Abstract
Rationale: In the United States, the number of annual reported cases of tuberculosis (TB) among U.S.-born persons declined by 62% from 1993 to 2004, but increased by 5% among foreign-born persons. Over half of all reported cases of TB in the United States occur among foreign-born persons, most of these due to activation of latent TB infection (LTBI). Current guidelines recommend targeting only foreign-born persons who entered the United States within the previous 5 yr for LTBI testing.
Objective: We sought to assess the epidemiologic basis for this guideline.
Methods: We calculated TB case rates among foreign-born persons, stratified by duration of United States residence and world region of origin. We determined the number of cases using 2004 U.S. TB surveillance data, and calculated case rates using population data from the 2004 American Community Survey.
Measurements and Main Results: In 2004, a total of 14,517 cases of TB were reported; 3,444 (24%) of these were among foreign-born persons who had entered the United States more than 5 yr previously. The rate of TB disease among foreign-born persons was 21.5/100,000, compared with 2.7/100,000 for U.S.-born persons, and varied by duration of residence and world region of origin.
Conclusions: Almost one-quarter of all TB cases in the United States occur among foreign-born persons who have resided in the United States for longer than 5 yr; case rates for such persons from selected regions of origin remain substantially elevated. To eliminate TB, we must address the burden of LTBI in this high-risk group.
Over half of all reported tuberculosis (TB) cases in the United States are among foreign-born persons; most of these are due to activation of latent TB infection (LTBI). Only foreign-born persons living in the United States for less than 5 years are targeted for LTBI testing.
Foreign-born persons have substantially elevated risk of TB even more than 5 years after entering the United States. To eliminate TB, we must begin addressing the burden of LTBI in this high-risk group.
Figure 1. Number of tuberculosis (TB) cases per year for foreign-born and U.S.-born persons from 1993 to 2004.
[More] [Minimize]The strategy for controlling and eliminating TB in the United States is based on three priorities: (1) detect and treat patients with TB disease; (2) investigate contacts of TB cases and treat those individuals for TB disease or latent TB infection (LTBI) as indicated; and (3) target tuberculin skin tests or other assays for Mycobacterium tuberculosis infection to persons likely to be infected with TB and provide LTBI treatment to those who are infected (2). The first two of these priorities focus on interrupting ongoing community TB transmission, and have been the main components of TB control in the United States. These strategies have been tremendously effective in controlling TB in the United States overall; however, they have been less effective in controlling TB among the foreign-born population. To eliminate TB, the United States must develop a successful strategy for controlling and preventing TB among foreign-born persons.
TB disease typically results from either recent transmission due to ongoing community TB transmission or from activation of LTBI. (3) Recent molecular epidemiology studies suggest that the majority of TB cases among foreign-born persons are due to activation of latent infection. (4–7) This may explain why strategies focused on interrupting ongoing community TB transmission have had little impact on TB among foreign-born persons and highlight the importance of addressing LTBI in foreign-born persons.
In 2000, the Centers for Disease Control and Prevention (CDC) and the American Thoracic Society published guidelines to aid in determining who is at high risk for LTBI and, thus, should be targeted for M. tuberculosis testing and treatment of LTBI if infected (2). Based on previous evidence that foreign-born persons living in the United States for 5 yr or less were at higher risk for TB disease than those living in the United States for more than 5 yr (8), these guidelines recommend testing and treating only foreign-born persons from high-incidence countries who have been in the United States for 5 yr or less (2).
Given the limited success of current strategies for controlling TB among the foreign-born population, we sought to evaluate this recommendation to determine: (1) which groups are at highest risk for TB disease and should be targeted for testing for LTBI, and (2) based on these determinations of risk, whether any changes to current guidelines may be needed to improve TB control among the foreign-born population and to eliminate TB.
We collected data on TB cases reported in 2004 from the U.S. National TB Surveillance database. Reports of TB cases are submitted to CDC by the 50 states and the District of Columbia using a standardized case report form (9). These TB case reports include information on country of birth, time of entry in to the United States, specified demographic and clinical characteristics, and other TB risk factors. Consistent with the U.S. Census definition of foreign born (10), a person is classified as U.S. born if that person was born in the United States or associated jurisdictions, or was born in a foreign country but at least one parent was a U.S. citizen. All others are classified as foreign born.
We used the Public Use Microdata Sample file from the 2004 American Community Survey to derive the population denominator for reported TB cases to calculate case rates (11). These data are derived from a survey, administered by the U.S. Census Bureau, of approximately 800,000 U.S. households. Data collected include country of birth and arrival year in the United States (11). These households are surveyed regardless of immigration status (11). Current guidelines classify foreign-born persons from low-incidence countries as low risk, but they do not define low-risk countries (2). We categorized Japan, Canada, Australia, New Zealand, and the countries of Western Europe as low-incidence countries, which is consistent with the way this guideline has been implemented in the only state with a large statewide targeted tuberculin testing program (C.A.H., unpublished data). We categorized all other countries according to a scheme, which has been used for previous analyses and was devised by the World Bank (8, 12, 13).
We compared rates of TB with respect to country of origin, world region of origin, and time from United States entry to TB diagnosis. Month, date, and year of entry in to the United States was specified for TB cases, whereas only year of entry in to the United States was recorded for the population denominator (11). For TB cases, the time since entry in to the United States was calculated by subtracting the date of entry in to the United States from the date of the case report. The American Community Survey is administered over an entire year, and is thus a midyear population estimate. As such, it includes data on approximately half of the foreign-born persons who entered the United States in 2004. Thus, all persons entering the United States during 2004, and half of the persons entering in 2003, were classified as being in the United States for 1 yr or less; all persons entering the United States from 2000 to 2002 plus half of the persons entering in 1999 and half of those entering in 2003 were classified as being in the United States for 1–5 yr; and persons entering the United States before 1999 and half of those entering in 1999 were classified as being in the United States for more than 5 yr.
In 2004, 14,517 persons in the United States were reported to have TB disease; 7,806 (54%) of these were foreign born, 6,683 (46%) were U.S. born, and 28 had an unknown country of origin (Table 1) (1). Of the 7,806 foreign-born persons, reports for 975 (12%) were missing the complete date of entry in to the United States. Of the 6,831 remaining foreign-born persons, 1,620 (24%) had resided in the United States for less than 1 yr at the time of case report, 1,767 (26%) had resided in the United States for 1–5 yr, and 3,444 (50%) had resided in the United States for more than 5 yr. Patients from Mexico, the Philippines, Vietnam, India, and China accounted for 58% of foreign-born persons with reported TB in 2004 (Figure 2).
Origin | Time in the United States (yr) | Cases in 2004† n (%) | Population‡§ | Case Rate‡ |
|---|---|---|---|---|
| U.S. born | — | 6,683 (46) | 249,424,045 | 2.7 |
| Foreign born* | Total | 7,806 (54) | 36,245,582 | 21.5 |
| ⩽ 1 | 1,620 (24) | 1,338,814 | 121.0 | |
| > 1 to ⩽ 5 | 1,767 (26) | 5,885,677 | 30.0 | |
| > 5 | 3,444 (50) | 29,021,090 | 11.9 |
In 2004, the rate of TB disease among foreign-born persons was 21.5/100,000 person-years, whereas the rate among U.S.-born persons was 2.7/100,000. The rate of TB among foreign-born persons varied by duration of time in the United States: 121.0/100,000 for persons residing in the United States for 1 yr or less, 30.0/100,000 for those residing in the United States for 1–5 yr, and 11.9/100,000 for those residing in the United States for more than 5 yr (Table 1). Table 2 shows rates of TB disease in foreign-born persons by time in the United States for the 10 countries of origin, accounting for the majority of cases in 2004; rates of TB disease for the countries of origin are also provided. Rates varied substantially by both country of origin and time in the United States. For all countries, rates were highest for those who had been in the United States for less than 1 yr, and lowest for those who had been in the United States for more than 5 yr. For foreign-born persons from most of these countries, rates of TB disease among those who had been in the United States for less than 1 yr were actually higher than rates in their respective countries of origin, and then decreased to a level below the rate in the country of origin for those who had resided in the United States for 1 yr or more.
Country | Time in the United States (yr) | Cases in 2004* n (%) | Population | Case Rate† | Estimated Case Rate in Country of Origin‡ |
|---|---|---|---|---|---|
| Mexico | Total | 1,976 | 10,404,919 | 19.0 | 33 |
| ⩽ 1 | 362 (22) | 482,926 | 75.0 | ||
| > 1 to ⩽ 5 | 435 (26) | 1,974,036 | 22.0 | ||
| > 5 | 876 (52) | 7,947,958 | 11.0 | ||
| Philippines | Total | 829 | 1,594,083 | 52.0 | 296 |
| ⩽ 1 | 216 (27) | 39,804 | 542.7 | ||
| > 1 to ⩽ 5 | 124 (15) | 187,778 | 66.0 | ||
| > 5 | 414 (51) | 1,366,500 | 30.3 | ||
| Vietnam | Total | 619 | 1,067,644 | 58.0 | 178 |
| ⩽ 1 | 113 (21) | 21,711 | 520.5 | ||
| > 1 to ⩽ 5 | 71 (13) | 81,606 | 87.0 | ||
| > 5 | 352 (66) | 964,328 | 36.5 | ||
| India | Total | 557 | 1,386,321 | 40.2 | 168 |
| ⩽ 1 | 104 (22) | 69,398 | 149.9 | ||
| > 1 to ⩽ 5 | 165 (35) | 326,999 | 50.5 | ||
| > 5 | 205 (43) | 989,924 | 20.7 | ||
| China | Total | 352 | 1,239,346 | 28.4 | 102 |
| ⩽ 1 | 63 (21) | 48,850 | 129.0 | ||
| > 1 to ⩽ 5 | 58 (19) | 218,521 | 26.5 | ||
| > 5 | 186 (61) | 971,975 | 19.1 | ||
| Haiti | Total | 248 | 450,366 | 55.1 | 323 |
| ⩽ 1 | 42 (19) | 9,809 | 428.2 | ||
| > 1 to ⩽ 5 | 74 (34) | 75,278 | 98.3 | ||
| > 5 | 103 (47) | 365,279 | 28.2 | ||
| South Korea | Total | 219 | 430,491 | 50.9 | 87 |
| ⩽ 1 | 28 (15) | 17,692 | 158.3 | ||
| > 1 to ⩽ 5 | 41 (22) | 61,298 | 66.9 | ||
| > 5 | 114 (62) | 351,501 | 32.4 | ||
| Guatemala | Total | 190 | 593,271 | 32.0 | 74 |
| ⩽ 1 | 49 (28) | 28,360 | 172.8 | ||
| > 1 to ⩽ 5 | 69 (40) | 118,275 | 58.3 | ||
| > 5 | 55 (32) | 446,636 | 12.3 | ||
| Ethiopia | Total | 169 | 106,310 | 159.0 | 356 |
| ⩽ 1 | 68 (43) | 4,488 | 1515.2 | ||
| > 1 to ⩽ 5 | 42 (27) | 22,239 | 188.9 | ||
| > 5 | 47 (30) | 79,583 | 59.1 | ||
| Peru | Total | 159 | 338,041 | 47.0 | 188 |
| ⩽ 1 | 27 (18) | 11,572 | 233.3 | ||
| > 1 to ⩽ 5 | 63 (43) | 69,778 | 90.3 | ||
| > 5 | 58 (39) | 256,691 | 22.6 |
In 2004, rates of TB disease among foreign-born persons residing in the United States for more than 5 yr were over 30/100,000 among those from the Philippines, Vietnam, South Korea, and Ethiopia. These rates were higher than those in persons from Mexico and China who had been in the United States for 1–5 yr (22.0/100,000 and 26.5/100,000, respectively) and 11–18 times higher than TB rates among U.S.-born persons (2.7/100,000).
Among persons from the Middle East and North Africa, those living in the United States for longer than 5 yr had rates of disease of below 6/100,000; among persons from Latin America, South America, the Caribbean, Eastern Europe, and Central Asia, this rate was 10–13/100,000; and among persons from sub-Saharan Africa, South Asia, and East Asia and the Pacific, this rate was over 21/100,000. The overall rate of TB disease among persons from low-incidence countries was 1.7/100,000 (Table 3).
Time in the United States | ||||||
|---|---|---|---|---|---|---|
| Region | Overall Rate | ⩽ 1 Yr | > 1 to ⩽ 5 Yr | > 5 Yr | ||
| Sub-Saharan Africa | 79.0 | 1,186.9 | 91.5 | 28.0 | ||
| South Asia | 35.5 | 178.5 | 51.6 | 21.6 | ||
| East Asia and the Pacific | 37.0 | 286.6 | 48.7 | 26.3 | ||
| Latin America, South America, and the Caribbean | 16.1 | 81.8 | 26.2 | 10.2 | ||
| Eastern Europe and Central Asia | 16.8 | 65.4 | 19.2 | 12.6 | ||
| Middle East and North Africa | 7.5 | 46.8 | 14.6 | 5.2 | ||
| Low-incidence countries† | 1.7 | 3.0 | 2.0 | 1.6 | ||
Previous studies have demonstrated that rates of TB disease were lower among foreign-born persons who had been in the United States for more than 5 yr (8, 13). These data contributed to the development of a public health recommendation that only those residing in the United States for 5 yr or less should be targeted for tuberculin skin testing and treatment of LTBI (2). Since the middle to late 1990s, when these studies were published, the rate of TB among U.S.-born persons has substantially declined, whereas the rate among foreign-born persons has decreased at a far slower pace, thus greatly widening the gap between case rates for U.S.-born and foreign-born persons (1). Our analysis confirmed that case rates for foreign-born persons from all world regions are extremely high in the first year after entry in to the United States (up to 440 times those of U.S.-born persons), and, though lower, remain substantially elevated 1–5 yr after entry in to the United States. However, we found that TB case rates for foreign-born persons from selected countries and world regions remain markedly elevated, even more than 5 yr after their arrival in the United States, with rates up to 10-fold those of U.S.-born persons.
In 2004, over half of all reported U.S. TB cases were among the foreign-born population, and half of those were among foreign-born persons who entered the United States more than 5 yr previously. Thus, 25% of all reported TB cases in the United States are among foreign-born persons who have lived in the United States for more than 5 yr. There is no policy to test foreign-born persons for LTBI before coming to the United States (14, 15), nor to test them after they have lived in the United States for more than 5 yr. As such, present guidelines do not currently address the burden of LTBI in this foreign-born subgroup. As of 2004, there were almost 29 million foreign-born U.S. residents who had entered the United States more than 5 yr previously. Overall, this population had a TB case rate of 11.9/100,000, such that over 3,400 TB cases would be expected from this group annually. The goal of TB control in the United States is TB elimination, which is defined as less than 1 case per million population, which would currently be less than 300 cases per year (16). Until we address the burden of LTBI in this group, achieving TB elimination will not be possible.
Current guidelines recommend that patients presenting to a healthcare provider for routine care, whether to a private provider or to a health department, should be tested for LTBI if they are at high risk for TB disease (2). Our findings highlight the fact that some populations of foreign-born persons who entered the United States more than 5 yr previously have TB case rates exceeding those of other groups classified as high risk by current guidelines, such as persons from Mexico and China who entered the United States 1–5 yr previously, and persons with diabetes (2, 17, 18). These findings suggest the need to consider updating current guidelines to include these additional high-risk populations. Considering that we documented elevated rates of TB disease for all foreign-born groups included in this study compared with U.S.-born persons, except for those from low-incidence countries, one approach would be to update the guidelines to classify all foreign-born persons from high-incidence countries as high risk, regardless of time since entry in to the United States.
The data presented here can also be used by TB control programs or groups interested in developing community-based LTBI testing programs aimed at foreign-born persons from the highest TB incidence countries or world regions. Communities in which the highest-risk individuals reside would provide ideal places to implement a targeted testing program, as foreign-born persons from specific countries or regions often cluster in certain areas (5, 19, 20). Because such programs could be associated with a perception of discrimination, targeting foreign-born persons for LTBI testing must be done in culturally sensitive ways, and should emphasize that this is an effort to offer specialized care to groups known to be at high risk (21, 22).
If current guidelines are expanded to include more high-risk, foreign-born persons, other barriers to implementation of testing for TB infection must be addressed. Current targeted M. tuberculosis testing guidelines have not been fully implemented in most areas, and there are limited resources designated for this activity. Furthermore, in places where targeted testing has been implemented, ensuring high LTBI treatment completion rates has been difficult (23, 24). Finally, many immigrants do not access established healthcare facilities as readily as U.S.-born persons. Efforts to improve successful detection and treatment of LTBI require collaboration with partners from affected communities to address and overcome these barriers.
Expanding LTBI testing and treatment to include foreign-born persons who have lived in the United States for longer than 5 yr is not the only possible approach to TB control in the foreign-born population, nor is it, in itself, sufficient. Other efforts must be aimed at studying best practices for controlling TB in the foreign-born population, such as assessments of the feasibility of expanding immigrant screening to include groups not currently screened (e.g., persons entering on work visas or student visas), improving overseas screening techniques to increase sensitivity of screening, finding and treating LTBI in immigrants before entry in to the United States, and investing in international TB control (14, 25–31). All of these approaches have great long-term potential to decrease the burden of TB in the foreign-born population. However, none of these strategies address the over 34 million foreign-born persons already living in the United States. Controlling and eliminating TB will require a comprehensive strategy, with different approaches for different groups.
There are some limitations to this study. First, we did not study the impact of other risk factors for TB disease, including frequency of travel back to the country of origin (32, 33). Second, the U.S. National TB Surveillance database does not collect information about immigration status, thus limiting the assessment of the contribution of absent overseas screening for TB disease to high rates of TB disease found in this study. Next, 975 foreign-born persons did not have complete information for date of entry in to the United States, which likely caused an underestimate in our calculation of rates. Because evidence from the surveillance system suggests that well over half of these patients entered the United States more than 5 yr previously, the magnitude of underestimation is likely greatest in this group. Finally, although current evidence suggests that most foreign-born TB cases are due to activation of LTBI and not to recent transmission, we cannot quantify the exact proportion attributable to each in this study.
Over the past 12 yr, the United States has made substantial progress toward achieving the goal of TB elimination among U.S.-born persons, but only limited progress among foreign-born persons. Despite this, and the increasing global burden of TB (34), resources for fighting the disease in the United States are decreasing (35). If the current trend in TB cases continues, TB in the United States may, in the future, be nearly eliminated among U.S.-born persons, while persisting at high levels among foreign-born populations. If we are to avoid another resurgence of TB, we must address the ongoing problem of TB in the foreign-born population. For the United States to achieve its goal of TB elimination, resources for targeted testing and treatment of LTBI are essential (14, 15). These data help to target additional groups for such testing and treatment.
The authors acknowledge the local and state tuberculosis (TB) programs, which are the sources of all reported TB data, and the American Community Survey for their assistance with population data. They also thank Jose E. Becerra, Thomas R. Navin, Valerie A. Robison, and Ann Lanner for their review of this manuscript, and J. Steve Kammerer and Robert H. Pratt for their assistance with data analysis.
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