Results

DESCRIPTIVE EPIDEMIOLOGY

In the entire study cohort (n = 107), 42 (39.3%) were index cases while 61 (57%) were found by contact tracing. Three cases were diagnosed following screening of new immigrants and one case was found during the school Heaf testing programme prior to BCG immunisation.

Table 1 describes the characteristics of the patient population by age and sex, showing the majority of children in the age group 5–9 years. Thirty eight (35.5%) children in the study were of south Asian subcontinent origin, of whom 25 were girls and 13 were boys, giving a female to male ratio of 1.9:1. The female to male ratio in white children was 1.02:1.

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Table 1

Frequency, proportion, and incidence of children diagnosed with tuberculosis by age group and by sex

Respiratory tuberculosis accounted for 88 (82%) of the cases (57 non-south Asian, 31 south Asian) while 17 (16%) had non-respiratory tuberculosis (11 non-south Asian, six south Asian), predominately tuberculous lymphadenitis (11 cases; 65% of non-respiratory tuberculosis).

Overall age–sex standardised incidence rate over the period 1982–1997 was 3.9 per 100 000 per year (95% confidence intervals 3.2 to 4.7 per 100 000 per year). Crude incidence rates for 0–18 year-olds of south Asian origin were 25.7 per 100 000 per year (95% confidence intervals 17.4 to 33.9 per 100 000 per year), and 2.7 per 100 000 per year (95% confidence intervals 2.1 to 3.3 per 100 000 per year) for the non-south Asian population. Figure 1 shows three year moving averages for these crude rates by year. There is a significant 13.3% average annual decrease in incidence for the non-south Asian population determined by linear regression (coefficient of log rate = −0.142, p = 0.002). The overall average annual percentage decrease was 6.5% but was not significant (coefficient of log rate = −0.0678, p = 0.067).

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Figure 1

Incidence of tuberculosis in Leeds District Health Authority 1982–1997; three year moving average for south Asian and non-south Asian 0–18 year olds.

Discussion

Childhood tuberculosis is often regarded as unimportant in the epidemiology of tuberculosis, as more than 95% of children with tuberculosis are smear negative15 and therefore do not contribute to the immediate spread of the disease. However, childhood tuberculosis is necessarily a result of recent infection and therefore the presence of tuberculosis in children, particularly the younger age groups, reflects continuing transmission in the community. Infected children represent a pool from which a larger proportion of future cases of adult tuberculosis will arise.15 The World Health Organisation estimated that there were 7.96 million new cases and 1.87 million deaths in all age groups as a result of tuberculosis in 1997.16

Under notification of tuberculosis in Britain is well recognised, but its extent is unknown.17 Leeds Health Authority has excellent cross checking systems to ensure accurate notification. The Consultant in Communicable Disease Control receives notifications of all positive cultures from the microbiology laboratories, histopathology laboratories, and the chest clinic. Local pharmacists inform the Consultant of all patients being prescribed combinations of antituberculous drugs. These mechanisms ensure continuous updating of the central tuberculosis register kept at the chest clinic and repeated local surveys have not detected any cases which were not already known to the chest clinic. It is therefore very unlikely that under notification is a significant problem in Leeds.

Our data showed that despite the fact that the total (adult and child) annual number of notified cases has been increasing in Leeds in the last three years of the study (J Watson, personal communication), the annual notifications for children alone have not shown a concomitant rise. The recent increase in adult notifications is likely to be caused by a combination of factors, for example an increase in homelessness, continued immigration, and increased reinfection of people visiting the Indian subcontinent.

Respiratory tuberculosis (82.2%) was much more common than non-respiratory disease (15.9%). There was an unexpected finding of a relatively higher number of south Asian girls with tuberculosis (male to female ratio 1.9:1 in south Asian and 1.02:1 in white children). Gender refers not only to physiological differences between the sexes, but also to the wide variety of behaviour, expectations, and roles attributed by culture to males and females. While much has been written about the influence of socioeconomic and cultural factors related to tuberculosis incidence, such studies have rarely analysed data by sex.18 There are some biological factors which may predispose females to tuberculosis infection. Animal studies suggest that the balance between the endogenous adrenal steroids cortisol and dehydroepiandrostenedione influences the balance of Th1 to Th2 cytokines which is thought to affect the immune response to tuberculosis.19 This would not explain the differential findings between south Asian and white girls in our study. Another recent study20 suggests that 25-hydroxycholecalciferol deficiency may contribute to the high occurrence of tuberculosis in Asians in west London. It is interesting to speculate about whether cultural factors, such as a tendency of Asian girls to spend more time at home, differentially affect vitamin D status, exposure to tuberculosis, or both. Prospective studies may help to explain the gender differential.

This study showed that the most affected age groups were children aged 0–4 years (24.3%) and 5–9 years (39%). These figures are of particular significance as children have been the target of a number of primary preventive measures against tuberculosis infection, including selective BCG immunisation of infants at higher risk. The neonatal BCG programme has been reported to provide between approximately 64%21 and at least 75%22 protection against childhood tuberculosis, with an overall rate of protection estimated at 65% against respiratory disease but almost complete protection against disseminated disease.23 Although the BCG status of our cohort was not fully documented, a previous study from Leeds6 found that none of the active cases received neonatal BCG.

The finding from the ecological analysis that the overall risk of tuberculosis is linked to deprivation, population density, and ethnicity is not new. It is of interest, however, that the risk for ethnicity in the multivariate analysis was independent of both population density and deprivation and therefore not explained by these factors.

The study population was considered to be as complete as possible, but the sources of cases were not independent so the ascertainment could not be formally tested. The numbers included were relatively small and caution in interpretation of the results is therefore important; however, the publication of similar findings from an independent study of tuberculosis9 lends weight to our results.

For the descriptive epidemiology, individuals were flagged as south Asian based on their name, a procedure which may be open to misclassification. However, the Nam Pehchan program,24which identifies part name (stem) or complete matches from a data dictionary of Asian names is used by the City of Bradford Metropolitan Council and Bradford Health Authorities in West Yorkshire and is particularly appropriate for the population in this study. Further checks were made with health care professionals dealing with the Asian families, along with visual inspection of the names; we therefore consider it unlikely that any major misclassification will have occurred.

The ecological analyses used census based variables to measure ethnicity, that is, the proportion of non-white children in the population; it should be noted that measuring summary characteristics of a population residing in an area, however restricted in size, does not necessarily represent the condition of any single individual.25 Despite this, a number of area based studies in the UK,26 ,27 although not all,28 ,29 have shown that census based investigations are a reasonable method of investigating the risk of disease in relation to population characteristics.

Examining our childhood populations of south Asians and non-south Asians (mainly white) separately, we found no links between deprivation or population density for south Asian children, reflecting a similar pattern shown in the combined childhood and adult population in Birmingham.9 For non-south Asian children there was an association with deprivation but not population density. These findings from the ecological analysis, in conjunction with the differential time trends, suggest that disease aetiology and the risk profile may be different for south Asian compared to other children. Our observations make it important for future analyses of overall trends and incidence rates to take account of ethnicity. Failure to do so will lead to misunderstanding of the dynamics of tuberculosis infection in the population.