The feasibility of using an 'opt-out' approach to achieve universal HIV testing of tuberculosis patients in Alberta.Among medical conditions that depress cellular immunity and facilitate progression of recent or remotely acquired tuberculosis (TB) infection to TB disease, none is more important than HIV. (1) For AIDS and HIV, the estimated risk of TB, relative to persons with no known risk factor, is 110-170 fold and 50-110 fold, respectively. (2-5) HIV-attributable TB adds to the burden of TB through transmission to others regardless of their HIV status. A diagnosis of HIV in a TB patient impacts the treatment of TB and identifies the need for HIV treatment and prevention services. (6,7) Screening for HIV has been determined to be cost effective when the prevalence of infection is 0.5% or greater. (8)
In 1989, the US Centers for Disease Control and Prevention recommended universal HIV testing of TB patients. (9) In 1992 and 2002, Canadian respiratory and infectious disease societies and Health Canada jointly made similar recommendations. (7,10) Despite these recommendations and the close biological and epidemiological links between the two pathogens, the policy of universal HIV testing of TB patients has not been implemented in Canada and the prevalence of HIV/TB co-infection is unknown. (11,12) Poor compliance with recommendations for HIV testing of TB patients was understandable before the advent of highly active antiretroviral therapy (HAART) and in the context of discrimination, when informed consent and extensive pre- and post-test counselling were advised. (13-15) However, poor compliance and the separation of counselling and testing from routine medical care are now difficult to defend, as is ignorance of the relationship between HIV and TB.
In Alberta, TB and HIV are reportable diseases and their testing is centralized. In 2003, an 'opt-out' approach to HIV testing of TB patients was implemented whereby testing became routine unless the patient specifically chose not to be tested. 'Opt-out' testing followed the basic tenets of informed consent. (16) To assess the ability of 'opt-out' testing to achieve universal testing targets, TB and HIV databases were cross-matched. To assess the risks of HIV positivity in HIV-tested TB patients, the age, gender, ethnic group and disease site of TB patients diagnosed between 1991 and 2006 were compared.
Patients diagnosed with TB over the 16-year period from 1991-2006 were identified in the TB Registry of Alberta Health and Wellness. TB case patients were cross-matched with the Provincial Laboratory for Public Health (PLPH) HIV database (96.7% to 98.0% of all HIV testing in Alberta is performed in the PLPH; 100% of all HIV-positive test results in the province are confirmed in the PLPH). Confirmation of a cross-match required that at least two of three identifiers (name, date of birth, and health care number) be identical. HIV test results and the date of testing relative to the date of diagnosis of TB (the start date of anti-TB drugs) were recorded. TB patients were then divided into three groups: i) those diagnosed before HAART (1991-1997) when HIV testing of TB patients was largely 'semi-selective' on the basis of a reported risk factor for HIV, but effective treatment of HIV was not available; ii) after HAART and before 'opt-out' testing (1998-2002), when HIV testing was 'selective-plus' with most of those with and some of those without risk factors accepting/being offered testing, likely as a result of the availability of effective treatment of HIV; and iii) after 'opt-out' testing was implemented (2003-2006), when HIV testing was intended to be universal. HIV-tested and HIV-positive TB patients in each group were described according to age, gender, ethnic group and disease type (respiratory, non-respiratory, or both). Ethnic group was categorized as Canadian-born Aboriginal (First Nations, Metis, and Inuit), Canadian-born 'other', foreign-born sub-Saharan African (Canadian International Development Agency), and foreign-born 'other'. (17)
In the 'semi-selective' and 'selective-plus' testing years (1991-2002), the 'post-TB' HIV status of TB patients aged 15-64 who were 1) either HIV negative or HIV untested 'at the time of diagnosis of TB', and 2) retested any time before the end of 2007, were compared. HIV test results 'at the time of diagnosis of TB' include those reported from 6 months before and up to 9 months after the date of diagnosis of TB. Thus, the 'post-TB' period refers to 9 months after the date of diagnosis of TB until the end of 2007. In the years 1991-2006, the demographic and clinical characteristics of TB patients who were HIV positive and negative at the time of diagnosis of TB and aged 15-64 years, were compared.
[FIGURE 1 OMITTED]
Clinical and laboratory features of HIV co-infected TB patients, as recorded in the TB Registry, the PLPH, the Capital and Calgary Health TB Clinics, and the HIV/AIDS Clinics of Northern and Southern Alberta, were described.
To compare the demographic and clinical characteristics of HIV-negative and -positive TB patients diagnosed between 1991 and 2006, odds ratios (OR) with their 95% confidence interval (95% CI) and p-values were estimated using logistic regression analysis. Multiple logistic regression analysis was used to determine adjusted odds ratios. The study was approved by the Health Research Ethics Board of the University of Alberta.
Over the 16-year period from 1991-2006, 2,340 patients were diagnosed with new active or relapsed TB in Alberta, 1,161 (49.6%) in 1991-1997, 683 (29.2%) in 1998-2002, and 496 (21.2%) in 2003-2006 (Table 1). For the three periods, respectively, the mean ([+ or -] SD) age of patients was 48.1 (23.6), 50.2 (22.2), and 48.2 (22.1) years, and the ratio of males to females was 0.96, 1.10 and 1.02. Between the first and last time period, the proportion of foreign-born TB patients increased from 58.1% to 74.4% and the proportion of foreign-born from sub-Saharan Africa from 6.8% to 20.6%. In each time period, the majority of Canadian-born TB patients were Aboriginal; 58.9%, 60.0%, and 52.0%, respectively.
In 1991-1997 (before HAART), 1998-2002 (after HAART but before 'opt-out' testing was implemented), and 2003-2006 (after 'opt-out' testing was implemented), respectively, HIV testing was performed at the time of diagnosis of TB in 11.5%, 44.9% and 81.9% of patients (Table 1 and Figure 1). Over the three time periods, a total of 50 TB patients were diagnosed with HIV co-infection, all in the age group 15-64 years. During the 'opt-out' testing years, 87.4% of TB patients aged 15-64 were HIV tested. During these years, the prevalence of HIV positivity in HIV-tested Canadian-born 'other', Canadian-born Aboriginal, foreign-born 'other' and foreign-born sub-Saharan African TB patients aged 15-64 years was 0.0%, 10.9%, 3.7 % and 18.0%, respectively, and the overall prevalence was 7.4% (data not shown).
Among TB patients aged 15-64 years who were diagnosed in the 'semi-selective' or 'selective-plus' testing years 1991-2002, 'post-TB' HIV test results were as follows: of 156 patients who were untested at the time of diagnosis of TB and underwent one or more 'post-TB' HIV tests, all had a negative first test while 1 had a positive subsequent test; of 78 HIV-negative TB patients who underwent a 'post-TB' HIV test, 3 had a positive first and 1 had a positive subsequent test (Table 2). Assuming they remained in Alberta, the median duration of follow-up of TB patients who were never HIV tested (n=660) was 12.9 (range 5.0-17.0) years.
Among TB patients aged 15-64 who were HIV tested over the 16 years from 1991-2006, those testing positive were significantly less likely to be female and less likely to have respiratory TB alone (Table 3). Co-infected patients were significantly more likely to have both respiratory and non-respiratory TB than respiratory TB alone. The prevalence of HIV positivity among HIV-tested TB patients aged 15-64 years was 7.8%.
TB was culture positive in 49 of 50 HIV co-infected patients; 5 isolates were mono-resistant. HIV was discovered prior to and at the time of diagnosis of TB in 18 (36%) and 32 (64%) patients, respectively. CD4 counts were < 200 x [10.sup.6]/L in 34 of 47 (72.3%) HIV co-infected TB patients who had record of a CD4 count, averaging 141.0 [+ or -] 118.2 x [10.sup.6]/L and 155.1 [+ or -] 199.7 x [10.sup.6]/L in those diagnosed prior to and at the time of diagnosis of TB, respectively. HIV exposure categories were: heterosexual contact--19 patients; injection drug use (IDU)--15 patients; men who have sex with men (MSM)--8 patients; MSM-IDU--1 patient; 'other'--1 patient; unknown--6 patients.18 Seven patients (14%) died during the period of activity of TB.
Over the 16-year period from 1991-2006, increasing proportions of TB patients in Alberta were HIV tested. Increased testing was temporally related to the availability of HAART and the implementation of 'opt-out' HIV testing (Figure 1). In the 'opt-out' years, HIV testing was considered universal, having met a recognized program performance target of testing more than 80% of TB patients. (19) Over 16 years, HIV-TB co-infection was diagnosed in 50 patients, all in the age group 15-64 years. HIV-TB co-infected patients were significantly less likely to be female and less likely to have respiratory TB alone; they were significantly more likely to have both respiratory and non-respiratory TB than non-respiratory TB alone--differences that were not surprising given that HIV is more prevalent in males in Canada, and TB is prone to disseminate in HIV co-infected patients. (1,18) Most HIV co-infected TB patients had advanced HIV disease (CD4 count < 200 x [10.sup.6]/L) at or before the diagnosis of TB. The prevalence of HIV co-infection in TB patients aged 15-64 years was 7.4% in the 'opt-out' testing years, similar to earlier Canadian (3.0-14.7%) and World Health Organization (8.7%) estimates. (11,20-22)
HIV co-infection was more likely to have been missed during the 'semi-selective' testing years 1991-1997 (before HAART) when very few TB patients were HIV tested; two new HIV-positive patients are known to have been discovered during anonymous testing of TB patients in 1990-1994. (23) HIV co-infection was less likely to have been missed in the 'selective-plus' testing years 1998-2002 (after HAART but before 'opt-out' testing) when many more TB patients were HIV tested.
To the extent that 'selective' HIV testing is focused upon the HIV exposure categories of MSM (men who have sex with men) and IDU, it is predicted to fail to detect a significant number of those at risk for dual infection in the future. (20,24,25) Many immigrants are now arriving from HIV-endemic countries in which heterosexual contact is the main HIV exposure category; IDU and/or heterosexual contact are increasingly the main HIV exposure categories in Aboriginal peoples. (1,18,26) Young adults from all ethnic groups may, through lack of awareness, be at risk for sexually transmitted disease and HIV/AIDS. In addition, experience from other programs suggests that anything other than truly universal HIV testing will fail to identify some individuals who are HIV infected. (27) For these reasons, together with the fact that universal testing does not discriminate and is less likely to be perceived as stigmatizing, and the fact that TB is an AIDS-defining illness, we support the recommendation for universal HIV testing of TB patients. As in other clinical situations, a strong provider recommendation outlining the benefits of testing is likely to increase the uptake of testing. (28) For diagnostic and treatment purposes, HIV testing should ideally be performed within one or two months of the diagnosis of TB. (19)
Limitations of this study include its retrospective design and possible underreporting of HIV status. Patients whose HIV status had been assessed outside of Alberta may not have been registered in the PLPH database and TB patients diagnosed prior to 1993 may not have had a computerized record of their HIV status in the PLPH. However, in both instances it is unlikely that HIV-positive patients were missed; patients testing positive out-of-province are usually retested when accessing health care services in Alberta, and record of the HIV-positive status of TB patients is maintained in the TB Registry.
We conclude that it is feasible to implement a non-discriminatory 'opt-out' approach to HIV testing of TB patients--one that is very similar to that adopted for prenatal HIV testing--and that this approach can achieve universal testing targets. (29,30) The relatively high rates of HIV in sub-Saharan African and Aboriginal TB patients in the age group 15-64 are of concern.
Received: May 6, 2008
Accepted: September 25, 2008
(1.) Canadian Lung Association, Public Health Agency of Canada. Canadian Tuberculosis Standards, 6th Ed. Ottawa, ON: Canadian Lung Association/ Public Health Agency of Canada, 2007. Available online at: http://www.phacaspc. gc.ca/tbpc-latb/pubs/tbstand07-eng.php (Accessed February 12, 2009).
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(8.) McCarthy BD, Wong JB, Munoz A, Sonnenberg FA. Who should be screened for HIV infection? A cost-effectiveness analysis. Arch Intern Med 1993;153:1107-16.
(9.) Centers for Disease Control and Prevention. Tuberculosis and immunodeficiency virus infection: Recommendations of the Advisory Committee for the Elimination of Tuberculosis (ACET). MMWR 1989;38(14):236-38, 243-50.
(10.) Canadian Thoracic Society, Tuberculosis Directors of Canada, Department of National Health and Welfare in consultation with the provincial and territorial epidemiologists, AIDS coordinators and HIV caregivers. Guidelines for the identification, investigation and treatment of individuals with concomitant tuberculosis and HIV infection. CCDR 1992;18:155-60.
(11.) Harris T, Panaro L, Phypers M, Choudhri Y, Archibald CP. HIV testing among Canadian tuberculosis cases from 1997 to 1998. Can J Infect Dis Med Microbiol 2006;17:165-68.
(12.) Tuberculosis in Canada 2003. Ottawa: Public Health Agency of Canada. Available online at: http://www.phac-aspc.gc.ca/tbpc-latb/surv-eng.php (Accessed February 12, 2009).
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(15.) Bayer R, Fairchild AL. Changing the paradigm for HIV testing--the end of exceptionalism. N Engl J Med 2006;355:647-49.
(16.) Joint United Nations Programme on HIV/AIDS (UNAIDS)/World Health Organization (WHO). UN/AIDS/WHO policy statement on HIV testing. Available online at: http://www.who.int/hiv/pub/vct/statement/en/ (Accessed February 12, 2009).
(17.) Canadian International Development Agency. Available online at: http://www.acdi-cida.gc.ca/index-e.htm (Accessed February 12, 2009).
(18.) Public Health Agency of Canada. HIV/AIDS Epi Updates, November 2007. Ottawa: Surveillance and Risk Assessment Division, Centre for Infectious Disease Prevention and Control, Public Health Agency of Canada, 2007.
(19.) Horsburgh C, Feldman S, Ridzon R. Practice guidelines for the treatment of tuberculosis. CID 2000;31:633-39.
(20.) Blenkush MF, Korzeniewska-kozela M, Elwood RK, Black W, Fitzgerald JM. HIV-related tuberculosis in British Columbia: Indications of a rise in prevalence and a change in risk groups. Clin Invest Med 1996;19:271-78.
(21.) Geduld J, Brassard P, Culman K, Tannenbaum TN. Testing for HIV among patients with tuberculosis in Montreal. Clin Invest Med 1999;22:111-18.
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(23.) Cowie RL, Sharpe JW. Extrapulmonary tuberculosis: A high frequency in the absence of HIV infection. Int J Tuberc Lung Dis 1997;1:159-62.
(24.) Korzeniewska-kosela M, FitzGerald JM, Vedal S, Allen EA, Schechter MT, Lawson L, et al. Spectrum of tuberculosis in patients with HIV infection in British Columbia: Report of 40 cases. CMAJ 1992;146:1927-34.
(25.) Brassard P, Remis RS. Incidence of tuberculosis among reported AIDS cases in Quebec from 1979 to 1996. CMAJ 1999;160:1838-42.
(26.) Public Health Agency of Canada. HIV and AIDS in Canada. Surveillance Report to June 30, 2006. Ottawa: Surveillance and Risk Assessment Division, Centre for Infectious Disease Prevention and Control, Public Health Agency of Canada, 2006.
(27.) Plitt S, Singh A, Lee B, Preiksaitis J. HIV seroprevalence among women opting out of prenatal HIV screening in Alberta, Canada: 2002-2004. CID 2007;45:1640-43.
(28.) Royce R, Walter E, Fernandez I, Wilson T, Ickovics J, Simonds R for the Perinatal Guidelines Evaluation Project. Barriers to universal prenatal HIV testing in 4 US locations in 1997. Am J Public Health 2001;91:727-33.
(29.) Jayaraman G, Preiksaitis J, Larke B. Mandatory reporting of HIV infection and opt-out prenatal screening for HIV infection: Effect on testing rates. CMAJ 2003;168:679-82.
(30.) Wang F-L, Larke B, Gabos S, Hanrahan A, Schopflocher D. Potential factors that may affect acceptance of routine prenatal HIV testing. Can J Public Health 2005;96(1):60-64.
Doris Sturtevant, MD,  Jutta Preiksaitis, MD,  Ameeta Singh, BMBS (UK), MSc,  Stan Houston, MD,  John Gill, MB ChB,  Gerry Predy, MD,  Dina Fisher, MD,  Ambikaipakan Senthilselvan, PhD,  Jure Manfreda, MD,  Jody Boffa, MIH,  Richard Long, MD [3,4,9]
[1.] Department of Medicine and School of Public Health, University of Alberta, Edmonton, AB
[2.] Provincial Laboratory for Public Health, Edmonton and Calgary, AB
[3.] Provincial Health Office, Alberta Health and Wellness, Edmonton, AB
[4.] Department of Medicine, University of Alberta, Edmonton, AB
[5.] Department of Medicine, University of Calgary, Calgary, AB
[6.] Capital Health Region, Edmonton, AB
[7.] Department of Public Health Sciences, University of Alberta, Edmonton, AB
[8.] Department of Medicine and Community Health Sciences, University of Manitoba, Winnipeg, MB
[9.] Tuberculosis Program Evaluation and Research Unit, University of Alberta, Edmonton, AB
Correspondence and reprint requests: Dr. Richard Long, Room 8325, Aberhart Hospital, 11402 University Avenue, Edmonton, AB T6G 2J3, Tel: 780-407-1427, Fax: 780-407-1429, E-mail: firstname.lastname@example.org
Acknowledgements: This work was supported by a grant from the University of Alberta Hospital Foundation. The authors thank the staff of the Disease Control and Prevention Branch, Alberta Health and Wellness and the staff of the Capital and Calgary TB Clinics for their assistance in assembling the TB data, the staff of the Northern and Southern Alberta HIV/AIDS Clinics for their assistance in assembling the HIV data, and the staff of the Provincial Laboratory for Public Health and the Tuberculosis Program Evaluation and Research Unit, University of Alberta, for their assistance in cross-matching HIV and TB data. The authors also thank Jennifer Parlevliet for her assistance in preparing the manuscript.
Table 1. HIV Status of TB Patients in Alberta by Demographic Group and Disease Site, 1991-1997 (before HAART *); 1998-2002 (after HAART but before 'opt-out' testing); 2003-2006 (after 'opt-out' testing) 1991-1997 1998-2002 TB HIV HIV Cases HIV Cases Tested Positive Tested [dagger] [dagger] [dagger] TB Total 1161 134 (11.5) 13 (9.7) 683 307 (44.9) Age (yrs) 0-14 85 4 (4.7) 0 (0.00) 33 2 (6.1) 15-34 318 51 (16.0) 5 (9.8) 166 87 (52.4) 35-64 401 61 (15.2) 8 (13.1) 273 143 (52.4) > 64 357 18 (5.0) 0 (0.00) 211 75 (35.6) Gender Male 568 81 (14.3) 9 (11.1) 358 183 (51.1) Female 593 53 (8.9) 4 (7.5) 325 124 (38.2) Ethnic Group* CBO 200 26 (13.0) 4 (15.4) 100 52 (52.0) CBA 287 45 (15.4) 3 (6.7) 150 91 (60.7) FBO 628 47 (7.5) 4 (8.5) 391 142 (36.3) FBSSA 46 16(34.8) 2 (12.5) 42 22 (52.4) Disease Site Non-- 380 29 (7.6) 7 (24.1) 192 63 (32.8) respiratory Respiratory 694 88 (12.7) 4 (4.5) 442 218 (49.3) Both 87 17 (19.5) 2 (11.8) 49 26 (53.1) 2003-2006 HIV Cases HIV HIV Positive Tested Positive [dagger] [dagger] [dagger] TB Total 15 (4.9) 496 406 (81.9) 22 (5.4) Age (yrs) 0-14 0 (0.00) 19 10 (52.6) 0 (0.00) 15-34 4 (4.6) 144 131 (91.0) 6 (4.6) 35-64 11 (7.7) 198 168 (84.9) 16 (9.5) > 64 0 (0.00) 135 97 (71.9) 0 (0.00) Gender Male 15 (8.2) 251 210 (83.7) 14 (6.7) Female 0 (0.00) 245 196 (80.0) 8 (9.5) Ethnic Group* CBO 5 (9.6) 61 52 (85.3) 0 (0.00) CBA 4 (4.4) 66 58 (87.9) 5 (8.6) FBO 5 (3.5) 293 231 (78.8) 6 (2.6) FBSSA 1 (4.6) 76 65 (85.5) 11 (16.9) Disease Site Non-- 3 (4.8) 172 144 (83.7) 6 (4.2) respiratory Respiratory 7 (3.2) 283 229 (80.9) 7 (3.1) Both 5 (19.2) 41 33 (80.5) 9 (27.3) * Abbreviations: HAART Highly active anti-retroviral therapy; CBO Canadian-born 'other'; CBA Canadian-born Aboriginal; FBO foreign-born 'other'; FBSSA foreign-born sub-Saharan Africa ([dagger]) Numbers in brackets are percentages Table 2. Results of 'Post-TB' HIV Testing of Patients Aged 15-64 Who Were Either HIV Negative or HIV Untested at the Time of Diagnosis of TB, Alberta 1991-1997 (semi-selective testing years) and 1998-2002 (selective-plus testing years) * HIV Status No. of No. (%) with No. (%) No. with at Diagnosis Patients One or More with More First (or of TB 'Post-TB' Than One Subsequent) Tests 'Post-TB' 'Post-TB' Test Test Positive HIV Negative [dagger] 1991-1997 99 27 (27.3) 12 (12.1) 3 (0) 1998-2002 215 51 (23.7) 14 (6.5) 0 (1) Total 314 78 (24.8) 26 (8.3) 3 (1) HIV Untested 1991-1997 607 118 (19.4) 37 (6.1) 0 (1) 1998-2002 209 38 (18.2) 10 (4.8) 0 (0) Total 816 156 (19.1) 47 (5.8) 0 (1) * HIV test results at the time of diagnosis of TB include those reported up to 6 months before and up to 9 months after the date of diagnosis of TB; post-TB HIV test results include those reported up to the end of 2007. ([dagger]) Numbers in brackets refer to patients who had a first 'post- TB' test that was negative and then a subsequent test--i.e., subsequent to the first 'post-TB' test--that was positive. The three first 'post-TB' HIV tests that were positive were performed 3.75, 5.17, and 8.67 years after the date of diagnosis of Table 3. Demographic and Clinical Characteristics of HIV-negative and HIV-positive TB Patients, Aged 15-64 Years, Alberta, 1991-2006 HIV Negative HIV Positive Univariate n=591 n=50 OR (95% CI) Age (yrs) 15-34 254 15 1 35-64 337 35 1.76 (0.94, 3.29) Gender Male 322 38 1 Female 269 12 0.38 (0.19, 0.74) ([dagger]) Ethnic Group * CBO 83 9 1 CBA 142 12 0.78 (0.32, 1.93) FBO 283 15 0.49 (0.21, 1.16) FBSSA 82 14 1.56 (0.64, 3.79) Disease Site Non-respiratory 167 16 1 Respiratory 375 18 0.50 (0.25, 1.01) ([section]) Both 49 16 3.41 (1.59, 7.31) ([dagger]) Multivariate OR (95% CI) Age (yrs) 15-34 1 35-64 1.96 (0.96, 4.01) ([paragraph]) Gender Male 1 Female 0.42 (0.21, 0.85) ([double dagger]) Ethnic Group * CBO 1 CBA 0.69 (0.27, 1.78) FBO 0.48 (0.19, 1.20) FBSSA 2.14 (0.79, 5.84) Disease Site Non-respiratory 1 Respiratory 0.44 (0.21, 0.92) ([double dagger]) Both 3.02 (1.34, 6.78) ([dagger]) * Abbreviations: CBO Canadian-born 'Other', CBA Canadian-born Aboriginal, FBO Foreign-born 'Other', FBSSA Foreign-born sub-Saharan Africa ([dagger]) p<0.01 ([double dagger]) p<0.05 ([section]) p=0.05 ([paragraph]) p=0.07