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Determination of Susceptibility Breakpoint for Cefquinome Against Streptococcus Suis in Pigs

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Determination of Susceptibility Breakpoint for Cefquinome Against Streptococcus Suis in Pigs antibiotics Article Determination of Susceptibility Breakpoint for Cefquinome against Streptococcus suis in Pigs Kun Mi 1 , Mei Li 1, Lei Sun 1, Yixuan Hou 2, Kaixiang Zhou 2, Haihong Hao 1 , Yuanhu Pan 2, Zhenli Liu 1,2, Changqing Xie 1,2 and Lingli Huang 1,2,* 1 National Reference Laboratory of Veterinary Drug Residues (HZAU) and MAO Key Laboratory for Detection of Veterinary Drug Residues, Huazhong Agricultural University, Wuhan 430070, China; [email protected] (K.M.); [email protected] (M.L.); [email protected] (L.S.); [email protected] (H.H.); [email protected] (Z.L.); [email protected] (C.X.) 2 MOA Laboratory for Risk Assessment of Quality and Safety of Livestock and Poultry Products, Huazhong Agricultural University, Wuhan 430070, China; [email protected] (Y.H.); fl[email protected] (K.Z.); [email protected] (Y.P.) * Correspondence: [email protected] Abstract: Streptococcus suis (S. suis), a zoonotic pathogen, causes severe diseases in both pigs and human beings. Cefquinome can display excellent antibacterial activity against gram-negative and gram-positive bacteria. The aim of this study was to derive an optimal dosage of cefquinome against S. suis with a pharmacokinetic/pharmacodynamic (PK/PD) integration model in the target infection site and to investigate the cutoffs monitoring the changes of resistance. The minimum inhibitory concentration (MIC) distribution of cefquinome against 342 S. suis strains was determined. Citation: Mi, K.; Li, M.; Sun, L.; Hou, MIC50 and MIC90 were 0.06 and 0.25 µg/mL, respectively. The wild-type cutoff was calculated Y.; Zhou, K.; Hao, H.; Pan, Y.; Liu, Z.; as 1 µg/mL. A two-compartmental model was applied to calculate the main pharmacokinetic Xie, C.; Huang, L. Determination of parameters after 2 mg/kg cefquinome administered intramuscularly. An optimized dosage regimen Susceptibility Breakpoint for of 3.08 mg/kg for 2-log10 CFU reduction was proposed by ex vivo PK/PD model of infected swine. Cefquinome against Streptococcus suis The pharmacokinetic-pharmacodynamic cutoff was calculated as 0.06 µg/mL based on PK/PD in Pigs. Antibiotics 2021, 10, 958. targets. Based on the clinical effectiveness study of pathogenic MIC isolates, the clinical cutoff was https://doi.org/10.3390/antibiotics µ µ 10080958 calculated as 0.5 g/mL. A clinical breakpoint was proposed as 1 g/mL. In conclusion, the results offer a reference for determining susceptibility breakpoint of cefquinome against S. suis and avoiding Academic Editor: Anthony William resistance emergence by following the optimal dosage regimen. Coleman Keywords: cefquinome; Streptococcus suis; clinical breakpoint; epidemiological cutoff; PD cutoff; Received: 6 July 2021 clinical cutoff; dosage regimen; PK/PD model Accepted: 3 August 2021 Published: 9 August 2021 Publisher’s Note: MDPI stays neutral 1. Introduction with regard to jurisdictional claims in Streptococcus suis (S. suis) is a gram-positive facultative anaerobe and increasingly published maps and institutional affil- emerging zoonotic infection with a global distribution [1]. Among the 35 serotypes (1/2, iations. 1–34) of S. suis classified by different capsule antigens, pathogenicity has been reported for serotype 7 strains isolated from diseased animals and humans [2]. Increasing emergence and dissemination of resistance has been reported in recent years, mainly caused by exposure to antibacterial abuse and misuse. Copyright: © 2021 by the authors. Cefquinome is a fourth-generation cephalosporin developed exclusively for veterinary Licensee MDPI, Basel, Switzerland. use in the clinic [3]. Due to its structure characteristic (Figure1), cefquinome displays This article is an open access article outstanding stability for beta-lactamase and exerts excellent antibacterial activity against distributed under the terms and gram-positive and gram-negative bacteria in vitro or in vivo antibacterial activity [4]. It has conditions of the Creative Commons been approved for the treatment of respiratory tract infections with a dosage of 2 mg/kg Attribution (CC BY) license (https:// by the European Medicines Agency (EMA) [5]. creativecommons.org/licenses/by/ 4.0/). Antibiotics 2021, 10, 958. https://doi.org/10.3390/antibiotics10080958 https://www.mdpi.com/journal/antibiotics AntibioticsAntibiotics2021 2021,,10 10,, 958 x FOR PEER REVIEW 22 of 1314 FigureFigure 1.1. Chemical structure ofof cefquinome.cefquinome. TheThe susceptibilitysusceptibility breakpointbreakpoint (SBPT) (SBPT) is is useful useful to to determine determine the the susceptibility susceptibility or or resis- re- tancesistance of aof bacterium a bacterium to to an an antibiotic antibiotic and and to to define define the the effect, effect, or or inappropriate inappropriate antibioticantibiotic treatments,treatments, on bacterial infections. infections. The The setting setting breakpoint breakpoint is iscomposed composed of ofthree three parts: parts: in invitro vitro susceptibisusceptibility,lity, in invivo vivo pharmacokineticspharmacokinetics of ofanimals, animals, and and clinical clinical or or bacteriological bacteriologi- caloutcome outcome [6]. [ 6Three]. Three terms terms,, epidemiological epidemiological cutoff cutoff (ECOFF), (ECOFF), pharmacodynamic cutoffcutoff (CO(COPDPD),), and and clinical clinical cutoff cutoff (CO (COCLCL) )are are employed employed to to describe describe these these concepts concepts [7,8] [7,8. ].ECOFF ECOFF is isa useful a useful tool tool for for laboratories laboratories conducting conducting susceptibility susceptibility testing testing and and for for clinicians clinicians testing test- inginfections. infections. COPD CO is PDtheis highest the highest MIC which MIC which can achieve can achieve probab probablele target targetattainment attainment (PTA) (PTA)(>90%) (>90%) in the inpopulation the population from fromthe target the target PK/PD PK/PD index index by Monte by Monte Carlo Carlo simulation. simulation. The The CO is a MIC-related clinical outcome. There is no previous investigation studying COCL isCL a MIC-related clinical outcome. There is no previous investigation studying the thesusceptibility susceptibility breakpoints breakpoints which which contains contains the the establishment establishment of of a aclinical clinical cutoff forfor cefquinomecefquinome againstagainst S.S. suissuis.. IrrationalIrrational useuse ofof antibioticsantibiotics inin thethe veterinaryveterinary clinicclinic isis thethe majormajor reasonreason leadingleading toto resistance.resistance. TheThe pharmacokinetic/pharmacodynamicpharmacokinetic/pharmacodynamic (PK/PD) (PK/PD) modelmodel cancan designdesign anan optimal dosing regimen to avoid resistance development [[9].9]. To our knowledge, no PK/PD model of cefquinome against S. suis has been developed in swine. It is useful to no PK/PD model of cefquinome against S. suis has been developed in swine. It is useful to assess the dose of cefquinome against S. suis, in order to guide clinical therapy. assess the dose of cefquinome against S. suis, in order to guide clinical therapy In this study, a terminal ECOFF (TECOFF), COPD, and COCL of cefquinome against In this study, a terminal ECOFF (TECOFF), COPD, and COCL of cefquinome against S. S. suis are explored which can provide evidence for the susceptibility breakpoint. The suis are explored which can provide evidence for the susceptibility breakpoint. The dosage dosage regimens of cefquinome against S. suis are optimized by an ex vivo PK/PD model. regimens of cefquinome against S. suis are optimized by an ex vivo PK/PD model. This This will be influential in protecting the efficacy of cefquinome. will be influential in protecting the efficacy of cefquinome. 2. Results 2.1.2. Results MIC Distribution of CEF against S. suis 2.1. MIC Distribution of CEF against S. suis The distribution of cefquinome against 342 S. suis isolates is shown in Figure2. MIC 50 and MICThe 90distrforibution cefquinome of cefquinome against S.against suis were 342 S. determined suis isolates to isbe shown 0.06 andin Figure 0.25 µ2.g/mL, MIC50 respectively.and MIC90 for The cefquinome minimum against inhibitory S. suis concentration were determined (MIC) to databe 0.06 of and 342 0.25S. suis μg/mL,isolates re- showedspectively. that The the MICminimum distribution inhibitory was consistentconcentration with (MIC) a normal data distribution of 342 S. bysuis normality isolates testshowed (p > that 0.2). the The MIC upper distribution tail (99.9%) was ofconsistent the wild-type with a normal cutoff value distribution was 1 µbyg/mL. normality The optimumtest (p > 0.2). MIC The range upper (0.015–1 tail (99.9%)µg/mL) of the was wild obtained-type usingcutoff thevalue NORMINV was 1 μg/mL. function, The opti- and themum probability MIC range of an(0.01 isolate5–1 μg/mL) with an was MIC obtained value higher using than the theNORMINV high cutoff functio was lowern, and than the 1.5%probability when employingof an isolate the with NORMDIST an MIC function.value higher The than difference the high between cutoff the was estimate lower (340)than and1.5% the when actual employing isolate number the NORMDIST (337) was function. minimal whenThe difference the optimum between fit was the 1 estimateµg/mL, and(340) 98.5% and the of theactual wild-type isolate number isolates (337) were was included minimal in the when ECOFF. the optimum As a result, fit was the tentative1 μg/mL, ECOFFand 98.5% was of defined the wild as-type 1 µg/mL isolates (Table were1).
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