The genus Mycobacterium is the only
member of the family Mycobacteriaceae and consists of slow-growing, rod-shaped,
non–spore-forming, nonmotile organisms that are acid fast; that is, once
stained, they resist destaining by acid alcohol treatment. This characteristic
is attributed to their cell walls that have unusually high content of lipids
(25%), in contrast to 0.5% for gram-positive bacteria and 3% for gram-negative
bacteria. Mycolic acids are the principal components of the complex cell walls
(1), some of which contribute to virulence. Wax D, a
complex of peptides, polysaccharides, and mycolic acid, enhances cell-mediated
immune responses against mycobacterial proteins. Cord factor is lethal to mice
and inhibits polymorphonuclear leukocyte migration. Sulfolipids inhibit
activation of macrophages and, thus, production of microbicidal molecules (2).
Mycobacteria are straight or slightly curved bacilli, 0.2 to 0.6
µm wide by 1.0 to 10 µm long, sometimes with branching (3). They are more strongly acid fast than organisms that are
weakly acid fast, such as Nocardia, Rhodococcus,
Corynebacterium, Tsukamurella, and Gordona
species. Acid fastness is partly or completed lost at some stages of growth in
some species and under conditions of starvation in Mycobacterium tuberculosis (4). On
cultivation, colony morphology is variable. Some species grow on simple
substrates, others are fastidious, and some are not cultivable (e.g., Mycobacterium leprae). Species requiring light to form
pigment are called photochromogens, and those forming
pigment with or without light are scotochromogens.
Growth rates are slow, with generation times ranging from 2 hours to more than
20 hours and with grossly visible colonies appearing at 2 days to 8 weeks.
Optimal growth temperatures vary from 30° to 45°C. Previously considered an
obligate aerobe, M. tuberculosis has been found to
survive anaerobic conditions (5).
There are now more than 100 species of mycobacteria identified, and
the number continues to grow, largely because of the contribution of molecular
genetics to taxonomic studies (6,7).
Before these developments, only about 30 culturable species had been previously
identified as “mycobacteria other than tuberculosis,†owing to the
limitations imposed by biochemical and culture-based tests (8). Mycobacteria are ubiquitous and range from organisms that
have no pathogenicity for humans to the highly virulent species of M. tuberculosis and M. leprae.
Between these extremes are species increasingly recognized as opportunistic
pathogens in patients with preexisting lung disease or immunosuppressed
patients. Although cumbersome, mycobacteria other than
tuberculosis (MOTT) is probably the most appropriate nomenclature because
“nontuberculous mycobacteria†(NTM) still form tubercles (9), although M. leprae remains a
special case. These organisms are also sometimes referred to as “atypical
mycobacteria†causing the diseases of “atypical tuberculosis†to
differentiate them from “typical†tuberculosis (TB) or as “environmental
mycobacteria†to reflect their ecological niches in soil or water.
MYCOBACTERIUM TUBERCULOSIS
Characteristics of the Pathogen
Robert Koch described M. tuberculosis as
“The Etiology of Tuberculosis†in 1882 (10). “They
are rod-shaped bacilli…often inside cells†(10). Some
taxonomists now consider the five members of the M.
tuberculosis complex to be so closely related that they should be
regarded as subspecies of M. tuberculosis rather than
distinct species (6). M.
tuberculosis and Mycobacterium bovis cause the
most disease in humans. Mycobacterium africanum may
cause 18% to 49% of TB in Africa (11,12). Mycobacterium microti is a
pathogen of rodents. Mycobacterium canetti is the most
recently described member of the complex. Humans are the only natural reservoir
for M. tuberculosis, despite its ability to infect
other primates, elephants, and experimental animal models (6).
M. tuberculosis grows slowly with a
doubling time of 12 to 18 hours. On complex solid media, colonies are visible in
3 to 6 weeks. Growth is enhanced by 10% carbon dioxide. Virulent strains form
strands or cords in liquid media. M. tuberculosis is
differentiated from other mycobacteria by its production of niacin, reduction of
nitrates, usual production of a heat-labile catalase, and characteristic
susceptibility to isoniazid (INH). A radiometric method using Middlebrook 7H12
culture medium with radiolabeled fatty acid (palmitate labeled with carbon 14)
as substrate (Bactec) has reduced the time required for isolation and
identification of M. tuberculosis by half, from 4
weeks to 2 weeks on average. Tubercle bacilli can be distinguished from NTM by
their sensitivity to p-nitro-o-acetylamino-3-hydroxypropiophenone or by nucleic acid
amplification tests. A major advance opening the field of molecular epidemiology
is DNA fingerprinting by restriction fragment length polymorphism (RFLP), which
has been successfully applied in outbreaks of TB (13). The
most widely used system is based on RFLP with
detection of the insertion element IS6110, which is present only in isolates of M. tuberculosis complex and in high copy numbers (14). The sequencing of the entire genome of M. tuberculosis is a landmark achievement that opens the door for major scientific advances in genomics and proteomics in the near future (15).
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detection of the insertion element IS6110, which is present only in isolates of M. tuberculosis complex and in high copy numbers (14). The sequencing of the entire genome of M. tuberculosis is a landmark achievement that opens the door for major scientific advances in genomics and proteomics in the near future (15).
Epidemiology
There were an estimated 8 million (range, 6.3 to 11.1 million)
incident cases of TB in the world in 1997, with 1.9 million (range, 1.4 to 2.8
million) deaths attributed to TB annually (16). Eighty
percent of the global burden of TB lies in 22 countries in Southeast Asia,
sub-Saharan Africa, and Eastern Europe. Ninety-five percent of all TB cases and
98% of TB deaths occur in developing countries, largely because of the global
human immunodeficiency virus (HIV) epidemic as well as to poverty, war,
migration, and poor political commitment to TB control. Nearly one third of new
TB cases in sub-Saharan Africa now occur in HIV-infected individuals, and 9 of
the 10 countries with the highest incidence rates are in Africa. Although only
5% to 10% of individuals with latent infection with tuberculosis (LTBI) develop
active disease, one third of the world’s population, or 1.86 billion people,
is estimated to be infected, an enormous reservoir of potential disease.
Multidrug-resistant tuberculosis (MDR-TB), defined as in vitro drug resistance to at least isoniazid and rifampin,
continues to be a global public health problem, despite recent significant
decreases in prevalence in France and the United States (17). Although the median prevalence among all new cases was only
1.0%, “hot spots†of MDR-TB in Eastern Europe and Asia continue to have
rates among new cases of 5 to 14.1%. In Estonia, the prevalence of MDR-TB among
all cases increased from 11.7% in 1994 to 18.1% in 1998. Although directly
observed short-course chemotherapy has decreased morbidity and mortality in TB
(18), it alone does not cure drug-resistant TB (19).
Case rates in the United States had been declining at a rate of 6%
per year, but there was a resurgence of TB from 1986 to 1992 attributed to
increased immigration, waning of the public health infrastructure, but probably
most importantly the HIV epidemic. The principal increase in the number of TB
patients occurred in the 25- to 44-year-old age group, and most cases were
reported from locations with high HIV prevalence, such as New York City, New
Jersey, and Florida. Nosocomial outbreaks involving multidrug-resistant strains
of M. tuberculosis with transmission to patients and
health care professionals (20) were alarming and led to
new action and investment in controlling TB (21).
Case rates in the United States have declined steadily since 1992;
in 2000, there were 16,377 reported cases for a rate of 5.9 per 100,000, the
lowest on record in the United States (22). Racial and
ethnic minorities remain disproportionately affected, accounting for 75% of all
reported cases. Nearly one third of cases occur in non-Hispanic blacks, 23% in
Hispanics, 21% in Asians and Pacific Islanders, and 1% in Native Americans and
Alaskan Natives. In 2000, the proportion of TB cases in foreign-born persons
increased from 24% to 46% of all cases, owing to increased immigration and
improved control of TB in U.S.-born persons. Similar changes have been noted in
other high-income countries, suggesting the need for developing a more global
approach to TB control. The impact of highly active antiretroviral therapy
(HAART) for HIV infection on the epidemiology of TB has been generally favorable
in the United States (23), Europe (24), and Brazil (25).
Transmission
After decades of debate about the mode of transmission, Wells and
Riley confirmed that most TB is transmitted by the airborne route (26,27). Close contacts of a smear-positive
patient are at maximal risk for being infected. Roughly 25% to 50% of those
exposed become infected, and the attack rate may be as high as 80% if a
sustained, heavy exposure occurs (28,29,30). The rate of infection for contacts
of smear-negative, culture-positive patients (5%) had previously been thought to
be similar to the background rate in the community (31). A
more recent study in San Francisco using molecular epidemiology (i.e., DNA
fingerprinting of isolates using RFLP to assess clustering) found that
smear-negative cases accounted for about 17% of recent transmission (32). Transmission by other means is rare. Infection can occur by
dermal inoculation of bacilli, occasionally seen in hospital personnel handling
infected tissues and cultures. In the developed countries, infection with M. bovis through milk from infected cows has been eliminated
by pasteurization of milk. Gastrointestinal transmission may still affect those
in developing countries, including cross-border travelers (33).
Spread of TB can be rapid in settings of overcrowding. Case rates
among prison inmates are among the highest reported prevalence rates (34). In the ex-USSR state of Georgia, there were 448 confirmed
TB cases among 7,473 inmates, for a prevalence of 5,995 per 100,000 (35). Nursing home residents also have higher case rates than
those of age-matched control subjects who live at home, probably owing to
cohabitation with infectious patients with TB and to waning of immunocompetence
secondary to aging (36). The prevalence of TB in homeless
persons is substantially higher than in the general population, and shelters
have been identified as sources of TB outbreaks (37,38).
Pathogenesis
Infectious particles of experimentally nebulized M. tuberculosis were estimated to be 1 to 5 µm by Wells
(26,39), a size range well suited to
deposition of particles in the alveoli (40). Riley and
co-workers used infections of guinea pigs exposed to the air from an
experimental TB ward to estimate the concentrations of aerosols of M. tuberculosis from infectious patients (41), and other exposures have been estimated by modeling data
based on those studies (42,43).
These data suggest that the production of infectious aerosols in pulmonary TB
varies over 3 orders of magnitude from 1.25 to more than 1,500 infectious units
per hour (44).
Bacilli that are deposited in the alveoli and that escape clearance
mechanisms then encounter a number of innate immune mechanisms, including
surfactant proteins (45), toll-like receptors (46), granulysin (47), defensins (48), and other antimicrobial peptides. Tubercle bacilli escaping
these defense mechanisms undergo phagocytosis by macrophages. After
phagocytosis, mycobacteria are contained within phagosomes. Although killed
mycobacteria are found in lysosomes, some mycobacteria appear to block the
maturation of the phagosome and to resist delivery to the lysosome (49).
The immune response to M. tuberculosis
contributes considerably to the pathology and is characterized by a paradoxical
mix of immune activation and suppression (50). Acquired
cellular immunity develops within 4 to 6 weeks. Subsets of T lymphocytes
producing macrophage-activating cytokines, in particular interferon-γ (IFN-γ),
enable the phagocytes to destroy intracellular bacilli. Macrophage production of
cytokines, such as tumor necrosis factor (TNF), proteases, and lipases, enhances
liquefaction of caseous foci, favoring extracellular bacillary growth and cavity
formation. Other cytokines, such as transforming
growth factor, may favor local bacillary growth, suppress T-cell responses, and promote fibrosis. Although pulmonary infection remains restricted anatomically, organisms spread to the draining hilar lymph nodes and then through the thoracic duct to the bloodstream. On pathologic examination, inflammation, caseation necrosis, cavity formation, and fibrosis occur sequentially (51). However, there may be a mixed response, with various stages occurring in different areas of the lungs at the same time. Spread within the lungs is by bronchial channels (bronchogenic spread) or directly to neighboring alveoli. Progression from minimal disease to advanced disease may occur within months but is accelerated to weeks with HIV co-infection. Extrapulmonary disease occurs when bacillemia results in the seeding of other tissues of the body. Such dissemination occurs more commonly among the immunosuppressed, notably in HIV infection. Bacilli are usually not totally eradicated because a lifelong potential for reactivation remains.
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growth factor, may favor local bacillary growth, suppress T-cell responses, and promote fibrosis. Although pulmonary infection remains restricted anatomically, organisms spread to the draining hilar lymph nodes and then through the thoracic duct to the bloodstream. On pathologic examination, inflammation, caseation necrosis, cavity formation, and fibrosis occur sequentially (51). However, there may be a mixed response, with various stages occurring in different areas of the lungs at the same time. Spread within the lungs is by bronchial channels (bronchogenic spread) or directly to neighboring alveoli. Progression from minimal disease to advanced disease may occur within months but is accelerated to weeks with HIV co-infection. Extrapulmonary disease occurs when bacillemia results in the seeding of other tissues of the body. Such dissemination occurs more commonly among the immunosuppressed, notably in HIV infection. Bacilli are usually not totally eradicated because a lifelong potential for reactivation remains.
The mechanisms underlying reactivation of latent TB are not well
understood. However, a critical role for TNF-α regulation is now recognized. In
an experimental murine model of chronic persistent TB, neutralization of TNF-α
resulted in fatal reactivation of TB with an increased bacillary burden in the
lungs and in severe lung pathology (52). These data are
consonant with clinical observations of 70 reported cases of reactivation TB
after treatment with infliximab, an antibody against TNF-α used in the
treatment of Crohn’s disease and rheumatoid arthritis (53). Similarly, the importance of IFN-γ in host defense is
supported by increased susceptibility to mycobacterial infections in those with
inherited deficiencies of IFN receptors, as discussed later regarding NTM
infections.
The pathogenesis of latent infection is even less well understood,
but it appears that the bacillus is capable of survival through at least two
stages of “nonreplicating persistence,†one of which is an anaerobic stage
(5). Persistence of M.
tuberculosis is facilitated by isocitrate lyase, an enzyme essential for
fatty acid metabolism, which is expressed more with activation of host
macrophages (54). Exposure to chemotherapy induces the
sigF gene, which is similar to genes involved in
bacterial stress responses (55), reflecting the ability of
the tubercle bacillus to respond not only to the host response to infection but
also to therapy.
Prevention
The most effective methods to prevent TB are (a) rapid, appropriate
drug treatment of active pulmonary disease to prevent further transmission; and
(b) treatment of latent infection to prevent reactivation. These interventions
are discussed in Chapter 156.
Vaccination
Although bacille Calmette Guérin (BCG) vaccine has been used
worldwide for decades except in a few developed countries, the value of BCG
vaccination as protection against TB remains unclear, with protection rates
varying from 0% to 80%. Genomic analyses of BCG strains reveals numerous
differences among strains, but their effects on the variability of effectiveness
are unknown (56). BCG vaccination may be beneficial in
reducing miliary and meningeal disease in children. BCG should not be
administered to children or adults who have symptomatic HIV infection because it
may lead to disseminated BCG infection. However, the World Health Organization
recommends BCG vaccination for asymptomatic HIV-infected children who are at
increased risk for tuberculous infection. The tuberculin skin test (TST) is the
mainstay of assessing exposure in contact investigations in developed countries;
therefore, BCG vaccination is usually not recommended because it may confuse the
interpretation of the TST. Intense efforts are underway to develop better TB
vaccines.
Tuberculosis Infection Control
In response to outbreaks of nosocomial MDR-TB involving fatalities
in both patients and health care workers, the Centers for Disease Control and
Prevention issued new “Guidelines for Preventing the Transmission of Mycobacterium tuberculosis in Health-Care Facilities,
1994†(57). These guidelines are being revised, but the
hierarchy of administrative, engineering, and personal respiratory protection
control measures remain the basis for TB infection control. The most important
strategy to prevent transmission of M. tuberculosis in
congregate settings is the rapid identification, isolation, and appropriate
treatment of infectious patients, which is the goal of administrative
controls.
The foundation of engineering controls is the negative-pressure
“airborne infection room.†Negative pressure within the room prevents
infectious aerosol from being carried outside, whereas dilution ventilation of 6
to 12 air changes per hour (ACH) removes the infectious particles. Adjunctive
measures include ultraviolet germicidal irradiation (UVGI) of either upper room
air or the inside of ducts and high-efficiency particulate air (HEPA)
filtration. Both require expertise in installation and periodic maintenance to
be efficacious. The adjunctive measures are probably most effective in high-risk
areas where there may be infectious TB patients but where there is inadequate
dilution ventilation.
Personal respiratory protection refers to
the use of masks designed to protect the wearer from inhalation hazards, such as
infectious aerosols. This continues to be the most controversial aspect of the
Centers for Disease Control and Prevention guidelines. The most commonly used
masks are disposable particulate respirators now certified as N95, meaning that
the filter material is 95% efficient at removing test particles. Better markers
of infectiousness are needed to prioritize more confidently and to implement
such resources, especially in crowded facilities in high-incidence areas.
M. tuberculosis has been transmitted not
only by the infectious aerosols generated during bronchoscopies also but
directly by contaminated bronchoscopes (58).
Pseudoinfections due to poor disinfection have also been reported (58) and can be costly. Improved disinfectants have become
available, and rigorous policies and procedures are required to clean and
disinfect such equipment (59).
MYCOBACTERIA OTHER THAN MYCOBACTERIUM
TUBERCULOSIS
Mycobacteria other than M. tuberculosis
and M. leprae are ubiquitous in the environment,
usually in water or soil, and have a varied spectrum of pathogenicity for
humans. With the greater frequency of disease due to some NTM and the increasing
numbers of immunocompromised patients, recognition of these infections is
important. As mycobacterial infections other than TB are not reportable to
public health departments, the best available data are from national surveys.
The most recent data in the U.S. are from 1981 to 1983, before the HIV epidemic,
when clinical and laboratory data were collected on 5,469 patients; almost 90%
of the isolates were from respiratory tract specimens (60). Prevalence rates were calculated using a diagnostic
algorithm, with most disease associated with Mycobacterium
avium complex (MAC; 1.3 per 100,000), Mycobacterium
kansasii
(0.3 per 100,000), and Mycobacterium fortuitum-chelonae (0.2 per 100,000). The prevalence rate of all NTM infections was estimated to be 1.78 per 100,000, corresponding to 4,201 prevalent cases in the United States. After the onset of the HIV epidemic, the number of infections due to disseminated infections with MAC and other MOTT increased tremendously in the United States and other developed countries (61).
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(0.3 per 100,000), and Mycobacterium fortuitum-chelonae (0.2 per 100,000). The prevalence rate of all NTM infections was estimated to be 1.78 per 100,000, corresponding to 4,201 prevalent cases in the United States. After the onset of the HIV epidemic, the number of infections due to disseminated infections with MAC and other MOTT increased tremendously in the United States and other developed countries (61).
The amount of disease due to MOTT in the developing world is even
less well understood, and detection is limited by laboratory capacity and by the
high prevalence of TB. In contrast to the United States, there is little to no
disease due to M. avium in Ugandan patients with
acquired immunodeficiency syndrome (AIDS) (62). This is
not explained by lack of environmental exposure because M.
avium has been isolated frequently in soil and water samples in Uganda
and other African sites (61). A decreased risk for
disseminated MAC infection has been observed among HIV-infected persons with a
history of active TB (relative risk, 0.52; p <
0.001) (63), suggesting a protective role of TB in
preventing disseminated MAC infection. In northern Malawi, IFN-γ responses were
highest for M. avium, M.
intracellulare, and M. scrofulaceum (the MAIS
complex), suggesting prior exposure to these MOTT (64).
The investigators found concordance between these results and skin test results,
with an additional observation that delayed hypersensitivity to rapidly growing
mycobacteria was associated with a decreased risk for TB and leprosy (65).
Although it appears that most NTM are acquired from the
environment, there are at least 10 reports in the literature of familial
clustering of cases, most often with M. kansasii
(66,67,68). In
only one of these was there microbiologic testing of the home tap water, which
yielded negative results (68). Thus, it is not clear
whether these clusters were due to a shared environmental exposure, such as to
tap water, or to person-to-person transmission. If the latter occurs, it
probably does so rarely given the small number of clusters reported over the
past 40 years. The most recently reported family cluster was clearly due to a
common environmental source: an indoor hot tub contaminated with multiple
mycobacterial species (69). NTM appear to have become part
of the ecology of indoor living; 90% of biofilm samples from water-treatment
plants, home plumbing, and aquaria were found to contain M.
chelonae, Mycobacterium flavescens, M. fortuitum, Mycobacterium gordonae, M.
kansasii, and Mycobacterium terrae-nonchromogenicum (70).
Mycobacteria have been implicated with uncertainty for years as
causative agents in both sarcoidosis and Crohn’s disease. It appears that
Propionibacterium species are more likely associated
with sarcoidosis than the mycobacteria (71). An
association between cell wall–deficient forms of M.
avium subspecies paratuberculosis and Crohn’s
disease has been suggested (72), but the role of
mycobacteria in Crohn’s disease remains controversial (61,73).
The most clinically important NTM and the clinical infections
associated with them are listed in Table 265.1 and
discussed
later. Nosocomial transmission and pseudoinfections have been reported most often due to contaminated water supplies, and iatrogenic infections have been associated with contaminated surgical materials. Because of the environmental sources of many MOTT, it is likely that additional species will be associated with nosocomial disease in the future. More detailed coverage of treatment can be found in Chapter 34, and additional clinical information is in Chapter 157.
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later. Nosocomial transmission and pseudoinfections have been reported most often due to contaminated water supplies, and iatrogenic infections have been associated with contaminated surgical materials. Because of the environmental sources of many MOTT, it is likely that additional species will be associated with nosocomial disease in the future. More detailed coverage of treatment can be found in Chapter 34, and additional clinical information is in Chapter 157.
TABLE 265.1. Infections Associated with
Mycobacteria
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Pathogenesis
The pathogenesis of mycobacterial infections other than TB is less
well understood, although there are some common features. Because these
organisms are ubiquitous in the environment but rarely cause disease, host
susceptibility factors may be more important determinants of infection than the
degree of exposure or the virulence of the organism. The most striking genetic
susceptibilities are conferred by deficiencies of IFN-γ receptor, involving
both the complete IFN-γ receptor ligand-binding chain (IFN-γR1) and the
signaling chain (IFN-γR2). These children are unable to form mature granulomas
and are susceptible to severe mycobacterial and salmonella infections. Milder
clinical presentations are associated with partial deficiencies of these
factors. These deficiencies highlight the essential role of IFN-γ in defense
against mycobacterial infections, also supported by the symptomatic and
radiographic improvement of seven patients with refractory, disseminated
infection with NTM in a small trial of therapeutic IFN-γ given subcutaneously
(74).
Acquired deficiency of cell-mediated immunity, most commonly due to
HIV infection, is also associated with disseminated MAC infection. Other host
factors that predispose to pulmonary mycobacterial infections are preexisting
lung disease, including underlying chronic lung diseases such as chronic
obstructive pulmonary disease (COPD) and pneumoconioses (75,76); bronchiectasis (77); and cystic fibrosis (78). Pulmonary
infections other than MOTT occur in women without recognized risk factors (79) or with pectus excavatum, thoracic scoliosis, and mitral
valve prolapse (80). However, the mechanisms underlying
the susceptibility in these women are not known.
Mycobacterium avium Complex
Mycobacterium avium and Mycobacterium intracellulare, previously differentiated by
their virulence for chickens and rabbits, respectively, are similar
biochemically and genetically and are referred to as MAC. Growth is slow and
optimal at 37°C. Colonies are usually not pigmented and are either opaque and
domed or transparent and flat. MAC, like many other MOTT, has been isolated from
both water and soil (81,82). In
addition, MAC has been isolated from bronchoscopes, raw milk, and cigarettes
(61). The source of MAC infection is usually unknown,
although cases have been linked to isolates from hospital and municipal tap
water (83). Hot tubs are another source of MAC aerosols
causing both infection and hypersensitivity pneumonitis in immunocompetent
patients (84,85). About 90% of MAC
isolates from AIDS patients have been identified as M.
avium by DNA probe, whereas about 40% of isolates from non-AIDS patients
were M. intracellulare (61).
Infection with more than one strain or species in AIDS patients appears common
(61). This is an important consideration because different
strains from the same patient may have different drug susceptibility patterns
(86).
MAC is the most common MOTT associated with human disease, and its
ability to cause human disease has only been recognized since 1943 (87). In a U.S. national survey from 1981 to 1983, the prevalence
of MAC disease was estimated to be 1.3 per 100,000. In a study of 670,000 U.S.
Navy recruits, delayed hypersensitivity responses to purified protein derivative
from MAC (PPD-B or the “Battey†antigen) were 70% or greater in those from
the Southeast compared with 10% to 20% in those from the North and West (88). This suggests at least greater exposure to MAC in the
southeastern United States, probably from environmental sources.
Risk factors for MAC infection are as suggested earlier: (a)
patients with preexisting lung disease, especially COPD, (b) thin middle-aged
and elderly women, and (c) patients with HIV infection. The epidemiology may be
changing because there are anecdotal reports among clinicians that there appear
to be fewer male patients with COPD and more thin women among their
non–HIV-infected patients with pulmonary MAC infections. These patients
present with symptoms similar to those of persons with underlying lung disease,
often with an insidious onset and indolent progression. Disseminated MAC disease
affects immunocompromised hosts, specifically AIDS patients (89). Cervical lymphadenitis (especially in children), bone and
joint infection, urinary tract involvement, and cutaneous infections, including
panniculitis, have been reported.
The diagnosis of pulmonary MAC requires the presence of pulmonary
symptoms with chest radiograph abnormalities of infiltrates, nodules, or
cavities. MAC may occasionally present as a chest mass. The microbiologic
diagnosis requires three positive acid-fast bacilli (AFB) cultures (or two
positive cultures and one positive smear) if sputum alone is obtained. If a
bronchoscopy is done, one positive culture (2 to 4+) is sufficient on washing or
biopsy, or if histopathology demonstrates AFB or granulomatous inflammation, any
growth on another specimen is adequate (90).
Chemotherapy for MAC is similar to that for TB in that it requires
multiple drugs to avoid the emergence of resistance, except that MAC is usually
resistant to isoniazid. Currently recommended therapy for pulmonary MAC without
HIV co-infection includes daily treatment with clarithromycin or azithromycin;
rifampin or rifabutin; and ethambutol (90). Sputa should
be examined monthly for AFB smears and cultures, and treatment should continue
for 1 year after conversion to culture negativity. Streptomycin given 2 to 3
times per week may be added for the first 2 months. Treatment of either
pulmonary or disseminated MAC infection in the HIV-infected patient is similar,
but rifabutin is the preferred rifamycin. AIDS patients with disseminated MAC
should receive lifelong therapy with (1) clarithromycin or azithromycin, and (2)
ethambutol, with or without rifabutin, unless immune reconstitution occurs due
to HAART (91). For HIV-infected patients with CD4 cell
counts below 50 cells/µL, the preferred primary prophylaxis regimen is
clarithromycin or azithromycin (91). Because of increasing
evidence that anti-MAC prophylaxis can usually be stopped safely in AIDS
patients responding to HAART (92,93), current recommendations suggest discontinuation if the CD4
count remains above 100 cells/µL for 3 months or more (91). See Chapter 34 for drug dosages and
additional recommendations. The utility of drug susceptibility testing for MAC
and other NTM has been debated in the literature. Although current
recommendations do not suggest routine drug susceptibility testing for all NTM,
they do suggest its utility as baseline testing in case the patient does not
respond to therapy or in the event of relapse (90).
Emergence of drug-resistant mutants in patients with AIDS is likely due to the
large numbers of bacilli present, and drug-resistant isolates have been
recovered in patients receiving both single- and multiple-drug therapy. Relapse
of symptoms has been associated with the emergence of drug resistance (61).
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Mycobacterium kansasii
Initially isolated in 1953, M. kansasii
is most commonly isolated from tap water but not from natural water (90). M. kansasii antigens cross-react
with PPD-S (from M. tuberculosis); hence, delayed
hypersensitivity skin testing has little utility. Reports suggest that M. kansasii disease is more common in the central United
States, England, and Wales. In the United States, the prevalence of M. kansasii disease is greatest in the metropolitan areas of
the Southeast and Midwest; the male-to-female ratio is 4:1. Eighty percent of
patients are white; their median age is 50 years. Chronic obstructive lung
disease and pneumoconiosis predispose to infection. Miners, welders,
sandblasters, and painters are at highest risk for development of disease.
Guinea pigs exposed to M. kansasii developed
progressive lung disease only if the inoculum contained dust aerosols (94).
The most common form of disease due to M.
kansasii is a chronic pneumonia, generally milder than TB but associated
with more hemoptysis. Extensive unilateral upper lobe disease is more common
than with MAC infection, but none of the radiographic features is specific for
any of the mycobacterioses, including TB. Cervical lymphadenitis (especially in
children), cutaneous abscesses or cellulitis mimicking pyogenic infection, and
musculoskeletal involvement including arthritis, fasciitis, tenosynovitis, or
osteomyelitis have been reported. Dissemination occurs rarely with far-advanced
disease or in immunocompromised hosts such as AIDS patients (95). M. kansasii does not cause as
much disease in AIDS patients as does MAC, for unknown reasons.
Trained microscopists can sometimes identify M.
kansasii by virtue of the long, beaded bacilli with Ziehl-Neelsen
staining, but culture is always needed for confirmation (96). It is the only mycobacterium that produces a bright-yellow
pigment on exposure to light. Although in vitro drug
resistance may be reported to isoniazid at 0.2 or 1.0 µg/mL and to streptomycin
at 1 µg/mL, this may not have clinical relevance as long as rifampin is being
used (90). All isolates are resistant to pyrazinamide;
thus, it is not recommended for treatment. Although there have been no clinical
treatment trials, the current American Thoracic Society (ATS) recommendation is
to treat disease due to M. kansasii with isoniazid,
rifampin, and ethambutol for 18 months, including at least 12 months during
which sputum cultures are negative (90). Clarithromycin
has excellent in vitro activity; hence, it is a
reasonable alternative drug.
Rapidly Growing Mycobacteria
Early studies classified the rapidly growing mycobacteria (RGM) by
phenotypic characteristics into subspecies of M.
fortuitum (M. fortuitum biovar fortuitum, M. fortuitum biovar peregrinum, and an unnamed biovariant complex) and of M. chelonae (M. chelonae
subspecies abscessus and M.
chelonae subspecies chelonae). However, more
recent taxonomy studies using molecular biologic tools have classified these as
separate species (97). Colonies grow at 25° to 40°C in 7
days on both mycobacterial medium and routine bacteriologic medium. Acid
fastness is often negative (98). A number of nosocomial
outbreaks have been associated with exposure to tap water (99). This may be due to biofilms, 90% of which may contain
mycobacteria (70).
Skin and soft tissue infection, the most common clinical form of
disease, is usually secondary to a puncture wound and occurs within 6 weeks to 6
months. Systemic symptoms are absent, and dissemination is extremely unusual.
Spontaneous resolution occurs within 1 to 2 years in as many as 20% of cases.
Nosocomial infections include skin infections of vaccination sites, surgical
wounds (including plastic surgery), and indwelling peritoneal or intravenous
catheters. Disseminated disease is uncommon in severely immunocompromised
persons and is associated with a high rate of mortality. Chronic pneumonia due
to RGM presents in a manner indistinct from disease caused by other mycobacteria
(100). Most patients are women who have no preexisting
lung disease. Risk factors include achalasia, cystic fibrosis, lipoid pneumonia,
and healed TB. On radiographic examination, a reticulonodular pattern is seen,
usually bilateral, sparing the upper lobes, and rarely associated with cavities.
Clinical exacerbations occur during a period of years, but there is no
spontaneous resolution. In general, these mycobacteria are resistant to
antituberculous drugs, except amikacin, and are sensitive to cefoxitin,
clarithromycin, and imipenem. The rapidly growing mycobacteria have varying
susceptibility patterns to drugs. A combination of parenteral antibiotics (e.g.,
amikacin and cefoxitin), followed by treatment with oral drugs for up to 6
months, has been effective. Surgical resection for infection by drug-resistant
species (M. abscessus) and with unilateral localized
disease may be considered.
Other Mycobacteria
M. marinum causes “swimming pool
granuloma†with sources from water and aquatic organisms. A photochromogen,
M. marinum grows optimally at 32°C; colonies appear
in 8 to 14 days. Cutaneous disease usually occurs as a result of trauma to skin
in contaminated, nonchlorinated fresh, or salty water. Two to 3 weeks after
inoculation, a single papulonodular lesion develops, which may later ulcerate. A
sporotrichoid pattern, with abscess formation and secondary nodules along the
lymphatics, can also occur. Dissemination in immunocompromised hosts, synovitis,
and osteomyelitis have been reported.
Mycobacterium simiae is a slow-growing
species that may cause pulmonary disease mimicking TB or pulmonary MAC. In some
laboratories relying on biochemical testing, it may be confused with M. tuberculosis because M. simiae
is the only NTM that is niacin positive. It is unique in having 16S ribosomal
RNA sequences similar to those found in both rapidly growing and slowly growing
mycobacteria. Drug resistance is common; thus, in
vitro susceptibility testing should guide therapy (90).
Mycobacterium scrofulaceum is a cause of
cervical lymphadenitis in children 1 to 5 years of age; it must be
differentiated from M. tuberculosis and MAC. Because
of antigenic and drug susceptibility similarities with MAC, some authors have
classified it in a group with M. avium and M. intracellulare as the MAIS complex.
Mycobacterium ulcerans is endemic to
Australia, Africa, and Mexico. It causes a chronic necrotizing skin infection
known as Bairnsdale ulcer in Australia and Buruli ulcer in Uganda, usually on
the distal aspect of an extremity following trauma. Satellite lesions and
extensive ulceration requiring wide surgical débridement may develop. Treatment
options include dapsone and streptomycin with or without ethambutol (87).
Unique among mycobacteria in its absolute requirement for iron,
Mycobacterium haemophilum is a fastidious bacillus
that grows at temperatures below 32°C. It most often causes nodular, popular,
or cystic skin lesions that may progress to painful ulcers in individuals
immunocompromised by HIV infection (101), organ or bone
marrow transplantation, or lymphoma (102). Osteomyelitis,
arthritis, sinusitis, pneumonitis, lymphadenitis, and bacteremia may also occur.
Successful treatment regimens have included ciprofloxacin, clarithromycin, and
rifampin (103).
Mycobacterium genavense is a slowly
growing fastidious organism that fails to grow on conventional solid media but
grows slowly in liquid culture. M. genavense infection
causes a syndrome indistinguishable from MAC and is estimated to be
responsible for 10% of disseminated NTM infections (104,105). Fever, weight loss, diarrhea, hepatomegaly, splenomegaly, and anemia are common. Response to antimycobacterial therapy directed against MAC and survival in patients with M. genavense infection are similar to those with MAC infection and are dependent on absolute CD4+ cell levels in AIDS patients.
P.2190
responsible for 10% of disseminated NTM infections (104,105). Fever, weight loss, diarrhea, hepatomegaly, splenomegaly, and anemia are common. Response to antimycobacterial therapy directed against MAC and survival in patients with M. genavense infection are similar to those with MAC infection and are dependent on absolute CD4+ cell levels in AIDS patients.
Mycobacterium xenopi grows optimally at
43°C; hence, its isolation from clinical specimens may require prolonged
incubation at 37°C or at higher temperatures. It is commonly isolated from tap
water and has been implicated in nosocomial pulmonary infections (106) and bronchoscopy-associated pseudoinfections (107). It has been increasingly recognized in Western Europe as a
cause of pulmonary disease (108). Extrapulmonary and
disseminated disease has been reported. Initial therapy should include a
macrolide, a rifamycin, and ethambutol (90).
Mycobacterium szulgai causes lung and
extrapulmonary disease indistinguishable from TB (109). It
occurs worldwide, but its source is unknown. Most patients respond to treatment
with antituberculous therapy (90). Mycobacterium, malmoense is slow growing, often requiring at
least 6 weeks of incubation (103). It is rare in the
United States but increasingly reported from northern Europe, England, and
Wales. It may cause pulmonary disease in patients with underlying lung disease
as well as extrapulmonary disease in children or immunosuppressed patients. Most
isolates are susceptible to ethambutol, rifampin, and streptomycin.
Members of the slowly growing M. terrae
complex may cause infections of the lungs, skin, bones, and joints. Drug
susceptibility testing should be done because patterns vary widely. Surgical
excision often is needed. Although the rapidly growing Mycobacterium smegmatis is often used in laboratories as an
avirulent environmental species, it may cause human disease (110). M. gordonae has been called the
“tap-water bacillus.†Although it may rarely cause infection in patients
with and without immunosuppression (111), it is more
commonly a source of pseudoinfections (103). Mycobacterium celatum may infect patients with AIDS and
rarely immunocompetent individuals (112), and it may cause
false-positive results on nucleic acid amplification tests for M. tuberculosis (113,114).
Largely due to the HIV epidemic and the increasing use of
immunosuppressive therapies, infections have been found to be caused by a
growing number of mycobacteria that are uncommon, unidentified, or previously
unrecognized as pathogens, including the following Mycobacterium species: M. alvei, M.
asiaticum, M. bohemicum, M. branderi, M. brumae, M. confluentis, M. conspicuum,
M. gastrii, M. flavescens, M. goodi, M. hassiacum, M. heckeshornense, M.
heidelbergense, M. intermedium, M. interjectum, M. kubicae, M. lentiflavum, M.
mageritense, M. mucogenicum, M. nvocastrense, M. peregrinum, M. phlei, M.
septicum, M. shimodei, M. thermoresistibile, M. triplex, M. tusciae, and
M. wolinskyi (115).
154 comments:
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