{"id":1726,"date":"2025-08-17T14:57:38","date_gmt":"2025-08-17T05:57:38","guid":{"rendered":"https:\/\/lmi.jp\/articles\/?p=1726"},"modified":"2025-11-26T14:27:38","modified_gmt":"2025-11-26T05:27:38","slug":"isolation-frequency-ofcarbapenem-nonsusceptible-bacteroides-spp-and-detection-methods-for-cfia-positive-bacteroides-fragilis","status":"publish","type":"post","link":"https:\/\/lmi.jp\/articles\/2025\/08\/17\/isolation-frequency-ofcarbapenem-nonsusceptible-bacteroides-spp-and-detection-methods-for-cfia-positive-bacteroides-fragilis\/","title":{"rendered":"Isolation frequency ofcarbapenem-nonsusceptible Bacteroides spp. and detection methods for cfiA-positive Bacteroides fragilis"},"content":{"rendered":"\n

Yukiko Takemori-Sakai<\/strong><\/a>*1<\/sup>, \u2020Yasunori Iwata<\/strong><\/a>*2,3<\/sup>, Hatsumi Otani<\/strong><\/a>*1<\/sup>, Akiko Maekawa<\/strong><\/a>*1<\/sup>, Hiroyasu Oe<\/strong><\/a>*1<\/sup>, Megumi Oshima<\/strong><\/a>*1,2<\/sup>, Mika Mori<\/strong><\/a>*1,4<\/sup>, Yoshio Sakai<\/a><\/strong>*5<\/sup>, Toshifumi Gabata<\/strong><\/a>*1<\/sup><\/p>\n\n\n\n

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\u2003 <\/span>Cite<\/span><\/i><\/i><\/span><\/summary>
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Takemori-Sakai Y, Iwata Y, Otani H, Maekawa A, Oe H, Oshima M, Mori M, Sakai Y, Gabata T. Isolation frequency ofcarbapenem-nonsusceptible Bacteroides spp. and detection methods for cfiA-positive Bacteroides fragilis. Lab Med Int 2025; 4(2): 62-68. doi: 10.51041\/lmi.4.2_62<\/p>\n<\/div><\/details>\n<\/div>\n\n\n\n

Original
Lab Med Int 2025; 4(2): 62-68<\/p>\n\n\n\n

\u2020\u0007Division of Infection Control, Department of Nephrology and Laboratory Medicine, Kanazawa University Hospital13-1 Takara-machi, Kanazawa 920-8641, Japan
E-mail: iwatay”@”staff.kanazawa-u.ac.jp
Received March 20, 2023; accepted January 13, 2025
*1 Division of Clinical Laboratory Medicine, Kanazawa University, Kanazawa, Japan
*2 Department of Nephrology and Laboratory Medicine, Kanazawa University, Kanazawa, Japan
*3 Division of Infection Control, Kanazawa University, Kanazawa, Japan
*4 Department of Cardiovascular and Internal Medicine, Kanazawa University, Kanazawa, Japan
*5 Department of Gastroenterology, Kanazawa University, Kanazawa, Japan<\/span><\/strong><\/p>\n\n\n\n

Download PDF<\/span><\/a><\/div>\n\n\n\n

ABSTRACT<\/strong><\/h2>\n\n\n\n

Aims:<\/strong> Bacteroides fragilis<\/em> is the most common anaerobic bacteria causing infectious diseases in humans. A cfiA <\/em>gene encoding metallo-\u03b2-lactamase, which degrades carbapenem, has been reported as a resistance mechanism against carbapenem. Therefore, the detection of cfiA<\/em> gene is important for determining appropriate antibiotic therapy. Although cfiA<\/em> gene is detected via polymerase chain reaction (PCR), simpler and easier methods are required in clinical settings. We compared the detectability of cfiA<\/em>-positive B.<\/em> fragilis <\/em>using multiple methods. Moreover, the isolation frequency of carbapenem-nonsusceptible Bacteroides<\/em> spp. was evaluated. 
Methods:<\/strong> Bacteroides<\/em> spp. was isolated from clinical specimens at the Kanazawa University Hospital. Antimicrobial susceptibility testing was performed via broth microdilution. We explored whether matrix-assisted laser desorption ionization\u2013time of flight mass spectrometry (MALDI-TOF MS) and modified carbapenem inactivation method (mCIM) can show cfiA<\/em> gene positivity. 
Results:<\/strong> Around 20-50 Bacteroides<\/em> spp. strains\/year were isolated from June 2015 to December 2020. Among these, 0-8 strains exhibited meropenem and\/or imipenem nonsusceptibility (intermediate and resistant) in each year. An increased rate of carbapenem resistance, including meropenem- and imipenem-nonsusceptible Bacteroides<\/em> spp., was observed. All carbapenem-nonsusceptible Bacteroides<\/em> spp. were susceptible to metronidazole. Four (66.7%) of 6 strains showed cfiA<\/em> gene positivity based on PCR. 
Conclusions:<\/strong> MALDI-TOF MS and mCIM detected cfiA<\/em>-positive strains. MALDI-TOF MS and mCIM are useful for detecting cfiA<\/em>-positive B.<\/em> fragilis<\/em>. Because the isolation frequency of carbapenem-nonsusceptible Bacteroides <\/em>spp. is increasing, determining their susceptibility is important for appropriate antimicrobial therapy.<\/p>\n\n\n\n

\u3014Lab Med Int 2025; 4(2): 62-68\u3015<\/p>\n\n\n\n

Key Words<\/strong><\/h3>\n\n\n\n

Bacteroides<\/em> spp., carbapenem resistance, cfiA <\/em>gene<\/p>\n\n\n\n

I. Introduction<\/strong><\/h2>\n\n\n\n

Bacteroides<\/em> spp. are anaerobic bacteria that form normal microbiota in the intestinal tract. They are important pathogenic bacteria for humans in diseased conditions. In particular, antimicrobial-resistant Bacteroides<\/em> spp. infection reportedly shows poor prognosis and prolonged hospitalization1)<\/strong><\/sup>. Bacteroides fragilis<\/em> is the most common anaerobic bacteria causing infectious disease in humans 2)<\/sup><\/strong>.
Carbapenem resistance in B. fragilis<\/em> was first reported in 1983 in Japan3)<\/strong><\/sup> and in 1986 in the United States4)<\/strong><\/sup>. Although their resistance mechanism to carbapenem remains unclear, the involvement of cfiA <\/em>gene encoding metallo-\u03b2-lactamase (MBL), which degradates carbapenem, has been reported5)<\/strong><\/sup>. Considering the poor prognosis of carbapenem-resistant B. fragilis<\/em> infection, the detection of cfiA<\/em> gene is important. While cfiA<\/em> gene is detected via polymerase chain reaction (PCR), this method is available only in some hospitals. Therefore, simpler and easier methods are required in clinical settings. In this study, the detectability of cfiA<\/em>-positive B. fragilis<\/em> was compared using multiple methods. Moreover, the isolation frequency of carbapenem-nonsusceptible Bacteroides<\/em> spp., especially cfiA<\/em>-positive strains, was evaluated.<\/p>\n\n\n\n

II. Materials and methods<\/strong><\/h2>\n\n\n\n

Strains and identification<\/em><\/strong>
Bacteroides<\/em> spp. were isolated from clinical specimens at the Kanazawa University Hospital between June 2015 and December 2020. The specimen was applied and cultured on brucella agar medium (Kyokuto, Tokyo, Japan) for 2 days under anaerobic conditions at 35\u2103. The isolated strains were identified using a Bacteroides Bile Esculin agar (BBE Agar, Kyokuto Pharmaceutical Industrial Co., Ltd., Tokyo, Japan) and AccuDiaTM<\/sup> Bacteroides Agar (BA, Shimadzu Diagnostics Corporation, Tokyo, Japan) according to the each directions. B. fragilis<\/em> group were identified by the change of only BBE Agar color from dark brown to black that appears as zones around the colonies. Non-B. fragilis<\/em> group were identified by the growth on BA and no color change in BBE Agar. Those that grew under aerobic conditions were excluded. Eight carbapenem-nonsusceptible strains, which were stored at our hospital, were re-identified using matrix-assisted laser desorption ionization\u2013time of flight mass spectrometry (MALDI-TOF MS) (MALDI Biotyper, Bruker, Billerica, MA, USA). The strain was applied to the MSP 96 target polished steel BC (Bruker). After drying, 1 \u00b5L of 70% formic acid (Beckman Coulter, Brea, CA, USA) was added. Then, the sample was loaded into MALDI Biotyper after 1 \u00b5L of HCCA portioned (Bruker) was added. The spectra were analyzed using the MALDI Biotyper Compass software (MBT Compass software) (Bruker) following the manufacturer\u2019s instructions.<\/p>\n\n\n\n

Antimicrobial susceptibility testing<\/em><\/strong>
The strain was suspended in ABCM broth (Eiken Chemical Co., Ltd., Tokyo, Japan) and adjusted with McFarland 2 standards. Then, 25 \u00b5L of sample were applied to Brucella Broth Eiken (Eiken Chemical Co., Ltd.). After 100 \u00b5L of the bacterial solution was added to Dry Plate Eiken (Eiken Chemical Co., Ltd.), the plate was incubated under anaerobic conditions at 35\u2103 for 48 h. After 48 h, the growth of the strain was visually observed. The minimum inhibitory concentration (MIC) and interpretive category were determined according to the Clinical and Laboratory Standards Institute M100-ED32 6)<\/sup><\/strong>. The additional MIC measurement of metronidazole (MNZ) was performed on 8 carbapenem-nonsusceptible strains, which were stored at our hospital.<\/p>\n\n\n\n

cfiA gene detection<\/em><\/strong>
cfiA<\/em> gene was detected via PCR. DNA extraction was prepared as follows. The strains were suspended in 200 \u00b5L of sterilized water. Then, 5 \u00b5L of proteinase K (350 U\/mL, Takara Bio Inc., Shiga, Japan) was added, followed by incubation at 50\u2103 for 5 min. After 7 min of incubation in a boiling water bath, the lysate was centrifuged at 10,000 rpm for 5 min. Then, the supernatant was used as a template. The primers were 5\u2019-CCCAACTCTCGGACAAAGTG-3\u2019 and 5\u2019-ACGATCTGCTTGGTATGCTC-3\u2019 7)<\/strong><\/sup>. PCR was performed using 1 \u00b5L of template DNA in a total reaction volume of 25 \u00b5L consisting of EmeraldAmp PCR Master Mix (Takara Bio Inc., Shiga, Japan) and 25 pmol of each primer. Reactions were run in a thermal cycler (Biometra, Gottingen, Germany). The PCR program was as follows: 98\u2103 for 60 s; 30 cycles of 98\u2103 for 10 s, 56\u2103 for 30 s, and 72\u2103 for 60 s; and 72\u2103 for 60 s. Then, 5 \u00b5L of amplicon was analyzed using 2% agarose gel. Strains in which an amplicon was observed at 625 bp were determined to have cfiA<\/em> gene.<\/p>\n\n\n\n

Detection of cfiA-positive B. fragilis by MALDI-TOF MS<\/em><\/strong>
MALDI Biotyper was used in the same way as for bacterial identification. The MALDI Biotyper Subtyping Module with the MBT Compass software automatically identifies not only bacterial species but also possession of cfiA<\/em> gene. Peaks shifts were reported from 4711 Da and 4817 Da (cfiA<\/em>-negative) to 4688 Da and 4826 Da (cfiA<\/em>-positive), respectively8)<\/strong><\/sup>. Strains that matched with the spectra of cfiA<\/em>-positive B. fragilis<\/em> were considered \u201cpresumptive cfiA<\/em>-positive\u201d.<\/p>\n\n\n\n

Detection of cfiA-positive B. fragilis using modified carbapenem inactivation method<\/em><\/strong>
We identified carbapenemase-producing B. fragilis<\/em> using modified carbapenem inactivation method (mCIM)6)<\/strong><\/sup> with a few changes. Briefly, 1 \u00b5L of inoculation loop of anaerobically cultured strain was firmly suspended in 2 mL of BD BBLTM<\/sup> TrypticaseTM<\/sup> Soy Broth (Becton, Dickinson and Company, New Jersey, USA). A meropenem (MEPM) or imipenem (IPM) disk (Eiken Chemical Co., Ltd.), each containing 10 \u00b5g of antibiotic, was added and suspended. After incubation under anaerobic conditions at 35\u2103 for 4 h, the disk was removed from the suspension and placed on a BD BBLTM<\/sup> Muller\u2013Hinton II agar medium (Becton, Dickinson and Company, New Jersey, USA) inoculated with a susceptible Escherichia coli<\/em> indicator (ATCC25922). After incubation under aerobic conditions at 35\u2103 for 24 h, the diameter of growth inhibition zones was measured. MBL-producing Klebsiella pneumoniae<\/em> was used as a positive control in mCIM analysis. The negative control was a culture medium only.<\/p>\n\n\n\n

III. Results<\/strong><\/h2>\n\n\n\n

Patient characteristics<\/em><\/strong>
The study period is from June 2015 to December 2020. Carbapenem-nonsusceptible Bacteroides<\/em> spp. were detected in 17 patients. The mean age of patients was 65.0 years, and 10 patients (59.0%) were female. Their underlying diseases were malignant tumors (11 patients, 64.7%), gastrointestinal disorders (6 patients, 35.3%), and hepatobiliary diseases (4 patients, 23.5%). The strains were detected from pus (9 patients, 52.9%), abdominal cavity and subdiaphragmatic drains (4 patients, 23.5%), bile (3 patients, 17.6%), and blood (1 patient, 5.9%). Fifteen specimens (88.2%) were of abdominal origin. Fourteen patients were treated, and 11 patients (78.5%) received antimicrobials. Especially, 7 (63.6%) of 11 patients were treated with noneffective carbapenems (Fig. 1<\/strong>).<\/p>\n\n\n\n

Isolation frequency of carbapenem-nonsusceptible Bacteroides spp.<\/em><\/strong>
The characters of isolated 233 Bacteroides<\/em> spp. were described in Fig. 2<\/strong>. Two hundred strains were B. fragilis <\/em>group, and 33 strains were non-B. fragilis <\/em>group. Around 20-50 strains\/year were isolated in Kanazawa University Hospital. Among these, 0-8 strains exhibited MEPM and\/or IMP nonsusceptibility (intermediate and resistant) in each year. Although no MEPM-nonsusceptible Bacteroides<\/em> spp. was detected in 2015, its isolation rate peaked at 16% in 2019 and decreased to 7% in 2020 (Fig. 2a<\/strong>). In contrast, the frequency of IPM-nonsusceptible Bacteroides<\/em> spp. increased from 0% in 2015 to 8% in 2020 (Fig. 2b<\/strong>). An increased rate of carbapenem resistance, including MEPM- and IPM-nonsusceptible Bacteroides<\/em> spp., was observed during the period.<\/p>\n\n\n\n

Antimicrobial susceptibility of carbapenem-nonsusceptible Bacteroides spp.<\/em><\/strong>
Nineteen strains of carbapenem-nonsusceptible Bacteroides<\/em> spp. were isolated between 2015 and 2020. Seventeen strains were B. fragilis<\/em> group and 2 were non-B. fragilis<\/em> group. Two patients were positive for both B. fragilis<\/em> group and non-B. fragilis<\/em> group. The antimicrobial susceptibility of these strains is shown in Table 1<\/strong>. Eight of 19 strains were available for susceptibility tests for MNZ. All of the 8 strains were B. fragilis <\/em>group and showed susceptibility to MNZ.<\/p>\n\n\n\n

Detection of cfiA gene from carbapenem-nonsusceptible B. fragilis<\/em><\/strong>
Six of 8 carbapenem-nonsusceptible strains that were stored at our hospital were re-identified as B. fragilis<\/em> via MALDI-TOF MS. The other 2 strains were re-identified as B. thetaiotaomicron<\/em> and B. uniformis<\/em>, respectively. We investigated whether these 6 B. fragilis<\/em> strains possessed cfiA<\/em> gene by performing PCR. Four strains (66.7%) were cfiA<\/em>-positive. Among the preserved strains, a cfiA<\/em>-positive strain was identified in 2016 and 2020 in each and 2 strains were identified in 2019. Then, MALDI-TOF MS was performed to identify strains with cfiA<\/em> gene (Table 2<\/strong>) and was compared to mCIM.<\/p>\n\n\n\n

MALDI-TOF MS detected strains with cfiA gene<\/em><\/strong>
Of 6 B. fragilis<\/em> isolates, 4 strains were detected as presumptive cfiA<\/em>-positive based on MALDI-TOF MS. The other 2 strains were detected as presumptive cfiA<\/em>-negative (Fig. 3<\/strong>). The results of cfiA<\/em>-positive B. fragilis <\/em>based on MALDI-TOF MS were consistent with those of cfiA<\/em> gene based on PCR.<\/p>\n\n\n\n

mCIM revealed the susceptibility of strains with\/without cfiA gene<\/em><\/strong>
Neither MEPM nor IPM disks inhibited the growth of E. coli<\/em> in mCIM analysis of 4 cfiA<\/em>-positive B. fragilis<\/em>. In the analysis of the other 2 cfiA<\/em>-negative B. fragilis<\/em>, E. coli<\/em> formed growth inhibition zones around MEPM disks, with a diameter larger than 20 mm. IPM disks also inhibited the growth of E. coli<\/em> in the analysis of 2 cfiA<\/em>-negative B. fragilis<\/em>, with growth inhibition zones larger than 18 mm (Fig. 4<\/strong>).<\/p>\n\n\n\n

\"\"<\/figure>\n\n\n\n

Figure 1<\/strong>   Treatment of patients infected with carbapenem-nonsusceptible Bacteroides<\/em> spp. Here, 63.6% of patients were treated with noneffective carbapenems.<\/p>\n\n\n\n

\"\"<\/figure>\n\n\n\n

Figure 2<\/strong>   Changes in carbapenem sensitivity from 2015 to 2020 Sensitivity to meropenem (a) and imipenem (b).  An increased rate of carbapenem-nonsusceptible Bacteroides<\/em> spp. was observed in meropenem and imipenem. dot: susceptible, oblique line: intermediate, black: resistant, S: susceptible, I: intermediate, R: resistant.<\/p>\n\n\n\n

Table 1<\/strong> Antimicrobial susceptibility of carbapenem-nonsusceptible Bacteroides spp.<\/p>\n\n\n\n

\"\"<\/figure>\n\n\n\n

S\/A: sulbactam-ampicillin, T\/P: tazobactam-piperacillin, MEPM: meropenem, IPM: imipenem, CLDM: clindamycin, MNZ: metronidazole, S: susceptible, I: intermediate, R: resistant.<\/p>\n\n\n\n

Table 2 <\/strong>Detection results of cfiA-positive B. fragilis via MALDI-TOF MS and mCIM<\/p>\n\n\n\n

\"\"<\/figure>\n\n\n\n

PCR: polymerase chain reaction, MALDI-TOF MS: matrix-assisted laser desorption ionization\u2013time of flight mass spectrometry, mCIM: modified carbapenem inactivation method, MEPM: meropenem, IPM: imipenem.<\/p>\n\n\n\n

\"\"<\/figure>\n\n\n\n

Figure 3<\/strong>   MALDI-TOF MS peaks of cfiA<\/em>-negative and cfiA<\/em>-positive B. fragilis<\/em>.
White arrows indicate peaks of cfiA<\/em>-positive B. fragilis<\/em>. Black arrows indicate peaks of cfiA<\/em>-negative B. fragilis<\/em>. <\/p>\n\n\n\n

\"\"<\/figure>\n\n\n\n

Figure 4 <\/strong>Results of modified carbapenem inactivation method
B. fragilis strains 1, 2, 3, 4 were cfiA-positive, whereas strains 5 and 6 were cfiA-negative. NC is the result of a bacteria-free test. PC is the result of metallo-\u03b2-lactamase-producing Klebsiella pneumoniae.
MEPM: meropenem, IPM: imipenem, NC: negative control, PC: positive control.<\/p>\n\n\n\n

IV. Discussion<\/strong><\/h2>\n\n\n\n

The isolation frequency of carbapenem-nonsusceptible Bacteroides<\/em> spp. was investigated, and methods for detecting cfiA<\/em>-positive B. fragilis<\/em> were examined. This study revealed that the maximum isolation frequency of MEPM- and IPM-nonsusceptible Bacteroides<\/em> spp. was 16% and 8%, respectively. The isolation rate of carbapenem-nonsusceptible Bacteroides<\/em> spp. increased over the past 6 years. Recent reports indicate that carbapenem-nonsusceptible Bacteroides<\/em> spp. have been isolated in some countries with various frequencies9)-11)<\/strong><\/sup>. The increased frequency of carbapenem-resistant Bacteroides<\/em> spp. was also reported in some studies9),12),13)<\/strong><\/sup>. The isolation frequency increased similar to that reported in other studies in Japan9)<\/strong><\/sup>. Therefore, monitoring the isolation frequency of carbapenem-nonsusceptible Bacteroides<\/em> spp. is important in hospitals. Moreover, the detection of carbapenem-nonsusceptible Bacteroides <\/em>spp. is important for determining appropriate antibiotic therapy. We should have investigated the isolation frequency of carbapenem-nonsusceptible B. fragilis<\/em>. Although MALDI-TOF MS analysis identify strains to B. fragilis<\/em>, the equipment was not available during the study period in our facility. Therefore, we investigated the isolation frequency of carbapenem-nonsusceptible strains in the genus Bacteroides<\/em>.<\/p>\n\n\n\n

The isolation rate of MEPM-nonsusceptible Bacteroides <\/em>spp. peaked at 16% in 2019 and decreased to 7% in 2020. Although the reason for the reduced MEPM-nonsusceptible Bacteroides<\/em> spp. frequency is not clear, small sample number may affect the change of frequency in this case.<\/p>\n\n\n\n

In our study, while 4 strains (66.7%) of carbapenem-nonsusceptible B. fragilis<\/em> were cfiA<\/em>-positive, the other 2 strains did not possess the gene. Other than cfiA <\/em>gene, the mechanisms of carbapenem nonsusceptibility remain unclear14)<\/strong><\/sup>. One study showed that functional changes in efflux pumps affect carbapenem sensitivity15)<\/strong><\/sup>. Further studies are needed to clarify the resistance mechanisms, especially in 2 carbapenem-nonsusceptible B. fragilis <\/em>without cfiA<\/em> gene.<\/p>\n\n\n\n

To date, there is no routine method to detect cfiA<\/em>-positive B. fragilis<\/em>. In this study, MALDI-TOF MS and mCIM were useful in detecting cfiA<\/em>-positive B. fragilis<\/em>. A recent study reported that the sensitivity and specificity of MALDI-TOF MS in detecting cfiA<\/em>-positive B. fragilis<\/em> were 100.0% and 99.7%, respectively16)<\/strong><\/sup>. Although MALDI-TOF MS is a simple and quick method, it can be performed only in the facilities with the required equipment. In facilities where MALDI-TOF MS is unavailable, mCIM may be useful. Because mCIM does not require specialized equipment or reagents, it is widely used and can be performed at any facility. Therefore, MALDI-TOF MS and mCIM might provide earlier and more accurate results in determining cfiA<\/em>-positive strains. This will help determine appropriate antimicrobial use for treating carbapenem-nonsusceptible B. fragilis<\/em> infection.<\/p>\n\n\n\n

In summary, even if MALDI-TOF MS or PCR is not available, mCIM is useful for detecting cfiA<\/em>-positive B. fragilis.<\/em> Because the isolation frequency of carbapenem-nonsusceptible Bacteroides<\/em> spp. is increasing, determining its susceptibility is important for appropriate antimicrobial therapy.<\/p>\n\n\n\n

Declarations<\/strong><\/h3>\n\n\n\n

Funding:<\/strong> This work was supported by the Funding Program for Female Researchers, Kanazawa University.<\/p>\n\n\n\n

Conflicts of interest:<\/strong> The authors have declared that no conflict of interest exists.<\/p>\n\n\n\n

Ethics approval:<\/strong> All experiments were performed in accordance with approved guidelines of Kanazawa University. This study was conducted with the approval of the ethics committee of Kanazawa University (approval number: 3596).<\/p>\n\n\n\n

Authorship contributions:<\/strong> YTS and YI designed the study and interpreted the data. YTS performed experiment and wrote the draft of the manuscript together with YI. All authors read the manuscript and commented.<\/p>\n\n\n\n

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