The Many Faces of Pulmonary Nontuberculous Mycobacterial Infection
Abstract
OBJECTIVE. The purpose of this article is to review clinical and radiologic manifestations of pulmonary nontuberculous mycobacterial infection.
CONCLUSION. Common and well-recognized patterns of infection include cavitary and bronchiectatic disease and infection in AIDS patients. Less common or well-recognized manifestations include nodules or masses mimicking malignancy, hypersensitivity pneumonitis, and others. Definitive diagnosis can be difficult and patterns may overlap. Timely diagnosis requires a high index of suspicion and knowledge of the spectrum of clinical and radiologic features.
Introduction
Nontuberculous mycobacteria were initially isolated shortly after Mycobacterium tuberculosis was isolated in the 19th century [1]. Although multiple reports in the first half of the 20th century describe human infection by “unusual,” “unclassified,” or “anonymous” mycobacteria, it was not until the 1950s that larger series began to confirm the nontuberculous mycobacteria as true human pathogens [1]. During the 1970s and early 1980s, Christensen et al. [2-4] showed the similarity of Mycobacterium avium-intracellulare complex (MAC) and Mycobacterium kansasii infection to postprimary pulmonary tuberculosis. This pattern of infection was subsequently termed “cavitary” or “classic” when an unusual form of the disease, later termed the “nonclassic” [5] or “bronchiectatic” [6] form, was described in the mid 1980s [7].
Epidemiology
By the early 1980s, the prevalence of non-tuberculous mycobacterial disease in the United States was estimated to be 1.8 cases per 100,000 inhabitants. Among nontuberculous mycobacterial isolates, mostly from respiratory secretions, 61% were MAC; 24%, M. kansasii; approximately 5%, Mycobacterium fortuitum; and 15%, other nontuberculous mycobacteria [8]. In the early 1980s, Zakowski et al. [9] reported an increasing incidence of MAC infection in patients with HIV infections. During the 1990s, analysis from the Centers for Disease Control and Prevention showed a dramatic increase in nontuberculous mycobacteria isolates to levels even higher than M. tuberculosis (MAC, 34% vs M. tuberculosis, 26%). Mycobacterium gordonae and M. fortuitum were identified in 18% and 5% of these isolates, respectively [10]. Although the exact reason for this apparent increased incidence is not clear, it is believed that increased clinical recognition and better techniques for diagnosis are at least partly responsible [11, 12].
Currently, MAC and, to a lesser extent, M. kansasii, account for most cases of nontuberculous mycobacteria infection among immunocompetent and immunosuppressed patients in the United States. Mycobacterium xenopi, Mycobacterium szulgai, and Mycobacterium simiae are less frequent causes of pulmonary disease. Mycobacterium scrofulaceum, Mycobacterium fortuitum-chelonei, and M. gordonae may also cause pulmonary disease but are more commonly isolated elsewhere in the body [5, 13].
Diagnosis
Definitive diagnoses of pulmonary nontuberculous mycobacteria infection are difficult. Because the organisms are often saprophytes, they may colonize airways rather than infect them. Cultures can be falsely positive in patients with chronic lung disease and falsely negative in infected patients without cavities [14]. Thus, identification of acid-fast bacilli at microscopy or isolation of nontuberculous mycobacteria in culture by itself is not enough evidence for establishing the diagnosis [6]. Further, there is cross-reactivity between MAC and M. tuberculosis on the purified protein derivative standard test [15]. Although many skin tests for diagnosis of nontuberculous mycobacteria, particularly MAC, have become available with good results, lack of standardization precludes their use in clinical practice [15].
The American Thoracic Society (ATS) recently revised and simplified criteria for diagnosis of nontuberculous mycobacterial lung disease in HIV-seropositive and seronegative hosts (Appendix 1) [12].
Microbiologic Perspective
Traditionally, nontuberculous mycobacteria have been classified according to the Runyon system established in the 1950s. Four groups of nontuberculous mycobacteria, according to pigmentation and growth rate in culture, are recognized in this classification. The rapid-growers (group IV), as the name implies, can be grown in culture and identified in fewer than 7 days [16, 17]. Conversely, the slow-growers (groups I-III) take weeks to months to grow in culture. However, new molecular identification techniques that allow detection and speciation in a matter of hours are becoming more available [11, 18]. For these reasons, the Runyon system is becoming less important clinically [5, 6]. Speciation has important clinical and prognostic implications [19]. For example, infection with Mycobacterium abscessus, a group IV organism, tends to have an unpredictable response to medical treatment, and surgical resection may be attempted when feasible [16]. On the other hand, M. fortuitum, also a group IV organism, is more susceptible to medical therapy [11]. Further, conventional treatment for the slowly growing organisms MAC and M. kansasii are different. Most treatment regimens for M. kansasii include isoniazid, whereas those for MAC do not [11]. Thus, accurate and rapid speciation is becoming more important than classification according to the Runyon system. Also of interest is the lack of correlation between in vitro and in vivo susceptibility shown in some species of nontuberculous mycobacteria (e.g., M. xenopi and Mycobacterium malmoense) [20, 21], a fact that raises some concern regarding the importance of this test.
Clinical and Radiologic Manifestations
The clinical and radiologic manifestations of pulmonary nontuberculous mycobacteria infection are protean and include the cavitary (“classic”) form, bronchiectatic (“nonclassic”) form, infection in immunocompromised patients (HIV and non-HIV), nodules or masslike opacities, infection in patients with deglutition problems, and hypersensitivity pneumonitis [5, 14, 22]. However, these manifestations are not mutually exclusive; several forms can be seen in an individual patient. Moreover, new manifestations of disease are occasionally reported that do not easily fit into these categories. However, this classification is useful for purposes of discussion and differential diagnosis, and it will be used here. The cavitary and the bronchiectatic forms of the disease are responsible for most nontuberculous mycobacteria infections in the immunocompetent patient [2, 3, 7, 23, 24]. The true incidence of other forms of nontuberculous mycobacteria infection is unknown.
Cavitary Form (Classic Infection)
The clinical and radiologic manifestations of the cavitary (or classic) form of the disease are quite similar to those of postprimary tuberculosis. This form of the disease is more prevalent among older white men with underlying chronic pulmonary disease (e.g., chronic obstructive pulmonary disease) [2-4, 24]. Some important predisposing conditions for pulmonary nontuberculous mycobacteria infection are listed in Appendix 2 [6]. Most cases are caused by MAC, although M. kansasii, and, to a lesser extent, M. xenopi [21, 25-27], M. abscessus [28], and M. malmoense [20, 29], can also manifest with this pattern.
Common findings in the chest radiograph include upper lobe cavitary lesions and endobronchial spread evidenced by nodules adjacent to foci of disease (Figs. 1A, 1B, 1C, 2A, 2B, 2C, 3A, and 3B), cicatricial atelectasis, and pleural thickening. In comparison with postprimary tuberculosis, disease progresses more slowly [5, 14] and cavities are more likely to be smaller or thin-walled [2, 14, 23]. CT can further characterize cavities (usually single with ill-defined margins) and show associated bronchiectasis and pleural thickening [5, 30, 31]. As in tuberculosis, adenopathy and pleural effusion are uncommon manifestations [7, 24, 32, 33].
Bronchiectatic (Nonclassic) Form
MAC and M. kansasii [7, 30, 31, 34-37] are the most common organisms responsible for this form of disease; however, other mycobacteria such as M. chelonae [38] and M. abscessus [16, 28, 39] can manifest in this way. The infection is more commonly seen among elderly white women with no predisposing factors [5, 7, 30, 31, 35, 36]. Whether the infection develops in the setting of preexisting bronchiectasis [34, 40, 41] or results in bronchiectasis [42] is controversial. However, some evidence indicates that bronchiectasis progresses more rapidly in the setting of infection with nontuberculous mycobacteria [34, 40]. Infection presents in an indolent fashion with a chronic cough; constitutional symptoms are uncommon [5, 35]. Some of these patients may voluntarily suppress their cough, leading to poor drainage of secretions and engraftment of nontuberculous mycobacteria, the so-called Lady Windermere syndrome [36, 43]. Because sputum cultures are not sensitive for diagnosis in this form of the disease, more invasive studies such as bronchoalveolar lavage and biopsy may be required [44]. On histopathologic examination, bronchiolectasis and bronchiolar and peribronchiolar inflammation with or without granuloma formation are seen [45].
Radiographic findings include randomly distributed nodular opacities; cavitation is uncommon [7]. CT characteristically shows small centrilobular nodules or tree-in-bud opacities, with cylindric bronchiectasis, usually in the same lobe [28, 30, 37, 42, 46] (Fig. 4). Although the right middle lobe and the lingula are most commonly affected [7, 36, 42, 46, 47], any segment can be involved [34, 40]. Other occasional findings include consolidation and ground-glass opacities [7, 30, 37, 38]. Atelectasis and mediastinal adenopathy are uncommon [5]. Recently it has been suggested that the coexistence of bronchiectasis and bronchiolitis (i.e., centrilobular nodules and a mosaic pattern) is highly suggestive of nontuberculous mycobacteria infection [48] (Figs. 5A, 5B, 5C, and 5D).
HIV Patients
Infection by nontuberculous mycobacteria in HIV-infected patients is characterized by disseminated disease [49]. MAC is the most common nontuberculous mycobacteria agent identified in patients with AIDS and is frequently cultured from blood, bone marrow, lung, liver, spleen, and lymph nodes [9, 49]. During the 1990s, the lifetime prevalence of the disease among homosexual men was near 30% [50, 51]. MAC infection occurs in the setting of low CD4 counts (usually < 100 cells/mm3) [52]. The gastrointestinal tract is thought to be the source of infection, with eventual dissemination by bacteremia [52, 53]. The clinical picture consists of systemic symptoms such as fever, weight loss, fatigue, abdominal pain, and diarrhea. Lymphadenopathy and hepatosplenomegaly are common findings on physical examination. The diagnosis is usually established by culture of blood, bone marrow, or other sterile body site [52].
Because MAC infection frequently coexists with other pulmonary infections (e.g., cytomegalovirus, pyogenic bacteria, Pneumocystis jiroveci, Candida albicans, Cryptosporidium organisms, and so forth) or even neoplasms (e.g., Kaposi sarcoma) [9, 49, 54, 55], pure radiographic findings are difficult to determine. Cases with MAC infection and no coexistent pulmonary infection are scant. In these reports, however, mediastinal lymphadenopathy seems to be the most common manifestation, with airspace opacities, miliary nodules, and pleural effusion reported infrequently. Normal chest radiographic findings are not infrequent [5, 49, 54, 55] (Figs. 6A, 6B, and 6C).
M. xenopi can also cause disseminated disease in patients with HIV [56]. Radiologic findings include heterogeneous peribronchial opacities, reticular opacities, miliary nodules, cavitation, atelectasis, pleural thickening, and lymphadenopathy [56, 57]. In patients with AIDS, infection with M. kansasii tends to be confined to the lungs. Reported radiographic findings include unifocal and unilateral alveolar opacities, mediastinal and hilar adenopathy, cavitation, and pleural effusion [58].
Recently, the immune reconstitution syndrome has been described in patients with HIV weeks to months after starting highly active antiretroviral therapy. This entity has been described with a variety of pathogens such as MAC, tuberculosis, Cryptococcus neoformans, cytomegalovirus, P. jiroveci, diverse viruses, and even inflammatory diseases such as sarcoidosis [59]. The immune reconstitution syndrome consists of an inflammatory response accompanied by clinical deterioration related to a wide range of inflammatory reactions in diverse organs directed against different preexisting microorganisms in tissues [59]. Thoracic disease manifests with cough or wheezing, fever, night sweats, dyspnea, weight loss, and chest pain. Radiographic and CT findings include mediastinal and hilar lymphadenopathy that may exhibit hypoattenuating centers, parenchymal opacities, cavitation, nodules, endobronchial nodules, tree-in-bud opacities, and pericardial effusion [60] (Figs. 7A and 7B).
Non-HIV Immunocompromised Patients
Disseminated nontuberculous mycobacteria infection in the non-HIV immunocompromised patient occurs in the setting of cytotoxic chemotherapy, solid organ transplantation, chronic corticosteroid therapy, leukemia, lymphoma, and so forth [61-63]. Although MAC and M. kansasii appear to be the most common infecting organisms, M. gordonae, Mycobacterium chelonei, and M. fortuitum have also been implicated [49, 61-63]. Clinical manifestations are nonspecific and include fever, weight loss, and malaise [49]. The lungs and the gastrointestinal tract appear to be the most likely source of disseminated infection, with hematogenous spread a posteriori [49]. Nontuberculous mycobacteria are more frequently cultured in bone marrow, sputum or lung, liver, spleen, and lymph nodes [49, 61, 62]. Unfortunately, reports of radiographic findings in this setting are limited and include reticular and nodular opacities, cavities, and mediastinal and hilar adenopathy [61, 63].
Nodules or Masses in Asymptomatic Patients
Pulmonary nontuberculous mycobacteria infection can manifest as nodules or masses in asymptomatic patients [64, 65] (Figs. 8A, 8B, 9A, and 9B). In a series of 20 patients with resected solitary pulmonary nodules caused by nontuberculous mycobacteria, MAC was cultured in 12 (60%) [66]. When multiple, nodules are usually clustered together and have a uniform size, a somewhat helpful feature for differentiation from malignancy. CT may show intralesional calcification or increased attenuation suggestive of a granulomatous cause [5, 14]. Both have 18F-FDG and 11C-choline focal uptake has been described in these nodules [65, 67]; however, the degree of uptake is usually less than that seen in cancer and tuberculosis [65].
Infection in Patients with Deglutition Problems
By the late 1990s, at least 20 cases of diffuse pulmonary infection caused by rapidly growing mycobacteria in patients with esophageal motility disorders had been reported [68]. M. fortuitum and M. chelonae account for most isolates in this setting. Associated esophageal disorders include achalasia, hiatal hernia, dysmotility due to stroke or Parkinson's disease, and colonic interposition. Infection may complicate areas of lipid pneumonia [68]. The clinical presentation frequently includes fever, cough, weight loss, night sweats, hemoptysis, and dyspnea. Radiologic findings include unilateral or bilateral heterogeneous reticulonodular or alveolar opacities without lobar predominance. Pleural effusion was present in 20% and cavitary disease in 15% of reported cases [68, 69] (Fig. 10).
Hypersensitivity Pneumonitis
By 2005, at least 37 cases of hypersensitivity pneumonitis associated with inhaled MAC, often from hot tub exposure, had been described [22]. Affected patients present with dyspnea, cough, and fever [22]. Pulmonary function tests show either an obstructive or a restrictive pattern, often with an impaired diffusion capacity for carbon monoxide [22]. Lung biopsies show features of hypersensitivity pneumonitis and cultures frequently grow MAC. However, whether this phenomenon represents true hypersensitivity pneumonitis or infection remains controversial [22, 70-74]. MAC has been shown to exist in natural sea water and in fresh water [75, 76] and can become concentrated in hot water systems [77]. Water jets from hot tubs are thought to promote aerosol formation of bacteria that eventually travel to the lung by inhalation [71, 77]. Affected patients have been treated with or without corticosteroids or antimycobacterial therapy with equally good results if removal from the source of exposure (i.e., the hot tub) is achieved [71, 72]. M. chelonae has been associated with hypersensitivity pneumonitis among workers exposed to metalworking fluid in the automotive industry [78, 79].
Chest radiographs usually show abnormal findings, including diffuse fine nodular and reticulonodular opacities, diffuse opacities, and areas of consolidation. Characteristic CT findings include ill-defined, ground-glass centrilobular nodules (Fig. 11), more diffuse ground-glass opacities, and air trapping on expiratory examination [22, 80].
Conclusion
Pulmonary nontuberculous mycobacteria infection is an increasingly important cause of morbidity and even mortality. The clinical and radiographic manifestations of infection are variable and frequently overlap. Diagnosis may be difficult and delayed, but consideration of nontuberculous mycobacteria disease as a possible diagnosis is the first step toward making the correct diagnosis and instituting appropriate treatment. Cooperation of pulmonary physicians and radiologists is mandatory because fiberoptic bronchoscopy with bronchoalveolar lavage or transbronchial lung biopsy is often the next most appropriate step after radiologic imaging for securing a definitive diagnosis.
APPENDIX 1: American Thoracic Society Criteria for Diagnosis of Pulmonary Nontuberculous Mycobacterial Infection (Adapted from [12])
Clinical Criteria
•
Pulmonary symptoms with
◦
- Nodular or cavitary opacities on chest radiography, or
◦
- Multifocal bronchiectasis with multiple small nodules on high-resolution CT
AND
•
Appropriate exclusion of other diagnoses
Microbiologic Criteria
•
Positive culture from at least two separate sputum samples
OR
•
Positive culture from at least one bronchial wash or lavage
OR
•
Transbronchial or other lung biopsy with mycobacterial features (granulomatous inflammation or acid-fast bacillus) and positive for nontuberculous mycobacteria or biopsy showing mycobacterial histopathologic features (granulomatous inflammation or acid-fast bacillus) and one or more sputum or bronchial washings that are culture-positive for nontuberculous mycobacteria
Note:
•
Expert consultation should be obtained when nontuberculous mycobacteria are recovered that are either infrequently encountered or usually representative of environmental contamination.
•
Patients who are suspected of having nontuberculous mycobacteria lung disease but do not meet the diagnostic criteria should be followed up until the diagnosis is firmly established or excluded.
•
Making the diagnosis of nontuberculous mycobacteria lung disease does not, per se, necessitate the institution of therapy, which is a decision based on the potential risks and benefits of therapy for the individual patient.
APPENDIX 2: Common Predisposing Conditions for Pulmonary Nontuberculous Mycobacterial Infection (Adapted from [6])
Underlying Lung Disease
•
Chronic obstructive pulmonary disease
•
Prior tuberculosis
•
Prior chest surgery
•
Lung carcinoma
•
Interstitial lung disease
•
Cystic fibrosis
Occupational Risk Factors
•
Mining
•
Welding
•
Sandblasting
•
Painting
Other
•
Immune Deficiency
•
Congenital
•
AIDS
•
Organ transplants
•
Corticosteroid administration
•
Achalasia
•
Previous gastrectomy
•
Renal failure, dialysis patients
•
Scoliosis, pectus excavatum
•
Collagen vascular disorders
•
Advancing age
•
Alcohol abuse
•
Smoking
Footnotes
Address correspondence to S. Martinez.
CME
This article is available for CME credit. See www.arrs.org for more information.
References
1.
Wolinsky E. Nontuberculous mycobacteria and associated diseases. Am Rev Respir Dis 1979; 119:107-159
2.
Christensen EE, Dietz GW, Ahn CH, et al. Initial roentgenographic manifestations of pulmonary Mycobacterium tuberculosis, M kansasii, and M intracellularis infections. Chest 1981; 80:132-136
3.
Christensen EE, Dietz GW, Ahn CH, et al. Pulmonary manifestations of Mycobacterium intracellularis. AJR 1979; 133:59-66
4.
Christensen EE, Dietz GW, Ahn CH, Chapman JS, Murry RC, Hurst GA. Radiographic manifestations of pulmonary Mycobacterium kansasii infections. AJR 1978; 131:985-993
5.
Miller WT Jr. Spectrum of pulmonary nontuberculous mycobacterial infection. Radiology 1994; 191:343-350
6.
Ellis SM, Hansell DM. Imaging of non-tuberculous (atypical) mycobacterial pulmonary infection. Clin Radiol 2002; 57:661-669
7.
Albelda SM, Kern JA, Marinelli DL, Miller WT. Expanding spectrum of pulmonary disease caused by nontuberculous mycobacteria. Radiology 1985; 157:289-296
8.
O'Brien RJ, Geiter LJ, Snider DE Jr. The epidemiology of nontuberculous mycobacterial diseases in the United States: results from a national survey. Am Rev Respir Dis 1987; 135:1007-1014
9.
Zakowski P, Fligiel S, Berlin GW, Johnson L Jr. Disseminated Mycobacterium avium-intracellulare infection in homosexual men dying of acquired immunodeficiency. JAMA 1982; 248:2980-2982
10.
Ostroff S, Hutwagner L, Collin S. Mycobacterial species and drug resistance patterns reported by state laboratories, 1992. In: 93rd American Society for Microbiology general meeting, May 16, 1993, abstract U-9. Washington, DC: ASM, 1993:170
11.
[no authors listed] Diagnosis and treatment of disease caused by nontuberculous mycobacteria. This official statement of the American Thoracic Society was approved by the Board of Directors, March 1997. Medical Section of the American Lung Association. Am J Respir Crit Care Med 1997; 156(2 pt 2):S1-S25
12.
Griffith DE, Aksamit T, Brown-Elliott BA, et al. An official ATS/IDSA statement: diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. AAm J Respir Crit Care Med 2007; 175:367-416
13.
Marras TK, Daley CL. Epidemiology of human pulmonary infection with nontuberculous mycobacteria. Clin Chest Med 2002; 23:553-567
14.
Erasmus JJ, McAdams HP, Farrell MA, Patz EF Jr. Pulmonary nontuberculous mycobacterial infection: radiologic manifestations. RadioGraphics 1999; 19:1487-1505
15.
Aksamit TR. Mycobacterium avium complex pulmonary disease in patients with pre-existing lung disease. Clin Chest Med 2002; 23:643-653
16.
Daley CL, Griffith DE. Pulmonary disease caused by rapidly growing mycobacteria. Clin Chest Med 2002; 23:623-632, vii
17.
Runyon EH. Anonymous mycobacteria in pulmonary disease. Med Clin North Am 1959; 43:273-290
18.
Brown-Elliot BA, Wallace RJ Jr. Infections caused by nontuberculous mycobacteria. In: Mandell GL, Bennett JE, Dolin R, eds. Principles and practice of infection diseases. Philadelphia, PA: Elsevier Churchill Livingstone, 2004:2909-2916
19.
Debrunner M, Salfinger M, Brandli O, von Graevenitz A. Epidemiology and clinical significance of nontuberculous mycobacteria in patients negative for human immunodeficiency virus in Switzerland. Clin Infect Dis 1992; 15:330-345
20.
[no authors listed] Pulmonary disease caused by M. malmoense in HIV negative patients: 5-yr follow-up of patients receiving standardised treatment. Eur Respir J 2003; 21:478-482
21.
Jenkins PA, Campbell IA. Pulmonary disease caused by Mycobacterium xenopi in HIV-negative patients: five-year follow-up of patients receiving standardised treatment. Respir Med 2003; 97:439-444
22.
Marras TK, Wallace RJ Jr, Koth LL, Stulbarg MS, Cowl CT, Daley CL. Hypersensitivity pneumonitis reaction to Mycobacterium avium in household water. Chest 2005; 127:664-671
23.
Levin DL. Radiology of pulmonary Mycobacterium avium-intracellulare complex. Clin Chest Med 2002; 23:603-612
24.
Woodring JH, Vandiviere HM, Melvin IG, Dillon ML. Roentgenographic features of pulmonary disease caused by atypical mycobacteria. South Med J 1987; 80:1488-1497
25.
Wittram C, Weisbrod GL. Mycobacterium xenopi pulmonary infection: evaluation with CT. J Comput Assist Tomogr 1998; 22:225-228
26.
Smith MJ, Citron KM. Clinical review of pulmonary disease caused by Mycobacterium xenopi. Thorax 1983; 38:373-377
27.
Simor AE, Salit IE, Vellend H. The role of Mycobacterium xenopi in human disease. Am Rev Respir Dis 1984; 129:435-438
28.
Han D, Lee KS, Koh WJ, Yi CA, Kim TS, Kwon OJ. Radiographic and CT findings of nontuberculous mycobacterial pulmonary infection caused by Myco-bacterium abscessus. AJR 2003; 181:513-517
29.
Evans AJ, Crisp AJ, Colville A, Evans SA, Johnston ID. Pulmonary infections caused by Mycobacterium malmoense and Mycobacterium tuberculosis: comparison of radiographic features. AJR 1993; 161:733-737
30.
Hartman TE, Swensen SJ, Williams DE. Mycobacterium avium-intracellulare complex: evaluation with CT. Radiology 1993; 187:23-26
31.
Wittram C, Weisbrod GL. Mycobacterium avium complex lung disease in immunocompetent patients: radiography-CT correlation. Br J Radiol 2002; 75:340-344
32.
Miller WT Jr, Miller WT. Pulmonary infections with atypical mycobacteria in the normal host. Semin Roentgenol 1993; 28:139-149
33.
Woodring JH, Vandiviere HM. Pulmonary disease caused by nontuberculous mycobacteria. J Thorac Imaging 1990; 5:64-76
34.
Kubo K, Yamazaki Y, Hachiya T, et al. Mycobacterium avium-intracellulare pulmonary infection in patients without known predisposing lung disease. Lung 1998; 176:381-391
35.
Prince DS, Peterson DD, Steiner RM, et al. Infection with Mycobacterium avium complex in patients without predisposing conditions. N Engl J Med 1989; 321:863-868
36.
Reich JM, Johnson RE. Mycobacterium avium complex pulmonary disease presenting as an isolated lingular or middle lobe pattern: the Lady Windermere syndrome. Chest 1992; 101:1605-1609
37.
Swensen SJ, Hartman TE, Williams DE. Computed tomographic diagnosis of Mycobacterium avium-intracellulare complex in patients with bronchiectasis. Chest 1994; 105:49-52
38.
Hazelton TR, Newell JD Jr, Cook JL, Huitt GA, Lynch DA. CT findings in 14 patients with Mycobacterium chelonae pulmonary infection. AJR 2000; 175:413-416
39.
Griffith DE, Girard WM, Wallace RJ Jr .Clinical features of pulmonary disease caused by rapidly growing mycobacteria: an analysis of 154 patients. Am Rev Respir Dis 1993; 147:1271-1278
40.
Primack SL, Logan PM, Hartman TE, Lee KS, Muller NL. Pulmonary tuberculosis and Mycobacterium avium-intracellulare: a comparison of CT findings. Radiology 1995; 194:413-417
41.
Hollings NP, Wells AU, Wilson R, Hansell DM. Comparative appearances of non-tuberculous mycobacteria species: a CT study. Eur Radiol 2002; 12:2211-2217
42.
Moore EH. Atypical mycobacterial infection in the lung: CT appearance. Radiology 1993; 187:777-782
43.
Dhillon SS, Watanakunakorn C. Lady Windermere syndrome: middle lobe bronchiectasis and Mycobacterium avium complex infection due to voluntary cough suppression. Clin Infect Dis 2000; 30:572-575
44.
Huang JH, Kao PN, Adi V, Ruoss SJ. Mycobacterium avium-intracellulare pulmonary infection in HIV-negative patients without preexisting lung disease: diagnostic and management limitations. Chest 1999; 115:1033-1040
45.
Jeong YJ, Lee KS, Koh WJ, Han J, Kim TS, Kwon OJ. Nontuberculous mycobacterial pulmonary infection in immunocompetent patients: comparison of thin-section CT and histopathologic findings. Radiology 2004; 231:880-886
46.
Obayashi Y, Fujita J, Suemitsu I, Kamei T, Nii M, Takahara J. Successive follow-up of chest computed tomography in patients with Mycobacterium avium-intracellulare complex. Respir Med 1999; 93:11-15
47.
Lynch DA, Simone PM, Fox MA, Bucher BL, Heinig MJ. CT features of pulmonary Mycobacterium avium complex infection. J Comput Assist Tomogr 1995; 19:353-360
48.
Koh WJ, Lee KS, Kwon OJ, Jeong YJ, Kwak SH, Kim TS. Bilateral bronchiectasis and bronchiolitis at thin-section CT: diagnostic implications in nontuberculous mycobacterial pulmonary infection. Radiology 2005; 235:282-288
49.
Aronchick JM, Miller WT Jr. Disseminated nontuberculous mycobacterial infections in immunosuppressed patients. Semin Roentgenol 1993; 28:150-157
50.
Hoover DR, Saah AJ, Bacellar H, et al. Clinical manifestations of AIDS in the era of pneumocystis prophylaxis: multicenter AIDS cohort study. N Engl J Med 1993; 329:1922-1926
51.
Katz MH, Hessol NA, Buchbinder SP, Hirozawa A, O'Malley P, Holmberg SD. Temporal trends of opportunistic infections and malignancies in homosexual men with AIDS. J Infect Dis 1994; 170:198-202
52.
Benson CA, Ellner JJ. Mycobacterium avium complex infection and AIDS: advances in theory and practice. Clin Infect Dis 1993; 17:7-20
53.
Horsburgh CR Jr. Mycobacterium avium complex infection in the acquired immunodeficiency syndrome. N Engl J Med 1991; 324:1332-1338
54.
Marinelli DL, Albelda SM, Williams TM, Kern JA, Iozzo RV, Miller WT. Nontuberculous mycobacterial infection in AIDS: clinical, pathologic, and radiographic features. Radiology 1986; 160:77-82
55.
Wallace JM, Hannah JB. Mycobacterium avium complex infection in patients with the acquired immunodeficiency syndrome: a clinicopathologic study. Chest 1988; 93:926-932
56.
el-Helou P, Rachlis A, Fong I, et al. Mycobacterium xenopi infection in patients with human immunodeficiency virus infection. Clin Infect Dis 1997; 25:206-210
57.
Bankier AA, Stauffer F, Fleischmann D, et al. Radiographic findings in patients with acquired immunodeficiency syndrome, pulmonary infection, and microbiologic evidence of Mycobacterium xenopi. J Thorac Imaging 1998; 13:282-288
58.
Fishman JE, Schwartz DS, Sais GJ. Mycobacterium kansasii pulmonary infection in patients with AIDS: spectrum of chest radiographic findings. Radiology 1997; 204:171-175
59.
Shelburne SA 3rd, Hamill RJ. The immune reconstitution inflammatory syndrome. AIDS Rev 2003; 5:67-79
60.
Phillips P, Bonner S, Gataric N, et al. Nontuberculous mycobacterial immune reconstitution syndrome in HIV-infected patients: spectrum of disease and long-term follow-up. Clin Infect Dis 2005; 41:1483-1497
61.
Horsburgh CR Jr, Mason UG 3rd, Farhi DC, Iseman MD. Disseminated infection with Mycobacterium avium-intracellulare: a report of 13 cases and a review of the literature. Medicine (Baltimore) 1985; 64:36-48
62.
Bennett C, Vardiman J, Golomb H. Disseminated atypical mycobacterial infection in patients with hairy cell leukemia. Am J Med 1986; 80:891-896
63.
Libshitz HI, Shuman LS, Gresik MV, Heaston DK. Pneumonia in hairy-cell leukemia. Radiology 1981; 139:19-24
64.
Yano S, Kusumoto M, Asamuara H, Tsuchiya R, Moriyama N. A case of Mycobacterium avium complex infection showing solitary pulmonary mass. Radiat Med 2002; 20:147-150
65.
Hara T, Kosaka N, Suzuki T, Kudo K, Niino H. Uptake rates of 18F-fluorodeoxyglucose and 11C-choline in lung cancer and pulmonary tuberculosis: a positron emission tomography study. Chest 2003; 124:893-901
66.
Gribetz AR, Damsker B, Bottone EJ, Kirschner PA, Teirstein AS. Solitary pulmonary nodules due to nontuberculous mycobacterial infection. Am J Med 1981; 70:39-43
67.
Bandoh S, Fujita J, Ueda Y, et al. Uptake of fluorine-18-fluorodeoxyglucose in pulmonary Mycobacterium avium complex infection. Intern Med 2003; 42:726-729
68.
Hadjiliadis D, Adlakha A, Prakash UB. Rapidly growing mycobacterial lung infection in association with esophageal disorders. Mayo Clin Proc 1999; 74:45-51
69.
Aronchick JM, Miller WT, Epstein DM, Gefter WB. Association of achalasia and pulmonary Mycobacterium fortuitum infection. Radiology 1986; 160:85-86
70.
Cappelluti E, Fraire AE, Schaefer OP. A case of “hot tub lung” due to Mycobacterium avium complex in an immunocompetent host. Arch Intern Med 2003; 163:845-848
71.
Embil J, Warren P, Yakrus M, et al. Pulmonary illness associated with exposure to Mycobacterium-avium complex in hot tub water: hypersensitivity pneumonitis or infection? Chest 1997; 111:813-816
72.
Khoor A, Leslie KO, Tazelaar HD, Helmers RA, Colby TV. Diffuse pulmonary disease caused by nontuberculous mycobacteria in immunocompetent people (hot tub lung). Am J Clin Pathol 2001; 115:755-762
73.
Mangione EJ, Huitt G, Lenaway D, et al. Nontuberculous mycobacterial disease following hot tub exposure. Emerg Infect Dis 2001; 7:1039-1042
74.
Rickman OB, Ryu JH, Fidler ME, Kalra S. Hypersensitivity pneumonitis associated with Mycobacterium avium complex and hot tub use. Mayo Clin Proc 2002; 77:1233-1237
75.
Wendt SL, George KL, Parker BC, Gruft H, Falkinham JO 3rd. Epidemiology of infection by nontuberculous mycobacteria. III. Isolation of potentially pathogenic mycobacteria from aerosols. Am Rev Respir Dis 1980; 122:259-263
76.
Pelletier PA, du Moulin GC, Stottmeier KD. Mycobacteria in public water supplies: comparative resistance to chlorine. Microbiol Sci 1988; 5:147-148
77.
du Moulin GC, Stottmeier KD, Pelletier PA, Tsang AY, Hedley-Whyte J. Concentration of Mycobacterium avium by hospital hot water systems. JAMA 1988; 260:1599-1601
78.
Beckett W, Kallay M, Sood A, Zuo Z, Milton D. Hypersensitivity pneumonitis associated with environmental mycobacteria. Environ Health Perspect 2005; 113:767-770
79.
Kreiss K, Cox-Ganser J. Metalworking fluid-associated hypersensitivity pneumonitis: a workshop summary. Am J Ind Med 1997; 32:423-432
80.
Pham RV, Vydareny KH, Gal AA. High-resolution computed tomography appearance of pulmonary Mycobacterium avium complex infection after exposure to hot tub: case of hot-tub lung. J Thorac Imaging 2003; 18:48-52
Information & Authors
Information
Published In
Copyright
© American Roentgen Ray Society.
History
Submitted: February 19, 2007
Accepted: February 22, 2007
First published: November 23, 2012
Keywords
Authors
Metrics & Citations
Metrics
Citations
Export Citations
To download the citation to this article, select your reference manager software.