Acquisition of W135 meningococcal carriage in Hajj pilgrims and transmission to household contacts: prospective study

The annual Islamic pilgrimage to Mecca and Medina (Hajj) attracts more than two million pilgrims from all over the world. Overcrowding provides ideal conditions for transmission of meningococci. During the Hajj 2000 an international outbreak of meningococcal disease occurred.¹ This outbreak generated particular interest as it was caused by serogroup W135, which hitherto had not played a major role in epidemics.^{2 3} Furthermore, many close contacts of asymptomatic returning pilgrims were affected.² Although vaccination can protect pilgrims against invasive disease due to W135, it does not prevent acquisition of pharyngeal carriage, which is the primary source for transmission.⁴ Returning pilgrims may spread the bacteria to their unvaccinated household contacts or even to the community at large. We investigated the extent of transmission of Neisseria meningitidis in Hajj pilgrims and their contacts, in order to provide evidence for developing a rational public health policy.

We conducted a prospective study of meningococcal carriage in Singaporean pilgrims before the Hajj 2001 and in pilgrims and their household contacts two weeks after return from the Hajj. We performed serogrouping and pulsed field gel electrophoresis on meningococcal isolates to determine the predominant serogroup and relatedness of the strains. We questioned participants about the occurrence of any symptoms of upper respiratory tract infection, use of antibiotics within the past month, and number of people in the household.

We took tonsillopharyngeal swabs from 204 Malay pilgrims at the time of vaccination with quadrivalent meningococcal vaccine (median 39 (range 18-72) days before their departure for the Hajj pilgrimage). Median age was 48 (24-74) years, and 92 (45%) were men. Only one of these pilgrims carried N meningitidis, which was identified as serogroup X.

We took repeat swabs from 171 (84%) of the pilgrims at a median of 17 (1-45) days after their return from the Hajj and found 29 (17.0%) to be meningococcal carriers (P<0.001 compared with carriage rate before the Hajj), as in the table. Ninety five (55.6%) returning pilgrims reported cough in the preceding month, and 70 (40.9%) reported use of antibiotics. Carriage was significantly higher in pilgrims who had not taken antibiotics than in in those who had taken antibiotics, but no relation existed between carriage and age, sex, or recent symptoms of upper respiratory tract infection (17/70 (24%) v 9/101 (9%); P=0.045).

*P<0.001 between pre-Hajj and post-Hajj pilgrims (McNemar test).

†Prevalence of pre-Hajj meningococcal carriage in the 171 pilgrims who returned for the post-Hajj swab was 0.6%.

Pulsed field gel electrophoresis showed that 26/29 (90%) meningococcal isolates in Hajj returnees were a single clone, identified as serogroup W135 in most cases and related to the strains that caused Hajj associated invasive meningococcal disease in Singapore.

The returning pilgrims reported a median of 4 (1-10) people living in their household. The total number of contacts (non-Hajj pilgrims within the same household) was 317. We took swabs from 233 (73.5%) of these household contacts at a median of 26 (3-45) days after the pilgrims return to the household. The median age of household contacts was 20 (1-67) years, and 165 (52%) were children under the age of 18. The prevalence of meningococcal carriage in household contacts was 8.2%, of whom 42% were carrying the W135 clone (3.4% of all household contacts). All but one of the contacts carrying the W135 clone were contacts of returning pilgrims with the W135 clone. Of the 26 pilgrims carrying the W135 clone (all from different households), six (23%) transmitted this strain to seven contacts, of whom two were from the same household. The acquisition rate of the W135 clone in contacts of returning carriers of the same strain was 13% (seven out of 54 contacts).

A high acquisition rate of a single clone of W135 N meningitidis occurred during the 2001 Hajj pilgrimage. Many countries currently give bivalent meningococcal vaccine (covering A and C) to Hajj pilgrims. Vaccination with the quadrivalent meningococcal vaccine (also covering W135) should be mandatory for all Hajj pilgrims and be considered for their household contacts. Transmission of this clone from vaccinated Hajj returnees to their unvaccinated household contacts was substantial, putting contacts at particular risk of developing invasive disease. Our findings support a policy of administering antibiotics to pilgrims before their return to their countries of origin to eradicate carriage and thereby protect household contacts.

We thank Fatimah Karim and Anushia Panchalingham for taking swabs, Bernard Peperstraete for logistical help, Sindhu Ravindran for performing pulsed field gel electrophoresis, and Gamini Kumarsinghe for providing some of the meningococcal isolates of clinical cases. We also thank all the pilgrims and their contacts for participating in this study.

Contributors: AW-S had the idea for the study and was responsible for study design and for collection, analysis, and interpretation of data. TMSB was responsible for the meningococcal cultures, serogrouping, and pulsed field gel electrophoresis. AE was responsible for data entry and analysis. NIP contributed to the study design and data analysis and interpretation. All authors contributed to the final manuscript. AW-S is the guarantor.

Funding: National Medical Research Council Singapore.

Competing interests: AW-S has been reimbursed by Glaxo SmithKline and Aventis for attending conferences. TMSB has been reimbursed by Oxoid, Bayer, and Bristol-Myers Squibb for attending conferences.

Annelies Wilder-Smith, Timothy M S Barkham, Arul Earnest, Nicholas I Paton
Travellers Health and Vaccination Centre, Tan Tock Seng Hospital, 11 Jalan Tan Tock Seng, Singapore 308433
Annelies Wilder-Smith head
Department of Pathology and Laboratory Medicine, Tan Tock Seng Hospital
Timothy M S Barkham
consultant microbiologist
Clinical Epidemiology Unit, Tan Tock Seng Hospital
Arul Earnest statistician
Department of Infectious Diseases, Tan Tock Seng Hospital
Nicholas I Paton head
Correspondence to: A Wilder-Smith epvws@pacific.net.sgk


studentBMJ 2002;10:353-396 October ISSN 0966-6494

1. Popovic T, Sacchi CT, Reeves MW, Whitney AM, Mayer LW, Noble CA, et al. Neisseria meningitidis serogroup W135 isolates associated with the ET- 37 complex. Emerg Infect Dis 2000;6:428-9
2. Taha MK, Achtman M, Alonso JM, Greenwood B, Ramsay M, Fox A, et al. Serogroup W135 meningococcal disease in Hajj pilgrims. Lancet2000;356:2159.
3. World Health Organization. Meningococcal disease, serogroup W135. Wkly Epidemiol Rec 2001;76:141-2.
4. Rosenstein NE, Perkins BA, Stephens DS, Popovic T, Hughes JM. Meningococcal disease. N Engl J Med 2001;344:1378-88.