Trends and Impact in Antimicrobial Resistance Among Bacteroides and Parabacteroides Species in 2007–2012 Compared to 2013

Abstract

Purpose:

The aim of this study was to analyze the susceptibility of Bacteroides and Parabacteroides spp. strains, isolated from patients hospitalized in the clinical hospital in Poland to penicillin, amoxicillin with clavulanic acid, imipenem, clindamycin, and metronidazole.

Methods:

We analyzed susceptibility of 476 isolates to routinely use for the treatment of anaerobic bacterial infections antibiotics. E test method was used to determining the minimal inhibitory concentration values. To show the trend of drug resistance, we compared data from two periods within the years 2003–2017.

Results:

Research results indicate that the problem of resistance is mainly related to strains belonging to non-fragilis Bacteroides. In the analyzed periods, there was an increase in the percentage of clindamycin-resistant isolates (35.21% vs. 53.33%), amoxicillin/clavulanic acid (2.83% vs. 8.15%), and imipenem (1.41% vs. 3.7%). In isolates belonging to Parabacteroides distasonis, we observed a constant high (∼50%) percentage of clindamycin-resistant strains. The overwhelming majority of B. fragilis strains were resistant to penicillin (>95%) and about 20% of the isolates were not susceptible to clindamycin.

Conclusions:

Clindamycin, due to the high and increasing percentage of resistant strains, may not be a good choice in the empirical therapy of infections caused by Bacteroides and P. distasonis. Our study highlighted the importance of a routine or at least periodic monitoring of antimicrobial susceptibility of anaerobic Gram-negative bacilli, providing important information for appropriate therapy. The study shows that infection caused (or suspected of being caused) by Bacteroides and Parabacteroides spp. can be empirically treated with metronidazole or imipenem.

Introduction

Obligate anaerobic bacteria are an integral component of the human microbiome. Many of these microorganisms are opportunistic pathogens responsible for endogenous and mixed infections (together with aerobic microflora). Anaerobic Gram-negative bacilli (AGNB) can be isolated from a variety of clinical specimens and are responsible for the occurrence of, for example, brain, head, and neck abscesses, intra-abdominal abscesses, gynecological infections, skin and soft tissue infections, and bacteremia.^1–4 Bacteroides and Parabacteroides spp. are the most clinically significant Gram-negative bacilli. They are characterized by the highest antibiotic resistance among anaerobes, visibly increasing for more than two decades.

In recent years multidrug-resistant strains, that is, those not susceptible to metronidazole, clindamycin, and carbapenems are increasingly isolated.^5–7

In the treatment of AGNB infections, antibiotic selection is based on documented findings indicating the effectiveness of a particular treatment (empirical treatment). Therefore, therapy should be implemented on the basis of clinical evaluation of the course of infection and the pattern of resistance to antibacterial drugs in the hospital and/or ward and corrected based on the antibiogram. It is, however, advisable to routinely or periodically monitor drug susceptibility and use targeted therapy based on the result of the antibiogram.^8,9 Metronidazole, clindamycin, and some β-lactam antibiotics (mainly carbapenems and β-lactams with β-lactamase inhibitor) are most commonly used to treat infections with Bacteroides and Parabacteroides spp. etiology in Poland.¹⁰ In addition, cephamycin and IV generation fluoroquinolones are also used in the treatment.^11,12

The aim of the study was to analyze the susceptibility of Bacteroides and Parabacteroides spp. strains isolated from clinical specimens to penicillin, amoxicillin with clavulanic acid, imipenem, clindamycin, and metronidazole.

Materials and Methods

Bacteroides and Parabacteroides spp. isolates obtained from patients hospitalized in one of the large clinical hospital in Poland were analyzed. The drug susceptibility of isolates was assessed in two studies, covering the periods: 2007–2012 (study I) and 2013–2017 (study II). In study I, we examined 200 clinical isolates (not duplicated) representing the Bacteroides fragilis group (BFG) (182): B. fragilis (111), B. thetaiotaomicron (38), B. ovatus (12), B. vulgatus (11), B. uniformis (7), B. stercoris (2), B. caccae (1), and belonging to the genus Parabacteroides—Parabacteroides distasonis (18). In study II, 276 clinical isolates (not duplicated) were analyzed, representing the BFG (250): B. fragilis (115), B. thetaiotaomicron (53), B. vulgatus (30) B. ovatus (22), B. ovatus/xylanisolvens (12), B. uniformis (11), B. pyogenes (3), B. stercoris (2), B. caccae (1), B. eggerthii (1), and P. distasonis (26). Tested strains were cultured from the following materials: swabs from wounds/abscesses, abdominal fluids, soft tissue fragments, and blood.

Clinical sample was plated on Schaedler Agar media with 5% sheep blood, vitamin K, and hemin (bioMérieux, France), and was incubated at 37°C in an anaerostat Genbox System (bioMérieux) providing air composition: 85% N₂, 10% H₂, and 5% CO₂. Incubation period lasted 48 hours. Bacterial identification was carried out using the matrix-assisted laser desorption ionization time-of-flight mass spectrometry method (bioMérieux). Drug susceptibility assessment was performed using the E test method (bioMérieux). Minimal inhibitory concentration (MIC) was determined using strips impregnated with a concentration gradient of benzylpenicillin (0.016–256 mg/L), amoxicillin with clavulanic acid (0.016–256 mg/L), imipenem (0.002–32 and 0.016–256 mg/L), clindamycin (0.016–256 mg/L), and metronidazole (0.016–256 mg/L). The interpretation was conducted in accordance with The European Committee on Antimicrobial Susceptibility Testing (EUCAST Version 10.0) recommendations.¹³ MIC₉₀ and MIC₅₀ values were defined as the lowest concentration of the antibiotic at which 90% and 50% of the isolates were inhibited, respectively. The strains from the American Type Culture Collection: Bacteroides fragilis ATCC 25285 and Bacteroides thetaiotaomicron ATCC 29741 were used as controls in all tests. The MICs for the two control strains were always within recommended limits.

Results

Antimicrobial susceptibility of clinical isolates of Bacteroides and Parabacteroides isolated from January 2007 to December 2012 is shown in Table 1. Of 200 strains tested, 98.5% showed penicillin resistance. Only three B. vulgatus isolates were susceptible to this antibiotic (MIC = 0.25 mg/L). Most of the tested strains were susceptible to other β-lactam antibiotics. Merely two B. thetaiotaomicron isolates were resistant to imipenem (MIC = 32 mg/L). Resistance to amoxicillin/clavulanic acid was observed in P. distasonis, B. thetaiotaomicron, and B. ovatus. All strains tested were susceptible to metronidazole. Although one B. thetaiotaomicron isolate had a metronidazole MIC of 4 mg/L (clinical breakpoint MIC ≤4 mg/L). Clindamycin resistance was found in 31% of all tested strains. Most common in species other than B. fragilis (non-fragilis Bacteroides [NFB]). It should be added that clindamycin resistance in Bacteroides and Parabacteroides strains isolated in the study period in our hospital increased by 20%, and the percentage of strains resistant to this antibiotic in subsequent years was as follows: 2007, 20%; 2008, 27%; 2009, 34.6%; 2010, 15.4%; 2011, 25%; 2012, 40%.

Table 1.

Activity of Antimicrobial Agents Against Bacteroides spp. and Parabacteroides distasonis in 2007–2012

Species (n)	Antibiotics	Range MIC (mg/L)	MIC₅₀	MIC₉₀	% Resistant
All isolates (n = 200)	Amoxicillin/clavulanic acid	0.016–256	0.25	2	5.5
	Penicillin	0.25–256	8	256	98.5
	Imipenem	0.006–32	0.064	0.5	0.5
	Clindamycin	0.016–256	1.5	256	31.0
	Metronidazole	0.016–4	0.125	0.25	0
Bacteroides fragilis (111)	Amoxicillin/clavulanic acid	0.016–256	0.19	1	1.8
	Penicillin	0.75–256	6	256	100.0
	Imipenem	0.006–1	0.032	0.125	0
	Clindamycin	0.016–256	0.5	256	22.5
	Metronidazole	0.094–0.47	0.023	0.19	0
Bacteroides thetaiotaomicron (38)	Amoxicillin/clavulanic acid	0.032–32	0.094	0.75	2.6
	Penicillin	2–256	12	256	100.0
	Imipenem	0.032–32	0.094	0.75	2.6
	Clindamycin	0.25–256	2	256	26.3
	Metronidazole	0.016–4	0.125	0.38	0
Bacteroides vulgatus (11)	Amoxicillin/clavulanic acid	0.094–2	0.25	1	0
	Penicillin	0.25–256	6	256	72.7
	Imipenem	0.016–0.94	0.047	0.25	0
	Clindamycin	0.016–256	0.5	256	27.2
	Metronidazole	0.016–0.19	0.064	0.125	0
Parabacteroides distasonis (18)	Amoxicillin/clavulanic acid	0.016–24	1.5	16	22.2
	Penicillin	3–256	32	256	100.0
	Imipenem	0.19–1	0.5	1	0
	Clindamycin	0.75–256	4	256	50.0
	Metronidazole	0.016–0.19	0.094	0.125	0
Bacteroides ovatus (12)	Amoxicillin/clavulanic acid	0.094–16	0.25	4	8.3
	Penicillin	1.5–256	24	256	100.0
	Imipenem	0.064–0.5	0.094	0.38	0
	Clindamycin	0.125–256	256	256	50.0
	Metronidazole	0.016–0.5	0.25	0.38	0
Other species^a	Amoxicillin/clavulanic acid	0.125–4	0.75	4	0
	Penicillin	4–256	256	256	100.0
	Imipenem	0.016–0.5	0.19	0.38	0
	Clindamycin	0.016–256	256	256	60
	Metronidazole	0.032–0.125	0.047	0.094	0.0

Bacteroides uniformis (7), Bacteroides stercoris (2), and Bacteroides caccae (1).

MIC, minimal inhibitory concentration.

Activity of antimicrobial agents against Bacteroides spp. and P. distasonis isolated in the period from January 2013 to December 2017 is shown in Table 2. Resistance to penicillin was detected in 96.0% strains. Analyzing the remaining β-lactam antibiotics, it was found that one B. fragilis isolate (MIC = 32 mg/L), three B. thetaiotaomicron isolates (MIC = 12 mg/L, MIC = 6 mg/L, MIC = 6 mg/L), one B. vulgatus isolate (MIC = 32 mg/L), and one B. uniformis isolate (MIC = 32 mg/L) were imipenem resistant. In 2017, a significant increase in resistance was observed compared with previous years. About 8% of strains resistant to this antibiotic were isolated. Of all strains tested, 7.6% were resistant to amoxicillin with clavulanic acid. In 2016 and 2017, significantly fewer strains resistant to amoxicillin with clavulanic acid (1.6% and 3.5%, respectively) were cultured compared with 2013, 2014, and 2015 (14.3%, 7.7%, and 12.8%, respectively). As in study I, all strains tested were susceptible to metronidazole. Metronidazole MIC values for isolated strains were ≤0.75 mg/L. Overall 38.8% of clindamycin-resistant strains were isolated (53.8% P. distasonis, 37.2% belonged to BFG). The frequency of isolation of clindamycin-resistant strains varied in subsequent years. The percentage of resistant strains in 2013–2017 was 37.5%, 21.1%, 42.5%, 53.1%, and 36.8%, respectively.

Table 2.

Activity of Antimicrobial Agents Against Bacteroides spp. and Parabacteroides distasonis in 2013–2017

Species (n)	Antibiotics	Range MIC (mg/L)	MIC₅₀	MIC₉₀	% Resistant
All isolates (n = 276)	Amoxicillin/clavulanic acid	0.016–256	0.38	8	7.6
	Penicillin	0.016–256	16	256	96.0
	Imipenem	0.002–256	0.094	0.75	2.1
	Clindamycin	0.016–256	1.5	256	38.8
	Metronidazole	0.016–0.75	0.125	0.25	0
Bacteroides fragilis (115)	Amoxicillin/clavulanic acid	0.016–256	0.25	1	1.7
	Penicillin	0.016–256	8	256	95.6
	Imipenem	0.008–256	0.047	0.125	0.9
	Clindamycin	0.016–256	0.5	256	18.3
	Metronidazole	0.016–0.38	0.19	0.25	0
Bacteroides thetaiotaomicron (53)	Amoxicillin/clavulanic acid	0.125–32	0.5	8	7.5
	Penicillin	0.5–256	32	256	100.0
	Pmipenem	0.064–12	0.125	1	5.7
	Clindamycin	0.094–256	24	256	50.9
	Metronidazole	0.016–0.5	0.125	0.25	0
Bacteroides vulgatus (30)	Amoxicillin/clavulanic acid	0.016–24	1	3	6.7
	Penicillin	0.125–256	256	256	96.7
	Imipenem	0.006–32	0.125	0.75	3.3
	Clindamycin	0.016–256	256	256	53.3
	Metronidazole	0.016–0.38	0.064	0.19	0
Parabacteroides distasonis (27)	Amoxicillin/clavulanic acid	0.38–64	2	32	30.8
	Penicillin	0.75–256	256	256	100.0
	Imipenem	0.002–4	0.5	1	0
	Clindamycin	0.016–256	256	256	53.8
	Metronidazole	0.016–0.38	0.125	0.25	0
Bacteroides ovatus (22)	Amoxicillin/clavulanic acid	0.047–16	0.038	12	18.2
	Penicillin	1–256	256	256	100.0
	Imipenem	0.064–0.75	0.125	0.5	0
	Clindamycin	0.125–256	256	256	50.0
	Metronidazole	0.016–0.5	0.25	0.38	0
Bacteroides ovatus/xylanisolvens (12)	Amoxicillin/clavulanic acid	0.016–6	0.5	6	0
	Penicillin	0.016–256	12	256	91.7
	Imipenem	0.012–3	0.125	0.38	0
	Clindamycin	1–256	256	256	58.3
	Metronidazole	0.047–0.25	0.125	0.25	0
Bacteroides uniformis (11)	Amoxicillin/clavulanic acid	0.19–24	0.38	4	9.1
	Penicillin	0.016–256	32	256	81.8
	Imipenem	0.25–32	0.19	2	9.1
	Clindamycin	0.25–256	256	256	63.6
	Metronidazole	0.016–0.38	0.047	0.064	0
Other species^a	Amoxicillin/clavulanic acid	0.016–1.0	0.19	1.0	0
	Penicillin	0.016–256	256	256	71.4
	Imipenem	0.002–1.5	0.064	1.5	0.0
	Clindamycin	0.125–256	256	256	57.1
	Metronidazole	0.016–0.075	0.047	0.75	0

Bacteroides pyogenes (3), Bacteroides stercoris (2), Bacteroides caccae (1), and Bacteroides eggerthii (1).

Table 3 compares isolation frequency of B. fragilis, P. distasonis, and NFB strains for selected antibiotics of both periods, that is, 2007–2012 and 2013–2017.

Table 3.

Comparison of Antimicrobial Susceptibilities for Two Time Periods, 2007–2012 and 2013–2017

Species/group	Bacteroides fragilis		Non-fragilis Bacteroides [NFB]		Parabacteroides distasonis
Period	2007–2012	2013–2017	2007–2012	2013–2017	2007–2012	2013–2017
Number of strains (n)	111	115	71	135	18	26

Antibiotic	% Resistant
Amoxicillin/clavulanic acid	1.8	1.74	2.82	8.15	22.22	30.77
Penicillin	100	95.65	95.77	95.56	100	100
Imipenem	0	0.87	1.41	3.70	0	0
Clindamycin	22.52	18.26	35.21	53.33	50.0	53.85
Metronidazole	0	0	0	0	0	0

The presented data show that the resistance problem mainly concerns NFB strains. In the analyzed periods, an increase in the percentage of isolates resistant to clindamycin (35.2% vs. 53.3%), amoxicillin with clavulanic acid (2.8% vs. 8.1%) and imipenem (1.4% vs. 3.7%) was recorded. Isolates belonging to P. distasonis exhibited a constant high (∼50%) percentage of clindamycin-resistant strains.

Discussion

Diagnostics of anaerobic bacterial infections and determination of drug susceptibility are technically difficult and time-consuming; therefore, the number of studies on AGNB is significantly limited, especially in Europe. Most laboratories usually reserve such analyses for cases where an anaerobic isolate is the predominant pathogen or is isolated from sites that are normally sterile.^5,8,14 Accordingly, the anaerobic treatment of infections based on the published patterns of susceptibility is a common practice.¹⁵ Our results, the first in Poland, the 11-year monitoring period for drug resistance in Bacteroides spp. and P. distasonis, can complement information from other microbiological clinical laboratories. One of the largest multicenter studies conducted by Nagy et al.¹⁶ evaluated the susceptibility of 824 isolates belonging to the BFG, originating in 13 European countries from the period 2008–2009. These data were compared with the results obtained in Europe 10 (1999–2001)¹⁷ and ∼20 years (1988–1989)¹⁸ earlier. Nagy et al. showed that 98.2% of BFG isolates were resistant to ampicillin.¹⁶ Hedberg et al.¹⁷ and Phillips et al.¹⁸ reported similarly high percentages of ampicillin-resistant strains. In this study, we examined penicillin susceptibility. On the basis of this assay, susceptibility to ampicillin as well as to amoxicillin and piperacillin can be predicted in accordance with EUCAST recommendations.¹³ In study I and II, very high percentages of penicillin-resistant B. fragilis and NFB strains were found. All P. distasonis strains were resistant to penicillin. Penicillin with the addition of β-lactamase inhibitor exhibits definitely better activity against anaerobic bacteria. Studies published by Nagy et al.¹⁶ showed that 8.7% of B. fragilis strains and 10.4% of BFG were resistant to amoxicillin with clavulanic acid. The frequency of resistance to this antibiotic was higher in NFB strains (12–30% depending on the species). It has been found that the percentage of strains resistant to this antibiotic has increased compared with previous studies.¹⁶ Resistance in NFB species increased almost threefold between the periods studied. However, the highest percentage of resistant strains occurred in P. distasonis. In a study on 283 clinical isolates of the genus Bacteroides, Veloo and van Winkelhoff showed that nearly 97% of BFG strains were resistant to ampicillin, whereas >96% of strains were susceptible to amoxicillin with clavulanic acid.¹⁴ The resistance mechanisms to β-lactam antibiotics combined with β-lactamase inhibitors are insufficiently understood, but the fact is that the resistance of Bacteroides spp. strains isolated from infections in both the United States (resistance to piperacillin with tazobactam ∼1% in 1997–2007) and in Europe (resistance to piperacillin with tazobactam ∼10% in 2008/2009) is steadily increasing probably due to the widespread use of these antibiotics.^{1,15,16,19,20}

Imipenem resistance has not changed dramatically in Europe or the United States for the past 20 years.^1,16,20 Nagy et al.¹⁶ showed that in the compared periods, the percentage of Bacteroides strains resistant to this antibiotic was 0%, <1%, and 1.2%, respectively. In this study, 0.5% of strains isolated in 2007–2012 and 2.17% of isolates from 2013 to 2017 were imipenem resistant. In NFB, we observed more than a 2.5-fold increase (1.4% vs. 3.7%) in the percentage of resistant strains. Nagy et al.¹⁶ noticed a dramatic increase in Bacteroides spp. resistance to clindamycin during the analyzed 20 years, as well. Among the isolates from 2008/2009, 32.4% of Bacteroides spp. strains, 28.5% of B. fragilis, 60% of B. uniformis and 47.6% of B. vulgatus were resistant to clindamycin.¹⁶ Our research showed resistance in 31% (study I) and 38.8% (study II) of all isolates in the examined group. The percentage of resistant strains in individual years ranged from 20% to 53.13% and was particularly high in P. distasonis species. A similar trend was observed by researchers from the Netherlands. Resistance of BFG bacteria to clindamycin has been demonstrated in 14%, 27%, and 21% of strains isolated from 2011 to 2013.¹⁴ Multicenter studies in Belgium also demonstrated increase in the resistance during the 25-year (1987–2012) monitoring period (12% in 1987; 42% in 2011/2012).² Therefore, the use of clindamycin in infections with suspected involvement of AGNB may be associated with a lack of therapeutic success.^1,2,10,21,22 All strains tested in our laboratory were susceptible to metronidazole. Other researchers have observed a relatively low, but in some centers, constant and geographically diverse increase in the prevalence of metronidazole-resistant Bacteroides strains.^1,14,16 Published studies showed that the resistance of Bacteroides isolates to metronidazole in most parts of the world was <3%. A higher percentage was recorded in Spain (4.8%), South Africa (8.7%), and Pakistan (16%).¹¹

The main conclusions from the study are a high percentage of the tested Bacteroides and Parabacteroides strains remained susceptible to metronidazole and β-lactam antibiotics such as amoxicillin with clavulanic acid or imipenem and the use of clindamycin in empirical treatment may cause failure in therapy.

Footnotes

Ethical Statement

Bacterial isolates were collected as part of routine hospitals surveillance. Ethical approval and informed consent were not required.

Authors' Contributions

M.K. and A.M. performed the collection of clinical specimens, isolation of strains, identification and drug susceptibility testing, literature review, and cowriting of the article. M.K. was responsible for biological materials, design of methodology, analysis and interpretation of data. A.M. constructed an idea for research. G.M. supervised the project, organized the execution of the study, and critical review. M.K., A.M., and GM were responsible for discussing the results and contribution to the final article.

Disclosure Statement

No competing financial interests exist.

Funding Information

This work was supported by Medical University of Warsaw.

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Trends and Impact in Antimicrobial Resistance Among Bacteroides and Parabacteroides Species in 2007–2012 Compared to 2013–2017

Abstract

Purpose:

Methods:

Results:

Conclusions:

Introduction

Materials and Methods

Results

Discussion

Footnotes

Ethical Statement

Authors' Contributions

Disclosure Statement

Funding Information

References