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Previous Article | Next Article 
Journal of Clinical Microbiology, February 2001, p. 816-819, Vol. 39, No. 2
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.2.816-819.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Fatal Pulmonary Infection Due to
Multidrug-Resistant Mycobacterium abscessus in a Patient
with Cystic Fibrosis
Maurizio
Sanguinetti,1,*
Fausta
Ardito,1
Ersilia
Fiscarelli,2
Marilena
La
Sorda,1
Patrizia
D'Argenio,3
Gabriella
Ricciotti,2 and
Giovanni
Fadda1
Istituto di Microbiologia, Università
Cattolica del S. Cuore,1 and Sezione
Microbiologia,2 and Dipartimento
Immunoinfettivologia,3 Ospedale Pediatrico
"Bambino Gesù," Rome, Italy
Received 12 September 2000/Returned for modification 22 October
2000/Accepted 18 November 2000
 |
ABSTRACT |
We report a case of fatal pulmonary infection caused by
Mycobacterium abscessus in a young patient with cystic
fibrosis, who underwent bipulmonary transplantation after a 1-year
history of severe lung disease. Fifteen days after surgery he developed
septic fever with progressive deterioration in lung function. M. abscessus, initially isolated from a pleural fluid specimen, was
then recovered from repeated blood samples, suggesting a disseminated
nature of the mycobacterial disease. Drug susceptibility testing assay, performed on two sequential isolates of the microorganism, showed a pattern of multidrug resistance. Despite aggressive therapy with several antimycobacterial drugs, including clarithromycin, the infection persisted, and the patient died.
| |
CASE REPORT |
A 20-year-old man with cystic
fibrosis (CF) underwent bilateral pulmonary transplantation in July of
1999. For approximately 1 year prior to admission he had been suffering
from severe pulmonary disease with intermittent episodes of septic
fever, and during this period he had been hospitalized several times.
Sputum cultures had yielded Pseudomonas aeruginosa and
Aspergillus fumigatus, whereas blood cultures (collected
either via catheter and by venipuncture) were positive for
Saccharomyces cerevisiae. On the basis of these microbiological findings, he had received several courses of antibiotic and antifungal therapy consisting of quinolones, third-generation cephalosporins, and amphotericin B, which had, however, produced only
temporary remission of the symptoms. All cultures for mycobacteria (blood, sputum, urine, etc.) were repeatedly negative; sputum culture
was contaminated by P. aeruginosa.
Bilateral lung transplantation was performed on 20 July 1999. There
were no intraoperative complications, and the patient was started on
immunosuppressive therapy.
On 5 August 1999, the patient developed a septic syndrome, and computed
tomography (CT) performed on 7 August 1999 revealed a hyperdense lesion
in the right paracardiac region with features of parenchymal
involvement and a reactive pleural effusion. In light of the previous
fungal recovery from clinical specimens, he was promptly started on
intravenous amphotericin B therapy. On 6 August 1999 the pleural fluid
was cultured for mycobacteria and was inoculated into Middlebrook 7H12
medium (BACTEC 12B; Becton Dickinson Diagnostic Instruments, Sparks,
Md.) and Löwenstein-Jensen slant (BioMerieux, Marcy l'Etoile,
France). On 8 August 1999, sputum and blood samples were also submitted
for mycobacterial studies. A smear of respiratory samples showed many
acid-fast bacilli.
All three specimens yielded a rapidly growing mycobacterium identified
as Mycobacterium chelonae and subsequently as M. abscessus, and on 20 August 1999 the patient was started on
intravenous ciprofloxacin, amikacin, and clarithromycin. Sensitivity
studies soon revealed, however, that the isolates were clearly
resistant to all three drugs, as well as to all of the others tested
(Table 1). In fact, after 1 month of
antibiotic therapy the patient was still febrile, and his pulmonary
disease had worsened. Computed tomography performed at this point
revealed diffuse nodular lesions throughout the entire pulmonary
parenchyma. Because of the critical nature of the patient's clinical
status, the treatment was empirically modified. Ciprofloxacin was
replaced with levofloxacin and meropenem, which were subsequently
changed to intravenous ethambutol and rifabutin, and later to
streptomycin and ethambutol. The blood and pleural fluid specimens
remained positive for acid-fast bacilli, and the patient died on 31 October 1999.
Microbiology.
Prior to cultivation, sputum specimens were
decontaminated by the NALC-NaOH method as previously described
(15), whereas pleural fluid and blood specimens were
directly cultured for mycobacteria. All of the specimens yielded a
rapidly growing mycobacterium that was detected by the BACTEC 460 radiometric system (Becton Dickinson) and by visual observation of the
Löwenstein-Jensen slants. Acid-fast staining was used to confirm
that the isolates were mycobacteria; no contamination with other
bacteria was observed. The isolates, subcultured on Middlebrook 7H11
agar (BBL Microbiology Systems, Cockeysville, Md.), grew within 3 days
of incubation and appeared as a nonpigmented, large, flat, rough, and
wrinkled colony, with a well-known morphotype (12) (Fig.
1). They were identified as M. chelonae on the basis of biochemical tests, including catalase, arylsulfatase 3-day, and nitrate reduction analyses and growth on
MacConkey agar (12), and were sent to the Microbiology
Laboratory of the Catholic University of the Sacred Heart for
confirmation.
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|
FIG. 1.
M. abscessus isolate grown on Middlebrook
7H11 agar. The colony appears large, flat, rough, and wrinkled,
findings consistent with one of the described M. abscessus
morphotypes.
|
|
The isolates were first subjected to PCR-reverse cross blot
hybridization of the amplified 16S ribosomal DNA (15),
which confirmed that they belonged to the M. chelonae group.
The microorganisms were then analyzed by the hsp65
PCR-restriction method (18), which yielded a profile that
matched that of M. abscessus obtained from Prasite
(www.hospvd.ch:8005) (G. Prod'hom, M. M'Pandi, C. Taillard, M. Moser,
A. Telenti, D. Blanc, V. Vincent, A. Strässle, G. Pfyffer, and J. Bille, Final Prog. Abstr. 20th Annu. Cong. Eur. Soc. Mycobacteriol.,
abstr. P59, p. 74, 1999). Alternatively, other biochemical tests, such
as citrate utilization (16), could be used to
differentiate the two organisms.
The MICs of 14 antimicrobial agents, including the first-line
antimycobacterial drugs, were determined with the Etest diffusion agar
method (PMD Epsilometer; AB Biodisk, Solna, Sweden). Briefly, a
suspension obtained by emulsifying the microorganism's colonies in
Mueller-Hinton broth to achieve a density equal to 1.0 McFarland turbidity standard, was used to inoculate the entire surface of three
Mueller-Hinton agar plates supplemented with 5% sheep blood (BBL
Microbiology Systems). Etest strips were applied on the plates according to the manufacturer's instructions. Plates were incubated at
30°C in ambient air, and the results were read after 72 h of incubation, as previously described (10). All of the
M. abscessus isolates showed the same susceptibility
pattern, with extremely high MIC values for all of the drugs tested
(Table 1). Surprisingly, the isolates were resistant to clarithromycin,
a drug commonly used for therapy of infections caused by rapidly
growing mycobacteria.
Discussion.
Historically considered quite rare, the recovery
of nontuberculous mycobacteria (NTM) from the pulmonary tracts of
patients suffering from CF appears to be increasing (1,
9). Among NTM, M. abscessus, M. chelonae,
and M. fortuitum are the species more frequently isolated
from respiratory specimens in these patients; in particular, from a
total of cases of cultures positive for mycobacteria, M. abscessus was found to be the second most common isolate after
M. avium complex (5, 13). Although the
significance of NTM in CF has not yet been firmly established
(7), there are well-documented cases of clinically
important pulmonary infections due to M. abscessus that
clearly evidence the pathogenetic role of this organism
(5). The case we presented addresses the severe nature of
M. abscessus pulmonary infection complicating CF and the
difficulty in eradicating the organism, particularly in patients with
underlying lung disease.
M. abscessus belongs to the group of NTM, a heterogeneous
group of microorganisms that can occasionally cause lung disease but
more commonly affect patients with underlying chronic lung disease,
such as bronchiectasis, pneumoconiosis, emphysema, or CF. As recently
reported (6), patients with CF are at high risk for NTM
disease, but in these individuals the clinical signs and symptoms of
NTM infections are often undistinguishable from those of the chronic
bacterial pulmonary infections that occur during the advanced stages of
CF (5, 13). The situation is further complicated by the
fact that other microorganisms, P. aeruginosa in particular,
colonize the respiratory tract of CF patients, and their overgrowth
often hampers the recovery of mycobacteria.
Misdiagnosis of mycobacterial infections can be a life-threatening
error. In the CF patient described here, lung transplantation was
followed by a severe pulmonary disease caused by a multidrug-resistant strain of M. abscessus. From the onset, the disease followed
a fulminant course that led to irreversible and ultimately fatal lung
damage. The dramatic outcome of the case highlights important issues.
Although M. chelonae, M. abscessus, and M. fortuitum are indeed the NTM species most frequently found in the
respiratory tract of CF patients (7), the chronic nature
of the pulmonary disease in CF makes it difficult to distinguish
between NTM colonization and disease. In fact, with the emergence of
high-resolution CT scanning, several cases of apparent
"colonization" have had to be reclassified (5, 17). In
our case, the CT documentation of a progressive decline in pulmonary
function, together with the persistent positivity for mycobacteria in
pleural fluid and blood cultures, were indicative of active NTM disease.
Bacterial overgrowth in clinical specimens, such as sputum, is a
problem, and it leads to an underestimation of the prevalence of
mycobacterial lung disease in CF patients. This phenomenon may explain
the low rate (6 to 22%) of mycobacteria recovery observed, particularly in young patients (6, 8, 20). Improved
methods are needed to detect mycobacteria in respiratory samples
contaminated with other overgrowing microorganisms, such as P. aeruginosa, Staphylococcus aureus, Candida albicans, and
Aspergillus fumigatus (2, 21). Molecular
methods, able to detect and identify mycobacteria directly from
clinical specimens, could improve the diagnosis of mycobacterial
pulmonary infections. In particular, PCR-reverse cross blot
hybridization, used in our case to identify pure culture isolates, has
successfully been adopted for the direct analysis of clinical specimens
from patients suspected of having mycobacterial disease (11,
14). Similarly, we have used this method on BACTEC broth
cultures to quickly detect and identify several clinical important
mycobacterial species (4, 15).
Lung transplantation is considered a therapeutic option in the CF
patient population, but the posttransplantation immunosuppressive therapy increases the risk for opportunistic infections, including those caused by mycobacteria. Moreover, CF candidates for
transplantation with true NTM colonization must be reliably identified
because lung transplantation in a patient with
acid-fast-bacillus-positive smears and cultures carries enormous risks.
In fact, cervical adenitis and skin abscesses caused by M. chelonae have even been observed in a CF lung transplantation
patient after a prolonged period of negative cultures (6,
19).
In our case, the question of whether or not the patient was colonized
by the mycobacterium prior to transplantation remains unanswered. It is
conceivable that the presence of P. aeruginosa could have
prevented mycobacterial growth in the preoperative cultures, which were
repeatedly negative, and that eradication of the P. aeruginosa infection with preoperative antibiotics allowed the NTM
to emerge in postoperative cultures. On the other hand, the prolonged
course of intravenous antibiotics that was administered for the
bacterial infections may itself have predisposed the patient to
nontuberculous colonization, as observed by Torrens et al. (20).
Although delayed diagnosis may have contributed to the fatal outcome of
this case, the latter appears to be primarily attributable to the
multidrug resistance of the M. abscessus isolate. To our knowledge, this is the first evidence of true resistance to
clarithromycin, which is considered the most active drug against
M. chelonae. In a study published in 1992, 100% of the
isolates tested were susceptible to this drug at an MIC of 
1 µg/ml
(3). However, a more recent report has described a
recurrent catheter-related infection due to a multidrug-resistant
strain of M. chelonae, in which even clarithromycin
displayed a significantly higher MIC (1.5 to 2 µg/ml)
(8). The molecular genetic basis of the drug resistance of
our isolate needs to be elucidated.
In conclusion, we illustrate here that M. abscessues
infections may present with a severe and fatal course as a consequence of either late diagnosis and/or broad-spectrum drug resistance of the microorganism.
| |
ACKNOWLEDGMENTS |
This work was supported in part by the National Tuberculosis
Project (Istituto Superiore di Sanità-Ministero della
Sanità), contract no. 96/D/T10.
We thank Marian Kent and Brunella Posteraro for their critical reading
of the manuscript.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Istituto di
Microbiologia, Università Cattolica del S. Cuore, Largo F. Vito,
1, 00168 Rome, Italy. Phone: 39-6-30154336. Fax: 39-6-3051152. E-mail: msanguinetti{at}rm.unicatt.it.
| |
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Journal of Clinical Microbiology, February 2001, p. 816-819, Vol. 39, No. 2
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.2.816-819.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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Abstract
Case Report
