Abstract
We calculated population-based tuberculosis (TB) rates among HIV-infected persons in New York City from 2001 through 2005 using data from the city's TB and HIV/AIDS surveillance registries, and we examined those rates using linear trend tests and incidence rate ratios (IRRs). HIV-infected individuals had 16 times the TB rate of a “non-HIV” population (HIV status negative or unknown; IRR = 16.0; 95% confidence interval = 14.9, 17.2). TB rates declined significantly among the US-born HIV-infected population (P trend < .001) but not among the foreign-born HIV-infected population (P trend = .355). Such disparities must be addressed if further declines are to be achieved.
HIV infection is the greatest known risk factor for progression from latent tuberculosis (TB) infection to active TB disease.1–3 For HIV-infected individuals with latent tuberculosis infection, the risk of progression to active TB ranges from 4% to 16% per year, whereas the risk among HIV-negative individuals is 10% per lifetime.4,5 Active disease among HIV-infected individuals can occur rapidly after TB infection.6 Although TB rates have declined 56% in the United States since the early 1990s,7–9 the estimated 56 300 new HIV infections in 200610–13 necessitate evaluation of HIV's impact on current TB epidemiology. We examined TB rates among HIV-infected individuals in New York City from 2001 through 2005.
METHODS
Our analysis used data from the New York City TB registry and included all TB cases verified in New York City from January 1, 2001, through December 31, 2005. Any TB case reported more than 1 year after that patient completed treatment of active TB or was lost to follow-up was considered a new incident case. TB patients were considered HIV-infected if they had a positive HIV test result via enzyme-linked immunosorbent assay (ELISA) or rapid HIV antibody testing at TB diagnosis, confirmed by western blot, or if a history of positive HIV test was self-reported or was recorded in their medical record.
We used New York City HIV/AIDS surveillance registry data to calculate annual population estimates of HIV-infected individuals by adding the number of known persons living with HIV/AIDS at the end of each year to the number of deaths among those with HIV/AIDS during that year. Annual TB rates per 100 000 persons were calculated and stratified by birth in the United States, sex, age, and race/ethnicity. Trends in rates were evaluated using the Cochran-Armitage test for trend. To enable us to compare TB rates among HIV-infected US-born and foreign-born populations, we calculated incidence rate ratios (IRRs). Analyses were performed using Microsoft Excel 2003 (Microsoft Corp, Redmond, WA) and SAS version 8.2 (SAS Institute, Cary, NC).
RESULTS
From 2001 through 2005, 16% of all patients with TB disease in New York City were HIV-infected (n = 872). The TB rate among HIV-infected persons decreased 26%, from 205.2 per 100 000 persons in 2001 to 151.4 per 100 000 persons in 2005 (P trend = .001; Table 1). The HIV-infected population had 16 times the TB rate of a “non-HIV” population comprising HIV-negative individuals or those with unknown HIV status (IRR = 16.0; 95% confidence interval [CI] = 14.9, 17.2). Significant declines in TB rates were seen among HIV-infected non-Hispanic Blacks, Asians, and females (P trend < .05).
TABLE 1.
Linear Trends of Tuberculosis (TB) Rates Among US-Born and Foreign-Born HIV-Infected Individuals: New York City, NY, 2001–2005
| 2001 |
2002 |
2003 |
2004 |
2005 |
2001–2005 |
||||||
| No. of TB Cases | TB Rate Per 100 000 Persons | No. of TB Cases | TB Rate Per 100 000 Persons | No. of TB Cases | TB Rate Per 100 000 Persons | No. of TB Cases | TB Rate Per 100 000 Persons | No. of TB Cases | TB Rate Per 100 000 Persons | Ptrenda | |
| All cases | |||||||||||
| Total | 181 | 205.2 | 195 | 211.5 | 177 | 186.1 | 169 | 174.0 | 150 | 151.4 | .001 |
| Age, y | |||||||||||
| 0–12 | 0 | 0.0 | 1 | 65.5 | 0 | 0.0 | 1 | 87.5 | 1 | 101.8 | .245 |
| 13–19 | 0 | 0.0 | 1 | 84.5 | 1 | 75.6 | 0 | 0.0 | 2 | 132.5 | .408 |
| 20–29 | 15 | 269.5 | 13 | 227.2 | 11 | 187.5 | 9 | 152.3 | 5 | 82.7 | .011 |
| 30–39 | 72 | 268.3 | 60 | 230.3 | 56 | 227.8 | 53 | 231.7 | 52 | 246.0 | .622 |
| 40–49 | 59 | 174.5 | 67 | 187.4 | 75 | 200.8 | 62 | 161.7 | 48 | 122.8 | .047 |
| 50–59 | 23 | 153.3 | 40 | 234.8 | 31 | 163.0 | 33 | 157.1 | 32 | 139.2 | .204 |
| ≥ 60 | 12 | 283.4 | 13 | 263.7 | 3 | 53.1 | 11 | 171.6 | 10 | 137.2 | .051 |
| Race/ethnicity | |||||||||||
| Non-Hispanic Black | 109 | 277.3 | 126 | 304.3 | 117 | 272.8 | 111 | 252.6 | 94 | 209.2 | .015 |
| Hispanic | 49 | 170.7 | 53 | 178.1 | 47 | 153.9 | 46 | 148.4 | 38 | 120.7 | .067 |
| Non-Hispanic White | 13 | 70.3 | 10 | 52.0 | 4 | 20.2 | 10 | 49.6 | 11 | 53.6 | .509 |
| Asian | 10 | 1210.7 | 6 | 650.1 | 9 | 892.9 | 2 | 180.8 | 6 | 500.0 | .025 |
| Sex | |||||||||||
| Male | 117 | 191.2 | 137 | 214.6 | 130 | 197.3 | 117 | 173.9 | 112 | 162.8 | .062 |
| Female | 64 | 236.9 | 58 | 204.6 | 47 | 160.7 | 52 | 174.2 | 38 | 125.6 | .001 |
| US-born | |||||||||||
| Total | 120 | 205.8 | 132 | 218.2 | 106 | 172.4 | 99 | 160.8 | 85 | 137.7 | <.001 |
| Age, y | |||||||||||
| 0–12 | 0 | 0.0 | 1 | 72.7 | 0 | 0.0 | 1 | 97.7 | 1 | 113.3 | .244 |
| 13–19 | 0 | 0.0 | 0 | 0.0 | 0 | 0.0 | 0 | 0.0 | 2 | 158.6 | … |
| 20–29 | 8 | 220.9 | 7 | 187.3 | 3 | 79.1 | 3 | 80.0 | 3 | 79.4 | .037 |
| 30–39 | 45 | 257.9 | 31 | 184.1 | 32 | 205.2 | 28 | 198.4 | 21 | 164.6 | .134 |
| 40–49 | 38 | 171.6 | 54 | 232.6 | 46 | 192.0 | 36 | 148.8 | 26 | 107.0 | .01 |
| 50–59 | 20 | 199.8 | 32 | 284.7 | 24 | 194.7 | 22 | 164.6 | 27 | 187.8 | .246 |
| ≥ 60 | 9 | 335.4 | 7 | 226.1 | 1 | 28.6 | 9 | 229.6 | 5 | 114.2 | .084 |
| Race/ethnicity | |||||||||||
| Non-Hispanic Black | 80 | 290.9 | 92 | 320.1 | 74 | 252.2 | 67 | 227.8 | 53 | 179.6 | .001 |
| Hispanic | 26 | 145.4 | 30 | 163.4 | 29 | 156.5 | 24 | 130.3 | 23 | 125.6 | .409 |
| Non-Hispanic White | 12 | 95.8 | 10 | 77.2 | 3 | 22.8 | 8 | 60.3 | 9 | 67.1 | .307 |
| Asian | 2 | 1030.9 | 0 | 0.0 | 0 | 0.0 | 0 | 0.0 | 0 | 0.0 | … |
| Sex | |||||||||||
| Male | 69 | 173.4 | 92 | 223.1 | 71 | 169.2 | 69 | 164.1 | 59 | 139.4 | .046 |
| Female | 51 | 275.4 | 40 | 207.8 | 35 | 179.1 | 30 | 153.6 | 26 | 134.0 | .001 |
| Foreign-born | |||||||||||
| Total | 61 | 549.4 | 61 | 511.4 | 71 | 561.7 | 70 | 523.7 | 64 | 453.8 | .355 |
| Age, y | |||||||||||
| 0–12 | 0 | 0.0 | 0 | 0.0 | 0 | 0.0 | 0 | 0.0 | 0 | 0.0 | … |
| 13–19 | 0 | 0.0 | 1 | 1250.0 | 1 | 1234.6 | 0 | 0.0 | 0 | 0.0 | … |
| 20–29 | 7 | 682.3 | 6 | 558.1 | 8 | 716.8 | 6 | 539.1 | 2 | 174.5 | .129 |
| 30–39 | 27 | 769.9 | 28 | 776.1 | 24 | 661.7 | 25 | 677.5 | 31 | 836.5 | .93 |
| 40–49 | 21 | 524.7 | 12 | 278.0 | 29 | 626.3 | 26 | 531.0 | 21 | 407.1 | .984 |
| 50–59 | 3 | 170.6 | 8 | 397.6 | 7 | 310.7 | 11 | 432.7 | 5 | 175.9 | .898 |
| ≥ 60 | 3 | 424.9 | 6 | 747.2 | 2 | 221.2 | 2 | 198.0 | 5 | 439.0 | .475 |
| Race/ethnicity | |||||||||||
| Non-Hispanic Black | 29 | 613.8 | 33 | 641.6 | 43 | 783.2 | 44 | 746.6 | 40 | 635.4 | .744 |
| Hispanic | 23 | 501.1 | 22 | 449.5 | 18 | 347.4 | 22 | 406.4 | 15 | 264.6 | .06 |
| Non-Hispanic White | 1 | 79.7 | 0 | 0.0 | 1 | 74.0 | 2 | 144.9 | 2 | 143.2 | .285 |
| Asian | 8 | 1687.8 | 6 | 1156.1 | 9 | 1633.4 | 2 | 325.7 | 6 | 894.2 | .087 |
| Sex | |||||||||||
| Male | 48 | 598.7 | 44 | 515.9 | 59 | 657.5 | 48 | 508.7 | 53 | 534.0 | .575 |
| Female | 13 | 421.3 | 17 | 500.0 | 12 | 327.2 | 22 | 559.7 | 11 | 263.3 | .403 |
Note. Ellipses indicate that the P value could not be calculated.
Cochrane-Armitage test for trend.
US-born persons, accounting for 62% of HIV-infected TB patients, experienced significant decreases in TB rates, from 205.8 per 100 000 persons to 137.7 per 100 000 persons (P trend < .001; Table 1). The most pronounced declines were among Blacks (–38%), females (–51%), and individuals aged 20 to 29 years (–64%).
No significant declines occurred among the HIV-infected foreign-born population overall or among any foreign-born subgroup (Table 1). Foreign-born subgroups with the highest case numbers and annual rates included those aged 30 to 39 years (41% of cases; rates 661.7–836.5 per 100 000 persons), males (77%; rates 508.7–598.7 per 100 000 persons), and Blacks (58%; rates 613.8–783.2 per 100 000 persons). Foreign-born Blacks experienced nonsignificant increases of 38% in TB case numbers and 4% in TB rates. Foreign-born TB rates were consistently higher than US-born TB rates for most subgroups, with an overall IRR of 2.9 (95% CI = 2.5, 3.5; Table 2).
TABLE 2.
Incidence Rate Ratios (IRRs) Comparing Foreign-Born to US-Born HIV-Infected Individuals by Year of Tuberculosis (TB) Case Verification: New York City, NY, 2001–2005
| 2001, IRR (95% CI) | 2002, IRR (95% CI) | 2003, IRR (95% CI) | 2004, IRR (95% CI) | 2005, IRR (95% CI) | 2001–2005, IRR (95% CI) | |
| Total | 2.7 (2.0, 3.6) | 2.3 (1.7, 3.2) | 3.3 (2.4, 4.4) | 3.3 (2.4, 4.4) | 3.3 (2.4, 4.6) | 2.9 (2.5, 3.3) |
| Age, y | ||||||
| 20–29 | 3.1 (1.1, 8.5) | 3.0 (1.0, 8.9) | 9.1 (2.4, 34.2) | 6.7 (1.7, 27.0) | 2.2 (0.4, 13.2) | 4.1 (2.4, 7.1) |
| 30–39 | 3.0 (1.9, 4.8) | 4.2 (2.5, 7.0) | 3.2 (1.9, 5.5) | 3.4 (2.0, 5.9) | 5.1 (2.9, 8.8) | 3.7 (2.9, 4.6) |
| 40–49 | 3.1 (1.8, 5.2) | 1.2 (0.6, 2.2) | 3.3 (2.1, 5.2) | 3.6 (2.2, 5.9) | 3.8 (2.1, 6.8) | 2.8 (2.2, 3.5) |
| 50–59 | 0.9 (0.3, 2.9) | 1.4 (0.6, 3.0) | 1.6 (0.7, 3.7) | 2.6 (1.3, 5.4) | 0.9 (0.4, 2.4) | 1.5 (1.0, 2.1) |
| ≥ 60 | 1.3 (0.3, 4.7) | 3.3 (1.1, 9.8) | 7.7 (0.7, 85.2) | 0.9 (0.2, 4.0) | 3.8 (1.1, 13.3) | 2.2 (1.3, 4.0) |
| Race/ethnicity | ||||||
| Non-Hispanic Black | 2.1 (1.4, 3.2) | 2.0 (1.3, 3.0) | 3.1 (2.1, 4.5) | 3.3 (2.2, 4.8) | 3.5 (2.3, 5.3) | 2.7 (2.3, 3.2) |
| Hispanic | 3.4 (2.0, 6.0) | 2.8 (1.6, 4.8) | 2.2 (1.2, 4.0) | 3.1 (1.7, 5.6) | 2.1 (1.1, 4.0) | 2.7 (2.1, 3.5) |
| Non-Hispanic White | 0.8 (0.1, 6.4) | NA | 3.2 (0.3, 31.1) | 2.4 (0.5, 11.3) | 2.1 (0.5, 9.9) | 1.4 (0.6, 3.3) |
| Asian | 1.6 (0.3, 7.7) | NA | NA | NA | NA | 6.7 (1.6, 28.0) |
| Sex | ||||||
| Male | 3.5 (2.4, 5.0) | 2.3 (1.6, 3.3) | 3.9 (2.8, 5.5) | 3.1 (2.1, 4.5) | 3.8 (2.6, 5.6) | 3.2 (2.8, 3.8) |
| Female | 1.5 (0.8, 2.8) | 2.4 (1.4, 4.2) | 1.8 (0.9, 3.5) | 3.6 (2.1, 6.3) | 2.0 (1.0, 4.0) | 2.2 (1.7, 2.8) |
Note. CI = confidence interval; NA = not applicable (IRR could not be computed).
DISCUSSION
Our analysis reemphasizes the elevated risk of TB disease among HIV-infected individuals. Unlike the significant declines in TB rates observed among the US-born HIV-infected population, there were no significant declines among the foreign-born. This issue is not only a concern in New York City, where the population is approximately 36% foreign-born,14 but to the United States as a whole, as immigrants from high-TB-burden countries continue to settle in areas other than large cities.15,16
The observed rise in TB cases among HIV-infected foreign-born Blacks is also troubling. One possible explanation for this finding could be the nationalities of recent immigrants to New York City. As of 2000, 24% of the foreign-born population in New York City was from the Caribbean or Africa,14 areas with high TB incidence; in 2006, 56% of new HIV diagnoses among New York City's foreign-born were among those of Caribbean origin.17 Further evaluation is needed to determine if there is a true increase in TB rates among HIV-infected foreign-born Blacks and to provide focused interventions if warranted.
To our knowledge, this is the first population-based analysis of TB rates among HIV-infected persons. Limitations include the potential underestimation of the HIV-infected population in New York City; thus, misestimates of TB rates in this population are possible. Also, approximately 22% of the HIV-infected population had an unknown country of birth, potentially causing overestimates of rates by country of origin. However, because misclassification would be consistent throughout the study period, observed trends would be unlikely to change importantly. Finally, we could not examine HIV disease severity because of lack of data on antiretroviral use, other opportunistic infections, CD4 cell count, and viral load. Despite these limitations, we observed disparities in the decline of TB rates in US-born and foreign-born HIV-infected groups.
HIV/AIDS poses a considerable challenge to TB control. Within New York City and the United States, overall TB rates have declined; however, in New York City this decrease has not been as significant among foreign-born HIV-infected populations. Such disparities must be addressed if further declines in TB rates are to be achieved.
Acknowledgments
The authors would like to thank Lucia Torian, PhD, Melissa Riley Pfeiffer, MPH, Tracy Agerton, RN, MPH, Arpi Terzian, PhD, MPH, and Ellen Weiss Wiewel, MHS, for their work on this project. The authors would also like to thank Holly Anger, MPH, Neil Schluger, MD, and Kieran Hartsough for their valued input on the article.
Human Participant Protection
This study protocol received approval from the institutional review boards of the New York City Department of Health and Mental Hygiene and the Centers for Disease Control and Prevention.
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