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Original Research: MYCOBACTERIAL DISEASE |

Detailed Analysis of the Radiographic Presentation of Mycobacterium kansasii Lung Disease in Patients With HIV Infection* FREE TO VIEW

Adithya Cattamanchi, MD; Payam Nahid, MD, MPH; Theodore K. Marras, MD, FCCP; Michael B. Gotway, MD; Theodore J. Lee, MD; Leah C. Gonzalez, DS; Alison Morris, MD, MS; W. Richard Webb, MD; Dennis H. Osmond, PhD; Charles L. Daley, MD
Author and Funding Information

Affiliations: *From the University of California, San Francisco (Drs. Cattamanchi, Nahid, Gotway, Lee, Webb, Osmond, and Gonzalez), San Francisco, CA; University of Toronto (Dr. Marras), Toronto, ON, Canada; University of Pittsburgh (Dr. Morris), Pittsburgh, PA; and National Jewish Medical and Research Center (Dr. Daley), Denver, CO.,  Drs. Cattamanchi and Nahid contributed equally to the study.

Correspondence to: Adithya Cattamanchi, MD, San Francisco General Hospital, Room 5K1, 1001 Potrero Ave, San Francisco, CA 94110; e-mail: acattamanchi@medsfgh.ucsf.edu



Chest. 2008;133(4):875-880. doi:10.1378/chest.07-2171
Text Size: A A A
Published online

Background: Published criteria for the diagnosis of Mycobacterium kansasii lung disease require the presence of clinical symptoms, positive microbiologic results, and radiographic abnormalities. In patients with HIV infection, the radiographic findings of M kansasii lung disease are not well described.

Methods: Medical records and chest radiographs of all patients with HIV infection and at least one respiratory specimen culture positive for M kansasii at San Francisco General Hospital between December 1989 and July 2002 were reviewed.

Results: Chest radiographic results were abnormal in 75 of 83 patients (90%) included in the study. Radiographic abnormalities were diverse, with consolidation (66%) and nodules (42%) as the most frequent findings. The mid or lower lung zones were involved in 89% of patients. The pattern of radiographic abnormalities did not differ based on acid-fast bacilli smear status, the presence or absence of coexisting pulmonary infections, or CD4+ T-lymphocyte count. In multivariate Cox regression analysis, cavitation was the only radiographic abnormality independently associated with mortality (hazard ratio, 4.8; 95% confidence interval, 1.2 to 19.6).

Conclusion: Patients with HIV infection and M kansasii lung disease present with diverse radiographic patterns, most commonly consolidation and nodules predominantly located in the mid and lower lung zones. This finding is in contrast to the upper-lobe cavitary presentation described in patients without HIV infection. Although rare, the presence of cavitary disease in patients with HIV infection and M kansasii independently predicts worse outcome. The diversity in the radiographic presentation of M kansasii lung disease implies that clinicians should obtain sputum mycobacterial culture samples from any patient with HIV infection and an abnormal chest radiograph finding.

Figures in this Article

Mycobacterium kansasii is the second-most- common nontuberculous mycobacteria (NTM) species isolated from patients with HIV infection and is considered to be the most pathogenic.13 When isolated from a respiratory specimen, M kansasii is far more likely than other NTM species to be associated with clinically significant disease.,1,4However, as with other NTM species, M kansasii is considered an environmental mycobacterium, with tap water as the primary reservoir, and isolation from respiratory specimens may not indicate true pulmonary disease. Consequently, diagnostic criteria for pulmonary disease revised by the American Thoracic Society (ATS) and the Infectious Diseases Society of America (IDSA) require the isolation of NTM in two or more sputum specimens in addition to clinical symptoms and chest radiographic abnormalities.5

In immunocompetent persons, symptoms of M kansasii lung disease and chest radiographic abnormalities are reported to be similar to postprimary pulmonary tuberculosis, including cavitary consolidation with an upper-lobe predilection.67 In patients with HIV infection, the clinical and radiographic presentation of M kansasii lung disease has not been well described, and the association between radiographic presentation and clinical outcome has not been assessed.

We previously demonstrated that in patients with HIV infection and M kansasii isolated from a respiratory specimen, mortality was independent of the 1997 ATS/IDSA diagnostic criteria and was instead associated with lower CD4+ T-lymphocyte cell counts, positive smear microscopy, lack of antiretroviral therapy, and failure to receive adequate treatment with a minimum of three medications with activity against M kansasii.8 In the current study, we provide a detailed analysis of radiographic findings in this cohort and evaluate whether radiographic presentation is associated with clinical outcome.

Study Population

The study cohort consists of all patients with HIV infection who had at least one respiratory specimen culture positive for M kansasii at the microbiology laboratories of San Francisco General Hospital between December 1989 and July 2002. The study was approved by the University of California, San Francisco Committee on Human Research. Patients were included if they had the following: (1) chest radiographs available for independent review, and (2) at least three respiratory specimens submitted for mycobacterial culture, in order to meet the minimum evaluation recommended by the ATS/IDSA for patients with suspected NTM lung disease.5 Radiographic findings were assessed in the population overall and in stratified analyses based on CD4+ T-lymphocyte count, acid-fast bacilli (AFB) smear status, presence or absence of coexisting pulmonary infections, and ATS/IDSA criteria for NTM lung disease. Patients were classified as having ATS/IDSA-defined disease if all four of the following criteria were present: (1) pulmonary symptoms; (2) reasonable exclusion of other disease as the cause of the symptoms; (3) parenchymal abnormalities on chest radiograph; and (4) positive M kansasii culture finding from at least two sputum specimens or positive culture result from one bronchial lavage or transbronchial lung biopsy (with consistent mycobacterial histopathologic features).,5

Chest Radiograph Interpretation

The chest radiographs chosen for review were those images closest in time to the date of the first positive respiratory culture result. All chest radiographs were reviewed by expert thoracic radiologists (M.B.G. and T.J.L.) and pulmonary physicians experienced with mycobacterial disease (T.K.M., C.L.D., A.M.). The radiographic findings were abstracted using a standardized form. When present, the following abnormalities were noted: cavitation, consolidation, nodules, reticulation, hilar or mediastinal lymphadenopathy, and pleural effusion. For parenchymal abnormalities, the location was classified as upper, middle, or lower lung zone by dividing the lungs into thirds. All reviewers were blinded to clinical information at the time of review. The two thoracic radiologists reviewed the cases independently, and resolved any differences through consensus discussion, providing a single review. The three pulmonary physicians also reviewed chest radiographs independently. At least two of the three pulmonologists reviewed each chest radiograph, providing a total of three independent reviews for each chest radiograph (one from the radiologists and two from pulmonologists). Agreement regarding findings was considered present when two of the three reviews agreed on the chest radiographic findings. When majority agreement regarding presence or absence of one or more radiographic findings among the three reviews was not present, an experienced thoracic radiologist (W.R.W.) provided adjudication.

Statistical Analysis

Data were analyzed using statistical software (STATA 9.0; Stata Corporation; College Station, TX; and Microsoft Excel; Microsoft Corporation; Redmond, WA). Proportions were compared using the χ2 or Fisher exact tests. Medians were compared using the Mann-Whitney U test. The associations between specific radiographic findings and overall mortality were assessed with Kaplan-Meier survival analysis (log-rank test) for categorical predictors and univariate Cox regression for continuous predictors. Patient charts were reviewed up to 2 years from the time of initial positive respiratory culture finding to assess overall mortality. Predictors of overall mortality with p < 0.25 in univariate analysis were assessed in a multivariate Cox proportional hazards model. The interaction of antiretroviral therapy and time was found to be significant and was modeled in the final analysis.

Study Population

Between 1989 and 2002, 123 patients with HIV infection were identified with M kansasii isolated from one or more respiratory specimens. Chest radiographs were not available for review in 31 patients, and an additional 9 patients had fewer than three sputum specimens submitted for mycobacterial culture. There were no significant differences in demographic or clinical characteristics between patients included and excluded from the study (data not shown). Of the 83 patients included in the analysis, 38 patients (46%) met ATS/IDSA criteria for NTM lung disease. There were 27 patients (33%) who did not meet microbiologic criteria, 26 patients (31%) who did not meet clinical criteria, and 8 patients (10%) who did not meet radiographic criteria. Of the 26 patients who did not meet clinical criteria, two did not have any symptoms. The remainder had coexisting pathogens that when treated resulted in complete symptom resolution during subsequent follow-up. Based on diagnostic criteria requiring exclusion of other disease as the cause of the symptoms, these symptoms were attributed solely to the coexisting pathogen and not M kansasii.

Clinical and demographic features of study patients are shown in Table 1 . The median CD4+ T-lymphocyte count was 34 cells/μL, indicating advanced immunosuppression in the study population. There were no significant differences between patients who did and did not satisfy 2007 ATS/IDSA criteria for M kansasii lung disease except for the proportion of patients with positive sputum AFB smear results (53% vs 15%, respectively; p < 0.001). The majority of patients (69%) had an additional respiratory pathogen identified at the time M kansasii was isolated from their respiratory specimen, most commonly Pneumocystis jirovecii (30%). Due to the high prevalence of coexisting infections in the study population, all analyses were repeated in the cohort with only M kansasii infection (n = 25), and no significant changes were seen in the findings.

Radiographic Findings

Chest radiographs were normal in 10% (n = 8) of patients (Fig 1 ). Multiple abnormalities were present in 39 patients (47%), most commonly the combination of consolidation and nodules (n = 18, 22%) or consolidation and pleural effusion (n = 18, 22%). Overall, consolidation (n = 55, 66%) and nodules (n = 35, 42%) were the most common radiographic abnormalities identified. Cavitation was uncommon, occurring in only 7% (n = 6) of patients. In patients with abnormal chest radiographic findings (n = 75), isolated upper-lobe abnormalities were uncommon overall (11%) as well as for each specific parenchymal radiographic abnormality (Table 2 ). Chest radiographs typically showed bilateral abnormalities (55%), and isolated involvement of the right or left lung was seen in approximately the same proportion of patients (24% and 20%, respectively).

Radiographic findings were compared in patients who did and did not satisfy ATS/IDSA criteria for NTM lung disease (Fig 1). Cavitation (13.2% vs 2.2%), nodules (55.3% vs 31.1%), and lymphadenopathy (15.8% vs 2.2%) were seen more often in patients who satisfied ATS/IDSA criteria for NTM lung disease (all p ≤ 0.05). However, cavitation and isolated upper-lobe disease (8%) were infrequent, and consolidation (73%) remained the most common radiographic abnormality. No significant association was found between radiographic findings and other key characteristics including AFB smear status, presence or absence of coexisting pulmonary infections, and CD4+ T-lymphocyte count assessed at various strata (< 100 cells/μL, < 200 cells/μL) and as a continuous variable (data not shown).

Multivariate Cox regression was performed to determine whether specific chest radiograph abnormalities were associated with overall mortality. When controlling for CD4+ T-lymphocyte count, antiretroviral therapy, AFB smear status, and M kansasii treatment, cavitation was the only radiographic abnormality independently associated with increased mortality (hazard ratio, 4.8; 95% confidence interval, 1.2 to 19.6) [Table 3 ].

In this study, we describe the radiographic features of 83 patient with HIV infection with M kansasii isolated from respiratory specimens. We found that chest radiograph findings were abnormal in 90% of patients. Consolidation and nodules were the most common radiographic abnormalities, and a distinct mid- or lower-lobe distribution was observed in 89% of patients. Cavitation was seen in only 7% of patients but was independently associated with increased mortality. These radiographic patterns were independent of ATS/IDSA criteria, initial AFB smear status, the presence or absence of coexisting pulmonary infections, and CD4+ T-lymphocyte count.

The 2007 ATS/IDSA statement on NTM describes upper-lobe cavitary lesions as the predominant radiographic pattern in patients with M kansasii lung disease.5 Radiographic series in immunocompetent patients are consistent with this description.910 In such studies, cavitary disease has been described in as many as 75 to 95% of patients and disease confined to the upper lobes in > 90% of patients. These findings differ markedly from the radiographic patterns observed in our sample of patient with HIV infection in which cavitation occurred in only 7% of patients and the upper lobes were involved in a minority of cases (11% overall, 17% in patients with cavitation). Previous studies of M kansasii lung disease in patients with HIV infection, although limited by incomplete microbiologic investigation in all patients and small sample sizes,11 have made similar observations to ours.1215 Collectively, these findings suggest that radiographic features in patients with HIV infection and M kansasii lung disease are strikingly different from the upper-lobe cavitary disease described in immunocompetent patients.

Such differences between patients with and without HIV infection have been well described in active pulmonary tuberculosis. Immunocompetent patients most commonly present with the “typical” chest radiographic findings of upper-lobe and cavitary disease characteristic of postprimary tuberculosis,16whereas patients with HIV infection are significantly more likely to present with “atypical” chest radiographic findings such as lower-lobe–predominant consolidation, pleural effusions, and intrathoracic lymphadenopathy1718 either due to rapidly progressive primary tuberculosis or as a consequence of altered immunity.17 In M kansasii lung disease, the paradigm of primary vs postprimary disease has not been previously reported. However, we found that an atypical radiographic pattern is the predominant manifestation seen in patients with HIV infection and M kansasii lung disease. Moreover, since radiographic presentation was independent of CD4+ T-lymphocyte count, it is feasible that the atypical radiographic pattern seen in patients with HIV infection may be due to rapidly progressive primary disease. This hypothesis needs further validation in larger studies because as only 16 patients with HIV infection in our sample had CD4+ T-lymphocyte counts > 200 cells/μL at the time of M kansasii diagnosis.

An unexpected finding in our study was that 69% of patients had both M kansasii and another pulmonary pathogen simultaneously isolated from respiratory specimens. In order to address the potential that the radiographic features seen were predominantly attributable to pathogens other than M kansasii, we repeated our analyses in the cohort of patients without any coexisting pulmonary infection and found that the radiographic patterns were similar to those observed in the entire study population. Consolidation (48%) and nodules (44%) remained the most common abnormalities, and isolated upper-lobe involvement (10%) remained uncommon. Due to the nonspecific radiographic presentation of M kansasii lung disease, this finding implies that clinicians should consider obtaining sputum mycobacterial culture samples from any patient with HIV infection and abnormal chest radiograph findings even when another pathogen is initially identified.

Several limitations should be considered. Our overarching objective was to describe the radiographic features of patients with HIV infection and M kansasii lung disease. Consequently, patients who did and did not meet ATS/IDSA criteria for NTM lung disease were included in the analysis because many experts believe even one positive M kansasii culture finding indicates disease in patients with HIV infection.3,15,1921 Additionally, the study would have benefited from comparative statistical analysis with an control group without HIV infection; however, there were only 15 patients without HIV infection identified with at least one of three sputum specimen cultures positive for M kansasii and medical records available for review during the nearly 13-year study period. Consequently, in the “Discussion” section, we compare our findings in patients with HIV infection to prior reports of immunocompetent patients as a point of reference. The differences noted are striking and biologically plausible. Lastly, 69% of patients in this cohort had both M kansasii and another pulmonary pathogen simultaneously isolated from respiratory specimens. When more than one pathogen is isolated, it is not possible to definitively determine whether the radiographic findings are attributable to M kansasii alone, another pathogen, or the combination of the two. However, we repeated our analyses limited to the cohort of patients without any coexisting pulmonary infection and found no significant changes to our results.

In summary, M kansasii lung disease presents with diverse chest radiographic features in patients with HIV infection that differ from the pattern seen in immunocompetent persons. This difference mirrors the atypical chest radiograph findings of patients with HIV infection and tuberculosis. Cavitary lesions and upper-lobe radiographic abnormalities are thus infrequently seen, but when present may independently predict worse outcome. Due to the highly variable radiographic presentation and frequent occurrence of coexisting pathogens, all patients with HIV and advanced immunosuppression and respiratory symptoms should be evaluated for mycobacterial disease. In contrast to 2007 ATS/IDSA guidelines, data from our cohort suggest that diagnosis and treatment of NTM lung disease when due to M kansasii should be considered even in the setting of a single positive sputum culture result. Normal chest radiographic findings may not exclude significant disease, and further evaluation with HRCT may be useful to determine disease status. Additional studies are needed to clarify the natural history of M kansasii infection and disease patients with HIV infection, particularly those with normal chest radiographic findings, and to determine whether cavitary disease is a surrogate marker for poor outcome.

Abbreviations: AFB = acid-fast bacilli; ATS = American Thoracic Society; IDSA = Infectious Diseases Society of America; NTM = nontuberculous mycobacteria

This publication was made possible in part by grant numbers KL2RR024130 from the National Center for Research Resources and K23HL092629 (Dr. Nahid) from the National Heart, Lung, and Blood Institute at the National Institutes of Health. The work was performed at the University of California, San Francisco.

The contents of this article are solely the responsibility of the authors and do not necessarily represent the official views of the National Institutes of Health.

The authors have no financial disclosures or conflicts of interest to report.

Table Graphic Jump Location
Table 1. Demographic and Clinical Characteristics
* 

Proportions were compared using the χ2 test and medians using the Mann-Whitney U test.

Figure Jump LinkFigure 1. Chest radiograph findings are shown for all study patients (n = 83) and stratified according to patients who did (ATS YES, n = 38, black bars) and did not (ATS NO, n = 45, gray bars) meet 2007 ATS/IDSA criteria for M kansasii lung disease. Patients who satisfied ATS/IDSA criteria by definition had abnormal chest radiographic findings and were more likely to have cavitation, nodules, and hilar or mediastinal lymphadenopathy. More than one radiographic abnormality was present in 39 patients (47%). *p ≤ 0.05 for comparison between ATS NO and ATS YES. LAD = hilar or mediastinal lymphadenopathy.Grahic Jump Location
Table Graphic Jump Location
Table 2. Distribution of Individual Parenchymal Radiographic Abnormalities
Table Graphic Jump Location
Table 3. Association Between Chest Radiograph Findings and Mortality*
* 

Data are presented as hazard ratio (95% confidence interval).

 

Multivariate model included each specific radiographic finding, and the following variables determined to meet the prespecified significance threshold (p < 0.25) in univariate analysis: CD4+ T-lymphocyte count, minimum adequate M kansasii therapy, antiretroviral therapy, and AFB smear status.

Bloch, KC, Zwerling, L, Pletcher, MJ, et al (1998) Incidence and clinical implications of isolation ofMycobacterium kansasii: results of a 5-year, population-based study.Ann Intern Med129,698-704. [PubMed]
 
Campo, RE, Campo, CE Mycobacterium kansasiidisease in patients infected with human immunodeficiency virus.Clin Infect Dis1997;24,1233-1238. [PubMed] [CrossRef]
 
Levine, B, Chaisson, RE Mycobacterium kansasii: a cause of treatable pulmonary disease associated with advanced human immunodeficiency virus (HIV) infection.Ann Intern Med1991;114,861-868. [PubMed]
 
Marras, TK, Daley, CL Epidemiology of human pulmonary infection with nontuberculous mycobacteria.Clin Chest Med2002;23,553-567. [PubMed]
 
Griffith, DE, Aksamit, T, Brown-Elliott, BA, et al An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases.Am J Respir Crit Care Med2007;175,367-416. [PubMed]
 
Evans, AJ, Crisp, AJ, Hubbard, RB, et al PulmonaryMycobacterium kansasiiinfection: comparison of radiological appearances with pulmonary tuberculosis.Thorax1996;51,1243-1247. [PubMed]
 
Evans, SA, Colville, A, Evans, AJ, et al PulmonaryMycobacterium kansasiiinfection: comparison of the clinical features, treatment and outcome with pulmonary tuberculosis.Thorax1996;51,1248-1252. [PubMed]
 
Marras, TK, Morris, A, Gonzalez, LC, et al Mortality prediction in pulmonaryMycobacterium kansasiiinfection and human immunodeficiency virus.Am J Respir Crit Care Med2004;170,793-798. [PubMed]
 
Christensen, EE, Dietz, GW, Ahn, CH, et al Radiographic manifestations of pulmonaryMycobacterium kansasiiinfections.AJR Am J Roentgenol1978;131,985-993. [PubMed]
 
Maliwan, N, Zvetina, JR Clinical features and follow up of 302 patients withMycobacterium kansasiipulmonary infection: a 50 year experience.Postgrad Med J2005;81,530-533. [PubMed]
 
Marras, TK, Daley, CL A systematic review of the clinical significance of pulmonaryMycobacterium kansasiiisolates in HIV infection.J Acquir Immune Defic Syndr2004;36,883-889. [PubMed]
 
Fishman, JE, Schwartz, DS, Sais, GJ Mycobacterium kansasiipulmonary infection in patients with AIDS: spectrum of chest radiographic findings.Radiology1997;204,171-175. [PubMed]
 
Lortholary, O, Deniel, F, Boudon, P, et al Mycobacterium kansasiiinfection in a Paris suburb: comparison of disease presentation and outcome according to human immunodeficiency virus status; Groupe dEtude Des Mycobacteries de la Seine-Saint-Denis.Int J Tuberc Lung Dis1999;3,68-73. [PubMed]
 
Pintado, V, Gomez-Mampaso, E, Martin-Davila, P, et al Mycobacterium kansasiiinfection in patients infected with the human immunodeficiency virus.Eur J Clin Microbiol Infect Dis1999;18,582-586. [PubMed]
 
Rooney, G, Nelson, MR, Gazzard, B Mycobacterium kansasii: its presentation, treatment and outcome in HIV infected patients.J Clin Pathol1996;49,821-823. [PubMed]
 
American Thoracic Society, Centers for Disease Control and Prevention, Infectious Disease Society of America.. Diagnostic standards and classification of tuberculosis in adults and children.Am J Respir Crit Care Med2000;161,1376-1395. [PubMed]
 
Geng, E, Kreiswirth, B, Burzynski, J, et al Clinical and radiographic correlates of primary and reactivation tuberculosis: a molecular epidemiology study.JAMA2005;293,2740-2745. [PubMed]
 
Jones, BE, Young, SM, Antoniskis, D, et al Relationship of the manifestations of tuberculosis to CD4 cell counts in patients with human immunodeficiency virus infection.Am Rev Respir Dis1993;148,1292-1297. [PubMed]
 
Corbett, EL, Blumberg, L, Churchyard, GJ, et al Nontuberculous mycobacteria: defining disease in a prospective cohort of South African miners.Am J Respir Crit Care Med1999;160,15-21. [PubMed]
 
Valainis, GT, Cardona, LM, Greer, DL The spectrum ofMycobacterium kansasiidisease associated with HIV-1 infected patients.J Acquir Immune Defic Syndr1991;4,516-520. [PubMed]
 
Witzig, RS, Fazal, BA, Mera, RM, et al Clinical manifestations and implications of coinfection withMycobacterium kansasiiand human immunodeficiency virus type 1.Clin Infect Dis1995;21,77-85. [PubMed]
 

Figures

Figure Jump LinkFigure 1. Chest radiograph findings are shown for all study patients (n = 83) and stratified according to patients who did (ATS YES, n = 38, black bars) and did not (ATS NO, n = 45, gray bars) meet 2007 ATS/IDSA criteria for M kansasii lung disease. Patients who satisfied ATS/IDSA criteria by definition had abnormal chest radiographic findings and were more likely to have cavitation, nodules, and hilar or mediastinal lymphadenopathy. More than one radiographic abnormality was present in 39 patients (47%). *p ≤ 0.05 for comparison between ATS NO and ATS YES. LAD = hilar or mediastinal lymphadenopathy.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1. Demographic and Clinical Characteristics
* 

Proportions were compared using the χ2 test and medians using the Mann-Whitney U test.

Table Graphic Jump Location
Table 2. Distribution of Individual Parenchymal Radiographic Abnormalities
Table Graphic Jump Location
Table 3. Association Between Chest Radiograph Findings and Mortality*
* 

Data are presented as hazard ratio (95% confidence interval).

 

Multivariate model included each specific radiographic finding, and the following variables determined to meet the prespecified significance threshold (p < 0.25) in univariate analysis: CD4+ T-lymphocyte count, minimum adequate M kansasii therapy, antiretroviral therapy, and AFB smear status.

References

Bloch, KC, Zwerling, L, Pletcher, MJ, et al (1998) Incidence and clinical implications of isolation ofMycobacterium kansasii: results of a 5-year, population-based study.Ann Intern Med129,698-704. [PubMed]
 
Campo, RE, Campo, CE Mycobacterium kansasiidisease in patients infected with human immunodeficiency virus.Clin Infect Dis1997;24,1233-1238. [PubMed] [CrossRef]
 
Levine, B, Chaisson, RE Mycobacterium kansasii: a cause of treatable pulmonary disease associated with advanced human immunodeficiency virus (HIV) infection.Ann Intern Med1991;114,861-868. [PubMed]
 
Marras, TK, Daley, CL Epidemiology of human pulmonary infection with nontuberculous mycobacteria.Clin Chest Med2002;23,553-567. [PubMed]
 
Griffith, DE, Aksamit, T, Brown-Elliott, BA, et al An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases.Am J Respir Crit Care Med2007;175,367-416. [PubMed]
 
Evans, AJ, Crisp, AJ, Hubbard, RB, et al PulmonaryMycobacterium kansasiiinfection: comparison of radiological appearances with pulmonary tuberculosis.Thorax1996;51,1243-1247. [PubMed]
 
Evans, SA, Colville, A, Evans, AJ, et al PulmonaryMycobacterium kansasiiinfection: comparison of the clinical features, treatment and outcome with pulmonary tuberculosis.Thorax1996;51,1248-1252. [PubMed]
 
Marras, TK, Morris, A, Gonzalez, LC, et al Mortality prediction in pulmonaryMycobacterium kansasiiinfection and human immunodeficiency virus.Am J Respir Crit Care Med2004;170,793-798. [PubMed]
 
Christensen, EE, Dietz, GW, Ahn, CH, et al Radiographic manifestations of pulmonaryMycobacterium kansasiiinfections.AJR Am J Roentgenol1978;131,985-993. [PubMed]
 
Maliwan, N, Zvetina, JR Clinical features and follow up of 302 patients withMycobacterium kansasiipulmonary infection: a 50 year experience.Postgrad Med J2005;81,530-533. [PubMed]
 
Marras, TK, Daley, CL A systematic review of the clinical significance of pulmonaryMycobacterium kansasiiisolates in HIV infection.J Acquir Immune Defic Syndr2004;36,883-889. [PubMed]
 
Fishman, JE, Schwartz, DS, Sais, GJ Mycobacterium kansasiipulmonary infection in patients with AIDS: spectrum of chest radiographic findings.Radiology1997;204,171-175. [PubMed]
 
Lortholary, O, Deniel, F, Boudon, P, et al Mycobacterium kansasiiinfection in a Paris suburb: comparison of disease presentation and outcome according to human immunodeficiency virus status; Groupe dEtude Des Mycobacteries de la Seine-Saint-Denis.Int J Tuberc Lung Dis1999;3,68-73. [PubMed]
 
Pintado, V, Gomez-Mampaso, E, Martin-Davila, P, et al Mycobacterium kansasiiinfection in patients infected with the human immunodeficiency virus.Eur J Clin Microbiol Infect Dis1999;18,582-586. [PubMed]
 
Rooney, G, Nelson, MR, Gazzard, B Mycobacterium kansasii: its presentation, treatment and outcome in HIV infected patients.J Clin Pathol1996;49,821-823. [PubMed]
 
American Thoracic Society, Centers for Disease Control and Prevention, Infectious Disease Society of America.. Diagnostic standards and classification of tuberculosis in adults and children.Am J Respir Crit Care Med2000;161,1376-1395. [PubMed]
 
Geng, E, Kreiswirth, B, Burzynski, J, et al Clinical and radiographic correlates of primary and reactivation tuberculosis: a molecular epidemiology study.JAMA2005;293,2740-2745. [PubMed]
 
Jones, BE, Young, SM, Antoniskis, D, et al Relationship of the manifestations of tuberculosis to CD4 cell counts in patients with human immunodeficiency virus infection.Am Rev Respir Dis1993;148,1292-1297. [PubMed]
 
Corbett, EL, Blumberg, L, Churchyard, GJ, et al Nontuberculous mycobacteria: defining disease in a prospective cohort of South African miners.Am J Respir Crit Care Med1999;160,15-21. [PubMed]
 
Valainis, GT, Cardona, LM, Greer, DL The spectrum ofMycobacterium kansasiidisease associated with HIV-1 infected patients.J Acquir Immune Defic Syndr1991;4,516-520. [PubMed]
 
Witzig, RS, Fazal, BA, Mera, RM, et al Clinical manifestations and implications of coinfection withMycobacterium kansasiiand human immunodeficiency virus type 1.Clin Infect Dis1995;21,77-85. [PubMed]
 
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