Home Print this page Email this page Users Online: 164
Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login 

 Table of Contents  
Year : 2020  |  Volume : 27  |  Issue : 1  |  Page : 27-32

Chest radiographic findings of pulmonary tuberculosis in human immunodeficiency virus-seropositive patients in a teaching hospital in Kano Northwest, Nigeria

1 Department of Radiology, Aminu Kano Teaching Hospital/Bayero University Kano, Kano, Nigeria
2 Department of Medical Radiography, University of Maiduguri, Maiduguri, Borno, Nigeria
3 Department of Internal Medicine/Radiology, Abubakar Tafawa Balewa University Teaching Hospital Bauchi, Bauchi State, Nigeria
4 Department of Medical Imaging Services, American University of Beirut, Beirut, Lebanon

Date of Submission05-Sep-2018
Date of Acceptance30-Apr-2019
Date of Web Publication13-Mar-2020

Correspondence Address:
Mr. Mohammed Sani Umar
Department of Radiology, Aminu Kano Teaching Hospital/Bayero University Kano, Kano
Login to access the Email id

DOI: 10.4103/wajr.wajr_33_18

Rights and Permissions

Background: Tuberculosis (TB) is one of the most common infections to occur in the course of human immunodeficiency virus (HIV) infection and remains a global emergency despite substantial investment in health services.
Aim: This study aims to determine the spectrum of chest X-ray findings in patients with HIV/TB coinfection.
Materials and Methods: A retrospective cross-sectional study of the clinical and radiographic features of pulmonary TB (PTB) in 244 confirmed HIV-seropositive patients aged 9 months to 80 years. Descriptive statistics was employed in analyzing mean percentages and frequencies. Level of statistical significance between clinical findings, radiographic findings, age group, and gender was determined using z-test. Statistical significance was set atP ≤ 0.05.
Results: The study constituted of 104 (42.62%) males and 140 (57.38%) females with mean age of 31.62 ± 16.93 years. The major clinical features among HIV-related PTB patients in this study are cough in 56.6% patients, chest pain in 11.44% patients, weight loss in 10.26% patients,P < 0.05. Chest X-rays with normal findings were found in 60.0% patients, while primary patterns of PTB such as reticulonodular opacities occurred in 16.61% patients, typical post primary patterns such as background cystic/fibrotic changes were found in 3.39% patients, and miliary pattern in 2.73% patients. The age group 26–38 years was frequently involved in TB coinfections in both sexes,P < 0.001. The percentages of males and females with TB infection were 40.98% and 56.15%, respectively.
Conclusions: Normal chest X-rays constitute the major findings; primary and postprimary patterns of PTB account for the least findings with the age group 26–38 years as the most occurring (91, 37.30%). Females were more frequently involved in TB coinfection. The preponderance of normal radiographs does not exclude the presence of TB coinfection.

Keywords: Chest, human immunodeficiency virus, pulmonary, radiographs, tuberculosis

How to cite this article:
Umar MS, Daniel SV, Suwaid MA, Luntsi G, Yusuf J, Zira JD, Abubakar A, Saade C, Barde M. Chest radiographic findings of pulmonary tuberculosis in human immunodeficiency virus-seropositive patients in a teaching hospital in Kano Northwest, Nigeria. West Afr J Radiol 2020;27:27-32

How to cite this URL:
Umar MS, Daniel SV, Suwaid MA, Luntsi G, Yusuf J, Zira JD, Abubakar A, Saade C, Barde M. Chest radiographic findings of pulmonary tuberculosis in human immunodeficiency virus-seropositive patients in a teaching hospital in Kano Northwest, Nigeria. West Afr J Radiol [serial online] 2020 [cited 2022 Jan 23];27:27-32. Available from: https://www.wajradiology.org/text.asp?2020/27/1/27/280606

  Introduction Top

Tuberculosis (TB) still remains a global pandemic despite substantial investment in healthcare services over the past two decades. It causes ill-health in approximately 10 million people each year and is one of the top ten causes of death worldwide.[1] It has been the leading cause of death from a single infectious agent, ranking above human immunodeficiency virus (HIV) and/or acquired immunodeficiency syndrome virus.[2] TB is the most common opportunistic disease and cause of death among those infected with HIV.[3],[4] Similarly, HIV infection is one of the most important risk factors associated with an increased risk of latent TB infection progressing to active TB.[5],[6] Moreover, the risk of developing TB is more than 40 times greater in people living with HIV than among people affected by risk factors such as undernutrition, diabetes, smoking, and alcohol consumption.[7]

The global impact of TB is extremely important considering the fact in 2016 about 6.3 million new cases of TB were reported.[8] Of the 10.4 million incident cases of TB in 2016, an estimated 1.9 million were attributable to undernourishment, 1.0 million to HIV infection, 0.8 million to smoking, and 0.8 million to diabetes. About 82% of the estimated incidence was reported to be living in sub-Saharan Africa.[9] A recently concluded national TB prevalence survey in Nigeria showed 560,000 cases in 2016 but only about 100,000 cases were reported according to the recent WHO global TB report 2017.[10],[11]

The pandemic of HIV has been pointed out as one of the major causes of the worldwide increase in TB cases.[12],[13] This is due to the fact that TB is one of the most common infections to occur in the course of HIV infection, either because of the reactivation of latent TB or as a result of new infection by the TB Mycobacterium, with a faster progression toward the active disease.[14] Respiratory infections, especially TB, are leading causes of illness and death in HIV-infected patients in sub-Saharan Africa.[15]

Patients with sputum-negative pulmonary TB (PTB) and extra PTB are difficult to diagnose and may be missed at all points of care. Clinical signs and symptoms in affected adults can be nonspecific and a high level of pretest clinical suspicion based on history is fundamental in the diagnostic workup. In most developing countries, diagnosis of PTB depends on the clinical symptoms, rapid molecular tests, chest radiography, tuberculin skin test, and sputum smear examination for acid-fast bacilli (AFB). Among diagnostic tools usually used for diagnosis of PTB, the chest X-ray plays an essential role, chiefly since it is widely available within the public healthcare system, even in poor populations.[16]

HIV infection leads to increased frequency of atypical radiographic features in patients with PTB with a tendency toward the pattern of primary disease.[17],[18],[19],[20] However, there is a paucity of literature on chest radiographic findings of PTB in HIV-infected patients in this locality. This necessitates the study. This study was designed to give an indepth knowledgeof patterns of chest radiographic findings of HIV-related PTB patients in a tertiary facility in Kano, Northwestern Nigeria.

  Materials and Methods Top

This was a retrospective cross-sectional study. The study reviewed all request forms and result sheets from the archives of the Radiology Department and Virology Centre of Aminu Kano Teaching Hospital Kano, Nigeria from June 2017 to January 2015 of confirmed HIV-seropositive patients as detected by the enzyme-linked immunosorbent assay and clinically proven Mycobacterium tuberculosi s (MTB) as detected by the AFB and sputum smear GeneXpert MTB/RIF Assay. Patients on direct observation short course therapy and patients on antiretroviral therapy were also included in the study. Request forms and result sheets with incomplete results and patient's information were excluded from the study. Patients' information such as age, sex, clinical history, radiographic findings were recorded and tabulated.

Statistical analysis was performed using statistical package for the social sciences for windows (Version 20.0; SPSS, Chicago, IL, USA). Z-test was used to determine the level of statistical significance between clinical findings, radiographic findings, age, and gender at 95% confidence interval. Level of significance was determined using student t-test. Statistical significance was set at P ≤ 0.05.

In line with Helsinki declaration, ethical approval (NHREC/21/08/2008/AKTH/EC/890) was obtained from Health Research and Ethics Committee of Aminu Kano Teaching Hospital.

  Results Top

A total of 244 result sheets of chest X-ray for HIV-seropositive-related PTB patients were assessed for the study. The study comprised 104 (42.62%) males and 140 (57.38%) females. The individuals were from the ages 9 months to 80 years, with mean age of 31.62 ± 16.93 years. Individuals within the age group of 26–38 years were predominant 91 (37.30%) in both sexes, while those within the age group of 65 years and above had the lowest frequency of 11 (4.5%), P < 0.001, with 42 (9.43%) pediatric patients. The percentages of males and females with TB infection were 40.98% and 56.15%, respectively, as shown in [Table 1].
Table 1: Frequency distribution of human immunodeficiency virus/tuberculosis coinfection based on age and gender of individuals

Click here to view

The major clinical features among patients with HIV-related PTB in this study were cough (recurrent, progressive, persistent, severe, and chronic) in 193 (56.6%) patients, chest pain in 39 (11.44%) patients, weight loss 35 (10.26%), hemoptysis 21 (6.16%), night sweat 21 (6.16%), and 12 (3.52%, P < 0.05) greenish sputum among others. About 1.47% of the individuals were known as PTB patients and were receiving treatment. Only one patient had normal chest X-ray [Table 2].
Table 2: Clinical history of patients with human immunodeficiency virus/pulmonary tuberculosis in the study

Click here to view

The distribution of chest radiographic findings among HIV-related PTB patients is shown in [Table 3]. Normal study comprised the highest 177 (60.0%) which constituted 72 (24.41%) males and (105) 35.59% females, followed by reticulonodular opacities in 49 patients (16.61%), hilar lymphadenopathy in 11 (3.73%) patients, consolidations and background cystic/fibrotic changes representing 10 (3.39%) each, respectively, miliary opacities in 7 (2.37%) patients. There was preponderance in bilateral lung involvement. The least findings were right hydrothorax, thick-walled cavity, pleural effusion, and silhouette sign representing 1 (0.34%), respectively.
Table 3: Chest radiographic findings of patients with human immunodeficiency virus/pulmonary tuberculosis coinfection in the study

Click here to view

There was no statistically significant difference in findings between male and female individuals (P < 0.005). However, females were more frequently involved in TB.

[Table 4] shows the distribution of radiographic findings in relation to age group. Of the 295 radiographic findings reported in this study, the age group 26–38 years had most occurring 109 (36.9%) findings constituting normal study (23.4%) being the highest followed by reticulonodular opacities (5.4%), blunting of costophrenic angles (1.7%), and 1.4% background cystic/fibrotic changes (P < 0.001) among others. Elderly patients within the age group of 65 years and above had the least radiographic findings of 18 (6.1%) which comprised mainly of reticulonodular opacities (2.4%); normal study (1.4%); consolidations (1.4%); cystic/fibrotic changes (0.7%) and about 0.3% apical opacities (P < 0.001).
Table 4: Pattern of chest radiographic findings in relation to age group in the study

Click here to view

  Discussion Top

The recent increase in the prevalence of TB globally, particularly in Africa has been attributed to the increase in number of HIV-infected patients.[1],[2],[3],[4],[5] There is a rising incidence of TB, especially PTB in HIV-infected patients as well as a high rate of HIV in patients suffering from TB in Nigeria and other parts of the world.[12] The diagnosis of active PTB is a major challenge, especially in individuals with severe immunosuppression, such as those coinfected with HIV. Such patients characteristically demonstrate an atypical radiographic pattern, for example, middle and lower lung involvement, absence of cavity formation, presence of lymphadenopathy and pleural effusions, or a miliary pattern.[21]

The mean age of the patients enrolled in this study (31.62 ± 16.93 years) is in line with other studies done in Nigeria such as Ahidjo et al. in Maiduguri, North East Nigeria (33.9 ± 8.42 years),[6] Desalu et al.(35.1 ± 8.4 years),[12] and Peters et al. in Calabar, South South Nigeria (34.60 ± 1.2 years).[16] It is also in line with some studies performed among African countries such as Said et al. in Bagamoyo, Rural Tanzania,[7] Kisembo et al. in Kampala, Uganda,[15] and other countries of the world such as Bermudez et al. in Cuba,[2],[5],[11] and Hadadi et al. in Iran who reported similar findings among HIV-related PTB patients.[22] The similarity in the reported findings may be attributed to the fact that HIV infection is more common among people in the productive and sexually active age groups. Overcrowding is another factor associated with high risk of airborne transmission of PTB among productive and sexually age groups. The study locality is one of the major densely populated cities in Nigeria with an estimated population of over 9.4 million people as stated by the National Bureau of Statistics of the Federal Republic of Nigeria.[23] As such person to person transmission of MTB may occur by aerosol droplets generated by a person with the active disease which are inhaled into the large and small airways, where infection can be established. It may also be due to use of high dose of corticosteroids among the sexually active age groups.

The gender distribution of patients in this study showed 140 (57.38%) for females and 104 (42.62%) for males, giving male:female of 1:1.3. This demonstrates that there is no wider margin of prevalence of HIV-related PTB among gender wise. This is in line with the study done by Bohara,[4],[5],[8],[15] Peters et al. (male:female of 1:1.1),[16] and Olatunji et al. (male:female of 1:1.9).[14] However, it is in contrast with the study of Ahidjo et al. in Maiduguri,[6] North East Nigeria who reported male to female ratio of 1.3:1, Desalu et al. (male:female of 1.4:1)[12] and Bermudez et al.[2],[11],[24] The variation in the reported values may be attributed to the fact that most of the people in this part of the country are polygamous in nature, suggesting the likelihood that the females got infected by their husbands.[6] Lack of information and good knowledge about HIV infection is another contributing factor as HIV infection is more pronounced among the less privileged.

The classical symptoms and clinical signs of PTB in HIV-seropositive patients such as low-grade fever, night sweats, cough, loss of appetite, chest pain, and hemoptysis demonstrated in this study are in consonance with the findings of other studies in Nigeria, African countries and other countries of the world such as Ahidjo et al.[6] reported productive cough (100%), oral thrush (87%), weight loss (83%), night sweats (78%), fever (75%), chest pain (50%), and herpes zoster (5%). Peters et al. reported chronic cough (89%), chest pain (74%), dyspnea (62%), nonproductive cough (11%), and cough with hemoptysis (18%).[16] Bermudez et al.[2],[4],[7],[22] among others also reported similar findings. The similarity in the reported findings may be attributed to the adoption of the same diagnostic standards and classification of HIV-related PTB in adults and children by the American Thoracic Society and Centre for Disease Control and Prevention.[17] However, findings such as oral thrush and dermatological manifestations as reported by Ahidjo et al.[6] were not reported in this study.

The most common chest radiographic pattern in HIV-related PTB patients in this study was normal chest X-rays (60%); whereas primary and postprimary radiological findings such as hilar lymphadenopathy, hydrothorax, background cystic/fibrotic changes, apical opacities, lower/midzone opacities, lung collapse, and pleural effusion accounted for the least. The reported finding is similar to those of Ahidjo et al.,[6] who reported normal radiographs in 15 (25%) patients, hilar adenopathy in 5 (8%) patients, pleural effusion in 10 (16.7%), lower/mid-zone opacities 7 (11.6%), and reticulonodular opacities in 2 (3%) patients. Olatunji et al. in Sagamu,[14] South West Nigeria reported normal radiographs in 68.5% patients, features of TB in 27.8%, and pneumonia in 2.7%. The high rate of normal radiographic findings in this study may be related to immune status, as immunosuppressed patients may not mount adequate immune response to MTB. However, it is in contrast with the study by Awoyemi et al. in Ibadan,[10] who reported low incidence of normal chest X-rays in 2 (11%); miliary pattern in 2 (11%); pleural effusion in 2 (11%); hilar adenopathy in 2 (11%), localized and diffused lesions in 7 (37%) individuals respectively and pulmonary cavities in 3 (16%). Bermudez et al. in Cuba,[2] also reported low prevalence of normal chest X-rays (25%) with predominance of the primary radiological patterns.

The prevalence of thick-walled cavitations in this study is very low and accounted for 1.36%. Whereas the study by Olatunji et al.[14] reported cavitations in 31 (37.8%) patients with less CD4 cell count below 200 cells/mm3. Ahidjo et al. reported apical opacities with cavitations in 9 (15%).[6] This might have been the patients involved in our study had higher CD4 cell count at point of presentation.

Age is also a factor which influence the clinical and radiographic features of TB.[17] However, the distribution of radiographic features of PTB according to age group were not reported by Ahidjo et al. among others.[6],[10] The distribution of radiographic findings according to age group in this study in decreasing order shows that the age groups 26–38, 0–12, 39–51, and 13–25 years demonstrate predominance in normal chest X-rays with 23.38%, 11.52%, 10.50%, and 8.81%, respectively (P ≤ 0.005). However, patients between 26–38 years shows predominance in reticulonodular opacities, 39–51 years shows predominance in miliary pattern and consolidations mostly seen in the elderly (65 years and above).

  Conclusions Top

Normal chest X-rays constitute the major findings. TB coinfections have more preponderance in females. Although this study provides spectrum of findings in TB and HIV co-infection in a resource-constrained setup in a developing country with high prevalence of the two disease conditions, it has some limitations which are subject to future studies. These includes: CD4 cell count was not performed which would have helped in clinical staging of HIV infection, lack of mycobacterial culture, other associated risk factors were not documented such as cigarette smoking, alcoholism, chronic renal failure to mention but a few and possibility that presence of other respiratory infections such as bacterial pneumonia which may influence the pattern of abnormalities seen on the radiographs were not considered.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

  References Top

World Health Organization. Global Tuberculosis Report. World Health Organization; 2017. Available from: http://www.who.int/tb/publications/global_report/en/. [Last accessed on 2018 Mar 21].  Back to cited text no. 1
Bermudez PT, Corcho VD, Mercolo Millan JC, Remirez DP, Perez Narciso AJ. Clincal-radiologic manifestations in patients with pulmonary tuberculosis and HIV/AIDS co-infection. Rev Cubana Med Gen Integral 2017;33:310-20.  Back to cited text no. 2
Sudha M, Meena M, Atul RR, Kurhade AM. Prevalence of pulmonary tuberculosis in HIV positive individuals and its association with CD4 count. J Evol Med Dent Sci 2015;4:3078-82.  Back to cited text no. 3
Bohara MS. Pulmonary tuberculosis and immunological profile of HIV/AIDS patients in far West Nepal. J Kathmandu Med Coll 2014;3:8-13.  Back to cited text no. 4
Ossibi Ibara BH, Bienvenu Rolland FH, Okombi O, Obengui, Mbemba Esther LP, Boumandouki JP, et al. Associated pulmonary Tuberculosis in HIV patients in depertments of infectious diseases of the university hospital of Brazzaville: Prevalence and associated factors. J Fran Viet Pneu 2016;20:24-8.  Back to cited text no. 5
Ahidjo A, Yusuph H, Tahir A. Radiographic features of pulmonary tuberculosis among HIV patients in Maiduguri, Nigeria. Ann Afr Med 2005;4:7-9.  Back to cited text no. 6
Said K, Verver S, Kalingonji A, Lwilla F, Mkopi A, Charalambous S, et al. Tuberculosis among HIV-infected population: Incidence and risk factors in rural Tanzania. Afr Health Sci 2017;17:208-15.  Back to cited text no. 7
Thorve SM, Patil N, Vora A. To study the incidence of pulmonary tuberculosis in newly diagnosed HIV patients. Asian Pac J Health Sci 2017;4:137-9.  Back to cited text no. 8
Badie BM, Mehran M, Mehran I, Maryam A, Neda A, Mehrnaz R. Comparing radiological features of pulmonary tuberculosis with and without HIV Infection. J AIDS Clin Res 2012;3:3.  Back to cited text no. 9
Awoyemi OB, Ige OM, Onadeko BO. Pattern of active pulmonary tuberculosis in human immunodeficiency virus seropositive adult patients in university college hospital, Ibadan, Nigeria. Afr J Med Med Sci 2002;31:25-31.  Back to cited text no. 10
Ali A, Ahmad F, Imran M, Atif M, Noor Y, Imran S, et al. Prevalence of pulmonary tubeculosis in HIV/AIDS subjects. Austin Virol Retrovirol 2016;3:1023.  Back to cited text no. 11
Desalu OO, Olokoba A, Danfulani M, Gambo Z, Salawu F, Danburam A, et al. Impact of immunosuppression on radiographic features of HIV related pulmonary tuberculosis among Nigerians. Turk Toraks Derg 2009;10:112-6.  Back to cited text no. 12
Bwana V, Tenu F, Magesa SM, Mfinanga SG. Smear positive pulmonary tuberculosis among HIV patients receiving highly active antiretroviral therapy in Dar es Salaam, Tanzania. Tanzan J Health Res 2011;13:14-20.  Back to cited text no. 13
Olatunji AA, Olatunji PO, Salako AA. Radiographic chest findings and immunological status in HIV-positive patients with tuberculosis coinfection in a sub-urban Nigerian tertiary hospital. Indian J Tuberc 2016;63:74-8.  Back to cited text no. 14
Kisembo HN, Boon SD, Davis JL, Okello R, Worodria W, Cattamanchi A, et al. Chest radiographic findings of pulmonary tuberculosis in severely immunocompromised patients with the human immunodeficiency virus. Br J Radiol 2012;85:e130-9.  Back to cited text no. 15
Peters EJ, Essien OE, Immananagha KK, Inah GA, Philip-Ephraim EE, Agbulu RE, et al. CD4 count levels and pattern of respiratory complications in HIV seropositive patients in Calabar, Nigeria. Niger J Physiol Sci 2007;22:93-7.  Back to cited text no. 16
Diagnostic standards and classification of tuberculosis in adults and children. This official statement of the American Thoracic Society and the centers for disease control and prevention was adopted by the ATS board of directors, July 1999. This statement was endorsed by the council of the infectious disease society of America, September 1999. Am J Respir Crit Care Med 2000;161:1376-95.  Back to cited text no. 17
Al-Ani A, Bingawi H, Hussein R. Status of HIV serology among pulmonary tuberculosis patients: The pattern of pulmonary tuberculosis and the characteristics of patients. J Int AIDS Soc 2012;15 Suppl 4:18414.   Back to cited text no. 18
Cardinale L, Parlatano D, Boccuzzi F, Onoscuri M, Volpicelli G, Veltri A, et al. The imaging spectrum of pulmonary tuberculosis. Acta Radiol 2015;56:557-64.  Back to cited text no. 19
Totad R, Lakkannavar SL, Ganganahalli P, Kalburgi MM. Study of pulmonary and extrapulmonary tuberculosis in HIV patients in co-relation to their CD4 count in Vijayapura district, Karanataka. Indian J Basic Appl Med Res 2016;5:537-42.  Back to cited text no. 20
Skoura E, Alimuddin Z, Jamshed B. Imaging in tuberculosis. Int J Infect Dis 2015;32:87-93.  Back to cited text no. 21
Hadadi A, Tajik P, Rasoolinejad M, Davoudi S, Mohraz M. Pulmonary tuberculosis in patients with HIV/AIDS in Iran. Iran J Public Health 2011;40:100-6.   Back to cited text no. 22
National Bureau of Statistics. Annual Abstract of Statistics National Bureau of Statistics; 2011. p. 1-698. Available from: http://www. nigerianstat.gov.ng. [Last accessed on 2018 May 20].   Back to cited text no. 23
Nadeemakar J, Mohammed AK. Pulmonary tuberculosis co-infection among HIV infected patients: A hospital based study from Bijapur, Southern India. J Evol Med Dent Sci 2015;4:2725-30.  Back to cited text no. 24


  [Table 1], [Table 2], [Table 3], [Table 4]

This article has been cited by
Aneri Parekh,Jigna Dave
[Pubmed] | [DOI]


Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
Access Statistics
Email Alert *
Add to My List *
* Registration required (free)

  In this article
Materials and Me...
Article Tables

 Article Access Statistics
    PDF Downloaded18    
    Comments [Add]    
    Cited by others 1    

Recommend this journal