Next Article in Journal / Special Issue
Kampo (Traditional Japanese Herbal) Formulae for Treatment of Stomatitis and Oral Mucositis
Previous Article in Journal
Association of Dietary Advanced Glycation End Products with Metabolic Syndrome in Young Mexican Adults
Previous Article in Special Issue
Quercetin Enhances the Thioredoxin Production of Nasal Epithelial Cells In Vitro and In Vivo
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Antimicrobial Susceptibilities of Oral Isolates of Abiotrophia and Granulicatella According to the Consensus Guidelines for Fastidious Bacteria

by
Taisei Kanamoto
1,2,*,
Shigemi Terakubo
2 and
Hideki Nakashima
2
1
Laboratory of Microbiology, Showa Pharmaceutical University, Machida, Tokyo 194-8543, Japan
2
Department of Microbiology, St. Marianna University School of Medicine, Kawasaki, Kanagawa 216-8511, Japan
*
Author to whom correspondence should be addressed.
Medicines 2018, 5(4), 129; https://doi.org/10.3390/medicines5040129
Submission received: 7 November 2018 / Revised: 29 November 2018 / Accepted: 29 November 2018 / Published: 3 December 2018

Abstract

:
Background: The genera Abiotrophia and Granulicatella, previously known as nutritionally variant streptococci (NVS), are fastidious bacteria requiring vitamin B6 analogs for growth. They are members of human normal oral microbiota, and are supposed to be one of the important pathogens for so-called “culture-negative” endocarditis. Methods: The type strains and oral isolates identified, by using both phenotypic profiles and the DNA–DNA hybridization method, were examined for susceptibilities to 15 antimicrobial agents including penicillin (benzylpenicillin, ampicillin, amoxicillin, and piperacillin), cephem (cefazolin, ceftazidime, ceftriaxone, and cefaclor), carbapenem (imipenem), aminoglycoside (gentamicin), macrolide (erythromycin), quinolone (ciprofloxacin), tetracycline (minocycline), glycopeptide (vancomycin), and trimethoprim-sulfamethoxazole complex. The minimum inhibitory concentration and susceptibility criterion were determined, according to the consensus guideline from the Clinical and Laboratory Standards Institute. Results: Isolates of Abiotrophia defectiva were susceptible to ampicillin, amoxicillin ceftriaxone, cefaclor, imipenem, ciprofloxacin, and vancomycin. Isolates of Granulicatella adiacens were mostly susceptible to benzylpenicillin, ampicillin, amoxicillin, cefazolin, ceftriaxone, imipenem, minocycline, and vancomycin. The susceptibility profile of Granulicatella elegans was similar to that of G. adiacens, and the susceptibility rate was higher than that of G. adiacens. Conclusions: Although Abiotrophia and Granulicatella strains are hardly distinguishable by their phenotypic characteristics, their susceptibility profiles to the antimicrobial agents were different among the species. Species-related differences in susceptibility of antibiotics should be considered in the clinical treatment for NVS related infections.

1. Introduction

The bacteria formerly known as nutritionally variant streptococci (NVS) are characterized by their growth as small satellite colonies supported by helper bacteria such as Staphylococcus aureus [1]. The NVS strains require vitamin B6 analogs for growth and produce bacteriolytic enzymes, pyrrolidonyl arylamidase and chromophore in common and were supposed to be auxotrophic variants of viridans group streptococci [2]. After several taxonomic alterations, they were finally transferred into two new genera, Abiotrophia and Granulicatella, on the basis of 16S rRNA gene sequence homology analysis [3,4]. They have been estimated as one of the important pathogens of so-called ‘culture-negative endocarditis’ [2,5,6]; however, because of their fastidiousness in growth, difficulty in identification, and complication in taxonomic position, the clinical importance of these bacteria has been underestimated by clinicians [7].
Although there have been several studies on the antimicrobial susceptibility of NVS, most of the previous studies dealt with a small number of strains, and methods and results were variable [2]. Furthermore, the taxonomic backgrounds of the tested isolates were uncertain. Commercial identification systems, based on the phenotypic characteristics of cultured bacteria, have often misidentified the clinical isolates of Granulicatella as Gemella morbillorum, and cannot distinguish Granulicatella adiacens and Granulicatella elegans [8,9,10]. To distinguish the two species of Granulicatella, molecular genetic analysis is required [11]. We previously isolated 91 strains of NVS from the human oral microbiota and classified them based on the phenotypic characteristics [9]. Among the oral isolates, 37 isolates confirmed their taxonomic identification by using DNA–DNA hybridization homology analysis, and we reported genetic heterogeneities in genus Granulicatella [10].
The Clinical and Laboratory Standards Institute (CLSI) published a laboratory guideline of antimicrobial susceptibility testing of infrequently encountered or fastidious bacteria, not covered in previous CLSI publications [12]. In this study, we determined the minimum inhibitory concentrations (MICs) of the taxonomically confirmed strains of Abiotrophia and Granulicatella, according to the consensus guideline provided by CLSI.

2. Materials and Methods

2.1. Bacterial Strains

Seven Abiotrophia defectiva, 17 Granulicatella adiacens, and six Granulicatella elegans (including type strains and oral isolates) were examined (see Table 1 and Table 2). All isolates were identified using the rapid ID32 STREP system (Bio Mérieux SA, Marcy-l’Etoile, France) and DNA-DNA hybridization homology analysis [10]. The reference strains, A. defectiva ATCC 49176T, NVS-47, and PE7, G. adiacens ATCC 49175T, and G. elegans DSM11693T, were from patients with endocarditis or bacteremia [13,14,15], and the other 25 isolates were derived from the oral cavity of healthy volunteers [9]. The strain Streptococcus pneumoniae ATCC 49619 was included in the assay to monitor accuracy of the MIC tests. The ATCC strains were obtained from American Type Culture Collection (Manassas, VA, USA), the DSM strain was obtained from Deutsche Sammlung von Mikroorganismen und Zellkulturen GmbH (Braunschweig, Germany), and the other strains were from the stock culture collection in our laboratory.

2.2. Antimicrobial Agents

Fifteen antimicrobial agents including penicillin, cephem, carbapenem, aminoglycoside, macrolide, tetracycline, quinolone, glycopeptide, and sulfonamide were used for this study (see Table 3). The following agents were purchased from Wako Pure Chemical Industries, Ltd. (Osaka, Japan): benzylpenicillin, cefazolin, piperacillin, ciprofloxacin, minocycline, and trimethoprim-sulfamethoxazole complex. Ampicillin, ceftazidime, ceftriaxone, cefaclor, gentamicin, erythromycin, and vancomycin were obtained from Sigma Chemical Co. (St. Louis, MO, USA). Amoxicillin was purchased from Fluka Biochemika (Bucks, Switzerland). Imipenem was kindly supplied by the Banyu Pharmaceutical Co., Ltd. (Tokyo, Japan).

2.3. MIC Testing

For preparation of inoculum, tested isolates were cultured anaerobically at 37 °C for 20 to 24 h with Mueller-Hinton broth (MHB; Difco Becton Dickinson and company, Sparks, MD, USA) containing 0.001% pyridoxal hydrochloride (Wako) and the bacterial cell suspensions were adjusted to yield about 5 × 105 CFU/mL. MICs for the Abiotrophia and Granulicatella strains were determined using the microdilution broth method with MHB containing 2.5% lysed horse blood (Strepto hemo supplement ‘Eiken’, Eiken Chemical Co., Ltd., Tokyo, Japan) and 0.001% pyridoxal hydrochloride, according to the consensus guideline from the CLSI for fastidious bacteria [12]. Briefly, the antimicrobial agents (100 µL/well) were diluted on 96-well round bottom plates (Sumilon, Sumitomo Bakelite Co., Ltd., Tokyo, Japan) in serial two-fold with the supplemented MHB, and 5 µL of the bacterial inoculum was added to each well. The plates were incubated at 35 °C in anaerobic condition for 20 h. The MIC values were defined as the lowest concentrations of antimicrobial agents that completely inhibited the bacterial growth in the microdilution wells, detected by unaided eyes. The strain of S. pneumoniae ATCC 49619 was used for quality control testing, and all MIC values for the strain were within the acceptable limits.

2.4. Susceptibility Criteria

The MIC values for bacterial isolates to the antimicrobial agents benzylpenicillin, ampicillin, ceftriaxone imipenem, erythromycin, ciprofloxacin, and vancomycin were interpreted into 3 categories: Susceptible, intermediate, and resistant, according to the CLSI guideline for Abiotrophia spp. and Granulicatella spp.
The MIC values for amoxicillin and piperacillin, and those for cefazolin, ceftazidime, and cefaclor were interpreted using criteria for ampicillin and cephems in the guideline for Abiotrophia and Granulicatella, respectively [16]. The MIC values for gentamicin and minocycline were interpreted using criteria in the CLSI guideline for S. aureus and for Streptococcus spp. Viridans group, respectively. The MIC values under 2/38 µg/mL for trimethoprim-sulfamethoxazole were interpreted as susceptible [17].

3. Results

The susceptibility percentage of the NVS isolates for 15 antimicrobial agents was summarized in Table 3. Although the phenotypic characteristics of the NVS isolates were similar, the profiles of susceptibility were unique among the species. The NVS isolates were susceptible to ampicillin (96.7%), amoxicillin (100%), imipenem (100%), and vancomycin (96.7%). In addition, A. defectiva strains were susceptible to ceftriaxone (100%), cefaclor (85.7%), and ciprofloxacin (100%); and G. adiacens strains were susceptible to benzylpenicillin (82.7%), cefazolin (88.2%), ceftriaxone (76.4%), and minocycline (94.1%). The susceptibility profile of G. elegans was similar to that of G. adiacens, and the susceptibility percentages of G. elegans to beta-lactams were higher than that of G. adiacens. On the other hand, no NVS strains were susceptible to gentamicin, and 93.3% of the strains were not susceptible to trimethoprim/sulfamethoxazole. Piperacillin susceptibility rate of A. defectiva was 0%, while that of G. adiacens and G. elegans were 52.9% and 100%, respectively. All A. defectiva strains were susceptible to ciprofloxacin, but only 17.4% of Granulicatella strains were susceptible to it.
Individual MIC values of A. defectiva and Granulicatella isolates to the antimicrobial agents were shown in Table 1 and Table 2, respectively. Benzylpenicillin-nonsusceptible oral isolates of A. defectiva C1-2 and YK-3 were highly resistant to cefazolin and ceftazidime (both MICs = 16 µg/mL) and C1-2 showed additional resistance to cefaclor (MIC = 32 µg/mL), but were susceptible to ceftriaxone (MIC ≤ 1 µg/mL). Oral isolate of G. adiacens HHC3 was highly multi-drug resistant to ceftazidime, gentamycin, ciprofloxacin, and minocycline. The benzylpenicillin-nonsusceptible oral isolate of G. adiacens P7-4 was resistant to cephems, including ceftazidime, ceftriaxone, and cefaclor (all MICs = 4 µg/mL). Among the NVS isolates, only G. elegans DSM11693T was resistant to vancomycin (MIC = 4 µg/mL).

4. Discussion

Abiotrophia and Granulicatella species are very common inhabitants in human normal oral microbiota, in spite of their fastidiousness in growth [9,11,18,19,20], and are significant causative pathogens of endocarditis, bacteremia, and other systemic infections [21,22,23,24]. They often cannot grow on commercial blood agar plates used for the usual clinical examination, and even if they could grow on supplemented culture plates, their colonies are sometimes small, 0.2 to 0.5 mm in diameter [1,25]. Therefore, these fastidious microorganisms have been overlooked in clinical specimens from foci of infective diseases, especially when they are concomitant with easily recovered bacteria (such as S. aureus). Based on their phenotypic characteristics, Abiotrophia and Granulicatella spp. were initially classified as members of genus Streptococcus. Although genera Abiotrophia and Granulicatella were transferred and divided into two groups, based on the 16S rRNA sequence homology analysis, they have been treated as a same bacterial group of NVS in the field of clinical infectious diseases because they have common phenotypic characteristics, such as requiring vitamin B6 analogs in growth and producing bacteriolytic enzymes. The human oral cavity is assumed to be a reservoir for the pathogens of many systemic infective diseases, so it is important to examine the antimicrobial susceptibilities of oral bacteria. In this study, we determined MICs of genetically identified seven Abiotrophia and 23 Granulicatella isolates (including oral isolates), according to the guideline from CLSI. Although NVS species have biochemical and phenotypic properties in common, and are difficult to distinguish without molecular genetical identification methods, the susceptibility profiles to antimicrobial agents were different among the species (Table 3).
Because of their fastidiousness, NVS species often were not recovered from the specimen in the usual clinical examination for infectious diseases caused by these bacteria. When no bacteria are recovered from the specimen of infective diseases, and that happens often, the empiric therapy with broad-spectrum antimicrobial agents (such as carbapenem, macrolide, quinolone, and tetracycline) is selected by the clinicians. As with the antimicrobials tested, all NVS isolates were susceptible to imipenem, and species-related differences were observed with respect to susceptibilities to ciprofloxacin and minocycline. The ciprofloxacin susceptibility rate for A. defectiva isolates was 100%, and that for Granulicatella isolates was 17.4%. In contrast, the susceptibility rate of minocycline for Abiotrophia isolates was 57.1%, and that for Granulicatella isolates was 95.7%. Species-related differences in susceptibility of antibiotics should be considered in the empiric therapy for NVS related infections.
In case of infective endocarditis (IE) caused by NVS, a combination of benzylpenicillin and gentamycin has been used for the antibiotic therapy [26,27,28,29]. However, 42.9% of A. defectiva isolates were not susceptible to benzylpenicillin and no strains of NVS isolates were susceptible to gentamycin in this study. Aminopenicillins, ampicillin, and amoxicillin showed better susceptible rates than benzylpenicillin and piperacillin. Ceftriaxone and ceftazidime are both third generation cephem, but the susceptible rates were contrary: Only three isolates of G. elegans (10.0% of the NVS isolates) were susceptible to ceftazidime. In contrast, 86.6% of the NVS isolates were susceptible to ceftriaxone (Table 3). According to the guidelines for endocarditis treatment by the British Society for Antimicrobial Chemotherapy, vancomycin can be used alone for the NVS IE patients with penicillin allergy [29]. The susceptibility rate of vancomycin for NVS isolates in our study was 96.7%. In the antimicrobial treatment of NVS IE, the recommended initial drugs (the combination of benzylpenicillin and gentamycin) may not be effective, and the regimen of initial drugs should be reconsidered.
Some isolates showed unique susceptibility profiles, for example, A. defectiva C1-2 showed multi-drug resistance to piperacillin, cefazolin, ceftazidime, cefaclor, gentamicin, erythromycin, and minocycline, but was susceptible to amoxicillin and ceftriaxone. Some G. adiacens isolates, such as HHC3, YTC1, and YTT3, were highly resistant to ceftazidime but susceptible to ceftriaxone, ampicillin, and amoxicillin. G. adiacens P7-4 was not susceptible to benzylpenicillin, piperacillin, and cefazolin, and was resistant to ceftriaxone, ceftazidime, and cefaclor, but was susceptible to ampicillin and amoxicillin. In the antimicrobial process, beta-lactams are bound to the penicillin binding protein (PBP) of the bacteria and inhibit their cell wall synthesis. The minor variations of PBP(s) may affect the antimicrobial susceptibilities of these isolates. Further molecular genetic research is needed to determine the mechanism of resistance in the NVS isolates with unique susceptibility profiles.

Author Contributions

T.K. and H.N. conceived the study. T.K. and S.T. performed the laboratory work. T.K. wrote the manuscript. All authors read and approved the final manuscript.

Funding

This study was supported by Department of Microbiology, St. Marianna University School of Medicine.

Acknowledgments

We thank Hiromu Takemura, for advice and stimulating discussions.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Frenkel, A.; Hirsch, W. Spontaneous development of L forms of streptococci requiring secretions of other bacteria or sulphydryl compounds for normal growth. Nature 1961, 191, 728–730. [Google Scholar] [CrossRef] [PubMed]
  2. Ruoff, K.L. Nutritionally variant streptococci. Clin. Microbiol. Rev. 1991, 4, 184–190. [Google Scholar] [CrossRef] [PubMed]
  3. Kawamura, Y.; Hou, X.G.; Sultana, F.; Liu, S.; Yamamoto, H.; Ezaki, T. Transfer of Streptococcus adjacens and Streptococcus defectivus to Abiotrophia gen. nov. as Abiotrophia adiacens comb. nov. and Abiotrophia defectiva comb. nov., respectively. Int. J. Syst. Bacteriol. 1995, 45, 798–803. [Google Scholar] [CrossRef] [PubMed]
  4. Collins, M.D.; Lawson, P.A. The genus Abiotrophia (Kawamura et al.) is not monophyletic: Proposal of Granulicatella gen. nov., Granulicatella adiacens comb. nov., Granulicatella elegans comb. nov. and Granulicatella balaenopterae comb. nov. Int. J. Syst. Evol. Microbiol. 2000, 50 Pt 1, 365–369. [Google Scholar] [CrossRef] [PubMed]
  5. Casalta, J.P.; Habib, G.; La Scola, B.; Drancourt, M.; Caus, T.; Raoult, D. Molecular diagnosis of Granulicatella elegans on the cardiac valve of a patient with culture-negative endocarditis. J. Clin. Microbiol. 2002, 40, 1845–1847. [Google Scholar] [CrossRef] [PubMed]
  6. Tattevin, P.; Watt, G.; Revest, M.; Arvieux, C.; Fournier, P.E. Update on blood culture-negative endocarditis. Med. Mal. Infect. 2015, 45, 1–8. [Google Scholar] [CrossRef] [PubMed]
  7. Tellez, A.; Ambrosioni, J.; Llopis, J.; Pericas, J.M.; Falces, C.; Almela, M.; Garcia de la Maria, C.; Hernandez-Meneses, M.; Vidal, B.; Sandoval, E.; et al. Epidemiology, Clinical Features, and Outcome of Infective Endocarditis due to Abiotrophia Species and Granulicatella Species: Report of 76 Cases, 2000–2015. Clin. Infect. Dis. 2018, 66, 104–111. [Google Scholar] [CrossRef]
  8. Coto, H.; Berk, S.L. Endocarditis caused by Streptococcus morbillorum. Am. J. Med. Sci. 1984, 287, 54–58. [Google Scholar] [CrossRef]
  9. Kanamoto, T.; Eifuku-Koreeda, H.; Inoue, M. Isolation and properties of bacteriolytic enzyme-producing cocci from the human mouth. FEMS Microbiol. Lett. 1996, 144, 135–140. [Google Scholar] [CrossRef] [Green Version]
  10. Kanamoto, T.; Sato, S.; Inoue, M. Genetic heterogeneities and phenotypic characteristics of strains of the genus Abiotrophia and proposal of Abiotrophia para-adiacens sp. nov. J. Clin. Microbiol. 2000, 38, 492–498. [Google Scholar]
  11. Sato, S.; Kanamoto, T.; Inoue, M. Abiotrophia elegans strains comprise 8% of the nutritionally variant streptococci isolated from the human mouth. J. Clin. Microbiol. 1999, 37, 2553–2556. [Google Scholar] [PubMed]
  12. Jorgensen, J.H.; Hindler, J.F. New consensus guidelines from the Clinical and Laboratory Standards Institute for antimicrobial susceptibility testing of infrequently isolated or fastidious bacteria. Clin. Infect. Dis. 2007, 44, 280–286. [Google Scholar] [CrossRef] [PubMed]
  13. Bouvet, A.; Grimont, F.; Grimont, P.A.D. Streptococcus defectivus sp. nov. and Streptococcus adjacens sp. nov., nutritionally variant streptococci from human clinical specimens. Int. J. Syst. Bacteriol. 1989, 39, 290–294. [Google Scholar] [CrossRef]
  14. van de Rijn, I.; George, M. Immunochemical study of nutritionally variant streptococci. J. Immunol. 1984, 133, 2220–2225. [Google Scholar] [PubMed]
  15. Roggenkamp, A.; Abele-Horn, M.; Trebesius, K.H.; Tretter, U.; Autenrieth, I.B.; Heesemann, J. Abiotrophia elegans sp. nov., a possible pathogen in patients with culture-negative endocarditis. J. Clin. Microbiol. 1998, 36, 100–104. [Google Scholar] [PubMed]
  16. CLSI. Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria; Approved Guideline M45-A; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2006; Volume 26, pp. 10–11. [Google Scholar]
  17. CLSI. Methods for Dilution Antimicirobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard-Seventh Edition M7-A7. In Performance Standards for Antimicrobial Susceptibility Testing; Eighteenth Informational Supplement M100-S18; Wikler, M.A., Ed.; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2008; Volume 27, pp. 86–161. [Google Scholar]
  18. Aas, J.A.; Paster, B.J.; Stokes, L.N.; Olsen, I.; Dewhirst, F.E. Defining the normal bacterial flora of the oral cavity. J. Clin. Microbiol. 2005, 43, 5721–5732. [Google Scholar] [CrossRef]
  19. Diaz, P.I.; Chalmers, N.I.; Rickard, A.H.; Kong, C.; Milburn, C.L.; Palmer, R.J., Jr.; Kolenbrander, P.E. Molecular characterization of subject-specific oral microflora during initial colonization of enamel. Appl. Environ. Microbiol. 2006, 72, 2837–2848. [Google Scholar] [CrossRef]
  20. Zaura, E.; Keijser, B.J.; Huse, S.M.; Crielaard, W. Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol. 2009, 9, 259. [Google Scholar] [CrossRef]
  21. Brouqui, P.; Raoult, D. Endocarditis due to rare and fastidious bacteria. Clin. Microbiol. Rev. 2001, 14, 177–207. [Google Scholar] [CrossRef]
  22. Woo, P.C.; To, A.P.; Lau, S.K.; Fung, A.M.; Yuen, K.Y. Phenotypic and molecular characterization of erythromycin resistance in four isolates of Streptococcus-like gram-positive cocci causing bacteremia. J. Clin. Microbiol. 2004, 42, 3303–3305. [Google Scholar] [CrossRef]
  23. Senn, L.; Entenza, J.M.; Greub, G.; Jaton, K.; Wenger, A.; Bille, J.; Calandra, T.; Prod’hom, G. Bloodstream and endovascular infections due to Abiotrophia defectiva and Granulicatella species. BMC Infect. Dis. 2006, 6, 9. [Google Scholar] [CrossRef] [PubMed]
  24. De Luca, M.; Amodio, D.; Chiurchiu, S.; Castelluzzo, M.A.; Rinelli, G.; Bernaschi, P.; Calo Carducci, F.I.; D’Argenio, P. Granulicatella bacteraemia in children: Two cases and review of the literature. BMC Pediatr. 2013, 13, 61. [Google Scholar] [CrossRef] [PubMed]
  25. Reimer, L.G.; Reller, L.B. Growth of nutritionally variant streptococci on laboratory media supplemented with blood of eight animal species. Med. Lab. Sci. 1982, 39, 79–81. [Google Scholar] [PubMed]
  26. Cargill, J.S.; Scott, K.S.; Gascoyne-Binzi, D.; Sandoe, J.A. Granulicatella infection: Diagnosis and management. J. Med. Microbiol. 2012, 61, 755–761. [Google Scholar] [CrossRef] [PubMed]
  27. Ohara-Nemoto, Y.; Kishi, K.; Satho, M.; Tajika, S.; Sasaki, M.; Namioka, A.; Kimura, S. Infective endocarditis caused by Granulicatella elegans originating in the oral cavity. J. Clin. Microbiol. 2005, 43, 1405–1407. [Google Scholar] [CrossRef] [PubMed]
  28. Lin, C.H.; Hsu, R.B. Infective endocarditis caused by nutritionally variant streptococci. Am. J. Med. Sci. 2007, 334, 235–239. [Google Scholar] [CrossRef] [PubMed]
  29. Gould, F.K.; Denning, D.W.; Elliott, T.S.; Foweraker, J.; Perry, J.D.; Prendergast, B.D.; Sandoe, J.A.; Spry, M.J.; Watkin, R.W.; Working Party of the British Society for Antimicrobial Chemotherapy. Guidelines for the diagnosis and antibiotic treatment of endocarditis in adults: A report of the Working Party of the British Society for Antimicrobial Chemotherapy. J. Antimicrob. Chemother. 2012, 67, 269–289. [Google Scholar] [CrossRef] [PubMed]
Table 1. MICs (µg/mL) of 15 antibiotics against Abiotrophia isolates.
Table 1. MICs (µg/mL) of 15 antibiotics against Abiotrophia isolates.
StrainsPENAMPAMXPIPCFZCAZCROCECIPMGENERYCIPMINVANSXT
A. defectiva
ATCC49176T0.1250.0160.016111610.1250.125320.510.0630.25256/4864
NVS-470.1250.0320.016121610.1250.125320.510.0320.25256/4864
PE70.0320.0160.01641810.1250.125320.510.0630.25256/4864
YTS20.0630.0160.0631480.50.50.125320.510.0630.25256/4864
C8-30.250.1250.0631280.50.50.125160.250.540.250.016/0.3
C1-220.50.25416161320.2516128180.25128/2432
YK-30.250.1250.12521616110.256441160.25128/2432
range0.0320.0160.0161180.50.1250.125160.250.50.0320.016/0.3
|||||||||||||0.25|
20.50.25416161320.2564128116256/4864
Type strain and strains NVS-47 and PE7 were derived from blood cultures with endocarditis and the others were oral isolates from healthy volunteers. MIC: minimum inhibitory concentration, PEN: benzylpenicillin, AMP: ampicillin, AMX: amoxicillin, PIP: piperacillin, CFZ: cefazolin, CAZ: ceftazidime, CRO: ceftriaxone, CEC: cefaclor, IPM: imipenem, GEN: gentamicin, ERY: erythromycin, CIP: ciprofloxacin, MIN: minocycline, VAN: vancomycin, SXT: sulfamethoxazole-trimethoprim complex.
Table 2. MICs (µg/mL) of 15 antibiotics against Granulicatella isolates.
Table 2. MICs (µg/mL) of 15 antibiotics against Granulicatella isolates.
StrainsPENAMPAMXPIPCFZCAZCROCECIPMGENERYCIPMINVANSXT
G. adiacens
ATCC49175T0.0320.0320.0160.50.125160.250.50.016320.520.0630.5128/2432
HHC30.1250.0630.03212320.520.032320.25480.564/1216
HHP10.0630.0320.0160.250.2540.2510.016320.520.0630.5256/4864
P6-10.0630.0320.0160.250.2540.2520.016640.2510.0630.564/1216
YTC10.1250.0630.0320.51320.520.016160.520.0320.5256/4864
S961-20.0320.0320.0160.250.25420.250.016320.520.0160.532/608
S1058-20.1250.0320.0320.250.2520.2510.016320.2510.0320.532/608
TK-T10.0320.0320.0320.250.25410.50.016320.520.1250.564/1216
HKT1-40.250.1250.0630.518140.032320.520.1250.532/608
HKT2-20.1250.1250.0630.5180.2540.032320.12520.0160.2532/608
C4-30.0160.0080.0080.0630.125410.50.016160.2540.0160.5256/4864
HKT1-10.250.1250.0630.5116240.032320.12510.0160.2564/1216
NMP20.1250.1250.0630.514120.032320.2520.0320.564/1216
P7-40.50.250.1250.524440.016320.2520.0160.516/304
S49-20.0320.0320.0320.250.25480.50.016320.2520.0630.5128/2432
YTT30.0630.0320.0320.250.25640.2510.032160.2520.1250.564/1216
TK-T20.0630.0630.0630.250.516110.016320.520.1250.5256/4864
range0.0160.0080.0080.0630.12520.250.250.016160.12510.0160.2516/304
|||||||||||||||
0.50.250.1251264840.032640.5480.5256/4864
G. elegans
DSM11693T0.0160.0630.1250.1250.12520.50.50.01616810.2540.5/9.5
NMP30.0320.0320.0160.1250.2510.0080.50.016160.520.0320.51/19
S1052-10.0160.0160.0160.250.520.0080.50.03216120.0630.52/38
YTM10.0320.0320.0160.250.2510.0160.50.016160.540.0630.5512/9728
HHC50.0320.0320.0160.250.520.0320.50.03280.520.0160.52/38
C9-20.0630.0630.0630.250.510.03220.0631632420.51/19
range0.0160.0160.0160.1250.12510.080.50.01680.510.0160.50.5/9.5
|||||||||||||||
0.0630.630.1250.250.520.520.631632424512/9728
Type strains were derived from blood cultures with endocarditis and the others were oral isolates from healthy volunteers. MIC: minimum inhibitory concentration, PEN: benzylpenicillin, AMP: ampicillin, AMX: amoxicillin, PIP: piperacillin, CFZ: cefazolin, CAZ: ceftazidime, CRO: ceftriaxone, CEC: cefaclor, IPM: imipenem, GEN: gentamicin, ERY: erythromycin, CIP: ciprofloxacin, MIN: minocycline, VAN: vancomycin, SXT: sulfamethoxazole-trimethoprim complex.
Table 3. Percentage of susceptible isolates of Abiotrophia and Granulicatella against antimicrobial agents.
Table 3. Percentage of susceptible isolates of Abiotrophia and Granulicatella against antimicrobial agents.
Antimicrobial Agent% of Susceptible Isolates
A. defectivaG. adiacensG. elegans
(n = 7)(n = 17)(n = 6)
Penicillin
Benzylpenicillin57.182.4100
Ampicillin85.7100100
Amoxicillin a100100100
Piperacillin a052.9100
Cephem
Cefazolin b28.688.2100
Ceftazidime b0050
Ceftriaxone10076.4100
Cefaclor b85.752.983.3
Carbapenem
Imipenem100100100
Aminoglycoside
Gentamicin c000
Macrolide
Erythromycin14.358.80
Quinolone
Ciprofloxacin10017.616.7
Tetracycline
Minocycline d57.194.1100
Glycopeptide
Vancomycin10010083.3
Other
Sulfamethoxazole-trimethoprim e14.3016.7
Susceptibilities of the strains to the antimicrobial agents were determined according to the CLSI guideline M45-A2 for Abiotrophia spp. and Granulicatella spp. Susceptibilities to the antimicrobial agents unlisted in the guideline were determined as below; a,b Determined according to the guideline for ampicillin and cephems, respectively; c Determined according to the CLSI guideline M100-S18 for S. aureus; d Determined according to the CLSI guideline M100-S18 for tetracycline for Streptococcus spp. Viridans group; e Determined by the MIC values under 2/38 µg/mL.

Share and Cite

MDPI and ACS Style

Kanamoto, T.; Terakubo, S.; Nakashima, H. Antimicrobial Susceptibilities of Oral Isolates of Abiotrophia and Granulicatella According to the Consensus Guidelines for Fastidious Bacteria. Medicines 2018, 5, 129. https://doi.org/10.3390/medicines5040129

AMA Style

Kanamoto T, Terakubo S, Nakashima H. Antimicrobial Susceptibilities of Oral Isolates of Abiotrophia and Granulicatella According to the Consensus Guidelines for Fastidious Bacteria. Medicines. 2018; 5(4):129. https://doi.org/10.3390/medicines5040129

Chicago/Turabian Style

Kanamoto, Taisei, Shigemi Terakubo, and Hideki Nakashima. 2018. "Antimicrobial Susceptibilities of Oral Isolates of Abiotrophia and Granulicatella According to the Consensus Guidelines for Fastidious Bacteria" Medicines 5, no. 4: 129. https://doi.org/10.3390/medicines5040129

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop