The Impact of HIV Infection on Mycobacterium kansasii
Disease in South African Gold Miners
ELIZABETH L. CORBETT, GAVIN J. CHURCHYARD, MALCOLM HAY, PHILIP HERSELMAN, TIM CLAYTON,
BRIAN WILLIAMS, RICHARD HAYES, DAAN MULDER,† and KEVIN M. DE COCK
Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom;
Departments of Medicine, Radiology, and Occupational Health, Ernest Oppenheimer Hospital, Welkom, South Africa;
Epidemiology Research Unit, Johannesburg, South Africa; and Tropical Epidemiology and Public Health, Institute of
Social Medicine, University of Amsterdam, Amsterdam, The Netherlands
The impact of human immunodeficiency virus (HIV) infection on Mycobacterium kansasii disease in
miners was investigated with a retrospective study covering a single workforce. M. kansasii, isolated
from 43 HIV-positive and 202 HIV-negative miners, was the most common nontuberculous mycobac-
terial (NTM) species in both HIV groups. CD4 counts were unusually high for M. kansasii disease
(mean 490 106/L, from 14 HIV-positive men). Treatment outcomes were similar: mortality during
treatment was higher in HIV-positive than in HIV-negative men (9% and 2%, respectively), but not
significantly so. The majority of a sample of 31 HIV-positive and 92 HIV-negative men had radiologi-
cal silicosis and/or old tuberculosis scarring prior to M. kansasii disease. A normal premorbid radio-
graph was more common in HIV-positive men (45% versus 24%; odds ratio [OR], 2.62; 95% confi-
dence interval [95% CI], 1.01 to 6.67). New cavitation was less common (55% versus 78%; OR, 0.34;
95% CI, 0.13 to 0.88) and new hilar adenopathy more common (OR, 5.07; 95% CI, 1.24 to 21.9) in
HIV-positive than in HIV-negative men. Miners, who have additional NTM risk factors, develop M. kan-
sasii disease that occurs at an earlier stage of HIV infection and more closely resembles disease in HIV-
negative men than has been found for HIV-associated M. kansasii disease in other settings. Corbett
EL, Churchyard GJ, Hay M, Herselman P, Clayton T, Williams B, Hayes R, Mulder D, De Cock KM.
The impact of HIV infection on Mycobacterium kansasii disease in South African gold miners.
AM J RESPIR CRIT CARE MED 1999;160:10–14.
The human immunodeficiency virus (HIV) epidemic has is known about the effect of HIV on NTM disease in develop-
changed the epidemiology of nontuberculous mycobacterial ing countries. Disseminated disease due to M. avium complex
(NTM) disease. Patients with advanced HIV infection living in does occur in HIV-positive Africans, but is identified in life
the United States and Europe have a high incidence of Myco- (12, 13) and at autopsy examination (14) less frequently than
bacterium avium complex disease (1) and a smaller increase in in the United States or Europe.
the risk of disease caused by other NTM (2). HIV infection The aims of this retrospective study were to investigate the
also affects the clinical presentation and treatment outcome of impact of HIV infection on the clinical and radiological char-
NTM disease. For HIV-associated M. avium complex the typi- acteristics of Mycobacterium kansasii disease in South African
cal picture is a disseminated infection in a patient with far ad- gold miners. Miners have a high prevalence of chronic chest
vanced immunosuppression and little or no focal pulmonary disease (15), and pulmonary NTM disease was common be-
disease (1–3). The clinical and radiological features of HIV-asso- fore the HIV epidemic (16). The HIV epidemic has only re-
ciated NTM disease caused by other mycobacterial species are cently reached South Africa, but is spreading rapidly (17).
more heterogeneous and include a higher proportion of pa- HIV infection is a risk factor for pulmonary NTM disease in
tients with apparently limited pulmonary disease (3–11). Less miners (15), and HIV prevalence among miners treated for
NTM disease has risen from 4% in 1993 to 35% in 1997 (E. L.
Corbett, unpublished observation).
(Received in original form August 11, 1998 and in revised form December 23, 1998 )
Dr. Corbett is supported by a Wellcome Trust Training Fellowship in Clinical
Tropical Medicine. Patient Identification and Microbiology
Dr. De Cock is currently Director, Division of HIV/AIDS–Surveillance and Epidemi- HIV-tested male mineworkers from whom a sputum specimen had
ology, National Center for HIV, STD and TB Prevention, Centers for Disease Con- grown NTM between January 1, 1993 and June 30, 1996 were identi-
trol and Prevention, Atlanta, Georgia. fied from the tuberculosis (TB) clinic database of the Ernest Oppen-
Correspondence and requests for reprints should be addressed to Dr. E. L. Cor- heimer Hospital, Welkom, South Africa. This hospital is the sole
bett, c/o Department of Medicine, Ernest Oppenheimer Hospital, P.O. Box 87, source of tertiary care for miners working for a single large mining
Welkom 9460, South Africa. E-mail: email@example.com company.
Am J Respir Crit Care Med Vol 160. pp 10–14, 1999 Miners presenting either with symptoms suggestive of mycobacte-
Internet address: www.atsjournals.org rial disease or who were noted to have new radiological changes at
Corbett, Churchyard, Hay, et al.: HIV Infection and M. kansasii Disease 11
their annual medical examination were routinely screened for myco- zone score. Decisions were reached by consensus in cases of initial
bacterial disease with sputum microscopy and culture. Concentrated disagreement.
sputum samples were examined for mycobacteria using fluorescent
microscopy. Positive slides were confirmed with Ziehl-Neelsen stain- Additional Risk Factors for NTM Disease
ing. Initial culture of all sputum samples was onto Lowenstein-Jensen The job at the time of diagnosis was ascertained from company
(LJ) slopes. The number of colonies on positive LJ slopes was re- records. Jobs based at the rock face or involving the underground
corded as: scanty (1 to 19); 1 (20 to 99); 2 (100 to 200); 3 (more transport of ore were classed as dusty. Records of previous TB treat-
than 200). Positive LJ slopes were sent to the South African Institute ment were obtained from the TB clinic and hospital case notes.
of Medical Research (SAIMR), Johannesburg, for species identifica-
tion and drug sensitivity testing. The hospital policy was to send only a Treatment Outcomes
single LJ slope for identification per disease episode, unless further The duration of treatment and regimen used were at the discretion
positive cultures were obtained more than 6 mo later. The SAIMR of the attending physicians. The most common regimen used was a
laboratory used standard biochemical tests to distinguish different combination of rifampicin, ethionamide, and ethambutol. Patients
NTM species. All miners found to have a positive mycobacterial iso- no longer taking treatment were classified into the following groups:
late were referred to the TB clinic and recorded on the database re- cured—a negative sputum culture within 3 mo of stopping treatment;
gardless of the species of the isolate. HIV testing has been offered to completed—completed treatment but no sputum cultures taken within
TB and NTM patients from 1993, with pre- and post-test counseling. 3 mo of stopping treatment; failure—positive sputum culture within
CD4 lymphocyte measurement (CD4 count) was carried out in some 3 mo of stopping treatment; defaulted—lost to follow-up before com-
but not all HIV-positive miners with mycobacterial disease. pletion of treatment; transferred out—left the mines before comple-
Ethical approval for the study was obtained from the ethics com- tion; died on treatment—died of any cause before completion.
mittees of the Ernest Oppenheimer Hospital and the London School
of Hygiene and Tropical Medicine. Statistical Analysis
Data were analyzed using STATA 5.0 (Stata Corporation, College
Radiology Station, TX) and EPI-INFO 6.02 (Centers for Disease Control, At-
A total of 108 HIV-negative and 36 HIV-positive M. kansasii patients lanta, GA) statistical software. Odds ratios (OR) and exact 95% con-
was selected for radiological review of both presenting and premorbid fidence intervals (95% CI) were used to compare radiological features
radiographs. Patients with relapsed disease and those who had been between patients grouped according to HIV status. A chi-squared test
treated for TB within the previous 12 mo were not considered for in- for trend was used to compare the number of NTM risk factors per
clusion because of the unavailability of a stable premorbid radiograph patient and the extent of radiological disease in HIV-positive and
in such cases. All HIV-positive patients who did not have either of HIV-negative men. In order to avoid including cases of nonpatho-
these exclusion criteria were included. The HIV-negative patients genic infection with a test for disease severity, patients who had no
were selected by including the next three HIV-negative patients pre- new radiological changes were excluded from the latter analysis.
senting after each HIV-positive patient.
For each patient a premorbid radiograph taken at least 12 mo be- RESULTS
fore diagnosis was identified either from the annual screening mini-
chest radiographs or from standard-sized radiographs when available.
There were 406 miners from whom a single fully identified
Serial radiographs were screened and only radiographs that had been NTM had been cultured during the specified time period. Of
static for 12 mo were included as premorbid radiographs, in order to these, 366 (90%) had been tested for HIV, and 69 (19%) of
avoid including radiographs with active slowly progressive mycobacte- those tested for HIV were positive. The NTM species distribu-
rial disease. Where this was suspected an earlier radiograph was used tion did not vary significantly according to HIV status (p
instead. Presenting radiographs, taken within 2 wk of mycobacterial 0.34): the most frequent species was M. kansasii, isolated from
disease diagnosis, were read together with the premorbid radiograph 202 (68%) HIV-negative and 43 (62%) HIV-positive men, fol-
by two independent readers using a standardized scoring system that lowed by Mycobacterium scrofulaceum, which was isolated
included an assessment of the presenting radiograph, the premorbid from 41 (14%) HIV-negative and eight (12%) HIV-positive
radiograph, and new changes apparent from the differences between
men. M. avium complex was isolated from 18 (6%) and four
the two radiographs. Thin-walled cavities were defined as cavities where
the thickness of part or all of the cavity wall was 1 mm or less. Abnor- (6%) HIV-negative and HIV-positive men, respectively, and
malities were defined as being either upper or lower field by their there were 36 (12%) and 14 (20%) other NTM isolates of spe-
position relative to the ipsilateral hilum. Each lung was divided cies not normally considered pathogenic isolated from HIV-
into three zones of equal vertical height at the midclavicular line. negative and HIV-positive men, respectively.
The number of zones that contained an abnormality was summed as a The patient characteristics, sputum smear results, and nonra-
diological NTM risk factors for HIV-positive and HIV-negative
men with M. kansasii isolates are shown in Table 1. All men
with M. kansasii isolates, apart from one HIV-negative man,
TABLE 1 were treated for M. kansasii disease. There was a lower propor-
tion of smear-positive patients in the HIV-positive group, but
CHARACTERISTICS OF HIV-POSITIVE AND
HIV-NEGATIVE MEN WITH M. kansasii ISOLATES
this was not significant (OR, 0.60; 95% CI, 0.27 to 1.41). The
proportion of patients with a past history of TB treatment was
HIV-positive HIV-negative 95% CI/ nonsignificantly higher in HIV-negative than in HIV-positive
Characteristic (n 43) (n 202) OR p Value men, and the majority of patients in both groups were working
Age, yr, mean SD 41.7 7.8 44.1 7.4 p 0.07* in dusty jobs at the time of their diagnosis.
Smear-positive 31 (72%) 164 (81%) 0.60 0.27–1.41 CD4 counts are not routinely requested on HIV-positive
LJ growth density† NTM patients, but 14 of the HIV-positive M. kansasii patients
1–19 colonies 19 (44%) 87 (43%)
(33%) had a CD4 count estimated within 6 mo of diagnosis.
20–99 colonies 10 (23%) 49 (24%)
100 colonies or more 14 (33%) 66 (33%)
The mean CD4 count was 490 106/L (SD, 388) with a range
Past TB treatment 14 (33%) 88 (44%) 0.63 0.29–1.31 of 1,431 to 73 106/L. Only two patients had a CD4 count be-
Dusty job 38 (88%) 178 (88%) 1.02 0.35–3.66 low 100 106/L.
Treatment outcomes for patients who were no longer on
* Student’s t test.
Number of mycobacterial colonies on the LJ slope from which M. kansasii was iden- treatment by January 1997 are shown in Table 2. The number
tified. of patients dying on treatment was small. This outcome was
12 AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE VOL 160 1999
TABLE 2 cant for the HIV-negative men (CI, 1.04 to 12.6) but not for the
TREATMENT OUTCOMES IN PATIENTS NO LONGER smaller HIV-positive group (CI, 0.52 to 50.1).
ON TREATMENT, ACCORDING TO HIV STATUS* The number of identifiable NTM risk factors per patient,
other than HIV infection, were calculated for the M. kansasii
Outcome (n 33) (n 179) patients who were included in the radiological study. The four
risk factors considered were: dusty job, past history of TB
Cured 14 (42%) 82 (46%)
treatment, silicosis, and premorbid focal radiological scarring.
Treatment completed 10 (30%) 62 (35%)
Treatment failure 0 (0%) 5 (3%)
These data are shown for men grouped according to HIV sta-
Transferred out 3 (9%) 22 (12%) tus in Table 4. There were fewer risk factors per man for HIV-
Defaulted 3 (9%) 5 (3%) positive than for HIV-negative patients ( 2 test for trend, p =
Died on treatment 3 (9%) 3 (2%) 0.01), but only 10% of HIV-positive men had no other risk
* Ten HIV-positive and 22 HIV-negative men were still on treatment at the time of
factor for NTM disease.
review. One HIV-negative man was not treated.
Most of the patients included in this study were treated for
M. kansasii disease on the basis of suggestive clinical and ra-
more common in the HIV-positive group, but not significantly
diological features in association with a single sputum NTM
so (OR, 5.9; 95% CI, 0.74 to 45.3). Drug choice and treatment
isolate. The diagnosis of NTM disease in individual cases can-
duration did not differ by HIV status (median duration, 17 mo
not be made with confidence on the basis of a single NTM iso-
for HIV-positive and HIV-negative patients). A higher pro-
late from nonsterile sites because of the alternative possibilities
portion of the HIV-positive patients were still on treatment at
of nonpathogenic colonization and specimen contamination.
the time of review, but this was because more were diagnosed
However, it is likely that most of the isolates from patients in
in the later years of the study period.
this study did represent NTM disease as the majority from
Either the presenting or a suitable premorbid radiograph
both HIV groups were associated with other features of active
could not be found for five (13%) of the HIV-positive and 16
mycobacterial disease and M. kansasii sputum isolates have
(15%) of the HIV-negative men selected for radiological re-
previously been shown to have a high likelihood of represent-
view. The radiological changes associated with M. kansasii iso-
ing NTM disease in both HIV-negative and HIV-positive indi-
lates are shown for both HIV-positive and HIV-negative men
viduals (4–9, 18).
in Table 3. Significant differences between the two HIV groups
The HIV epidemic in the United States and Europe has
were that the HIV-positive men were more likely to have a
been accompanied by both an increasing incidence and a
normal premorbid radiograph (OR, 2.62; 95% CI, 1.01 to 6.67)
changing spectrum of NTM disease. Before the HIV epi-
and less likely to have focal scarring suggestive of previous
demic, NTM disease occurred with a low incidence, mainly in
healed TB (OR, 0.27; 95% CI, 0.10 to 0.68). New cavitation
older individuals with underlying chronic lung disease. The
was significantly less common (OR, 0.34; 95% CI, 0.13 to 0.88)
predominant disease-associated NTM organism varied from
and new hilar adenopathy was significantly more common
one geographical location to another and the typical presenta-
(OR, 5.07; 95% CI, 1.24 to 21.9) in the HIV-positive group.
tion of NTM disease in adults was as a localized pulmonary in-
Men with new cavities were more commonly smear-positive
fection that resembled tuberculosis radiologically. This con-
than men without new cavities in both HIV groups (OR, 3.70
trasts with HIV-associated NTM disease in the United States
for HIV-negative men and 4.17 for HIV-positive men). The as-
and Europe, which occurs with a high incidence and where the
sociation between new cavities and smear positivity was signifi-
majority of patients present with a disseminated M. avium in-
fection with no pulmonary focus and no predisposing factors
apart from advanced HIV infection (1–3). HIV-associated
TABLE 3 M. kansasii disease is less common, but still occurs with an in-
RADIOLOGICAL FEATURES ASSOCIATED WITH ISOLATES OF creased incidence, mainly in patients with advanced immuno-
M. kansasii FROM HIV-POSITIVE AND HIV-NEGATIVE MEN suppression. Previous reports of the radiological manifesta-
tions of HIV-associated M. kansasii have identified focal
Feature (n 31) (n 92) OR 95% CI
pulmonary disease in most patients, with apparently limited
pulmonary disease in a sizeable minority, but have found cavi-
Premorbid radiograph tation to be atypical and present in the minority (4–9). The
Silicosis 10 (32%) 43 (47%) 0.54 0.21–1.37
Focal scarring 10 (32%) 59 (64%) 0.27 0.10–0.68
prognosis after a diagnosis of disseminated NTM disease has
Old cavitation 8 (26%) 28 (30%) 0.80 0.27–2.13
Normal radiograph 14 (45%) 22 (24%) 2.62 1.01–6.67
New changes TABLE 4
Cavitation 17 (55%) 72 (78%) 0.34 0.13–0.88
Thin-walled cavities 12 (39%) 42 (46%) 0.75 0.30–1.86 NUMBER OF NON-HIV RISK FACTORS* FOR NTM
Fibrosis/volume loss 8 (26%) 40 (44%) 0.45 0.16–1.19 DISEASE IN HIV-POSITIVE AND HIV-NEGATIVE
Upper field infiltrate 26 (84%) 82 (89%) 0.63 0.18–2.60 PATIENTS WITH M. kansasii ISOLATES
Lower field infiltrate 9 (29%) 17 (19%) 1.80 0.62–5.00
Number of HIV-positive HIV-negative
Pleural thickening 7 (23%) 30 (33%) 0.60 0.20–1.66
Risk Factors (n 31) (n 92)
Pleural effusion 3 (10%) 7 (8%) 1.30 0.20–6.18
Hilar adenopathy 7 (23%) 5 (5%) 5.07 1.24–21.86 0 3 (10%) 2 (2%)
Extent of new disease 1 10 (32%) 19 (21%)
None 1 (3%) 5 (5%) 2 9 (29%) 28 (30%)
1 zone 15 (48%) 42 (48%) 1 pT 0.87* 3 8 (26%) 32 (35%)
2 zones 6 (19%) 23 (25%) 0.73 0.22–2.38 4 1 (3%) 11 (12%)
3 zones or more 9 (29%) 22 (24%) 1.15 0.38–3.34
* Risk factors considered were: dusty job, past history of TB treatment, silicosis, and
* Test for trend for zone scores (not including patients who had no new changes). premorbid focal radiological scarring. Test for trend, 2 6.0, p 0.01.
Corbett, Churchyard, Hay, et al.: HIV Infection and M. kansasii Disease 13
been poor, mainly reflecting the advanced degree of immuno- and mortality are likely to increase further among miners as
suppression although NTM disease itself contributes to the the HIV epidemic progresses. Clinicians should be aware that
high mortality (4–9, 19). Before the availability of highly ac- HIV-infected individuals who also have other NTM risk fac-
tive antiretroviral regimens, the median survival time after a tors may be at an increased risk of developing pulmonary
diagnosis of disseminated M. avium disease was in the order of NTM disease early in the course of their HIV disease. The
6 mo (19) and was similar for M. kansasii disease (4–9). NTM good short-term prognosis found in this study for pulmonary
disease, with a similar clinical picture and predominance of NTM disease associated with early HIV infection may be rele-
M. avium complex, has also been identified in patients with vant for similar patients elsewhere.
acquired immunodeficiency syndrome (AIDS) from several
Acknowledgment : Daan Mulder died in October 1998 and will be greatly
African countries, but with a much lower prevalence (12–14). missed by his colleagues. The authors gratefully acknowledge Carol Van
The effect of HIV infection on NTM disease in the South Blommestein, who manages the TB database and helped with patient iden-
African miners described here is different from that found tification and microbiological data; Jake Mjandana and Tuso Ramolahloane
elsewhere. There was no significant effect of HIV infection on for locating the radiographs used in the study, and Hetta Steyn and Louis
Von Rensberg for supplying occupational records.
the bacteriological spectrum of NTM disease, with the pre-
dominant isolates being M. kansasii followed by M. scrofula-
ceum in both HIV status groups. The majority of HIV-positive References
M. kansasii patients presented with typical upper field cavitary 1. Nightingale, S. D., L. T. Byrd, P. M. Southern, J. D. Jockusch, S. X. Cal,
disease and 72% of the HIV-positive men not still on treat- and B. A. Wynne. 1993. Incidence of Mycobacterium avium-intracellu-
ment were known to have survived the full duration of their lare complex bacteraemia in human immunodeficiency virus–positive
treatment course. The available CD4 counts were consider- patients. J. Infect. Dis. 165:1082–1085.
2. Falkinham, J. O. 1996. Epidemiology of infection by nontuberculous my-
ably higher than those reported from HIV-positive M. kan- cobacteria. Clin. Microbiol. Rev. 9:177–212.
sasii patients in the United States (2, 4–9), suggesting that 3. Rigsby, M. O., and A. M. Curtis. 1994. Pulmonary disease from nontu-
M. kansasii disease is occurring earlier in the course of HIV berculous mycobacteria in patients with human immunodeficiency vi-
infection. This is in keeping with the low mortality during rus. Chest 106:913–919.
treatment in the HIV-positive group. 4. Lillo, M., S. Orengo, P. Ceroch, and R. L. Harris. 1990. Pulmonary and
There were, however, differences in the manifestations of disseminated infection due to Mycobacterium kansasii: a decade of ex-
perience. Rev. Infect. Dis. 12:760–767.
M. kansasii disease between the two HIV status groups. HIV- 5. Levine, B., and R. E. Chaisson. 1991. Mycobacterium kansasii: a cause of
positive men were less likely to have new cavitation. There treatable pulmonary disease associated with advanced human immu-
was a higher proportion of patients with hilar adenopathy and nodeficiency virus infection. Ann. Intern. Med. 114:861–868.
a less clear-cut upper field predominance in the radiographs 6. Carpenter, J. L., and J. M. Parks. 1991. Mycobacterium kansasii infec-
from HIV-positive compared with HIV-negative M. kansasii tions in patients positive for human immunodeficiency virus. Rev. In-
patients. There was also a higher mortality during treatment in fect. Dis. 13:788–796.
7. Valainis, G. T., L. M. Cardona, and D. L. Greer. 1991. The spectrum of
the HIV-positive patients, although numbers were small and Mycobacterium kansasii disease associated with HIV-1 infected pa-
the difference was not significant. tients. J. Acquired Immune Defic. Syndr. 4:516–520.
The clinical and radiological appearances of HIV-associ- 8. Bamberger, D. M., M. R. Driks, M. R. Gupta, M. C. O’Connor, P. M.
ated M. kansasii disease at this location are reminiscent of Jost, R. E. Neihart, D. S. McKinsey, L. A. Moore, and the Kansas City
patients with early HIV infection and Mycobacterium tubercu- AIDS Research Consortium. 1994. Mycobacterium kansasii among
losis disease (20, 21). The impact of HIV infection on the ra- patients infected with human immunodeficiency virus in Kansas City.
Clin. Infect. Dis. 18:395–400.
diological presentation of M. tuberculosis disease becomes 9. Witzig, R. S., B. A. Fazal, R. M. Mera, D. M. Mushatt, P. M. J. T. Dejace,
more marked with increasing immunosuppression (20, 21). D. L. Greer, and N. E. Hyslop. 1995. Clinical manifestations and im-
The limited impact of HIV infection found in this study, com- plications of coinfection with Mycobacterium kansasii and human im-
pared with previous reports of a marked effect in patients with munodeficiency virus. Clin. Infect. Dis. 21:77–85.
more advanced HIV disease, supports a similar relationship 10. Shafer, R. W., and M. F. Sierra. 1992. Mycobacterium xenopi, Mycobac-
between the degree of HIV-associated immunosuppression terium fortuitum, Mycobacterium kansasii, and other nontuberculous
mycobacteria in an area of endemicity for AIDS. Clin. Infect. Dis. 15:
and the radiological presentation of M. kansasii disease. 161–162.
The question as to why HIV-associated M. kansasii disease 11. Saunders, J. W., A. D. Walsh, R. L. Snider, and E. E. Sahn. 1994. Dis-
is occurring at such an early stage of HIV infection in miners seminated Mycobacterium scrofulaceum infection: a potentially treat-
may be best answered by considering other risk factors for able complication of AIDS. Clin. Infect. Dis. 20:549–556.
NTM disease. NTM disease was common in this workforce be- 12. Morrisey, A. B., T. O. Aisu, J. O. Falkinham, P. P. Eriki, J. J. Ellner, and
fore the HIV epidemic (16), probably attributable to the high T. M. Daniel. 1993. Absence of bacteraemia with Mycobacterium
avium complex in patients with AIDS in Uganda. J. Infect. Dis. 162:
prevalence of other risk factors such as a dusty job, silicosis, 208–210.
and post-tuberculous lung disease, each of which has been 13. Gilks, C. F., R. J. Brindle, C. Mwachari, B. Batchelor, J. Bwayo, J. Ki-
shown to be significantly associated with NTM disease in min- mari, D. A. Arbeit, and C. F. von Reyn. 1995. Disseminated Mycobac-
ers (15). HIV infection is also a significant risk factor for NTM terium avium infection among HIV-infected patients in Kenya. J. Ac-
disease in miners, but is not currently the predominant one quired Immune Defic. Syndr. Hum. Retrovirol. 8:195–198.
(15). Of note, only a small minority of the HIV-positive men 14. Lucas, S. B., A. Hounnou, C. Peacock, A. Beaumel, G. Djomand, J.
N’Gbichi, K. Yeboue, M. Hond’, M. Diomande, C. Giordano, R.
described here had no additional NTM risk factor identified, Doorly, K. Brattegaard, L. Kestens, R. Smithwick, A. Kadio, N.
although they did tend to have fewer other risk factors than Ezani, A. Yapi, and K. M. De Cock. 1993. The mortality and pathol-
the HIV-negative men. ogy of HIV infection in a West African city. AIDS 7:1569–1579.
Taken together, the results from this study suggest that the 15. Corbett, E. L., G. J. Churchyard, T. Clayton, P. Herselman, B. Williams,
effects of different NTM risk factors in this population may be R. Hayes, D. Mulder, and K. M. De Cock. 1999. Risk factors for pul-
combining and so allowing HIV infection to result in M. kan- monary mycobacterial disease in South African gold miners: a case-
control study. Am. J. Respir. Crit. Care Med. 159:94–99.
sasii disease that occurs at a considerably lesser degree of 16. Cowie, R. L. 1990. The mycobacteriology of pulmonary tuberculosis in
immunosuppression and more closely resembles disease in South African gold miners. Tubercle 71:39–42.
HIV-negative men than is the case with HIV-associated NTM 17. Williams, B., and C. Campbell. 1998. Understanding the epidemic of
disease in other settings. NTM disease incidence, morbidity, HIV in South Africa. S. Afr. Med. J. 88:247–251.
14 AMERICAN JOURNAL OF RESPIRATORY AND CRITICAL CARE MEDICINE VOL 160 1999
18. O’Brien, R. J., I. J. Geiter, and D. E. Snider. 1987. The epidemiology of 20. Greenberg, S. D., D. Frager, B. Suster, S. Walker, C. Stavropoulos, and
nontuberculous mycobacterial disease in the United States: results A. Rothpearl. 1994. Active pulmonary tuberculosis in patients with
from a national survey. Am. Rev. Respir. Dis. 135:1007–1014. AIDS: spectrum of radiographic findings (including a normal appear-
19. Shafran, S. D., J. Singer, D. P. Zarowny, P. Phillips, I. Salit, S. L. Walms- ance). Radiol. 193:115–119.
ley, I. Fong, J. Gill, A. R. Rachlis, R. G. Lalonde, M. M. Fanning, and 21. Abouya, L., I.-M. Coulibaly, D. Coulibaly, S. Kassin, A. Ackah, A. E.
C. M. Tsoukas. 1996. A comparison of two regimens for the treatment Greenberg, S. Z. Wiktor, and K. M. De Cock. 1995. Radiological man-
of Mycobacterium avium complex bacteraemia in AIDS: rifabutin, ifestations of pulmonary tuberculosis in HIV-1 and HIV-2-infected
ethambutol and clarithromycin versus rifampin, ethambutol, clo- patients in Abidjan, Cote d’Ivoire. Tub. Lung Dis. 76:436–440.
fazamine and ciprofloxacin. N. Engl. J. Med. 335:377–383.