Burden of HIV and tuberculosis co-infection in Montreal, Quebec.
Rivest, Paul ; Sinyavskaya, Liliya ; Brassard, Paul 等
Early initiation of antiretroviral therapy in HIV-infected
individuals can improve survival outcomes (1,2) and reduce HIV
transmission. (3,4) Unfortunately in North America, there is a reported
tendency for late first presentation for HIV care. (5) In addition, a
French multicentre study asserted that 82% of HIV-positive patients who
contacted health care facilities with HIV-related conditions (6) prior
to their HIV diagnosis were not offered HIV testing at that time.
Globally, tuberculosis (TB) is the most common, potentially fatal
opportunistic infection affecting HIV-positive individuals. (7-9) HIV
increases morbidity and mortality in patients with latent and active TB.
(10-12) Failure to recognize HIV infection in TB patients in a timely
fashion leads to inadequate clinical case management. The World Health
Organization (WHO) considers HIV surveillance among TB patients as a
critical component of comprehensive HIV/AIDS care. (13)
In Canada, universal HIV testing of TB cases has been recommended
since 2002. (14,15) However, despite these recommendations, HIV-testing
report rates remain low. Thus, in 2009, there were 1,658 new active and
relapsed TB cases reported to the Canadian Tuberculosis Reporting System
(CTBRS) with a corresponding incidence rate of 4.9 per 100,000
population. HIV status was known for 650 of those cases (39%) and 9.8%
were positive. (16)
Montreal, the major Quebec census metropolitan area, accounts for
70% of all new TB cases (17) and 65% of all newly diagnosed HIV cases
(18) reported in the province.
In the current study, we quantified the proportion of TB patients
in Montreal who were tested for HIV, evaluated the burden of HIV-TB
co-infection, and examined the predictors of HIV testing at time of TB
diagnosis.
METHODS
Data source
In Quebec, it is mandatory to report incident TB cases. In
Montreal, each case is assigned to the nurse case manager at the public
health department (Direction de sante publique, DSP) and standardized
information on clinical, epidemiological, and socio-demographic
characteristics is collected. The nurse also ensures that adequate
treatment is initiated according to baseline drug sensitivities of the
Mycobacterium tuberculosis (MTB) isolate, verifies patient adherence to
treatment and initiates contact investigation.
All incident cases reported from January 1, 2004 to December 31,
2009, confirmed by culture or diagnosed on the basis of clinical and
radiological signs were retrieved for analysis. Data were also extracted
on demographic characteristics, clinical information, HIV testing and
HIV status, as well as on medical and socio-behavioural HIV or TB risk
factors.
Statistical analysis
The outcome variables were reported HIV testing, HIV testing at the
time of TB diagnosis, and HIV status. For this analysis, site of TB
infection was classified as pulmonary if any part of the lungs was
affected, including miliary TB. Patients' countries of birth were
grouped according to geographical region. If patient data were missing
on any HIV or TB risk factor of interest (alcohol abuse, intravenous
drug use (IV drug use), history of incarceration and/or homelessness,
close contact with an active TB case and co-morbidities such as cancer,
diabetes, silicosis, and renal insufficiency), the patients were
classified as not having this risk factor.
Descriptive summary statistics were presented as median and
interquartile range (IQR) for continuous variables, and as frequencies
and percentages for categorical variables. Chi-square, Fisher's
exact tests and Student's t-test were used to evaluate univariate
associations according to level of measurement.
For the HIV prevalence analysis, rates with 95% confidence
intervals (CI) were estimated for TB cases with reported HIV status and
for all incident TB cases. Among the latter, patients for whom
information on HIV testing was missing were assumed to be HIV negative.
Unconditional logistic regression was performed to examine the
effects of various patient characteristics on likelihood of HIV testing
at time of TB diagnosis. Variables that showed statistical significance
at p<0.05 in the univariate analysis were included in the final model
(region of birth, site of infection, IV drug use, year of TB diagnosis,
and reported co-morbidities). The variables sex and age were included in
the final model irrespective of their strength of association. Crude
odds ratios (OR) and adjusted odds ratios (AOR) with 95% CI were
estimated. HIV testing at time of TB diagnosis was defined as testing
done in a time interval from one month before to six months after date
of TB diagnosis, that is, HIV testing done around the time of initial
clinical investigation for TB and at any time throughout the standard TB
treatment period. Ninety-six cases with reported HIV testing but for
whom information on the date of the test was missing, as well as seven
cases known to be HIV-positive prior to TB diagnosis were excluded from
the analysis.
[FIGURE 1 OMITTED]
A chi-squared test for trends was performed on the annual
proportions of HIV-tested and HIV-positive cases over the study period.
Data were analyzed using SAS software (version 9.3, SAS Institute, Cary,
NC).
This evaluation of the DSP's surveillance program did not
require ethics approval.
RESULTS
A total of 778 incident TB cases were reported to Montreal's
DSP during the study period, 54.2% of whom were male. Median age was
38.0 (IQR: 28.0-57.0). There were 104 Canadian-born non-Aboriginal and 4
Canadian-born Aboriginal TB cases. Cases born in Canada made up 13.9% of
the study population. The majority of TB cases were foreign-born and
came from Asia (35.2%), Sub-Saharan Africa (15.4%), the Caribbean
(13.1%), Europe (8.5%), the Middle East and North Africa (5.9%), Central
or South America (3.6%), or other regions (4.4%). Among all cases, 93.2%
of TB diagnoses were confirmed microbiologically, 70.7% of cases had
pulmonary disease and 14.5% had at least one recorded HIV or TB risk
factor (Table 1).
Overall, HIV testing was reported for 50.8% (n=395) of TB incident
cases. The proportion of HIV-tested cases significantly increased from
43% in 2004 to 70% in 2009 (p<0.001) (Figure 1). Information on HIV
status was available for 90% of those for whom HIV testing was reported.
Of 39 HIV-tested cases but for whom information of HIV status was
missing, 35 (85.9%) were immigrants and 22 (56.4%) female, the median
age was 33.0 years (IQR: 25.0-47.0).
Of the 356 TB cases for whom HIV status had been reported, 33
(9.3%; 95% CI: 6.2-12.3) had HIV infection, that is, 4.2% (95% CI:
2.8-5.7) of the overall cohort. There was no significant change in the
annual prevalence of HIV-TB co-infected cases among all new TB patients
over the study period (p=0.6) (Table 2). The median age of HIV-positive
individuals was 39.0 years (IQR: 32.0-48.0), and there were 3.7 times
more men than women. Among the overall cohort of incident TB cases, HIV
prevalence was higher in those originating from high HIV burden
countries: 14.2% (95% CI: 7.8-20.5) of individuals from Sub-Saharan
Africa and 8.8% (95% CI: 3.2-14.4) from the Caribbean were HIV positive.
HIV prevalence in Canadian-born incident TB patients was 3.7% (95% CI:
0.1-7.3). There were no HIV-positive TB cases among Aboriginals, and
those originating from Central or South America, Europe, the Middle East
and North Africa, or those from the group of countries classified as
unknown/other (Table 3).
A total of 675 incident TB cases were included in the analysis on
predictors of HIV testing at time of TB diagnosis (Table 4). The 96
cases with reported HIV testing but with missing values on the date of
the test were compared to the cases for whom information on the date of
HIV test was available. There were no significant differences in
distribution by age, sex and ethnicity between the groups.
Estimated crude odds ratios for likelihood of HIV testing at time
of TB diagnosis were significant for age, region of birth, site of
infection, reported history of IV drug use and reported presence of
co-morbidities (Table 1).
Adjusted regression analysis revealed that the likelihood of being
tested for HIV at time of TB diagnosis declines with increasing age.
Thus, compared with those aged 30-39, cases aged 50-59 years and 60
years or older were 2.5 and 5 times less likely, respectively, to have
been tested for HIV (adjusted odds ratio (AOR) = 0.4; 95% CI: 0.2-0.7
and AOR = 0.2; 95% CI: 0.1-0.3, respectively) (Table 1). Subjects born
in the Caribbean (AOR = 2.6; 95% CI: 1.3-5.5), Central or South America
(AOR = 3.7; 95% CI: 1.3-10.7) and Sub-Saharan Africa (AOR = 2.5; 95% CI:
1.2-5.3) were more likely to be tested for HIV than Canadian-born cases.
Cases with pulmonary TB had a higher likelihood of being tested than
cases with extrapulmonary TB (AOR = 4.5; 95% CI: 2.9-6.9). Injection
drug users were 4 times more likely to undergo HIV testing than nonusers
(AOR = 4.0; 95% CI: 1.2-13.4) (Table 1).
DISCUSSION
In 2004-2009, an average of 50.8% of incident TB cases had reported
HIV testing in Montreal. The proportion of cases with reported HIV
testing rose significantly during the study period and reached 70% in
2009. However, the actual proportion of TB cases tested for HIV may
differ: in our study no medical file reviews were performed by the case
managers, who had to rely on information given by various sources (e.g.,
treating physicians, TB clinic nurses or the patients themselves).
Furthermore, information on the date of the test was missing for 24% of
individuals tested, and information on HIV test results had not been
recorded for 10% of HIV-tested TB cases. Case managers should direct
more efforts towards the immigrants as this group had the most missing
data. Since 2002, Citizenship and Immigration Canada (CIC) has required
mandatory HIV testing as a part of the Immigration Medical Examination
for immigrants and refugees. (19) However, during our study period, the
transfer of information from CIC to the Montreal DSP was not effectuated
and thus our figures on HIV prevalence are likely underestimated.
Based on the information available, HIV prevalence among the
overall cohort of incident TB cases was 4.2% (95% CI: 2.8-5.7) with no
significant change from 2004 to 2009, a figure substantially higher than
the estimated national HIV prevalence (208.0 per 100,000). (20) There
were almost 4 times more men than women among HIV-infected TB cases,
which is consistent with Canadian estimates. (5)
In 2004-2009, HIV prevalence among all incident TB cases was
positively correlated with patient age up to 60 years, after which it
fell significantly. Although patients aged 50-59 were less likely to be
tested, the age-specific HIV prevalence was high in this group. This is
consistent with the results of the North American AIDS Cohort
Collaboration on Research and Design (NA-ACCORD) study, which
demonstrated that from 1997 to 2007 there was an increase in the
proportion of newly diagnosed HIV-infected individuals over 50 years
old. (21) In our study, burden of infection remains high in vulnerable
populations, that is, those who reported alcohol abuse, history of IV
drug use, homelessness and detention at a correctional facility. HIV
prevalence was higher among foreign-born cases originating from the
HIV-endemic regions of Sub-Saharan Africa and the Caribbean. Of the 33
HIV-positive TB cases, 29 (87.9%) were immigrants. Among the latter, 7
cases had a known positive HIV status before TB diagnosis. Although we
were unable to get information on clinical management of their HIV
infections, these cases could be regarded as missed opportunities for TB
prevention.
Our study shows that despite likely improvements in physician
compliance with Canadian standards, targeted HIV testing remains. At the
time of TB diagnosis, physicians are more likely to order an HIV test if
a patient reports a history of IV drug use or originates from
Sub-Saharan Africa, the Caribbean, South or Central America. Although
reporting requirements in Montreal do not differ according to site of
TB, case managers carry out less extensive follow-up procedures in terms
of contact investigation and detailed clinical management, including HIV
testing and HIV status, for extrapulmonary forms of TB. Thus, missing
information could introduce a potential misclassification of
non-HIV-tested extrapulmonary TB patients; it could also partially
explain why patients with pulmonary disease had higher odds of being
tested for HIV compared to those with extrapulmonary TB, which
contradicts what has been reported elsewhere. (22)
Patient selection was similar in a study analyzing screening
practices for TB among HIV-infected patients in a Montreal HIV clinic.
Despite acknowledging HIV patients as a target group for universal
latent TB screening, clinicians were more likely to test those
originating from WHO-recognized high-burden TB countries or HIV-endemic
countries. (23)
Overall, knowledge of HIV status of TB cases has risen in Montreal
over the period 2004-2009. This may be due to continual improvement in
screening practices and surveillance (better data entry, collection of
information from TB patients, reporting of HIV status by clinicians).
However, screening rates are most likely still below target values.
Although it may be desirable to promote universal HIV screening of TB
patients, our data tend to indicate that the current targeted testing
seems to identify most of the TBHIV co-infections as the rates of
overall co-infected cases remained stable regardless of a notable
increase in reported screening. Nonetheless, enhanced reporting of
information concerning TB cases, including information on HIV status, is
essential to efficiently monitor the burden of dual infection and to
plan and evaluate programs for control and prevention.
Conflict of Interest: None to declare.
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Received: October 2, 2013
Accepted: May 5, 2014
Paul Rivest, MD, MSc, [1,2] Liliya Sinyavskaya, mph, [3] Paul
Brassard, MD, MSc [3]
Author Affiliations
[1.] Direction de sante publique, Agence de la sante et des
services sociaux de Montreal, Montreal, QC
[2.] Departement de Medecine Sociale et Preventive, Universite de
Montreal, Montreal, QC
[3.] Centre for Clinical Epidemiology, Lady Davis Research
Institute, Jewish General Hospital, Montreal, QC
Correspondence: Dr. Paul Brassard, Centre for Clinical Epidemiology
and Community Studies, JGH, 3755 Cote Ste-Catherine, H-424, Montreal, QC
H3T 1E2, Tel: 514-340-7563, E-mail: paul.brassard@mcgill.ca
Table 1. Characteristics of TB cases, proportion tested for
HIV infection and factors associated with HIV testing, Montreal,
2004-2009
Characteristic Number (%) % tested for HIV
Sex
Male 422 (54.2) 53.6
Female 356 (45.8) 47.5
Age group * (years)
0-18 34 (4.4) 55.9
19-29 183 (23.5) 56.3
30-39 186 (23.9) 64.0
40-49 119 (15.3) 61.3
50-59 84 (10.8) 46.4
60 and over 172 (22.1) 24.4
Region of birth *
Asia 274 (35.2) 46.7
Caribbean 102 (13.1) 58.8
Central/South America 28 (3.6) 67.9
Europe 66 (8.5) 43.9
Middle East/North Africa 46 (5.9) 47.8
Canada 108 (13.9) 39.0
Sub-Saharan Africa 120 (15.4) 70.0
Unknown/Other 34 (4.4) 32.4
TB status ([dagger])
Positive culture 701 (93.2) 50.8
Negative culture 51 (6.8) 47.1
Infection site *
Pulmonary 550 (70.7) 57.6
Other 228 (29.3) 34.2
Alcohol use 37 (4.8) 62.2
IV drug use * 25 (3.2) 80.0
Incarceration 10 (1.3) 50.0
Homelessness 10 (1.3) 70.0
Recent TB exposure 65 (8.3) 58.5
Co-morbidities * 90 (11.6) 36.7
Total 778 (100) 50.8
Characteristic OR (95% CI) AOR (95% CI)
([double dagger]) ([double dagger])
Sex
Male 1.2 (0.9-1.7) 1.0 (0.7-1.4)
Female Reference Reference
Age group * (years)
0-18 0.8 (0.4-1.8) 0.6 (0.3-1.7)
19-29 0.8 (0.5-1.3) 0.7 (0.4-1.1)
30-39 Reference Reference
40-49 0.6 (0.4-1.1) 0.6 (0.3-1.001)
50-59 0.4 (0.2-0.8) 0.4 (0.2-0.7)
60 and over 0.2 (0.1-0.4) 0.2 (0.1-0.3)
Region of birth *
Asia 1.6 (0.9-2.6) 1.6 (0.9-3.0)
Caribbean 2.4 (1.3-4.5) 2.6 (1.3-5.5)
Central/South America 4.8 (1.9-12.1) 3.7 (1.3 -10.7)
Europe 1.4 (0.7-2.9) 2.1 (0.9-4.9)
Middle East/North Africa 1.5 (0.7-3.3) 1.2 (0.5-2.9)
Canada Reference Reference
Sub-Saharan Africa 3.4 (1.9-6.3) 2.5 (1.2-5.3)
Unknown/Other 1.2 (0.5-2.8) 1.4 (0.5-4.0)
TB status ([dagger])
Positive culture 1.7 (0.9-3.4)
Negative culture Reference
Infection site *
Pulmonary 3.7 (2.5-5.4) 4.5 (2.9-6.9)
Other Reference Reference
Alcohol use 1.3 (0.6-2.8)
IV drug use * 3.7 (1.3-10.7) 4.0 (1.2-13.4)
Incarceration 0.6 (0.1-3.1)
Homelessness 1.5 (0.3-7.5)
Recent TB exposure 1.4 (0.8-2.4)
Co-morbidities * 0.5 (0.3-0.8) 1.0 (0.5-1.8)
Total
* p<0.05.
([dagger]) 26 values were missing.
([double dagger]) Number of cases in the analysis is 675.
Table 2. Incident TB-HIV co-infected cases by year,
Montreal, 2004-2009
2004 2005 2006 2007
N 5 5 4 7
% among TB cases with 9.8 10.2 7.7 12.3
reported HIV testing
% among all TB cases 3.8 3.8 2.9 5.5
2008 2009 p *
N 8 4 --
% among TB cases with 11.0 5.4 0.60
reported HIV testing
% among all TB cases 6.1 3.4 0.60
* Chi-squared test for trend.
Table 3. Rates of HIV seroprevalence among TB cases,
Montreal, 2004-2009
Characteristic Cases with HIV
reported positive
HIV status
N N
Sex
Female 147 7
Male 209 26
Age group (years)
0-29 108 7
30-39 107 10
40-49 66 9
50-59 35 6
60 and over 40 1
Region of birth
Asia 113 3
Caribbean 54 9
Central/South America 18 0
Europe 26 0
Middle East/North Africa 18 0
Canada 39 4
Sub-Saharan Africa 80 17
Unknown/Other 8 0
TB status *
Positive culture 320 30
Negative culture 22 0
Infection site
Pulmonary 287 28
Other 69 5
Alcohol use 21 3
IV drug use 18 3
Incarceration 4 1
Homelessness 6 3
Recent TB exposure 35 1
Co-morbidities 30 7
Total 356 33
Characteristic HIV positive HIV positive
among cases among all
with reported incident TB
HIV status cases
% (95% CI) % (95% CI)
Sex
Female 4.8 (1.3-8.2) 2.0 (0.5-3.4)
Male 12.4 (7.9-17.0) 6.2 (3.9-8.5)
Age group (years)
0-29 6.5 (1.8-11.2) 3.2 (0.9-5.6)
30-39 9.3 (3.7-15.0) 5.4 (2.1-8.6)
40-49 13.6 (5.1-22.1) 7.6 (2.7-12.3)
50-59 17.1 (4.0-30.3) 7.1 (1.5-12.8)
60 and over 2.5 (0.0-7.6) 0.6 (0.0-1.7)
Region of birth
Asia 2.7 (0.0-5.7) 1.1 (0.0-2.3)
Caribbean 16.7 (6.4-26.9) 8.8 (3.2-14.4)
Central/South America
Europe
Middle East/North Africa
Canada 10.3 (0.3-20.2) 3.7 (0.1-7.3)
Sub-Saharan Africa 21.3 (12.1-30.4) 14.2 (7.8-20.5)
Unknown/Other
TB status *
Positive culture 9.4 (6.2-12.6) 4.3 (2.8-5.8)
Negative culture
Infection site
Pulmonary 9.8 (6.3-13.2) 5.1 (3.2-6.9)
Other 7.3 (1.0-13.5) 2.2 (0.3-4.1)
Alcohol use 14.3 (0.0-30.6) 8.1 (0.0-17.3)
IV drug use 16.7 (0.0-35.7) 12.0 (0.0-25.7)
Incarceration 25.0 (0.0-100.0) 10.0 (0.0-32.6)
Homelessness 50.0 (0.0-100.0) 30.0 (0.0-64.6)
Recent TB exposure 2.9 (0.0-8.7) 1.5 (0.0-4.6)
Co-morbidities 23.3 (7.3-39.4) 7.8 (2.1-13.4)
Total 9.3 (6.2-12.3) 4.2 (2.8-5.7)
* 26 values were missing for all patients and 14 for those with
reported HIV test results.
Table 4. Partition of reported incident TB cases for the analysis of
predictors of HIV testing at the time of TB diagnosis, Montreal,
2004-2009
Reported HIV Excluded from
testing at the analysis
the time of
TB diagnosis
Yes No
HIV testing done from 1 month 270
before to 6 months after TB
HIV (+) cases with HIV testing 7
more than 1 month before TB
HIV (-) cases with HIV testing 17
more than 1 month before TB
HIV testing more than 6 months 5
after TB
Reported HIV testing, but 96
missing information of the
date of the test
No reported HIV testing 383
Total 270 405 103
