Tuberculosis in migrants moving from high-incidence to low-incidence countries: a population-based cohort study of 519 955 migrants screened before entry to England, Wales, and Northern Ireland

Abstract

Background: Tuberculosis elimination in countries with a low incidence of the disease necessitates multiple interventions, including innovations in migrant screening. We examined a cohort of migrants screened for tuberculosis before entry to England, Wales, and Northern Ireland and tracked the development of disease in this group after arrival.

Methods: As part of a pilot pre-entry screening programme for tuberculosis in 15 countries with a high incidence of the disease, the International Organization for Migration screened all applicants for UK visas aged 11 years or older who intended to stay for more than 6 months. Applicants underwent a chest radiograph, and any with results suggestive of tuberculosis underwent sputum testing and culture testing (when available). We tracked the development of tuberculosis in those who tested negative for the disease and subsequently migrated to England, Wales, and Northern Ireland with the Enhanced Tuberculosis Surveillance system. Primary outcomes were cases of all forms of tuberculosis (including clinically diagnosed cases), and bacteriologically confirmed pulmonary tuberculosis.

Findings: Our study cohort was 519 955 migrants who were screened for tuberculosis before entry to the UK between Jan 1, 2006, and Dec 31, 2012. Cases notified on the Enhanced Tuberculosis Surveillance system between Jan 1, 2006, and Dec 31, 2013, were included. 1873 incident cases of all forms of tuberculosis were identified, and, on the basis of data for England, Wales, and Northern Ireland, the estimated incidence of all forms of tuberculosis in migrants screened before entry was 147 per 100 000 person-years (95% CI 140-154). The estimated incidence of bacteriologically confirmed pulmonary tuberculosis in migrants screened before entry was 49 per 100 000 person-years (95% CI 45-53). Migrants whose chest radiographs were compatible with active tuberculosis but with negative pre-entry microbiological results were at increased risk of tuberculosis compared with those with no radiographic abnormalities (incidence rate ratio 3·2, 95% CI 2·8-3·7; p<0·0001). Incidence of tuberculosis after migration increased significantly with increasing WHO-estimated prevalence of tuberculosis in migrants' countries of origin. 35 of 318 983 pre-entry screened migrants included in a secondary analysis with typing data were assumed index cases. Estimates of the rate of assumed reactivation tuberculosis ranged from 46 (95% CI 42-52) to 91 (82-102) per 100 000 population.

Interpretation: Migrants from countries with a high incidence of tuberculosis screened before being granted entry to low-incidence countries pose a negligible risk of onward transmission but are at increased risk of tuberculosis, which could potentially be prevented through identification and treatment of latent infection in close collaboration with a pre-entry screening programme.

Funding: Wellcome Trust, UK National Institute for Health Research, UK Medical Research Council, Public Health England, and Department of Health Policy Research Programme.

Figure 1

Locations of pre-entry screening sites Includes both International Organization for Migration sites and other sites. The pre-entry pilot scheme was done in Bangladesh, Burkina Faso, Cambodia, Côte d'Ivoire, Eritrea, Ghana, Kenya, Laos, Niger, Pakistan, Somalia, Sudan, Tanzania, Thailand, and Togo. Pre-entry screening was subsequently rolled out to 101 countries in four phases between May, 2012, and March 31, 2014.

Figure 2

Study participant flow chart IOM=International Organization for Migration. *Numbers assumed to migrate to Scotland varied by imputation, and the sum of those excluded does not equal the difference between total visa applicants and the number of migrants included in the final cohort, because groups were not mutually exclusive.

Figure 3

Cases of tuberculosis notified in migrants to England, Wales, and Northern Ireland (A), and incidence rates for tuberculosis (B), by time since entry (A) Includes 439 pre-entry prevalent cases detected between Jan 1, 2006, and Dec 31, 2012, post-entry missed prevalent cases (41 cases notified within 90 days after migration), and all tuberculosis cases (1873 cases) notified in the UK among migrants by year since migration. The error bars in (B) are 95% CIs.