Factors influencing the higher incidence of tuberculosis among migrants and ethnic minorities in the UK

Introduction

Tuberculosis (TB) is a bacterial disease caused by Mycobacterium tuberculosis (M.tb), which most commonly affects the lungs¹. M.tb infection is acquired by inhalation of infectious particles released from close contacts². While 10% of those infected develop active disease, the majority of individuals mount an effective immune response leading to successful containment of M.tb growth; a condition known as latent M.tb infection or LTBI³. Latent infection, which is asymptomatic, ordinarily has a 5–10% lifetime risk of reactivation². The main symptoms of active disease include persistent coughing (sometimes producing blood), sweating, fever, weakness and weight loss³. Untreated, the 10-year case fatality rate is between 54 and 86% in HIV-negative individuals⁴. In 15–20% of active cases, and usually in those with immunosuppression, the infection spreads outside the lungs causing extra-pulmonary TB⁵. LTBI may be diagnosed through cutaneous tuberculin skin test (TST) or interferon-γ release assays (IGRA), while clinically suspected TB disease is evaluated through chest radiograph and diagnostic microbiology for acid-fast bacilli. Effective antibiotic treatment is available, but involves long and complex regimens. Furthermore, rates of multi-drug-resistant TB (MDR-TB) and extensively-drug-resistant TB (XDR-TB) are increasing⁶.

Globalisation, conflict and financial reasons have become increasingly important drivers of migration flows, leading to more permanent migrants moving from low/middle income to high-income countries⁷. In the UK, a significant proportion of foreign-born migrants arrive from former colonies in sub-Saharan Africa and the Indian Subcontinent (ISC)⁸. Incidence of TB disease is higher among all migrant and ethnic minority groups living in the UK compared with the UK-born population. In 2015, 72.5% of individuals with diagnosed TB disease were foreign-born, with India and Pakistan the most frequent countries of birth among such cases⁹. While TB rates have been falling slowly across all UK populations since 2011, they remain 15 times higher in the foreign-born than the UK-born population. Furthermore, within the UK-born population, non-white ethnic groups had TB rates 3 to 19 times higher than the white ethnic group⁹. There is much heterogeneity in both absolute number of cases and incidence rates (per 100,000 of population group) among migrants from different countries and among different ethnic groups. While number of cases is confounded by size of population group, variation in incidence rate reflects varying levels of risk for different migrant and ethnic groups. Migrants from the ISC (India, Pakistan and Bangladesh) and black ethnic groups demonstrate particularly high incidence⁹.

We discuss the biological, social and cultural factors relating to risk of pathogen exposure, vulnerability to infection or development of active disease, and access to treatment which contribute to the increased incidence of TB in migrant and ethnic minorities in the UK (Figure 1).

Figure 1. Summary of factors contributing to the increased incidence of TB in migrant and ethnic minorities in the UK.

Epidemiology

The higher burden of TB observed among foreign-born individuals in the UK could be due to arrival of migrants with active TB, reactivation of remotely-acquired LTBI post-arrival, or local transmission¹⁰. Meta-analyses of screening for active TB at entry have indicated that only a small proportion (~0.35%) of immigrants have active TB at time of arrival in the EU/EEA^11,12. Since 2012, the UK Home Office has required pre-arrival screening for active pulmonary TB disease for all long-term visa applicants from endemic countries; those diagnosed with active disease are denied a medical clearance certificate¹³. Thus arrival of migrants with active TB is not thought to contribute significantly to the overall burden of disease among foreign-born individuals in the UK; rather several studies suggest a more prominent role for the reactivation of remotely-acquired LTBI post-arrival^10,14,15. In the initial years following arrival in a lower incidence setting, migrants with LTBI have a higher risk of reactivation than the host population^16–18.

Local transmission within immigrant communities in the UK may also contribute to the higher incidence of TB cases observed in migrants and ethnic minorities. Such groups are more likely to live in densely-populated areas with a high concentration of their ethnic community, which may foster spread of TB, particularly given the mode of transmission¹⁹. Moreover, Bakhshi suggests that larger household size among migrants and ethnic minorities - perhaps due to cultural factors favouring a multi-generational rather than nuclear family structure - increases M.tb transmission, as approximately one-third of household contacts will become infected in a household with an active TB case²⁰.

In order to establish the relative importance of local transmission versus reactivation of LTBI, molecular fingerprinting and typing techniques have been applied since the 1990s. Genomic clusters are assumed to represent epidemiologically linked chains of recent transmission, whereas unique isolates represent reactivational disease²¹. Early findings were conflicting, likely due to the inability of such techniques to reliably distinguish past and recent transmission²². The advent of whole-genome sequencing of M.tb offered additional resolution, and in one such study of Oxfordshire TB cases in 2007–2012, those born in a high-incidence country were less likely to be part of a genomic cluster than those born in a low-incidence country (especially the UK), even when adjusting for social risk factors²³. Furthermore, Aldridge et al. identified only 35 of over 300,000 migrants screened prior to entry into England, Wales and Northern Ireland as assumed index cases, defined as the first case in a genomic cluster²⁴. These findings suggest that reactivation of LTBI is more important in explaining the higher incidence of TB among migrants than exogenous infection due to local transmission.

Differential exposure

Rates of active TB disease diagnosed after arrival in the UK correlate with TB incidence in the country of origin²⁴, indicating that differential exposure among migrants is a key factor influencing TB incidence in foreign-born populations. 13% of foreign nationals in the UK are from a country where TB incidence is ≥250 cases per 100,000⁸. After the Second World War, substantial numbers of migrants arrived from the Commonwealth and former British Empire; particularly from the ISC. These movements were driven by factors such as Britain’s labour shortages for post-war reconstruction and political turbulence after decolonisation, for example following the creation of Pakistan²⁵. Many Commonwealth countries have high TB incidences: the highest incidences globally are found in Africa (275 per 100,000 population in 2015) and South East Asia (246 per 100,000)⁶. Migrants from these countries are at a greater risk of having been exposed to M.tb and contracting LTBI. Indeed, of the 11 countries that were each the source of more than 2% of foreign-born cases in 2001–2003 (collectively accounting for 73% of foreign-born cases), all were in South Asia or sub-Saharan Africa²⁶.

It is useful to consider migration to the UK from the perspective of transnationalism, defined as “the process by which immigrants forge and sustain multi-stranded social relations that link together their societies of origin and settlement”²⁷. From the 1920s until recently, migration research has tended to focus on the incorporation of migrants in their destination country rather than continued ties with their country of origin. However, since the 1990s, “the transnational turn” has provided “a new analytic optic”²⁸. From this perspective, given that migrants maintain ties across the borders of nation-states, return visits to their country of origin and overseas visitors to the UK may result in increased exposure to M.tb. Where data was available, 23.2% of TB cases between May and December 2015 in England had travelled outside the UK (excluding Western Europe, US, Canada, New Zealand and Australia) in the two years before diagnosis, and 6.8% had received an overseas visitor⁹. Such movements are increasing as globalisation leads to the intensification of international interconnectedness: in the UK, travel to visit family and friends abroad increased by 67% between 1998 and 2007²⁹. In 2007, UK residents made nearly 900,000 trips to the ISC for the purpose of visiting friends and family²⁹.

There is evidence to suggest that travel to countries with high TB incidence increases the risk of acquiring LTBI, with greater risk associated with more prolonged travel and higher TB burden in the destination country³⁰. Such individuals are then at risk of developing active disease after returning to the UK. A study in Blackburn, Hyndburn and Ribble Valley found that 12.8% of active cases among Indian, Pakistani and Bangladeshi ethnic groups occurred within 3 years of revisiting the ISC³¹. Furthermore, a case-control study in Liverpool found that TB cases were 7.4 times more likely to have recently received visitors from abroad³². A case-control study of patients of ISC ethnic origin in North West England found a weak association between revisiting the ISC and TB cases within the following 3 years³³.

BCG vaccination

Mycobacterium bovis Bacille Calmette-Guerin (BCG) is the only currently available vaccine against TB. BCG confers reliable protection against disseminated forms of TB such as miliary disease and meningitis in infants^34,35. However, protection against pulmonary TB (the most common form of disease) varies considerably by geographical region³⁶. While the UK has one of the highest levels of BCG efficacy (~80%), a low level, or complete lack of, protection has been reported in many migrant countries of origin such as India^36–38. The problem may be further confounded by limited access to vaccines and other healthcare in low-income country settings, but prevalence of M.tb infection in endemic countries remains high even where there is good BCG coverage^39,40.

It has been hypothesised that exposure to non-tuberculous environmental mycobacteria (NTM), which increases with proximity to the equator, plays a central role in limiting BCG efficacy⁴¹. Individuals may develop an immune response to NTM that either ‘masks’ or ‘blocks’ the ability of BCG to induce a protective response^41–44. In a trial in Chingleput, India, 95% of individuals were PPD positive by 15–20 years of age⁴⁵. In a trial in Malawi where there is high NTM exposure and poor BCG efficacy, individuals with lower immune responses to NTM showed greater IFN-γ responses to BCG⁴⁶. Furthermore, in mice sensitised with NTMs, the protective effect of BCG (but not a TB subunit vaccine) was considerably reduced⁴⁷. The low levels of BCG protection found in countries with high TB incidence likely contribute to the prevalence of LTBI among migrant populations.

Genetic susceptibility

The idea of a heritable component to TB was suggested as early as 1886 by Hirsch: “That phthisis [TB] propagates itself in many families from generation to generation is so much a matter of daily experience, that the severest sceptic [sic] can hardly venture to deny a hereditary element in the case”⁴⁸. It is now well-established that host genetic factors can contribute to TB susceptibility and resistance⁴⁹. Early studies demonstrated that monozygotic twins have a higher risk of developing active TB compared with dizygotic twins^50,51, and several relevant loci have since been identified using candidate gene studies and genome-wide association studies^52–57. Variation in susceptibility to M.tb infection and progression to active disease has been observed in different ethnic and geographic populations^58,59. A study of >25,000 residents in racially-integrated nursing homes in Arkansas, USA, found that 13.8% of African-American compared with 7.2% of Caucasian residents had evidence of a new M.tb infection⁶⁰. Furthermore, in a study of three TB outbreaks in two prisons, African-Americans had approximately twice the relative risk compared with Caucasians of becoming infected with M.tb⁶⁰. However, although these studies largely controlled for environmental factors, confounders such as differing vitamin D levels cannot be ruled out.

More recently, genotyping technologies have supported a role for genetic ancestry in TB susceptibility. A case-control study genotyped a panel of ancestry informative markers to estimate the ancestry proportions in a South African Coloured population. African ancestry (particularly San ancestry) was higher in TB cases than controls, and European and Asian ancestries were lower in TB cases than controls⁵⁸. However, a limitation is that the study did not adjust for socioeconomic confounders. Differences in alleles that encode components of the immune response provide a possible mechanism for ethnic variation in TB susceptibility. Indeed, a study of African and Eurasian pulmonary TB patients in London indicated ethnic differences in the host inflammatory profile at presentation including lower neutrophil counts, lower serum concentrations of CCL2, CCL11 and DBP, and higher serum concentrations of CCL5 in those of African ancestry⁶¹. These differences became more marked following initiation of antimicrobial therapy, and were associated with ethnic variation in host genotype but not M.tb strain⁶¹.

Host-pathogen co-evolution is a likely driver of variation in TB susceptibility in different human populations⁶². M.tb has been co-evolving with humans for millennia, with evidence that humans were exposed before the Neolithic transition⁶³. The differential susceptibility of particular populations may be based on M.tb exposure history, with long-term exposure resulting in strong positive selection for resistance-related alleles. There is evidence from European colonialism that previously underexposed populations are more susceptible to TB, which played a large part in the deaths of many Qu’Appelle Indian and Inuit populations in Canada^64,65. Similarly, in contrast to Europeans, Southern African populations have only been exposed to modern M.tb strains relatively recently⁵⁸. It has been suggested that selection pressure for resistance would have been strongest in areas of high population density. Accordingly, duration of urban settlement is correlated with the frequency of the SLC11A1 1729 + 55del4 allele which plays a role in natural resistance to intracellular pathogens including M.tb⁶⁶. Lower rates of TB among those of European ancestry could be due to centuries of exposure in densely populated settlements driving the evolution of increased resistance.

Vitamin D deficiency

It has long been recognised that low vitamin D levels are associated with active TB, with sunlight exposure in sanatoria and direct administration of vitamin D commonly used as treatments prior to the advent of antibiotics⁶⁷. Today, evidence supporting a link between TB and vitamin D deficiency is accumulating^68–71. A meta-analysis indicated a 70% probability that, when chosen at random from a population, an individual with TB disease would have a lower serum vitamin D level than a healthy individual⁷², although the direction of causality is not clear. It has been demonstrated that 1,25(OH)₂D, the active metabolite of vitamin D, promotes the ability of macrophages to phagocytose M.tb and enhances the production of cathelicidin LL-37, an antimicrobial peptide that has direct bactericidal activity and attracts other immune cells to the site of infection⁷³. There is evidence that a drop in serum vitamin D compromises the immune response and can lead to reactivation of LTBI⁷⁴.

Vitamin D can be acquired from the diet or endogenously synthesised in the skin by the photolytic action of solar UV light on the precursor molecule 7-dehydrocholesterol^75,76. Certain migrant and ethnic minority groups are at a greater risk of vitamin D deficiency^77–79. Indeed, vitamin D levels have been shown to be lower among Asian children living in England compared with children of the same age in the general population⁸⁰. Vegetarians are at increased risk of vitamin D deficiency since oily fish are a major dietary source⁸¹, and Hindu Asians are more frequently vegetarian due to socio-religious factors⁸². A study of Asian immigrants with TB disease in Wandsworth found that Hindus were at higher risk of contracting TB than Muslims⁸³. Darker skin pigmentation also increases risk of deficiency, as melanin reduces the efficiency of vitamin D synthesis from UVR^79,84. Hindu women in particular have been found to be at high risk, as in a 1976 study by Hunt et al. they spent on average only 2.5 hours a week outside for cultural reasons, whereas men were exposed to sunlight travelling to work⁸⁵.

1,25(OH)₂D mediates its immune activity through binding to the vitamin D receptor (VDR) on target cells; thus receptor abnormalities as well as vitamin D deficiencies may impair host immunity to M.tb⁸⁶. Some polymorphisms in the VDR gene increase susceptibility to TB, while others increase resistance^87,88. In a systematic review of seven studies comparing the prevalence of VDR polymorphisms in TB patients and healthy controls, BsmI and FokI VDR polymorphisms were found to increase TB susceptibility⁸⁹. The VDR gene shows striking genetic variation in allele frequency between populations⁹⁰. Moreover, certain polymorphisms play different roles in different populations⁸⁹, although further research is required to elucidate how this translates into variation in patterns of susceptibility and resistance to TB in different ethnic groups. Epigenetic variation in the VDR gene in different ethnic groups, arising from differential exposure to environmental factors, may influence gene regulation and therefore contribute to differential TB susceptibility. Indeed, methylation variable positions at the 3' end of VDR have been identified that are significantly correlated with ethnicity and TB status⁹¹.

Co-morbidities

Risk of progression to active TB disease is increased in those with conditions that impair immunity, such as diabetes mellitus (DM), human immunodeficiency virus (HIV) and chronic kidney disease (CKD)⁹². Certain migrant and ethnic groups are at a higher risk of these conditions; diabetes mellitus disproportionately affects South Asians whereas HIV is more prevalent among those of African origin, and chronic kidney disease affects both groups.

a) Diabetes mellitus

Clinicians have noted a possible association between TB and DM since the early 20^th century⁹³. More recently, a meta-analysis of 13 cohort studies found that DM increases the risk of active TB 3.11-fold⁹⁴. A causal relationship between DM and impaired immunity to TB is supported by studies of diabetic mice, which have higher bacterial loads when infected with M.tb than non-diabetic mice⁹⁵. DM-TB comorbidity increases both the risk of new and reactivational TB⁹⁶. Various mechanisms have been suggested including impaired immune function due to DM, complications of DM, and deficiencies in vitamins A, C and D associated with both TB and DM risk⁹⁷.

Type 2 DM (T2DM) and associated risk factors, especially obesity, show marked associations with ethnicity⁹⁸. In the UK, obesity and T2DM risk is significantly higher among South Asians (including those of ISC origin), and moderately higher among black African-Caribbeans compared with white Europeans⁹⁹. The prevalence of DM among South Asians in England was 14% in 2010; approximately double the 6.9% prevalence in the general population¹⁰⁰. Some studies have suggested that ethnic differences in T2DM can be explained by differences in socio-economic status¹⁰¹, while others do not support this⁹⁸. It is clear there are complex genetic and environmental explanations for ethnic differences in T2DM prevalence, which are beyond the scope of this review (for example, see 102).

b) Human immunodeficiency virus

Infection with HIV is the strongest known risk factor for the development of TB disease¹⁰³. TB-HIV co-infection synergistically worsens both conditions, leading it to be termed ‘the cursed duet’¹⁰⁴. HIV increases both the risk of rapid progression to active disease following infection and reactivation of LTBI, with an increased risk of TB throughout the course of HIV-1 disease^105,106 and incidence rate ratios >5 when averaged across all levels of immunodeficiency¹⁰⁷. The depletion of CD4+ T cells associated with HIV-1 infection is thought to play a major role in the increased risk of TB and its extra-pulmonary dissemination in infected individuals, as M.tb infected macrophages require CD4+ T cells to augment intracellular clearance¹⁰⁸. Furthermore, peripheral blood lymphocytes of HIV-positive patients produce less interferon-γ when exposed to M.tb in vitro than those of HIV-negative patients¹⁰⁹. These and other possible immune mechanisms such as chronic inflammation promoting an immunoregulatory phenotype and attenuation of phagocytosis have been recently reviewed¹¹⁰.

A systematic review on the prevalence, incidence and mortality of HIV-TB co-infection in Europe observed a disproportionate vulnerability of migrants to co-infection across studies¹¹¹. Given that only 3.1% of TB cases in England in 2014 involved co-infection with HIV⁹, TB-HIV co-infection cannot be considered a major driver of higher TB incidence among migrants and ethnic minorities in the UK. However, it undoubtedly plays a role in explaining the higher incidence rates among those of African origin. Between 2010 and 2014, 87% of TB-HIV co-infected cases in England were foreign-born, of which 77.5% were born in sub-Saharan Africa⁹. This reflects the global distribution of TB-HIV co-infection. In the WHO African region, 38% of new TB cases were co-infected¹⁰⁷. In turn, the global pattern of TB-HIV co-infection reflects the global distribution of HIV: 69.5% of all people living with HIV are in the WHO African region¹¹².

c) Chronic kidney disease

The association between CKD and TB was first reported in 1974¹¹³, and has been subsequently confirmed by several studies^114–116. The mechanism is thought to be impaired immunity: CKD is associated with functional abnormalities in various immune cells, such as B and T cells, monocytes, neutrophils, and natural killer cells¹¹⁷. This increases the risk of both newly acquired and reactivated TB. Furthermore, immunosuppressive medications in kidney transplant patients are aimed at T cell-mediated immunity, which is central to maintaining TB latency in LTBI individuals¹¹⁸. Patients with CKD are 10–25 times more likely to develop active TB¹¹⁹.

Ethnic minorities in the UK are at a 3–5 times higher risk of developing CKD¹²⁰. A study in London from 1994–1997 found that the incidence rate among white Caucasians was 58/million adult population per year, 221 among South Asians, and 163 among African-Caribbeans¹²¹. More recently, in a study of CKD patients with TB in South East London, 74% were born outside of the UK¹²². CKD also interacts with other risk factors that contribute to higher incidence of TB among migrants and ethnic minorities. DM patients are 4–5 times more likely to have CKD¹²³, CKD patients are more likely to have low vitamin D levels¹²⁴, and CKD is a complication associated with HIV¹²⁵. Furthermore, CKD disproportionately affects economically disadvantaged groups, possibly due to the direct impact of poverty or malnutrition, or indirect effects of poverty-associated co-morbidities including DM and HIV¹²⁶. Given the complex interactions between multiple risk factors, it is difficult to establish the direction of causality.

Socio-economic status

The association between deprivation and TB has long been recognised, leading it to be dubbed a “social disease”¹²⁷ and “poverty’s penalty”¹²⁸. There is a strong socio-economic gradient in TB burden between and within countries and communities, with economically disadvantaged groups having the highest risk¹²⁹. The importance of social factors in TB risk is supported by McKeown’s observation that a considerable proportion of the decline in TB-associated mortality occurred before the advent of antibiotics and the BCG vaccine, implicating improved living standards and nutrition as the main drivers¹³⁰. Szreter contests the McKeown thesis, emphasising the key role of public health measures in regulating the urban environment¹³¹. Either way, it is clear that TB disproportionately affects the socially and economically marginalised, with a recognised role for poverty, homelessness, and overcrowding in both the spread of infection and number of active cases¹³². In the UK in 2009, TB cases among the homeless were 20 times higher than the general population at 300 cases per 100,000¹³³. In a study of London districts, the TB notification rate increased by 12% for every 1% rise in the number of people living in overcrowded conditions¹³⁴.

The wider social determinants of health are entwined with ethnicity, meaning that ethnic socio-economic disparities throughout the life course often lead to health inequalities¹³⁵. There are marked economic inequalities between ethnic groups in the UK, with both Asian and black ethnic groups having lower employment probability than the population average¹³⁶. Alongside economic issues of unemployment, low income and poor working conditions, migrants and ethnic minorities are also more likely to face problems of homelessness, poor housing, and overcrowding¹³⁷. Foreign nationals accounted for 13% of the general UK population in 2015¹³⁸, but 20% of the homeless population¹³⁹. In 2011, dwellings with a Household Reference Person (HRP) from a minority ethnic group represented 16.1% of all households in England and Wales, but 47.9% of overcrowded households. The most commonly overcrowded households were those with a Bangladeshi HRP (30.2% overcrowded), followed by Pakistani (22.3%) and black-African (21.8%)¹⁴⁰.

King rejects what he terms ‘essentialist’ explanations for the higher TB incidence of migrants and ethnic minorities, which claim that TB disproportionately affects certain groups due to intrinsic differences, which may be biological, genetic, physiological or cultural. Instead he suggests that “Disparities in health that may at first seem to arise from essential racial or ethnic differences are often in fact the result of contingent socioeconomic differences”¹³². Similarly, Farmer rejects psychological or cultural explanations, emphasising that “tuberculosis is inextricably tied to poverty and inequality”. He criticises studies that neglect to address the political-economic forces that shape TB distribution, and calls for anthropologists to pay more attention to structural violence (the systematic ways in which social structures disadvantage individuals) and social inequality¹⁴¹.

King and Farmer claim that, given that socio-economic status affects TB risk, biological and genetic approaches are largely irrelevant^132,141. Similarly, the medical anthropologist Singer criticised the use of adaptation as a conceptual tool on the basis that such explanations ignore how the political economy shapes the environment that humans adapt to. She argues that differential mortality between socio-economic groups is “unnaturally selected” by the conditions created to further the interests of the dominant class¹⁴². However, as discussed, there is evidence to suggest that adaptation resulting from host-pathogen co-evolution influences direct and indirect genetic susceptibility to TB infection and progression to active disease. Perhaps as Mason et al. suggest, a more constructive approach is required, recognising that “the social model is an important complement to the biomedical model”¹⁴³.

Given the complex association between ethnicity and socio-economic status, it is hard to disentangle the extent to which socio-economic disadvantage influences TB incidence in migrant and ethnic minority populations¹⁴⁴. One study in children from Leeds found that overall, ethnicity explained a high proportion of TB incidence independently of deprivation and population density, although for non-South Asian children, the strongest risk factor was deprivation¹⁴⁵. Similarly, a study in Liverpool suggested an association between ethnicity and TB incidence that was independent of deprivation level¹⁴⁶, and a study investigating TB trends in England in 1999–2003 indicated that affluent ethnic minority groups are still at greater risk¹⁴⁴. It has been suggested that the absence of a strong correlation between deprivation and M.tb infection in the South Asian community may be due to the smaller relative differences in deprivation within this group than across the general population¹⁴⁷. Indeed, a study in Newham found an association between the proportion of non-white residents and TB diagnosis in each ward, but no association with deprivation as the borough as a whole was deprived¹⁴⁸.

There is significant heterogeneity in the role that social risk factors play in increasing TB risk in different migrant and ethnic groups. Among UK-born cases notified in 2010–2015, 33.0% of those in the black-Caribbean ethnic group had at least one social risk factor (homelessness, imprisonment, drug or alcohol misuse), higher than any other ethnic group⁹. 19.2% of black-Caribbean cases were drug users, and 18.4% had a history of imprisonment. The countries of origin with the highest number of homeless TB cases were Somalia, at 84 cases, and Eritrea, at 71 cases⁹. This suggests that socio-economic disadvantage may play a particularly important role in explaining higher TB incidence among the black-African and black-Caribbean ethnic groups.

Experiences of migration

The difficulties faced during and shortly after migration may increase risk of progression to active disease by compromising immunity, including poor nutrition, concurrent poor health, socioeconomic marginalisation, and the stress of relocation¹³². In an anthropological study of illegal Chinese immigrants with TB in New York, it was found that migrants often experience shortages of food and water during long migratory journeys. Upon arrival, temporary residence in detention centres or illegal refuges is associated with overcrowding and malnutrition¹⁴⁹. Migrants then face additional challenges including loss of a social support network, communication issues, discrimination, and acculturation¹⁵⁰. Ho calls for a focus on the macro-level structural forces that shape TB risk on migratory journeys, such as a lack of government regulation and exploitation by human traffickers¹⁴⁹.

Psychological effects include higher rates of anxiety among refugees and asylum seekers compared with the general population or other migrant groups¹⁵¹, and poorer mental health in forced compared with voluntary migrants¹⁵². Furthermore, Africans in Britain are at a higher risk of mental illness than non-Africans¹⁵³, and survey data suggests that immigration is a primary cause of mental distress in about 40% of Africans in the UK¹⁵⁴. It has been suggested that the psychological stress and depression associated with migration may play a role in increasing risk of progression to active disease, potentially via neuroendocrine pathways or a negative effect on the cell-mediated immune system¹⁵⁵.

Importantly, rather than transporting active cases of TB across national borders, the majority of immigrant cases of active TB disease develop following arrival in the UK¹⁰. This supports King’s assertion that “The higher rate of TB among immigrants owes as much to the hardships they face during and shortly after migration, as it does to their country of origin”¹³². Further research is required to establish the extent to which stress and adverse migratory journeys affect specific migrant groups. However, experiences of migration are likely to contribute at least in part to the higher rates of active TB among migrants compared with UK-born ethnic minorities and the general population, especially for those who are marginalised or are travelling illegally.

Treatment-seeking

Knowledge about TB among migrants and ethnic minorities is shaped by cultural beliefs, often arising from experiences in the country of origin¹⁵⁶. Certain ideas, including misconceptions about TB causation, transmission and risk, can act as barriers to clinical treatment. Gerrish et al. suggest that “TB is not just a medical disease to be treated with antibiotic therapy but an entity with historical and cultural roots”¹⁵⁷. Several studies have identified widespread misconceptions about TB causation and transmission among migrant communities, and a limited understanding of LTBI in particular¹⁵⁰. The disease has been variously erroneously attributed to climate conditions¹⁵⁸, poisoning, pneumonia¹⁵⁹, exposure to chemical products¹⁶⁰, and witchcraft¹⁶¹. Several members of a focus group of Somali women believed TB to be a punishment for past ill deeds¹⁵⁶.

Migrants may feel a false sense of having ‘left behind’ the high risk of TB in their country of origin¹⁵⁰, and TB may be considered by migrants to be a different, more severe, disease in their country of origin¹⁶². In some cases, TB may be thought of as incurable due to poor health services in low-income countries¹⁶³. Moreover, immigrants may favour traditional systems of care and healing over Western medicine upon arrival¹⁶⁴, making them more likely to turn to traditional folk healers, self-diagnosis or self-medication before accessing public healthcare facilities¹³⁷. Cultural beliefs that lead to delays in treatment-seeking and patient non-compliance may increase the risk of TB transmission within such communities.

Conversely, some have suggested that the cultural beliefs held by migrants are not barriers to treatment-seeking, but rather promote such behaviour. The higher prevalence of TB in migrants’ countries of origin could lead to greater awareness; as Bakhshi argues, “people born in developing countries are too familiar with the disease to neglect it”²⁰. Moreover, Ho describes how traditional Chinese medical beliefs are often complementary to clinical TB treatment in New York, such as through the use of traditional Chinese medicine to reduce the side effects of anti-TB drugs¹⁴⁹.

TB-related stigmatisation of immigrants has been reported in multiple studies (reviewed in 150). Stigma is defined as “the situation of the individual who is disqualified from full social acceptance”, and is therefore “reduced in our minds from a whole and usual person to a tainted, discounted one”¹⁶⁵. Some cultures consider TB to be sinful and dirty¹⁵⁶. The feelings of guilt and shame¹⁶⁶ and risk of rejection and discrimination¹⁶⁷ that may result from stigmatisation affect attitudes towards diagnosis, treatment and prevention, and therefore hinder control of TB and facilitate its transmission within certain migrant and ethnic groups¹⁶⁸. Sufferers may hide their illness to avoid stigma and discrimination and protect personal or family dignity¹⁶¹. One study indicated that stigma prevented some immigrants from sharing information with their doctors, even TB-related symptoms¹⁶⁹. Furthermore, patients may be less likely to identify contacts due to concerns about social repercussions, meaning that subsequent preventable TB cases may occur¹⁵⁷. Feelings of stigma produced by attitudes in the country of origin are likely to be exacerbated by the negative stereotyping of migrant groups as ‘dirty’ or ‘diseased’ due to the association of TB with immigrants, which may lead to xenophobia and discrimination of sufferers¹⁶³, termed ‘sociomedical racism’ by McBride (1991)¹⁷⁰.

The Somali community in the UK provides an informative case study of the socio-cultural meaning and perceived consequences of TB. In Somalia, TB is associated with extreme stigma and social isolation. In a focused ethnography of Somali-born UK residents, Gerrish et al. found that interviewees tended to base their attitudes towards TB on those prevalent in Somalia¹⁵⁷. The stigma associated with TB led to expectations of social isolation, shame and loss of self-worth, sometimes extending to the whole family. Although most had an understanding that TB is contagious, it was also commonly believed that people remain infectious after treatment, as TB was often thought to be hereditary and therefore impossible to eradicate. This led to fears that friends would not resume normal social interactions after treatment, and that a diagnosis would jeopardise marriage prospects. Therefore, sufferers tended to isolate themselves or conceal their illness. In reality, anticipated consequences tended to be worse than actual experiences of discrimination, but felt stigma was nonetheless a powerful deterrent to disclosing illness, leading to delays in diagnosis and treatment¹⁵⁷.

Access to healthcare

Migrants may have difficulties establishing ‘entitlement’ to good healthcare¹⁷¹. For example, a study in the UK found that only 32.5% of new migrants who were instructed to register with a GP had done so, and the migrant groups with the smallest proportion registered were likely to have greatest need¹⁷². This is consistent with the Inverse Care Law, that those with the greatest need are least able to access healthcare services¹⁷³. Various studies have found that migrants face barriers in accessing healthcare services for TB diagnosis or treatment. These include lack of awareness of the local health system, including availability of free services¹⁷⁴, language barriers¹⁷⁵, and fears about loss of privacy due to the use of interpreters¹⁶². Therefore, even in cases where there are minimal geographic or economic barriers to accessing health facilities, there are often racial, linguistic and cultural barriers to using these facilities effectively and adhering to treatment regimens¹⁷⁶.

Studies have found that migrants face various structural barriers to accessing healthcare services, such as transport difficulties associated with poor services in deprived areas¹⁵⁶, and rigid opening hours for medication that do not fit with the working hours and lifestyles of patients¹⁷⁷. Moreover, economic barriers include not only direct costs associated with illness, such as the costs of repeated journeys to clinics for treatment, but also indirect costs including losing a job or being evicted by a landlord¹⁷⁸. Farmer criticises anthropological investigations for conflating structural violence with cultural difference, tending to exaggerate the role of patient agency and minimise the role of poverty and the barriers that it creates to accessing adequate care and completing treatment¹⁴¹. Nevertheless, whether structural or cultural, barriers to healthcare access among migrant and ethnic groups can lead to delays in diagnosis and treatment, resulting in increased transmission and incidence.

Access to healthcare services varies across different migrant populations. Although treatment of TB is free for all in the UK, refugees and asylum seekers have poorer access to health services¹⁷⁹. Irregular residence status is likely to lead to significant delays in seeking medical assistance, due to uncertainties surrounding entitlement to services and fears of deportation, since TB patients can be legally deported while receiving ongoing treatment¹⁸⁰. Furthermore, irregular migrants may face difficulties in completing long-term TB treatment, which involves repeated consultations, if they do not have housing or employment and are short-term residents. Irregular migrants are also less likely to be willing to provide details of their migratory route¹⁶² and provide information about contacts¹⁶¹. Contact tracing is further compromised given the high mobility of migrants, and the fact that many do not reside at their official address, but with family and friends¹⁶².

Conversely, there is evidence to suggest that UK-born cases experience longer delays from symptom onset to commencement of treatment than foreign-born cases⁹. Moreover, TB treatment completion is actually marginally higher in migrants (85%) than the UK-born (81%)¹⁸¹. However, these observations are problematic in that UK-born TB cases are often drawn from homeless individuals, problem drug users and prisoners, and so are frequently lost to follow-up and poorly adherent¹⁸²; they are not representative of the UK-born population as a whole. Furthermore, migrants are at a higher risk of contracting TB due to the various unique factors discussed (including genetics, vitamin D deficiency, co-morbidities, and experiences of migration), which do not apply to the UK-born, making socio-economic issues the key driver of TB incidence in this group. Indeed, in 2016, nearly three times as many UK-born cases (22%) as foreign-born cases (8%) had at least one social risk factor (drug misuse, alcohol misuse, homelessness, or imprisonment)⁹, which is incongruent with the higher overall rates of deprivation in foreign-born compared with UK-born populations²³.

Conclusions

It is a common misconception that migrants have a higher incidence of TB disease compared with the general population simply because they ‘import’ it from abroad. Bakhshi suggests that they “present a tuberculosis picture from the country of origin and not the United Kingdom where the disease eventually manifests”²⁰. Indeed, differential pathogen exposure can explain much of the higher incidence of TB among migrants and ethnic minorities, due to both pre-migration residence in high-incidence countries and maintenance of transnational links with the country of birth or ethnic origin. However, positing this as the sole driver fails to address the complex interplay of factors driving the vulnerability of particular migrant and ethnic groups to infection and progression to active disease. These include genetic susceptibility, vitamin D deficiency due to climatic and dietary factors, co-morbidities including DM, HIV and CKD, socio-economic deprivation, and factors linked to the experience of migration itself. Furthermore, certain migrant and ethnic groups face barriers to accessing treatment including cultural differences in treatment-seeking behaviours, stigmatisation of sufferers, and barriers to healthcare access. As stated by Offer et al., “TB in ethnic minorities does not occur in isolation but against a backdrop of socioeconomic, political and cultural context that affects their knowledge, attitudes and behaviours”¹⁴⁷. The resultant delays in diagnosis and treatment lead to increased transmission and incidence in these communities.

In this way, there are factors disadvantaging migrants and ethnic minorities at each stage of the disease, relating to risk of pathogen exposure, vulnerability to infection, development of active disease, and access to treatment. Although heterogeneity between and within broad migrant and ethnic groups leads to variation in risk at each of these stages, there is a net effect of higher incidence among migrants and ethnic minorities compared with the general UK population. It is important to understand the complex and multifactorial drivers of this disparity in order to implement effective policies for tackling TB in these vulnerable groups. Currently, migrants from countries with high TB incidences are screened for active TB before entry to the UK. However, to complement such measures, which only consider the driver of differential pathogen exposure, more consideration is needed regarding policies that address the factors making migrants and ethnic minorities more vulnerable to reactivation of LTBI following their arrival in the UK. This might include vitamin D supplementation, measures targeting co-morbidities, and policies that promote socio-economic equity and migrant rights. In order to reduce delays in diagnosis and treatment, and thereby minimise transmission within migrant and ethnic minority communities, increased health education on TB causation, risk and transmission is required, as well as tackling stigmatisation of vulnerable groups. It is also important to raise awareness of migrants’ entitlement to diagnosis and treatment through the NHS, alongside reducing cultural and economic barriers to its access.

Data availability

No data are associated with this article.