INT J TUBERC LUNG DIS 19(8):943–953 Q 2015 The Union http://dx.doi.org/10.5588/ijtld.14.0642
HIV counseling and testing in tuberculosis contact investigations in the United States and Canada Y. Hirsch-Moverman,* W. A. Cronin,† B. Chen,‡ J. A. Moran,* E. Munk,§ M. R. Reichler,‡ and the Tuberculosis Epidemiological Studies Consortium Task Order 2 Team *ICAP, Mailman School of Public Health, Columbia University, New York, New York, †Maryland Department of Health and Mental Hygiene, Baltimore, Maryland, ‡Centers for Disease Control and Prevention, Atlanta, Georgia, § Johns Hopkins University School of Medicine, Baltimore, Maryland, USA SUMMARY B A C K G R O U N D : Determining the human immunodeficiency virus (HIV) status of tuberculosis (TB) patients and contacts is important. Despite existing guidelines, not all patients are tested, and testing of contacts is rarely performed. M E T H O D S : In a study conducted at nine US/Canadian sites, we introduced formal procedures for offering HIV testing to TB patients and contacts. Data were collected via interviews and medical record review. Characteristics associated with offering and accepting HIV testing were examined. R E S U LT S : Of 651 TB patients, 601 (92%) were offered testing, 511 (85%) accepted, and 51 (10%) were HIVinfected. Of 4152 contacts, 3099 (75%) were offered testing, 1202 (39%) accepted, and 24 (2%) were HIVinfected. Contacts aged 15–64 years, non-Whites,
foreign-born persons, smokers, those with positive TB screening, and household contacts were more likely to be offered testing, whereas contacts exposed to HIVnegative patients were less likely to be offered testing. Contacts aged 15–64 years, smokers, drug/alcohol users, diabetics, and those with positive TB screening were more likely to accept testing. Foreign-born persons, Blacks, Hispanics, and contacts exposed to HIV-positive patients were less likely to accept testing. C O N C L U S I O N S : High rates of HIV were detected among patients and contacts. Despite structured procedures to offer HIV testing, some patients and most contacts did not accept testing. Strategies are needed to improve testing acceptance rates. K E Y W O R D S : TB; contact investigation; HIV; HIV testing
TUBERCULOSIS (TB) is epidemic throughout much of the world, and is a leading cause of death among human immunodeficiency virus (HIV) infected persons.1 In the United States, which reports approximately 14 000 TB cases annually, an estimated 8% of patients with a known HIV test result are coinfected.2 Knowledge of HIV status is essential for decision making about anti-tuberculosis treatment.3 In the United States and Canada, contacts exposed to pulmonary TB patients are routinely evaluated for TB disease and latent tuberculous infection (LTBI). Determining the HIV status of contacts is essential, as HIV is a major predictor for progression from LTBI to TB;4 persons with low CD4 counts may be anergic, and be negative on the tuberculin skin test (TST);4 and interferon-gamma release assays for diagnosing TB may be less useful in patients with CD4 counts ,200 cells/mm3.5 Furthermore, HIV prevalence has been reported to be greater among TB contacts than
in the general population.6 The US Centers for Disease Control and Prevention (CDC) recommend LTBI treatment for HIV-infected close contacts of TB cases, regardless of TST status. The CDC has recommended HIV testing for all TB patients since 1987, and for contacts of TB patients since 2001.7,8 The Canadian TB Committee has recommended that contacts of TB patients be tested for HIV since 2002.9 Nevertheless, not all TB patients in the United States and Canada are being tested for HIV, and reports suggest HIV testing may still not be a routine part of contact investigations. In a multisite evaluation of contact investigations in the United States reported in 2002, only 64% of TB patients and 19% of contacts were tested for HIV.6 Our study objectives were 1) to introduce routine offering of HIV testing to both TB patients and contacts in the TB clinic or field setting as an intervention to improve HIV testing rates, 2) to determine clinical and epidemiologic
Correspondence to: Yael Hirsch-Moverman, ICAP, Mailman School of Public Health, Columbia University, 215 West 125th St, Suite A, New York, NY 10027, USA. Tel: (þ1) 646 524 8344. e-mail: [email protected] Mary Reichler, Division of Tuberculosis Elimination, National Center for HIV, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30333, USA. Tel: (þ1) 404 639 5350. e-mail: [email protected] Article submitted 2 September 2014. Final version accepted 1 April 2015.
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characteristics associated with offering and accepting HIV testing among infectious TB patients and their contacts, 3) to explore why health department personnel did not offer testing to all TB patients and contacts, and 4) to determine why some TB patients and contacts did not accept testing.
METHODS Contact investigation We enrolled TB patients and their contacts prospectively from January 2002 to December 2006 at nine (seven US and two Canadian) TB Epidemiologic Studies Consortium (TBESC) sites. All sites included a large urban area, and three also included surrounding rural areas. Eligible participants included TB patients with positive sputum cultures for Mycobacterium tuberculosis and their close contacts, defined as persons sharing airspace for 715 h per week on average, the minimum exposure time established by investigator consensus as constituting extensive exposure. TB patient interview and data collection Dedicated study staff hired by the participating TBESC sites collected demographics, clinical symptoms, smoking, HIV testing history, exposure environments, and persons exposed in each environment using standardized questionnaires. Study staff had translators available at all sites. Medical records and surveillance data were reviewed for information on drug and alcohol use, homelessness, incarceration, sputum smear, lung cavitation, and HIV results. Contact interview and data collection Contacts were interviewed regarding demographics, smoking, HIV history, drug and alcohol use, diabetes, and use of systemic steroids. Medical records were reviewed for TST and HIV test results. HIV testing intervention Study personnel were trained to offer HIV testing to all TB patients and contacts with no documented prior positive or negative test within the preceding 6 weeks according to a written protocol. Results of HIV offering, acceptance, and reasons for not offering and not accepting testing were recorded. Definitions We defined ‘drug use’ as self-reported current use of injectable or non-injectable drugs; ‘heavy alcohol use’ as self-reported 712 beers, 71 bottle of wine, or 71 pint of hard liquor per week; ‘smokers’ as persons who self-reported smoking in the past 6 months; positive TST as induration 75 mm;10 and TST converter as documented negative TST at baseline, but a positive test .10 weeks post-exposure.
Analysis HIV offering, acceptance, infection rates, and characteristics associated with not being offered or not accepting HIV testing were evaluated. Bivariate analyses were performed using the v2 or Fisher’s exact test. Multivariable logistic regression for risk factors for offering and acceptance for contacts was performed using backward elimination. All analyses were conducted using SAS 9.1 (Statistical Analysis System Institute, Cary, NC, USA). P , 0.05 was considered significant. Human subjects approvals were obtained from the CDC and from all local sites.
RESULTS TB patients offered and accepting testing Of 718 TB patients, 65 (9%) had previous positive HIV test results, and HIV test offering and accepting status was undocumented for 2 patients (Figure). Of the 651 remaining patients, 601 (92%) were offered testing. Patients less likely to be offered testing were those aged 765 years, Hispanics, and smokers. Of 601 patients offered HIV testing, 511 (85%) accepted. Being aged 2544 or 765 years, Hispanic, foreign-born, or a current smoker were associated with non-acceptance (data not shown). HIV results among TB patients Of 511 TB patients who accepted testing, results were documented for 500 (98%), 51 (10%) of whom were newly diagnosed as HIV-infected (Table 1). There were a total of 116 HIV-infected patients (21% of 565 with known results). Compared with noninfected patients, those with newly detected HIV infection were more likely to be aged 2544 years (P ¼ 0.02), non-Hispanic Black or American Indian/First Nations race/ethnicity (P , 0.01), US/Canada-born (P ¼ 0.01), drug users (P , 0.01), homeless (P , 0.01), and have no acid-fast bacilli detected on sputum smear microscopy and pulmonary cavities on radiography (P ¼ 0.03). Of those tested, newly detected HIV infection was higher among injection drug users (9/22, 41%) than non-injection drug users (16/60, 27%); 13% (40/304) of US/Canada-born patients were HIV-infected compared to 6% (11/196) of foreign-born persons (P , 0.01 for all comparisons). Compared to previously diagnosed HIVinfected patients, newly diagnosed HIV-infected patients were more likely to be male, and less likely to report heavy alcohol use. Patients who were aged 765 years, Hispanic, or foreign-born were less likely to have known HIV status. Contacts offered testing Of 4586 close contacts, 47 (1%) reported previous positive HIV test results, and an additional 387 did
HIV testing in TB contact investigations
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exposed to HIV-positive index TB patients were less likely to accept testing. Among foreign-born contacts, age ,15 years was a more common reason for refusing to be tested, while among US/Canada-born contacts the most frequent reason was unwillingness to know their HIV status. HIV results among contacts Of 1208 contacts with results available, 47 (4%) had a previous HIV diagnosis, 24 (2%) had new positive HIV results, and 1137 (94%) had new negative HIV results (Table 5). Overall, US/Canada-born contacts were more likely to be HIV-infected than foreignborn contacts (P , 0.001). Compared with HIVnegative contacts, newly diagnosed HIV-infected contacts were older and more likely to be male, US/ Canada-born, or a contact of an HIV-infected index patient. Contacts with newly diagnosed and previously known infection were similar across all variables. Among all contacts with known status, HIV infection rates were 17% (10/60) among injecting drug users, 9% (22/241) among noninjecting drug users, and 23% (43/184) among contacts of an HIV-infected index case. Figure Summary of numbers of TB patients and contacts, from identification to offering, accepting, and results of HIV testing. TB ¼ tuberculosis; HIV ¼ human immunodeficiency virus; þ ¼ positive; ¼ negative.
not have test offering and accepting status recorded; these were excluded from further analyses (Figure). Of the 4152 remaining patients, 3099 (75%) were offered HIV testing. Bivariate results are shown in Table 2, multivariable results in Table 3, and reasons given by staff for not offering testing in Table 4. Exposure to TB occurred in households (63%), social environments (18%), workplaces (15%), and schools (3%). Of contacts not offered testing, 102 (10%) were contacts of HIV-infected TB patients, and 398 (38%) did not complete TST screening. In multivariable analysis, contacts aged 15–64 years, nonWhites, foreign-born persons, smokers, those with positive screening results for LTBI and TB disease, and household contacts were more likely to be offered testing; contacts exposed to an HIV-negative index TB patient were less likely to be offered testing. The most common reasons for staff not offering testing differed by the contact’s birth country (Table 4). Contacts accepting testing Of 3099 contacts offered HIV testing, 1202 (39%) accepted. In multivariable analysis, contacts aged 15– 64 years, smokers, street drug users, alcohol users, diabetics, and those with positive screening results for LTBI and TB disease were more likely to accept testing. Foreign-borns, Blacks, Hispanics, and those
DISCUSSION In our large multisite study, HIV status was identified in only 79% of TB patients and 26% of contacts, despite existing public health guidelines recommending HIV testing8–10 and a study intervention to offer HIV testing to all TB patients and contacts as part of the contact investigation. Of those tested, 21% of TB patients and 6% of contacts were HIV-infected. We found that 20% of untested TB patients and 25% of untested contacts were drug users, a group likely to be at increased risk for HIV infection. Our study describes risk factors for not offering and not accepting HIV testing, and identifies important missed opportunities for appropriate evaluation and treatment for HIV for both TB patients and exposed contacts. These findings are important for devising procedures and interventions aimed at improving HIV testing rates, and are of relevance to medical providers and public health professionals. Past studies have demonstrated increases in HIV testing rates among TB patients over the past decade.11–16 HIV testing rates reported for TB patients in the United States reached 84% in 2012,12 and testing in Alberta, Canada, using an opt-out approach reached 95% in 2007–2008.15 In keeping with these reports, more than 90% of TB patients in our study were offered HIV testing. Very young and older TB patients were offered HIV testing less frequently than other age groups, and when offered testing, they often refused. CDC-published TB surveillance reports include HIV testing status for
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Table 1 Characteristics of 718 infectious tuberculosis patients by HIV status at the nine participating Tuberculosis Epidemiologic Studies Consortium Sites, 2002–2006 HIV status
Case characteristics
Prior HIVþ (n ¼ 65) n (%)
Age groups, years 15–24 (reference) 25–44 45–64 765
1 34 28 2
(1.5) (52.3) (43.1) (3.1)
4 (7.8) 30 (58.8) 17 (33.3) 0
80 172 136 61
Sex Male (reference) Female
34 (52.3) 31 (47.7)
37 (72.5) 14 (27.5)
1 5 55 3 1
2 3 39 6 1
Race/ethnicity Hispanic Non-Hispanic White (reference) Non-Hispanic Black American Indian/Alaskan Native Asian Other
(1.5) (7.7) (84.6) (4.6) (1.5) 0
New HIVþ (n ¼ 51) n (%)
(3.9) (5.9) (76.5) (11.8) (2.0) 0
New HIV (n ¼ 449) n (%) (17.8) (38.3) (30.3) (13.6)
Unknown status (n ¼ 153) n (%) (11.1) (35.9) (22.2) (30.7)
0.62 0.85 ,0.01
283 (63.0) 166 (37.0)
86 (56.2) 67 (43.8)
0.15
98 71 202 18 58 2
45 17 64 5 21 1
(21.8) (15.8) (45.0) (4.0) (12.9) (0.4)
17 55 34 47
Unknown vs. known status P value
(29.4) (11.1) (41.8) (3.3) (13.7) (0.7)
0.02 0.99 0.79 0.19 0.46
,0.01
Birthplace US/Canada (reference) Foreign-born
55 (84.6) 10 (15.4)
40 (78.4) 11 (21.6)
264 (58.8) 185 (41.2)
77 (50.3) 76 (49.7)
Smoking in past 6 months Yes No (reference) Unknown/missing
39 (60.0) 23 (35.4) 3 (4.6)
27 (52.9) 23 (45.1) 1 (2.0)
194 (43.2) 255 (56.8) 0
42 (27.5) 110 (71.9) 1 (0.7)
,0.01
Injection drug use Yes No (reference) Unknown/missing
18 (27.7) 38 (58.5) 9 (13.8)
9 (17.6) 31 (60.8) 11 (21.6)
13 (2.9) 372 (82.9) 64 (14.3)
2 (1.3) 121 (79.1) 30 (19.6)
0.01
Non-injection drug use Yes No (reference) Unknown/missing
30 (46.2) 27 (41.5) 8 (12.3)
16 (31.4) 24 (47.1) 11 (21.6)
44 (9.8) 341 (75.9) 64 (14.3)
12 (7.8) 111 (72.5) 30 (19.6)
Excess alcohol use Yes No (reference) Unknown/missing
34 (52.3) 23 (35.4) 8 (12.3)
8 (15.7) 32 (62.7) 11 (21.6)
65 (14.5) 319 (71.0) 65 (14.5)
20 (13.1) 103 (67.3) 30 (19.6)
Homeless in past year Yes No (reference) Unknown
11 (16.9) 47 (72.3) 7 (10.8)
8 (15.7) 32 (62.7) 11 (21.6)
22 (4.9) 368 (82.0) 59 (13.1)
8 (5.2) 121 (79.1) 24 (15.7)
Sputum AFB smear status Positive Negative (reference) Not performed
38 (58.5) 27 (41.5) 0
32 (62.7) 18 (35.3) 1 (2.0)
345 (76.8) 97 (21.6) 7 (1.6)
103 (67.3) 45 (29.4) 5 (3.3)
0.23
Cavity seen on chest radiograph Yes No (reference) Unknown/missing
14 (21.5) 49 (75.4) 2 (3.1)
12 (23.5) 38 (74.5) 1 (2.0)
201 (44.8) 242 (53.9) 6 (1.3)
59 (38.6) 90 (58.8) 4 (2.6)
0.78
0.73
,0.01 0.02 0.01 0.15 0.28 0.41 0.58
0.10
0.38
HIV ¼ human immunodeficiency virus; AFB ¼ acid-fast bacilli.
cases aged 2544 years, the population at greatest risk for infection during the early years of the epidemic.12,17 However, persons from that era are now aging, older persons may be newly infected, and adolescents and young adults may also be exposed. Of note, TB patients in Alberta, Canada, who are middle aged were recently shown to have a significantly higher HIV infection rate than those in younger age groups.15 Nearly half of our participants with newly identified HIV infection were aged ,25 or .44 years. Further efforts to raise awareness among
physicians and other clinical staff about the importance of HIV testing for TB patients of all ages may well lead to further increases in HIV test offering and acceptance. HIV testing rates in the United States and Canada remain poor among contacts,6,11,13,18 despite recommendations in both countries to universally test TB contacts.8–10 In a 2003 New York City intervention to improve HIV testing, only 29% of contacts with unknown status were tested.14 In our study, 75% of contacts were offered testing, but only 39%
HIV testing in TB contact investigations
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Table 2 Characteristics of 4152 TB contacts who were offered/not offered HIV testing, and who accepted/did not accept HIV testing at the nine participating Tuberculosis Epidemiologic Studies Consortium Sites, 2002–2006 Offered testing
Contact characteristics
Yes (n ¼ 3099) n (%)
No (n ¼ 1053) n (%)
Age groups, years 0–5 6–14 15–24 (reference) 25–44 45–64 765 Unknown/missing
255 264 642 1117 656 157 8
165 121 134 278 227 42 86
Sex Male (reference) Female Unknown/missing Race/ethnicity Hispanic Non-Hispanic White (reference) Non-Hispanic Black American Indian/Alaskan Native Asian Other Unknown/missing Birthplace US/Canada (reference) Foreign born Unknown/missing Smoking past 6 months Yes No (reference) Unknown/missing
(8.2) (8.5) (20.7) (36.0) (21.2) (5.1) (0.3)
Accepted testing
P value
Yes (n ¼ 1202) n (%)
(15.7) (11.5) (12.7) (26.4) (21.6) (4.0) (8.2)
0.13 ,0.01 0.21 ,0.01
42 53 287 459 312 48 1
1581 (51.0) 1517 (49.0) 1 (0.0)
541 (51.4) 491 (46.6) 21 (2.0)
0.44 ,0.01
655 (54.5) 547 (45.5) 0
880 318 1556 119 215 7 4
144 159 529 26 46 3 146
(28.4) (10.3) (50.2) (3.8) (6.9) (0.2) (0.1)
,0.01 ,0.01
(13.7) (15.1) (50.2) (2.5) (4.4) (0.3) (13.9)
,0.01 ,0.01 ,0.01 0.82 ,0.01
247 179 540 111 119 4 2
1946 (62.8) 1145 (36.9) 8 (0.3)
778 (73.9) 100 (9.5) 175 (16.6)
,0.01 ,0.01
782 (25.2) 2244 (72.4) 73 (2.4)
116 (11.0) 477 (45.3) 460 (43.7)
,0.01
,0.01 ,0.01
(3.5) (4.4) (23.9) (38.2) (26.0) (4.0) (0.1)
(20.5) (14.9) (44.9) (9.2) (9.9) (0.3) (0.2)
480 (39.9) 684 (56.9) 38 (3.2)
302 (15.9) 1560 (82.2) 35 (1.8)
,0.01
53 (4.4) 1111 (92.4) 38 (3.2)
16 (0.8) 1846 (97.3) 35 (1.8)
,0.01
86 (4.5) 1774 (93.5) 37 (2.0)
,0.01 ,0.01 ,0.01
1492 244 123 38
,0.01 ,0.01 ,0.01
,0.01
231 (19.2) 933 (77.6) 38 (3.2)
Alcohol use None (reference) Mild Heavy Unknown/missing
2170 540 312 77
459 87 44 463
0.03 0.02 ,0.01
678 296 189 39
Diabetes Yes No (reference) Unknown/missing
146 (4.7) 2896 (93.4) 57 (1.8)
48 (4.6) 717 (68.1) 288 (27.4)
Index case’s sputum smear status Positive Negative (reference) Not done
2528 (81.6) 535 (17.3) 36 (1.2)
899 (85.4) 145 (13.8) 9 (0.9)
0.01
Index case cavitary Yes No (reference) Unknown/missing
1365 (44.0) 1684 (54.3) 50 (1.6)
447 (42.5) 582 (55.3) 24 (2.3)
0.46
Index case’s HIV status Positive Negative (reference) Unknown
473 (15.3) 1950 (62.9) 676 (21.8)
102 (9.7) 754 (71.6) 197 (18.7)
,0.01
Contact preliminary diagnosis Active TB TST convertor TST-positive TST-negative (reference) No post-exposure screen Not screened
139 168 1176 1120 451 45
37 29 178 411 178 220
0.10 ,0.01 ,0.01
(4.5) (5.4) (37.9) (36.1) (14.6) (1.5)
(3.5) (2.8) (16.9) (39.0) (16.9) (20.9)
0.10 ,0.01
0.41
0.16
0.03
0.49 ,0.01
,0.01 NA
,0.01 0.32
45 (4.3) 543 (51.6) 465 (44.2) (43.6) (8.3) (4.2) (44.0)
926 (48.8) 970 (51.1) 1 (0.1)
1119 (59.0) 772 (40.7) 6 (0.3)
317 (10.2) 2707 (87.4) 75 (2.4) (70.0) (17.4) (10.1) (2.5)
0.14 0.30 ,0.01 0.07
(56.4) (24.6) (15.7) (3.2)
633 139 1016 8 96 3 2
,0.01 ,0.01
827 (68.8) 373 (31.0) 2 (0.2)
14 (1.3) 576 (54.7) 463 (44.0)
0.04
(11.2) (11.1) (18.7) (34.7) (18.1) (5.7) (5.7)
,0.01 ,0.01 0.83 0.96 0.80
69 (2.2) 2957 (95.4) 73 (2.4)
,0.01
213 211 355 658 344 109 7
P value
(33.4) (7.3) (53.6) (0.4) (5.1) (0.2) (0.1)
Injection drug use Yes No (reference) Unknown/missing ‘Street drug’ use Yes No (reference) Unknown/missing
0.89
No (n ¼ 1897) n (%)
(78.7) (12.9) (6.5) (2.0)
,0.01
0.12
0.03
74 (6.2) 1096 (91.2) 32 (2.7)
72 (3.8) 1800 (94.9) 25 (1.3)
,0.01
965 (80.3) 228 (19.0) 9 (0.7)
1563 (82.4) 307 (16.2) 27 (1.4)
0.06
532 (44.3) 652 (54.2) 18 (1.5)
833 (43.9) 1032 (54.4) 32 (1.7)
0.88
160 (13.3) 818 (68.1) 224 (18.6)
313 (16.5) 1132 (59.7) 452 (23.8)
95 79 458 393 149 28
(7.9) (6.6) (38.1) (32.7) (12.4) (2.3)
44 89 718 727 302 17
(2.3) (4.7) (37.8) (38.3) (15.9) (0.9)
0.49
0.09
0.04 ,0.01 ,0.01 ,0.01 0.05 0.06 0.44 ,0.01
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Table 2
(continued) Offered testing
Contact characteristics
Yes (n ¼ 3099) n (%)
No (n ¼ 1053) n (%)
Environment for exposure Household (reference) Non-household/social School Workplace
2072 560 74 393
559 197 66 231
(66.9) (18.1) (2.4) (12.7)
(53.1) (18.7) (6.3) (21.9)
Accepted testing
P value
Yes (n ¼ 1202) n (%)
No (n ¼ 1897) n (%)
,0.01 ,0.01 ,0.01
802 240 36 124
1270 320 38 269
(66.7) (20.0) (3.0) (10.3)
(66.9) (16.9) (2.0) (14.2)
P value
0.07 0.08 0.01
TB ¼ tuberculosis; HIV ¼ human immunodeficiency virus; NA ¼ not available; TST ¼ tuberculin skin test.
of contacts agreed to be tested, resulting in a testing rate of 26%, similar to the New York study. Although clinic and research workers were strongly encouraged by a structured intervention, 25% of contacts in our study were not offered testing. Similar to our findings among TB patients, very young and older contacts were offered HIV testing less frequently than other age groups, and when offered testing, they often refused. These findings point to the need for further efforts to raise awareness among public health staff of the importance of HIV testing among exposed contacts of all ages. Previously identified negative influencing factors for accepting HIV testing among contacts have included self-perception of low risk, younger or older age, foreign birth, and poor testing environment, whereas positive factors have included homelessness, substance use, and recent history of TST positivity.6,13,14,18 Our study also identified being Black or Hispanic and lack of an optimal testing environment as important risk factors for not accepting HIV testing. Based on these findings, health departments are encouraged to take the necessary steps to ensure that a good testing Table 3 testing
environment is available and utilized for offering HIV testing. Additional time and effort may also be required to counsel contacts who may perceive themselves to be at low risk or be otherwise reluctant to accept HIV testing, with particular focus on Blacks and Hispanics. The HIV co-infection rate among TB patients in our study was somewhat higher than the annual national HIV co-infection rates in the United States, coinciding with the study enrollment time period (21% of TB patients in our study vs. 12–17% of all US TB patients17), but lower than rates reported in a US study that enrolled patients in 1996, in which 27% of 224 TB patients were co-infected.6 All three studies underscore the continued importance of HIV as a co-factor for TB disease, and the need to routinely test all TB patients for HIV. The HIV infection rate among contacts in our study, at 6%, was somewhat lower than among contacts in a 1996 US study (9% of 220 contacts).6 Nevertheless, HIV rates among contacts in both studies were considerably higher than the estimated seroprevalence in the general US population (0.5%), highlighting the importance of considering contacts
Multivariable analysis of TB contacts who were offered/not offered HIV testing, and who accepted/did not accept HIV Offered testing
Contact characteristics Age 15–64 years American Indian/Alaskan native Asian Hispanic Non-Hispanic Black Other race Foreign-born Smoking in past 6 months ‘Street drug’ use Any alcohol use Diabetes Steroids Index case HIV-negative Positive TB screening Household contact
Accepted testing
b
aOR
95%CI
b
aOR
95%CI
0.8878 1.8323 0.3245 0.4948 0.4343 1.5168 1.4391 0.3083 0.0220 NA NA NA 0.7145 0.3219 0.5247
2.43* 6.25* 0.72 1.64* 1.54* 0.22 4.22* 1.36* 1.02
1.96–3.02 3.20–12.20 0.45–1.18 1.17–2.31 1.19–2.00 0.05–1.06 3.05–5.82 1.05–1.77 0.71–1.48
0.49* 1.38* 1.69*
0.37–0.65 1.11–1.71 1.40–2.04
1.0103 2.7429 0.5291 0.6819 0.7868 0.8146 0.6435 0.5400 0.6394 0.4263 0.4781 0.6629 0.4640 0.4261 NA
2.75* 15.53* 1.70* 0.51* 0.46* 2.26 0.53* 1.72* 1.90* 1.53* 3.29* 1.94 1.47* 1.67*
2.15–3.51 6.98–34.59 1.13–2.56 0.37–0.70 0.35–0.60 0.48–10.61 0.41–0.68 1.38–2.14 1.39–2.58 1.25–1.88 1.08–9.99 0.93–4.04 1.14–1.88 1.37–2.03
* Statistically significant. TB ¼ tuberculosis; HIV ¼ human immunodeficiency virus; aOR ¼ adjusted odds ratio; CI ¼ confidence interval; NA ¼ not applicable.
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HIV testing in TB contact investigations
Table 4 Reasons for staff not offering and contacts not accepting HIV testing, by country of origin, at the nine participating Tuberculosis Epidemiologic Studies Consortium Sites, 2002–2006 Total n (%)
Foreign-born contacts n (%)
US-born contacts n (%)
Reason HIV testing not offered Environment not appropriate Child aged ,15 years No interviewer time Interviewer not trained for testing and counseling (reference) Interviewer forgot/no equipment available Prior HIV-positive, not eligible Prior HIV-negative, tested in past 6 weeks Other Unknown
(n ¼ 1053) 311 (29.5) 162 (15.4) 9 (0.9) 44 (4.2) 0 (0.0) 0 (0.0) 1 (0.1) 247 (23.5) 279 (26.5)
(n ¼ 275) 19 (6.9) 5 (1.8) 5 (1.8) 13 (4.7) 0 (0.0) 0 (0.0) 1 (0.4) 127 (46.2) 105 (38.2)
(n ¼ 778) 292 (37.5) 157 (20.2) 4 (0.5) 31 (4.0) 0 (0.0) 0 (0.0) 0 (0.0) 120 (15.4) 174 (22.4)
Reason HIV testing not accepted Child aged ,15 years Don’t want to know result Recently tested (,6 weeks previously) Recently tested (.6 weeks previously) HIV test pending (reference) Not believed to be at risk Other reason Unknown
(n ¼ 1897) 197 (10.4) 25 (1.3) 529 (27.9) 1 (0.1) 30 (1.6) 1 (0.1) 307 (16.2) 807 (42.5)
(n ¼ 1119) 179 (16.0) 20 (1.8) 230 (20.6) 0 (0.0) 19 (1.7) 0 (0.0) 193 (17.2) 478 (42.7)
(n ¼ 778) 18 (2.3) 5 (0.6) 299 (38.4) 1 (0.1) 11 (1.4) 1 (0.1) 114 (14.7) 329 (42.3)
P value ,0.01 ,0.01 0.13 NA NA NA ,0.01 ,0.01 ,0.01 0.18 0.03 NA NA 0.96 0.65
HIV ¼ human immunodeficiency virus; NA ¼ not applicable.
of TB patients as a high-risk group for HIV infection.19 Most previous studies have not distinguished between overall and newly diagnosed HIV infection. In our study, we identified 51 patients and 24 contacts with previously undiagnosed HIV infection, representing prevalence rates for newly diagnosed HIV infection among TB patients and contacts of respectively 10% and 2%. The proportion of TB patients with newly diagnosed HIV infection in our study is higher than reported among TB patients in Alberta, Canada (5% in 2003–2005 and 8% in 2007–2008),15 but similar to that of a 2000 UK study, in which 11% of TB patients had newly diagnosed HIV infection. 11 The proportion of contacts with newly identified HIV infection in our study was slightly lower than that reported in the UK study (5%).11 These findings underscore the value of universal HIV testing of TB patients and exposed contacts for diagnosing and treating previously unrecognized HIV infections in these high-risk groups. HIV infection rates were similar for foreign and US/Canada-born TB patients, while US/Canadaborn contacts were more than five times as likely to be infected as foreign-born contacts. One possible explanation is that before January 2010, HIV-infected immigrants and visitors were banned from entering the United States without special waivers.20 Nevertheless, health care and study staff offered testing more frequently to foreign-born contacts. To change this practice, we need to understand why US/Canada-born contacts were offered testing less often but were far more likely to be HIV-infected. Among foreign-born contacts,
lack of privacy in workplace investigations and young age appear to have affected offering rates. Fear of deportation cannot be excluded as a possible additional reason for some refusals among foreignborn persons. These findings identify the need for further emphasis among clinical care providers and public health professionals to offer HIV testing to all TB patients, regardless of national origin, and highlight the need for greater efforts to ensure privacy in workplace settings as well as confidentiality of test results. The Canadian government recommends universal HIV screening for TB patients, and HIV risk assessment-based testing of contacts.9 In the United States, TB patients are asked about substance use, but contacts are generally not asked about the same HIV risk factors.6 We found that even when participants were aware of increased HIV risk, one in four contacts who reported drug use and nearly half of those who were heavy alcohol users declined testing when offered. This represents an opportunity to improve testing rates among a key subpopulation at high risk for HIV. Our study revealed that having diabetes had a positive influence on HIV testing rates, which may be the result of the more frequent and comprehensive clinical care among persons with underlying illnesses. These findings emphasize the potential importance of involving clinical care providers in efforts to offer and explain the importance of HIV testing. Among the factors that influenced offering and accepting testing was having active TB or LTBI. Health care workers may have educated contacts about the importance of knowing their HIV status before initiating TB or LTBI treatment.
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The International Journal of Tuberculosis and Lung Disease
Table 5 Characteristics of 4586 contacts of culture-positive pulmonary TB cases* by HIV test status at the nine participating Tuberculosis Epidemiologic Studies Consortium Sites, 2002–2006 HIV status
Case characteristics Age groups, years 10–14 (reference) 15–24 25–44 45–64 765 Unknown/missing Sex Male (reference) Female Unknown/missing
Prior HIVþ (n ¼ 47) n (%) 5 3 18 20 1
New HIVþ (n ¼ 24) n (%)
New HIV (n ¼ 1137) n (%)
(10.6) (6.4) (38.3) (42.6) (2.1) 0
0 2 (8.3) 10 (41.7) 12 (50.0) 0 0
95 272 430 291 48 1
25 (53.2) 22 (46.8) 0
18 (75.0) 6 (25.0) 0
Race/ethnicity Hispanic Non-Hispanic White (reference) Non-Hispanic Black American Indian/Alaskan Native Asian Other Unknown/missing Birthplace US/Canada (reference) Foreign-born Unknown/missing
0 2 (4.3) 42 (89.4) 2 (4.3) 0 0 1 (2.1)
1 3 17 3
43 (91.5) 3 (6.4) 1 (2.1)
22 (91.7) 2 (8.3) 0
Smoking in past 6 months Yes No (reference) Unknown/missing
22 (46.8) 21 (44.7) 4 (8.5)
Injection drug use Yes No (reference) Unknown/missing
(23.6) (16.6) (30.9) (19.3) (5.2) (4.4)
,0.01 ,0.01 ,0.01 ,0.01 ,0.01
611 (53.7) 526 (46.3) 0
1699 (50.3) 1649 (48.8) 30 (0.9)
0.04 NA
236 166 507 108 115 3 2
847 381 1707 34 183 7 219
0.05 ,0.01 0.03 0.95 ,0.01
780 (68.6) 355 (31.2) 2 (0.2)
2131 (63.1) 992 (29.4) 255 (7.5)
0.23 ,0.01
8 (33.3) 14 (58.3) 2 (8.3)
459 (40.4) 643 (56.6) 35 (3.1)
437 (12.9) 2082 (61.6) 859 (25.4)
9 (19.1 ) 34 (72.3) 4 (8.5)
1 (4.2) 21 (87.5) 2 (8.3)
50 (4.4) 1052 (92.5) 35 (3.1)
33 (1.0) 2483 (73.5) 862 (25.5)
Non-injection drug use Yes No (reference) Unknown/missing
18 (38.3) 25 (53.2) 4 (8.5)
4 (16.7) 18 (75.0) 2 (8.3)
219 (19.3) 883 (77.7) 35 (3.1)
143 (4.2) 2369 (70.1) 866 (25.6)
Alcohol consumption Heavy None or mild (reference) Unknown/missing
6 (12.8) 37 (78.7) 4 (8.5)
7 (29.2) 15 (62.5) 2 (8.3)
173 (15.2) 928 (81.6) 36 (3.2)
178 (5.3) 2335 (69.1) 865 (25.6)
,0.01
Diabetes Yes No (reference) Unknown/missing
2 (4.3) 41 (87.2) 4 (8.5)
1 (4.2) 21 (87.5) 2 (8.3)
73 (6.4) 1035 (91.0) 29 (2.6)
121 (3.6) 2574 (76.2) 683 (20.2)
,0.01
Index case’s sputum smear status Positive Negative (reference) Not done
34 (72.3) 12 (25.5) 1 (2.1)
19 (79.2) 5 (20.8) 0
912 (80.2) 216 (19.0) 9 (0.8)
2825 (83.6) 504 (14.9) 49 (1.5)
,0.01
Index case cavitary Yes No (reference) Unknown/missing
19 (40.4) 28 (59.6) 0
7 (29.2) 17 (70.8) 0
512 (45.0) 607 (53.4) 18 (1.6)
1460 (43.2) 1861 (55.1) 57 (1.7)
0.46
HIV status of index cases Prior or new positive New negative (reference) Unknown
28 (59.6) 14 (29.8) 5 (10.6)
15 (62.5) 8 (33.3) 1 (4.2)
141 (12.4) 784 (69.0) 212 (18.6)
715 (21.2) 2181 (64.6) 739 (21.9)
0.27
Contact’s preliminary diagnosis Active TB TST convertor TST-positive TST-negative (reference) No post-exposure screen Not screened
13 (27.7) 0 7 (14.9 ) 19 (40.4) 6 (12.8) 2 (4.3)
90 78 437 374 132 26
83 121 981 1261 573 359
(16.7) (4.2) (4.2) (33.3) (37.5) (4.2)
(20.8) (14.6) (44.6) (9.5) (10.1) (0.3) (0.2)
797 562 1044 652 174 149
Unknown vs. known HIV status P value
(25.1) (11.3) (50.5) (1.0) (5.4) (0.2) (6.5)
4 1 1 8 9 1
(4.2) (12.5) (70.8) (12.5) 0 0 0
(8.40) (23.9) (37.8) (25.6) (4.2) (0.1)
Unknown HIV status (n ¼ 3378) n (%)
(7.9) (6.9) (38.4) (32.9) (11.6) (2.3)
(2.5) (3.6) (29.0) (37.3) (17.0) (10.6)
,0.01
,0.01 ,0.01 ,0.01 ,0.01 ,0.01 ,0.01
,0.01
,0.01
0.02
0.70
0.01 ,0.01 ,0.01 ,0.01 0.05 ,0.01
HIV testing in TB contact investigations
Table 5
951
(continued) HIV status
Case characteristics
Prior HIVþ (n ¼ 47) n (%)
New HIVþ (n ¼ 24) n (%)
Exposure environment Household (reference) Non-household/social School Workplace
36 (87.8) 8 (19.5) 0 3 (7.3)
14 (58.3) 10 (41.9) 0 0
New HIV (n ¼ 1137) n (%) 761 222 33 121
(66.9) (19.5) (2.9) (10.6)
Unknown HIV status (n ¼ 3378) n (%) 2043 624 111 600
(60.5) (18.5) (3.3) (17.8)
Unknown vs. known HIV status P value
0.71 0.15 ,0.01
* 41 offered HIV testing, accepted, no result available. TB ¼ tuberculosis; HIV ¼ human immunodeficiency virus; NA ¼ not applicable; TST ¼ tuberculin skin test.
In the 1996 US study, contacts whose index patients had known HIV status were more than twice as likely to be tested for HIV.6 Furthermore, the same US study and a Brazilian study demonstrated that contacts of HIV-infected TB patients are more likely to be infected themselves.6,21 In our study, contacts of HIV-infected TB patients were more likely to be offered testing, but were less likely to accept. Among those tested, nearly 25% were also infected. It is worrying that most contacts in this very high-risk group were never tested. Based on our findings, further efforts are needed to promote acceptance of testing among contacts of HIV-infected TB patients. Options to consider include modifying the message delivered at the time of offering testing to increase the knowledge base for and awareness of infection and the benefits of testing among high-risk groups. Dart et al. found that TB out-patients were less likely than hospitalized patients to be offered HIV testing (49% vs. 74%); reasons given for not offering testing were lack of TB nurses, being outside the TB service, and lack of appropriate space.13 Nearly half of hospitalized TB patients declined HIV testing because they were unable to cope with a dual diagnosis. 13 In our study, workplace contacts were far less likely to be tested than household contacts. The main reason given for not offering HIV testing among contacts was lack of privacy. Facility-based contact investigations are often carried out en masse, and contact screening is performed in open rooms with little to no privacy. Safeguarding privacy in these settings may be a low priority for busy, short-staffed TB program workers. Creation of a private testing environment may therefore be an important measure for increasing testing among workplace contacts. Attempts to increase HIV testing have included staff training and support systems,13 and changes in policy supported by pamphlets and education for staff,14 but the results have been disappointing. Our intervention encouraged offering HIV counseling and testing, and included interim monitoring and
promotion by principal investigators. Nonetheless, HIV testing among contacts was poor overall, and only slightly better than program testing with no intervention. To improve the offer of HIV testing, creative approaches to providing a private testing environment should be explored. Better communication between TB clinics and health departments to identify the HIV status of TB contacts is critical. Placing the responsibility of contact testing on TB clinics may be a way to solve this problem, particularly in this time of shrinking health budgets. Oral HIV tests do not require staff to have phlebotomy skills and avoid refusals by patients due to fear of needles. Furthermore, an ‘opt-out’ approach to HIV testing, as has been adopted in some US and Canadian TB clinics, emergency rooms, and other health care settings,15,22 and now promoted also by the CDC,23,24 could minimize the influence of a major barrier, i.e., perceived risk. This approach encourages acceptance,25 and has improved HIV testing rates among US and Canadian TB patients by as much as 45%,15,22,26 as well as increasing the proportion of patients with newly identified HIV co-infection among South African TB patients by three-fold.27 Both opt-out testing and use of oral testing can facilitate screening in the clinic and in the field. Limitations to our study include missing substance use status for some participants, less than universal offering of HIV testing, less than universal acceptance of HIV testing, inability to distinguish with certainty what HIV test offering and acceptance rates would have been without a specific study intervention aimed at strengthening these program components, and no information on the language skills or demographic characteristics of the interviewers. Strengths of our study include the inclusion of multiple sites, making the study more generalizable to the US/Canadian population; determining HIV offering and testing rates; and collection of good epidemiologic data to identify risk factors for not offering and not accepting HIV testing.
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The International Journal of Tuberculosis and Lung Disease
CONCLUSION Screening and treatment for HIV is urgent in TB patients, for whom treatment regimens may need to be altered, and in contacts who, if HIV-infected, are far more likely to progress to TB disease. In our large, multisite study, HIV testing identified previously unknown infection in 10% of TB patients and 2% of contacts. High proportions of TB patients were offered and accepted HIV testing. Despite structured study procedures to offer HIV testing as part of contact investigations, low acceptance rates resulted in poor testing rates. Offering and acceptance of HIV testing were closely tied to risk perceptions among health care workers and patients. Further strategies are needed to improve HIV testing acceptance rates, especially among US/Canada-born persons and those who may not perceive themselves to be at risk. Promotion of an opt-out strategy within TB control programs might increase HIV testing rates in TB patients and contacts. Acknowledgements The authors thank L Bozeman, J Elder, D Garrett, R Horsburgh, T Navin, and A Vernon for helpful guidance and input into scientific, data management, and administrative aspects of the project, and special thanks to P Bessler for her excellent contribution to the multivariable analysis. The Tuberculosis Epidemiological Studies Consortium Task Order 2 Team: 1) TBESC Task Order 2 study sites, investigators, and study coordinators: Arkansas Department of Health, Little Rock, AR, USA (I Bakhtawar, C LeDoux); Respiratory Health Association of Metropolitan Chicago and Rush University Chicago, IL, USA (J McAuley, J Beison); University of British Columbia, Cancouver, BC, Canada (M FitzGerald, M Naus, M Nakajima); Columbia University, New York, NY, USA (N Schluger, Y Hirsch-Moverman, J Moran); Emory University, Atlanta, GA, USA (H Blumberg, J Tapia, L Singha); University of Manitoba, Winnipeg, MB, Canada (E Hershfeld, B Roche); New Jersey Medical School National Tuberculosis Center, Newark, NJ, USA (B Mangura, A Sevilla); Vanderbilt University and Tennessee Department of Health, Nashville, TN, USA (T Sterling, T Chavez-Lindell, F Maruri); Maryland Department of Health, Balitimore, MD, USA (S Dorman, W Cronin, E. Munk). 2) CDC Task Order 2 Data management team: B Chen, P Bessler, Y Yuan, F Yan, Y Shen, H Zhao, H Zhang, M Fagley, M Reichler. 3) Task Order 2 Protocol Team: M Reichler (Chair), T Sterling (Co-chair), J Tapia, C Hirsch, C Luo. This work was supported by the Centers for Disease Control and Prevention through funding to the Tuberculosis Epidemiologic Studies Consortium (TBESC). Conflicts of interest: none declared. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention or supporting agencies.
References 1 World Health Organization. Global tuberculosis control: WHO report 2011. WHO/HTM/TB/2011.16. Geneva, Switzerland: WHO; 2011: http://www.who.int/tb/publications/global_ report/2011/gtbr11_full.pdf. Accessed April 2015.
2 Centers for Disease Control and Prevention. Trends in tuberculosis – United States, 2011. MMWR Morb Mortal Wkly Rep 2012; 61: 181–185. 3 American Thoracic Society, Center for Disease Control and Prevention, Infectious Diseases Society of America: controlling tuberculosis in the United States. Am J Respir Crit Care Med 2005; 172: 1169–1227. 4 Selwyn P A, Sckell B M, Alcabes P, Friedland G H, Klein R S, Schoenbaum E E. High risk of active tuberculosis in HIV-infected drug users with cutaneous anergy. JAMA 1992; 268: 504–509. 5 Sauzullo I, Mengoni F, Scrivo R, et al. Evaluation of QuantiFERON-TB Gold In-Tube in human immunodeficiency virus infection and in patient candidates for anti-tumour necrosis factor-alpha treatment. Int J Tuberc Lung Dis 2010; 14: 834–840. 6 Reichler M R, Bur S, Reves R, et al. Results of testing for human immunodeficiency virus infection among recent contacts of infectious tuberculosis cases in the United States. Int J Tuberc Lung Dis 2003; 7 (Suppl 3): S471–S478. 7 Centers for Disease Control and Prevention. Tuberculosis provisional data—United States, 1986. MMWR Morb Mortal Wkly Rep 1987; 36: 254–255. 8 Centers for Disease Control and Prevention. Revised guidelines for HIV counseling, testing, and referral. MMWR Morb Mortal Wkly Rep 2001; 50 (RR-19): 1–58. 9 Canada Tuberculosis Committee. Recommendations for the screening and prevention of tuberculosis in patients with HIV and the screening for HIV in tuberculosis patients and their contacts. Can Commun Dis Rep 2002; 28: 1–6. 10 Centers for Disease Control and Prevention. Guidelines for the investigation of contacts of persons with infectious tuberculosis: recommendation from the national Tuberculosis Controllers Association and CDC. MMWR Morb Mortal Wkly Rep 2005; 54 (RR-15): 1–47. 11 Bowen E F, Rice P S, Cooke N T, Whitfield R J, Rayner C F. HIV seroprevalence by anonymous testing in patients with Mycobacterium tuberculosis and in tuberculosis contacts. Lancet 2000; 356: 1488–1489. 12 Centers for Disease Control and Prevention. Reported tuberculosis in the United States, 2011. Atlanta, GA, USA: US Department of Health and Human Services, CDC, 2012. 13 Dart S, Alder D, Mamdani M, et al. HIV testing in TB clinics: a problem in practice? Thorax 2006; 61: 271–272. 14 Li J, Marks S M, Driver C R, et al. Human immunodeficiency virus counseling, testing, and referral of close contacts to patients with pulmonary tuberculosis: feasibility and costs. J Public Health Manag Pract 2007; 13: 252–262. 15 Long R, Boffa J. High HIV-TB co-infection rates in marginalized populations: evidence from Alberta in support of screening TB patients for HIV. Can J Public Health 2010; 101: 202–204. 16 Marks S M, Taylor Z, Qualls N L, Shrestha-Kuwahara R J, Wilce M A, Nguyen C H. Outcomes of contact investigations of infectious tuberculosis patients. Am J Respir Crit Care Med 2000; 162: 2033–2038. 17 Centers for Disease Control and Prevention. Reported tuberculosis in the United States, 2006. Atlanta, GA, USA: US Department of Health and Human Services, CDC, 2007. 18 Rodger A J, Story A, Fox Z, Hayward A. HIV prevalence and testing practices among tuberculosis cases in London: a missed opportunity for HIV diagnosis? Thorax 2010; 65: 63–69. 19 McQuillan G M, Kruszon-Moran D, Granade T, Feldman J W. Seroprevalence of HIV in the US household population aged 18–49 years: the National Health and Nutrition Examination Surveys, 1999–2006. J Acquir Immune Defic Syndr 2010; 53: 117–123. 20 US Citizenship and Immigration Services. Public Law 110-293, 42 CFR 34.2 (b) and Inadmissibility Due to Human Immunodeficiency Virus (HIV) Infection. Washington DC, USA: USCIS, 2009. http://d.yimg.com/kq/groups/4317947/ 1952933142/name/11.24.09%20USCIS%20Memorandum %20 on %20HI V%20 In ad mis si bi li t y%20a nd %20F in a Accessed May 2015.
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21 Carvalho A C, DeRiemer K, Nunes Z B, et al. Transmission of Mycobacterium tuberculosis to contacts of HIV-infected tuberculosis patients. Am J Respir Crit Care Med 2001; 164: 2166–2171. 22 Gardner A, Naureckas C, Beckwith C, Losikoff P, Martin C, Carter E J. Experiences in implementation of routine human immunodeficiency virus testing in a US tuberculosis clinic. Int J Tuberc Lung Dis 2012; 16: 1241–1246. 23 Centers for Disease Control and Prevention. Integrated prevention services for hiv infection, viral hepatitis, sexually transmitted diseases, and tuberculosis for persons who use drugs illicitly: summary guidance from CDC and the US Department of Health and Human Services. MMWR Morb Mortal Wkly Rep 2012; 61 (RR05): 1–40.
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24 Centers for Disease Control and Prevention Fact Sheet. Recommendations for human immunodeficiency virus (HIV) screening in tuberculosis (TB) clinics. Atlanta, GA, USA: CDC, 2012. 25 World Health Organization. Guidance on provider-initated HIV testing and counselling in health facilities. Geneva, Switzerland: WHO, 2007. http://whqlibdoc.who.int/publications/2007/ 9789241595568_eng.pdf. Accessed April 2015. 26 Sturtevant D, Preiksaitis J, Singh A, et al. The feasibility of using an ’opt-out’ approach to achieve universal HIV testing of tuberculosis patients in Alberta. Can J Public Health 2009; 100: 116–120. 27 Pope D S, Deluca A N, Kali P, et al. A cluster-randomized trial of provider-initiated (opt-out) HIV counseling and testing of tuberculosis patients in South Africa. J Acquir Immune Defic Syndr 2008; 48: 190–195.
HIV testing in TB contact investigations
i
RESUME
D´eterminer le statut par rapport au virus de l’immunod´eficience humaine (VIH) des patients avec un diagnostic de la tuberculose (TB) et de leurs contacts est important. Cependant, en de´ pit des directives existantes, tous les patients ne sont pas test´es et encore beaucoup moins, leurs contacts. M E´ T H O D E : Dans une e´ tude r´ealis´ee dans neuf sites aux Etats-Unis et au Canada, nous avons introduit des proc´edures formelles visant a` offrir le test VIH aux patients TB et a` leurs contacts. Les donn´ees ont e´ t´e recueillies a` travers des entretiens et une revue des dossiers me´ dicaux. On a alors examine´ les caract´eristiques associ´ees avec l’offre et l’acceptation du test VIH. R E´ S U LT A T S : Sur 651 patients TB, 601 (92%) se sont vus offrir le test, 511 (85%) l’ont accept´e et 51 (10%) e´ taient infect´es par le VIH. Sur 4152 contacts, 3099 (75%) se sont vus offrir le test, 1202 (39%) l’ont accept´e CONTEXTE :
et 24 (2%) e´ taient infect´es par le VIH. Les contacts ag´ ˆ es de 15 a` 64 ans, non blancs, n´es a` l’´etranger, fumeurs, ceux qui avaient eu un d´epistage positif de TB et les contacts domestiques avaient davantage de chances de se voir proposer le test ; les contacts expos´es a` des patients VIH n´egatifs avaient moins de chances de se voir proposer le test. Les contacts ag´ ˆ es de 15 a` 64 ans, fumeurs, consommateurs de drogues/d’alcool, diab´etiques et ceux dont le d´epistage TB e´ tait positif ont plus souvent accept´e le test. Les contacts n´es a` l’´etranger, noirs, hispaniques et expos´es a` des patients VIH positifs ont moins souvent accept´e le test. C O N C L U S I O N S : Des taux e´ lev´es d’infections a` VIH ont e´ t´e d´etect´es parmi les patients et les contacts. En d´epit de proc´edures structur´ees d’offre du test VIH, une partie des patients et la majorit´e des contacts n’ont pas accept´e le test. Il est n´ecessaire d’´elaborer des strat´egies nouvelles pour am´eliorer l’acceptation du test. RESUMEN
Es importante determinar la situacion ´ frente al virus de la inmunodeficiencia humana (VIH) de los pacientes con diagnostico ´ de tuberculosis (TB) y sus contactos. Pese a las directrices existentes, las pruebas diagnosticas ´ no se practican a todos los pacientes y rara vez se investigan los contactos. M E´ T O D O S: En un estudio de nueve centros en ciudades del Canada´ y los Estados Unidos se introdujeron procedimientos estructurados, encaminados a ofrecer la prueba diagnostica ´ del VIH a los pacientes con TB y a los contactos. Los datos se recogieron mediante entrevistas y ana´lisis de las historias cl´ınicas y se examinaron las caracter´ısticas asociadas con el ofrecimiento y la aceptaci on ´ de las pruebas diagnosticas ´ del VIH. R E S U LT A D O S: De los 651 pacientes con diagnostico ´ de TB, se ofrecio´ la prueba del VIH a 601 (92%), 511 pacientes la aceptaron (85%) y 51 obtuvieron un resultado positivo (10%). Se propuso la prueba del VIH a 3099 de los 4152 contactos (75%), 1202 la aceptaron (39%) y se obtuvieron 24 resultados positivos (2%). Fue ma´s probable que se ofreciese la prueba M A R C O D E R E F E R E N C I A:
diagnostica ´ del VIH a los contactos de edad de 15–64 anos, de una etnia diferente de la blanca, nacidos en el ˜ extranjero, fumadores, a los contactos con una investigaci on ´ de TB positiva y a los contactos domiciliarios; fue menos frecuente proponer la serolog´ıa del VIH a los contactos expuestos a pacientes con serolog´ıa negativa. Se observ o´ una mayor probabilidad de aceptacion ´ de la prueba del VIH en los contactos de edad de 15–64 anos, fumadores, ˜ consumidores de alcohol o de drogas, en los pacientes diab´eticos y los contactos cuya deteccion ´ sistema´tica de la TB fue positiva. Fue menos probable que aceptaran la serolog´ıa del VIH las personas nacidas en el extranjero, de etnia negra, los hispanoamericanos y los contactos expuestos a pacientes seropositivos. ´ N: Se observaron altas tasas de infeccion CONCLUSIO ´ por el VIH en los pacientes con diagnostico ´ de TB y en sus contactos. Pese a la existencia de mecanismos estructurados de oferta de la prueba diagnostica ´ del VIH, algunos pacientes y la mayor´ıa de los contactos no aceptaron la prueba. Es preciso establecer estrategias que mejoren las tasas de aceptacion. ´
HIV counseling and testing in tuberculosis contact investigations in the United States and Canada Y. Hirsch-Moverman,* W. A. Cronin,† B. Chen,‡ J. A. Moran,* E. Munk,§ M. R. Reichler,‡ and the Tuberculosis Epidemiological Studies Consortium Task Order 2 Team *ICAP, Mailman School of Public Health, Columbia University, New York, New York, †Maryland Department of Health and Mental Hygiene, Baltimore, Maryland, ‡Centers for Disease Control and Prevention, Atlanta, Georgia, § Johns Hopkins University School of Medicine, Baltimore, Maryland, USA SUMMARY B A C K G R O U N D : Determining the human immunodeficiency virus (HIV) status of tuberculosis (TB) patients and contacts is important. Despite existing guidelines, not all patients are tested, and testing of contacts is rarely performed. M E T H O D S : In a study conducted at nine US/Canadian sites, we introduced formal procedures for offering HIV testing to TB patients and contacts. Data were collected via interviews and medical record review. Characteristics associated with offering and accepting HIV testing were examined. R E S U LT S : Of 651 TB patients, 601 (92%) were offered testing, 511 (85%) accepted, and 51 (10%) were HIVinfected. Of 4152 contacts, 3099 (75%) were offered testing, 1202 (39%) accepted, and 24 (2%) were HIVinfected. Contacts aged 15–64 years, non-Whites,
foreign-born persons, smokers, those with positive TB screening, and household contacts were more likely to be offered testing, whereas contacts exposed to HIVnegative patients were less likely to be offered testing. Contacts aged 15–64 years, smokers, drug/alcohol users, diabetics, and those with positive TB screening were more likely to accept testing. Foreign-born persons, Blacks, Hispanics, and contacts exposed to HIV-positive patients were less likely to accept testing. C O N C L U S I O N S : High rates of HIV were detected among patients and contacts. Despite structured procedures to offer HIV testing, some patients and most contacts did not accept testing. Strategies are needed to improve testing acceptance rates. K E Y W O R D S : TB; contact investigation; HIV; HIV testing
TUBERCULOSIS (TB) is epidemic throughout much of the world, and is a leading cause of death among human immunodeficiency virus (HIV) infected persons.1 In the United States, which reports approximately 14 000 TB cases annually, an estimated 8% of patients with a known HIV test result are coinfected.2 Knowledge of HIV status is essential for decision making about anti-tuberculosis treatment.3 In the United States and Canada, contacts exposed to pulmonary TB patients are routinely evaluated for TB disease and latent tuberculous infection (LTBI). Determining the HIV status of contacts is essential, as HIV is a major predictor for progression from LTBI to TB;4 persons with low CD4 counts may be anergic, and be negative on the tuberculin skin test (TST);4 and interferon-gamma release assays for diagnosing TB may be less useful in patients with CD4 counts ,200 cells/mm3.5 Furthermore, HIV prevalence has been reported to be greater among TB contacts than
in the general population.6 The US Centers for Disease Control and Prevention (CDC) recommend LTBI treatment for HIV-infected close contacts of TB cases, regardless of TST status. The CDC has recommended HIV testing for all TB patients since 1987, and for contacts of TB patients since 2001.7,8 The Canadian TB Committee has recommended that contacts of TB patients be tested for HIV since 2002.9 Nevertheless, not all TB patients in the United States and Canada are being tested for HIV, and reports suggest HIV testing may still not be a routine part of contact investigations. In a multisite evaluation of contact investigations in the United States reported in 2002, only 64% of TB patients and 19% of contacts were tested for HIV.6 Our study objectives were 1) to introduce routine offering of HIV testing to both TB patients and contacts in the TB clinic or field setting as an intervention to improve HIV testing rates, 2) to determine clinical and epidemiologic
Correspondence to: Yael Hirsch-Moverman, ICAP, Mailman School of Public Health, Columbia University, 215 West 125th St, Suite A, New York, NY 10027, USA. Tel: (þ1) 646 524 8344. e-mail: [email protected] Mary Reichler, Division of Tuberculosis Elimination, National Center for HIV, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30333, USA. Tel: (þ1) 404 639 5350. e-mail: [email protected] Article submitted 2 September 2014. Final version accepted 1 April 2015.
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The International Journal of Tuberculosis and Lung Disease
characteristics associated with offering and accepting HIV testing among infectious TB patients and their contacts, 3) to explore why health department personnel did not offer testing to all TB patients and contacts, and 4) to determine why some TB patients and contacts did not accept testing.
METHODS Contact investigation We enrolled TB patients and their contacts prospectively from January 2002 to December 2006 at nine (seven US and two Canadian) TB Epidemiologic Studies Consortium (TBESC) sites. All sites included a large urban area, and three also included surrounding rural areas. Eligible participants included TB patients with positive sputum cultures for Mycobacterium tuberculosis and their close contacts, defined as persons sharing airspace for 715 h per week on average, the minimum exposure time established by investigator consensus as constituting extensive exposure. TB patient interview and data collection Dedicated study staff hired by the participating TBESC sites collected demographics, clinical symptoms, smoking, HIV testing history, exposure environments, and persons exposed in each environment using standardized questionnaires. Study staff had translators available at all sites. Medical records and surveillance data were reviewed for information on drug and alcohol use, homelessness, incarceration, sputum smear, lung cavitation, and HIV results. Contact interview and data collection Contacts were interviewed regarding demographics, smoking, HIV history, drug and alcohol use, diabetes, and use of systemic steroids. Medical records were reviewed for TST and HIV test results. HIV testing intervention Study personnel were trained to offer HIV testing to all TB patients and contacts with no documented prior positive or negative test within the preceding 6 weeks according to a written protocol. Results of HIV offering, acceptance, and reasons for not offering and not accepting testing were recorded. Definitions We defined ‘drug use’ as self-reported current use of injectable or non-injectable drugs; ‘heavy alcohol use’ as self-reported 712 beers, 71 bottle of wine, or 71 pint of hard liquor per week; ‘smokers’ as persons who self-reported smoking in the past 6 months; positive TST as induration 75 mm;10 and TST converter as documented negative TST at baseline, but a positive test .10 weeks post-exposure.
Analysis HIV offering, acceptance, infection rates, and characteristics associated with not being offered or not accepting HIV testing were evaluated. Bivariate analyses were performed using the v2 or Fisher’s exact test. Multivariable logistic regression for risk factors for offering and acceptance for contacts was performed using backward elimination. All analyses were conducted using SAS 9.1 (Statistical Analysis System Institute, Cary, NC, USA). P , 0.05 was considered significant. Human subjects approvals were obtained from the CDC and from all local sites.
RESULTS TB patients offered and accepting testing Of 718 TB patients, 65 (9%) had previous positive HIV test results, and HIV test offering and accepting status was undocumented for 2 patients (Figure). Of the 651 remaining patients, 601 (92%) were offered testing. Patients less likely to be offered testing were those aged 765 years, Hispanics, and smokers. Of 601 patients offered HIV testing, 511 (85%) accepted. Being aged 2544 or 765 years, Hispanic, foreign-born, or a current smoker were associated with non-acceptance (data not shown). HIV results among TB patients Of 511 TB patients who accepted testing, results were documented for 500 (98%), 51 (10%) of whom were newly diagnosed as HIV-infected (Table 1). There were a total of 116 HIV-infected patients (21% of 565 with known results). Compared with noninfected patients, those with newly detected HIV infection were more likely to be aged 2544 years (P ¼ 0.02), non-Hispanic Black or American Indian/First Nations race/ethnicity (P , 0.01), US/Canada-born (P ¼ 0.01), drug users (P , 0.01), homeless (P , 0.01), and have no acid-fast bacilli detected on sputum smear microscopy and pulmonary cavities on radiography (P ¼ 0.03). Of those tested, newly detected HIV infection was higher among injection drug users (9/22, 41%) than non-injection drug users (16/60, 27%); 13% (40/304) of US/Canada-born patients were HIV-infected compared to 6% (11/196) of foreign-born persons (P , 0.01 for all comparisons). Compared to previously diagnosed HIVinfected patients, newly diagnosed HIV-infected patients were more likely to be male, and less likely to report heavy alcohol use. Patients who were aged 765 years, Hispanic, or foreign-born were less likely to have known HIV status. Contacts offered testing Of 4586 close contacts, 47 (1%) reported previous positive HIV test results, and an additional 387 did
HIV testing in TB contact investigations
945
exposed to HIV-positive index TB patients were less likely to accept testing. Among foreign-born contacts, age ,15 years was a more common reason for refusing to be tested, while among US/Canada-born contacts the most frequent reason was unwillingness to know their HIV status. HIV results among contacts Of 1208 contacts with results available, 47 (4%) had a previous HIV diagnosis, 24 (2%) had new positive HIV results, and 1137 (94%) had new negative HIV results (Table 5). Overall, US/Canada-born contacts were more likely to be HIV-infected than foreignborn contacts (P , 0.001). Compared with HIVnegative contacts, newly diagnosed HIV-infected contacts were older and more likely to be male, US/ Canada-born, or a contact of an HIV-infected index patient. Contacts with newly diagnosed and previously known infection were similar across all variables. Among all contacts with known status, HIV infection rates were 17% (10/60) among injecting drug users, 9% (22/241) among noninjecting drug users, and 23% (43/184) among contacts of an HIV-infected index case. Figure Summary of numbers of TB patients and contacts, from identification to offering, accepting, and results of HIV testing. TB ¼ tuberculosis; HIV ¼ human immunodeficiency virus; þ ¼ positive; ¼ negative.
not have test offering and accepting status recorded; these were excluded from further analyses (Figure). Of the 4152 remaining patients, 3099 (75%) were offered HIV testing. Bivariate results are shown in Table 2, multivariable results in Table 3, and reasons given by staff for not offering testing in Table 4. Exposure to TB occurred in households (63%), social environments (18%), workplaces (15%), and schools (3%). Of contacts not offered testing, 102 (10%) were contacts of HIV-infected TB patients, and 398 (38%) did not complete TST screening. In multivariable analysis, contacts aged 15–64 years, nonWhites, foreign-born persons, smokers, those with positive screening results for LTBI and TB disease, and household contacts were more likely to be offered testing; contacts exposed to an HIV-negative index TB patient were less likely to be offered testing. The most common reasons for staff not offering testing differed by the contact’s birth country (Table 4). Contacts accepting testing Of 3099 contacts offered HIV testing, 1202 (39%) accepted. In multivariable analysis, contacts aged 15– 64 years, smokers, street drug users, alcohol users, diabetics, and those with positive screening results for LTBI and TB disease were more likely to accept testing. Foreign-borns, Blacks, Hispanics, and those
DISCUSSION In our large multisite study, HIV status was identified in only 79% of TB patients and 26% of contacts, despite existing public health guidelines recommending HIV testing8–10 and a study intervention to offer HIV testing to all TB patients and contacts as part of the contact investigation. Of those tested, 21% of TB patients and 6% of contacts were HIV-infected. We found that 20% of untested TB patients and 25% of untested contacts were drug users, a group likely to be at increased risk for HIV infection. Our study describes risk factors for not offering and not accepting HIV testing, and identifies important missed opportunities for appropriate evaluation and treatment for HIV for both TB patients and exposed contacts. These findings are important for devising procedures and interventions aimed at improving HIV testing rates, and are of relevance to medical providers and public health professionals. Past studies have demonstrated increases in HIV testing rates among TB patients over the past decade.11–16 HIV testing rates reported for TB patients in the United States reached 84% in 2012,12 and testing in Alberta, Canada, using an opt-out approach reached 95% in 2007–2008.15 In keeping with these reports, more than 90% of TB patients in our study were offered HIV testing. Very young and older TB patients were offered HIV testing less frequently than other age groups, and when offered testing, they often refused. CDC-published TB surveillance reports include HIV testing status for
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Table 1 Characteristics of 718 infectious tuberculosis patients by HIV status at the nine participating Tuberculosis Epidemiologic Studies Consortium Sites, 2002–2006 HIV status
Case characteristics
Prior HIVþ (n ¼ 65) n (%)
Age groups, years 15–24 (reference) 25–44 45–64 765
1 34 28 2
(1.5) (52.3) (43.1) (3.1)
4 (7.8) 30 (58.8) 17 (33.3) 0
80 172 136 61
Sex Male (reference) Female
34 (52.3) 31 (47.7)
37 (72.5) 14 (27.5)
1 5 55 3 1
2 3 39 6 1
Race/ethnicity Hispanic Non-Hispanic White (reference) Non-Hispanic Black American Indian/Alaskan Native Asian Other
(1.5) (7.7) (84.6) (4.6) (1.5) 0
New HIVþ (n ¼ 51) n (%)
(3.9) (5.9) (76.5) (11.8) (2.0) 0
New HIV (n ¼ 449) n (%) (17.8) (38.3) (30.3) (13.6)
Unknown status (n ¼ 153) n (%) (11.1) (35.9) (22.2) (30.7)
0.62 0.85 ,0.01
283 (63.0) 166 (37.0)
86 (56.2) 67 (43.8)
0.15
98 71 202 18 58 2
45 17 64 5 21 1
(21.8) (15.8) (45.0) (4.0) (12.9) (0.4)
17 55 34 47
Unknown vs. known status P value
(29.4) (11.1) (41.8) (3.3) (13.7) (0.7)
0.02 0.99 0.79 0.19 0.46
,0.01
Birthplace US/Canada (reference) Foreign-born
55 (84.6) 10 (15.4)
40 (78.4) 11 (21.6)
264 (58.8) 185 (41.2)
77 (50.3) 76 (49.7)
Smoking in past 6 months Yes No (reference) Unknown/missing
39 (60.0) 23 (35.4) 3 (4.6)
27 (52.9) 23 (45.1) 1 (2.0)
194 (43.2) 255 (56.8) 0
42 (27.5) 110 (71.9) 1 (0.7)
,0.01
Injection drug use Yes No (reference) Unknown/missing
18 (27.7) 38 (58.5) 9 (13.8)
9 (17.6) 31 (60.8) 11 (21.6)
13 (2.9) 372 (82.9) 64 (14.3)
2 (1.3) 121 (79.1) 30 (19.6)
0.01
Non-injection drug use Yes No (reference) Unknown/missing
30 (46.2) 27 (41.5) 8 (12.3)
16 (31.4) 24 (47.1) 11 (21.6)
44 (9.8) 341 (75.9) 64 (14.3)
12 (7.8) 111 (72.5) 30 (19.6)
Excess alcohol use Yes No (reference) Unknown/missing
34 (52.3) 23 (35.4) 8 (12.3)
8 (15.7) 32 (62.7) 11 (21.6)
65 (14.5) 319 (71.0) 65 (14.5)
20 (13.1) 103 (67.3) 30 (19.6)
Homeless in past year Yes No (reference) Unknown
11 (16.9) 47 (72.3) 7 (10.8)
8 (15.7) 32 (62.7) 11 (21.6)
22 (4.9) 368 (82.0) 59 (13.1)
8 (5.2) 121 (79.1) 24 (15.7)
Sputum AFB smear status Positive Negative (reference) Not performed
38 (58.5) 27 (41.5) 0
32 (62.7) 18 (35.3) 1 (2.0)
345 (76.8) 97 (21.6) 7 (1.6)
103 (67.3) 45 (29.4) 5 (3.3)
0.23
Cavity seen on chest radiograph Yes No (reference) Unknown/missing
14 (21.5) 49 (75.4) 2 (3.1)
12 (23.5) 38 (74.5) 1 (2.0)
201 (44.8) 242 (53.9) 6 (1.3)
59 (38.6) 90 (58.8) 4 (2.6)
0.78
0.73
,0.01 0.02 0.01 0.15 0.28 0.41 0.58
0.10
0.38
HIV ¼ human immunodeficiency virus; AFB ¼ acid-fast bacilli.
cases aged 2544 years, the population at greatest risk for infection during the early years of the epidemic.12,17 However, persons from that era are now aging, older persons may be newly infected, and adolescents and young adults may also be exposed. Of note, TB patients in Alberta, Canada, who are middle aged were recently shown to have a significantly higher HIV infection rate than those in younger age groups.15 Nearly half of our participants with newly identified HIV infection were aged ,25 or .44 years. Further efforts to raise awareness among
physicians and other clinical staff about the importance of HIV testing for TB patients of all ages may well lead to further increases in HIV test offering and acceptance. HIV testing rates in the United States and Canada remain poor among contacts,6,11,13,18 despite recommendations in both countries to universally test TB contacts.8–10 In a 2003 New York City intervention to improve HIV testing, only 29% of contacts with unknown status were tested.14 In our study, 75% of contacts were offered testing, but only 39%
HIV testing in TB contact investigations
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Table 2 Characteristics of 4152 TB contacts who were offered/not offered HIV testing, and who accepted/did not accept HIV testing at the nine participating Tuberculosis Epidemiologic Studies Consortium Sites, 2002–2006 Offered testing
Contact characteristics
Yes (n ¼ 3099) n (%)
No (n ¼ 1053) n (%)
Age groups, years 0–5 6–14 15–24 (reference) 25–44 45–64 765 Unknown/missing
255 264 642 1117 656 157 8
165 121 134 278 227 42 86
Sex Male (reference) Female Unknown/missing Race/ethnicity Hispanic Non-Hispanic White (reference) Non-Hispanic Black American Indian/Alaskan Native Asian Other Unknown/missing Birthplace US/Canada (reference) Foreign born Unknown/missing Smoking past 6 months Yes No (reference) Unknown/missing
(8.2) (8.5) (20.7) (36.0) (21.2) (5.1) (0.3)
Accepted testing
P value
Yes (n ¼ 1202) n (%)
(15.7) (11.5) (12.7) (26.4) (21.6) (4.0) (8.2)
0.13 ,0.01 0.21 ,0.01
42 53 287 459 312 48 1
1581 (51.0) 1517 (49.0) 1 (0.0)
541 (51.4) 491 (46.6) 21 (2.0)
0.44 ,0.01
655 (54.5) 547 (45.5) 0
880 318 1556 119 215 7 4
144 159 529 26 46 3 146
(28.4) (10.3) (50.2) (3.8) (6.9) (0.2) (0.1)
,0.01 ,0.01
(13.7) (15.1) (50.2) (2.5) (4.4) (0.3) (13.9)
,0.01 ,0.01 ,0.01 0.82 ,0.01
247 179 540 111 119 4 2
1946 (62.8) 1145 (36.9) 8 (0.3)
778 (73.9) 100 (9.5) 175 (16.6)
,0.01 ,0.01
782 (25.2) 2244 (72.4) 73 (2.4)
116 (11.0) 477 (45.3) 460 (43.7)
,0.01
,0.01 ,0.01
(3.5) (4.4) (23.9) (38.2) (26.0) (4.0) (0.1)
(20.5) (14.9) (44.9) (9.2) (9.9) (0.3) (0.2)
480 (39.9) 684 (56.9) 38 (3.2)
302 (15.9) 1560 (82.2) 35 (1.8)
,0.01
53 (4.4) 1111 (92.4) 38 (3.2)
16 (0.8) 1846 (97.3) 35 (1.8)
,0.01
86 (4.5) 1774 (93.5) 37 (2.0)
,0.01 ,0.01 ,0.01
1492 244 123 38
,0.01 ,0.01 ,0.01
,0.01
231 (19.2) 933 (77.6) 38 (3.2)
Alcohol use None (reference) Mild Heavy Unknown/missing
2170 540 312 77
459 87 44 463
0.03 0.02 ,0.01
678 296 189 39
Diabetes Yes No (reference) Unknown/missing
146 (4.7) 2896 (93.4) 57 (1.8)
48 (4.6) 717 (68.1) 288 (27.4)
Index case’s sputum smear status Positive Negative (reference) Not done
2528 (81.6) 535 (17.3) 36 (1.2)
899 (85.4) 145 (13.8) 9 (0.9)
0.01
Index case cavitary Yes No (reference) Unknown/missing
1365 (44.0) 1684 (54.3) 50 (1.6)
447 (42.5) 582 (55.3) 24 (2.3)
0.46
Index case’s HIV status Positive Negative (reference) Unknown
473 (15.3) 1950 (62.9) 676 (21.8)
102 (9.7) 754 (71.6) 197 (18.7)
,0.01
Contact preliminary diagnosis Active TB TST convertor TST-positive TST-negative (reference) No post-exposure screen Not screened
139 168 1176 1120 451 45
37 29 178 411 178 220
0.10 ,0.01 ,0.01
(4.5) (5.4) (37.9) (36.1) (14.6) (1.5)
(3.5) (2.8) (16.9) (39.0) (16.9) (20.9)
0.10 ,0.01
0.41
0.16
0.03
0.49 ,0.01
,0.01 NA
,0.01 0.32
45 (4.3) 543 (51.6) 465 (44.2) (43.6) (8.3) (4.2) (44.0)
926 (48.8) 970 (51.1) 1 (0.1)
1119 (59.0) 772 (40.7) 6 (0.3)
317 (10.2) 2707 (87.4) 75 (2.4) (70.0) (17.4) (10.1) (2.5)
0.14 0.30 ,0.01 0.07
(56.4) (24.6) (15.7) (3.2)
633 139 1016 8 96 3 2
,0.01 ,0.01
827 (68.8) 373 (31.0) 2 (0.2)
14 (1.3) 576 (54.7) 463 (44.0)
0.04
(11.2) (11.1) (18.7) (34.7) (18.1) (5.7) (5.7)
,0.01 ,0.01 0.83 0.96 0.80
69 (2.2) 2957 (95.4) 73 (2.4)
,0.01
213 211 355 658 344 109 7
P value
(33.4) (7.3) (53.6) (0.4) (5.1) (0.2) (0.1)
Injection drug use Yes No (reference) Unknown/missing ‘Street drug’ use Yes No (reference) Unknown/missing
0.89
No (n ¼ 1897) n (%)
(78.7) (12.9) (6.5) (2.0)
,0.01
0.12
0.03
74 (6.2) 1096 (91.2) 32 (2.7)
72 (3.8) 1800 (94.9) 25 (1.3)
,0.01
965 (80.3) 228 (19.0) 9 (0.7)
1563 (82.4) 307 (16.2) 27 (1.4)
0.06
532 (44.3) 652 (54.2) 18 (1.5)
833 (43.9) 1032 (54.4) 32 (1.7)
0.88
160 (13.3) 818 (68.1) 224 (18.6)
313 (16.5) 1132 (59.7) 452 (23.8)
95 79 458 393 149 28
(7.9) (6.6) (38.1) (32.7) (12.4) (2.3)
44 89 718 727 302 17
(2.3) (4.7) (37.8) (38.3) (15.9) (0.9)
0.49
0.09
0.04 ,0.01 ,0.01 ,0.01 0.05 0.06 0.44 ,0.01
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Table 2
(continued) Offered testing
Contact characteristics
Yes (n ¼ 3099) n (%)
No (n ¼ 1053) n (%)
Environment for exposure Household (reference) Non-household/social School Workplace
2072 560 74 393
559 197 66 231
(66.9) (18.1) (2.4) (12.7)
(53.1) (18.7) (6.3) (21.9)
Accepted testing
P value
Yes (n ¼ 1202) n (%)
No (n ¼ 1897) n (%)
,0.01 ,0.01 ,0.01
802 240 36 124
1270 320 38 269
(66.7) (20.0) (3.0) (10.3)
(66.9) (16.9) (2.0) (14.2)
P value
0.07 0.08 0.01
TB ¼ tuberculosis; HIV ¼ human immunodeficiency virus; NA ¼ not available; TST ¼ tuberculin skin test.
of contacts agreed to be tested, resulting in a testing rate of 26%, similar to the New York study. Although clinic and research workers were strongly encouraged by a structured intervention, 25% of contacts in our study were not offered testing. Similar to our findings among TB patients, very young and older contacts were offered HIV testing less frequently than other age groups, and when offered testing, they often refused. These findings point to the need for further efforts to raise awareness among public health staff of the importance of HIV testing among exposed contacts of all ages. Previously identified negative influencing factors for accepting HIV testing among contacts have included self-perception of low risk, younger or older age, foreign birth, and poor testing environment, whereas positive factors have included homelessness, substance use, and recent history of TST positivity.6,13,14,18 Our study also identified being Black or Hispanic and lack of an optimal testing environment as important risk factors for not accepting HIV testing. Based on these findings, health departments are encouraged to take the necessary steps to ensure that a good testing Table 3 testing
environment is available and utilized for offering HIV testing. Additional time and effort may also be required to counsel contacts who may perceive themselves to be at low risk or be otherwise reluctant to accept HIV testing, with particular focus on Blacks and Hispanics. The HIV co-infection rate among TB patients in our study was somewhat higher than the annual national HIV co-infection rates in the United States, coinciding with the study enrollment time period (21% of TB patients in our study vs. 12–17% of all US TB patients17), but lower than rates reported in a US study that enrolled patients in 1996, in which 27% of 224 TB patients were co-infected.6 All three studies underscore the continued importance of HIV as a co-factor for TB disease, and the need to routinely test all TB patients for HIV. The HIV infection rate among contacts in our study, at 6%, was somewhat lower than among contacts in a 1996 US study (9% of 220 contacts).6 Nevertheless, HIV rates among contacts in both studies were considerably higher than the estimated seroprevalence in the general US population (0.5%), highlighting the importance of considering contacts
Multivariable analysis of TB contacts who were offered/not offered HIV testing, and who accepted/did not accept HIV Offered testing
Contact characteristics Age 15–64 years American Indian/Alaskan native Asian Hispanic Non-Hispanic Black Other race Foreign-born Smoking in past 6 months ‘Street drug’ use Any alcohol use Diabetes Steroids Index case HIV-negative Positive TB screening Household contact
Accepted testing
b
aOR
95%CI
b
aOR
95%CI
0.8878 1.8323 0.3245 0.4948 0.4343 1.5168 1.4391 0.3083 0.0220 NA NA NA 0.7145 0.3219 0.5247
2.43* 6.25* 0.72 1.64* 1.54* 0.22 4.22* 1.36* 1.02
1.96–3.02 3.20–12.20 0.45–1.18 1.17–2.31 1.19–2.00 0.05–1.06 3.05–5.82 1.05–1.77 0.71–1.48
0.49* 1.38* 1.69*
0.37–0.65 1.11–1.71 1.40–2.04
1.0103 2.7429 0.5291 0.6819 0.7868 0.8146 0.6435 0.5400 0.6394 0.4263 0.4781 0.6629 0.4640 0.4261 NA
2.75* 15.53* 1.70* 0.51* 0.46* 2.26 0.53* 1.72* 1.90* 1.53* 3.29* 1.94 1.47* 1.67*
2.15–3.51 6.98–34.59 1.13–2.56 0.37–0.70 0.35–0.60 0.48–10.61 0.41–0.68 1.38–2.14 1.39–2.58 1.25–1.88 1.08–9.99 0.93–4.04 1.14–1.88 1.37–2.03
* Statistically significant. TB ¼ tuberculosis; HIV ¼ human immunodeficiency virus; aOR ¼ adjusted odds ratio; CI ¼ confidence interval; NA ¼ not applicable.
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HIV testing in TB contact investigations
Table 4 Reasons for staff not offering and contacts not accepting HIV testing, by country of origin, at the nine participating Tuberculosis Epidemiologic Studies Consortium Sites, 2002–2006 Total n (%)
Foreign-born contacts n (%)
US-born contacts n (%)
Reason HIV testing not offered Environment not appropriate Child aged ,15 years No interviewer time Interviewer not trained for testing and counseling (reference) Interviewer forgot/no equipment available Prior HIV-positive, not eligible Prior HIV-negative, tested in past 6 weeks Other Unknown
(n ¼ 1053) 311 (29.5) 162 (15.4) 9 (0.9) 44 (4.2) 0 (0.0) 0 (0.0) 1 (0.1) 247 (23.5) 279 (26.5)
(n ¼ 275) 19 (6.9) 5 (1.8) 5 (1.8) 13 (4.7) 0 (0.0) 0 (0.0) 1 (0.4) 127 (46.2) 105 (38.2)
(n ¼ 778) 292 (37.5) 157 (20.2) 4 (0.5) 31 (4.0) 0 (0.0) 0 (0.0) 0 (0.0) 120 (15.4) 174 (22.4)
Reason HIV testing not accepted Child aged ,15 years Don’t want to know result Recently tested (,6 weeks previously) Recently tested (.6 weeks previously) HIV test pending (reference) Not believed to be at risk Other reason Unknown
(n ¼ 1897) 197 (10.4) 25 (1.3) 529 (27.9) 1 (0.1) 30 (1.6) 1 (0.1) 307 (16.2) 807 (42.5)
(n ¼ 1119) 179 (16.0) 20 (1.8) 230 (20.6) 0 (0.0) 19 (1.7) 0 (0.0) 193 (17.2) 478 (42.7)
(n ¼ 778) 18 (2.3) 5 (0.6) 299 (38.4) 1 (0.1) 11 (1.4) 1 (0.1) 114 (14.7) 329 (42.3)
P value ,0.01 ,0.01 0.13 NA NA NA ,0.01 ,0.01 ,0.01 0.18 0.03 NA NA 0.96 0.65
HIV ¼ human immunodeficiency virus; NA ¼ not applicable.
of TB patients as a high-risk group for HIV infection.19 Most previous studies have not distinguished between overall and newly diagnosed HIV infection. In our study, we identified 51 patients and 24 contacts with previously undiagnosed HIV infection, representing prevalence rates for newly diagnosed HIV infection among TB patients and contacts of respectively 10% and 2%. The proportion of TB patients with newly diagnosed HIV infection in our study is higher than reported among TB patients in Alberta, Canada (5% in 2003–2005 and 8% in 2007–2008),15 but similar to that of a 2000 UK study, in which 11% of TB patients had newly diagnosed HIV infection. 11 The proportion of contacts with newly identified HIV infection in our study was slightly lower than that reported in the UK study (5%).11 These findings underscore the value of universal HIV testing of TB patients and exposed contacts for diagnosing and treating previously unrecognized HIV infections in these high-risk groups. HIV infection rates were similar for foreign and US/Canada-born TB patients, while US/Canadaborn contacts were more than five times as likely to be infected as foreign-born contacts. One possible explanation is that before January 2010, HIV-infected immigrants and visitors were banned from entering the United States without special waivers.20 Nevertheless, health care and study staff offered testing more frequently to foreign-born contacts. To change this practice, we need to understand why US/Canada-born contacts were offered testing less often but were far more likely to be HIV-infected. Among foreign-born contacts,
lack of privacy in workplace investigations and young age appear to have affected offering rates. Fear of deportation cannot be excluded as a possible additional reason for some refusals among foreignborn persons. These findings identify the need for further emphasis among clinical care providers and public health professionals to offer HIV testing to all TB patients, regardless of national origin, and highlight the need for greater efforts to ensure privacy in workplace settings as well as confidentiality of test results. The Canadian government recommends universal HIV screening for TB patients, and HIV risk assessment-based testing of contacts.9 In the United States, TB patients are asked about substance use, but contacts are generally not asked about the same HIV risk factors.6 We found that even when participants were aware of increased HIV risk, one in four contacts who reported drug use and nearly half of those who were heavy alcohol users declined testing when offered. This represents an opportunity to improve testing rates among a key subpopulation at high risk for HIV. Our study revealed that having diabetes had a positive influence on HIV testing rates, which may be the result of the more frequent and comprehensive clinical care among persons with underlying illnesses. These findings emphasize the potential importance of involving clinical care providers in efforts to offer and explain the importance of HIV testing. Among the factors that influenced offering and accepting testing was having active TB or LTBI. Health care workers may have educated contacts about the importance of knowing their HIV status before initiating TB or LTBI treatment.
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The International Journal of Tuberculosis and Lung Disease
Table 5 Characteristics of 4586 contacts of culture-positive pulmonary TB cases* by HIV test status at the nine participating Tuberculosis Epidemiologic Studies Consortium Sites, 2002–2006 HIV status
Case characteristics Age groups, years 10–14 (reference) 15–24 25–44 45–64 765 Unknown/missing Sex Male (reference) Female Unknown/missing
Prior HIVþ (n ¼ 47) n (%) 5 3 18 20 1
New HIVþ (n ¼ 24) n (%)
New HIV (n ¼ 1137) n (%)
(10.6) (6.4) (38.3) (42.6) (2.1) 0
0 2 (8.3) 10 (41.7) 12 (50.0) 0 0
95 272 430 291 48 1
25 (53.2) 22 (46.8) 0
18 (75.0) 6 (25.0) 0
Race/ethnicity Hispanic Non-Hispanic White (reference) Non-Hispanic Black American Indian/Alaskan Native Asian Other Unknown/missing Birthplace US/Canada (reference) Foreign-born Unknown/missing
0 2 (4.3) 42 (89.4) 2 (4.3) 0 0 1 (2.1)
1 3 17 3
43 (91.5) 3 (6.4) 1 (2.1)
22 (91.7) 2 (8.3) 0
Smoking in past 6 months Yes No (reference) Unknown/missing
22 (46.8) 21 (44.7) 4 (8.5)
Injection drug use Yes No (reference) Unknown/missing
(23.6) (16.6) (30.9) (19.3) (5.2) (4.4)
,0.01 ,0.01 ,0.01 ,0.01 ,0.01
611 (53.7) 526 (46.3) 0
1699 (50.3) 1649 (48.8) 30 (0.9)
0.04 NA
236 166 507 108 115 3 2
847 381 1707 34 183 7 219
0.05 ,0.01 0.03 0.95 ,0.01
780 (68.6) 355 (31.2) 2 (0.2)
2131 (63.1) 992 (29.4) 255 (7.5)
0.23 ,0.01
8 (33.3) 14 (58.3) 2 (8.3)
459 (40.4) 643 (56.6) 35 (3.1)
437 (12.9) 2082 (61.6) 859 (25.4)
9 (19.1 ) 34 (72.3) 4 (8.5)
1 (4.2) 21 (87.5) 2 (8.3)
50 (4.4) 1052 (92.5) 35 (3.1)
33 (1.0) 2483 (73.5) 862 (25.5)
Non-injection drug use Yes No (reference) Unknown/missing
18 (38.3) 25 (53.2) 4 (8.5)
4 (16.7) 18 (75.0) 2 (8.3)
219 (19.3) 883 (77.7) 35 (3.1)
143 (4.2) 2369 (70.1) 866 (25.6)
Alcohol consumption Heavy None or mild (reference) Unknown/missing
6 (12.8) 37 (78.7) 4 (8.5)
7 (29.2) 15 (62.5) 2 (8.3)
173 (15.2) 928 (81.6) 36 (3.2)
178 (5.3) 2335 (69.1) 865 (25.6)
,0.01
Diabetes Yes No (reference) Unknown/missing
2 (4.3) 41 (87.2) 4 (8.5)
1 (4.2) 21 (87.5) 2 (8.3)
73 (6.4) 1035 (91.0) 29 (2.6)
121 (3.6) 2574 (76.2) 683 (20.2)
,0.01
Index case’s sputum smear status Positive Negative (reference) Not done
34 (72.3) 12 (25.5) 1 (2.1)
19 (79.2) 5 (20.8) 0
912 (80.2) 216 (19.0) 9 (0.8)
2825 (83.6) 504 (14.9) 49 (1.5)
,0.01
Index case cavitary Yes No (reference) Unknown/missing
19 (40.4) 28 (59.6) 0
7 (29.2) 17 (70.8) 0
512 (45.0) 607 (53.4) 18 (1.6)
1460 (43.2) 1861 (55.1) 57 (1.7)
0.46
HIV status of index cases Prior or new positive New negative (reference) Unknown
28 (59.6) 14 (29.8) 5 (10.6)
15 (62.5) 8 (33.3) 1 (4.2)
141 (12.4) 784 (69.0) 212 (18.6)
715 (21.2) 2181 (64.6) 739 (21.9)
0.27
Contact’s preliminary diagnosis Active TB TST convertor TST-positive TST-negative (reference) No post-exposure screen Not screened
13 (27.7) 0 7 (14.9 ) 19 (40.4) 6 (12.8) 2 (4.3)
90 78 437 374 132 26
83 121 981 1261 573 359
(16.7) (4.2) (4.2) (33.3) (37.5) (4.2)
(20.8) (14.6) (44.6) (9.5) (10.1) (0.3) (0.2)
797 562 1044 652 174 149
Unknown vs. known HIV status P value
(25.1) (11.3) (50.5) (1.0) (5.4) (0.2) (6.5)
4 1 1 8 9 1
(4.2) (12.5) (70.8) (12.5) 0 0 0
(8.40) (23.9) (37.8) (25.6) (4.2) (0.1)
Unknown HIV status (n ¼ 3378) n (%)
(7.9) (6.9) (38.4) (32.9) (11.6) (2.3)
(2.5) (3.6) (29.0) (37.3) (17.0) (10.6)
,0.01
,0.01 ,0.01 ,0.01 ,0.01 ,0.01 ,0.01
,0.01
,0.01
0.02
0.70
0.01 ,0.01 ,0.01 ,0.01 0.05 ,0.01
HIV testing in TB contact investigations
Table 5
951
(continued) HIV status
Case characteristics
Prior HIVþ (n ¼ 47) n (%)
New HIVþ (n ¼ 24) n (%)
Exposure environment Household (reference) Non-household/social School Workplace
36 (87.8) 8 (19.5) 0 3 (7.3)
14 (58.3) 10 (41.9) 0 0
New HIV (n ¼ 1137) n (%) 761 222 33 121
(66.9) (19.5) (2.9) (10.6)
Unknown HIV status (n ¼ 3378) n (%) 2043 624 111 600
(60.5) (18.5) (3.3) (17.8)
Unknown vs. known HIV status P value
0.71 0.15 ,0.01
* 41 offered HIV testing, accepted, no result available. TB ¼ tuberculosis; HIV ¼ human immunodeficiency virus; NA ¼ not applicable; TST ¼ tuberculin skin test.
In the 1996 US study, contacts whose index patients had known HIV status were more than twice as likely to be tested for HIV.6 Furthermore, the same US study and a Brazilian study demonstrated that contacts of HIV-infected TB patients are more likely to be infected themselves.6,21 In our study, contacts of HIV-infected TB patients were more likely to be offered testing, but were less likely to accept. Among those tested, nearly 25% were also infected. It is worrying that most contacts in this very high-risk group were never tested. Based on our findings, further efforts are needed to promote acceptance of testing among contacts of HIV-infected TB patients. Options to consider include modifying the message delivered at the time of offering testing to increase the knowledge base for and awareness of infection and the benefits of testing among high-risk groups. Dart et al. found that TB out-patients were less likely than hospitalized patients to be offered HIV testing (49% vs. 74%); reasons given for not offering testing were lack of TB nurses, being outside the TB service, and lack of appropriate space.13 Nearly half of hospitalized TB patients declined HIV testing because they were unable to cope with a dual diagnosis. 13 In our study, workplace contacts were far less likely to be tested than household contacts. The main reason given for not offering HIV testing among contacts was lack of privacy. Facility-based contact investigations are often carried out en masse, and contact screening is performed in open rooms with little to no privacy. Safeguarding privacy in these settings may be a low priority for busy, short-staffed TB program workers. Creation of a private testing environment may therefore be an important measure for increasing testing among workplace contacts. Attempts to increase HIV testing have included staff training and support systems,13 and changes in policy supported by pamphlets and education for staff,14 but the results have been disappointing. Our intervention encouraged offering HIV counseling and testing, and included interim monitoring and
promotion by principal investigators. Nonetheless, HIV testing among contacts was poor overall, and only slightly better than program testing with no intervention. To improve the offer of HIV testing, creative approaches to providing a private testing environment should be explored. Better communication between TB clinics and health departments to identify the HIV status of TB contacts is critical. Placing the responsibility of contact testing on TB clinics may be a way to solve this problem, particularly in this time of shrinking health budgets. Oral HIV tests do not require staff to have phlebotomy skills and avoid refusals by patients due to fear of needles. Furthermore, an ‘opt-out’ approach to HIV testing, as has been adopted in some US and Canadian TB clinics, emergency rooms, and other health care settings,15,22 and now promoted also by the CDC,23,24 could minimize the influence of a major barrier, i.e., perceived risk. This approach encourages acceptance,25 and has improved HIV testing rates among US and Canadian TB patients by as much as 45%,15,22,26 as well as increasing the proportion of patients with newly identified HIV co-infection among South African TB patients by three-fold.27 Both opt-out testing and use of oral testing can facilitate screening in the clinic and in the field. Limitations to our study include missing substance use status for some participants, less than universal offering of HIV testing, less than universal acceptance of HIV testing, inability to distinguish with certainty what HIV test offering and acceptance rates would have been without a specific study intervention aimed at strengthening these program components, and no information on the language skills or demographic characteristics of the interviewers. Strengths of our study include the inclusion of multiple sites, making the study more generalizable to the US/Canadian population; determining HIV offering and testing rates; and collection of good epidemiologic data to identify risk factors for not offering and not accepting HIV testing.
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The International Journal of Tuberculosis and Lung Disease
CONCLUSION Screening and treatment for HIV is urgent in TB patients, for whom treatment regimens may need to be altered, and in contacts who, if HIV-infected, are far more likely to progress to TB disease. In our large, multisite study, HIV testing identified previously unknown infection in 10% of TB patients and 2% of contacts. High proportions of TB patients were offered and accepted HIV testing. Despite structured study procedures to offer HIV testing as part of contact investigations, low acceptance rates resulted in poor testing rates. Offering and acceptance of HIV testing were closely tied to risk perceptions among health care workers and patients. Further strategies are needed to improve HIV testing acceptance rates, especially among US/Canada-born persons and those who may not perceive themselves to be at risk. Promotion of an opt-out strategy within TB control programs might increase HIV testing rates in TB patients and contacts. Acknowledgements The authors thank L Bozeman, J Elder, D Garrett, R Horsburgh, T Navin, and A Vernon for helpful guidance and input into scientific, data management, and administrative aspects of the project, and special thanks to P Bessler for her excellent contribution to the multivariable analysis. The Tuberculosis Epidemiological Studies Consortium Task Order 2 Team: 1) TBESC Task Order 2 study sites, investigators, and study coordinators: Arkansas Department of Health, Little Rock, AR, USA (I Bakhtawar, C LeDoux); Respiratory Health Association of Metropolitan Chicago and Rush University Chicago, IL, USA (J McAuley, J Beison); University of British Columbia, Cancouver, BC, Canada (M FitzGerald, M Naus, M Nakajima); Columbia University, New York, NY, USA (N Schluger, Y Hirsch-Moverman, J Moran); Emory University, Atlanta, GA, USA (H Blumberg, J Tapia, L Singha); University of Manitoba, Winnipeg, MB, Canada (E Hershfeld, B Roche); New Jersey Medical School National Tuberculosis Center, Newark, NJ, USA (B Mangura, A Sevilla); Vanderbilt University and Tennessee Department of Health, Nashville, TN, USA (T Sterling, T Chavez-Lindell, F Maruri); Maryland Department of Health, Balitimore, MD, USA (S Dorman, W Cronin, E. Munk). 2) CDC Task Order 2 Data management team: B Chen, P Bessler, Y Yuan, F Yan, Y Shen, H Zhao, H Zhang, M Fagley, M Reichler. 3) Task Order 2 Protocol Team: M Reichler (Chair), T Sterling (Co-chair), J Tapia, C Hirsch, C Luo. This work was supported by the Centers for Disease Control and Prevention through funding to the Tuberculosis Epidemiologic Studies Consortium (TBESC). Conflicts of interest: none declared. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention or supporting agencies.
References 1 World Health Organization. Global tuberculosis control: WHO report 2011. WHO/HTM/TB/2011.16. Geneva, Switzerland: WHO; 2011: http://www.who.int/tb/publications/global_ report/2011/gtbr11_full.pdf. Accessed April 2015.
2 Centers for Disease Control and Prevention. Trends in tuberculosis – United States, 2011. MMWR Morb Mortal Wkly Rep 2012; 61: 181–185. 3 American Thoracic Society, Center for Disease Control and Prevention, Infectious Diseases Society of America: controlling tuberculosis in the United States. Am J Respir Crit Care Med 2005; 172: 1169–1227. 4 Selwyn P A, Sckell B M, Alcabes P, Friedland G H, Klein R S, Schoenbaum E E. High risk of active tuberculosis in HIV-infected drug users with cutaneous anergy. JAMA 1992; 268: 504–509. 5 Sauzullo I, Mengoni F, Scrivo R, et al. Evaluation of QuantiFERON-TB Gold In-Tube in human immunodeficiency virus infection and in patient candidates for anti-tumour necrosis factor-alpha treatment. Int J Tuberc Lung Dis 2010; 14: 834–840. 6 Reichler M R, Bur S, Reves R, et al. Results of testing for human immunodeficiency virus infection among recent contacts of infectious tuberculosis cases in the United States. Int J Tuberc Lung Dis 2003; 7 (Suppl 3): S471–S478. 7 Centers for Disease Control and Prevention. Tuberculosis provisional data—United States, 1986. MMWR Morb Mortal Wkly Rep 1987; 36: 254–255. 8 Centers for Disease Control and Prevention. Revised guidelines for HIV counseling, testing, and referral. MMWR Morb Mortal Wkly Rep 2001; 50 (RR-19): 1–58. 9 Canada Tuberculosis Committee. Recommendations for the screening and prevention of tuberculosis in patients with HIV and the screening for HIV in tuberculosis patients and their contacts. Can Commun Dis Rep 2002; 28: 1–6. 10 Centers for Disease Control and Prevention. Guidelines for the investigation of contacts of persons with infectious tuberculosis: recommendation from the national Tuberculosis Controllers Association and CDC. MMWR Morb Mortal Wkly Rep 2005; 54 (RR-15): 1–47. 11 Bowen E F, Rice P S, Cooke N T, Whitfield R J, Rayner C F. HIV seroprevalence by anonymous testing in patients with Mycobacterium tuberculosis and in tuberculosis contacts. Lancet 2000; 356: 1488–1489. 12 Centers for Disease Control and Prevention. Reported tuberculosis in the United States, 2011. Atlanta, GA, USA: US Department of Health and Human Services, CDC, 2012. 13 Dart S, Alder D, Mamdani M, et al. HIV testing in TB clinics: a problem in practice? Thorax 2006; 61: 271–272. 14 Li J, Marks S M, Driver C R, et al. Human immunodeficiency virus counseling, testing, and referral of close contacts to patients with pulmonary tuberculosis: feasibility and costs. J Public Health Manag Pract 2007; 13: 252–262. 15 Long R, Boffa J. High HIV-TB co-infection rates in marginalized populations: evidence from Alberta in support of screening TB patients for HIV. Can J Public Health 2010; 101: 202–204. 16 Marks S M, Taylor Z, Qualls N L, Shrestha-Kuwahara R J, Wilce M A, Nguyen C H. Outcomes of contact investigations of infectious tuberculosis patients. Am J Respir Crit Care Med 2000; 162: 2033–2038. 17 Centers for Disease Control and Prevention. Reported tuberculosis in the United States, 2006. Atlanta, GA, USA: US Department of Health and Human Services, CDC, 2007. 18 Rodger A J, Story A, Fox Z, Hayward A. HIV prevalence and testing practices among tuberculosis cases in London: a missed opportunity for HIV diagnosis? Thorax 2010; 65: 63–69. 19 McQuillan G M, Kruszon-Moran D, Granade T, Feldman J W. Seroprevalence of HIV in the US household population aged 18–49 years: the National Health and Nutrition Examination Surveys, 1999–2006. J Acquir Immune Defic Syndr 2010; 53: 117–123. 20 US Citizenship and Immigration Services. Public Law 110-293, 42 CFR 34.2 (b) and Inadmissibility Due to Human Immunodeficiency Virus (HIV) Infection. Washington DC, USA: USCIS, 2009. http://d.yimg.com/kq/groups/4317947/ 1952933142/name/11.24.09%20USCIS%20Memorandum %20 on %20HI V%20 In ad mis si bi li t y%20a nd %20F in a Accessed May 2015.
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21 Carvalho A C, DeRiemer K, Nunes Z B, et al. Transmission of Mycobacterium tuberculosis to contacts of HIV-infected tuberculosis patients. Am J Respir Crit Care Med 2001; 164: 2166–2171. 22 Gardner A, Naureckas C, Beckwith C, Losikoff P, Martin C, Carter E J. Experiences in implementation of routine human immunodeficiency virus testing in a US tuberculosis clinic. Int J Tuberc Lung Dis 2012; 16: 1241–1246. 23 Centers for Disease Control and Prevention. Integrated prevention services for hiv infection, viral hepatitis, sexually transmitted diseases, and tuberculosis for persons who use drugs illicitly: summary guidance from CDC and the US Department of Health and Human Services. MMWR Morb Mortal Wkly Rep 2012; 61 (RR05): 1–40.
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24 Centers for Disease Control and Prevention Fact Sheet. Recommendations for human immunodeficiency virus (HIV) screening in tuberculosis (TB) clinics. Atlanta, GA, USA: CDC, 2012. 25 World Health Organization. Guidance on provider-initated HIV testing and counselling in health facilities. Geneva, Switzerland: WHO, 2007. http://whqlibdoc.who.int/publications/2007/ 9789241595568_eng.pdf. Accessed April 2015. 26 Sturtevant D, Preiksaitis J, Singh A, et al. The feasibility of using an ’opt-out’ approach to achieve universal HIV testing of tuberculosis patients in Alberta. Can J Public Health 2009; 100: 116–120. 27 Pope D S, Deluca A N, Kali P, et al. A cluster-randomized trial of provider-initiated (opt-out) HIV counseling and testing of tuberculosis patients in South Africa. J Acquir Immune Defic Syndr 2008; 48: 190–195.
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i
RESUME
D´eterminer le statut par rapport au virus de l’immunod´eficience humaine (VIH) des patients avec un diagnostic de la tuberculose (TB) et de leurs contacts est important. Cependant, en de´ pit des directives existantes, tous les patients ne sont pas test´es et encore beaucoup moins, leurs contacts. M E´ T H O D E : Dans une e´ tude r´ealis´ee dans neuf sites aux Etats-Unis et au Canada, nous avons introduit des proc´edures formelles visant a` offrir le test VIH aux patients TB et a` leurs contacts. Les donn´ees ont e´ t´e recueillies a` travers des entretiens et une revue des dossiers me´ dicaux. On a alors examine´ les caract´eristiques associ´ees avec l’offre et l’acceptation du test VIH. R E´ S U LT A T S : Sur 651 patients TB, 601 (92%) se sont vus offrir le test, 511 (85%) l’ont accept´e et 51 (10%) e´ taient infect´es par le VIH. Sur 4152 contacts, 3099 (75%) se sont vus offrir le test, 1202 (39%) l’ont accept´e CONTEXTE :
et 24 (2%) e´ taient infect´es par le VIH. Les contacts ag´ ˆ es de 15 a` 64 ans, non blancs, n´es a` l’´etranger, fumeurs, ceux qui avaient eu un d´epistage positif de TB et les contacts domestiques avaient davantage de chances de se voir proposer le test ; les contacts expos´es a` des patients VIH n´egatifs avaient moins de chances de se voir proposer le test. Les contacts ag´ ˆ es de 15 a` 64 ans, fumeurs, consommateurs de drogues/d’alcool, diab´etiques et ceux dont le d´epistage TB e´ tait positif ont plus souvent accept´e le test. Les contacts n´es a` l’´etranger, noirs, hispaniques et expos´es a` des patients VIH positifs ont moins souvent accept´e le test. C O N C L U S I O N S : Des taux e´ lev´es d’infections a` VIH ont e´ t´e d´etect´es parmi les patients et les contacts. En d´epit de proc´edures structur´ees d’offre du test VIH, une partie des patients et la majorit´e des contacts n’ont pas accept´e le test. Il est n´ecessaire d’´elaborer des strat´egies nouvelles pour am´eliorer l’acceptation du test. RESUMEN
Es importante determinar la situacion ´ frente al virus de la inmunodeficiencia humana (VIH) de los pacientes con diagnostico ´ de tuberculosis (TB) y sus contactos. Pese a las directrices existentes, las pruebas diagnosticas ´ no se practican a todos los pacientes y rara vez se investigan los contactos. M E´ T O D O S: En un estudio de nueve centros en ciudades del Canada´ y los Estados Unidos se introdujeron procedimientos estructurados, encaminados a ofrecer la prueba diagnostica ´ del VIH a los pacientes con TB y a los contactos. Los datos se recogieron mediante entrevistas y ana´lisis de las historias cl´ınicas y se examinaron las caracter´ısticas asociadas con el ofrecimiento y la aceptaci on ´ de las pruebas diagnosticas ´ del VIH. R E S U LT A D O S: De los 651 pacientes con diagnostico ´ de TB, se ofrecio´ la prueba del VIH a 601 (92%), 511 pacientes la aceptaron (85%) y 51 obtuvieron un resultado positivo (10%). Se propuso la prueba del VIH a 3099 de los 4152 contactos (75%), 1202 la aceptaron (39%) y se obtuvieron 24 resultados positivos (2%). Fue ma´s probable que se ofreciese la prueba M A R C O D E R E F E R E N C I A:
diagnostica ´ del VIH a los contactos de edad de 15–64 anos, de una etnia diferente de la blanca, nacidos en el ˜ extranjero, fumadores, a los contactos con una investigaci on ´ de TB positiva y a los contactos domiciliarios; fue menos frecuente proponer la serolog´ıa del VIH a los contactos expuestos a pacientes con serolog´ıa negativa. Se observ o´ una mayor probabilidad de aceptacion ´ de la prueba del VIH en los contactos de edad de 15–64 anos, fumadores, ˜ consumidores de alcohol o de drogas, en los pacientes diab´eticos y los contactos cuya deteccion ´ sistema´tica de la TB fue positiva. Fue menos probable que aceptaran la serolog´ıa del VIH las personas nacidas en el extranjero, de etnia negra, los hispanoamericanos y los contactos expuestos a pacientes seropositivos. ´ N: Se observaron altas tasas de infeccion CONCLUSIO ´ por el VIH en los pacientes con diagnostico ´ de TB y en sus contactos. Pese a la existencia de mecanismos estructurados de oferta de la prueba diagnostica ´ del VIH, algunos pacientes y la mayor´ıa de los contactos no aceptaron la prueba. Es preciso establecer estrategias que mejoren las tasas de aceptacion. ´
