly, during and following the Hajj. Meningococcal meningitis, gastroenteritis, hepatitis A, B and C, and various zoonotic diseases comprise some of the possible infectious hazards at the Hajj. Many of these infectious and noninfectious hazards can be avoided or averted by adopting appropriate prophylactic measures. Physicians and health personnel must be aware of these risks to appropriately educate, immunize and prepare these travellers facing the unique epidemiological challenges of Hajj in an effort to minimize untoward effects. Travel epidemiology related to the Hajj is a new and exciting area, which offers valuable insights to the travel specialist. The sheer scale of numbers affords a rare view of migration medicine in action. As data is continually gathered and both national and international policy making is tailored to vital insights gained through travel epidemiology, the Hajj will be continually safeguarded. Practitioners will gain from findings of travel related epidemiological changes in evolution at the Hajj: the impact of vaccinating policies, infection control policies and public health are afforded a real-world laboratory setting at each annual Hajj, allowing us to learn from this unique phenomenon of migration medicine. # 2002 Elsevier Science B.V. and the International Society of Chemotherapy. All rights reserved. Keywords: Saudi Arabia; Hajj; Infectious diseases; Non-infectious hazards; Travel
1. Introduction The Kingdom of Saudi Arabia occupies four-fifths of the Arabian Peninsula, with a land area of about 2 million square kilometres (900 000 square miles) [1]. The largest and most populated of the six Gulf Cooperation Council (GCC) states in the Middle East, Saudi Arabia is bounded by the Persian Gulf in the East and the Red Sea in the West (Fig. 1). Of its estimated 22 million population, which includes 5.3 million expatriates, three-fourths live in urban areas. Nomadic Bedouins
* Corresponding author. Tel.: /966-01-2520088x3718; fax: /96601-2520437. E-mail address: [email protected] (Z.A. Memish).
form 7% of the rural populace. Saudi Arabia has a desert climate with the temperature reaching around 55 8C in summer months. Saudi Arabia has an advanced health care system. The World Health Organization has recognized its health programmes as an exemplary health care model for developing nations and ranks it 26th of 176 nations in overall health system performance [2]. The Saudi Arabian Ministry of Health provides 60% of the health care services and operates 188 hospitals, with a cumulative bed count of 27 994. Additionally the MOH runs 1766 Primary Health Care centres throughout the Kingdom. Other important health care providers in Saudi Arabia include the fast-growing private sector (20%), military organizations (13%) and teaching hospi-
0924-8579/02/$30 # 2002 Elsevier Science B.V. and the International Society of Chemotherapy. All rights reserved. PII: S 0 9 2 4 - 8 5 7 9 ( 0 2 ) 0 0 3 6 4 - 3
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pilgrims arrived by air (1 208 502), a minority travelled over land (132 829) and some arrived by sea (22 661). The number of pilgrims continues to increase: 2002 saw a total of 1 834 168 pilgrims arrive in the Kingdom (international travellers numbering 1 354 184 and domestic travellers amounting to 479 984). The various factors contributing to the health risks faced by the Hajj travellers are listed in Table 1. The Ministry of Health of the Saudi Arabian Government provides free health care to all pilgrims during the Hajj as well as implementing vigilant infection control measures. Mecca has seven modern, fully equipped hospitals, which together provide 2160 beds. Along the pilgrimage route, 73 medical centres of the Ministry of Health, the Saudi National Guard, the Internal Security Forces and the Saudi Red Crescent Society provide 24-h free medical care. A brief review of the health-related communicable and non-communicable hazards during Hajj listed in Table 2 is discussed. Fig. 1. Map of the kingdom of Saudi Arabia.
tals (7%). The country has 1.42 hospital beds per 1000 capita. Saudi Arabia has a unique position as the custodian of the two holiest places of Islam: Mecca, and Medina. The ruling monarch, HM King Fahad Bin Abdul Aziz expressed his capacity as the de facto custodian of the two holy mosques through aggressive investment to improve and protect visiting pilgrims. Since 1986, large scale public works to expand the places of worship core to the Hajj, (costing an estimated $22.5 million USD) have been carried out by royal decree. As a result, each mosque at Medina and Mecca can welcome 800 000 worshippers at one time. 1.1. Hajj pilgrimage The annual religious pilgrimage to Mecca, called Hajj, represents an unparalleled view of travel epidemiology today. Hajj is one of the five fundamental tenets of Islam and each Muslim is duty-bound to perform one such Hajj before death. During each Hajj season, over 2 million Muslim pilgrims (Hajjis) from over 140 countries visit Mecca, the focal point of Islam. Serious communicable and non-communicable hazards are faced by the pilgrim-travellers in such mass migration. With on going globalization, rising affluence and ever more affordable air travel, pilgrim burden at the Hajj is set to rise, unchecked, as more people set out on pilgrimage each year. Increasing numbers compound the risk of all of these hazards both to the visiting pilgrim and his contacts on return home. In 2001, 1 804 800 pilgrims performed Hajj including 1 363 992 international travellers from over 140 countries and 440 808 domestic pilgrims. Most international
2. Communicable hazards 2.1. Meningococcal meningitis Overcrowding, high humidity and dense air pollution during the Hajj contribute to carrier rates for meningococcal disease as high as 80% [3]. With such abnormally high carrier rates, outbreaks become a real public health threat. Upper respiratory tract infections (URTI), a common occurrence in the Hajj season, compromise airway integrity and predispose to invasive infection in carriers for meningococcal disease [4]. During the 2000 Hajj season, an outbreak of more than 400 cases of N. meningitidis serogroup W135 was reported in Saudi Arabia and nine other countries among the Hajj pilgrims or their close contacts [5 /7]. This was the largest outbreak in the world of serogroup W135 meningococcal disease, a relatively uncommon cause of a meningococcal epidemic. Electrophoretic enzyme typing confirmed that the 2000 W135 outbreak was not caused by emergence of a new Neisseria meningitidis W135 strain but by expansion of the W135 (ET-37) clone that has been circulating since Table 1 Factors magnifying health risks for the Hajj pilgrim Mass gatherings of travelers, numbering in the millions Advanced age of many pilgrims Pre-morbid health status of pilgrim Demanding and physically arduous rituals Prolonged stay at the Hajj sites (several weeks) Prevailing heat and humidity Shared facilities Overwhelming congestion of people and vehicles Inadequate food preparation, cooking, storage and vending
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Table 2 Communicable and non-communicable hazards to health at the Hajj Communicable hazards Meningococcal meningitis Respiratory Tract infections (Upper and Lower) / Influenza / Tuberculosis / Bacterial Pneumonia Blood borne Diseases Diarrhoeal Diseases Zoonosis Non-communicable hazards Trauma / Stampede Trauma / Motor vehicle trauma / Slaughter related injury Environmental / Fire-related injury / Sunburn / Heat stroke, heat exhaustion / Dehydration
1970. The most likely source of this strain is a very closely related isolate recovered in outbreaks from Algeria, Mali and Gambia in the 1990s [8]. The W135 outbreak at Mecca in 2000 highlighted the need to revise the vaccination policy for the Hajj in favour of using the quadrivalent A/C/Y/W135 vaccine instead of the bivalent formulation. Because of the short supply of the quadrivalent meningococcal vaccine, the MOH was unable to mandate a shift in vaccination policy from bivalent to quadrivalent vaccine. Although only a small number of cases of meningococcal meningitis appeared in Mecca during the 2001 Hajj week, 109 cases of meningococcal meningitis (predominantly Hajj pilgrims from outside the Kingdom of Saudi Arabia), including 35 deaths, were reported cumulatively during the period 9 February /22 March, 2001 [9]. More than 50% of these cases were confirmed to be due to N. meningitidis serogroup W135. Prompted by the changing pattern of meningococcal disease in 2000 and 2001, the Ministry of Health in Saudi Arabia changed its policy for meningococcal vaccination for the Hajj season in 2002 and mandated quadrivalent meningococcal vaccination (A, C, Y and W-135) for all pilgrims [10]. For the 2002 Hajj season, the Saudi health authority had also recommended that local pilgrims use ciprofloxacin before leaving Mecca to avoid carrying the endemic strain of meningococcus back to their families. With the crowded conditions prevalent at the Hajj, antimicrobial prophylaxis can be a powerful tool for limiting the spread of meningococcal infection [11]. While single-dose oral ciprofloxacin is effective for prophylaxis, [11] its disadvantages must be carefully considered, including the small risk for anaphylaxis-like reaction [12]. There is also a growing problem of
antibiotic-resistant organisms, with fluoroquinolone resistance in the related species N. gonorrhoeae already emerging in many countries [13]. Children and pregnant women, who form a small proportion of the Hajj pilgrims, could be given intramuscular ceftriaxone, but there is also a risk of anaphylaxis, besides the disadvantages of parenteral therapy. 2.2. Respiratory infections Acute respiratory tract infections are very common at the Hajj, especially lately since the Hajj has been occurring in winter. URTI account for the majority of these infections; lower respiratory tract involvement is also seen, though less often. Over 200 viruses can cause URTI, but those predominantly encountered at the Hajj are the respiratory syncytial virus, parainfluenzae, influenzae and adenovirus [14]. In a study of 64 patients with community-acquired pneumonia admitted to two large hospitals during the 1994 Hajj pilgrimage to Mecca, a microbiological diagnosis could be established in 46 cases (72%). Mycobacterium tuberculosis was the most common causative pathogen (20%), followed by Gram-negative bacilli (18.8%), S. pneumoniae (10%), and atypical pathogens, including viruses, Mycoplasma pneumoniae and Legionella pneumophila (6%) [15]. The prevalence of resistant tuberculosis and the annual risk of infection are three times higher in Saudi Arabian cities hosting pilgrims compared with the national average [16,17]. This can be attributed to the influx of pilgrims from developing countries where tuberculosis is endemic. The use of simple surgical masks can reduce both the expectoration and inhalation of aerosolized droplet nuclei of TB, influenza and other airborne infections [18]. Additionally, barrier masks minimize the effects of dense smoke and pollution, which accompany the Hajj. A recent study from Indonesia showed that the use of face mask continuously during the Hajj reduced the incidence of URTI by up to 82% [19]. Influenza vaccine is highly advisable for prospective Hajj pilgrims in an effort to limit complicating bacterial infection [20]. This is especially so for pilgrims over 60 years of age or those with co-morbidities. Such comorbidities include cardiovascular disease, chronic lung disease, diabetes, alcoholism, liver disease, functional or anatomic asplenia, and those with cerebrospinal fluid leaks. A recent study from Pakistan has documented the benefit of influenza vaccination of its pilgrims prior to performing the Hajj in reducing both the incidence of influenza-like illness and medication use [21]. Antiviral chemoprophylaxis can act as an adjunct but not as a substitute for vaccination. In populations where amantadine has been used for both treatment and prophylaxis of influenza, amantadine resistance has followed. New oral selective neuraminidase inhibitors
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are available, though their clinical utility is limited by currently prohibitive costs [22]. 2.3. Blood-borne diseases The Hajj poses a unique risk to male pilgrims of blood-borne diseases, such as hepatitis B (HBV), hepatitis C (HCV) and HIV. Most male pilgrims have their heads shaved by barbers to signify the end of Hajj, in keeping with correct Hajj rites. Barbers often re-use razor blades for several men. Scalp abrasions from razor nicks are common among pilgrims. On testing 158 barbers for hepatitis, 10% were found positive for hepatitis C virus, 4% for hepatitis B surface antigen (HbsAg) and 0.6% for hepatitis B surface antigen (HBeAg) [23 /25]. No barber was HIV-positive. These data point to the very real threat of blood-borne disease transmission and the urgent need for active public health campaigns. Saudi Arabia now requires all barbers to be licensed, standardizing shaving practices. It is therefore advisable for pilgrims to be protected against Hepatitis B. For the Hepatitis B immunization to be effective, the Hajj pilgrim should ideally commence vaccination 6 months prior to his/her travel [26]. 2.4. Diarrhoeal disease Diarrhoeal diseases are among the commonest medical problems associated with the Hajj. Despite this, no study has reported on its incidence and its most common aetiological agents. Episodes may begin, either during travel, at the time of pilgrimage, or on returning home. Among factors likely to determine the risk for diarrhoeal diseases are the country of origin, type of travel, host factors, food habits and environmental factors. The lack of refrigeration and improper food handling at the Hajj can contribute to the pilgrim’s risk. The Kingdom makes every effort to accommodate these needs and clean drinking water is readily available in Saudi Arabia, including at the holy sites themselves. For prevention against diarrhoeal diseases, the pilgrims have to be educated to promote proper food habits and avoid buying from unhygienic street vendors, avoid raw uncooked vegetables or products made with raw uncooked eggs. Use of ice cubes is also better avoided, as there is no certainty of their origin. Travellers can be immunized against hepatitis A virus (HAV). Where indicated, they can be checked for immunoglobulin G for HAV prior to administration of the vaccine, so that unnecessary vaccination is avoided. It is advisable for the pilgrims to carry a 3-day course of antibiotic therapy, an anti-motility agent like loperamide and a thermometer. When diarrhoeal disease occurs, proper hydration of the patient with appropriate fluid intake is vital to prevent dehydration. For moder-
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ate to severe travellers’ diarrhoea, self-administered antibiotics with an extended spectrum macrolide, azithromycin or an oral quinolone are probably indicated. In view of the harsh climatic and environmental conditions at Hajj, if oral rehydration is not readily tolerated, pilgrims with diarrhea should seek medical attention immediately. Prompt medical attention could be life saving. 2.5. Zoonotic diseases Zoonotic disease at Hajj is a real threat. Close contact between populations of animals and humans leads to the risk of brucellosis, echinococcosis, leishmaniasis, rabies and zoonotic salmenollosis. Factors that especially focus risks of zoonosis transmission to man include the consumption of contaminated milk (raw or unpasteurized camel or sheep or goat milk), changes in nutritional habits, intensified animal production practices, illegal slaughtering and inadequate disposal of animal remains. Some of these factors, particularly the slaughtering and by products of butchering the thousands of cattle head that occur during the end of Hajj (to celebrate Eid) represent a particular opportunity for Zoonosis to imperil Pilgrims. In fact, Saudi Arabia is now a collaborator in the Mediterranean Zoonosis Control program that aims to prevent, survey and to control zoonoses and foodborne diseases due to animal products, providing much needed insights into this area of travel epidemiology [27]. Saudi Arabia is highly endemic for brucellosis and imports animals for slaughter during Hajj from brucellaendemic countries with practically no quarantine or testing [28]. Despite this, no study has documented brucellosis outbreaks during the Hajj. The country has yet to launch a national programme for brucella eradication. The Crimean-Congo haemorrhagic fever (CCHF) virus was first seen in Mecca in 1990 [29]. Between 1989 and 1990, serological surveys among abattoir workers detected 40 confirmed or suspected cases of CCHF in Mecca with 12 fatalities. Exposure to animal blood or tissue in abattoirs was found to be a significant risk factor. It is possible that the CCHF virus was introduced to Saudi Arabia by infected ticks on imported sheep arriving by sea at Jeddah. Ebola, another haemorrhagic fever and is endemic to Uganda. Though the Hajj is the right of every Muslim, Saudi authorities have regretfully banned all Ugandans from attending Hajj, to protect from the possible catastrophe of an Ebola outbreak at Mecca. An Ebola haemorrhagic fever outbreak occurred in Uganda in 2001 with 170 fatalities [30,31]. A similar outbreak at Mecca could have much greater impact. From late 2000 and early 2001, Saudi Arabia was recovering from an outbreak of Rift Valley haemor-
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rhagic fever (RVF), a cattle-borne zoonotic disease, which resulted in more than 100 Saudi mortalities [32 / 34]. The Ministries of Health and Agriculture jointly took timely and stringent measures which prevented a greater public health disaster at the Hajj in 2001. These included banning the import of sheep from RVF endemic countries, restricting the entry of sheep from the southern region of Saudi Arabia, which is endemic for RVF, launching education campaigns directed at the abattoir workers in Mecca, and enforcing strict surveillance and supervision. Finally, orf is a viral disease of sheep and goats caused by a parapox virus. Human infection can result from direct contact with infected animals and manifests as skin lesions on exposed parts of the body, especially the hands. Orf infection of the hands, acquired by the slaughtering of sheep during the Hajj month, can result in Orf outbreaks. Hawary et al. documented 13 such cases [35].
3.2. Fire hazards and sun burn A fire in 1997, probably caused by open gas stoves used for cooking, destroyed many tents and led to several deaths. These open stoves have since been banned. All the tents in the Mina area, where the pilgrims reside during most of their Hajj, have been replaced with semi-permanent structures comprising aluminium frames with fiberglass teflon coated awnings. Exposure to the sun has also resulted in sunburn on the faces of women and on the upper body of men in the past. When the heat is too intense, many pilgrims may perform their rites at night. Use of appropriate protection, such as sunscreens, is recommended. Walking barefoot in the holy areas, and standing on scorching marble on a hot day can cause severe burns on the soles [36,37]. At the Holy Mosque at Mecca, a subterranean system of cooling water in pipes have been installed along with new marble surfaces recently which do not absorb heat to the same degree. 3.3. Accidental hand injury during animal slaughter
3. Non-communicable hazards
3.1. Stampede and trauma The extraordinary pressure of numbers in a limited, space can result in stampedes. Even a couple of pilgrims stumbling and falling can cause panic in the crowd and precipitate a stampede. Fatalities are usually due to head injury or asphyxiation, either at the stampede itself or subsequent to other injuries when crushed or trampled underfoot. In 2001, stampedes caused injuries to over 80 pilgrims, with some elderly pilgrims succumbing to their injuries. The pilgrims should be advised of this risk, and the need to always remain with their families or groups as they afford some protection. They should be especially cautious in the more confined areas. Elderly and infirm individuals may require wheelchairs and reliable companions to escort them. For a major part of the Hajj, the pilgrims move about on foot or in dense traffic for hours at a time. Inordinate traffic congestion and failure to use seatbelts can result in road traffic accidents involving passengers or pedestrians. The Saudi National Committee for Traffic Safety reported that during the year 2000, there were 267 772 road accidents, resulting in 4848 deaths and 32 361 injuries. Mecca Province had the highest number of accidents (94 669) followed by Riyadh Province (80 067). The main cause of accidents was speeding (106 670 cases), followed by traffic-light violations (36 042 cases). Most drivers (119 124) involved in accidents were aged 18 /30 years; followed by those between 40 and 50 (85 901) and those between 30 and 40 years (15 654).
During the three days of celebration immediately following the Hajj, known as Eid, hundreds of thousands of cattle are slaughtered. In the Hajj season of 2001, 603 393 sheep and 6136 cows and camel were slaughtered. Much of the slaughtering is done by laypersons, with no prior experience in butchering animals. As a result, accidental hand injuries are very common. In one study of 298 hand injuries related to animal slaughter presenting to an emergency department in Mecca over a 4-year period, 80% were from knives and could have been avoided [38]. Pilgrims for the Hajj should be reassured that slaughtering can be arranged by a professional. Mecca now has government regulated slaughterhouses, where qualified butchers slaughter sheep, cows, and some camel, thus limiting these hazards.
4. Conclusion The Hajj brings together for a very brief period, a very large and diverse population from all corners of the world. Travellers to Mecca face multiple challenges in the form of communicable and non-communicable hazards, many of which they can avoid or avert by adopting appropriate measures.
References [1] Central Intelligence Agency. Saudi Arabia. The World fact book 2000. Available at: http://www.cia.gov/cia/publications/factbook/.
Z.A. Memish et al. / International Journal of Antimicrobial Agents 21 (2003) 96 /101 [2] World Health Organization. The World Health reports 2000. Health systems: improving performance. Geneva: World Health Organization, 2000. [3] Al-Gahtani YM, Al-Bushra, Al-Qarawi SM, et al. Epidemiological investigation of an outbreak of meningococcal meningitis in Makkah, Saudi Arabia, 1992. Epidemiol Infect 1995;115:399 / 409. [4] Moore PS, Hierholzer J, Dewitt W, et al. Respiratory viruses and mycoplasma as cofactors for epidemic group A meningococcal meningitis. JAMA 1990;264:1271 /5. [5] Samuelssen A, Handysides S, Ramsay M, et al. Meningococcal infection in pilgrims returning from the Hajj: update from Europe and beyond. Euro Surveillance Wkly 2000;17:1 /5. [6] Centres for Disease Control and Prevention. Serogroup W135 meningococcal disease among travellers returning from Saudi Arabia: United States, 2000. MMWR Morb, Mortal Wkly Rep 2000; 49: 345 /6. [7] Popovic T, Sacchi CT, Reeves MW, et al. Neisseria meningitides serogroup W135 isolates associated with ET-37 complex. (letter) Emerg Infect Dis 2000;6:428 /9. [8] Mayer LW, Reeves MW, Al-Hamdan N, Sacchi CT, Taha M, A Jello GW, et al. Outbreak of W135 meningococcal disease in not Emergency of a New W135 strain but clonal expansion within the Electrophoretic Type-37 Complex. J Infect Dis 2002;185:1596 / 605. [9] World Health Organization (WHO). Outbreak verification list. Geneva: WHO, 4 April 2001. [10] Meningococcal disease, serogroup W135. Wkly Epidemiol. Rec. 2001; 76: 141 /2. [11] Centres for Disease Control and Prevention. Prevention and control of meningococcal disease. Recommendations of the Advisory Committee on Immunization Practices. MMWR Morb Mortal Wkly Rep 2000; 49:RR-7. [12] Communicable Disease Surveillance Centre. Ciprofloxacin as a chemoprophylactic agent for meningococcal disease / low risk of anaphylactoid reactions. Commun Dis Rep CDR Wkly 2001; 11: 2. [13] Knapp JS, Fox KK, Trees DL, Whittington WL. Fluoroquinolone resistance in Neisseria gonorrhoeae . Emerg Infect Dis 1997;3:33 /9. [14] El-Sheikh SM, El-Assouli SM, Mohammed KA, Albar M. Bacteria and viruses that cause respiratory tract infections during the pilgrimage (hajj) season in Makkah, Saudi Arabia. Trop Med Int Health 1998;3:205 /9. [15] Alzeer A, Mashlah A, Fakin N, et al. Tuberculosis is the commonest cause of pneumonia requiring hospitalization during Hajj (pilgrimage to Makkah). J Infect 1998;36:303 /6. [16] Kassimi FA, Abdullah AK, Al-Hajjaj, et al. Nationwide community survey of tuberculosis epidemiology in Saudi Arabia. Tub Lung Dis 1993;74:254 /60. [17] Khan MY, Kinsara AJ, Osoba OA, Wali S, Samman Y, Memish Z. Increasing resistance of M. tuberculosis to anti-TB drugs in Saudi Arabia. Int J Antimicrob Agents 2001;17:415 /8.
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[18] MMWR recommendations. Guidelines for preventing the transmission of Mycobacterium tuberculosis in health-care facilities, MMWR Morb Mort Wkly Rep 1994; 43(RR-13): 1 /132. [19] Zein U. Role of using masks to reduce acute upper respiratory tract infection in pilgrims. (Abstract No. 7) 4th Asia Pacific Travel Health Conference, Shanghai, P.R. China. October 20 /23, 2002 [20] An Advisory Committee Statement (ACS). National Advisory Committee on Immunization (NACI). Statement on influenza vaccination for the 2001 /2002 season. Can. Comm. Dis. Rep. 2001; 27: 1 /3. [21] Quereshi H, Gessner BD, Leboulleux D, et al. The incidence of vaccine preventable influenza-like illness and medication use among Pakistani pilgrims to the Hajj in Saudi Arabia. Vaccine 2000;18:2956 /62. [22] Memish ZA, Ahmed QAA. Mecca bound: the challenges ahead. J Travel Med 2002;9:202 /10. [23] Turkistani A, Al Rumikhan A, Mustafa T. Blood-borne diseases among barbers during hajj, 1419H (1999). Saudi Epidemiol Bull 2000;7:1 /2. [24] Al Salamah AA, El Bushra HE. Head shaving practices of barbers and pilgrims to Makkah. Saudi Epidemiol Bull 1998;5:3 /4. [25] Gatrad AR, Sheikh A. Hajj and risk of blood-borne infections. Arch Dis Child 2001;84:375. [26] World Health Organization. International travel and health. Vaccination requirements and health advice. Geneva: WHO, 2000 [27] World Health Organization. Regional Health Report, Cairo: WHO Eastern Mediterranean Regional Office, 2001 [28] Memish ZA. Brucellosis control in Saudi Arabia: prospects and challenges. J Chemother 2001;13(1):11 /7. [29] El-Azazy OME, Scrimgeour EM. Crimean-congo hemorrhagic fever virus infection in the Western province of Saudi Arabia. Trans R Soc Trop Med Hyg 1997;91:275 /8. [30] Outbreak of Ebola hemorrhagic fever, Uganda, Aug 2000 to Jan 2001. Can Commun Dis Rep 2001; 27: 49 /53. [31] MacDonald R. Ebola virus claims more lives in Uganda. Br Med J 2000;321:1037. [32] Shawky S. Rift valley fever. Saudi Med J 2000;21:1109 /15. [33] Rift Valley fever, Saudi Arabia. Aug /Oct 2000. Wkly Epidemiol. Rec. 2000; 75: 370 /1. [34] Ahmad K. More deaths from rift valley fever in Saudi Arabia and Yemen. Lancet 2000;21(356):1422. [35] Hawary MB, Hassanain JM, Al-Rasheed SK, et al. The yearly outbreak of ORF infection of the hand in Saudi Arabia. J Hand Surg 1997;4:550 /1. [36] Al Qattan MM. The ‘Friday Mass’ burns of the feet in Saudi Arabia. Burns 2000;26:102 /5. [37] Fried M, Kahanovitz S, Dagan R. Full thickness foot burn of a pilgrim to Mecca. Burns 1996;22:644 /5. [38] Rahman MM, Al-Zahrani S, Al Qattan MM. Outbreak of hand injuries during hajj festivities in Saudi Arabia. Ann Surg 1999;43:154 /5.
Travel epidemiology: the Saudi perspective Ziad A. Memish a,b,*, S. Venkatesh c, Qanta A. Ahmed d a
Department of Medicine, King Abdulaziz Medical City, King Fahad National Guard Hospital, P.O. Box 22490, Riyadh 11426, Saudi Arabia Department of Infection Prevention and Control, King Abdulaziz Medical City, King Fahad National Guard Hospital, P.O. Box 22490, Riyadh 11426, Saudi Arabia c Department of Medical Affairs, King Abdulaziz Medical City, King Fahad National Guard Hospital, P.O. Box 22490, Riyadh 11426, Saudi Arabia d Respiratory Medicine, Royal Berkshire and Battle Hospitals, Reading, UK
b
Abstract The Kingdom of Saudi Arabia occupies four-fifths of the Arabian Peninsula, with a land area of 2 million square kilometres. Saudi Arabia holds a unique position in the Islamic world, as the custodian of the two holiest places of Islam, in Mecca and Medina. Annually, some 2 million Muslims from over 140 countries embark on Hajj. This extraordinary en masse migration is a unique forum for the study of travel epidemiology since the Hajj carries various health risks, both communicable and non-communicable, often on a colossal scale. Non-communicable hazards of the Hajj include stampede and motor vehicle trauma, fire-related burn injuries and accidental hand injury during animal slaughter. Communicable hazards in the form of outbreaks of multiple infectious diseases have been reported repeatedly, during and following the Hajj. Meningococcal meningitis, gastroenteritis, hepatitis A, B and C, and various zoonotic diseases comprise some of the possible infectious hazards at the Hajj. Many of these infectious and noninfectious hazards can be avoided or averted by adopting appropriate prophylactic measures. Physicians and health personnel must be aware of these risks to appropriately educate, immunize and prepare these travellers facing the unique epidemiological challenges of Hajj in an effort to minimize untoward effects. Travel epidemiology related to the Hajj is a new and exciting area, which offers valuable insights to the travel specialist. The sheer scale of numbers affords a rare view of migration medicine in action. As data is continually gathered and both national and international policy making is tailored to vital insights gained through travel epidemiology, the Hajj will be continually safeguarded. Practitioners will gain from findings of travel related epidemiological changes in evolution at the Hajj: the impact of vaccinating policies, infection control policies and public health are afforded a real-world laboratory setting at each annual Hajj, allowing us to learn from this unique phenomenon of migration medicine. # 2002 Elsevier Science B.V. and the International Society of Chemotherapy. All rights reserved. Keywords: Saudi Arabia; Hajj; Infectious diseases; Non-infectious hazards; Travel
1. Introduction The Kingdom of Saudi Arabia occupies four-fifths of the Arabian Peninsula, with a land area of about 2 million square kilometres (900 000 square miles) [1]. The largest and most populated of the six Gulf Cooperation Council (GCC) states in the Middle East, Saudi Arabia is bounded by the Persian Gulf in the East and the Red Sea in the West (Fig. 1). Of its estimated 22 million population, which includes 5.3 million expatriates, three-fourths live in urban areas. Nomadic Bedouins
* Corresponding author. Tel.: /966-01-2520088x3718; fax: /96601-2520437. E-mail address: [email protected] (Z.A. Memish).
form 7% of the rural populace. Saudi Arabia has a desert climate with the temperature reaching around 55 8C in summer months. Saudi Arabia has an advanced health care system. The World Health Organization has recognized its health programmes as an exemplary health care model for developing nations and ranks it 26th of 176 nations in overall health system performance [2]. The Saudi Arabian Ministry of Health provides 60% of the health care services and operates 188 hospitals, with a cumulative bed count of 27 994. Additionally the MOH runs 1766 Primary Health Care centres throughout the Kingdom. Other important health care providers in Saudi Arabia include the fast-growing private sector (20%), military organizations (13%) and teaching hospi-
0924-8579/02/$30 # 2002 Elsevier Science B.V. and the International Society of Chemotherapy. All rights reserved. PII: S 0 9 2 4 - 8 5 7 9 ( 0 2 ) 0 0 3 6 4 - 3
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pilgrims arrived by air (1 208 502), a minority travelled over land (132 829) and some arrived by sea (22 661). The number of pilgrims continues to increase: 2002 saw a total of 1 834 168 pilgrims arrive in the Kingdom (international travellers numbering 1 354 184 and domestic travellers amounting to 479 984). The various factors contributing to the health risks faced by the Hajj travellers are listed in Table 1. The Ministry of Health of the Saudi Arabian Government provides free health care to all pilgrims during the Hajj as well as implementing vigilant infection control measures. Mecca has seven modern, fully equipped hospitals, which together provide 2160 beds. Along the pilgrimage route, 73 medical centres of the Ministry of Health, the Saudi National Guard, the Internal Security Forces and the Saudi Red Crescent Society provide 24-h free medical care. A brief review of the health-related communicable and non-communicable hazards during Hajj listed in Table 2 is discussed. Fig. 1. Map of the kingdom of Saudi Arabia.
tals (7%). The country has 1.42 hospital beds per 1000 capita. Saudi Arabia has a unique position as the custodian of the two holiest places of Islam: Mecca, and Medina. The ruling monarch, HM King Fahad Bin Abdul Aziz expressed his capacity as the de facto custodian of the two holy mosques through aggressive investment to improve and protect visiting pilgrims. Since 1986, large scale public works to expand the places of worship core to the Hajj, (costing an estimated $22.5 million USD) have been carried out by royal decree. As a result, each mosque at Medina and Mecca can welcome 800 000 worshippers at one time. 1.1. Hajj pilgrimage The annual religious pilgrimage to Mecca, called Hajj, represents an unparalleled view of travel epidemiology today. Hajj is one of the five fundamental tenets of Islam and each Muslim is duty-bound to perform one such Hajj before death. During each Hajj season, over 2 million Muslim pilgrims (Hajjis) from over 140 countries visit Mecca, the focal point of Islam. Serious communicable and non-communicable hazards are faced by the pilgrim-travellers in such mass migration. With on going globalization, rising affluence and ever more affordable air travel, pilgrim burden at the Hajj is set to rise, unchecked, as more people set out on pilgrimage each year. Increasing numbers compound the risk of all of these hazards both to the visiting pilgrim and his contacts on return home. In 2001, 1 804 800 pilgrims performed Hajj including 1 363 992 international travellers from over 140 countries and 440 808 domestic pilgrims. Most international
2. Communicable hazards 2.1. Meningococcal meningitis Overcrowding, high humidity and dense air pollution during the Hajj contribute to carrier rates for meningococcal disease as high as 80% [3]. With such abnormally high carrier rates, outbreaks become a real public health threat. Upper respiratory tract infections (URTI), a common occurrence in the Hajj season, compromise airway integrity and predispose to invasive infection in carriers for meningococcal disease [4]. During the 2000 Hajj season, an outbreak of more than 400 cases of N. meningitidis serogroup W135 was reported in Saudi Arabia and nine other countries among the Hajj pilgrims or their close contacts [5 /7]. This was the largest outbreak in the world of serogroup W135 meningococcal disease, a relatively uncommon cause of a meningococcal epidemic. Electrophoretic enzyme typing confirmed that the 2000 W135 outbreak was not caused by emergence of a new Neisseria meningitidis W135 strain but by expansion of the W135 (ET-37) clone that has been circulating since Table 1 Factors magnifying health risks for the Hajj pilgrim Mass gatherings of travelers, numbering in the millions Advanced age of many pilgrims Pre-morbid health status of pilgrim Demanding and physically arduous rituals Prolonged stay at the Hajj sites (several weeks) Prevailing heat and humidity Shared facilities Overwhelming congestion of people and vehicles Inadequate food preparation, cooking, storage and vending
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Table 2 Communicable and non-communicable hazards to health at the Hajj Communicable hazards Meningococcal meningitis Respiratory Tract infections (Upper and Lower) / Influenza / Tuberculosis / Bacterial Pneumonia Blood borne Diseases Diarrhoeal Diseases Zoonosis Non-communicable hazards Trauma / Stampede Trauma / Motor vehicle trauma / Slaughter related injury Environmental / Fire-related injury / Sunburn / Heat stroke, heat exhaustion / Dehydration
1970. The most likely source of this strain is a very closely related isolate recovered in outbreaks from Algeria, Mali and Gambia in the 1990s [8]. The W135 outbreak at Mecca in 2000 highlighted the need to revise the vaccination policy for the Hajj in favour of using the quadrivalent A/C/Y/W135 vaccine instead of the bivalent formulation. Because of the short supply of the quadrivalent meningococcal vaccine, the MOH was unable to mandate a shift in vaccination policy from bivalent to quadrivalent vaccine. Although only a small number of cases of meningococcal meningitis appeared in Mecca during the 2001 Hajj week, 109 cases of meningococcal meningitis (predominantly Hajj pilgrims from outside the Kingdom of Saudi Arabia), including 35 deaths, were reported cumulatively during the period 9 February /22 March, 2001 [9]. More than 50% of these cases were confirmed to be due to N. meningitidis serogroup W135. Prompted by the changing pattern of meningococcal disease in 2000 and 2001, the Ministry of Health in Saudi Arabia changed its policy for meningococcal vaccination for the Hajj season in 2002 and mandated quadrivalent meningococcal vaccination (A, C, Y and W-135) for all pilgrims [10]. For the 2002 Hajj season, the Saudi health authority had also recommended that local pilgrims use ciprofloxacin before leaving Mecca to avoid carrying the endemic strain of meningococcus back to their families. With the crowded conditions prevalent at the Hajj, antimicrobial prophylaxis can be a powerful tool for limiting the spread of meningococcal infection [11]. While single-dose oral ciprofloxacin is effective for prophylaxis, [11] its disadvantages must be carefully considered, including the small risk for anaphylaxis-like reaction [12]. There is also a growing problem of
antibiotic-resistant organisms, with fluoroquinolone resistance in the related species N. gonorrhoeae already emerging in many countries [13]. Children and pregnant women, who form a small proportion of the Hajj pilgrims, could be given intramuscular ceftriaxone, but there is also a risk of anaphylaxis, besides the disadvantages of parenteral therapy. 2.2. Respiratory infections Acute respiratory tract infections are very common at the Hajj, especially lately since the Hajj has been occurring in winter. URTI account for the majority of these infections; lower respiratory tract involvement is also seen, though less often. Over 200 viruses can cause URTI, but those predominantly encountered at the Hajj are the respiratory syncytial virus, parainfluenzae, influenzae and adenovirus [14]. In a study of 64 patients with community-acquired pneumonia admitted to two large hospitals during the 1994 Hajj pilgrimage to Mecca, a microbiological diagnosis could be established in 46 cases (72%). Mycobacterium tuberculosis was the most common causative pathogen (20%), followed by Gram-negative bacilli (18.8%), S. pneumoniae (10%), and atypical pathogens, including viruses, Mycoplasma pneumoniae and Legionella pneumophila (6%) [15]. The prevalence of resistant tuberculosis and the annual risk of infection are three times higher in Saudi Arabian cities hosting pilgrims compared with the national average [16,17]. This can be attributed to the influx of pilgrims from developing countries where tuberculosis is endemic. The use of simple surgical masks can reduce both the expectoration and inhalation of aerosolized droplet nuclei of TB, influenza and other airborne infections [18]. Additionally, barrier masks minimize the effects of dense smoke and pollution, which accompany the Hajj. A recent study from Indonesia showed that the use of face mask continuously during the Hajj reduced the incidence of URTI by up to 82% [19]. Influenza vaccine is highly advisable for prospective Hajj pilgrims in an effort to limit complicating bacterial infection [20]. This is especially so for pilgrims over 60 years of age or those with co-morbidities. Such comorbidities include cardiovascular disease, chronic lung disease, diabetes, alcoholism, liver disease, functional or anatomic asplenia, and those with cerebrospinal fluid leaks. A recent study from Pakistan has documented the benefit of influenza vaccination of its pilgrims prior to performing the Hajj in reducing both the incidence of influenza-like illness and medication use [21]. Antiviral chemoprophylaxis can act as an adjunct but not as a substitute for vaccination. In populations where amantadine has been used for both treatment and prophylaxis of influenza, amantadine resistance has followed. New oral selective neuraminidase inhibitors
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are available, though their clinical utility is limited by currently prohibitive costs [22]. 2.3. Blood-borne diseases The Hajj poses a unique risk to male pilgrims of blood-borne diseases, such as hepatitis B (HBV), hepatitis C (HCV) and HIV. Most male pilgrims have their heads shaved by barbers to signify the end of Hajj, in keeping with correct Hajj rites. Barbers often re-use razor blades for several men. Scalp abrasions from razor nicks are common among pilgrims. On testing 158 barbers for hepatitis, 10% were found positive for hepatitis C virus, 4% for hepatitis B surface antigen (HbsAg) and 0.6% for hepatitis B surface antigen (HBeAg) [23 /25]. No barber was HIV-positive. These data point to the very real threat of blood-borne disease transmission and the urgent need for active public health campaigns. Saudi Arabia now requires all barbers to be licensed, standardizing shaving practices. It is therefore advisable for pilgrims to be protected against Hepatitis B. For the Hepatitis B immunization to be effective, the Hajj pilgrim should ideally commence vaccination 6 months prior to his/her travel [26]. 2.4. Diarrhoeal disease Diarrhoeal diseases are among the commonest medical problems associated with the Hajj. Despite this, no study has reported on its incidence and its most common aetiological agents. Episodes may begin, either during travel, at the time of pilgrimage, or on returning home. Among factors likely to determine the risk for diarrhoeal diseases are the country of origin, type of travel, host factors, food habits and environmental factors. The lack of refrigeration and improper food handling at the Hajj can contribute to the pilgrim’s risk. The Kingdom makes every effort to accommodate these needs and clean drinking water is readily available in Saudi Arabia, including at the holy sites themselves. For prevention against diarrhoeal diseases, the pilgrims have to be educated to promote proper food habits and avoid buying from unhygienic street vendors, avoid raw uncooked vegetables or products made with raw uncooked eggs. Use of ice cubes is also better avoided, as there is no certainty of their origin. Travellers can be immunized against hepatitis A virus (HAV). Where indicated, they can be checked for immunoglobulin G for HAV prior to administration of the vaccine, so that unnecessary vaccination is avoided. It is advisable for the pilgrims to carry a 3-day course of antibiotic therapy, an anti-motility agent like loperamide and a thermometer. When diarrhoeal disease occurs, proper hydration of the patient with appropriate fluid intake is vital to prevent dehydration. For moder-
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ate to severe travellers’ diarrhoea, self-administered antibiotics with an extended spectrum macrolide, azithromycin or an oral quinolone are probably indicated. In view of the harsh climatic and environmental conditions at Hajj, if oral rehydration is not readily tolerated, pilgrims with diarrhea should seek medical attention immediately. Prompt medical attention could be life saving. 2.5. Zoonotic diseases Zoonotic disease at Hajj is a real threat. Close contact between populations of animals and humans leads to the risk of brucellosis, echinococcosis, leishmaniasis, rabies and zoonotic salmenollosis. Factors that especially focus risks of zoonosis transmission to man include the consumption of contaminated milk (raw or unpasteurized camel or sheep or goat milk), changes in nutritional habits, intensified animal production practices, illegal slaughtering and inadequate disposal of animal remains. Some of these factors, particularly the slaughtering and by products of butchering the thousands of cattle head that occur during the end of Hajj (to celebrate Eid) represent a particular opportunity for Zoonosis to imperil Pilgrims. In fact, Saudi Arabia is now a collaborator in the Mediterranean Zoonosis Control program that aims to prevent, survey and to control zoonoses and foodborne diseases due to animal products, providing much needed insights into this area of travel epidemiology [27]. Saudi Arabia is highly endemic for brucellosis and imports animals for slaughter during Hajj from brucellaendemic countries with practically no quarantine or testing [28]. Despite this, no study has documented brucellosis outbreaks during the Hajj. The country has yet to launch a national programme for brucella eradication. The Crimean-Congo haemorrhagic fever (CCHF) virus was first seen in Mecca in 1990 [29]. Between 1989 and 1990, serological surveys among abattoir workers detected 40 confirmed or suspected cases of CCHF in Mecca with 12 fatalities. Exposure to animal blood or tissue in abattoirs was found to be a significant risk factor. It is possible that the CCHF virus was introduced to Saudi Arabia by infected ticks on imported sheep arriving by sea at Jeddah. Ebola, another haemorrhagic fever and is endemic to Uganda. Though the Hajj is the right of every Muslim, Saudi authorities have regretfully banned all Ugandans from attending Hajj, to protect from the possible catastrophe of an Ebola outbreak at Mecca. An Ebola haemorrhagic fever outbreak occurred in Uganda in 2001 with 170 fatalities [30,31]. A similar outbreak at Mecca could have much greater impact. From late 2000 and early 2001, Saudi Arabia was recovering from an outbreak of Rift Valley haemor-
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rhagic fever (RVF), a cattle-borne zoonotic disease, which resulted in more than 100 Saudi mortalities [32 / 34]. The Ministries of Health and Agriculture jointly took timely and stringent measures which prevented a greater public health disaster at the Hajj in 2001. These included banning the import of sheep from RVF endemic countries, restricting the entry of sheep from the southern region of Saudi Arabia, which is endemic for RVF, launching education campaigns directed at the abattoir workers in Mecca, and enforcing strict surveillance and supervision. Finally, orf is a viral disease of sheep and goats caused by a parapox virus. Human infection can result from direct contact with infected animals and manifests as skin lesions on exposed parts of the body, especially the hands. Orf infection of the hands, acquired by the slaughtering of sheep during the Hajj month, can result in Orf outbreaks. Hawary et al. documented 13 such cases [35].
3.2. Fire hazards and sun burn A fire in 1997, probably caused by open gas stoves used for cooking, destroyed many tents and led to several deaths. These open stoves have since been banned. All the tents in the Mina area, where the pilgrims reside during most of their Hajj, have been replaced with semi-permanent structures comprising aluminium frames with fiberglass teflon coated awnings. Exposure to the sun has also resulted in sunburn on the faces of women and on the upper body of men in the past. When the heat is too intense, many pilgrims may perform their rites at night. Use of appropriate protection, such as sunscreens, is recommended. Walking barefoot in the holy areas, and standing on scorching marble on a hot day can cause severe burns on the soles [36,37]. At the Holy Mosque at Mecca, a subterranean system of cooling water in pipes have been installed along with new marble surfaces recently which do not absorb heat to the same degree. 3.3. Accidental hand injury during animal slaughter
3. Non-communicable hazards
3.1. Stampede and trauma The extraordinary pressure of numbers in a limited, space can result in stampedes. Even a couple of pilgrims stumbling and falling can cause panic in the crowd and precipitate a stampede. Fatalities are usually due to head injury or asphyxiation, either at the stampede itself or subsequent to other injuries when crushed or trampled underfoot. In 2001, stampedes caused injuries to over 80 pilgrims, with some elderly pilgrims succumbing to their injuries. The pilgrims should be advised of this risk, and the need to always remain with their families or groups as they afford some protection. They should be especially cautious in the more confined areas. Elderly and infirm individuals may require wheelchairs and reliable companions to escort them. For a major part of the Hajj, the pilgrims move about on foot or in dense traffic for hours at a time. Inordinate traffic congestion and failure to use seatbelts can result in road traffic accidents involving passengers or pedestrians. The Saudi National Committee for Traffic Safety reported that during the year 2000, there were 267 772 road accidents, resulting in 4848 deaths and 32 361 injuries. Mecca Province had the highest number of accidents (94 669) followed by Riyadh Province (80 067). The main cause of accidents was speeding (106 670 cases), followed by traffic-light violations (36 042 cases). Most drivers (119 124) involved in accidents were aged 18 /30 years; followed by those between 40 and 50 (85 901) and those between 30 and 40 years (15 654).
During the three days of celebration immediately following the Hajj, known as Eid, hundreds of thousands of cattle are slaughtered. In the Hajj season of 2001, 603 393 sheep and 6136 cows and camel were slaughtered. Much of the slaughtering is done by laypersons, with no prior experience in butchering animals. As a result, accidental hand injuries are very common. In one study of 298 hand injuries related to animal slaughter presenting to an emergency department in Mecca over a 4-year period, 80% were from knives and could have been avoided [38]. Pilgrims for the Hajj should be reassured that slaughtering can be arranged by a professional. Mecca now has government regulated slaughterhouses, where qualified butchers slaughter sheep, cows, and some camel, thus limiting these hazards.
4. Conclusion The Hajj brings together for a very brief period, a very large and diverse population from all corners of the world. Travellers to Mecca face multiple challenges in the form of communicable and non-communicable hazards, many of which they can avoid or avert by adopting appropriate measures.
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