Predictors of early mortality in Human Immunodeficiency Virus (HIV)-tuberculosis co-infection

Abstract

Background

This study aimed to identify people living with HIV (PLWH) with tuberculosis (TB) co-infection, explore their demographic and clinical characteristics, and determine predictors of early mortality within 6 months of TB diagnosis.

Methods

A cross-sectional study was conducted in a tertiary referral center in Türkiye of PLWH diagnosed with TB between 2004 and 2023. Demographic, clinical, and laboratory data were reviewed, and statistical analyses were performed to identify early mortality predictors.

Results

Among 1541 PLWH, 62 (4%) had TB, and 23 (37%) died within 6 months. TB presentations were pulmonary (44%), extrapulmonary (27%), and both (29%). Predictors significantly associated with early mortality included lymphopenia (p = 0.009), a CD4 + T lymphocyte count ≤50 cells/mm³ (p = 0.015), anemia (p = 0.009), and thrombocytopenia (p = 0.034), particularly platelet counts below 150,000/mm³ (p = 0.001). Clinical predictors also included symptoms such as fever (p = 0.017), anorexia (p = 0.012), weight loss (p = 0.012), and altered mental status (p = 0.043). Additionally, receiver operating characteristic (ROC) analysis demonstrated that CD4 + T lymphocyte count ≤50 cells/mm³ (AUC = 0.76, p = 0.039) and platelet count <150,000/mm³ (AUC = 0.71, p = 0.034) were significant predictive cutoffs for early mortality. TB culture positivity was high (84%), while PCR positivity was low (15%). Opportunistic infections were seen in 11% of cases.

Conclusions

High early mortality among people living with HIV/TB co-infection is associated with advanced immunosuppression and hematological abnormalities. These results highlight the importance of early HIV detection and close clinical monitoring to reduce mortality.

Keywords

HIV tuberculosis mortality

Introduction

Tuberculosis (TB) remains one of the leading chronic infectious diseases associated with high mortality and severe outcomes, especially among people living with HIV (Human Immunodeficiency Virus) (PLWH). Current guidelines recommend routine HIV testing and counseling for all individuals diagnosed with tuberculosis. In people living with HIV/TB co-infection, initiation of antiretroviral therapy (ART) is essential for effective management and improved outcomes.^1,2

More than 10 million people continue to fall ill with TB every year and the number has been rising since 2021. TB co-infection continues to represent a substantial public health burden among PLWH particularly in low and middle income countries where both infections are highly prevalent. Immunosuppression caused by HIV increases the risk of progression from latent to active TB and worsens clinical outcomes, including mortality. According to the World Health Organization’s (WHO) Global TB Report 2023, approximately 10.6 million new TB cases were diagnosed in 2022, with 7% of these occurring in PLWH. Furthermore, of the estimated 1.3 million TB-related deaths reported globally that year, 13% (167,000) were among PLWH, underscoring the deadly synergy between these two infections.³ Despite advancements in diagnostic tools and the scale-up of ART, TB remains the leading cause of death among PLWH, highlighting the need for integrated, timely, and patient-centered approaches to diagnosis, treatment, and prevention.

Among PLWH, the annual risk of developing active TB following latent TB infection is approximately 10% (ranging from 3% to 21%), with HIV infection recognized as the most significant risk factor for disease progression. The likelihood of TB reactivation increases as immunosuppression progresses. Even with the initiation and maintenance of effective ART, PLWH continue to face a substantially higher risk of developing TB compared to the general population.⁴ In Türkiye, although the incidence of tuberculosis has steadily declined, the number of newly diagnosed HIV cases has increased significantly, rising from 2687 in 2016 to 5710 in 2022. As of 2021, the estimated prevalence of HIV among TB patients was approximately 1%.⁵

This study aimed to identify cases of HIV/TB co-infection among PLWH explore their demographic and clinical characteristics, and determine the predictors of early mortality within this population.

Methods

This study was conducted with the approval of the Ethics Committee for Clinical Researches at University of Health Sciences Haseki Training and Research Hospital, Istanbul, Türkiye (desicion no: 153-2023, date: 20.09.2023).

Study design and data collection

We conducted a preliminary analysis of a cross-sectional study on TB co-infection in PLWH based at a single center in Istanbul, Türkiye. The aim of the study was to identify predictors associated with early non-traumatic mortality within 6 months following an HIV/TB co-infection diagnosis. The study included 62 PLWH who were diagnosed and treated for TB between January 2004 and January 2023, and were followed for mortality until August 2023. The inclusion criteria required participants to be 18 years of age or older, have a confirmed diagnosis of TB among PLWH, and have complete medical records available for review. Patients who were not followed for at least 1 year after HIV diagnosis or had missing key clinical data were excluded from the study. (Figure 1).

Figure 1.

Participant selection for the HIV/TB co-infection.

CD4 + T lymphocyte count below 50 cells/µL was considered indicative of advanced HIV disease.⁶ Thrombocytopenia was defined as a platelet count <150,000/mm³, consistent with standard hematologic criteria.⁷

Case definition

The diagnosis of TB in PLWH was established based on strong clinical evidence consistent with active TB such as cough lasting more than 2 weeks, fever, night sweats, anorexia, weight loss, fatigue, headache, mental status changes, chest pain, lymphadenopathy, and supportive radiological findings along with at least one of the following diagnostic criteria: 1) The microbiological diagnosis was made using acid-fast bacilli (AFB) smear microscopy, nucleic acid amplification (NAA) testing (including GeneXpert MTB/RIF and GeneXpert MTB/RIF Ultra), and isolation of Mycobacterium tuberculosis from body fluids (e.g., sputum, bronchoalveolar lavage, pleural fluid) or tissues (e.g., biopsy specimens). 2) Pathological criterion: AFB detection from clinical samples (fluids or tissues) was performed using the Ehrlich–Ziehl–Neelsen (EZN) staining method. M. tuberculosis cultures were grown on Löwenstein–Jensen (LJ) medium and in Mycobacterial Growth Indicator Tubes (MGIT; Becton Dickinson). Additionally, M. tuberculosis DNA was detected using polymerase chain reaction (PCR). 3) A combination of pathological and microbiological criteria: AFB detection from clinical samples (fluids or tissues) was performed using the EZN staining method. M. tuberculosis cultures were grown on LJ medium and in MGIT. Additionally, M. tuberculosis DNA was detected using PCR.⁸

A case was classified as TB when a clinician established the diagnosis based on clinical and radiological findings and initiated a full course of anti-TB therapy, even in the absence of microbiological or pathological confirmation. Consequently, all PLWH for whom the clinician commenced anti-TB treatment were considered to have HIV/TB co-infection.

Tuberculosis clinical presentations were categorized based on the Centers for Disease Control and Prevention (CDC) guidelines into three groups: pulmonary TB, extrapulmonary TB (EPTB), and combined pulmonary and extrapulmonary TB.⁹

Mortality was recorded via identity numbers of the patients using the National Death Certificate Database (https://obs. saglik.gov.tr).

Statistical analysis

Data were evaluated in the IBM Statistical Package for Social Sciences Statistics 25.0 statistical package program. For descriptive statistics, continuous variables were expressed as mean ± standard deviation (SD) or as median with interquartile range (IQR) when appropriate, depending on the distribution of the data. Categorical variables were presented as frequencies (n) and percentages (%). The chi-square test was used to evaluate associations between categorical variables. For continuous variables, group comparisons were performed using the independent samples t-test for normally distributed data and the Mann–Whitney U test for non-normally distributed data. A p-value <0.05 was considered statistically significant.

Results

Over the 19 years, TB occurred in 62 (4%) of 1541 PLWH under follow-up. Among the 62 patients, 23 (37%) died, while 39 (63%) survived first 6 months after TB diagnosis. The median age at TB diagnosis was 39.5 years (range,30-47). Most patients were male (89%) and of Türkiye origin (89%). Of the TB diagnoses, 44% were pulmonary, 27% extrapulmonary, and 29% involved both forms. 13 percent developed TB before starting ART, while 11% developed TB despite already being on ART. Early mortality was more frequent among those who developed TB without ART (22%) compared with those who presented with TB at HIV diagnosis (70% of deaths occurred in this group). PLWH who developed TB under ART represented a smaller proportion of both deceased (9%) and surviving individuals (13%). The initiation of ART after tuberculosis treatment varied considerably across the study. In most PLWH, ART was started within 2–12 weeks following the initiation of anti-TB therapy. However, due to the long study period and changes in treatment practices over time, some patients experienced substantial delays. In certain cases, ART was initiated several years later, with the longest interval being a 5-years delay after starting TB treatment.

Univariable analysis identified several significant perdictors of mortality fever (p = 0.017), anorexia (p = 0.012), weight loss (p = 0.012), fatigue (p = 0.021), headache (p = 0.010), altered consciousness (p = 0.043). Among all people living with HIV/TB co-infection (n = 62), the majority (76%) were diagnosed with HIV at the time they presented with tuberculosis. Clinical and and demographic characteristics at admission are summarized in Table 1.

Table 1.

Initial clinical and demographic features of people living with HIV/TB co-infection.

Characteristic	All patients n = 62	Deceased patients, n = 23	Survived patients, n = 39	p-value*
Age (at the time of TB diagnosis) median (Q1-Q3)	39.5 (30-47)	39.0 (29-48)	40.0 (30-46)	0.977†
Sex				1.000
Female	7 (11%)	3 (13%)	4 (10%)
Male	55 (89%)	20 (87%)	35 (89%)
Nationality				1.000
Turkish	55 (89%)	21 (91%)	34 (87%)
Non-Turkish	7 (11%)	2 (9%)	5 (13%)
Transmission route				0.449
Heterosexual	23 (61%)	9 (75%)	14 (54%)
Homosexual	11 (29%)	2 (17%)	9 (35%)
Bisexual	4 (11%)	1 (8%)	3 (12%)
HIV/TB co-infection				0.270
HIV presented with TB	47 (76%)	16 (70%)	31 (80%)
TB developed without ART	8 (13%)	5 (22%)	3 (8%)
TB developed under ART	7 (11%)	2 (9%)	5 (13%)
Clinical form				0.157
Only pulmonary	27 (44%)	8 (35%)	19 (49%)
Only extrapulmonary	17 (27%)	5 (22%)	12 (31%)
Pulmonary and extrapulmonary	18 (29%)	10 (44%)	8 (21%)
Clinical manifestations
Cough	43 (69%)	19 (83%)	24 (62%)	0.096
Fever	45 (73%)	21 (91%)	24 (62%)	0.017
Anorexia	41 (66%)	20 (87%)	21 (54%)	0.012
Weight loss	41 (66%)	20 (87%)	21 (54%)	0.012
Fatigue	54 (87%)	23 (100%)	31 (80%)	0.021
Headache	9 (15%)	7 (30%)	2 (5%)	0.010
Mental changes	8 (13%)	6 (26%)	2 (5%)	0.043
Hemoptysis	2 (3%)	0 (0%)	2 (5%)	0.526
Dyspnea	4 (7%)	2 (9%)	2 (5%)	0.623
Neck stiffness	2 (3%)	2 (9%)	0 (0%)	0.134
Generalized lymphadenopathy	19 (31%)	7 (30%)	12 (31%)	1.000

P-values calculated using Chi-square test (*) for categorical variables and Mann-Whitney U test (†) for continuous variables. Significance set at p < 0.05. The bold values indicate statistically significant p-values.

Abbreviations: ART: antiretroviral therapy; Q1-Q3, interquartile range; TB: tuberculosis.

Early mortality was found to be higher among PLWH who had lymphopenia (p = 0.009) and CD4 + T lymphocyte count of ≤50 cells/mm³ (p = 0.015) at the time of TB diagnosis, as well as those with anemia (p = 0.009), low platelet levels (p = 0.003), particularly when platelet counts were <150,000/ml (p = 0.001). Laboratory characteristics at admission are summarized in Table 2.

Table 2.

Baseline laboratory profile of people living with HIV/TB co-infection.

Characteristic	All patients n = 62	Deceased patients, n = 23	Survived patients, n = 39	p-value
HIV RNA (IU/mL), median (Q1-Q3)	581933.0 (146094.0-2347206.0)	698562.0 (148727.0-3472569.5)	550000.0 (158600.0-1434591.5)	0.347†
HIV RNA level (copies/mL)				1.000*
<100,000	12 (19%)	4 (17%)	8 (21%)
≥100,000	50 (81%)	19 (83%)	31 (80%)
CD4 + T lymphocyte count (cells/mm3), median (Q1-Q3)	109.0 (39.0-249.8)	38.0 (19.0-121.5)	164.0 (62.5-298.0)	0.005†
CD4 + T lymphocyte count (cells/mm3)				0.015*
≤50	22 (36%)	13 (57%)	9 (23%)
>50; ≤200	17 (27%)	6 (26%)	11 (28%)
>200	23 (37%)	4 (17%)	19 (49%)
Hemoglobin, median (Q1-Q3)	11.7 (10.2-13.3)	11.1 (10.3-12.4)	12.4 (10.2-13.6)	0.107†
Anemia (Hgb male < 13 g/dl, female <12)	44 (71%)	21 (91%)	23 (59%)	0.009*
Leukocyte (/ml), median (Q1-Q3)	5050.0 (3450.0-8150.0)	4100.0 (2350.0-4760.0)	6400.0 (4550.0-8215.0)	0.020†
Leukopenia (<4000/ml)	19 (31%)	10 (44%)	9 (23%)	0.153*
Lymphocyte (/ml), median (Q1-Q3)	960.0 (427.5-1717.5)	530.0 (185.0-1225.0)	1160.0 (725.0-1970.0)	0.009†
Lymphopenia (<1000/ml)	33 (53%)	16 (70%)	17 (44%)	0.066*
Platelet (/ml), median (Q1-Q3)	228500.0 (121750.0-289500.0)	120000.0 (87500.0-233000.0)	252000.0 (177500.0-316000.0)	0.003†
Thrombocytopenia (<150.000/ml)	19 (31%)	13 (57%)	6 (15%)	0.001*
ALT, median (Q1-Q3)	23.0 (16.2-28.8)	24.0 (17.5-34.0)	22.0 (16.0-27.0)	0.422†
Albumin (g/dL), median (Q1-Q3)	3.0 (2.6-3.7)	2.8 (2.5-3.5)	3.0 (2.8-3.7)	0.170†
Hypoalbuminemia (<3.5 g/dL)	45 (73%)	17 (74%)	28 (72%)	1.000*
CRP (mg/L), median (Q1-Q3)	23.5 (8.0-61.8)	24.0 (10.5-72.5)	23.0 (7.0-60.5)	0.827†
ESR (mm/h), median (Q1-Q3)	62.5 (48.2-77.5)	66.0 (49.5-83.0)	59.0 (47.5-75.5)	0.521†

P-values calculated using Chi-square test (*) for categorical variables, Mann-Whitney U test (†) for continuous variables and independent sample t-test (¥) for continuous variables group comparisons. Significance set at P < 0.05. The bold values indicate statistically significant p-values.

Abbreviations: ALT: alanine transaminase; CRP: C- Reactive Protein; ESR: Erythrocyte Sedimentation Rate; Hgb: haemoglobin; Q1-Q3, interquartile range.

Receiver Operating Characteristic (ROC) analysis identified cutoffs of ≤ 50 cells/mm³ for CD4 + T lymphocyte count (sensitivity 56.5%, specificity 76.9%), <150,000/ml for platelet count (sensitivity 56.5%, specificity 84.6%) (Figure 2).

Figure 2.

ROC curve analysis of CD4 and platelet counts for predicting early mortality in people living with HIV/TB co-infection.

Positivity rates for EZN, PCR, and TB cultures in clinical samples were 54%, 15%, and 84%, respectively (Table 3).

Table 3.

Analysis of clinical specimens for microbial pathogens in HIV/TB co-infection.

Sample	EZN positivity ratio n (%)	PCR positivity rate n (%)	TB culture positivity rate n (%)
Sputum	24 (39%)	4 (7%)	37 (60%)
Sterile body fluid (pleural fluid and bos)	2 (3%)	2 (3%)	4 (7%)
Tissue biopsy (lap)	7 (11%)	1 (2%)	8 (13%)
Urine	1 (2%)	0 (0%)	7 (11%)
Total	33 (54%)	9 (15%)	52 (84%)

Opportunistic infections and malignancies were observed in 11% (n = 7) of people living with HIV/TB co-infection, including one case of toxoplasma encephalitis, one case of Pneumocystis jirovecii pneumonia (PCP), two cases of cryptococcal meningitis, two cases of Kaposi’s sarcoma, and one case of cytomegalovirus (CMV) retinitis.

Discussion

Early mortality remains a significant concern among people living with HIV/TB co-infection. In this study, 37% of PLWH died within the first 6 months following their TB diagnosis, indicating a notably high early mortality rate. Key predictors of mortality included severe immunosuppression, anemia, lymphopenia, and thrombocytopenia.

Reported mortality rates during TB treatment in people living with HIV/TB co-infection range from 5% to 37.6%.^10,11 However, TB meningitis in PLWH carries a particularly high mortality rate of approximately 40%.¹² The six-month mortality rate observed in our study was even higher than the total mortality rates reported in previous studies. This discrepancy may be partly explained by the disease severity in our study, as 80% of patients with miliary tuberculosis (8/10) and all patients with tuberculous meningitis (4/4) died within the first 6 months. Anemia, CD4 + T lymphopenia (particularly CD4 <50 cells/mm³), thrombocytopenia (especially <150,000/ml) were identified as perdictors of mortality.

In Türkiye, screening HIV among TB patients became mandatory in 2011. The Turkish HIV/AIDS Guideline, which is compatible with international guidelines on strategies to screen and therapies to treat HIV/AIDS, has encouraged initiating ART regardless of CD4 + T lymphocyte count since 2013. Additionally, the Social Security Institution’s health benefits package in Türkiye is comprehensive. Free screning and treatment for TB and HIV are available for all people. Moreover, all patients are mostly screened before surgical procedures. Also, premarital HIV screening is commonly practiced. HIV/TB co-infection show this co-occurrence ranging from 28% to 90%.¹³ The lower co-occurrence rate observed in our study, compared to others, may be explained by the cross-sectional design and heterogeneous nature of those studies, which likely contributed to variations in case distribution.

Prior to 2010, the diagnosis of tuberculosis largely depended on EZN staining and culture methods, both of which had significant limitations particularly the low sensitivity of AFB smears and the prolonged time required for culture results. The introduction of FDA-approved NAA tests, such as Xpert MTB/RIF in 2010 and Xpert MTB/RIF Ultra in 2017, significantly shortened the time needed for both diagnosis and detection of rifampicin resistance to approximately 2 h. As a result, the WHO has recommended their use as initial diagnostic tools in suspected TB cases.¹⁴ In our study, TB culture was positive in the majority of cases (84%); EZN was positive in approximately half of the samples. The overall TB PCR positivity rate was relatively low (15%), which may be attributed to the absence of an in-house tuberculosis laboratory at our hospital. As a result, PCR testing often required external requests, which may have led to missed or delayed sample submissions.

The standard first-line treatment for pulmonary or extrapulmonary tuberculosis caused by drug-susceptible strains includes isoniazid (H), rifampin (R), pyrazinamide (Z), and ethambutol (E). The recommended regimen (2HRZE/4HR) is administered over a minimum duration of 6 months, regardless of patient age, HIV status, or disease severity.³ However, the treatment duration and regimen including the intensive and continuation phases may be modified based on the site of disease or the presence of drug resistance. In this study, all people living with HIV/TB co-infection received ART regimens appropriately selected to be compatible with rifampicin-containing TB treatment, and survivors were managed with timely and appropriate treatment plans, including TB treatment durations adjusted according to the type of TB.

In the USA in 2022, most TB cases were pulmoner TB (PTB) only (70%), followed by EPTB only (19%), and both (11%) (8). Of the 8925 TB cases reported in Türkiye in 2020, 65% (n = 5802) were PTB, and 35% (n = 3123) were EPTB (10). In this study, we found 44% (n = 27) PTB only, 27% EPTB (n = 17) only, and 29% (n = 29) both. TB lymphadenitis is the most common form of EPTB.¹⁵ Consistent with this, in our study, TB lymphadenitis was also the most frequently observed type of EPTB, accounting for 34% of cases.

Studies have found factors such as anemia and thrombocytopenia, delayed diagnosis have contributed to higher mortality.¹⁶ In this study the hazard of death among TB/HIV patients with anemia was higher than their counterparts (p = 0.009). This is because of worsening immunosuppression and might be due to decreased oxygen saturation among patients with anemia. The study also found that early mortality was significantly higher among patients with thrombocytopenia, particularly those with platelet counts below 150,000/mm³ (p = 0.003). This suggests a strong association between low platelet levels and increased risk of early death in people living with HIV/TB co-infection.

In the literature, the high mortality rates observed in HIV/TB coinfected patients have been consistently linked to several factors, including advanced age, the degree of immunosuppression, limited access to ART, low CD4 + T lymphocyte counts, and delayed diagnosis of HIV infection.^17,18 In the present study, early TB mortality was associated with lymphopenia (p = 0.009) and a CD4 + T lymphocyte count below 50 cells/mm³ (p = 0.015). These findings underscore the importance of early HIV detection, timely initiation of ART, and comprehensive management strategies to reduce TB-related mortality in PLWH.

Clinical manifestations vary depending on the location and the patient’s immune status. Our findings indicated that people living with HIV/TB co-infection presenting with anorexia and weight loss had a significantly higher risk of death compared to those with adequate nutritional status (p = 0.012). This result is consistent with previous studies.^19,20 PLWH who the presence of fever, fatigue, headache, and mental status changes was predictive of early mortality (p = 0.017, p = 0.021, p = 0.010, and p = 0.043, respectively).

Opportunistic infections (OIs) are common and remain a leading cause of mortality in PLWH. TB, which can occur at all stages of HIV infection, is one of the most frequent OIs. A systematic review from Türkiye reported an overall OI rate of 17% among PLWH with TB accounting for 5.5% of cases.²¹ In the present study, TB was identified in 4% of PLWH, while OIs were present in approximately 11% of those with HIV/TB co-infection. These findings underscore the ongoing burden of TB as a major OI among PLWH and highlight the importance of early diagnosis and comprehensive management approaches.

Study limitations

This study has several limitations. First, it was conducted at a single center, which may limit the generalizability of the findings. Second, its cross-sectional design restricts the ability to infer causal relationships between variables. Third, the analysis depends on the availability and completeness of medical records, which may introduce information bias. Additionally, TB diagnosis methods evolved over time (2004–2023), especially with the introduction of molecular tests like Xpert MTB/RIF. Although all cases met the diagnostic criteria valid at the time, no separate analysis was performed based on diagnostic period, which is a limitation.

Conclusion

This study revealed a high early mortality rate among people living with HIV/TB co-infection, primarily associated with severe immunosuppression, anemia, lymphopenia and thrombocytopenia. Clinical symptoms such as fever, anorexia, weight loss, and mental status changes were also linked to increased risk of death. These findings indicate that HIV/TB co-infection in individuals presenting with advanced disease requires particular attention due to the increased risk of mortality, and that those with marked immunosuppression and hematologic abnormalities constitute a high-risk group requiring closer clinical monitoring.

Footnotes

ORCID iD

Melike Nur Ozcelik

Author contributions

MNO: Conceptualization, Data curation, Formal Analysis, Investigation, Methodology, Project administration, Resources, Software, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing. EZ: Conceptualization, Data curation, Validation, Writing – original draft. IYN: Conceptualization, Data curation, Methodology, Visualization. FP: Conceptualization, Data curation, Resources, Software, Supervision, Validation, Visualization, Writing – original draft

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Data Availability Statement

The datasets generated and/or analyzed during the current study are available from the corresponding author upon reasonable request.*

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