ABSTRACT
The minocycline susceptibility of 3,856 isolates including Burkholderia, Achromobacter, Alcaligenes, Aeromonas, and Stenotrophomonas maltophilia from the SENTRY surveillance (2014 to 2019) were analyzed. The susceptibilities of these species (%S) were Achromobacter spp. (n = 411; 92.6%), Burkholderia cepacia species complex (n = 199; 85.9%), Aeromonas spp. (n = 127; 99.2%), Chryseobacterium spp. (n = 59; 94.9%), Alcaligenes faecalis (n = 42; 88.1%), and S. maltophilia (n = 2,287; 99.5%). These data suggest that minocycline is a useful treatment option for infections caused by unusual Gram-negative pathogens.
KEYWORDS: Achromobacter, Aeromonas, minocycline, surveillance
INTRODUCTION
Unusual Gram-negative (GN) pathogens, including Achromobacter spp., Alcaligenes spp., Aeromonas spp., Burkholderia spp., and other genera, are primarily opportunistic pathogens that can cause serious infections (1–3). Achromobacter spp., particularly A. xylosoxidans, have been isolated from cystic fibrosis (CF) patients, and the incidence has increased recently (4–6). Aeromonas spp. have been associated with necrotizing fasciitis (7, 8). Burkholderia cepacia species complex and Stenotrophomonas maltophilia have been recognized as causes of bloodstream infections and pneumonia in immunocompromised patients (9, 10). Minocycline in vitro activity has been published in recent studies on Acinetobacter baumannii-calcoaceticus species complex, B. cepacia complex, and S. maltophilia (10–13). However, recent publications with susceptibilities of the less frequently isolated GN isolates are uncommon (14). In this study, we analyzed the susceptibilities of uncommon species to minocycline and comparators.
From 2014 to 2019, 3,856 unusual GN isolates were consecutively collected from hospitalized patients as part of the global SENTRY Antimicrobial Surveillance program (15). Briefly, laboratories submitted 1 isolate per patient per infection episode. Chart reviews were not performed to determine if the isolate was a colonizer rather than a pathogen. Identifications were performed by the submitting laboratory and confirmed at JMI Laboratories with matrix-assisted laser desorption ionization-time of flight mass spectrometry (MALDI-TOF; current BioTyper Compass software version 4.1.100.1; Bruker Daltonics, Billerica, MA, USA). BioTyper software updates were applied as available from the manufacturer throughout the surveillance period.
The most common GN species, Pseudomonas aeruginosa and Acinetobacter baumannii-calcoaceticus complex, were excluded from this analysis, as the focus was on less commonly isolated species. Each genus selected for analysis had at least 10 isolates. Some genera had multiple species, each with a small number of isolates that were combined for analysis; therefore, these results should be interpreted with caution.
Isolates were tested for susceptibility to minocycline and comparators using frozen-form broth microdilution (16). CLSI M100 or M45 breakpoints were used, as appropriate (17, 18). If minocycline breakpoints were not available for an organism, CLSI breakpoints for “other non-Enterobacterales” (≤4/8/≥16 mg/liter) were applied.
Pneumonia in hospitalized patients (PIHP) was the most frequent infection from which the organisms were isolated, including Stenotrophomonas maltophilia (n = 1,586/2,285; 69.4%), Achromobacter spp. (n = 290/411; 70.6%), non-aeruginosa Pseudomonas (n = 129/340; 38.1%), and Burkholderia spp. (n = 180/243; 73.2%). Non-baumannii-calcoaceticus Acinetobacter spp. were primarily isolated from bloodstream infections (n = 179/422; 42.4%). Aeromonas spp. were primarily isolated from skin and soft tissue infections (n = 49/127; 38.6%), closely followed by bloodstream infections (n = 41/127; 32.3%). Alcaligenes faecalis was primarily isolated from skin and soft tissue infections (n = 30/42; 71.4%), while Chryseobacterium spp. and Elizabethkingia spp. were primarily isolated from PIHP (n = 39/59 [59.3%] and n = 16/23 [69.5%], respectively). Isolates were primarily from the United States (54.3%) and Europe (36.4%).
The MIC frequency distribution and MIC50/90 values of minocycline for the genera analyzed are shown in Table 1. Susceptibility for all isolates was 97.0% (3,739/3,856) and was over 90% for the genera shown, except for Alcaligenes faecalis, Burkholderia spp., and non-aeruginosa Pseudomonas spp. Minocycline susceptibility of A. faecalis was 88.1%, Burkholderia spp. was 86.8%, and B. cepacia species complex was 86.3%. The susceptibility of non-aeruginosa Pseudomonas spp. was 89.7%.
TABLE 1.
MIC distribution of minocycline tested against various unusual nonfermentative Gram-negative species with at least 10 isolates
| Organism (no. of isolates) | Minocycline MIC (mg/liter) ata: |
MIC50 (mg/liter) | MIC90 (mg/liter) | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|
| 0.06 | 0.12 | 0.25 | 0.5 | 1 | 2 | 4 | 8 | >8 | |||
| Acinetobacter non-baumannii complex. (422) | 166 (39.2) | 129 (70.0) | 80 (88.9) | 32 (96.5) | 9 (98.6) | 0 (98.6) | 1 (98.8) | 1 (99.1) | 4 (100.0) | 0.12 | 0.5 |
| Achromobacter spp. (411) | 2 (0.5) | 7 (2.2) | 21 (7.3) | 62 (22.4) | 141 (56.7) | 97 (80.3) | 51 (92.7) | 22 (98.1) | 8 (100.0) | 1 | 4 |
| Aeromonas spp. (127) | 0 (0.0) | 2 (1.6) | 10 ( | 9.4)60 (56.7) | 35 (84.3) | 16 (96.9) | 3 (99.2) | 0 (99.2) | 1 (100.0) | 0.5 | 2 |
| A. hydrophila (35) | 0 (0.0) | 1 (2.9) | 4 (14.3) | 17 (62.9) | 10 (91.4) | 2 (97.1) | 1 (100.0) | 0.5 | 1 | ||
| Alcaligenes faecalis (42) | 0 (0.0) | 1 (2.4) | 1 (4.8) | 8 (23.8) | 19 (69.0) | 8 (88.1) | 3 (95.2) | 2 (100.0) | 2 | 8 | |
| Burkholderia spp. (243) | 1 (0.4) | 1 (0.8) | 1 (1.2) | 14 (7.0) | 57 (30.5) | 89 (67.1) | 48 (86.8) | 12 (91.8) | 20 (100.0) | 2 | 8 |
| B. cepacia complex (226) | 1 (0.40) | 0 (0.40) | 1 (0.90) | 13 (6.6) | 51 (29.2) | 82 (65.5) | 47 (86.3) | 11 (91.2) | 20 (100.00) | 2 | 8 |
| Non-cepacia Burkholderia spp. (17) | 0 (0.0) | 1 (5.9) | 0 (5.9) | 1 (11.8) | 6 (47.1) | 7 (88.2) | 1 (94.1) | 1 (100.0) | 2 | 4 | |
| Chryseobacterium spp. (59) | 0 (0.0) | 1 (1.7) | 0 (1.7) | 6 (11.9) | 14 (35.6) | 21 (71.2) | 14 (94.9) | 3 (100.0) | 2 | 4 | |
| Delftia spp. (13) | 1 (7.7) | 2 (23.1) | 5 (61.5) | 5 (100.0) | 0.25 | 0.5 | |||||
| Elizabethkingia spp. (23) | 0 (0.0) | 1 (4.3) | 12 (56.5) | 8 (91.3) | 1 (95.7) | 0 (95.7) | 1 (100.0) | 0.5 | 1 | ||
| Ochrobactrum spp. (16) | 0 (0.0) | 1 (6.2) | 1 (12.5) | 8 (62.5) | 6 (100.0) | 0.5 | 1 | ||||
| Non-aeruginosa Pseudomonas spp. (340) | 0 (0.0) | 1 (0.3) | 9 (2.9) | 24 (10.0) | 76 (32.4) | 119 (67.4) | 76 (89.7) | 20 (95.6) | 15 (100.0) | 2 | 8 |
| Rhizobium spp. (15) | 3 (20.0) | 6 (60.0) | 5 (93.3) | 0 (93.3) | 1 (100.0) | 0.12 | 0.25 | ||||
| Shewanella spp. (14) | 0 (0.0) | 1 (7.1) | 6 (50.0) | 6 (92.9) | 1 (100.0) | 0.25 | 0.5 | ||||
| Sphingomonas spp. (19) | 13 (68.4) | 4 (89.5) | 0 (89.5) | 1 (94.7) | 1 (100.0) | ≤0.06 | 0.5 | ||||
| Stenotrophomonas maltophilia (2,285) | 4 (0.2) | 87 (4.0) | 491 (25.5) | 973 (68.1) | 443 (87.4) | 195 (95.9) | 81 (99.5) | 9 (99.9) | 2 (100.0) | 0.5 | 2.0 |
| Non-maltophilia Stenotrophomonas spp. (12) | 2 (16.7) | 6 (66.7) | 1 (75.0) | 3 (100.0) | 0.12 | 0.5 | |||||
CLSI (M100 or M45) minocycline susceptible breakpoint (4 mg/liter) is indicated in the column with boldfaced text.
The MIC50/90 values and susceptibilities to minocycline and comparators, including meropenem and meropenem-vaborbactam, for the largest organism groups are shown in Table 2. Minocycline had the highest susceptibility (98.8%) of the agents tested against Acinetobacter spp., followed by levofloxacin at 97.2%. Imipenem and meropenem also had 95% or greater susceptibility.
TABLE 2.
Activity of minocycline and comparator antimicrobial agents tested against uncommon Gram-negative species collected from 2014–2019
| Organism/antimicrobial | MIC50 (mg/liter) | MIC90 (mg/liter) | MIC range (mg/liter) | CLSI criteriona (%) |
||
|---|---|---|---|---|---|---|
| S | I | R | ||||
| Acinetobacter spp.b (n = 422) | ||||||
| Minocycline | 0.12 | 0.5 | ≤0.06–>8 | 98.8 | 0.2 | 0.9 |
| Meropenem-vaborbactam | 0.25 | 1 | ≤0.015–>32 | |||
| Meropenem | 0.25 | 1 | ≤0.015–>32 | 95.0 | 0.5 | 4.5 |
| Imipenem | ≤0.12 | 0.5 | ≤0.12–>8 | 95.3 | 0.2 | 4.5 |
| Piperacillin-tazobactam | ≤0.5 | 64 | ≤0.5–>64 | 88.1 | 3.1 | 8.8 |
| Tetracycline | 2 | 4 | ≤0.5–>8 | 94.1 | 2.2 | 3.6 |
| Amikacin | 1 | 4 | ≤0.25–>32 | 95.3 | 1.7 | 3.1 |
| Ceftazidime | 4 | >16 | ≤0.25–>16 | 79.5 | 8.3 | 12.3 |
| Colistin | ≤0.5 | 2 | ≤0.5–>8 | 90.5c | 9.5 | |
| Gentamicin | ≤1 | 2 | ≤1–>8 | 94.3 | 1.7 | 4 |
| Levofloxacin | ≤0.12 | 0.5 | ≤0.12–>4 | 97.2 | 0.9 | 1.9 |
| Achromobacter spp.d (n = 411) | ||||||
| Minocycline | 1 | 4 | ≤0.06–>8 | 92.7 | 5.4 | 1.9 |
| Meropenem-vaborbactam | 0.12 | 4 | 0.03–>32 | |||
| Meropenem | 0.25 | 16 | 0.03–>32 | 85.9 | 3.9 | 10.2 |
| Imipenem | 1 | 4 | 0.25–>8 | 90.3 | 4.9 | 4.9 |
| Amikacin | >32 | >32 | ≤0.25–>32 | 9.5 | 5.6 | 84.9 |
| Aztreonam | >16 | >16 | 2–>16 | 1.0 | 1.0 | 98.1 |
| Cefepime | >16 | >16 | ≤0.12–>16 | 10.7 | 27.3 | 62.0 |
| Ceftazidime | 4 | 16 | 0.25–>16 | 76.9 | 13.1 | 10.0 |
| Colistin | 1 | 4 | ≤0.5–>8 | |||
| Gentamicin | >8 | >8 | ≤0.12–>8 | 6.1 | 2.7 | 91.2 |
| Levofloxacin | 4 | >4 | ≤0.12–>4 | 36.0 | 30.7 | 33.3 |
| Piperacillin-tazobactam | ≤0.5 | 16 | ≤0.5–>64 | 92.2 | 3.6 | 4.1 |
| Tetracycline | >8 | >8 | ≤0.5–>8 | 16.7 | 3.0 | 80.3 |
| Trimethoprim-sulfamethoxazole | ≤0.5 | 4 | ≤0.5–>4 | 86.1 | 13.9 | |
| Burkholderia cepacia complex (n = 226) | ||||||
| Minocycline | 2 | 8 | ≤0.06–>8 | 86.3 | 4.9 | 8.8 |
| Meropenem-vaborbactam | 0.5 | 2 | 0.03–>32 | |||
| Meropenem | 2 | 8 | 0.03–>32 | 88.9 | 5.8 | 5.3 |
| Amikacin | >32 | >32 | ≤0.25–>32 | |||
| Cefepime | 16 | >16 | ≤0.5–>16 | |||
| Ceftazidime | 2 | 16 | 0.12–>16 | 87.1 | 5.8 | 7.1 |
| Colistin | >8 | >8 | ≤0.5–>8 | |||
| Gentamicin | >8 | >8 | ≤1–>8 | |||
| Levofloxacin | 2 | >4 | ≤0.12–>4 | 65.5 | 16.4 | 18.1 |
| Piperacillin-tazobactam | 4 | 64 | ≤0.5–>64 | |||
| Tetracycline | >8 | >8 | 1–>8 | |||
| Trimethoprim-sulfamethoxazole | ≤0.5 | 4 | ≤0.5–>4 | 89.8 | 10.2 | |
| Pseudomonas spp.e (n = 340) | ||||||
| Minocycline | 2 | 8 | 0.12–>8 | 89.7 | 5.9 | 4.4 |
| Meropenem-vaborbactam | 2 | 8 | ≤0.015–>32 | |||
| Meropenem | 2 | 8 | ≤0.015–>32 | 85.6 | 9.7 | 4.7 |
| Imipenem | 0.5 | 4 | ≤0.12–>8 | 93.8 | 3.8 | 2.4 |
| Tetracycline | 4 | 8 | ≤0.5–>8 | 78.7 | 13.4 | 7.8 |
| Amikacin | 1 | 2 | ≤0.25–>32 | 97.6 | 0.6 | 1.8 |
| Aztreonam | 16 | >16 | ≤0.12–>16 | 26.2 | 24.4 | 49.4 |
| Cefepime | 2 | 8 | ≤0.5–>16 | 92.6 | 3.2 | 4.1 |
| Ceftazidime | 2 | 8 | ≤0.25–>16 | 90.9 | 3.5 | 5.6 |
| Colistin | ≤0.5 | 2 | ≤0.5–>8 | |||
| Gentamicin | ≤1 | 2 | ≤1–>8 | 94.1 | 1.2 | 4.7 |
| Levofloxacin | 0.5 | 4 | ≤0.12–>4 | 89.1 | 2.6 | 8.2 |
| Piperacillin-tazobactam | 8 | 16 | ≤0.5–>64 | 90.6 | 7.6 | 1.8 |
| Stenotrophomonas maltophilia (n = 2,287) | ||||||
| Minocycline | 0.5 | 2 | ≤0.06–>8 | 99.5 | 0.4 | 0.1 |
| Meropenem-vaborbactam | >32 | >32 | ≤0.015–>32 | |||
| Meropenem | >32 | >32 | ≤0.015–>32 | |||
| Ceftazidime | >16 | >16 | 0.25–>16 | 24.0 | 8.8 | 67.2 |
| Colistin | 4 | >8 | ≤0.5–>8 | |||
| Gentamicin | >8 | >8 | ≤1–>8 | |||
| Levofloxacin | 1 | >4 | ≤0.12–>4 | 79.6 | 9.2 | 11.2 |
| Tetracycline | >8 | >8 | 2–>8 | |||
| Trimethoprim-sulfamethoxazole | ≤0.5 | ≤0.5 | ≤0.5–>4 | 95.0 | 5.0 | |
Criteria as published by CLSI (18).
Organisms include Acinetobacter beijerinckii (3), A. berezinae (34), A. courvalinii (6), A. guillouiae (8), A. haemolyticus (14), A. johnsonii (20), A. junii (27), A. lwoffii (78), A. nosocomialis (8), A. pittii (35), A. proteolyticus (2), A. radioresistens (49), A. schindleri (3), A. soli (10), A. towneri (2), A. ursingii (83), A. variabilis (6), A. vivianii (1), and unspeciated Acinetobacter (33).
CLSI removed the susceptible criteria for colistin; all isolates with MIC values of ≤2 mg/liter are considered colistin intermediate (18).
Organisms include Achromobacter denitrificans (12), A. insolitus (6), A. marplatensis (1), A. xylosoxidans (202), and unspeciated Achromobacter (190).
Organisms include Pseudomonas alcaligenes (3), P. alcaliphila (2), P. chlororaphis group (1), P. citronellolis (5), P. fluorescens (14), P. fluorescens group (38), P. fluorescens/putida (5), P. fulva (6), P. guariconensis (2), P. koreensis (11), P. luteola (2), P. mendocina (19), P. monteilii (5), P. mosselii (5), P. nitroreducens/multiresinivorans group (3), P. oleovorans/pseudoalcaligenes group (1), P. oryzihabitans (7), P. otitidis (6), P. peli (2), P. plecoglossicida (6), P. protegens (3), P. psychrotolerans (2), P. putida (35), P. putida group (84), P. stutzeri (32), and unspeciated Pseudomonas (41).
Minocycline and piperacillin-tazobactam had the highest susceptibilities against Achromobacter species, with 92.7% and 92.2% susceptible, respectively (Table 2). Imipenem and meropenem susceptibilities were 90.3% and 85.9%, respectively, and trimethoprim-sulfamethoxazole susceptibility was 86.1%. Achromobacter species isolates were resistant to the aminoglycosides amikacin and gentamicin and had poor susceptibility to aztreonam (1.0%), cefepime (10.7%), and levofloxacin (36.0%).
Most (93.1%) Burkholderia species isolates were B. cepacia complex (Table 2). Of the agents tested, 5 antimicrobials have CLSI breakpoints for Burkholderia spp. (17, 18). Trimethoprim-sulfamethoxazole had the highest susceptibility of 89.8%; the susceptibilities of meropenem, ceftazidime, and minocycline were 88.9%, 87.1%, and 86.3%, respectively.
Of the 340 non-aeruginosa Pseudomonas species isolates, the P. putida group (n = 84) was the most common species (Table 2). As CLSI breakpoints for P. aeruginosa are no longer applicable to non-aeruginosa species, the CLSI breakpoints for other non-Enterobacterales were applied (18). Minocycline inhibited 89.7% of isolates with a MIC value of ≤4 mg/liter. The two drugs with the highest susceptibilities were amikacin (97.6%) and gentamicin (94.1%).
Minocycline susceptibility against S. maltophilia was 99.5%, the highest of the four antimicrobials tested with CLSI breakpoints (Table 2). Trimethoprim-sulfamethoxazole susceptibility was 95.0%, levofloxacin was 79.6%, and ceftazidime was 24.0%.
Although minocycline was first introduced in 1967, its use for the treatment of infections caused by unusual GN has increased due to its potent in vitro activity, good tissue penetration, and low toxicity (19–22). In addition, the approval of an improved intravenous formulation in the United States in 2015 facilitated its use in hospitalized patients with serious infections (22–24). Combination therapy with minocycline and various antimicrobials, including colistin and cefiderocol, have also been studied, although there is no consensus about which combinations are the most useful (25–27).
Overall, minocycline susceptibility was greater than 85% for the various species tested, including 99.2% susceptibility for Aeromonas spp., 98.8% for non-baumannii Acinetobacter, 92.7% for Achromobacter spp., and 99.5% for S. maltophilia. While colistin was also active against several species, its clinical use is discouraged due to toxicity and poor efficacy (28). Trimethoprim-sulfamethoxazole also had good in vitro activity against Achromobacter spp., Burkholderia spp., and S. maltophilia. Resistance to trimethoprim-sulfamethoxazole has been reported in S. maltophilia (29, 30). In this study, 5.0% of isolates were resistant to trimethoprim-sulfamethoxazole and 92.9% of those isolates were susceptible to minocycline.
This study has several limitations: the recently approved drugs cefiderocol and eravacycline may have activity against these isolates but were not tested; most of the isolates analyzed were from the United States; there was no medical chart review, so it is unknown if any isolates were colonizers rather than pathogens; MALDI-TOF was used for isolate identification, which may not distinguish among relevant species of some analyzed genera; and no molecular characterization was performed.
The number of antimicrobials that the clinical laboratory can test against unusual GN pathogens and report interpretive criteria for is limited. This study provides useful susceptibility information for several genera that are less frequently included in publications. These in vitro data suggest that minocycline remains a useful treatment option for infections caused by unusual GN.
ACKNOWLEDGMENTS
We thank the hospitals that submit isolates to the SENTRY Antimicrobial Surveillance Program.
This study was performed by JMI Laboratories and supported by Melinta Therapeutics, Inc., which included funding for services related to preparing the manuscript.
JMI Laboratories contracted to perform services in 2020 for Affinity Biosensors, Allergan, Amicrobe, Inc., Amplyx Pharma, Artugen Therapeutics USA, Inc., Astellas, Basilea, Beth Israel Deaconess Medical Center, BIDMC, bioMérieux, Inc., BioVersys Ag, Bugworks, Cidara, Cipla, Contrafect, Cormedix, Crestone, Inc., Curza, CXC7, Entasis, Fedora Pharmaceutical, Fimbrion Therapeutics, Fox Chase, GlaxoSmithKline, Guardian Therapeutics, Hardy Diagnostics, IHMA, Janssen Research & Development, Johnson & Johnson, Kaleido Biosciences, KBP Biosciences, Luminex, Matrivax, Mayo Clinic, Medpace, Meiji Seika Pharma Co., Ltd., Melinta, Menarini, Merck, Meridian Bioscience Inc., Micromyx, MicuRx, N8 Medical, Nabriva, National Institutes of Health, National University of Singapore, North Bristol NHS Trust, Novome Biotechnologies, Paratek, Pfizer, Prokaryotics Inc., QPEX Biopharma, Rhode Island Hospital, RIHML, Roche, Roivant, Salvat, Scynexis, SeLux Diagnostics, Shionogi, Specific Diagnostics, Spero, SuperTrans Medical LT, T2 Biosystems, The University of Queensland, Thermo Fisher Scientific, Tufts Medical Center, Universite de Sherbrooke, University of Iowa, University of Iowa Hospitals and Clinics, University of Wisconsin, UNT System College of Pharmacy, URMC, UT Southwestern, VenatoRx, Viosera Therapeutics, and Wayne State University. There are no speakers’ bureaus or stock options to declare.
REFERENCES
- 1.Gabrielaite M, Bartell JA, Norskov-Lauritsen N, Pressler T, Nielsen FC, Johansen HK, Marvig RL. 2021. Transmission and antibiotic resistance of Achromobacter in cystic fibrosis. J Clin Microbiol 59:e02911-20. doi: 10.1128/JCM.02911-20. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Spencer HK, Spitznogle SL, Borjan J, Aitken SL. 2020. An overview of the treatment of less common non-lactose-fermenting Gram-negative bacteria. Pharmacotherapy 40:936–951. [DOI] [PubMed] [Google Scholar]
- 3.Isler B, Kidd TJ, Stewart AG, Harris P, Paterson DL. 2020. Achromobacter infections and treatment options. Antimicrob Agents Chemother 64:e01025-20. doi: 10.1128/AAC.01025-20. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Ridderberg W, Bendstrup KE, Olesen HV, Jensen-Fangel S, Norskov-Lauritsen N. 2011. Marked increase in incidence of Achromobacter xylosoxidans infections caused by sporadic acquisition from the environment. J Cyst Fibros 10:466–469. doi: 10.1016/j.jcf.2011.07.004. [DOI] [PubMed] [Google Scholar]
- 5.Coward A, Kenna DTD, Woodford N, Turton JF, UK CF Surveillance Working Group. 2020. Structured surveillance of Achromobacter, Pandoraea, and Ralstonia species from patients in England with cystic fibrosis. J Cyst Fibros 19:388–393. doi: 10.1016/j.jcf.2019.11.005. [DOI] [PubMed] [Google Scholar]
- 6.Marion-Sanchez K, Pailla K, Olive C, Le Coutour X, Derancourt C. 2019. Achromobacter spp. healthcare associated infections in the French West Indies: a longitudinal study from 2006 to 2016. BMC Infect Dis 19:795. doi: 10.1186/s12879-019-4431-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Hutchinson LE, Franke JD, Mailey BA. 2021. Necrotizing fasciitis secondary to lake water inoculation with Aeromonas sobria: a case report. Medicine (Baltimore, MD) 100:e24981. doi: 10.1097/MD.0000000000024981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Huang TY, Peng KT, Hsu WH, Hung CH, Chuang FY, Tsai YH. 2020. Independent predictors of mortality for aeromonas necrotizing fasciitis of limbs: an 18-year retrospective study. Sci Rep 10:7716. doi: 10.1038/s41598-020-64741-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.El Chakhtoura NG, Saade E, Wilson BM, Perez F, Papp-Wallace KM, Bonomo RA. 2017. A 17-year nationwide study of Burkholderia cepacia complex bloodstream infections among patients in the United States Veterans Health Administration. Clin Infect Dis 65:1253–1259. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Gales AC, Seifert H, Gur D, Castanheira M, Jones RN, Sader HS. 2019. Antimicrobial susceptibility of Acinetobacter calcoaceticus-Acinetobacter baumannii complex and Stenotrophomonas maltophilia clinical isolates: results from the SENTRY Antimicrobial Surveillance Program (1997–2016). Open Forum Infect Dis 6:S34–S46. doi: 10.1093/ofid/ofy293. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Flamm RK, Shortridge D, Castanheira M, Sader HS, Pfaller MA. 2019. In vitro activity of minocycline against U.S. isolates of Acinetobacter baumannii-Acinetobacter calcoaceticus species complex, Stenotrophomonas maltophilia, and Burkholderia cepacia complex: results from the SENTRY Antimicrobial Surveillance Program, 2014 to 2018. Antimicrob Agents Chemother 63:e01154-19. doi: 10.1128/AAC.01154-19. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Sader HS, Duncan LR, Arends SJR, Carvalhaes CG, Castanheira M. 2020. Antimicrobial activity of aztreonam-avibactam and comparator agents when tested against a large collection of contemporary Stenotrophomonas maltophilia isolates from medical centers worldwide. Antimicrob Agents Chemother 64:e01433-20. doi: 10.1128/AAC.01433-20. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Castanheira M, Mendes RE, Jones RN. 2014. Update on Acinetobacter species: mechanisms of antimicrobial resistance and contemporary in vitro activity of minocycline and other treatment options. Clin Infect Dis 59(Suppl 6):S367–S373. doi: 10.1093/cid/ciu706. [DOI] [PubMed] [Google Scholar]
- 14.Sader HS, Jones RN. 2005. Antimicrobial susceptibility of uncommonly isolated non-enteric Gram-negative bacilli. Int J Antimicrob Agents 25:95–109. doi: 10.1016/j.ijantimicag.2004.10.002. [DOI] [PubMed] [Google Scholar]
- 15.Fuhrmeister AS, Jones RN. 2019. The importance of antimicrobial resistance monitoring worldwide and the origins of SENTRY Antimicrobial Surveillance Program. Open Forum Infect Dis 6:S1–S4. doi: 10.1093/ofid/ofy346. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.CLSI. 2018. Methods for dilution antimicrobial susceptibility testing for bacteria that grow aerobically. M07, 11th ed. Clinical and Laboratory Standards Institute, Wayne, PA. [Google Scholar]
- 17.CLSI. 2015. Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria. M45, 3rd ed. Clinical and Laboratory Standards Institute, Wayne, PA. [DOI] [PubMed] [Google Scholar]
- 18.CLSI. 2020. Performance standards for antimicrobial susceptibility testing. M100, 30th ed. Clinical and Laboratory Standards Institute, Wayne, PA. [Google Scholar]
- 19.Bishburg E, Bishburg K. 2009. Minocycline–an old drug for a new century: emphasis on methicillin-resistant Staphylococcus aureus (MRSA) and Acinetobacter baumannii. Int J Antimicrob Agents 34:395–401. doi: 10.1016/j.ijantimicag.2009.06.021. [DOI] [PubMed] [Google Scholar]
- 20.Fragkou PC, Poulakou G, Blizou A, Blizou M, Rapti V, Karageorgopoulos DE, Koulenti D, Papadopoulos A, Matthaiou DK, Tsiodras S. 2019. The role of minocycline in the treatment of nosocomial infections caused by multidrug, extensively drug and pandrug resistant Acinetobacter baumannii: a systematic review of clinical evidence. Microorganisms 7:e7060159. doi: 10.3390/microorganisms7060159. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Jonas M, Cunha BA. 1982. Minocycline. Ther Drug Monit 4:137–145. [PubMed] [Google Scholar]
- 22.Colton B, McConeghy KW, Schreckenberger PC, Danziger LH. 2016. I.V. minocycline revisited for infections caused by multidrug-resistant organisms. Am J Health Syst Pharm 73:279–285. doi: 10.2146/ajhp150290. [DOI] [PubMed] [Google Scholar]
- 23.Ritchie DJ, Garavaglia-Wilson A. 2014. A review of intravenous minocycline for treatment of multidrug-resistant Acinetobacter infections. Clin Infect Dis 59(Suppl 6):S374–S380. doi: 10.1093/cid/ciu613. [DOI] [PubMed] [Google Scholar]
- 24.The Medicines Company. 2015. Minocin, minocycline for injection, prescribing information. The Medicines Company, Parsippany-Troy Hills, NJ. [Google Scholar]
- 25.Abbott IJ, Peleg AY. 2015. Stenotrophomonas, Achromobacter, and nonmelioid Burkholderia species: antimicrobial resistance and therapeutic strategies. Semin Respir Crit Care Med 36:99–110. doi: 10.1055/s-0034-1396929. [DOI] [PubMed] [Google Scholar]
- 26.Seok H, Choi WS, Lee S, Moon C, Park DW, Song JY, Cheong HJ, Kim J, Kim JY, Park MN, Kim YR, Lee HJ, Kim B, Pai H, Jo YM, Kim JH, Sohn JW. 2021. What is the optimal antibiotic treatment strategy for carbapenem-resistant Acinetobacter baumannii (CRAB)? A multicentre study in Korea. J Glob Antimicrob Resist 24:429–439. doi: 10.1016/j.jgar.2021.01.018. [DOI] [PubMed] [Google Scholar]
- 27.Biagi M, Vialichka A, Jurkovic M, Wu T, Shajee A, Lee M, Patel S, Mendes RE, Wenzler E. 2020. Activity of cefiderocol alone and in combination with levofloxacin, minocycline, polymyxin B, or trimethoprim-sulfamethoxazole against multidrug-resistant Stenotrophomonas maltophilia. Antimicrob Agents Chemother 64:e00559-20. doi: 10.1128/AAC.00559-20. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Satlin MJ, Lewis JS, Weinstein MP, Patel J, Humphries RM, Kahlmeter G, Giske CG, Turnidge J. 2020. Clinical and Laboratory Standards Institute (CLSI) and European Committee on Antimicrobial Susceptibility Testing (EUCAST) position statements on polymyxin B and colistin clinical breakpoints. Clin Infect Dis 71:e523–e529. [DOI] [PubMed] [Google Scholar]
- 29.Hand E, Davis H, Kim T, Duhon B. 2016. Monotherapy with minocycline or trimethoprim/sulfamethoxazole for treatment of Stenotrophomonas maltophilia infections. J Antimicrob Chemother 71:1071–1075. doi: 10.1093/jac/dkv456. [DOI] [PubMed] [Google Scholar]
- 30.Mendes ET, Paez JIG, Ferraz JR, Marchi AP, Silva I, Batista MV, Lima ALM, Rossi F, Levin AS, Costa SF. 2020. Clinical and microbiological characteristics of patients colonized or infected by Stenotrophomonas maltophilia: is resistance to sulfamethoxazole/trimethoprim a problem? Rev Inst Med Trop Sao Paulo 62:e96. doi: 10.1590/S1678-9946202062096. [DOI] [PMC free article] [PubMed] [Google Scholar]