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 Table of Contents  
Year : 2019  |  Volume : 8  |  Issue : 3  |  Page : 244-251

Survival model analysis of tuberculosis treatment among patients with human immunodeficiency virus coinfection

Department of Statistics, University of Fort Hare, Alice, Eastern Cape, South Africa

Date of Web Publication12-Sep-2019

Correspondence Address:
Dr Adeboye Azeez
Department of Statistics, University of Fort Hare, P. Bag X1314, Alice, Eastern Cape
South Africa
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ijmy.ijmy_101_19

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Background: Tuberculosis (TB) with human immunodeficiency virus (HIV) coinfection is the highest clinical epidemiology and public health issue. Despite many programs established to tackle the epidemic, TB target controls have not been reached. One of the many factors attributed to the failure in TB treatment is HIV coinfection. The aim of this study is to assess the survival rate of HIV infection among TB patients and the risk factors of death among the TB patients with HIV coinfection during the retro of directly observed treatment, short-course (DOTS) program.
Methods: This study is a retrospective cohort conducted to compare the survivorship between TB/HIV patients for 8 months DOTS. Death among TB patients was considered as failures and those defaulted or survived were censored. The Cox proportional-hazards regression and log-linear model were used to establish the hazard ratio (HR) of death for each variable at baseline and estimate the risk factors effect among TB patients.
Results: The findings revealed that 50% of death from TB/HIV patients were from HIV coinfection (advanced HR = 2.01, 95% confidence interval = 1.13–3.17). The risk of death was significantly higher in HIV-positive TB patients (P = 0.000) during the extension care phase. TB/HIV-positive patients on antiretroviral therapy have decreased survival rate (log-rank test = 14.88, df = 2, P = 0.0001). The probability of TB patients surviving is significantly decreased in HIV positive with some factors such as age, weight, smoking, and alcohol found significant.
Conclusion: The probability of survival in HIV-positive TB patients was significantly lower during the TB treatment. Weight loss, age, alcohol, smoking, and pregnancy were showed to affect the survival probability of TB/HIV patients' coinfection significantly.

Keywords: Bactrim, drug-resistant, hazard ratio, tuberculosis/human immunodeficiency virus coinfection, treatment outcomes

How to cite this article:
Azeez A, Mutambayi R, Odeyemi A, Ndege J. Survival model analysis of tuberculosis treatment among patients with human immunodeficiency virus coinfection. Int J Mycobacteriol 2019;8:244-51

How to cite this URL:
Azeez A, Mutambayi R, Odeyemi A, Ndege J. Survival model analysis of tuberculosis treatment among patients with human immunodeficiency virus coinfection. Int J Mycobacteriol [serial online] 2019 [cited 2020 Sep 23];8:244-51. Available from: http://www.ijmyco.org/text.asp?2019/8/3/244/266483

  Introduction Top

Tuberculosis (TB) and human immunodeficiency virus (HIV) are both drivers of morbidity and mortality in the world.[1] TB is a universal endemic, with an estimated 9 million newly diagnosed cases and at least 1.5 million deaths by the year 2013.[2] Mycobacterium tuberculosis, Mycobacterium bovis, Mycobacterium africanum, Mycobacterium microti, and Mycobacterium canettii are the five mycobacteria responsible for TB and by far the most common.[1],[3] Human contact with M. bovis infection has reduced considerably among technologically advanced countries due to pasteurization of milk, vaccination, and relatively rare to have infection with the other organisms.[1],[4],[5],[6] The global encumbrance of TB and HIV coinfection falls heavily on poor and low-income countries, including those of Sub-Saharan African countries.[2],[7],[8]

The region of Southern Africa is the epicenter of the HIV endemic. South Africa precisely suffers the highest effect of this epidemic with an estimated figure of 6.4 millions of people living with HIV with 18.8% prevalence among the age group of 15–49 years and TB with HIV coinfection rate of >60%.[9] The problem is pronounced by the emergence of very costly and more difficult to treat drug-resistant (DR) strains of TB.[2],[10],[11],[12] Subsequently, HIV infection has resulted in diagnostic challenges as well as delays in identifying TB that intensely affects treatment outcome.[13]

The aim of TB with HIV coinfection studies is to minimize morbidity, mortality, default, relapse, and prevent DR-TB and outcomes of TB treatment.[14],[15] Most studies have demonstrated survival rate of TB treatment with HIV-positive TB patients when compared to HIV-negative TB patients,[16] and few studies have shown vital survival time of death.[17] Early diagnosis and treatment of TB are essential to prevent death from TB or its complications.[18] Even not all the aims are achieved with anti-TB drugs because M. tuberculosis strains increase the occurrence of DR and long-term TB treatment.[18],[19] TB patients who fail to complete treatment pose potential and significant public health risk through reactivation of disease, increase the progression of transmission, and DR.[20] TB/HIV patients with comorbidity diseases such as diabetes, liver diseases, renal failure, hepatitis, and silicosis were found to be associated with unsuccessful treatment.[21] Adequate supervision, monitoring, and the evaluation of patients' guarantees early detection of adverse side effects and treatment compliance of the medication.[22]

Despite the extensive of directly observed treatment, short-course (DOTS) activities in TB control and prevention, the patients sometimes fail to complete the treatment to declare cured or treatment completed.[22],[23] Patients on TB services require standardized anti-TB treatment, and at the same time, TB/HIV-positive patients also require trimethoprim-sulfamethoxazole (co-trimoxazole) prophylaxis and antiretroviral treatment (ART)[24] and should not be long to initiate after start of the treatment of anti-TB.[25],[26],[27] TB/HIV-positive patients are more challengeable to TB services, prolonged diagnostic delays, longer infections, and have poorer outcomes of TB treatment.[28]

Various studies from Sub-Saharan Africa countries were used to investigate the effect of HIV coinfection on TB treatment outcomes. In some studies, TB treatment outcomes in TB/HIV-positive patients were expounded to be poorer when compared to HIV-negative TB patients,[14],[29],[30],[31] while others found no difference between the two groups.[32],[33] ART demonstrated benefit on TB treatment outcomes in randomized controlled trials [25],[26],[27],[32],[33] and observational studies.[34],[35] Furthermore, studies of systematic review conducted in Sub-Saharan Africa revealed the benefit of ART on TB death, and showed that 71% reduction in risk of TB mortality.[36]

The aim of this study, therefore, was to establish the influence of HIV coinfection on the survivorship of patients with TB during the retro of DOTS program, to determine time to treatment lost to follow-up, to identify associated risk factors among TB patients, and to assess TB treatment outcome in association to HIV coinfection on pregnancy status and CD4 count among TB patients in Eastern Cape, South Africa.

  Methods Top

Study setting

This study was carried out at Fort Grey TB Hospital, East London, Eastern Cape in South Africa. Fort Grey TB hospital is a specialized provincial government-funded TB hospital. It was established in 1955 and used to be a SANTA TB Hospital. It is located at Farm Grey Dell Airport Phase 1, Fort Grey location, Greenfields, East London. Fort Grey TB Hospital is located 20 km from East London city and 6 km from the East London Airport. It serves the following districts: Amatole, Chris Hani, O. R Tambo, and Western District in Eastern Cape. It provides services such as ARVs, TB services, X-ray, pediatrics, and emergency services.

Tuberculosis diagnosis and treatment

South Africa Department of Health uses South Africa National TB Management Guidelines for TB program, which is a recognized international criterion for TB patients diagnosis and treatment.[1] The TB diagnosis algorithms, drug susceptibility test (DST), and patients' management on individuals who have symptoms of pulmonary TB based on the test results and examine their sputum specimen for TB disease bacteriological confirmation. Tests such as Xpert of line probe assay, culture, and DST were used for DR TB confirmation and to initiate treatment for patients with DR-TB and multi-DR-TB. For monitoring treatment progress, smear microscopy was used.

TB patients with HIV coinfection regardless of their CD4-cell count need ART. The initiation of ART is predetermined if the patient develops TB or TB presents before starting the therapy. ART was recommended according to the South African guidelines for ART, which proposed that patients with a CD4 cell counts <50 cells/μL should fast tract-start ART within 2 weeks after starting treatment of TB. Patients that have a CD4-cell count >50 cells/μL should start ART within 2–8 weeks immediately after starting TB treatment. Moreover, patients with TB meningitis regardless of CD4-cell count should suspend ART till 8 weeks after starting TB treatment.[1] The standardized regimens for anti-TB of a new TB cases for adult is the combination of isoniazid pyrazinamide, rifampicin, and ethambutol for 2 months intensive care phase followed by rifampicin plus isoniazid during 4 months follow-up care phase.[37]

Tuberculosis treatment outcome descriptions

TB treatment outcomes under the following classification: cured, failure, treatment completed, died, transferred, or defaulted [6],[8] were used in patient with TB category. Cure rates were defined as the number of smear-positive retreatment that was negative in the last month of treatment. Treatment complete referred to the total number of cured patients and those with treatment complete but were not up to the standard cure or failure. Treatment success referred to the total number of TB patients cured and have compete treatment. The loss to follow-up referred to as number of patients that smear positive for intermittent treatment for 2 months or more consecutively. Death was described as the number of TB patients that died during treatment. Failure rate is defined as number of TB patients at the end of treatment that are still smear positive. Transfer-out referred to as record of registered pulmonary TB patients transferred to another center. Not evaluated was defined as retreatment TB patients without any outcome at the end of treatment. A defaulter is a patient who left treatment for 2 or more consecutive months.[1],[8]

Study design and population

This was a retrospective cohort study conducted on record review of TB patients with HIV coinfection admitted for treatment and started ART among TB patients under DOTS program for 2013–2015. Our source population was all the TB patients registered who were placed under DOTS program for anti-TB treatment and those TB patients who started ART after tested positive to HIV. The sample size was determined using stratified random sampling technique by setting type one error at 5% probability value for TB patients lost to follow-up, power at 80% and the nonexposed ratio at 1.0.[2],[16],[38] Data were extracted using worksheets designed by the researchers. EPI Info version 7.1.5 (CDC, Atlanta, Georgia, USA) was used to minimize data entry errors. Data were analyzed using the Stata SE 13 (StataCorp., Lakeway Drive, College Station, Texas, USA) and SAS (SAS Institute Inc., Cary, NC, USA) statistical packages.

Data collection and analysis

Two stratified sampling frames were used as a tool for sample selection, in which HIV-positive and HIV-negative strata comprised 660 and 979 TB patients, respectively, registered at the hospital for treatment. TB patients of 450 each HIV positive and HIV negative under DOTS period of 7 months were randomly selected from each sampling frame using the EPI info 7.1.5 (CDC, Atlanta, Georgia, USA) from the standardized program TB register records of Fort Grey TB Hospital. Information on loss to follow-up was obtained from the patients' card. Survivor time was described as the time (days) from the date of initial treatment of TB to TB disease cured (not died) while in the case of patients who die during the treatment and/or loss to follow-up recorded in the TB register at the health center. However, the death of patients was referred to as failures and survived or defaulted patients were censored.

To determine the hazard ratio (HR) of death for the baseline predictors, Cox proportional hazards regression model was applied. Log-linear model was applied to estimate the effect of risk factors among the TB patients. Bivariate and multivariate analysis were fitted with the predictors in the Cox hazards model. Life table analysis was also used to assess the probability of DOTS survival of TB patients. The assumption of proportional of hazards was check using Schoenfeld residuals plots log (−log (st)). A 95% confidence interval and P < 0.05 for multivariate and P < 0.25 for bivariate were considered to be statistically significant. Kaplan–Meier curve and log-rank test were used to estimate survival probability graph between HIV-positive and -negative TB patients.


The study was approved by the Govan Mbeki research ethics committee of the University of Fort Hare, Alice, Eastern Cape, South Africa. Furthermore, a letter of permission to collect data was obtained from the Eastern Cape Department of Health to conduct such research in the province. Any information regarding the study participants had a number on it instead of their name and was kept confidential.

  Results Top

Descriptive statistics of the cohort

Under the DOTS program among the TB patients registered and started TB treatment from 2013 to 2015, the records of 910 TB patients (455 HIV negative and HIV positive each) were extracted from the TB treatment record used in the hospitals. From this study, 316 (69.5%) of HIV-negative and 265 (58.2%) of HIV-positive TB patients were male, 124 (27.3%) of HIV-negative and 101 (22.1%) of HIV-positive TB patients were married, 197 (43.3%) of HIV negative were from urban area, whereas 224 (49.2%) of HIV positive were from peri-urban area. The median age and weight of both HIV-negative and -positive TB patients were 38 years, 53 kg and 41 years 55 kg, respectively. Smoking was predominant among positive TB patients with 239 (52.5%) HIV-negative and 342 (74.2%) HIV-positive TB patients, respectively. Few proportion of TB patients of 29 (6.4%) HIV negative and 82 (18.0%) HIV positive were heavy users of alcohol. Fewer percentages of HIV-negative TB patients compare to HIV-positive TB patients were involved in the use of drug substance.

Out of female TB patients in the study, 102 (73.0%) HIV-negative and 94 (49.5%) HIV-positive TB patients were not on contraceptive methods. Of these, 25 (24.5%) were pregnant and 14 (13.7%) were in their menopause for HIV-negative TB patients, whereas 5 (5.3%) were pregnant and 18 (19.2%) were in their menopause for HIV-positive TB patients during the course of DOTS program. A higher proportion of HIV negative 294 (64.5%) than HIV-positive 256 (56.3%) TB patients were treated for TB as new cases TB patients' category of cohort study.

Among the TB patients with HIV positive, 240 (52.7%) were recorded to have started bactrim antibiotic treatment to prevent opportunistic infections and 158 (34.7%) were revealed to have started co-trimoxazole prophylactic therapy. In relation to ART initiation, 68 (15.2%) were identified to have started ART initiation and the rest of 386 (84.8%) were identified not have a history of ART initiation.

Time to death and survival probabilities of tuberculosis patients

It was observed that 189 deaths occurred throughout the treatment of TB. HIV-positive TB patients had the majority of death 121 (64%) and two-thirds of the deaths 127 (67.2%) were recorded during the intensive care unit of TB treatment. However, the mean and median estimation of time death for the TB patients who did not survive during TB treatment was 127.3 and 84 days, respectively [Table 1].
Table 1: Baseline information of TB/HIV co-infected patients on DOTs treatment

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During the course of intensive care unit to show the association between the time at risk of death and HIV status of TB patients, the risk associated was not significantly different between HIV-negative and HIV-positive TB patients (P < 0.02). Moreover, there was higher risk among the HIV positive during the period of intensive care unit of 13.6/1000 (61 of 447) compared to HIV negative (34 of 442) 7.7/1000, which indicates that up to half of the death recorded among HIV-positive TB patients were attributed to HIV and opportunistic infections.

The TB patients with HIV co-infections were followed up for 8 months, 68 (14.9%) of HIV negative and 121 (26.6%) of HIV-positive TB patients died and were treated in the analysis as event failure, whereas the remaining part of HIV-negative 387 (85.1%) and HIV-positive 334 (73.4%) TB patients were censored for the follow-up period with minimum follow-up period of 1 and 3 days.

Survival probabilities estimation of TB patients was done by life table analysis. At the end of the intensive care unit, the survival rate for both HIV negative and positive were 97.8% and 97.3%, respectively. The survival rate after the intensive care unit of HIV-positive TB patients reduced abruptly 84.5% within the rest of the days till the last patient was censored. In contrast, HIV-negative TB patients at the end of intensive care unit by the time all patients were censored had survival rate of 91.0% [Table 2]. In accordance with life table analysis, the Kaplan–Meier survival curve [Figure 1] indicated that survival in HIV-positive TB patients was statistically lower compared to HIV-negative TB patients (log-rank test = 14.88, df = 2, P = 0.0001).
Table 2: Survival of tuberculosis patients with human immunodeficiency virus coinfection

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Figure 1: Survival estimates by human immunodeficiency virus status of tuberculosis patients, Fort Grey Tuberculosis Hospital

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Risk of death factors of tuberculosis patients with human immunodeficiency virus coinfection on directly observed treatment, short-course

Cox proportional hazard regression model was used to analyze the association between the survival of TB patients and baseline covariates. Cox PH assumptions were checked by plotting Schoenfeld residual plot to test for independence between time and residual before fitting the covariates into the model and assessing log (log (st)) plots. The variables that violate the PH assumptions were excluded from the model. It was found that age, alcohol use, smoking, pregnancy, TB DR used, and HIV status were significantly increase the risk of death of TB patients throughout the duration of DOTS program [Table 3].
Table 3: Cox regression model (Breslow's method for ties) for risk factors of death among tuberculosis patients on directly observed treatment short-course

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The HR of HIV-positive TB patients was significantly increase the risk of being dead and more TB patients' exposure to the risk of death by 57% compared to HIV-negative TB patients. There is a low mortality rate and a longer survivor time controlling for age, which is significantly increased by about 5%. From the survival curve (adjusted) to baseline information in [Table 1], the HIV-negative TB patients' survival rate was >65% at the end of 8 months. While the median survival rate for HIV-positive TB patients was geared up to >55% at the end of the intensive care unit for all the TB patients left were censored [Figure 2].
Figure 2: Adjusted survival curve for tuberculosis patients with human immunodeficiency virus coinfection Fort Grey Tuberculosis Hospital

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  Discussion Top

TB still remains one of the major causes of preventable and treatable death in the world. The TB prevalence has exponentially increased with HIV coinfection and rated as third causes of overall maternal mortality. This study was used to assess the outcome of survival of TB patients with HIV coinfection during and after the intensive care unit of DOTS duration by evaluating the difference between the survival time of HIV negative and positive TB patients. Similarly, the study has explained the difference in significance of the time of death with HIV coinfection. The findings in this study revealed that half of the deaths recorded in HIV--positive TB patients were from HIV coinfection. HIV infection increased the progression of risk of M. tuberculosis infection and reactivated its latent by >50% periodically. This 50% of the deaths observed would not have happened if the TB patients were not HIV co-infected. The finding is similar to studies [8],[33],[34],[37] were reported to have higher overall death rate among TB patients that have coinfection with HIV.[39]

However, the result from this study showed that the probability of TB patients surviving is significantly decrease in HIV positive compared to HIV negative, which means that the rate of death is significantly increased in HIV-positive TB patients. Moreover, the median survival probability of HIV-positive TB patients when some factors such as age, weight, smoking, and alcohol were kept constant, would be 50% within the intensive care unit and eventually increases to more than 60% at the end of follow-up phase. This differs from a study conducted in rural South Africa, where the median survival probability is higher than 50% when modifiable factors are considered.[40]

Weight at baseline and HIV coinfection were seen as predictors of death among TB patients [41] through the adjusted Cox regression model. In this study, baseline weight was showed to be significantly decrease among the HIV-positive TB patients from the Cox regression model, which indicates that the risk of death from TB/HIV coinfection increase in patients with weight loss. This is similar to studies which showed that weight loss is well noticeable in patients with TB and HIV positive compared to HIV negative.[14],[42] However, weight loss opens the door for many opportunistic infections leading to the death of TB patients and can also be described by loss of energy and appetite due to the progression of HIV in TB patients.

TB and smoking were found to be independently predicting the risk of death among TB patients on DOTS from the Cox regression hazard model. The active and passive exposure to smoking is significantly associated with TB disease and death. Active smoking is significantly increased the recurrent of TB disease and death. The risk is higher in older TB patients and those children who were exposed to passive smoking. Moreover, alcohol consumption was showed not to be significantly associated with risk of TB disease, but the use of alcohol disorder is associated with some medical conditions that may weaken the immune system of TB patients with HIV coinfection with direct toxic effects. High consumption of alcohol (above 45 g alcohol/day) with or without an alcohol use disorder is associated with three risk folds of TB progression and death.[1]

The study also revealed that TB disease prevalence is significantly higher among patients with diabetes mellitus compared to patients without diabetes concomitant. The risk of death is relatively higher among TB patients with diabetes mellitus due to weak immune system. HIV infection represses the immune system in the body by decreasing the number of CD4-T cells. The results from multivariate Cox regression model summarized in [Table 4], showed that CD4 count was not significantly decrease the risk of death in TB patients due to loss of bodies' agility to avert the spread of tubercle bacilli from localized granulomas subsequently in circulating the disease. Therefore, TB disease is an agent in reducing the CD4 cells and increasing the viral load in accelerating the HIV infection progression among TB patients.[34] This finding is similar to other studies where CD4 count is not significant effect [21],[43] but differ to another study conducted in the same province.[44]
Table 4: Multivariate Cox regression model for factors associated with death among tuberculosis patients on directly observed treatment short-course

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The multivariate Cox regression model for TB patients with HIV coinfection in pregnancy was significantly increased exponentially the risk of death among TB patients. This is usually as a result to perinatal outcomes of infants born with TB diseases, which is significantly more severe particularly when the diagnosis is confirmed late in pregnancy and where the treatment of TB with HIV coinfection is poor.

  Conclusions Top

This study showed the key medium of DOTS in the formation and continuation of monitoring case system detection and TB treatment outcomes. The result from this study substantially established that the survival probability of HIV-positive TB patients was significantly lower during the period of TB treatment.[34],[39] Higher risk of death was confirmed in HIV-positive TB patients compared with HIV-negative TB patients from the intensive care and follow-up phases. Weight loss was showed as key risk factor of death in TB patients with HIV coinfection with a decreased CD4-cell count and high viral load. Age in elderly TB patients with HIV infection was significantly reduced the survival rate of the patients. Alcoholism, smoking, drug substances, and pregnancy were discovered to affect the survival probability significantly of TB/HIV patients.

Financial support and sponsorship

This study was financially supported by Govan Mbeki Research and Development Center.

Conflicts of interest

There are no conflicts of interest.

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