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Hazards of hepatitis at the Hajj
Travel Medicine and Infectious Disease (2009) 7, 239e246
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Hazards of hepatitis at the Hajj Shafquat M. Rafiq a,*, Harunor Rashid b, Elizabeth Haworth c, Robert Booy b,d a
Unit of Gastroenterology, Department of Medicine, Epsom and St Helier University Hospitals NHS Trust, Dorking Road, KT18 7EG, Surrey, UK b Academic Unit of Child Health, Barts and the London Queen Mary’s School of Medicine and Dentistry, London, UK c Health Protection Agency, South East, London, UK d National Centre for Immunisation Research and Surveillance of Vaccine Preventable Diseases, The Children’s Hospital at Westmead and The University of Sydney, New South Wales, Australia Received 25 August 2008; accepted 8 September 2008 Available online 21 November 2008
KEYWORDS Accelerated vaccination schedule; Blood borne hepatitis; Enteral viral hepatitis; Muslims; Pilgrimage; Travel
Summary While an increased risk of hepatitis is associated with travel, the risk of hepatitis associated with the Islamic Hajj pilgrimage to Mecca, Saudi Arabia has not been carefully quantified. Conditions unique to this gathering can pose the risk of both enteral and parenteral viral hepatitis. During this congregation, pilgrims stay in tents shared by 100 or more people often living on foods from street vendors and sharing common toilet facilities that can expose them to both hepatitis A and E. To mark the end of the festival, head shaving or trimming by fellow pilgrims or street barbers, who often re-use their razor may expose them to hepatitis B or C. Pilgrims are also at risk of cuts to the hands and feet while sacrificing cattle and walking barefooted, which may further increase the risk of parenteral viral hepatitis. Emerging diseases such as Alkhumra virus and Rift Valley fever, which may cause hepatitis, are also potentially important for the Hajj pilgrims. Improved health education to increase awareness about the risk of these diseases and appropriate immunisations, particularly hepatitis A and B vaccines, could play an important role. ª 2008 Elsevier Ltd. All rights reserved.
Introduction For over 1400 years practicing Muslims have undertaken the annual Hajj pilgrimage in Mecca, Saudi Arabia, said to be the world’s largest organised annual mass gathering. While performing the Hajj to improve their spiritual health,
* Corresponding author. Tel.: þ44 (0) 1372 735119; fax: þ44 (0) 1372 735955. E-mail address: [email protected] (S.M. Rafiq).
through unity, goodwill and sacrifice, faithful Muslims may put their physical health at risk, particularly from infections.1,2 Swiss traveller John Lewis Burckhardt, who made his journey to Mecca in 1813 in disguise as a Muslim pilgrim, is believed to be the first European to record the infectious hazards of the Hajj.3 Studying the works of Arab historians Asamy and Fasy, Burckhardt recorded that there was an outbreak of an unspecified ‘pestilence’ in Arabic year 671 (circa 1271 AD) that killed 50 persons a day and another in Arabic year 829 (circa 1424 AD), when 2000 people died
1477-8939/$ - see front matter ª 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tmaid.2008.09.008
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during the Hajj.3 Burckhardt himself reported occurrence of ‘intermittent fever’ (probably referring to malaria), ‘putrid fever’ (probably referring to diphtheria or typhus fever) and dysentery in Mecca during his visit. The Hajj more recently came to world attention because of outbreaks of meningococcal diseases (of note Meningococcus W135) that affected more than 2400 people all over the world during and following the Hajj 2000 and 2001.4,5 At least three distinct categories of health risks are associated with the Hajj: those related to travel e.g., travellers’ diarrhoea, malaria, jet lag; those related to crowding e.g., respiratory infections including meningococcal disease, influenza and tuberculosis; and those relating to ritual practices e.g., stampede, blood borne infections. The rites of the Hajj start well before reaching Greater Mecca when pilgrims change their garments to a pair of white unstitched sheets symbolising death shrouds as a ‘departure from the mundane world’.6,7 They then refrain from using scented toiletries, having sexual relationships, shaving or trimming hair and cutting nails. After days of physically demanding rituals that involve walking long distances barefooted, marching between two hillocks named Safa and Marwah, a daylong stay at the plain of Arafat, pelting stones at a symbolic Satan and sacrificing cattle, pilgrims have their hair shaved or cut to mark the end of the festival (Fig. 1).1,7,8 Risk of both blood borne, and food and water borne viral hepatitis associated with travel is well recognised,9,10 but the risk of hepatitis in relation to the Hajj pilgrimage has not been formally assessed. We have therefore reviewed the published literature to inform the risks of viral hepatitis in relation to the Hajj pilgrimage.
Search strategy We undertook a Medline search using terms ‘Hajj AND Hepatitis’, ‘Hajj AND Liver disease’, ‘Saudi Arabia AND
Hepatitis’, ‘Mecca AND Hepatitis’ and ‘Travel AND Hepatitis’ and the alternative spelling ‘Haj’ or ‘Hadj’, with emphasis on the latest publications. Hand searching of identified articles was done to spot other relevant articles from the references they cited. Journals in hepatology, hepatitis, gastroenterology and infectious diseases, which are not indexed in Medline, were also searched from their respective websites through the ‘Google’ search engine. Archives or older publications were accessed from the British Library and the library of Islamic Cultural Centre, London, UK.
Hepatitis A Epidemiology Hepatitis A virus (HAV) is an RNA virus with worldwide distribution and the disease it causes is the commonest vaccine preventable illness among international travellers.10 Evidence of past infection is nearly universal in adults from sanitation poor areas of Africa, Asia and South America where people usually acquire asymptomatic infections in childhood.11 Since infection usually confers lifelong immunity,12 those born and raised in endemic countries and those born in developed countries before 1945 (when HAV was still common there) are likely to be immune to the disease.13 Thus pilgrims under the age of 60 travelling from low endemic zone i.e., Europe, USA, Canada, Australia, New Zealand, Japan and other countries with decreasing anti-HAV status, are usually susceptible to infection, while residents from endemic zones are not. Estimated attack rates for European travellers to Middle East are approximately 181 per 1000 journeys.10 Transmission is generally by the faeco-oral route and spreads person-to-person because of overcrowding and poor personal hygiene or via ingestion of contaminated water or food.11 Rarely (<5%) spread may occur through transfusion of blood or blood products.14
Hajj-associated risks
Figure 1
Pilgrims are helping each other by shaving heads.
Safe drinking water is supplied during the Hajj and the risk of water borne transmission is low. However, ice used to cool water and beverages in hot and humid weather may be from unknown sources, and thus runs the risk of contamination. Foods, particularly unpeeled fruits and vegetables, also may be contaminated with HAV. Although Saudi Arabia has banned visitors and pilgrims from bringing foods into the country, a survey among the Hajj pilgrims suggest that 37% did bring foodstuff from home countries.15 Thirty-four percent pilgrims bought foods from street vendors, many of whom were hawkers or operated from makeshift shops with dubious hygiene standards.15 Communal use of toilets, avoidance of soaps and detergents (due to their perfume) or alcohol hand rubs during tent living in Mina may increase the risk of HAV infection.16 Person-to-person contact during different rituals e.g., during circumambulation, SafaeMarwah marching and Arafat standing also may increase infection risks.
Hazards of hepatitis at the Hajj
Prevention Good personal, food and drink hygiene reduces infection risks. Key advice is ‘boil it, cook it, peel it or leave it’.13 Pre-travel advice, contact tracing and post-exposure prophylaxis will help in prevention of spread.17 At least 6 inactivated hepatitis A vaccines as well as 2 combined hepatitis A and hepatitis B vaccines confer active immunity.12,18 Inactivated HAV vaccines are safe, highly immunogenic and provide long-term (up to 25 years) protection from HAV infection.19 They can be administered simultaneously with a number of other vaccines without compromising immunogenicity.20 Although the antibody level achieved after immunisation with vaccine is 10e100 times lower than that achieved through natural infection,21 protective levels (>10 IU/mL) are achieved in 98% after 4 weeks and even in 70% 2 weeks after vaccination.21,22 Testing for immunity before vaccination may be costeffective in people highly likely to be immune from previous exposure e.g., first generation adult immigrants to low prevalence countries.21 If administered no more than 14 days after exposure, intramuscular immunoglobin can confer short-term immunity to prevent symptoms in 70e 90%, or attenuate them and reduce further transmission.23,24 The immunoglobulin can be administered to children who do not have or have lost protection due to transferred maternal antibodies.25
Hepatitis B Epidemiology Hepatitis B virus (HBV) is an enveloped DNA virus containing partially double stranded, circular genome.26,27 The virus has eight major genotypes (AeH) clustered in different parts of the world to create a somewhat heterogeneous clinical history, and response to treatment.28 HBV is highly adaptive, producing vaccine-related escape mutants and drug resistance. Chronic infection can lead to cirrhosis, hepatocellular carcinoma (HCC) and death from liver failure. Worldwide more than 2 billion people (one third of the world population) have been infected with HBV (Fig. 2), and up to 80% of all HCC have been attributed to HBV infection.29 Although most of those infected develop anti-HBs antibody and remain well, chronicity (persistence of surface antigenaemia 6 month) develops in approximately 350 million people worldwide.30 Among those infected, more than 4 million of acute clinical cases and more than 1 million of chronic carriers die from liver diseases each year.31 Of 40 million known HIV positives, 3 million are coinfected with HBV and 4.5 million with hepatitis C virus (HCV) respectively.32 Depending on geographical location, co-infection of HBV with HCV varies from 9% to 30%.33,34 The prevalence of HBV infections varies from about 8% in the Far East, parts of Middle East, sub-Saharan Africa and Amazon basin i.e., high prevalence areas to <1% in low prevalence countries such as the UK, Australia and North America. Mass travel, migration and introduction of vaccine are, however, changing the epidemiology of HBV infection.29,31,35,36 HBV is transmitted parenterally or through
241 a breach in skin or mucus membrane when these encounter infected blood or body fluids. It can remain infective on surfaces it is exposed to, e.g., razor blades and tabletops, for up to one week.32 All hepatitis B surface antigen (HbsAg) positive individuals are potentially infectious. Where HBV is endemic most transmission occurs from mother to children or from child to child in household settings but in western countries with low endemicity most infections are acquired in adulthood as a result of high risk sexual activity and/or sharing needles and syringes for injecting drugs.29,37 Risk of chronicity is inversely related to age: chronic carriage will develop in up to 90% of infants when infected at birth compared with 5e10% of those who become infected as adults.29,38
Hajj-associated risks A large number of pilgrims attending the Hajj pilgrimage are from countries with intermediate to high HBV prevalence (Table 1) and HBV infection is endemic in Saudi Arabia.39 The head shaving practice among pilgrims is of particular concern in transmitting HBV and other blood borne diseases.40e42 To mark the end of the festival around 90% men get their heads shaved either by barbers or by fellow pilgrims (Fig. 1).43 In two separate studies, 61% Hajjis had cuts to scalp (maximum of 18 cuts) and 25% used shared razors.15,43 Although testing for HBV and HCV, and the use of disposable blades are mandatory for barbers, a 1999-survey among barbers showed that 4% were HBsAg positive, 0.6% hepatitis B e antigen (HbeAg) positive and 10% positive for HCV.43 During the Hajj period a large number of unlicensed barbers operate, most of them arriving from high prevalence areas, practise along roadsides and are unaware of infection control. In a study in 1998, 23% of barbers had open hand wounds, 21% used the same blade for more than one shave and 82% threw at least one used blade to the ground.40 The latter finding is significant as pilgrims walk long distances barefooted or lose their slippers in the crowds after pebble throwing.
Prevention Active immunisation remains the single most effective measure for HBV prevention.44 Routine infant hepatitis B vaccination with 90% coverage and the first dose administered at birth would prevent most HBV infection and an estimated 84% of global HBV-related deaths.45 Although response to vaccination is somewhat lower in adults over 40, the risk of infection in travellers who receive 3 doses is negligible (post-immunisation testing is not routine).10 A 4dose schedule (at 0, 1, 2, 12 months) of HBV vaccine is also highly effective immediately after exposure.46 An accelerated schedule is available for last minute travellers (at 0, 7, 21 days) and may be useful for Hajj pilgrims.42,47 As 70% of Hajj pilgrims and 20% of barbers were not aware of risks of infections associated with razor blades,40 pre-Hajj health education of pilgrims and barbers, tighter control of barbers and safe disposal of razor blades and other shaving waste is also necessary. Promising results have been obtained from culturally tailored lectures on prevention of hepatitis B among AsianeAmerican communities in the USA.48
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Figure 2
Global distribution of hepatitis B.
Hepatitis C Epidemiology Hepatitis C virus (HCV) is an enveloped single stranded RNA virus that was isolated in 1989 as the cause for most transfusion related non-A non-B viral hepatitis in humans.49 So far, 11 genotypes with several distinct subtypes have been identified across the world and this variation relates to the significant heterogeneity in response to treatment and is a major obstacle to developing a single effective vaccine. Genotype 4 is the commonest (70%) in the western province of Saudi Arabia where Mecca is situated.50 Chronicity develops in up to 80% people infected with HCV,51,52 10e15% of whom develop cirrhosis within 20 years and ‘‘the progression to cirrhosis is often clinically silent, and some patients are not known to have hepatitis C until they present with the complications of end-stage liver disease or HCC’’.53
Table 1 Examples of some countries that send a major proportion of pilgrims to the Hajj and their hepatitis B prevalence. Country
Population Number of pilgrims % HBsAg (millions) per year prevalence
Saudi Arabia Indonesia Pakistan India Turkey Iran Nigeria Egypt Bangladesh UK USA
24.7 231.6 163.9 1135.9 70.6 70.5 148.1 75 153.6 60.6 304.7
1000000 200000 150000 170000 120000 100000 90000 75000 65000 25000 10000
5 4 3.3 4.7 6.6 3 15 10.1 5 0.6 0.5
It is estimated that approximately 170 million individuals (3% of world population) have been infected with HCV with the prevalence ranging from <1.0% in Northern Europe to >10% in the African and Eastern Mediterranean countries (Fig. 3).49,54 HCV is transmitted by sharing needles or syringes with an infected person or by exposure to infected blood.49 Sexual transmission is less efficient than for HBV or HIV, and vertical transmission is generally uncommon but still well documented and is the most frequent mode of hepatitis C acquisition in children.55 In a tenth of HCV carriers no source can be identified.56 Community acquired HCV is thought to be associated with sharing personal articles such as toothbrushes, razors and nail scissors or with contaminations of wounds.54
Hajj-associated risks As is the case with HBV, people from hepatitis C endemic countries converge at the Hajj pilgrimage. Well-defined risk factors for hepatitis C transmission e.g., unsafe sex and intravenous drug use are not known to be problems due to prohibitions (sexual intercourse even with the own partner is prohibited during the key festival) and strong religious commitments. However, risks related to transfusion of blood or blood products and nosocomial infection cannot be understated as huge number of Hajjis require admission to hospitals. For instance, of 689 pilgrims belonging to 49 countries (many of these were HCV endemic countries) who were admitted to one of the six tertiary hospitals in Mecca for treatment of medical conditions during the Hajj 2005 5% (n Z 32) were admitted for complications of chronic liver disease and another 5% (n Z 34) for upper gastrointestinal bleeding, a common presentation of variceal bleeding.57 Although routine screening of blood has been implemented in Saudi Arabia, the prevalence of anti HCV antibody is 4.3% of blood donors and 2.2% of medical staff in a tertiary hospital close to Mecca.58 In a study of 30 HCV infected patients to assess possibility of transmission via tooth brushing saliva and
Hazards of hepatitis at the Hajj
243
Figure 3
Global distribution of hepatitis C.
rinsing water were tested for HCV RNA before and after brushing. Saliva was positive in 30% and 36.7% cases before and after brushing respectively, while rinsed water was positive in 40% cases.59 This demonstrates at least theoretical risk of transmission through gurgling and sharing utensils including dental sticks, which many devout Muslims use regularly to clean their teeth before every prayer.60 As pilgrims stay together as groups in tents, they are also likely to share personal articles such as nail clippers and scissors to add to the risk of HCV transmission.
Prevention So far, no effective vaccine or immunoglobulin has been available to prevent HCV. Clinical awareness of the disease associated with early diagnosis and treatment with combination therapy with pegylated interferon and ribavirin improves its prognosis.61,62 Preventive strategies include implementation and practice of infection control measures, general pre-Hajj advice on personal care and covering of cuts and wounds and counselling known infected or at risk persons, although the latter might be difficult in Hajj settings. Newer sensitive quick immune chromatographic tests could help rapid detection of high risk cases to initiate early treatment and take necessary measures for secondary prevention.62,63
Hepatitis D Hepatitis D or delta virus (HDV) is a defective RNA virus, which uses HBsAg as its own virion coat and requires coinfection with HBV for replication.64 Approximately 5% of chronic HBV carriers are co-infected with HDV either concurrently or as a super-infection in those already HBsAg positive. Although a declining trend has been observed for a decade, recent increase in prevalence is being reported in some areas, for example in parts of London.65e67 Coinfection may lead to more severe disease or higher risks of
severe complications e.g., cirrhosis or HCC. Its distribution is as for HBV infection with epidemics occurring in the Mediterranean, Amazon basin and Central Africa. It has a similar transmission pattern to HBV since HBsAg envelops it, and risks associated with Hajj are as for HBV. Fulminant viral hepatitis is several times higher with HDV infection than in infection with HBV alone.68 There is no effective vaccine for HDV but immune prophylaxis is available indirectly through HBV vaccination. Routine screening for blood and blood products for HDV is unnecessary, as it cannot infect alone. The worldwide overall prevalence of HDV is decreasing due at least partly to improved HBV immunisation.69
Hepatitis E Epidemiology Hepatitis E virus (HEV) infection is a relatively new emerging infectious disease endemic in Central and Southeast Asia from where the majority of pilgrims attend the Hajj. Outbreaks affecting several hundred to several thousand people have been reported in the Middle East, and Northern and Western Africa.70 There it accounts for a substantial proportion of sporadic acute hepatitis predominantly affecting male adults and causing mild or subclinical disease in children. People from non-endemic countries e.g., Europe and North America who travel to high prevalence countries are at risk of infection.71 Like hepatitis A, once excreted in faeces it can survive in sewage, and the faeco-oral route is the predominant mode of transmission. Person to person transmission is uncommon but not impossible in crowded settings. Viral excretion predates the onset of illness; symptoms develop 2e10 weeks after becoming infected. Although HEV infections do not become chronic and have overall low mortality of less than 0.1% they cause high mortality in pregnant women.72
244
Hajj-associated risks The true incidence of HEV among Hajjis is difficult to establish as the disease often runs an anicteric sub-clinical course with non-specific symptoms resembling acute viral febrile illness and most patients are likely to present after they have left Mecca. However, the potential for outbreaks is not easily understated as the virus is usually acquired by drinking water.71 Pilgrims usually drink plenty of fluids and are advised to do so to prevent heat exhaustion that affect thousands of Hajj pilgrims during the hot weather.73 HEV outbreaks related to water contamination are well documented in some parts of Saudi Arabia.74 While the Saudi authorities provide safe potable water that is free of charge during the Hajj, a large number of pilgrims do not participate in organised programmes, sleep in streets and are unaware of health advice and do not accept drinking water provided.
Prevention As yet, no vaccine is available for HEV and preventive measures are otherwise similar to those of HAV. However, several potential vaccines are undergoing trials and a recombinant protein vaccine seems promising.75
Other types of hepatitis Arthropod borne viral haemorrhagic fevers due to arboviruses have the potential of causing outbreaks in the Arabian Peninsula. Two, which may cause hepatitis, are Alkhumra haemorrhagic fever virus and Rift Valley fever virus.
Alkhumra hemorrhagic fever virus This is a tick borne encephalitis virus within the genus flavivirus discovered in 1995, and associated with the Hajj because of increased animal movement and slaughtering.76,77 Its vector Ornithodoros savignyi, the sand tampan, is a multiple-host seeking, nocturnally active, cryptic tick that commonly attacks humans and other animals resting under trees.78 Thirty-seven cases of Alkhumra virus infections were reported solely in Mecca in 2001e2002.76,77 All cases isolated from 1994 to 1995 in Mecca or Jeddah were likely to have been contacted through a skin wound, tick bite or consumption of unpasteurised camel milk.79 Clinical features in Saudi outbreaks include acute febrile flu-like illness and hepatitis (100%), hemorrhagic manifestations (55%), and encephalitis (20%). The case-fatality rate is >30%.77 Genetic analysis of several human strains sequentially isolated over a 5-year period showed a very low diversity suggesting a slow microevolution and advantage for producing an effective vaccine.79
S.M. Rafiq et al. believed to be the explanation for the outbreak in Saudi Arabia between August and November 2000.80 Although the Saudi government has since imposed movement restriction for cattle and compulsory vaccination with live attenuated vaccine, infected cattle were identified in Saudi Arabia in 2004.81 The risk of transmission of the virus is greatest at the time of killing, when aerosols of infected blood may be generated, particularly through traditional slaughtering practices. The Somali black-headed or fat-tailed sheep, which originate in high prevalence areas fetch the highest price at the Hajj may also be infected and if viraemic at the time of slaughter, may be infectious to humans.81 This virus can disseminate easily via droplet, aerosol or direct contamination of a wound. Unlike brucellosis many animals will be asymptomatic but infectious. An inactivated vaccine has been developed for human use but has not yet been licensed.80 Therefore, careful hygiene in handling animals is the only current preventive measure, though the Saudi Arabian Ministry of Agriculture and Water uses systematic mosquito control as well as restricting animal movement and requiring their vaccination.
Conclusions Viral hepatitis is a risk of the Hajj, yet no study has quantified this risk. Most pilgrims attend lectures organised by the tour groups, mosques or other community organisations to prepare them for the Hajj events and their travel, including their travel immunisations. Education for infection control, safe food and water handling, head shaving and the disposal of sharps could be offered during these pre-travel lectures/seminars. Vaccination against hepatitis A and B should be recommended for all non-immune pilgrims. Mandatory screening for hepatitis B, C and HIV for the barbers and banning unlicensed barbers, chefs, butchers and cuppers should also be considered. This opportunity should also be taken to undertake a prospective prevalence study to assess the burden of hepatitis and risk factors among Hajj pilgrims from the UK, whence 25,000 or more pilgrims travel to the Hajj annually.
Conflict of interest statement On occasion RB has received financial support by vaccine producers, including CSL, Sanofi, GSK, Roche and Wyeth, to attend/present at scientific meetings; if fees were offered, these were placed in a university research account. The other authors declare that they have no conflict of interest in relation to this work.
Rift Valley fever
Acknowledgements
Rift Valley fever is a zoonotic phleboviral infection transmitted by mosquitoes and endemic in Africa. Hepatitis and hepato-renal syndrome are common and when haemorrhagic, mortality is high. Importation of livestock from African countries for slaughter at the Hajj is
The authors wish to thank Dr Nasser Al Hamdan, supervisor of the Field Epidemiology Training Program (FETP) Saudi Arabia, for supplying the image of head shaving during the Hajj (Fig. 1) and rare copies of Saudi Epidemiology Bulletin.
Hazards of hepatitis at the Hajj
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246 51. Hutchinson SJ, Bird SM, Goldberg DJ. Modeling the current and future disease burden of hepatitis C among injecting drug users in Scotland. Hepatology 2005;42:711e23. 52. Anonymous. EASL international consensus conference on hepatitis C. Paris, 26e27 February 1999. Consensus statement. J Hepatol 1999;31:3e8. 53. Bruno S, Facciotto C. The natural course of HCV infection and the need for treatment. Ann Hepatol 2008;7:114e9. 54. Alter MJ. Epidemiology of hepatitis C virus infection. World J Gastroenterol 2007;13:2436e41. 55. Zein NN. Hepatitis C in children: recent advances. Curr Opin Pediatr 2007;19:570e4. 56. Alter MJ. Prevention of spread of hepatitis C. Hepatology 2002; 36:S93e8. 57. Khan NA, Ishag AM, Ahmad MS, El-Sayed FM, Bachal ZA, Abbas TG. Pattern of medical diseases and determinants of prognosis of hospitalization during 2005 Muslim pilgrimage Hajj in a tertiary care hospital. Saudi Med J 2006;27:1373e80. 58. Mahaba H, el-Tayeb Ael-K, Elbaz H. The prevalence of antibodies to hepatitis C virus in Hail region, Saudi Arabia. Egypt Public Health Assoc 1999;74:69e80. 59. Lock G, Dirscherl M, Obermeier F, et al. Hepatitis C e contamination of toothbrushes: myth or reality? J Viral Hepat 2006;13:571e3. 60. Gatrad AR, Aziz S. Risk factors for HIV/AIDS in Muslim communities. Divers Health Soc Care 2004;1:65e9. 61. Foster G, Mathurin P. Hepatitis C virus therapy to date. Antivir Ther 2008;13:3e8. 62. D’Souza R, Foster GR. Diagnosis and treatment of hepatitis C. R Soc Med 2004;97:223e5. 63. Desbois D, Vaghefi P, Savary J, Dussaix E, Roque-Afonso AM. Sensitivity of a rapid immuno-chromatographic test for hepatitis C antibodies detection. J Clin Virol 2008;41:129e33. 64. Taylor JM. Structure and replication of hepatitis delta virus RNA. Curr Top Microbiol Immunol 2006;307:1e23. 65. Hadziyannis SJ. Decreasing prevalence of hepatitis D virus infection. J Gastroenterol Hepatol 1997;12:745e6. 66. Huo TI, Wu JC, Lin RY, Sheng WY, Chang FY, Lee SD. Decreasing hepatitis D virus infection in Taiwan: an analysis of contributory factors. J Gastroenterol Hepatol 1997;12:747e51. 67. Cross TJ, Rizzi P, Horner M, Jolly A, Hussain MJ, Smith HM, et al. The increasing prevalence of hepatitis delta virus (HDV) infection in south London. J Med Virol 2008;80:277e82.
S.M. Rafiq et al. 68. Flodgren E, Bengtsson S, Knutsson M, et al. Recent high incidence of fulminant hepatitis in Samara, Russia: molecular analysis of prevailing hepatitis B and D virus strains. J Clin Microbiol 2000;38:3311e6. 69. Hsieh TH, Liu CJ, Chen DS, Chen PJ. Natural course and treatment of hepatitis D virus infection. J Formos Med Assoc 2006;105:869e81. 70. Krawczynski K, Kamili S, Aggarwal R. Global epidemiology and medical aspects of hepatitis E. Forum (Genova) 2001;11: 166e79. 71. Zuckerman JN. Hepatitis E and the traveller. Travel Med Infect Dis 2003;1:73e6. 72. Navaneethan U, Al Mohajer M, Shata MT. Hepatitis E and pregnancy: understanding the pathogenesis. Liver Int 2008;28: 1190e9. 73. Khogali M. Epidemiology of heat illnesses during the Makkah pilgrimages in Saudi Arabia. Int J Epidemiol 1983;12: 267e73. 74. Arif M, Qattan I, al-Faleh F, Ramia S. Epidemiology of hepatitis E virus (HEV) infection in Saudi Arabia. Ann Trop Med Parasitol 1994;88:163e8. 75. Shrestha MP, Scott RM, Joshi DM, et al. Safety and efficacy of a recombinant hepatitis E vaccine. N Engl J Med 2007;356: 895e903. 76. Charrel RN, Zaki AM, Attoui H, et al. Complete coding sequence of the alkhurma virus, a tick-borne flavivirus causing severe hemorrhagic fever in humans in Saudi Arabia. Biochem Biophys Res Commun 2001;287:455e61. 77. Zaki AM. Isolation of a flavivirus related to the tick-borne encephalitis complex from human cases in Saudi Arabia. Trans R Soc Trop Med Hyg 1997;91:179e81. 78. Charrel RN, Fagbo S, Moureau G, Alqahtani MH, Temmam S, de Lamballerie X. Alkhurma hemorrhagic fever virus in ornithodoros savignyi ticks. Emerg Infect Dis 2007;13:153e5. 79. Charrel RN, Zaki AM, Fakeeh M, et al. Low diversity of alkhurma hemorrhagic fever virus, Saudi Arabia, 1994e1999. Emerg Infect Dis 2005;11:683e8. 80. Madani TA, Al-Mazrou YY, Al-Jeffri MH, et al. Rift valley fever epidemic in Saudi Arabia: epidemiological, clinical, and laboratory characteristics. Clin Infect Dis 2003;37: 1084e92. 81. Davies FG. Risk of a rift valley fever epidemic at the haj in Mecca, Saudi Arabia. Rev Sci Tech 2006;25:137e47.
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Hazards of hepatitis at the Hajj Shafquat M. Rafiq a,*, Harunor Rashid b, Elizabeth Haworth c, Robert Booy b,d a
Unit of Gastroenterology, Department of Medicine, Epsom and St Helier University Hospitals NHS Trust, Dorking Road, KT18 7EG, Surrey, UK b Academic Unit of Child Health, Barts and the London Queen Mary’s School of Medicine and Dentistry, London, UK c Health Protection Agency, South East, London, UK d National Centre for Immunisation Research and Surveillance of Vaccine Preventable Diseases, The Children’s Hospital at Westmead and The University of Sydney, New South Wales, Australia Received 25 August 2008; accepted 8 September 2008 Available online 21 November 2008
KEYWORDS Accelerated vaccination schedule; Blood borne hepatitis; Enteral viral hepatitis; Muslims; Pilgrimage; Travel
Summary While an increased risk of hepatitis is associated with travel, the risk of hepatitis associated with the Islamic Hajj pilgrimage to Mecca, Saudi Arabia has not been carefully quantified. Conditions unique to this gathering can pose the risk of both enteral and parenteral viral hepatitis. During this congregation, pilgrims stay in tents shared by 100 or more people often living on foods from street vendors and sharing common toilet facilities that can expose them to both hepatitis A and E. To mark the end of the festival, head shaving or trimming by fellow pilgrims or street barbers, who often re-use their razor may expose them to hepatitis B or C. Pilgrims are also at risk of cuts to the hands and feet while sacrificing cattle and walking barefooted, which may further increase the risk of parenteral viral hepatitis. Emerging diseases such as Alkhumra virus and Rift Valley fever, which may cause hepatitis, are also potentially important for the Hajj pilgrims. Improved health education to increase awareness about the risk of these diseases and appropriate immunisations, particularly hepatitis A and B vaccines, could play an important role. ª 2008 Elsevier Ltd. All rights reserved.
Introduction For over 1400 years practicing Muslims have undertaken the annual Hajj pilgrimage in Mecca, Saudi Arabia, said to be the world’s largest organised annual mass gathering. While performing the Hajj to improve their spiritual health,
* Corresponding author. Tel.: þ44 (0) 1372 735119; fax: þ44 (0) 1372 735955. E-mail address: [email protected] (S.M. Rafiq).
through unity, goodwill and sacrifice, faithful Muslims may put their physical health at risk, particularly from infections.1,2 Swiss traveller John Lewis Burckhardt, who made his journey to Mecca in 1813 in disguise as a Muslim pilgrim, is believed to be the first European to record the infectious hazards of the Hajj.3 Studying the works of Arab historians Asamy and Fasy, Burckhardt recorded that there was an outbreak of an unspecified ‘pestilence’ in Arabic year 671 (circa 1271 AD) that killed 50 persons a day and another in Arabic year 829 (circa 1424 AD), when 2000 people died
1477-8939/$ - see front matter ª 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tmaid.2008.09.008
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during the Hajj.3 Burckhardt himself reported occurrence of ‘intermittent fever’ (probably referring to malaria), ‘putrid fever’ (probably referring to diphtheria or typhus fever) and dysentery in Mecca during his visit. The Hajj more recently came to world attention because of outbreaks of meningococcal diseases (of note Meningococcus W135) that affected more than 2400 people all over the world during and following the Hajj 2000 and 2001.4,5 At least three distinct categories of health risks are associated with the Hajj: those related to travel e.g., travellers’ diarrhoea, malaria, jet lag; those related to crowding e.g., respiratory infections including meningococcal disease, influenza and tuberculosis; and those relating to ritual practices e.g., stampede, blood borne infections. The rites of the Hajj start well before reaching Greater Mecca when pilgrims change their garments to a pair of white unstitched sheets symbolising death shrouds as a ‘departure from the mundane world’.6,7 They then refrain from using scented toiletries, having sexual relationships, shaving or trimming hair and cutting nails. After days of physically demanding rituals that involve walking long distances barefooted, marching between two hillocks named Safa and Marwah, a daylong stay at the plain of Arafat, pelting stones at a symbolic Satan and sacrificing cattle, pilgrims have their hair shaved or cut to mark the end of the festival (Fig. 1).1,7,8 Risk of both blood borne, and food and water borne viral hepatitis associated with travel is well recognised,9,10 but the risk of hepatitis in relation to the Hajj pilgrimage has not been formally assessed. We have therefore reviewed the published literature to inform the risks of viral hepatitis in relation to the Hajj pilgrimage.
Search strategy We undertook a Medline search using terms ‘Hajj AND Hepatitis’, ‘Hajj AND Liver disease’, ‘Saudi Arabia AND
Hepatitis’, ‘Mecca AND Hepatitis’ and ‘Travel AND Hepatitis’ and the alternative spelling ‘Haj’ or ‘Hadj’, with emphasis on the latest publications. Hand searching of identified articles was done to spot other relevant articles from the references they cited. Journals in hepatology, hepatitis, gastroenterology and infectious diseases, which are not indexed in Medline, were also searched from their respective websites through the ‘Google’ search engine. Archives or older publications were accessed from the British Library and the library of Islamic Cultural Centre, London, UK.
Hepatitis A Epidemiology Hepatitis A virus (HAV) is an RNA virus with worldwide distribution and the disease it causes is the commonest vaccine preventable illness among international travellers.10 Evidence of past infection is nearly universal in adults from sanitation poor areas of Africa, Asia and South America where people usually acquire asymptomatic infections in childhood.11 Since infection usually confers lifelong immunity,12 those born and raised in endemic countries and those born in developed countries before 1945 (when HAV was still common there) are likely to be immune to the disease.13 Thus pilgrims under the age of 60 travelling from low endemic zone i.e., Europe, USA, Canada, Australia, New Zealand, Japan and other countries with decreasing anti-HAV status, are usually susceptible to infection, while residents from endemic zones are not. Estimated attack rates for European travellers to Middle East are approximately 181 per 1000 journeys.10 Transmission is generally by the faeco-oral route and spreads person-to-person because of overcrowding and poor personal hygiene or via ingestion of contaminated water or food.11 Rarely (<5%) spread may occur through transfusion of blood or blood products.14
Hajj-associated risks
Figure 1
Pilgrims are helping each other by shaving heads.
Safe drinking water is supplied during the Hajj and the risk of water borne transmission is low. However, ice used to cool water and beverages in hot and humid weather may be from unknown sources, and thus runs the risk of contamination. Foods, particularly unpeeled fruits and vegetables, also may be contaminated with HAV. Although Saudi Arabia has banned visitors and pilgrims from bringing foods into the country, a survey among the Hajj pilgrims suggest that 37% did bring foodstuff from home countries.15 Thirty-four percent pilgrims bought foods from street vendors, many of whom were hawkers or operated from makeshift shops with dubious hygiene standards.15 Communal use of toilets, avoidance of soaps and detergents (due to their perfume) or alcohol hand rubs during tent living in Mina may increase the risk of HAV infection.16 Person-to-person contact during different rituals e.g., during circumambulation, SafaeMarwah marching and Arafat standing also may increase infection risks.
Hazards of hepatitis at the Hajj
Prevention Good personal, food and drink hygiene reduces infection risks. Key advice is ‘boil it, cook it, peel it or leave it’.13 Pre-travel advice, contact tracing and post-exposure prophylaxis will help in prevention of spread.17 At least 6 inactivated hepatitis A vaccines as well as 2 combined hepatitis A and hepatitis B vaccines confer active immunity.12,18 Inactivated HAV vaccines are safe, highly immunogenic and provide long-term (up to 25 years) protection from HAV infection.19 They can be administered simultaneously with a number of other vaccines without compromising immunogenicity.20 Although the antibody level achieved after immunisation with vaccine is 10e100 times lower than that achieved through natural infection,21 protective levels (>10 IU/mL) are achieved in 98% after 4 weeks and even in 70% 2 weeks after vaccination.21,22 Testing for immunity before vaccination may be costeffective in people highly likely to be immune from previous exposure e.g., first generation adult immigrants to low prevalence countries.21 If administered no more than 14 days after exposure, intramuscular immunoglobin can confer short-term immunity to prevent symptoms in 70e 90%, or attenuate them and reduce further transmission.23,24 The immunoglobulin can be administered to children who do not have or have lost protection due to transferred maternal antibodies.25
Hepatitis B Epidemiology Hepatitis B virus (HBV) is an enveloped DNA virus containing partially double stranded, circular genome.26,27 The virus has eight major genotypes (AeH) clustered in different parts of the world to create a somewhat heterogeneous clinical history, and response to treatment.28 HBV is highly adaptive, producing vaccine-related escape mutants and drug resistance. Chronic infection can lead to cirrhosis, hepatocellular carcinoma (HCC) and death from liver failure. Worldwide more than 2 billion people (one third of the world population) have been infected with HBV (Fig. 2), and up to 80% of all HCC have been attributed to HBV infection.29 Although most of those infected develop anti-HBs antibody and remain well, chronicity (persistence of surface antigenaemia 6 month) develops in approximately 350 million people worldwide.30 Among those infected, more than 4 million of acute clinical cases and more than 1 million of chronic carriers die from liver diseases each year.31 Of 40 million known HIV positives, 3 million are coinfected with HBV and 4.5 million with hepatitis C virus (HCV) respectively.32 Depending on geographical location, co-infection of HBV with HCV varies from 9% to 30%.33,34 The prevalence of HBV infections varies from about 8% in the Far East, parts of Middle East, sub-Saharan Africa and Amazon basin i.e., high prevalence areas to <1% in low prevalence countries such as the UK, Australia and North America. Mass travel, migration and introduction of vaccine are, however, changing the epidemiology of HBV infection.29,31,35,36 HBV is transmitted parenterally or through
241 a breach in skin or mucus membrane when these encounter infected blood or body fluids. It can remain infective on surfaces it is exposed to, e.g., razor blades and tabletops, for up to one week.32 All hepatitis B surface antigen (HbsAg) positive individuals are potentially infectious. Where HBV is endemic most transmission occurs from mother to children or from child to child in household settings but in western countries with low endemicity most infections are acquired in adulthood as a result of high risk sexual activity and/or sharing needles and syringes for injecting drugs.29,37 Risk of chronicity is inversely related to age: chronic carriage will develop in up to 90% of infants when infected at birth compared with 5e10% of those who become infected as adults.29,38
Hajj-associated risks A large number of pilgrims attending the Hajj pilgrimage are from countries with intermediate to high HBV prevalence (Table 1) and HBV infection is endemic in Saudi Arabia.39 The head shaving practice among pilgrims is of particular concern in transmitting HBV and other blood borne diseases.40e42 To mark the end of the festival around 90% men get their heads shaved either by barbers or by fellow pilgrims (Fig. 1).43 In two separate studies, 61% Hajjis had cuts to scalp (maximum of 18 cuts) and 25% used shared razors.15,43 Although testing for HBV and HCV, and the use of disposable blades are mandatory for barbers, a 1999-survey among barbers showed that 4% were HBsAg positive, 0.6% hepatitis B e antigen (HbeAg) positive and 10% positive for HCV.43 During the Hajj period a large number of unlicensed barbers operate, most of them arriving from high prevalence areas, practise along roadsides and are unaware of infection control. In a study in 1998, 23% of barbers had open hand wounds, 21% used the same blade for more than one shave and 82% threw at least one used blade to the ground.40 The latter finding is significant as pilgrims walk long distances barefooted or lose their slippers in the crowds after pebble throwing.
Prevention Active immunisation remains the single most effective measure for HBV prevention.44 Routine infant hepatitis B vaccination with 90% coverage and the first dose administered at birth would prevent most HBV infection and an estimated 84% of global HBV-related deaths.45 Although response to vaccination is somewhat lower in adults over 40, the risk of infection in travellers who receive 3 doses is negligible (post-immunisation testing is not routine).10 A 4dose schedule (at 0, 1, 2, 12 months) of HBV vaccine is also highly effective immediately after exposure.46 An accelerated schedule is available for last minute travellers (at 0, 7, 21 days) and may be useful for Hajj pilgrims.42,47 As 70% of Hajj pilgrims and 20% of barbers were not aware of risks of infections associated with razor blades,40 pre-Hajj health education of pilgrims and barbers, tighter control of barbers and safe disposal of razor blades and other shaving waste is also necessary. Promising results have been obtained from culturally tailored lectures on prevention of hepatitis B among AsianeAmerican communities in the USA.48
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Figure 2
Global distribution of hepatitis B.
Hepatitis C Epidemiology Hepatitis C virus (HCV) is an enveloped single stranded RNA virus that was isolated in 1989 as the cause for most transfusion related non-A non-B viral hepatitis in humans.49 So far, 11 genotypes with several distinct subtypes have been identified across the world and this variation relates to the significant heterogeneity in response to treatment and is a major obstacle to developing a single effective vaccine. Genotype 4 is the commonest (70%) in the western province of Saudi Arabia where Mecca is situated.50 Chronicity develops in up to 80% people infected with HCV,51,52 10e15% of whom develop cirrhosis within 20 years and ‘‘the progression to cirrhosis is often clinically silent, and some patients are not known to have hepatitis C until they present with the complications of end-stage liver disease or HCC’’.53
Table 1 Examples of some countries that send a major proportion of pilgrims to the Hajj and their hepatitis B prevalence. Country
Population Number of pilgrims % HBsAg (millions) per year prevalence
Saudi Arabia Indonesia Pakistan India Turkey Iran Nigeria Egypt Bangladesh UK USA
24.7 231.6 163.9 1135.9 70.6 70.5 148.1 75 153.6 60.6 304.7
1000000 200000 150000 170000 120000 100000 90000 75000 65000 25000 10000
5 4 3.3 4.7 6.6 3 15 10.1 5 0.6 0.5
It is estimated that approximately 170 million individuals (3% of world population) have been infected with HCV with the prevalence ranging from <1.0% in Northern Europe to >10% in the African and Eastern Mediterranean countries (Fig. 3).49,54 HCV is transmitted by sharing needles or syringes with an infected person or by exposure to infected blood.49 Sexual transmission is less efficient than for HBV or HIV, and vertical transmission is generally uncommon but still well documented and is the most frequent mode of hepatitis C acquisition in children.55 In a tenth of HCV carriers no source can be identified.56 Community acquired HCV is thought to be associated with sharing personal articles such as toothbrushes, razors and nail scissors or with contaminations of wounds.54
Hajj-associated risks As is the case with HBV, people from hepatitis C endemic countries converge at the Hajj pilgrimage. Well-defined risk factors for hepatitis C transmission e.g., unsafe sex and intravenous drug use are not known to be problems due to prohibitions (sexual intercourse even with the own partner is prohibited during the key festival) and strong religious commitments. However, risks related to transfusion of blood or blood products and nosocomial infection cannot be understated as huge number of Hajjis require admission to hospitals. For instance, of 689 pilgrims belonging to 49 countries (many of these were HCV endemic countries) who were admitted to one of the six tertiary hospitals in Mecca for treatment of medical conditions during the Hajj 2005 5% (n Z 32) were admitted for complications of chronic liver disease and another 5% (n Z 34) for upper gastrointestinal bleeding, a common presentation of variceal bleeding.57 Although routine screening of blood has been implemented in Saudi Arabia, the prevalence of anti HCV antibody is 4.3% of blood donors and 2.2% of medical staff in a tertiary hospital close to Mecca.58 In a study of 30 HCV infected patients to assess possibility of transmission via tooth brushing saliva and
Hazards of hepatitis at the Hajj
243
Figure 3
Global distribution of hepatitis C.
rinsing water were tested for HCV RNA before and after brushing. Saliva was positive in 30% and 36.7% cases before and after brushing respectively, while rinsed water was positive in 40% cases.59 This demonstrates at least theoretical risk of transmission through gurgling and sharing utensils including dental sticks, which many devout Muslims use regularly to clean their teeth before every prayer.60 As pilgrims stay together as groups in tents, they are also likely to share personal articles such as nail clippers and scissors to add to the risk of HCV transmission.
Prevention So far, no effective vaccine or immunoglobulin has been available to prevent HCV. Clinical awareness of the disease associated with early diagnosis and treatment with combination therapy with pegylated interferon and ribavirin improves its prognosis.61,62 Preventive strategies include implementation and practice of infection control measures, general pre-Hajj advice on personal care and covering of cuts and wounds and counselling known infected or at risk persons, although the latter might be difficult in Hajj settings. Newer sensitive quick immune chromatographic tests could help rapid detection of high risk cases to initiate early treatment and take necessary measures for secondary prevention.62,63
Hepatitis D Hepatitis D or delta virus (HDV) is a defective RNA virus, which uses HBsAg as its own virion coat and requires coinfection with HBV for replication.64 Approximately 5% of chronic HBV carriers are co-infected with HDV either concurrently or as a super-infection in those already HBsAg positive. Although a declining trend has been observed for a decade, recent increase in prevalence is being reported in some areas, for example in parts of London.65e67 Coinfection may lead to more severe disease or higher risks of
severe complications e.g., cirrhosis or HCC. Its distribution is as for HBV infection with epidemics occurring in the Mediterranean, Amazon basin and Central Africa. It has a similar transmission pattern to HBV since HBsAg envelops it, and risks associated with Hajj are as for HBV. Fulminant viral hepatitis is several times higher with HDV infection than in infection with HBV alone.68 There is no effective vaccine for HDV but immune prophylaxis is available indirectly through HBV vaccination. Routine screening for blood and blood products for HDV is unnecessary, as it cannot infect alone. The worldwide overall prevalence of HDV is decreasing due at least partly to improved HBV immunisation.69
Hepatitis E Epidemiology Hepatitis E virus (HEV) infection is a relatively new emerging infectious disease endemic in Central and Southeast Asia from where the majority of pilgrims attend the Hajj. Outbreaks affecting several hundred to several thousand people have been reported in the Middle East, and Northern and Western Africa.70 There it accounts for a substantial proportion of sporadic acute hepatitis predominantly affecting male adults and causing mild or subclinical disease in children. People from non-endemic countries e.g., Europe and North America who travel to high prevalence countries are at risk of infection.71 Like hepatitis A, once excreted in faeces it can survive in sewage, and the faeco-oral route is the predominant mode of transmission. Person to person transmission is uncommon but not impossible in crowded settings. Viral excretion predates the onset of illness; symptoms develop 2e10 weeks after becoming infected. Although HEV infections do not become chronic and have overall low mortality of less than 0.1% they cause high mortality in pregnant women.72
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Hajj-associated risks The true incidence of HEV among Hajjis is difficult to establish as the disease often runs an anicteric sub-clinical course with non-specific symptoms resembling acute viral febrile illness and most patients are likely to present after they have left Mecca. However, the potential for outbreaks is not easily understated as the virus is usually acquired by drinking water.71 Pilgrims usually drink plenty of fluids and are advised to do so to prevent heat exhaustion that affect thousands of Hajj pilgrims during the hot weather.73 HEV outbreaks related to water contamination are well documented in some parts of Saudi Arabia.74 While the Saudi authorities provide safe potable water that is free of charge during the Hajj, a large number of pilgrims do not participate in organised programmes, sleep in streets and are unaware of health advice and do not accept drinking water provided.
Prevention As yet, no vaccine is available for HEV and preventive measures are otherwise similar to those of HAV. However, several potential vaccines are undergoing trials and a recombinant protein vaccine seems promising.75
Other types of hepatitis Arthropod borne viral haemorrhagic fevers due to arboviruses have the potential of causing outbreaks in the Arabian Peninsula. Two, which may cause hepatitis, are Alkhumra haemorrhagic fever virus and Rift Valley fever virus.
Alkhumra hemorrhagic fever virus This is a tick borne encephalitis virus within the genus flavivirus discovered in 1995, and associated with the Hajj because of increased animal movement and slaughtering.76,77 Its vector Ornithodoros savignyi, the sand tampan, is a multiple-host seeking, nocturnally active, cryptic tick that commonly attacks humans and other animals resting under trees.78 Thirty-seven cases of Alkhumra virus infections were reported solely in Mecca in 2001e2002.76,77 All cases isolated from 1994 to 1995 in Mecca or Jeddah were likely to have been contacted through a skin wound, tick bite or consumption of unpasteurised camel milk.79 Clinical features in Saudi outbreaks include acute febrile flu-like illness and hepatitis (100%), hemorrhagic manifestations (55%), and encephalitis (20%). The case-fatality rate is >30%.77 Genetic analysis of several human strains sequentially isolated over a 5-year period showed a very low diversity suggesting a slow microevolution and advantage for producing an effective vaccine.79
S.M. Rafiq et al. believed to be the explanation for the outbreak in Saudi Arabia between August and November 2000.80 Although the Saudi government has since imposed movement restriction for cattle and compulsory vaccination with live attenuated vaccine, infected cattle were identified in Saudi Arabia in 2004.81 The risk of transmission of the virus is greatest at the time of killing, when aerosols of infected blood may be generated, particularly through traditional slaughtering practices. The Somali black-headed or fat-tailed sheep, which originate in high prevalence areas fetch the highest price at the Hajj may also be infected and if viraemic at the time of slaughter, may be infectious to humans.81 This virus can disseminate easily via droplet, aerosol or direct contamination of a wound. Unlike brucellosis many animals will be asymptomatic but infectious. An inactivated vaccine has been developed for human use but has not yet been licensed.80 Therefore, careful hygiene in handling animals is the only current preventive measure, though the Saudi Arabian Ministry of Agriculture and Water uses systematic mosquito control as well as restricting animal movement and requiring their vaccination.
Conclusions Viral hepatitis is a risk of the Hajj, yet no study has quantified this risk. Most pilgrims attend lectures organised by the tour groups, mosques or other community organisations to prepare them for the Hajj events and their travel, including their travel immunisations. Education for infection control, safe food and water handling, head shaving and the disposal of sharps could be offered during these pre-travel lectures/seminars. Vaccination against hepatitis A and B should be recommended for all non-immune pilgrims. Mandatory screening for hepatitis B, C and HIV for the barbers and banning unlicensed barbers, chefs, butchers and cuppers should also be considered. This opportunity should also be taken to undertake a prospective prevalence study to assess the burden of hepatitis and risk factors among Hajj pilgrims from the UK, whence 25,000 or more pilgrims travel to the Hajj annually.
Conflict of interest statement On occasion RB has received financial support by vaccine producers, including CSL, Sanofi, GSK, Roche and Wyeth, to attend/present at scientific meetings; if fees were offered, these were placed in a university research account. The other authors declare that they have no conflict of interest in relation to this work.
Rift Valley fever
Acknowledgements
Rift Valley fever is a zoonotic phleboviral infection transmitted by mosquitoes and endemic in Africa. Hepatitis and hepato-renal syndrome are common and when haemorrhagic, mortality is high. Importation of livestock from African countries for slaughter at the Hajj is
The authors wish to thank Dr Nasser Al Hamdan, supervisor of the Field Epidemiology Training Program (FETP) Saudi Arabia, for supplying the image of head shaving during the Hajj (Fig. 1) and rare copies of Saudi Epidemiology Bulletin.
Hazards of hepatitis at the Hajj
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