|Year : 2023 | Volume
| Issue : 1 | Page : 24-30
Radiographic manifestations of tuberculosis in HIV-co-infected patients and correlation of the findings with CD4 counts
Rajendra Prasad Takhar1, Rama Kishan Saran2, Sanya Saran3, Lokesh Maan4, Mahendra Kumar Bainara5, Gopal Purohit6
1 Department of Respiratory Medicine, Government Medical College, Kota, Rajasthan, India
2 Department of Surgery, Dr. S. N. Medical College, Jodhpur, Rajasthan, India
3 Department of Paediatrics, Government Medical College, Kota, Rajasthan, India
4 Department of Respiratory Medicine, Mahatma Gandhi Medical College, Jaipur, Rajasthan, India
5 Department of Respiratory Medicine, R N T Medical College, Udaipur, Rajasthan, India
6 Department of Respiratory Medicine, Dr. S. N. Medical College, Jodhpur, Rajasthan, India
|Date of Submission||16-Jul-2022|
|Date of Decision||02-Jan-2023|
|Date of Acceptance||11-Jan-2023|
|Date of Web Publication||15-Mar-2023|
Rajendra Prasad Takhar
Department of Respiratory Medicine, Government Medical College, Qtr No 1/4, Medical College Campus, Kota, Rajasthan
Source of Support: None, Conflict of Interest: None
Background: Chest X-ray plays a vital role in diagnosis of tuberculosis (TB) in HIV infection. These patients present with variable chest radiographic presentation, making diagnosis and treatment of TB notoriously challenging and increasing the risk of treatment failure, relapse, and even death. Aims: The objective of this study was to identify various radiological patterns of TB in HIV-TB-co-infected patients and to correlate with CD4 count. Setting and Design: This was an analytical cross-sectional study conducted in a tertiary care center in the southern part of Rajasthan, India. Materials and Methods: In our study, 110 consecutive patients with pulmonary TB-HIV co-infection were subjected to chest radiographs and evaluated for the types of lesion/TB; anatomical distribution, and type of radiological shadows. The findings were correlated with CD4 counts and sputum acid-fast bacilli (AFB) status. The main outcome measures were radiological shadows and their correlation with level of immune suppression. The sample size was 110 patients. Results: Patients of Group I (CD4 <200) had significantly more involvement of mid and lower zones than Group II (CD4 >200). Nodular shadow (54.1% vs. 46.9%), consolidation (28.4% vs. 25.0%), hilar lymphadenopathy (23.0% vs. 9.4%), and miliary shadow (9.5% vs. 3.1%) in Group I, while cavitation (25.0% vs. 20.3%) and pleural effusion (18.8% vs. 16.2%) were more frequent in Group II. In Group I, consolidation (44.8% vs. 17.8%, P = 0.012) while in Group II, both consolidation (46.2% vs. 10.5%, P = 0.038) and cavitation (46.2% vs. 10.5%, P = 0.038) were present in significantly higher proportion in AFB-positive cases. Conclusion: A wide spectrum of radiographic shadows in consonance with varying CD4 counts was observed in the study. Along with well-known atypical radiological findings, some features were present throughout spectrum of CD4 counts, indicating that TB should be considered in this group of patients with these radiographic presentations, regardless of CD4 count. The small study population, majority of the patients' already hospitalized indicating serious nature of illness. In addition, no prospective follow-up of the study population to identify over the time changes in radiological pattern.
Keywords: HIV infection, immune suppression, radiological presentation, tuberculosis
|How to cite this article:|
Takhar RP, Saran RK, Saran S, Maan L, Bainara MK, Purohit G. Radiographic manifestations of tuberculosis in HIV-co-infected patients and correlation of the findings with CD4 counts. Saudi J Health Sci 2023;12:24-30
|How to cite this URL:|
Takhar RP, Saran RK, Saran S, Maan L, Bainara MK, Purohit G. Radiographic manifestations of tuberculosis in HIV-co-infected patients and correlation of the findings with CD4 counts. Saudi J Health Sci [serial online] 2023 [cited 2023 Mar 31];12:24-30. Available from: https://www.saudijhealthsci.org/text.asp?2023/12/1/24/371715
| Introduction|| |
HIV and tuberculosis (TB) both have some harmful and bidirectional synergistic interactions by reinforcing the natural course of each other leading to progression of the illness with increased morbidity and mortality which is dramatically more than caused by each infection alone. Consequently, the global TB problem has worsened and TB has emerged as the leading cause of preventable death, especially in developing countries where around 95% of concurrent TB-HIV infections are found.
Globally one-third of the population is infected with Mycobacterium tuberculosis while it is approximately 50% in Indian population and the emergence of HIV infection may lead to a drastic rise in the number of TB cases.
HIV has a great effect on course and outcome of TB. By virtue of its ability to undermine the cell-mediated immune system through depletion of CD4 lymphocytes, HIV has emerged as the most important risk factor not only for reactivation of the latent TB infection leading to clinical disease but also associated with an accelerated progression of recently acquired infection toward active disease due to failure to containment of new infections.,
In comparison to 5% to 10% likelihood of progression of latent TB to active TB in HIV-negative persons during their lifetime, it is a 5% to 15%/year or 30%–70% lifetime risk in HIV-positive patients., In India, TB is the most frequent opportunistic infection in HIV-positive patients and it is estimated that approximately 60%–70% of HIV-positive persons will develop TB once in a while during their lifetime.
TB may present with both typical and atypical clinicoradiographic features in patients co-infected with HIV depending on the degree of immunosuppression due to the alteration in the cell-mediated immunity. In cases of TB, chest radiography is an essential tool for the diagnosis, to determine the extent or severity of the disease, and to evaluate the response to therapy. However, a wide spectrum of radiological presentation of TB is seen among HIV patients depending on their varying immune status.,
Some studies from Western countries have shown that patients with low CD4 lymphocyte count may present with atypical radiographic features such as lower frequency of cavitation, higher frequency of intra/extrathoracic lymphadenopathy, lower lung zone infiltrates, miliary nodule (s), pleural effusion, and even a normal chest radiograph (features of primary TB), while those with a high CD4 count will have features typical of postprimary TB such as upper lung zone infiltrate/fibrosis often with cavitation, bilateral infiltrates, and middle or lower zone consolidation mimicking bacterial pneumonia., However, there is a dearth of studies on this subject in India, and published data on the relationship between radiographic manifestations and CD4 count are still scarce. Hence, this study was undertaken to assess the common radiographic appearances of TB in HIV patients and the impact of CD4 + lymphocyte count on it. An attempt was also made to correlate the radiological patterns and CD4 counts as it may be helpful in early identification of the disease and initiation of treatment as TB may prove a potentially perilous disease in this group of patients if left untreated or delayed.
| Materials and Methods|| |
This analytical cross-sectional study was done at a tertiary care hospital located in Western India. The study was approved by the research ethics committee of the institute.
Adult patients with current diagnosis of TB confirmed by standard clinical criteria and mycobacteriologic or pathologic confirmation along with a confirmed HIV-positive status by standard serology tests (two positive enzyme-linked immunosorbent assay and one Western blot test) as per the National AIDS Control Organization guidelines after necessary pre- and posttest counseling and presented at the hospital within the study period were included in the study.
Patients with other immunosuppressive disorders such as diabetes mellitus, malignancies, any known primary immune deficiencies, or other causes of immune suppression, e.g., use of long-term steroids, or other immunosuppressive therapy, as well as those who denied for the consent, were excluded from the study.
After written informed consent from the patients, each participant completed a structured questionnaire concerning sociodemographic characteristics, and laboratory data including CD4+ cell count were collected into the datasheet. Absolute CD4+ counts were obtained by flow cytometry technique using BD FACSCount machine with Facscount™ reagents (Becton Dickinson, USA). We categorized the patients into two groups based on their immune status (Group I with CD4 cell count of <200 cells/μl and Group II with ≥200 cells/μl). The diagnosis of current TB was based on clinical manifestations, history of contact with TB patients, and supportive investigations either alone or in combination including sputum smear/culture for acid-fast bacilli (AFB), chest X-ray/lateral posteroanterior views, tuberculin/Mantoux test, relevant fluid (pleural/ascitic fluid, cerebrospinal fluid, etc.) analysis, and tissue biopsy/fine-needle aspiration cytology/cytopathological examination of relevant site. Other relevant investigations such as ultrasound abdomen/thorax and computerized tomography of the abdomen/thorax were also performed as and when required. First, these chest radiographs were assessed independently by two experienced pulmonologists/radiologists, who had no knowledge of the results of HIV testing and CD4 T-lymphocyte count for evidence of lesions suggestive of TB. They also evaluated the radiographs for the types of lesion/TB; anatomical distribution of radiological features on X-ray (bilateral lung involvement versus solitary lung involvement, number of lung zones involved or predominantly affected lung zones); along with type of radiological shadows (nodular infiltrates, consolidation, cavitation, fibro-calcified shadows, hilar lymphadenopathy, mediastinal lymphadenopathy, pericardial effusion, pleurisy/pleural effusion, and collapse hydropneumothorax, localized or miliary shadows, interstitial nodules, bronchiectasis, and pleural thickening or any combination thereof). In case of inconsistency between the evaluations, the chest X-rays were jointly examined, and in the event of the persistent disagreement, a third pulmonologist/radiologist was consulted so that a consensus could be reached. A subanalysis of these radiological features was then correlated with level of immunosuppression and sputum AFB status.
The data were presented as mean and standard deviation for continuous variables and as frequency and percentages for categorical variables. We used Student's t-test for comparing continuous data and Chi-square test or Fisher's exact test for categorical data. P < 0.05 was considered statistically significant. We used IBM Corp. Released 2020. IBM SPSS Statistics for Windows, Version 27.0. (Armonk, NY: IBM Corp) software for data analysis and Microsoft Excel for data assimilation.
| Results|| |
A total of 110 HIV-TB-co-infected patients were recruited into the study. The baseline characteristics of the patients are summarized in [Table 1]. These did not differ significantly in the two study groups. The mean age was 34.1 years in overall population, and males were more in number (70.9%). A proportionally higher number of patients in Group I were from rural background than Group II (39.0% vs. 21.2%, P = 0.071). On X-ray chest, abnormality was evident in 96.4% of cases whereas four cases had completely normal X-ray without any specific findings among which three were in Group I and one case was in Group II.
|Table 1: Demographic and medical history characteristics in three groups of CD4 cell count|
Click here to view
The anatomical distribution features of X-ray are shown in [Table 2]. Bilateral lung involvement was seen in most cases (77.4%) whereas solitary lung (either right – 9.4% or left – 12.2%) involvement occurred in the rest of the cases. The occurrence of lesion in any lung was not statistically different in the two groups (P = 0.658). From total 6 lung zones, we found that involvement of 2 or more lung zones was common in both the groups. No lung zone involvement was seen in 4 cases, all of which were in Group I. Anatomically, the right middle zone was most frequently (56.6%) affected than rest all which were affected with nearly similar proportion of patients in overall population. However, in Group I, a significantly higher proportion of patients had involvement of right-middle (63.5% vs. 40.6%, P = 0.029), left-middle (51.4% vs. 28.1%, P = 0.027), and left-lower (56.8% vs. 21.9%, P = 0.001) zones. The remaining zones were also involved with higher frequency in Group I than Group II except for upper zones of both lungs which were involved slightly with greater frequency in Group II.
Nodular shadow (51.9%) was the most common feature evident on X-ray followed by consolidation (27.4%), cavitation (21.7%), hilar lymphadenopathy (18.9%), and pleural effusion (17.0%) among others, as projected in [Table 3]. In Group I, nodular shadow (54.1% vs. 46.9%), consolidation (28.4% vs. 25.0%), hilar lymphadenopathy (23.0% vs. 9.4%), and miliary shadow (9.5% vs. 3.1%) were more frequent along with fibro-calcified shadows, hydropneumothorax, and mediastinal lymphadenopathy in almost similar frequency in both the groups while pleurisy, pericardial effusion, and collapse were seen exclusively in patients having CD4 counts below 200. In comparison, cavitation (25.0% vs. 20.3%) and pleural effusion (18.8% vs. 16.2%) were more frequent in Group II than Group I, respectively. The differences in proportion of patients with these features on X-ray did not differ significantly in the two groups.
We further did a subanalysis of features of X-ray in patients with sputum positive or negative for AFB. This analysis revealed that in Group I, a significantly higher proportion of patients having consolidation as a feature in AFB-positive cases than AFB-negative ones (44.8% vs. 17.8% respectively, P = 0.012). No other features showed a significant difference in proportion of patients in Group I. In Group II, consolidation (46.2% vs. 10.5%, P = 0.038) and cavitation (46.2% vs. 10.5%, P = 0.038) were more frequent in AFB-positive cases than AFB-negative patients. Features such as hilar lymphadenopathy, pleural effusion, miliary shadows, and fibro-calcified shadow were more frequent in AFB-negative cases in Group II.
| Discussion|| |
The radiographic presentations of adult TB in the HIV-co-infected patients are varied. Pulmonary TB (PTB) can manifest with two radiographic patterns, namely typical reactivation or postprimary TB and atypical pattern or primary TB pattern. Radiologically, patients with mild immunosuppression usually present with bilateral/unilateral upper lobe infiltrates, pulmonary fibrosis, cavitation, atelectasis, and/or shrinkage,, while severely immunocompromised patients present with atypical radiological features including minimal interstitial infiltrates, especially in the mid and/or lower zones, without any cavitation, and fibrosis. In these patients, cavities are present in only 25% of patients, because of poor delayed-type hypersensitivity response and lymphocyte reactivity to M. tuberculosis antigen which are required forcavity formation. Sometimes, these patients present with features similar to primary TB seen in children having mediastinal or hilar adenopathy, pleural effusion, miliary TB, involvement of anterior segment of upper lobe, middle and inferior lobes as well as sometimes even normal X-ray.,
The results from this study showed that a higher number of patients of Group I (CD4 <200) were from rural background than Group II having CD4 ≥200 (39.0% vs. 21.2%, P = 0.071) probably due to delayed presentation to the health-care facility because of poor financial condition and lack of awareness, especially profound in this tribal area of the state. A total of 96.4% of patients had some abnormalities on X-ray chest, whereas four cases had completely normal X-ray among which three were in Group I and one case was in Group II, corroborating with previous studies stating chances of normal chest X-ray increases with increasing immune suppression.
The mean age of the overall population was 34.1 years, and majority (70.9%) were males; similar to other recent studies from the region. The right middle zone was most frequently (56.6%) affected than rest all which were affected with a nearly similar proportion of patients in both the groups without any relation with CD4 counts. A statistically significantly higher proportion of patients had involvement of right-middle (63.5% vs. 40.6%, P = 0.029), left-middle (51.4% vs. 28.1%, P = 0.027), and left-lower (56.8% vs. 21.9%, P = 0.001) zones in Group I patients. This finding is also corroborating with the other previous studies, stating that involvement of mid and lower zones (atypical presentation of TB) is predominant in severely immunocompromised patients (CD4+ counts <200)., Similarly, Maniar et al. also observed upper zone involvement among 3.7%, middle zone involvement among 62.5%, and lower zone involvement in 33.8%.
We also observed involvement of upper zones of both lungs with greater frequency in Group II (CD4+≥200) similar to other previous studies.,, The diffuse radiological involvement is common in patients with HIV and TB co-infection. We also observed bilateral lung involvement among 82 (77.4%) of the chest radiographs, similar to a recent study. While, contrary to this, Maniar et al. observed unilateral disease in 71.8% and bilateral in 28.2% of the patients.
An analysis of type of shadows in this study revealed nodular pulmonary infiltrates (51.9%) as the most frequent radiological feature on X-ray similar to other recent studies. It was similar to a study by Mohd and Zuber followed by consolidation (27.4%), cavitation (21.7%), hilar lymphadenopathy (18.9%), and pleural effusion (17.0%)., In patients of Group I having CD4 counts below 200, in comparison to Group II (CD4 counts ≥200), nodular shadow/infiltrates (54.1% vs. 46.9%), consolidation (28.4% vs. 25.0%), hilar lymphadenopathy (23.0% vs. 9.4%), and miliary shadow (9.5% vs. 3.1%) were more frequently present along with fibro-calcified shadows, hydropneumothorax, and mediastinal lymphadenopathy in almost similar frequency in both the groups while pleurisy, pericardial effusion, and collapse were seen exclusively in patients having CD4 counts below 200. A recent study from the region also observed infiltration (39%), followed by consolidation (30%), cavity (11%), lymphadenopathy (9%), pleural effusion (9%), and miliary (7%) in these types of patients. Similarly, another study from the region by Maniar et al. also observed infiltration (62.5%), hilar lymphadenopathy (17.5%), pleural effusion (16.5%), and consolidation (7.5%) as major findings. A study from the Western world by Perlman et al. also revealed infiltrates among 52%, lymphadenopathy in 30%, interstitial disease in 27%, pulmonary nodule in 18%, cavity in 7%, and pleural effusion in 7%. The findings were similar to other recent studies.,, The association of severe immunosuppression (CD4 count <200 cells/mm3) with the presence of mediastinal lymphadenopathy and/or miliary TB is in keeping with other studies worldwide.,,
Most of the normal radiographs were in Group I (CD4 <200) similar to studies by Jaryal et al. and others who also found a significant association between severe immunosuppression and normal radiograph. It was similar to the findings of other authors from the region., According to Tripathy et al., this finding may be due to relatively decreased cell-mediated immunity in these patients resulting in reduced granuloma formation, caseation, liquefaction, and ultimately healing by fibrosis and calcification. While, contrarily, a study done in the USA found no significant association between decreased CD4 count and normal chest radiograph. It remains uncertain whether the normal X-ray or absence of radiological findings represents early stages of PTB, or disease in the form of intrathoracic adenopathy which has not been detected by radiographic examination. While, cavitation (25.0% vs. 20.3%) and pleural effusion (18.8% vs. 16.2%) were more frequent in Group II than Group I, but the finding was not statistically significant. Previous studies have found that cavity formation and other features of postprimary TB on chest radiograph were significantly associated with more immunocompetence (CD4 count ≥200 cells/mm3).,,
Contrary to this theory, we observed that cavitation and fibro-calcified lesions are not directly correlated to CD4 count. A similar observation has also been made by other researchers., One probable explanation for this finding could be the high incidence/prevalence of TB in this region where patients may acquire TB infection early in the course of HIV infection, when the immune system is relatively intact and leads to formation of cavitary lesion. Contrarily, some studies have suggested using molecular epidemiology that the radiological presentation of TB is more related to host immunity than to whether the infection occurred recently or remotely. This needs further research to clarify this issue and to identify the factors associated with the presence or absence of cavitary lesions among HIV-seropositive patients.
Some studies have found pleural effusion more frequently in patients with a CD4+ T-cell count >200 cells/mm3 while other authors in a group with a CD4+ T-cell count <200 cells/mm3. The mean CD4 + T-cell count of the patients analyzed in the present study was somewhat close to the cutoff point of 200 cells/mm3, and this might have influenced the results obtained (18.8% vs. 16.2%). A study consisting larger number of patients having significantly lower and higher CD4+ T-cell counts than the cutoff point might yield data that are more robust.
Further analysis of X-ray features in relation to sputum AFB status revealed a significantly higher proportion of patients having consolidation in AFB-positive cases than AFB-negative ones (44.8% vs. 17.8%, P = 0.012) in Group I. No other radiological feature was statistically significant in Group I. While, in Group II, consolidation (46.2% vs. 10.5%, P = 0.038) and cavitation (46.2% vs. 10.5%, P = 0.038) were more frequent in AFB-positive cases than AFB-negative patients. [Table 4] shows that sputum-positive status may be observed even in the absence of cavitation or any other abnormality in the parenchyma and it is not related to the level of CD4+ T-lymphocytes. Similar findings were also noted in the past. As it is obvious, features such as hilar lymphadenopathy, pleural effusion, miliary shadows, and fibro-calcified shadow were more frequent in AFB-negative cases in both the groups. We found that 39.6% of patients had sputum positive almost similar to a study by Padyana et al. (27%).
|Table 4: X-ray features according to sputum acid-fast bacilli status in two groups|
Click here to view
It is also evident from [Table 4] showing cross-tabulation between sputum smear and chest X-ray findings that most of the patients with atypical chest X-ray findings also had negative sputum AFB status. Another recent study has also reported a statistically significant relationship between these two.
In our study, the percentage of sputum AFB-positive or AFB-negative cases was almost similar in both the groups [Table 4] and not dependent on CD4 levels, while the study by Garcia et al. found that the proportion of AFB-positive patients with a CD4+ >200 cells/mm3 was almost twice that of patients with lower CD4 + cell counts, although this difference was not statistically significant.
Some studies in the past have observed that majority of the patients with atypical radiological manifestations were not related to CD4 count, while in some other studies, a statistically significant correlation between the CD4 count and radiographic presentations has been reported. In these studies, it has been suggested that the radiologic presentation of TB in HIV+ patients has not been perfectly understood and host response to TB in HIV+ patients is not determined by CD4 count alone, but some other factors may also be involved., We found a mixed picture in this regard where atypical presentation in the form of localization of the disease, we observed a statistically significant more chance of lower or mid zone predominance in Group I (CD4 <200) in comparison to Group II (CD4 >200) where upper zone predominance was observed. Second, we found that nodular shadows, hilar lymphadenopathy, and miliary shadows were more common in Group I than in Group II, but not statistically significant. Other radiological findings like consolidation, cavitation, pleural effusion, and calcification/fibro-calcified shadow were present in almost equal frequency in both groups. This is contrary to other studies which observed cavities to be commonly present in the immune preserved group, as the formation of cavities requires an intact delayed-type hypersensitivity response and strong lymphocyte reactivity to M. tuberculosis antigen.
The predominance of the nodular shadows/alveolar patterns over the consolidation and cavitation can be explained by the large proportion of the study sample from the severe immunosuppression group (Group I). Similarly, we also identified nodules in 54.1% and 46.9% (overall 51.9%) of the cases in Groups I and II, respectively, which is more than previously reported by various authors. Some studies have found an even higher incidence (82.0%) of nodules in CT. This disparity is clearly attributed to the use of more sensitive imaging tools. The presence of pleural effusion in the present study (17%) is in consonance with other studies reporting it to be 5.3%–18.0%.,
The limitations of our study include the small study population, the majority of the patients were already hospitalized indicating the serious nature of the illness. In addition, no prospective follow-up of the study population to identify over the time changes in radiological patterns.
Unique thing about our study is that we have not categorized the radiological features into the postprimary pattern and primary pattern or into typical (reactivation) or atypical pattern, which have been done by all previous studies.
| Conclusion|| |
In our study, majority (77.4%) of the patients had bilateral lung involvement in HIV-TB-co-infected patients and right middle zone was most frequently involved unlike previous studies (Lower lobe predominance.). We also found lower and mid zone involvement predominantly in patients with CD4 <200. Features such as consolidation, cavitation, and calcification/fibro-calcified shadow may also be found in patients with CD4 <200. The presence of consolidation was significantly associated with AFB-positive status in both Group I and Group II while cavitation was more frequent in AFB-positive cases than AFB-negative patients in Group II.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Raviglione M, Sulis G. Tuberculosis 2015: Burden, challenges and strategy for control and elimination. Infect Dis Rep 2016;8:6570.
Swaminathan S, Ramachandran R, Baskaran G, Paramasivan CN, Ramanathan U, Venkatesan P, et al.
Risk of development of tuberculosis in HIV-infected patients. Int J Tuberc Lung Dis 2000;4:839-44.
Nunn PP, Elliott AM, McAdam KP. Tropical respiratory medicine. 2. Impact of human immunodeficiency virus on tuberculosis in developing countries. Thorax 1994;49:511-8.
Daley CL, Small PM, Schecter GF, Schoolnik GK, McAdam RA, Jacobs WR Jr., et al.
An outbreak of tuberculosis with accelerated progression among persons infected with the human immunodeficiency virus. An analysis using restriction-fragment-length polymorphisms. N Engl J Med 1992;326:231-5.
Chapman SJ. Can your genes make you more prone to pneumococcal disease? Expert Rev Anti Infect Ther 2010;8:967-72.
Kawooya VK, Kawooya M, Okwera A. Radiographic appearances of pulmonary tuberculosis in HIV-1 seropositive and seronegative adult patients. East Afr Med J 2000;77:303-7.
Murray J, Sonnenberg P, Shearer SC, Godfrey-Faussett P. Human immunodeficiency virus and the outcome of treatment for new and recurrent pulmonary tuberculosis in African patients. Am J Respir Crit Care Med 1999;159:733-40.
Perlman DC, el-Sadr WM, Nelson ET, Matts JP, Telzak EE, Salomon N, et al.
Variation of chest radiographic patterns in pulmonary tuberculosis by degree of human immunodeficiency virus-related immunosuppression. The Terry Beirn Community Programs for Clinical Research on AIDS (CPCRA). The AIDS Clinical Trials Group (ACTG). Clin Infect Dis 1997;25:242-6.
Aderaye G, Bruchfeld J, Assefa G, Feleke D, Källenius G, Baat M, et al.
The relationship between disease pattern and disease burden by chest radiography, M. tuberculosis
Load, and HIV status in patients with pulmonary tuberculosis in Addis Ababa. Infection 2004;32:333-8.
Darraj MA. Pulmonary tuberculosis among HIV/AIDS patients: Chest X-ray characteristics. Suez Canal Univ Med J 2020;23:1-14.
San KE, Muhamad M. Pulmonary tuberculosis in HIV infection: The relationship of the radiographic appearance to CD4 T-lymphocytes count. Malays J Med Sci 2001;8:34-40.
Garcia GF, Moura AS, Ferreira CS, Rocha MO. Clinical and radiographic features of HIV-related pulmonary tuberculosis according to the level of immunosuppression. Rev Soc Bras Med Trop 2007;40:622-6.
Gold JA, Rom WN, Harkin TJ. Significance of abnormal chest radiograph findings in patients with HIV-1 infection without respiratory symptoms. Chest 2002;121:1472-7.
Affusim C, Abah V, Kesieme EB, Anyanwu K, Salami TA, Eifediyi R. The effect of low CD4+lymphocyte count on the radiographic patterns of HIV patients with pulmonary tuberculosis among Nigerians. Tuberc Res Treat 2013;2013:535769.
Jaryal A, Raina R, Sarkar M, Sharma A. Manifestations of tuberculosis in HIV/AIDS patients and its relationship with CD4 count. Lung India 2011;28:263-6. [Full text]
Padyana M, Bhat RV, Dinesha M, Nawaz A. HIV-tuberculosis: A study of chest X-ray patterns in relation to CD4 count. N Am J Med Sci 2012;4:221-5.
Maniar JK, Kamath RR, Mandalia S, Shah K, Maniar A. HIV and tuberculosis: Partners in crime. Indian J Dermatol Venereol Leprol 2006;72:276-82.
] [Full text]
Mohd S, Zuber A. Manifestations of tuberculosis in HIV infected patients. J Indian Acad Clin Med 2005;6:302-5.
Tripathy S, Menon P, Joshi DR, Patil U, Gadkari DA, Paranjape RS. Preliminary observations on lymphocyte subpopulations in HIV seropositive & HIV seronegative tuberculosis patients in Pune, India. Indian J Med Res 2000;111:195-8.
Zumla A, Malon P, Henderson J, Grange JM. Impact of HIV infection on tuberculosis. Postgrad Med J 2000;76:259-68.
Goodman PC. Tuberculosis and AIDS. Radiol Clin North Am 1995;33:707-17.
Geng E, Kreiswirth B, Burzynski J, Schluger NW. Clinical and radiographic correlates of primary and reactivation tuberculosis: A molecular epidemiology study. JAMA 2005;293:2740-5.
da Silva RM, da Rosa L, Lemos RN. Radiographic alterations in patients presenting human immunodeficiency virus/tuberculosis coinfection: Correlation with CD4+ T cell counts. J Bras Pneumol 2006;32:228-33.
Smith RL, Yew K, Berkowitz KA, Aranda CP. Factors affecting the yield of acid-fast sputum smears in patients with HIV and tuberculosis. Chest 1994;106:684-6.
Karam MB, Tabarsi P, Mirsaiedi SM, Amiri MV, Zahirifard S, Mansoori SD, et al
. Radiographic manifestations in TB/HIV patients. Tanaffos 2004;3:33-9.
Post FA, Wood R, Pillay GP. Pulmonary tuberculosis in HIV infection: Radiographic appearance is related to CD4+ T-lymphocyte count. Tuber Lung Dis 1995;76:518-21.
Burrill J, Williams CJ, Bain G, Conder G, Hine AL, Misra RR. Tuberculosis: A radiologic review. Radiographics 2007;27:1255-73.
Bombarda S, Figueiredo CM, Funari MB, Soares J Jr., Seiscento M, Filho MT. Imagem em tuberculose pulmonar. J Pneumol 2001;27:329-40.
[Table 1], [Table 2], [Table 3], [Table 4]