ClinicalRadiology(1992) 46, 387 390
Tuberculosis in HIV Positive Patients in South Africa: A Comparative Radiological Study With HIV Negative Patients A. M. SAKS and R. P O S N E R *
Department of Radiology, Coronation Hospital, Johannesburg and *Department of Radiology, Morningside Hospital, Johannesburg, South Africa The radiological appearances of active tuberculosis in human immunodeficiency virus (HIV) positive patients was reviewed. A study group of 61 Black HIV positive patients and a control group of 50 Black HIV negative patients were analysed. The chest radiographs of the HIV seropositive group showed a significantly higher percentage of lymphadenopathy (50%), pleural effusions (38 %) and miliary (8%) or interstitial patterns (11%), as compared with those in the seronegative group (8%, 20%, 0% and 4% respectively). Cavitation (38%) and ateleetasis (31%) were less common in the seropositive group than in the seronegative group (82% in each category). Thus in an endemic TB environment an awareness of this difference in appearances will allow the radiologist to alert the referring clinician to the possibility of concomitant HIV seropositivity. Saks, A.M. & Posner, R. (1992). Clinical Radiology 46, 387-390. Tuberculosis in HIV Positive Patients in South Africa: A Comparative Radiological Study With H I V Negative Patients
Accepted for Publication 28 July 1992
Since 1985 several studies have drawn attention to the fact that H I V related tuberculosis (TB) presents with an atypical radiological picture, especially in patients with progressively severe immune suppression [1-3]. M a n y of these studies originated from the United States where TB is not endemic [4-6]. Studies from endemic TB areas have included reviews from Haiti, northern and central Africa [7-9]. To date, no studies have documented the radiological features in patients from Southern Africa. P A T I E N T S AND M E T H O D S A total of 111 chest radiographs of Black adults with active tuberculosis were reviewed, consisting of a study group of 61 H I V positive patients and a control group of 50 H I V negative patients. All the patients were admitted to either Baragwanath Hospital, Soweto, or to Rietfontein Sanatorium, which is a 300 bed referral centre for tuberculosis patients in the greater Johannesburg area. The control and study groups were age- and sexmatched (Fig. 1). Both groups of patients had similar socio-economic backgrounds. All diagnoses of active TB were confirmed either by positive sputum culture, which excluded Mycobacterium avium intraeellulare, or by appropriate lymph node, pleural, bone marrow or liver biopsy. South Africa has a government-funded compulsory neonatal Bacillus Calmette-Guerin (BCG) vaccination programme, and it was therefore assumed that most, if not all patients, had prior B C G vaccine exposure. Positive serology for H I V was confirmed on the E L I S A test for HIV-1 or the Western blot immunofluorescence test [10,11]. Frontal and lateral chest radiographs were interpreted Correspondence toi Dr A. M. Saks, Department of Radiology, Universityof Witwatersrand, Medical School, 7 York Road; Parktown, Johannesburg, 2193, South Africa.
independently by two qualified radiologists without prior knowledge of the H I V status of the patient. Discrepancies of interpretation were settled by consensus (four H I V negative cases; three H I V positive cases)~ Radiographs on which consensus could not be reached were discarded (one case from each group). Wherever concomitant chest infections were known to be present the patients were excluded from the study (seven patients). Both groups of chest films were evaluated for lymph node enlargement, pleural effusions, calcification, cavitation and parenchymal pattern. The abnormal parenchymal shadowings were categorized into six patterns: miliary, interstitial, nodular, alveolar consolidation, fibro-cavitatory or mixed (interstitial plus alveolar). More than one pattern could be recorded for a given film. The assessment of mediastinal lymph node enlargement was complicated by mediastinal distortion by adjacent
30
g -~ 2O ~6 E
10
Z
0 ~
< 24
25-34
35-44
45-54
> 55
Age (years)
I I Males Females lHIV+ (n = 61) [l~J ] MFemales ales lHIV- (n = Fig. 1 Age-sexdistribution of HIV + and HIV-- patients.
388
CLINICAL RADIOLOGY
fibrosis. Most of the cases were referred with only routine chest radiographs as computed tomography is not generally available outside the larger centres. All active TB cases in South Africa are hospitalized on presentation to undergo supervised anti-TB treatment. The radiographs used in our study were the presenting radiographs on admission to hospital. It can therefore be assumed that the radiographs represented fairly recent onset TB. The exact duration of disease could not be defined by many patients. Significant differences in findings were analysed using the Chi squared test and statistical significance was taken at P < 0.05. RESULTS During an 18 month period 111 chest radiographs were reviewed. Our study confirmed previous reports [8] that the mean age of HIV positive men (40 years), was significantly higher than that of HIV positive women (30 years). A comparison of the two groups of results showed that the HIV positive group had a significantly higher proportion ofadenopathy and effusions, and significantly less cavitation and atelectasis than the HIV negative group. Miliary and interstitial patterns were also more common in the seropositive group (Fig. 2).
Fig. 3 Frontal chest radiograph showing mediastinal adenopathy in an adult HIV seropositive patient with pulmonary tuberculosis.
Adenopathy Thirty of the 61 (50%) HIV positive patients demonstrated adenopathy on chest radiography. Of these 30 cases, 16 (51%) had hilar nodes, 22 (71%) had paratracheal nodes, nine (29%) aorta-pulmonary window nodes and five (16%) subcarinal nodes (Figs 3 and 4). Only four of the control cases had adenopathy. This was statistically significant ( P < 0.05). Pleural Effusions A total of 23 seropositive cases had radiographic evidence of basal effusions (38%). These were equally distributed on the left and right. The seronegative group had considerably fewer effusions (20%) (P < 0.05). Atelectasis Nineteen of the 61 study group radiographs (31%) revealed significant areas of fibrosis and resultant volume
1oo[ 80[-
Fig. 4 Frontal chest radiograph in an HIV seropositive patient, showing subcarinal adenopathy resulting in narrowing of the bronchus intermedius.
60p
,\\\'~
$ 40 13-
20
0Adenopathy •
Effusions
Calcificatiori
HIV+ (n = 61)
Cavitation
Atelectasis
[] H I V - (n = 50)
Fig. 2 - Comparison of radiological findings in HIV positive and HIV negative adult patients with pulmonary tuberculosis.
loss. This compared with 82% (41 cases) in the control group (P < 0.05). Both groups showed a strong upper lobe predominance for the atelectasis. There was no significant difference in either group between left or right sided involvement. Fifteen of the 19 study group cases with atelectasis had coexisting cavitatory changes, while all 41 of the control group showed fibrocavitatory changes. Calcifications Eight of the 61 (13%) HIV positive radiographs revealed obvious calcification within the lung paren-
TUBERCULOSIS IN HIV POSITIVE PATIENTS
389
demonstrated more nodular, mixed and fibrocayitatory patterns (Fig. 6). There was no statistically significant difference between the two groups in the number of patients with alveolar consolidation. In three HIV positive cases the lung parenchymal pattern was normal. Two of the cases had adenopathy only, and one had adenopathy plus an effusion. All the HIV negative cases had abnormal parenchymal patterns.
DISCUSSION
Fig. 5 - F r o n t a l chest radiograph in an HIV seropositive patient, demonstrating a bilateral reticulo-nodular pattern and mediastinal and hilar adenopathy.
100 8o
& 60
,N~
O~
,\"
40
Miliary Interstitial Fibrocav Normal Nodules Alveolar Mixed
Parenchymal pattern •
H I V + (n = 61)
[] H I V - (n = 50)
Fig. 6 - Comparison of lung parenchymal pattern in HIV + and H I V - adults with pulmonary tuberculosis.
chyma or within mediastinal nodes. This was not statistically different from 10 out of 50 cases present in the control group (P > 0.05).
Cavitation Twenty-three out of 61 radiographs (38 %) of the study group revealed cavitation and of these, 15 patients also had fibrotic disease. Forty-one of the 50 control cases (82%) had cavitation (P < 0.05). All 41 cases had significant areas of fibrosis associated with the cavitation.
Parenchymal Pattern A distinct difference in parenchymal patterns was found between the two groups. Patients with concomitant HIV and TB infections showed more miliary and interstitial patterns (Fig. 5), while the HIV negative patients
Tuberculosis is endemic in the Black population of South Africa with 68 578 new cases reported in 1990 [12]. However, it is estimated that less than 50% of the total number of new cases are diagnosed annually [13]. Up to 10 million individuals in South Africa are infected with the TB bacillus [13]. The number of HIV infected individuals in South Africa has shown a sharp increase in the past few years. There were an estimated 123 000 infected persons at the beginning of 1991, while the estimate for January 1992 has risen to 446 000 [14]. In recent years several articles have drawn attention to the fact that TB may be an early manifestation of HIV infection [3,15] and TB is now regarded as one of the most common infections in HIV-1 individuals in developing countries [9]. Reports from Africa reveal that up to 55% of patients in TB sanatoria are HIV positive [9]. The typical manifestation o f TB in South African adults is that of post-primary TB. The radiographic appearances are usually of cavitation, calcifications and upper lobe fibro-cavitatory changes. Studies of HIV patients with pulmonary TB have shown atypical appearances of adult onset TB [1,2,16], with an increased incidence of adenopathy, pleural effusions and abnormal parenchymal patterns, but less cavitation than in HIV negative tuberculosis patients. This primary pattern has been documented in areas where TB is an uncommon infection [6,15] as well as in TB endemic communities [7-9]. Our study confirms the atypical TB appearance, described in previous studies. The prevalence ofadenopathy (50%) and pleural effusions (38%) in our series is similar to previous reports. In HIV positive tuberculosis patients, adenopathy has been reported in 25-59% of cases [2-4, 6]. Pleural effusions have been recorded in 12-29% of cases [2,3,6]. Cavitation has been noted in various series varying from 0-22% [3,4,6,17]. Many of these studies, however, originated in the United States [4,6,17]. Studies from north and central Africa have shown a higher incidence of cavitation. Colebunders et al. [8] report 34% in Zaire. Our figure of 38% is more in line with the higher percentage noted in African studies. To the authors' knowledge, no other studies confirming this have been performed in Southern Africa. The high percentage of cavitation in African series may suggest a higher degree of infectivity in the endemic TB areas of Africa than in first world communities, where the percentage of patients with open tuberculous lesions is lower. In the African context, many TB patients are assessed and diagnosed on chest radiographs and sputum culture alone, without access to further costly laboratory or imaging procedures [9]. Despite the atypical appearance of TB in HIV related cases, few studies have stressed the
390
CLINICAL RADIOLOGY
importance of suspecting the diagnosis of HIV infection in patients with known pulmonary tuberculosis. A primary appearance of TB in an adult from a TB endemic area, should alert the radiologist to the possibility of concurrent HIV infection.
8
9 REFERENCES
1 Goldman KP. Aids and tuberculosis. British Medical Journal 1987;295:511-512. 2 Chaisson RE, Slutkin G. AIDS commentary. Tuberculosis and human immunodeficiency virus infection. Journal of Infectious Diseases 1989;159:96-100. 3 Barnes PF, Bloch AB, Davidson PT, Snider DE. Tuberculosis in patients with human immunodeficiency virus infection. Review article. New England Journal of Medicine 1991;324:1644 1650. 4 Pitchenik AE, Rubinson HA. The radiographic appearance of tuberculosis in patients with the acquired immunodeficiency syndrome (AIDS) and pre-AIDS. American Review of Respiratory Disease 1985;131:393 396. 5 Sunderam G, McDonald RJ, Maniatis T, Oleske J, Kapila R, Reichman LB. Tuberculosis as a manifestation of the acquired immunodeficiency syndrome (AIDS). Journal of the American Medical Association 1986;256:362-366. 6 Chaisson RE, Schecter GF, Theuer CP, Rutherford GW, Echenberg DF, Hopewell PC. Tuberculosis in patients with the acquired immunodeficiency syndrome. American Review o f Respiratory Disease 1987;136:570-574. 7 Mann JM, Snider DE, Francis H, Quinn TC, Colebunders RL, Piot Pet al. Association between HTLV- 111/LAV infection and tubercu-
10
11 12 13 14 15
16 17
losis in_ Zaire. Letter. Journal of American Medical Association 1986;256:346. Colebunders RL, Ryder RW, Nzilambi N, Dikilu K, Willarne j, Kaboto M e t al. H1V infection in patients with tuberculosis in Kinshasa, Zaire. American Review of Respiratory Disease 1989; 139:1082 1085. Harries AD. Tuberculosis and human immunodeficiency virus infection in developing countries. Review article. Laneet 1990;335:387 390. Shapiro M, Crookes RL, O'Sullivan E. Screening antenatal blood samples for anti-human immunodeficiency virus antibodies by a l~rge-pool enzyme-linked immunosorbent assay system. South African Medical Journal 1989;76:245 247. Abdool K, Salim S. Should AIDS be made notifiable? South African Medical Journal 1991;79:179-181. Kustner HGV. Tuberculosis in the Cape province. Epidemiological Comments 1991;18:30. Taylor SP, Benatar SR. The tuberculosis control programme a time to re-evaluate? Editorial. South African Medical Journal 1989;76:639-640. Schoub BD. AIDS in South Africa into the second decade. South African Medical Journal 1992;81:55-56. Buckner CB, Leithiser RE, Walker CW, Allison JW. Changing epidemiology of tuberculosis and other bacterial infections in the United States: Implications for the radiologist. Review article. American Journal of Radiology 1991;156:255-264. Rieder HL, Snider DE. Tuberculosis and the acquired immunodeficiency syndrome, Editorial. Chest 1986;90:469-470. Pitchenik AE, Burr J, Suarez M, Fertel D, Gonzalez G, Moas C, HTLV-I 11 seropositivity and related disease among 71 consecutive patients in whom tuberculosis was diagnosed. American Review of Respiratory Disease 1987; 135:875-879.
Tuberculosis in HIV Positive Patients in South Africa: A Comparative Radiological Study With HIV Negative Patients A. M. SAKS and R. P O S N E R *
Department of Radiology, Coronation Hospital, Johannesburg and *Department of Radiology, Morningside Hospital, Johannesburg, South Africa The radiological appearances of active tuberculosis in human immunodeficiency virus (HIV) positive patients was reviewed. A study group of 61 Black HIV positive patients and a control group of 50 Black HIV negative patients were analysed. The chest radiographs of the HIV seropositive group showed a significantly higher percentage of lymphadenopathy (50%), pleural effusions (38 %) and miliary (8%) or interstitial patterns (11%), as compared with those in the seronegative group (8%, 20%, 0% and 4% respectively). Cavitation (38%) and ateleetasis (31%) were less common in the seropositive group than in the seronegative group (82% in each category). Thus in an endemic TB environment an awareness of this difference in appearances will allow the radiologist to alert the referring clinician to the possibility of concomitant HIV seropositivity. Saks, A.M. & Posner, R. (1992). Clinical Radiology 46, 387-390. Tuberculosis in HIV Positive Patients in South Africa: A Comparative Radiological Study With H I V Negative Patients
Accepted for Publication 28 July 1992
Since 1985 several studies have drawn attention to the fact that H I V related tuberculosis (TB) presents with an atypical radiological picture, especially in patients with progressively severe immune suppression [1-3]. M a n y of these studies originated from the United States where TB is not endemic [4-6]. Studies from endemic TB areas have included reviews from Haiti, northern and central Africa [7-9]. To date, no studies have documented the radiological features in patients from Southern Africa. P A T I E N T S AND M E T H O D S A total of 111 chest radiographs of Black adults with active tuberculosis were reviewed, consisting of a study group of 61 H I V positive patients and a control group of 50 H I V negative patients. All the patients were admitted to either Baragwanath Hospital, Soweto, or to Rietfontein Sanatorium, which is a 300 bed referral centre for tuberculosis patients in the greater Johannesburg area. The control and study groups were age- and sexmatched (Fig. 1). Both groups of patients had similar socio-economic backgrounds. All diagnoses of active TB were confirmed either by positive sputum culture, which excluded Mycobacterium avium intraeellulare, or by appropriate lymph node, pleural, bone marrow or liver biopsy. South Africa has a government-funded compulsory neonatal Bacillus Calmette-Guerin (BCG) vaccination programme, and it was therefore assumed that most, if not all patients, had prior B C G vaccine exposure. Positive serology for H I V was confirmed on the E L I S A test for HIV-1 or the Western blot immunofluorescence test [10,11]. Frontal and lateral chest radiographs were interpreted Correspondence toi Dr A. M. Saks, Department of Radiology, Universityof Witwatersrand, Medical School, 7 York Road; Parktown, Johannesburg, 2193, South Africa.
independently by two qualified radiologists without prior knowledge of the H I V status of the patient. Discrepancies of interpretation were settled by consensus (four H I V negative cases; three H I V positive cases)~ Radiographs on which consensus could not be reached were discarded (one case from each group). Wherever concomitant chest infections were known to be present the patients were excluded from the study (seven patients). Both groups of chest films were evaluated for lymph node enlargement, pleural effusions, calcification, cavitation and parenchymal pattern. The abnormal parenchymal shadowings were categorized into six patterns: miliary, interstitial, nodular, alveolar consolidation, fibro-cavitatory or mixed (interstitial plus alveolar). More than one pattern could be recorded for a given film. The assessment of mediastinal lymph node enlargement was complicated by mediastinal distortion by adjacent
30
g -~ 2O ~6 E
10
Z
0 ~
< 24
25-34
35-44
45-54
> 55
Age (years)
I I Males Females lHIV+ (n = 61) [l~J ] MFemales ales lHIV- (n = Fig. 1 Age-sexdistribution of HIV + and HIV-- patients.
388
CLINICAL RADIOLOGY
fibrosis. Most of the cases were referred with only routine chest radiographs as computed tomography is not generally available outside the larger centres. All active TB cases in South Africa are hospitalized on presentation to undergo supervised anti-TB treatment. The radiographs used in our study were the presenting radiographs on admission to hospital. It can therefore be assumed that the radiographs represented fairly recent onset TB. The exact duration of disease could not be defined by many patients. Significant differences in findings were analysed using the Chi squared test and statistical significance was taken at P < 0.05. RESULTS During an 18 month period 111 chest radiographs were reviewed. Our study confirmed previous reports [8] that the mean age of HIV positive men (40 years), was significantly higher than that of HIV positive women (30 years). A comparison of the two groups of results showed that the HIV positive group had a significantly higher proportion ofadenopathy and effusions, and significantly less cavitation and atelectasis than the HIV negative group. Miliary and interstitial patterns were also more common in the seropositive group (Fig. 2).
Fig. 3 Frontal chest radiograph showing mediastinal adenopathy in an adult HIV seropositive patient with pulmonary tuberculosis.
Adenopathy Thirty of the 61 (50%) HIV positive patients demonstrated adenopathy on chest radiography. Of these 30 cases, 16 (51%) had hilar nodes, 22 (71%) had paratracheal nodes, nine (29%) aorta-pulmonary window nodes and five (16%) subcarinal nodes (Figs 3 and 4). Only four of the control cases had adenopathy. This was statistically significant ( P < 0.05). Pleural Effusions A total of 23 seropositive cases had radiographic evidence of basal effusions (38%). These were equally distributed on the left and right. The seronegative group had considerably fewer effusions (20%) (P < 0.05). Atelectasis Nineteen of the 61 study group radiographs (31%) revealed significant areas of fibrosis and resultant volume
1oo[ 80[-
Fig. 4 Frontal chest radiograph in an HIV seropositive patient, showing subcarinal adenopathy resulting in narrowing of the bronchus intermedius.
60p
,\\\'~
$ 40 13-
20
0Adenopathy •
Effusions
Calcificatiori
HIV+ (n = 61)
Cavitation
Atelectasis
[] H I V - (n = 50)
Fig. 2 - Comparison of radiological findings in HIV positive and HIV negative adult patients with pulmonary tuberculosis.
loss. This compared with 82% (41 cases) in the control group (P < 0.05). Both groups showed a strong upper lobe predominance for the atelectasis. There was no significant difference in either group between left or right sided involvement. Fifteen of the 19 study group cases with atelectasis had coexisting cavitatory changes, while all 41 of the control group showed fibrocavitatory changes. Calcifications Eight of the 61 (13%) HIV positive radiographs revealed obvious calcification within the lung paren-
TUBERCULOSIS IN HIV POSITIVE PATIENTS
389
demonstrated more nodular, mixed and fibrocayitatory patterns (Fig. 6). There was no statistically significant difference between the two groups in the number of patients with alveolar consolidation. In three HIV positive cases the lung parenchymal pattern was normal. Two of the cases had adenopathy only, and one had adenopathy plus an effusion. All the HIV negative cases had abnormal parenchymal patterns.
DISCUSSION
Fig. 5 - F r o n t a l chest radiograph in an HIV seropositive patient, demonstrating a bilateral reticulo-nodular pattern and mediastinal and hilar adenopathy.
100 8o
& 60
,N~
O~
,\"
40
Miliary Interstitial Fibrocav Normal Nodules Alveolar Mixed
Parenchymal pattern •
H I V + (n = 61)
[] H I V - (n = 50)
Fig. 6 - Comparison of lung parenchymal pattern in HIV + and H I V - adults with pulmonary tuberculosis.
chyma or within mediastinal nodes. This was not statistically different from 10 out of 50 cases present in the control group (P > 0.05).
Cavitation Twenty-three out of 61 radiographs (38 %) of the study group revealed cavitation and of these, 15 patients also had fibrotic disease. Forty-one of the 50 control cases (82%) had cavitation (P < 0.05). All 41 cases had significant areas of fibrosis associated with the cavitation.
Parenchymal Pattern A distinct difference in parenchymal patterns was found between the two groups. Patients with concomitant HIV and TB infections showed more miliary and interstitial patterns (Fig. 5), while the HIV negative patients
Tuberculosis is endemic in the Black population of South Africa with 68 578 new cases reported in 1990 [12]. However, it is estimated that less than 50% of the total number of new cases are diagnosed annually [13]. Up to 10 million individuals in South Africa are infected with the TB bacillus [13]. The number of HIV infected individuals in South Africa has shown a sharp increase in the past few years. There were an estimated 123 000 infected persons at the beginning of 1991, while the estimate for January 1992 has risen to 446 000 [14]. In recent years several articles have drawn attention to the fact that TB may be an early manifestation of HIV infection [3,15] and TB is now regarded as one of the most common infections in HIV-1 individuals in developing countries [9]. Reports from Africa reveal that up to 55% of patients in TB sanatoria are HIV positive [9]. The typical manifestation o f TB in South African adults is that of post-primary TB. The radiographic appearances are usually of cavitation, calcifications and upper lobe fibro-cavitatory changes. Studies of HIV patients with pulmonary TB have shown atypical appearances of adult onset TB [1,2,16], with an increased incidence of adenopathy, pleural effusions and abnormal parenchymal patterns, but less cavitation than in HIV negative tuberculosis patients. This primary pattern has been documented in areas where TB is an uncommon infection [6,15] as well as in TB endemic communities [7-9]. Our study confirms the atypical TB appearance, described in previous studies. The prevalence ofadenopathy (50%) and pleural effusions (38%) in our series is similar to previous reports. In HIV positive tuberculosis patients, adenopathy has been reported in 25-59% of cases [2-4, 6]. Pleural effusions have been recorded in 12-29% of cases [2,3,6]. Cavitation has been noted in various series varying from 0-22% [3,4,6,17]. Many of these studies, however, originated in the United States [4,6,17]. Studies from north and central Africa have shown a higher incidence of cavitation. Colebunders et al. [8] report 34% in Zaire. Our figure of 38% is more in line with the higher percentage noted in African studies. To the authors' knowledge, no other studies confirming this have been performed in Southern Africa. The high percentage of cavitation in African series may suggest a higher degree of infectivity in the endemic TB areas of Africa than in first world communities, where the percentage of patients with open tuberculous lesions is lower. In the African context, many TB patients are assessed and diagnosed on chest radiographs and sputum culture alone, without access to further costly laboratory or imaging procedures [9]. Despite the atypical appearance of TB in HIV related cases, few studies have stressed the
390
CLINICAL RADIOLOGY
importance of suspecting the diagnosis of HIV infection in patients with known pulmonary tuberculosis. A primary appearance of TB in an adult from a TB endemic area, should alert the radiologist to the possibility of concurrent HIV infection.
8
9 REFERENCES
1 Goldman KP. Aids and tuberculosis. British Medical Journal 1987;295:511-512. 2 Chaisson RE, Slutkin G. AIDS commentary. Tuberculosis and human immunodeficiency virus infection. Journal of Infectious Diseases 1989;159:96-100. 3 Barnes PF, Bloch AB, Davidson PT, Snider DE. Tuberculosis in patients with human immunodeficiency virus infection. Review article. New England Journal of Medicine 1991;324:1644 1650. 4 Pitchenik AE, Rubinson HA. The radiographic appearance of tuberculosis in patients with the acquired immunodeficiency syndrome (AIDS) and pre-AIDS. American Review of Respiratory Disease 1985;131:393 396. 5 Sunderam G, McDonald RJ, Maniatis T, Oleske J, Kapila R, Reichman LB. Tuberculosis as a manifestation of the acquired immunodeficiency syndrome (AIDS). Journal of the American Medical Association 1986;256:362-366. 6 Chaisson RE, Schecter GF, Theuer CP, Rutherford GW, Echenberg DF, Hopewell PC. Tuberculosis in patients with the acquired immunodeficiency syndrome. American Review o f Respiratory Disease 1987;136:570-574. 7 Mann JM, Snider DE, Francis H, Quinn TC, Colebunders RL, Piot Pet al. Association between HTLV- 111/LAV infection and tubercu-
10
11 12 13 14 15
16 17
losis in_ Zaire. Letter. Journal of American Medical Association 1986;256:346. Colebunders RL, Ryder RW, Nzilambi N, Dikilu K, Willarne j, Kaboto M e t al. H1V infection in patients with tuberculosis in Kinshasa, Zaire. American Review of Respiratory Disease 1989; 139:1082 1085. Harries AD. Tuberculosis and human immunodeficiency virus infection in developing countries. Review article. Laneet 1990;335:387 390. Shapiro M, Crookes RL, O'Sullivan E. Screening antenatal blood samples for anti-human immunodeficiency virus antibodies by a l~rge-pool enzyme-linked immunosorbent assay system. South African Medical Journal 1989;76:245 247. Abdool K, Salim S. Should AIDS be made notifiable? South African Medical Journal 1991;79:179-181. Kustner HGV. Tuberculosis in the Cape province. Epidemiological Comments 1991;18:30. Taylor SP, Benatar SR. The tuberculosis control programme a time to re-evaluate? Editorial. South African Medical Journal 1989;76:639-640. Schoub BD. AIDS in South Africa into the second decade. South African Medical Journal 1992;81:55-56. Buckner CB, Leithiser RE, Walker CW, Allison JW. Changing epidemiology of tuberculosis and other bacterial infections in the United States: Implications for the radiologist. Review article. American Journal of Radiology 1991;156:255-264. Rieder HL, Snider DE. Tuberculosis and the acquired immunodeficiency syndrome, Editorial. Chest 1986;90:469-470. Pitchenik AE, Burr J, Suarez M, Fertel D, Gonzalez G, Moas C, HTLV-I 11 seropositivity and related disease among 71 consecutive patients in whom tuberculosis was diagnosed. American Review of Respiratory Disease 1987; 135:875-879.
