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Amy L. Davidow, PhD, Bonita T. Mangura, MD, Eileen C. Napolitano, BA and Lee B. Reichman, MD, MPH

The authors are with the New Jersey Medical School National Tuberculosis Center, Newark. Amy L. Davidow and Lee B. Reichman are also with the Department of Preventive Medicine and Community Health, University of Medicine and Dentistry–New Jersey Medical School. Bonita T. Mangura, Eileen C. Napolitano, and Lee B. Reichman are also with the Department of Medicine–New Jersey Medical School.

Correspondence: Requests for reprints should be sent to Amy L. Davidow, PhD, Department of Preventive Medicine and Community Health, Medical Science Bldg, F596-A, 185 S Orange Ave, Newark, NJ 07103 (e-mail: davidoal{at}umdnj.edu).

	ABSTRACT

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION References

 

Objectives. This study investigated the socioeconomic profile of foreign-born tuberculosis patients in New Jersey.

Methods. Foreign- and US-born tuberculosis patients in 1994–1999 were compared using various measures of socioeconomic status.

Results. Out of 4295 tuberculosis patients, 2005 (47%) were foreign-born. Foreign-born patients resided in more affluent, more educated, and less crowded areas than did US-born patients (P < .005). They were also more likely to have been employed during the 2 years before diagnosis (62% vs 41%, P < .001). Private physicians treated the majority of South Asian–born patients.

Conclusions. Substantial numbers of employed foreign-born tuberculosis patients now reside in affluent New Jersey locations. Changes in tuberculosis control programs may be required when the socioeconomic status and place of residence of foreign-born populations diverge from traditional assumptions linking poverty with tuberculosis.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION References

 
With reports that tuberculosis (TB) rates among the foreign-born have not declined in tandem with those among the US-born, TB among the foreign-born residents of United States has become a persistent concern.^1,2 Talbot et al.³ reported that although the US-born TB rate fell 40% from 1993 to 1998 (7.4 per 100 000 in 1993 vs 4.4 per 100 000 in 1998), the foreign-born TB rate fell only 12% in the same period (34.1 per 100 000 vs 30.1 per 100 000). Nationwide, according to the 1990 US census, 8% of the total population was foreign-born, whereas 36% of TB cases occurred among the foreign-born during the years 1993–1998.³

Foreign birth is only 1 risk factor for TB in the United States. Other risk factors for TB, such as AIDS and injection drug use, have been identified in recent decades.^4,5 In contrast, the epidemiological evidence connecting TB with socioeconomic deprivation is long-standing, extending even to the last years of the 19th century.^6,7 Early-20th-century declines in TB rates in the United States and England have been attributed in part to reduced crowding and improved nutrition.⁸

More recent evidence points to the continuing influence of poverty on TB rates. On the macro (institutional) scale, Brudney and Dobkin⁹ identified underfunding of TB control programs during the New York City fiscal crisis of the 1970s as a contributing element in the increased TB rates seen in the 1980s. A recent Institute of Medicine report on TB came to a similar conclusion.¹⁰ On the local scale, several studies have found neighborhood crowding to be strongly associated with TB rates; in 1 of these studies, the association persisted even after control for AIDS prevalence.^11–13

We conceived this article out of concern that the close connection between poverty and TB may have been complicated by immigration patterns in the past decade, with potential consequences for TB treatment and control programs. Several demographic and health trends motivated our analysis. First, whereas 47% of New Jersey’s TB cases occurred among foreign-born residents during 1994–1999, only 13% of New Jersey residents are foreign-born (according to the 1990 US census, the most recent for which figures on place of birth are available). This percentage of foreign-born residents is the fourth greatest among US states; in absolute numbers of foreign-born residents, New Jersey ranks fifth. The population of New Jersey is 7.7 million, with more than 1.1 million persons born either abroad (approximately 967 000) or in Puerto Rico (approximately 144 000).¹⁴ Second, of the 22 high-burden TB countries so classified by the World Health Organization,¹⁵ 19 appear on New Jersey’s surveillance records for the years 1994–1999 (Table 1). Third, approximately 40% of New Jersey’s foreign-born population arrived in the United States during the years 1980–1989,¹⁴ and New Jersey has remained an important destination for new immigrants to the United States in the years since then. This last point has potentially significant implications for New Jersey TB rates, because recent (< 5 years) immigration is a risk factor both for TB resulting from reactivation of latent Mycobacterium tuberculosis infection and for undiagnosed, active TB disease acquired elsewhere.¹ Fourth, the distribution of the foreign-born US population by region of birth has changed substantially since 1960, when the European-born population accounted for 75% of the foreign-born US population. By 1990, European-born persons accounted for only 23% of the foreign-born population, and Asians, who had accounted for only 5% of the foreign-born US population in 1960, now accounted for 26%. The Latin American–born population of the United States also experienced a large increase, growing from 9% of the foreign-born population in 1960 to 44% in 1990.¹⁶ Fifth, the median age of the foreign-born has declined, from 52 years in 1970 to 37 years in 1990.¹⁷ New Jersey has been affected by changes in immigration patterns observed at the national level.^18,19

	SUBJECTS AND METHODS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION References

 
Tuberculosis cases counted by the New Jersey Department of Health and Senior Services for the years 1994–1999 were analyzed. These records contain the age, type of treatment supervision at case report (health department, private provider, both health department and private provider), employment status within the past 2 years, place of birth, date of report, and date of entry into the United States (when relevant) of each patient, among other variables. We grouped TB cases by place of birth into 10 areas: Asia and the Pacific Rim, United States and Canada, Caribbean islands, Central America, Europe, Mexico, Middle East and North Africa, South America, South Asia (Afghanistan, Pakistan, India, and Bangladesh), and Sub-Saharan Africa. Patients born in Puerto Rico were classified with others from the Caribbean. For foreign-born TB patients, we calculated the time to diagnosis from the date of entry into the United States.

For each New Jersey zip code area in which at least 1 TB case was diagnosed, the following variables were obtained from the 1990 census: percentage of population aged 25 years or older, proportion of collegeeducated persons aged 25 years or older, per capita income, and proportion of occupied housing units with more than 1 person per room (household crowding). Individual-level TB records were matched with the educational attainment, per capita income, and household crowding measures of the zip code area of residence to assess the socioeconomic context within which the patient resided.

The variables per capita income and household crowding have been used in previous analyses of TB cases.^12,13 We also analyzed educational attainment, because we believe that this variable reflects longer term or potential socioeconomic status, whereas per capita income and household crowding may reflect short-term circumstances when new immigrants are involved. A dichotomous summary measure of ecological socioeconomic status was created from the 3 socioeconomic variables: a zip code area was classified as affluent if its per capita income and educational attainment were in the highest tertile and its household crowding was in the lowest tertile, and as nonaffluent otherwise.

We compared US-born and foreign-born TB patients with respect to variables representing the socioeconomic context of the place of residence: educational attainment, per capita income, household crowding, and affluence. We also compared variables capturing aspects of subject-level socioeconomic status—working status within the 2 years before diagnosis for patients aged 25 to 65 years and type of health care provider at diagnosis. Age at diagnosis was also compared by place of birth. All of these comparisons were conducted using a Wilcoxon rank-sum test or a ² test. Mantel–Haenszel ² tests for trend were conducted to assess how the proportion of patients that are foreign-born changes with the level of each residential socioeconomic factor (e.g., the level of household crowding). A subanalysis for children aged 12 years or younger was also conducted to see whether the results applied to pediatric TB cases—that is, cases that are more likely due to recent infection rather than reactivation of latent disease.

To assess heterogeneity of the results, we made all comparisons by world region of birth with the Kruskal–Wallis test. We also performed a pairwise comparison of each of the world regions of birth with the US-born. Non–European-born patients were compared with European-born patients with respect to time from immigration. Because European-born patients tended to have immigrated at an earlier time than the non–European-born, some of the differences observed may be due to cohort effects.

	RESULTS

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION References

 
During the years 1994–1999, 4295 TB cases were identified in New Jersey—2290 among US-born residents, 1 among Canadian-born residents, and 2004 among other foreign-born residents. Of the 2005 foreign-born patients, 991 (49.4%) were born in World Health Organization–designated high-burden TB countries.¹⁵ The New Jersey average annual case rate during these 6 years was 30.1 per 100 000 among the foreign-born and 5.8 per 100 000 among the US-born. Table 2 shows the counts and annual rates by year and by place of birth.

Table 3 shows the distribution of tertiles of household crowding, per capita income, and educational attainment by place of birth. In each case, the Mantel–Haenszel ² test for trend is highly significant (P < .0001); the proportion of patients who are foreign-born rises as residential socioeconomic status increases. Of the 2005 foreign-born patients, 542 (27%) lived in affluent areas; of the 2290 US-born patients, 402 (18%) lived in areas so designated (P < .001).

Tuberculosis Among Children
During 1994–1999, 65 foreign-born patients and 190 US-born patients aged 12 years or younger were included in the study population. The median age at diagnosis was 3 years for foreign-born children and 8 years for US-born children (P < .001). Like their adult counterparts, foreign-born pediatric patients tended to reside in zip code areas exhibiting less crowding (9.0% vs 10.3% occupied housing units with more than 1 person per room; P = .009), higher per capita income (median $13 000 vs $11 700; P < .001), and higher educational attainment (median 34.8% with some college education vs 32.7%; P = .014). The proportion of pediatric patients who were foreign-born increased as residential socioeconomic status increased, although this effect was somewhat more modest than the one observed overall (P = .012, .003, and .03, respectively, for household crowding, per capita income, and educational achievement).

Foreign-Born by Region
Table 4 shows the distribution of numbers of TB patients and the zip code–level socioeconomic indicators by world region of birth. (Because denominator data by world region for New Jersey cases were not available, it was not possible to present region-specific rates.) Educational attainment, household crowding, and per capita income of patients in the zip code areas where foreign-born patients resided differed significantly among the different world regions (P < .001). Post hoc analysis showed that, in general, the zip code areas in which Asian and South Asian TB patients lived had higher educational attainment, less household crowding, and higher per capita incomes than the areas in which US-born TB patients resided (P < .001 for all comparisons). Levels of the 3 variables in zip code areas where Mexican-born patients resided were similar to levels in areas where US-born patients resided (P > .3 for all).

There was a statistically significant association between world region of birth and both employment status and health care provider type (P < .001 for both). With the exception of patients born in the Middle East (n = 19) and in the United States plus Canada (n = 2291), the majority of patients aged 25 to 65 years born in each of the world regions were employed during the 2 years before diagnosis. Only among patients born in Europe and South Asia had a majority been treated exclusively by a private physician (57.9% and 54.8%, respectively).

	DISCUSSION

TOP ABSTRACT INTRODUCTION SUBJECTS AND METHODS RESULTS DISCUSSION References

 
Just as the AIDS epidemic altered the age distribution of TB, recent immigration patterns may have produced changes that challenge the conventional wisdom pairing TB and poverty. An epidemic of TB among young foreign-born residents living in relatively affluent areas of New Jersey flies in the face of long-held stereotypes regarding the socioeconomics of TB overall and in particular among the foreign-born. This observation especially applies to immigrants from Asian and South Asian countries, who constitute 43.6% of foreign-born TB patients in New Jersey. Our results agree with those of a study of TB in Great Britain, which found that although poverty was associated with TB among Whites, no such relationship existed among persons of Asian origin.²⁰

The original Centers for Disease Control and Prevention plan to eliminate TB in the United States by 2010 was based on the assumption that elimination could be accomplished by means of targeted interventions aimed at high-risk groups such as the HIVinfected, substance abusers, homeless persons, and the foreign-born.²¹ It was theorized that such groups were burdened with multiple health and social problems, and treatment programs were designed accordingly. However, our analysis shows foreign-born TB patients to be more likely than US-born patients to live in relatively affluent locations, to seek medical treatment outside the public health system, and to be employed during the 2-year period before diagnosis.

These results have implications for TB control activities and treatment. First, if current trends continue, New Jersey can soon expect more than 300 new foreign-born patients annually, with approximately one third residing in relatively affluent areas. As a result, resource allocation for TB control may need to be adjusted to meet the challenge of foreign-born TB patients residing in affluent areas. However, the modification should be cautious, given that nearly two thirds of foreign-born patients still reside in areas whose lower socioeconomic profile is the one that is traditionally associated with TB.

Second, if large numbers of foreign-born patients obtain treatment from private physicians, those physicians will need to be better informed about the correct treatment of TB and latent TB infection. Previous studies have shown that private physicians are less likely than physicians working in public health settings to provide correct TB treatment.^22,23 This physician education could be accomplished by means of better collaboration between local TB control and prevention agencies and private providers, including consultation to discuss appropriate drug regimens and case management strategies and provision of American Thoracic Society/Centers for Disease Control and Prevention treatment recommendations and guidelines. Other essential ingredients for the successful treatment of foreign-born TB patients by private providers would include broadening the use of directly observed therapy and incentives in the treatment of private patients and distributing educational materials in languages other than English. Moreover, if a relatively affluent TB patient does seek medical care from a public chest clinic, incentives such as food, clothes, and bus tokens to ensure compliance with a demanding TB regimen may be less likely to succeed.²⁴

Third, if large numbers of foreign-born TB patients are employed during the 2-year period before diagnosis, they are also more likely to be working during the course of their treatment and during their infectious period. With respect to treatment, public clinic hours, which typically are limited and thus represent a possible barrier to treatment for a person with a demanding work schedule, will need to be expanded. With respect to the possibility of working during the infectious period, more resources will be needed for conducting contact investigations in the workplace. The importance of allocating sufficient resources to contact investigations overall is substantiated by our observation that foreign-born TB patients are likely to be younger at diagnosis than US-born TB patients and hence have a greater probability of transmission, as documented in a number of studies.^25,26 TB control officers carrying out contact investigations involving undocumented or noncitizen foreign-born patients and their possibly undocumented/noncitizen foreign-born contacts will need to convey that cooperation will not increase the risk of deportation.

The subanalysis of pediatric TB patients also showed that foreign-born pediatric patients resided in socioeconomically more advantaged areas than US-born pediatric patients. However, the absolute socioeconomic levels reflect the relatively deprived circumstances of almost all pediatric patients, regardless of place of birth. Because children are more likely than adults to have been recently infected, this connection is evidence that recent transmission is still linked to socioeconomically deprived environments.

The epidemiology of pediatric TB is not clear, given the likelihood that some US-born pediatric TB patients have foreign-born parents. (Note that the median age of nonEuropean, foreign-born patients is 37 years, an age at which parenthood is likely.) A study of largely US-born (84%) children in California found that having a foreign-born parent was a risk factor for a positive tuberculin skin test, as was travel to and receiving visitors from countries where TB is endemic.²⁷ In Great Britain, McCarthy found that approximately one fifth of TB infections among Asian immigrants were most likely acquired during a return visit to Asia.²⁸ Anonymous surveillance data such as those analyzed here do not permit us to resolve the question of whether a child’s infection was recently acquired (either in the United States or abroad during a visit to a parent’s country of origin) or due to reactivation of latent infection. Another possibility is that active disease in a child was present before immigration but remained undiagnosed until residence was established in the United States.

This study was limited by (1) the unavailability of country-specific estimates of New Jersey’s foreign-born population, and (2) imperfect data on individual socioeconomic status of TB patients. As is the case in many disease registries maintained by state health departments, indicators of individual socioeconomic status in New Jersey’s TB registry are largely missing.²⁹ Because information about health insurance carriers and specific employment at diagnosis was not available, we sketched out the individual socioeconomic status of the patients, using the variables provider type and employment status during the 2 years before diagnosis. Although both of these variables do point toward a higher socioeconomic status, they also have programmatic implications.

In 1997, New Jersey was one of 6 states in which the foreign-born population was estimated to exceed 1 million.³⁰ The other 5 states were California, Florida, Illinois, New York, and Texas; in these states, as in New Jersey, a large proportion of the foreign-born population—from a minimum of 39% (Illinois) to a maximum of 50% (California)—arrived in the United States between 1980 and 1989.¹⁴ These 5 states also exhibit the largest US TB burden.³¹ The particular socioeconomic profile of the foreign-born TB patients in each of these states is determined by a complex array of economic, demographic, and historical factors. Some of the differences observed in this study can be attributed to cohort effects; for example, the difference between nonEuropean-born patients and European-born patients with respect to time to diagnosis reflects the fact that the majority of European-born patients immigrated as part of an earlier cohort. Each state will need to perform its own analysis to tailor the measures appropriate to its own foreign-born population.

The Immigration Act of 1990, which established the H-1B visa category, enabled highly trained professionals from abroad to enter the United States, many of whom settled in northern New Jersey and elsewhere—for example, so-called "Silicon Valley" in California.^32,33 These relatively affluent and well-educated immigrants lifted the socioeconomic profile of the foreign-born in the states where they settled. As is the case in New Jersey, a large proportion of these "high-tech" immigrants arrived from high-burden TB countries. Thus, the relationship between socioeconomic status and TB among the foreign-born we observed in New Jersey may well be discernible elsewhere in the United States.

Nationwide, the higher socioeconomic status enjoyed by some immigrants from Asian and South Asian countries is reflected in the fact that nearly 36% of workers from these countries are employed in managerial and professional specialties, a figure significantly higher than that for immigrants from other countries where TB is endemic.¹⁶ Although some of these immigrants currently reside in relatively affluent communities, it is difficult to escape the legacy of Mycobacterium tuberculosis infection bequeathed by their place of birth. Even those escaping infection before arrival in the United States may become infected later, given that immigration is no longer the 1-way ticket from place of birth to adopted homeland it was early in the 20th century.

Our analysis has revealed that the underserved population residing in urban areas long recognized to be at risk for TB lives alongside another population whose relative personal affluence and location defy time-honored epidemiological notions. There is substantial variability among foreign-born patients with respect to both personal and environmental socioeconomic indicators. As a result, future progress in TB control and elimination in the United States will require more complex solutions than have previously been recognized. TB among foreign-born residents and their children will continue to be a challenge to TB control measures, a challenge likely to persist as long as TB remains endemic in much of the developing world.

	Acknowledgments

 
This work was supported in part by the Aaron Diamond Foundation (A. L. Davidow), National Institutes of Health grant R21 AI42521–01 (A. L. Davidow), New Jersey State Department of Health and Senior Services Health Service grant 00–57-TB-S2, TB Model Center (B. T. Mangura, E. C. Napolitano, L. B. Reichman), Cooperative Agreement 1999N0083, Tuberculosis Trials Consortium (B. T. Mangura, L. B. Reichman), TB Career Academic Award K07 HL03015 (L. B. Reichman).

The authors are grateful to Kenneth Shilkret, Manager, TB Program, New Jersey Department of Health and Senior Services, Trenton, NJ, for provision of TB surveillance records and helpful suggestions.

Human Participant Protection

This study was determined to be exempt from protocol approval by the institutional review board of the University of Medicine and Dentistry of New Jersey.

	Footnotes

 
Contributors

A. L. Davidow planned the study, analyzed the data, and wrote the article. B. T. Mangura, E. Napolitano, and L. B. Reichman contributed to the formulation of the study hypothesis, the interpretation of data analyses, and the writing of this article.

Peer Reviewed

Accepted for publication August 23, 2002.

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This Article Abstract Full Text (PDF) Submit a response Purchase Article View Shopping Cart Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Services Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (10) Citing Articles via Google Scholar Google Scholar Articles by Davidow, A. L. Articles by Reichman, L. B. Search for Related Content PubMed PubMed Citation Articles by Davidow, A. L. Articles by Reichman, L. B. Related Collections Tuberculosis Socioeconomic Factors