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Journal of Clinical Microbiology, January 2000, p. 398-401, Vol. 38, No. 1
Servei de Microbiologia, Hospital "Princeps
d'Espanya," Ciutat Sanitària i Universitària de
Bellvitge, 08907 L'Hospitalet de Llobregat, Barcelona,
Spain,1 and Cap de Drassanes,
Institut Català de la Salut, Barcelona, Spain2
Received 20 April 1999/Returned for modification 26 August
1999/Accepted 15 October 1999
A total of 120 mycobacterial isolates were recovered from 1,068 clinical specimens. Of these, 82.5% were in MGIT 960, 83.3% were in
MB/BacT, 80% were in BACTEC 460, and 70% were on
Löwenstein-Jensen medium. Mean times to detection of
Mycobacterium tuberculosis (n = 96) were
significantly shorter with MGIT 960 (12.6 days, P = 0.003) and BACTEC 460 (11.8 days, P < 0.001) than
with MB/BacT (15.9 days). Although, MGIT 960 showed the lowest rate of
recovery of M. kansasii genotype I (64.3%), the earliest
growth was detected with this system (8.9 days). Low and similar rates
of contamination were obtained with MGIT 960 (3.3%) and MB/BacT (3%).
The AccuProbe test for identification showed excellent sensitivities
with MGIT 960 (96.8%) and MB/BacT (100%) cultures. In addition to
being nonradiometric, both MGIT 960 and MB/BacT are accurate, rapid, and labor-saving detection systems which could replace the radiometric method.
Today the conventional procedures of
microscopy and culture are irreplaceable diagnostic tools for
mycobacterial infections (19, 24). A combination of solid
and liquid media is currently the "gold standard" for primary
isolation of mycobacteria (13, 19, 24). The implementation
of the radiometric BACTEC 460 system (Becton Dickinson, Sparks, Md.) in
the last two decades has been a major step forward and, together with a
DNA probe (AccuProbe; GenProbe, San Diego, Calif.), has dramatically
reduced the time to diagnosis of mycobacterial infections (13, 17,
19). However, BACTEC 460 TB has a number of well-known
disadvantages: (i) it requires the use of radioactive reagents
([14C]palmitic acid), (ii) it is labor-intensive in the
handling of vials and maintainence of the instrument, and (iii) there
is a potential risk of cross-contamination of the cultures
(6). Recently, several nonradiometric methods for continuous
monitoring of growth have been introduced in order to resolve some of
these problems (3, 5, 6, 10, 12, 15, 18, 21, 23, 25, 27).
The aim of this study was to evaluate in parallel the BACTEC MGIT 960 system (Becton Dickinson) and the MB/BacT system (Organon Teknika,
Boxtel, The Netherlands) for recovery of mycobacteria and also to
determine the feasibility of the direct application of AccuProbe to
both media for rapid mycobacterial identification. Results of
simultaneous cultures in the BACTEC 460 system and on
Löwenstein-Jensen (LJ) medium were used as the standard for comparison.
A total of 1,066 clinical specimens collected between April and
September 1998 were studied. The specimens from the respiratory tract
(76%) included 605 sputum specimens, 172 bronchial- or
tracheal-aspirate specimens, 24 bronchoalveolar-lavage specimens, and 1 bronchial-brushing specimen. The nonrespiratory specimens (23.8%)
comprised 64 pleural fluid, 64 urine, 30 stool, 36 tissue, 19 gastric
fluid, 14 synovial fluid, 13 cerebrospinal fluid, 12 ascitic fluid, and
2 pericardic fluid specimens. In addition, two environmental samples
(from tap water) suspected of having mycobacterial contamination were included. All samples were processed within 24 h of specimen
collection. The specimens from nonsterile body sites were processed
according to the conventional
N-acetyl-L-cysteine-NaOH
digestion-decontamination procedure (9, 13). Sterile
specimens were centrifuged without decontamination. After being
processed and concentrated, the final sediment of specimens was
suspended in 2 ml of phosphate buffer (pH 6.8). This suspension was
then used for making smears for acid-fast staining with
auramine-rhodamine fluorochrome (13, 19) and for inoculation
into containers with four media: an MGIT tube (Becton Dickinson),
an MB/BacT bottle (Organon Teknika), a BACTEC 12B vial (Becton
Dickinson), and an LJ slant (MAIM, Barcelona, Spain) (solid medium).
All MGIT tubes and BACTEC 12B vials were supplemented with the specific
antibiotic solution PANTA, while the MB/BacT antibiotic supplement was
added only to the MB/BacT bottles for culture of nonsterile specimens,
as recommended by the manufacturer. Equal volumes (0.5 ml) of the
processed specimens were inoculated in each liquid medium, while LJ
medium was inoculated with 0.4 ml of these treated specimens. The order
of the inoculation was randomized. All cultures were incubated at 35 to
37°C for up to 6 weeks. The MGIT tubes were placed in the BACTEC MGIT
960 system, which is a fluorescence-based detection system, and the
MB/BacT bottles were introduced into the MB/BacT instrument, which uses
a colorimetric CO2 detection system. The specimens in LJ
medium were incubated in a 5% CO2 incubator and were
examined once a week. BACTEC 12B vials were read with the BACTEC 460 instrument twice a week for the first two weeks and then weekly up to
the end of incubation. Any BACTEC 12B vial with a growth index (GI) of
All isolates were identified by PCR-restriction fragment length
polymorphism analysis of the hsp65 gene (20) and
conventional biochemical and cultural tests (13, 19). The
AccuProbe assay was performed within 72 h of a positive result
to identify Mycobacterium tuberculosis complex, M. avium complex, and M. kansasii. These gene probes were
selectively applied to each positive culture on the basis of the
pigmentation of the pellet and morphological characteristics by
microscopic examination (14, 26). For all liquid media, 1.5 ml was centrifuged (10 min at 13,000 × g) and the
pellet was used in the hybridization test. Samples producing signals
greater than or equal to 30,000 relative light units (RLUs) were
considered positive (11). Statistical analyses were
performed by the chi-square test, Fisher's exact test, one-way
analysis of variance, and the Kruskal-Wallis one-way analysis of
variance, when appropriate. P values of A total of 120 mycobacterial isolates were recovered in at least one of
the media from 1,068 specimens studied and comprised 106 isolates from
respiratory specimens, 13 isolates from nonrespiratory specimens, and 1 isolate from environmental specimens.
As for total rates of recovery of mycobacteria, the three liquid
systems were comparable, with slightly better sensitivities (not
statistically significant) being shown for the MGIT 960 and MB/BacT
systems (Table 1). This finding was more
outstanding for recovery of M. tuberculosis complex from
smear-negative specimens (Table 1) and suggests that the media and
supplements used in these nonradiometric systems are appropriate and
permit good growth of mycobacteria, even with specimens with low
numbers of bacilli.
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Copyright © 2000, American Society for Microbiology. All rights reserved.
Evaluation of the BACTEC MGIT 960 and the MB/BacT Systems for
Recovery of Mycobacteria from Clinical Specimens and for Species
Identification by DNA AccuProbe
ABSTRACT
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30 was read daily until the GI reached 500. When positive cultures
were detected and a GI of a specimen in BACTEC 12B was 500, such
specimens were removed for confirmation by microscopy and
identification of the microorganism. All positive MGIT tubes, MB/BacT
bottles, and BACTEC 12B vials, which were acid-fast-stain negative,
were reincubated up to the sixth week of incubation. Whenever growth was detected in only the MGIT 960 or MB/BacT system, the negative culture of the another system was subcultured in the LJ medium at the
end of the incubation period.
0.05 were
considered to be statistically significant.
TABLE 1.
Detection of mycobacteria from 1,068 smear-positive and
smear-negative specimens with each culture system
Interestingly, all M. kansasii isolates in this study were
of genotype I (Table 2), and the recovery
rates obtained with the BACTEC 460 system (100%) were significantly
superior to those obtained with the MGIT 960 system (64.3%,
P = 0.04) but not those obtained with the MB/BacT
system (92.9%). In addition, one M. kansasii genotype I
isolate that was not detected with the MGIT 960 instrument was
recovered by subculture of the MGIT tube on LJ medium (false negative).
These results are important, because M. kansasii (mainly
genotype I) is one of the most frequent and virulent nontuberculous
mycobacterium (NTM) species (1, 4). In contrast, the MB/BacT
system had problems in detecting specimens yielding M. xenopi (Table 2). Of the five M. xenopi isolates recovered by all culture systems combined, four isolates (80%) were
detected by the MGIT 960 system and all were missed by the MB/BacT
system. These four undetected M. xenopi isolates grew in the
MB/BacT medium, as could be demonstrated by microscopy and subculture
of the bottles (false negatives). The reason for this discrepancy
between detection and recovery is not exactly known. A possible
explanation may be the inability of the software-based positive
algorithms of the instrument to detect the slow growth of M. xenopi in the MB/BacT medium. After completion of this study, a
new algorithm was developed for the MB/BacT system to improve the
detection of some slow-growth species.
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The combination of liquid and solid media improved the recovery rates
by each medium alone (Table 3). Although
no significant differences were found, the greatest number of M. tuberculosis complex isolates was recovered when LJ medium was
combined with the MB/BacT or MGIT 960 system, whereas for NTM species
the best sensitivity was obtained with LJ medium plus BACTEC 460.
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The short time required to detect growth is one of the most important
advantages of the radiometric culture method. However, MGIT 960's mean
time of mycobacterium detection was similar to that of BACTEC 460 (Table 4). The mean times until detection of M. tuberculosis complex were significantly shorter in the
MGIT 960 and BACTEC 460 systems than in the MB/BacT system
(P = 0.003 and P < 0.001,
respectively). For NTM isolates, it was surprising that MGIT 960 was
the most rapid culture tested. For M. kansasii genotype I,
the earliest growth was detected with MGIT 960, and statistically
significant differences with MB/BacT (P = 0.012) were
found. Nevertheless, MB/BacT allowed the detection of this microorganism within the same amount of time as BACTEC 460.
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The contamination rates for all specimens were as follows: 3.3% for MGIT 960, 3% for MB/BacT, 1.6% for BACTEC 460, and 4.1% for LJ cultures. Nine false-positive specimens were detected for both the MGIT 960 and MB/BacT systems (false-positivity rate, 0.95%). The contamination rates obtained with MGIT 960 and MB/BacT with the different antibiotic supplements and protocols recommended by the manufactures were similar and among the lowest reported for nonradiometric culture systems (2, 3, 5, 7, 8, 10, 12, 15, 16, 18, 21-23, 25, 27).
All hybridizations by AccuProbe from MB/BacT cultures yielding M. tuberculosis complex, M. avium complex, and M. kansasii genotype I (n = 99) were positive (mean,
595,699 RLUs; range, 33,379 to >900,000 RLUs). Among the 94 positive
MGIT 960 cultures for M. tuberculosis complex, M. avium complex, and M. kansasii genotype I, only three
M. tuberculosis complex isolates could not hybridize with
AccuProbe (mean, 445,535 RLUs; range, 30,625 to >900,000 RLUs).
Therefore, the identification of the most frequent and important
mycobacterium species by AccuProbe within 72 h of positive
nonradiometric liquid culture is rapid and precise. However, BACTEC 460 may require additional days of incubation of positive cultures until
the GI is 500 to achieve a positive hybridization by the AccuProbe
test (18).
Finally, the MGIT 960 and MB/BacT systems have other improvements over the traditional culture techniques. (i) These nonradiometric cultures are continuously monitored, easy-to-use systems with fewer handling requirements than those of the BACTEC 460 system. (ii) The risk of cross-contamination is practically eliminated, because the tubes and bottles do not have to be handled and punctured during readings. Furthermore, the MGIT 960 tubes use screw caps and needle inoculation is not necessary. Also, the MB/BacT culture bottles have been coated with plastic to minimize the risk of shattering glass. (iii) The MB/BacT system has better computerized data management and interface capabilities, but the MGIT 960 software is enough for practical laboratory purposes. (iv) Additionally, the MB/BacT instrument occupies more space in the laboratory than the MGIT 960 instrument, though the new modular design (BacT/Alert 3D) has practically resolved this problem.
In conclusion, the nonradiometric MGIT 960 and MB/BacT systems are automated, sensitive, rapid, and less labor-intensive mycobacterial culturing systems which allow a rapid identification by DNA AccuProbe and may be considered a substitute for the radiometric BACTEC 460 system.
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ACKNOWLEDGMENTS |
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We are grateful to S. H. Siddiqi, P. Kuyt, and J. L. Pérez for critical review of the manuscript. We also thank Becton Dickinson and Organon Teknika for providing us with the MGIT 960 and MB/BacT media and instruments and bioMérieux for AccuProbe culture confirmation kits.
M. A. Benítez was partially supported by a grant from CSUB/ CHIRON-ESPAÑA 1998 (Ciutat Sanitària i Universitària de Bellvitge).
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FOOTNOTES |
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* Corresponding author. Mailing address: Servei de Microbiologia, Hospital "Princeps d'Espanya," Ciutat Sanitària i Universitària de Bellvitge, C/Feixa Llarga s/n, 08907 L'Hospitalet de Llobregat, Barcelona, Spain. Phone: 34-93-2607930. Fax: 34-93-2607547. E-mail: falcaide{at}csub.scs.es.
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Journal of Clinical Microbiology, January 2000, p. 398-401, Vol. 38, No. 1
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