SUMMARY
Setting:
The GHESKIO Centers (Port-au-Prince, Haiti) facilitate “test and treat” strategies by screening all patients for tuberculosis (TB) at HIV testing.
Objective:
We determined the proportion of patients with chronic cough at HIV testing who were diagnosed with TB, stratified by HIV test results. We also evaluated the additional diagnostic yield of Xpert MTB/RIF vs. sputum microscopy.
Design:
We conducted a retrospective cohort analysis including all adults who were tested for HIV at GHESKIO from August 2014 to July 2015.
Results:
Of 29,233 adult patients tested for HIV, 2953 (10%) were diagnosed as HIV-positive. Chronic cough (≥2 weeks in duration) was reported by 1116 (38%) HIV-positive patients; 984 (88%) were tested and 265 (27%) were diagnosed with TB. Chronic cough was reported by 5985 (23%) HIV-negative patients; 5654 (94%) were tested and 1179 (21%) were diagnosed with TB. Twenty-seven percent of bacteriologically-confirmed cases were smear-negative and Xpert MTB/RIF positive. Eighty-one percent of TB cases were diagnosed in patients with negative HIV tests.
Conclusions:
Screening for TB at HIV testing was high-yield, both among HIV-infected and HIV-negative individuals. Testing for both diseases should be conducted among patients who present with chronic cough at HIV testing.
Keywords: HIV, AIDS, tuberculosis, voluntary counseling and testing, Haiti
INTRODUCTION
Active case finding for tuberculosis (TB) among patients newly diagnosed with HIV has resulted in a high yield of TB diagnoses. However, though combined testing strategies have been implemented in mobile HIV testing clinics, most facility-based HIV testing centers do not conduct TB screening at the time of HIV testing.1–9 This may contribute to delays in antiretroviral therapy (ART) initiation for symptomatic patients, which is associated with loss to follow-up and increased mortality.10–13 In addition to facilitating rapid ART initiation, which is recommended by the World Health Organization (WHO), TB screening at HIV testing also provides the opportunity for rapid TB treatment initiation in co-infected patients.14 Furthermore, it facilitates early identification and isolation of infectious patients, reducing nosocomial TB transmission, and timely prescription of prophylactic therapy for HIV-infected patients without active TB.15,16 Symptomatic patients who test negative for HIV also benefit from TB testing. For achievement of the WHO End TB Strategy milestones of reducing TB incidence by 90% from 2015 to 2035, it will be essential to screen patients for TB at all health encounters in high burden settings, particularly at visits such as HIV testing, where patients may have higher risks of TB, regardless of HIV test results.17,18
Data are limited on the optimal diagnostic strategy to evaluate for TB at HIV testing. Though the WHO recommends Xpert MTB/RIF (Cepheid, Sunnyvale, California) as an initial diagnostic test for HIV-infected patients, due to superior test characteristics, data are limited on the clinical impact of replacing sputum smear microscopy with Xpert MTB/RIF testing in patients who report TB symptoms at HIV testing, regardless of HIV test results.19
At the Haitian Group for the Study of Kaposi’s Sarcoma and Opportunistic Infections (GHESKIO) Centers in Port-au-Prince, Haiti, patients have been screened for cough at the time of HIV testing for the past 20 years. In this report, we describe the proportion of patients who are diagnosed with TB at HIV testing, stratified by HIV test results. We also evaluate the proportion of patients with bacteriologically-confirmed TB with the implementation of Xpert MTB/RIF, compared to smear microscopy. In addition, we compare our results to findings from two decades ago to determine if there has been a change in the diagnostic yield of active case finding with the scale-up of ART.20
METHODS
Setting and Population
Haiti has an estimated HIV prevalence of 1.7%, and TB incidence of 188/100,000.21,22 Among patients diagnosed with TB, 15% are co-infected with HIV. GHESKIO, a Haitian non-governmental organization located in Port-au-Prince, is the largest provider of HIV and TB services in the Caribbean. GHESKIO primarily serves an impoverished urban population who live on less than $1 US per day, and provides diagnostic and treatment services for HIV, TB, and other infectious diseases free of charge. This study included patients ≥18 years of age who presented for HIV testing at GHESKIO from August 1, 2014 to July 31, 2015.
TB Screening and Diagnostic Algorithm
At pre-test HIV counseling, the social worker administered a symptom checklist, querying patients about chronic cough (cough ≥2 weeks in duration) and other TB symptoms. Individuals who reported chronic cough were separated from other patients and referred for same-day physician evaluation, which included a digital chest radiograph (CXR) on-site the same day, and sputum testing, regardless of CXR results. Smear microscopy was conducted on a spot specimen, with Xpert MTB/RIF testing on an early morning specimen, in accordance with Ministry of Health guidelines.23 Specimens were refrigerated upon collection and transported to the centralized GHESKIO biosafety-level 3 laboratory across Port-au-Prince. Spot sputum specimens were stained by the Ziehl-Neelsen method and examined by microscopy for the presence of acid-fast bacilli (AFB). The Xpert MTB/RIF test was performed directly on sputum samples according to the manufacturer’s instructions. HIV testing was conducted using rapid antibody tests (Determine, Alere, Waltham, MA),
We defined a pulmonary TB case according to WHO criteria, which included both bacteriologically-confirmed and clinically-diagnosed TB cases.24 Standard TB treatment was initiated according to WHO and national guidelines.23,25 Patients with negative sputum test results were further evaluated and treated appropriately for other conditions. Patients who were diagnosed with HIV received antiretroviral therapy at GHESKIO, according to WHO and national guidelines.26
Data Collection and Statistical Analyses
Routinely collected demographic and clinical data were extracted from patient records. De-identified data were entered into an Excel database (Microsoft, Redmond, WA) and then converted to SAS version 9.2 (SAS Institute, Inc, Cary, NC). The study was approved by Institutional Review Boards at all participating institutions.
Baseline characteristics of patients who reported chronic cough were summarized using proportions for categorical variables and medians with interquartile ranges (IQR) for continuous variables. We calculated the number needed to screen (NNS) by dividing the number of patients screened for chronic cough by the number diagnosed with TB. We calculated the number needed to test (NNT) as the number of persons tested for TB divided by the number diagnosed with TB.
We also compared the findings of our current study with those of a historical cohort to describe changes in HIV and TB prevalence using two-sample proportion tests.20 The historical cohort consisted of 1327 adults (>18 years) who presented for HIV testing at GHESKIO from January to April 1997. At that time, the HIV prevalence in Haiti was 5.2%, and the TB incidence was over 250/100,000.27,28 A total of 474 (36%) patients were diagnosed with HIV, and of these, 128 (27%) reported chronic cough, and 50 (39% of those with chronic cough) were diagnosed with TB. Of the 50 TB cases among HIV-infected patients, 25 (50%) were culture-positive and 25 (50%) were culture-negative. Among the 853 patients who were HIV-negative, 113 (13%) reported chronic cough, and 26 (23% of those with chronic cough) were diagnosed with TB. Of the 26 cases of TB among HIV-negative patients, 17 (65%) were culture-positive and 9 (35%) were culture-negative.
RESULTS
From August 1, 2014 to July 31, 2015, 29,233 adults (age ≥18 years) presented to GHESKIO for HIV testing, and 2953 (10%) were diagnosed with HIV. Among HIV-infected patients, 1116 (38%) reported chronic cough. Among the 26,039 patients who were HIV-negative, 5985 (23%) reported chronic cough. Among the 241 patients with indeterminate HIV test results, 50 (21%) reported chronic cough. Further analyses were restricted to the 7151 patients who reported chronic cough. See Table 1 for a description of their baseline demographic and clinical variables.
Table 1.
Baseline Characteristics of Patients Who Reported Cough (n=7151)
| Variable | HIV-Positive (n=1116) | HIV-Negative (n=5985) | HIV Indeterminate (n=50) | Total (n=7151) |
|---|---|---|---|---|
| Female Sex – no. (%) | 643 (58) | 3543 (59) | 29 (58) | 4215 (59) |
| Age (years) – median (IQR) | 34 (27–43) | 32 (24–47) | 32 (25–45) | 32 (24–46) |
| Annual Income ≤$150 USD* | 577 (52) | 3647 (61) | 27 (54) | 4500 (63) |
| Education – no. (%)* | ||||
| No school | 259 (23) | 1191 (20) | 11 (22) | 1461 (20) |
| Primary school | 392 (35) | 1751 (29) | 13 (26) | 2156 (30) |
| Secondary school and higher | 421 (38) | 2852 (48) | 24 (48) | 3297 (46) |
| Marital Status – no. (%)* | ||||
| Single | 414 (37) | 2777 (46) | 20 (40) | 3211 (45) |
| Married or co-habiting | 481 (43) | 2476 (41) | 26 (52) | 2983 (42) |
| Previously married | 176 (16) | 540 (9) | 2 (4) | 718 (10) |
| Place of Residence – no. (%)* | ||||
| Residence zone with a slum in PAP** | 645 (58) | 3770 (63) | 28 (56) | 4443 (62) |
| Residence zone without a slum in PAP** | 367 (33) | 1981 (33) | 21 (42) | 2369 (33) |
| Residence zone outside of PAP** | 82 (7) | 167 (3) | 0 | 249 (3) |
| Baseline CD4 count – no. (%) | ||||
| <200 cells/mm3 | 288 (26) | |||
| 200 to 350 cells/mm3 | 169 (15) | |||
| 351 to 500 cells/mm3 | 142 (13) | |||
| >500 cells/mm3 | 215 (19) | |||
| Missing*** | 302 (27) | |||
Notes:
If fewer than 5% of values were missing, then proportions were calculated without the missing values;
PAP=Port-au-Prince;
During the study period, all patients newly diagnosed with HIV did not receive CD4 count, due to a change in national guidelines to focus on HIV viral load testing over baseline CD4 count.
Of the patients reporting chronic cough, 6683 (93%) were tested for TB; this includes 984 (88%) HIV-positive and 5654 (94%) HIV-negative patients. Among the 6683 patients who received at least one test for TB, 5539 (83%) received both smear microscopy and Xpert MTB/RIF testing; 393 (6%) received smear microscopy but not Xpert MTB/RIF and 191 (3%) received Xpert MTB/RIF but not smear microscopy. Five hundred sixty (8%) patients received CXR only.
Diagnostic Yield of Testing for Tuberculosis
Overall, 6683 patients were tested for TB at the time of HIV testing and 1454 (22%) were diagnosed with active disease; 1132 cases (78%) were bacteriologically-confirmed. Among the 963 HIV-positive patients who were tested for TB, 265 (27%) were diagnosed with active TB. Of these, 163 (62%) were bacteriologically-confirmed, meaning they were smear and/or Xpert MTB/RIF positive (SS+/Bac+); the remainder were clinically diagnosed based on symptoms and CXR. Among 5654 HIV-negative patients who were tested, 1179 (21%) were diagnosed with TB (see Table 2). Of these, 963 (82%) were bacteriologically-confirmed, and the remainder were clinically diagnosed. Forty-five patients with unknown or indeterminate HIV status were tested for TB and 10 (25% of those tested) were diagnosed with TB; 6 (60%) had bacteriologically-confirmed disease.
Table 2.
Method of Tuberculosis Diagnosis, by HIV Status
| Method of Tuberculosis Diagnosis | HIV-Positive (n=2953) | HIV-Negative (n=26,039) | HIV-Indeterminate (n=241) | Total (n=29,233) |
|---|---|---|---|---|
| Patients reporting cough – no. (%) | 1116 (38%) | 5985 (23%) | 50 (21%) | 7151 (24%) |
| Patients reporting cough who were tested for TB – no. (%) | 984 (88%) | 5654 (94%) | 45 (90%) | 6683 (93%) |
| TB cases diagnosed – no. (%)* | 265 (27) | 1179 (21) | 10 (22%) | 1454 (22%) |
| Smear and Xpert positive – no. (%) | 77 (29) | 633 (54) | 4 (40) | 714 (49) |
| Smear negative and Xpert positive – no. (%) | 62 (23) | 240 (20) | 1 (10) | 303 (21) |
| Smear positive and Xpert negative – no. (%) | 3 (1) | 32 (3) | 0 (0) | 35 (2) |
| Smear positive and Xpert not done – no. (%) | 14 (5) | 33 (3) | 1 (10) | 48 (3) |
| Smear not done and Xpert positive – no. (%) | 7 (3) | 25 (2) | 0 (0) | 32 (2) |
| Clinically diagnosed – no. (%)** | 102 (38) | 216 (18) | 4 (40) | 322 (22) |
The denominator is the number of patients who were tested for TB
Of the 322 clinically diagnosed patients, 212 (66%) were smear and Xpert MTB/RIF negative; the remainder were treated empirically, without sputum testing.
Out of the 1454 TB cases diagnosed, 303 (21%) were smear-negative but Xpert MTB/RIF positive; these cases comprised 27% of all bacteriologically-confirmed TB cases. Of the 265 HIV-infected and 1179 HIV-negative patients diagnosed with TB, 62 (23%) and 240 (20%) were smear-negative but Xpert MTB/RIF positive; this comprised 38% and 25% of bacteriologically-confirmed cases, respectively.
Among the 29,233 patients who presented for HIV testing, 5% were diagnosed with TB. The number needed to screen (NNS) was 20 (11 among HIV-positive patients; 22 among HIV-negative patients) and number needed to test (NNT) was five for every patient diagnosed with TB (4 among HIV-positive patients; 5 among HIV-negative patients). Eighty-one percent of TB cases were diagnosed among patients who tested negative for HIV.
Historical comparison
The proportion of patients testing positive for HIV at GHESKIO decreased over time, from 36% in the 1997 historical cohort (pre-ART era) to 10% in the current cohort (p<0.001) (see Table 3). Among HIV-infected patients, the proportion reporting cough increased from 27% to 38% (p<0.001), but the proportion of coughing patients who were diagnosed with TB decreased from 39% to 27% (p=0.004). The overall proportion of HIV-infected patients who were diagnosed with TB was similar between the two cohorts (11% vs. 9%; p=0.158). Among HIV-negative patients, the proportion reporting cough increased from 13% to 23% (p<0.001), but the proportion of coughing patients diagnosed with TB was not significantly different (decreased from 23% to 21%; p=0.381). The overall proportion of HIV-negative patients who were diagnosed with TB increased over time, from 3% to 5% (p=0.040).
Table 3:
Proportion of Patients with Cough and Tuberculosis in Historical and Current Cohorts
| Historical Cohort (n=1327) | Current Cohort (n=29,233) | p-value | |
|---|---|---|---|
| Proportion Diagnosed with HIV | 474 (36%) | 2953/29,233 (10%) | <0.001 |
| HIV-Infected Patients | |||
| Proportion Reporting Cough | 128/474 (27%) | 1116/2953 (38%) | <0.001 |
| Proportion of Coughing Patients Diagnosed with TB* | 50/128 (39%) | 265/984 (27%) | 0.004 |
| Proportion with Bacteriological Confirmation of TB | 25/50 (50%) | 163/265 (62%) | 0.128 |
| Proportion of HIV-Infected Patients Diagnosed with TB | 50/474 (11%) | 265/2953 (9%) | 0.158 |
| HIV-Negative Patients | |||
| Proportion Reporting Cough | 113/853 (13%) | 5985/26,039 (23%) | <0.001 |
| Proportion of Coughing Patients Diagnosed with TB* | 26/113 (23%) | 1179/5654 (21%) | 0.381 |
| Proportion with Bacteriological Confirmation of TB | 17/26 (65%) | 963/1179 (82%) | 0.035 |
| Proportion of HIV-Negative Patients Diagnosed with TB | 26/853 (3%) | 1179/26,039 (5%) | 0.040 |
The denominator is the number of patients who were tested for TB
DISCUSSION
We found that screening for chronic cough at the time of HIV testing, with TB testing for symptomatic patients, was a high-yield strategy for diagnosing TB. Among all patients tested for HIV, 10% were found to be HIV-positive, and 5% were diagnosed with TB. Among coughing patients who were tested for TB, 27% of HIV-positive and 21% of HIV-negative patients were diagnosed with active TB. For each TB case detected, 20 individuals were screened for chronic cough, and five were tested for TB. Over four-fifths of TB cases were diagnosed in patients who tested negative for HIV, demonstrating the importance of testing all symptomatic patients for TB, regardless of HIV test results.
These findings are similar to the results from a separate study of active case finding for TB that we conducted over the same time period.29 A total of 7% of individuals queried for cough at the household level in several slums of Port-au-Prince reported chronic cough, and 27% of HIV-infected patients and 19% of HIV-negative patients were diagnosed with active TB.
The benefits of TB testing prior to ART initiation have been well documented, with diagnoses of active TB in up to one-third of patients in high burden settings.6,9,30 Testing for TB at HIV testing also facilitates the new WHO guidelines for rapid ART initiation.14 HIV-infected patients who are diagnosed with TB can be immediately treated for TB, reducing the risk of pre-treatment attrition, while those who are determined not to have TB can be offered ART and isoniazid prophylaxis.5–7,9–11 Furthermore, given the high rates of TB in patients with chronic cough in endemic settings, HIV testing centers may be real-time incubators of TB. The failure to conduct early TB screening may facilitate transmission of active TB to a cohort of immunosuppressed patients.
If patients testing negative for HIV are not also screened for TB symptoms, an opportunity to diagnose active TB may be lost, delaying effective therapy and leading to ongoing transmission. Yet, most patients who test negative for HIV are not screened for TB. In a systematic review of the yield of active TB case finding, only five of 601 studies included HIV VCT centers.18 These studies were conducted in Africa and Asia, and all found a benefit of screening for TB symptoms, regardless of HIV test result, with 15% to 56% of TB diagnoses occurring in patients who tested negative for HIV. This reinforces our finding of an untapped target population for integrated testing.31
Our results add to the evidence base indicating that Xpert MTB/RIF testing results in a higher proportion of patients with bacteriologic confirmation of TB, compared with sputum microscopy. We found that 25% of HIV-negative and 38% of HIV-positive patients with bacteriologically-confirmed TB were smear-negative and Xpert MTB/RIF positive. These findings support the WHO recommendation for Xpert MTB/RIF as a first-line test among HIV-infected patients, and also demonstrate the added benefit of Xpert MTB/RIF for those who test negative for HIV. The proportion of patients with bacteriologic confirmation of TB is likely to be even higher with the roll-out of the newly available Xpert MTB/RIF Ultra test, which is more sensitive than the Xpert MTB/RIF test, particularly among smear-negative and HIV-positive patients.32
The proportion of patients who test positive for HIV at GHESKIO has decreased over the past 20 years, from about 36% to about 10%, which reflects the decline in national HIV prevalence, from 5.2% to 1.7% over this time period.20,22,28 However, the proportion of HIV-infected patients who are diagnosed with TB at HIV testing has remained stable, and the proportion of HIV-negative patients diagnosed with TB at HIV testing has increased over this time period, though the estimates for national TB incidence have declined from over 250/100,000 to 188/100,000.21 The increase in the proportion of HIV-negative patients who are diagnosed with TB may be due to the high TB burden in the slum population surrounding GHESKIO, as described above, and demonstrate that screening for TB at time of HIV testing continues to be an effective strategy for detecting undiagnosed cases of TB.29 It also further highlights the need for TB screening among HIV-negative patients.
This study has several limitations. It was conducted at one site in an urban setting, which may limit generalizability of study findings. Also, GHESKIO provides integrated HIV and TB testing and treatment services. TB testing may not be feasible at all HIV testing sites. Furthermore, active TB would have been missed in patients who presented without chronic cough, potentially resulting in an under-estimation of the true burden of TB at HIV testing in this cohort.
CONCLUSION
This study emphasizes the importance of TB screening at HIV testing in high burden settings, regardless of HIV test results, and confirms the benefits of Xpert MTB/RIF testing to increase the proportion of patients with bacteriological confirmation of TB.
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