New concepts in the field of cephalosporins: C-3' quaternary ammonium cephems (Group IV)
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1 New concepts in the field of cephalosporins: C-3' quaternary ammonium cephems (Group IV) Anart! Bryskier Hoechst Marion Roussel, Direction des Recherches Anti-infectieuses, Clinical Pharmacology, Romainville, France The C-3' quaternary ammonium cephems belong to group IV of the microbiological classification of cephalosporins. This group is divided into two subgroups according to the position of the quaternary ammonium moiety (C-3 or C-7). These compounds are structurally related to the third-generation cephalosporins (or group 111 of the microbiological classification), but in addition are featured with two or more of the following properties: broad-spectrum activity including Pseudomonas aeruginosa; activity against Enterobacteriaceae producing type 1 p-lactamase; the presence of a quaternary moiety. The zwitterionic properties of the C-3' quaternary cephalosporins allow rapid penetration through the outer membrane of Gram-negative bacteria, stability to and low affinity for type 1 j3-lactamases in the periplasmic space and high affinity for the penicillin binding proteins (PBPs). Among the currently available analogues cefpirome and cefozopran exhibit a well-balanced antibacterial spectrum against Gram-negative bacilli and Gram-positive cocci. Cefepime is less active against Staphylococcus aureus. Key words: Cephalosporin, quaternary ammonium, zwitterion, cefpirome, cefepime, cefozopran INTRODUCTION Since cephalothin and cephaloridine were introduced in 1964, cephalosporins have become a widely used and rapidly expanding class of antibacterial agents. A large number of derivatives have been synthesized by moditjring the 7-amino-cephalosponnic-acid (7 ACA). In recent years a number of highly active cephem derivatives have been reported, and some of them developed and introduced into clinical practice. Many of the currently marketed injectable cephalosporins, such as cefotaxime, ceftriaxone or cefiazidime have the common feature of a 2-amino- 5-thiazolyl-acetamido group at the 7-p position of the cephem nucleus. They show excellent activity against Gram-negative bacilli, except Pseudomonas aerugiuosa, and moderate activity against Staphylococcus aureus isolates susceptible to oxacillin and methicillin (MSSA). The wide-spread use of these agents was followed by the emergence of resistant mutant strains of microorganisms such as Enterobacter cloacae, Serratia marcescens and P. aeruginosa which constitutively produced high level of type 1 p-lactamases. One of Address for correspondence and reprints: Professor A. Bryskier, Hoescht Marion Roussel, Direction des Recherches Anti-infectieuses, Clinical Pharmacology, 102, route de Noisy, Romainville, France Tel: +33 (0)l Fax: +33 (0)l the most apparent defects of these compounds is the lack of activity against Enterobacteriaceae producing derepressed AmpC enzymes [ 11. Despite the number of cephalosporins and other antibacterial agents available, the treatment of patients with severe infections remains a common problem in daily clinical practice. Any progress should therefore be welcomed. Among significant advances, the recent introduction of a positively-charged substituent at the C-3' position of the cephem nucleus has overcome certain short-comings of earlier 2-amino-5-thiazolyl cephalosporins includmg activity against P. aeuttginosa and Gram-negative bacilli producing type 1 P-lactamases. NOVELTIES IN THE FIELD OF CHEMICAL STRUCTURES The substituent at the C-3 position and the side chain at the 7-p position of the cephem nucleus are key functions to alter the antibacterial activity. Extensive modifications of the 7-p acylamido side chain in combination with the C-3 substitution has led to many useful cephalosporin drugs. A significant step in the advance of the chemistry of cephalosporins was the introduction of the 2-amino-5-thiazolyl nucleus. The combination of this moiety with the syn (Z)-methoxyiniino chain found in cefuroxime gave rise to the new so-called thirdgeneration cephalosporins of which cefotaxime was the lead compound [2]. The introduction of the s1
2 s2 Clinical Microbiology and Infection, Volume 3 Supplement 1, April amino-5-thiazolyl moiety greatly enhances the antibacterial activity against Gram-negative bacilli. The addition of the syn (Z)-methoxyimino residue enhanced the stability to broad spectrum p-lactamase hydrolysis. After the discovery of cefotaxime, one of the aims of research in the field of cephalosporins was to mo&@ the C-3 heterocyclic moiety to increase the plasma halflife. This target was reached with the synthesis of cefiriaxone [3]. Many of the earlier compounds have a N-methyl-tetrazol thio at the C-3 position of the cephem nucleus which was found to give rise to problems of disulfiram-like reactions and coagulation abnormalities in man. The goal of the research in the field of cephalosporins was to improve the antibacterial activity against P. aeruginosa, S. aureus and other Gram-positive cocci and Gram-negative bacilli producing type 1 p-lactamases. Cefsulodin and ceftazidime were the first cephalosporins with improved activity against P. aeruginosa to be used in this clinical setting. They bear a 1-pyridinium group at the C-3 position. This observation prompted the researchers to prepare a new series of cephalosporins with a 2-amino-5-thiazolyloxiimino chain at the 7-P-position and a positively charged group at C-3 (azolium group). Most of the C-3' quaternary ammonium cephems are characterized by a condensed azolium moiety except for cefluprenam (Figure 1). All these derivatives are zwitterionic compounds and have no net charge, since the negative charge of the carboxylic acid group is (internally) neutralized (compensated for) by the positive c'harge of the C-3' quaternary ammonium group. Ceftazidirne is the earlier member of the oxiimino-2-amino-5-thiazolyl quaternary ammonium cephalosporins. Other cephalosporins contain a C-3' pyridinium such as cefsulodin, cefpimizole or cephaloridine, but none of them possess a 2-amino-5- thiazolyl moiety. Ceftazidime is a dianionic cephalosporin, in contrast to other compounds (e.g. cefpirome and cefepime) which are zwitterionic derivatives. Cefiazidime contains a carboxypropyloxiimino substituent attached to the acetyl chain. This additional carboxylic group provides acidic (negative charge) properties to this compound. The carboxylate anion of the cephem ring is neutralized by the positively charged quaternary ammonium group. The extra negative charge strongly influences the biological properties of ceftazidime (Figure 2). 7 -N3 H3C,+ Cefepime 0 t Cefclidin coo- Cefozopran H3C 0 A NbANH2 Cefluprenam H2C-CH3 CH2CH20H Figure 1 Structure of C-3' quaternary ammonium cephenis
3 Bryskier: C-3' quaternary ammonium cephems Modifications of the 2-amino-5-thiazolyl ring have been performed. It was found that substitution of the thiazolyl ring with a chlorine atom increased the antibacterial activity against P. aeruginosa, whereas the activity against other Gram-negative bacilli decreased. Introduction of a 5-amino-2-thiadiazolyl nucleus instead of a 2-amino-5-thiazolyl ring enhanced the antipseudomonal activity but slightly decreased the overall activity against Enterobacteriaceae [4]. Studies have demonstrated that analogues bearing an hydroxyimino residue exhibit higher activity against S. aureus, but they are less active against Gramnegative bacteria than their methoxyimino counterparts. Introduction of a monofluoromethoxyimino group at the 7-position led to a two-fold increase in activity against most bacteria as compared with the methoxyimino counterpart (cefluprenam). Among all the C-3' quaternary ammonium cephalosporins, only a few of them, such as cefpirome, cefepime and cefozopran were introduced into clinical practice. A number of compounds are in clinical development in Japan, such as cefclidin, cefluprenam and cefoselis. In the field of C-3' quaternary ammonium cephems, research continues in order to overcome the production of extendedspectrum p-lactamases by Enterobacteriaceae, to increase the antipseudomonal activity and to try to obtain compounds active against methicillin-resistant isolates of S. aureus. Extended-spectrum P-lactamases are recognized for their abilities to provide resistance to cefotaxime, ceftriaxone, ceftazidime and aztreonam and to some extent to C-3' quaternary ammonium cephalosporins. However, MIC values for cefpirome or cefepime to TEM-type enzyme producing Enterobacteriaceae HZN 0 11 H 0 0 Negative charge No charge -(SO3- or COO-) (-0CH3) v Dianionic cephems v Zwitterionic compounds Figure 2 Structure of dianionic and zwitterionic cephalosporins s3 are 5 8 mg/l, but these compounds are less stable to the hydrolysis by SHV-type enzynies (MIC values I 16 mg/l) except for SHV-5 (MIC 2-4 mg/l) [5]. Substitution by catechol or pyridone moities gives rise to a new wave of cephalosporins which are stable to hydrolysis by these enzymes, such as RU [6]. NOVELTIES IN THE FIELD OF MECHANISM OF ACTION The effectiveness of cephalosporins against Gramnegative bacilli is due to a combination of the ability to penetrate the outer membrane, the stability to p-lactamase hydrolysis in the periplasmic space, and affinity for penicillin binding proteins (PBPs). Nikaido et al. [7], using proteoliposome, demonstrated that cefclidin, cefpirome and cefepinie penetrated the porin channel of Exherichia coli and E. cloacae more rapidly than did ceftazidime. Yoshimura et al. [8] showed that the C-7-p methoxyiniino residue decreases the rate of penetration of monoanionic cephalosporins by a factor of 2 10, through the outer membrane into the OmpF porin of E. coli. Non-2- amino-5-thiazolyl quaternary ammonium cephalosporins are hydrolysed at low concentrations (I 10 pm) of type 1 p-lactamases [9]. Type 1 p-lactaniases hydrolyse these cephalosporins (cefpirome, cefepime, cefclidin) more slowly than did the earlier compounds at low substrate concentrations. Cefpirome, cefepime and cefclidin share low affinities or high Kin values for type 1 0-lactamases and would be expected to be hydrolysed slowly in vivo [10,11]. It has been shown that cefpirome, cefepime, cefclidin, and ceftazidime share a high affinity for PBP 3 of E. coli K-12 [12]. CLASSIFICATION OF C-3' QUATERNARY AMMONIUM CEPHALOSPORINS Cephalosporins belong to a complex class of p-lactam antibiotics. Numerous classifications have been proposed: chemical [13], pharmacokinetic [14], biological [I51 and microbiologcal [I 51. Within the microbiological classification, cephalosporins could be divided into six groups. Groups 111, IV and V represent the broad-spectrum cephalosporins, while the C-3' quaternary ammonium cephalosponns belong to group IV. This group of compounds can be divided into two subgroups, according to the position (C-3 or C-7) ofthe quaternary ammonium chain (Figure 3). Group IV-1 C-7 quaternary ammonium cephalosporins Few compounds have been designed in this subgroup.
4 s4 Clinical Microbiology and Infection, Volume 3 Supplement 1, April 1997 Three derivatives of this series, L , L , and L bind preferentially to PBP 2 of E. coli. Group IV-2 C-3' quaternary ammonium cephalosporins These derivatives have been divided into two classes according to the aryl substituent at C-7: 2-amino-5- thiazolyl or 5-amino-2-thiadiazolyl nucleus. Group IV-2A 2-aminod-thiazolyl derivatives Numerous compounds were described but only ceepirome and cefepime were introduced into clinical practice. All these compounds contain a syn alkoxyimino moiety at C-7. Cefpirome contains a cyclopentenopyridinium group at the C-3' position. Cefepime has a N-methylpyrrolidinium group at the C-3' position. Cefoselis (FK 037) is currently under development in Japan and cefquinone (HR 111) is used in veterinary medicine. Group lv-26 5-amino-2-thiadiazolyl derivatives Two compounds are under development in Japan: cefclidin, which contains a 4-carbamoyl-lquinuclidinium moiety. Cefluprenam has an original chemical structure with a fluoromethoxyimino moiety at C-7 and a propenyl side chain at C-3. Cefozopran with an imidazolopyridium was recently introduced in clinical practice. DEFINITION OF GROUP IV CEPHALOSPORINS Group IV covers molecules that differ in their chemical structure and antibacterial activity. Cephems, which belong to group IV possess two or more of the following characteristics: the presence of a C-3' quaternary ammonium side chain and are zwitterionic compounds; a broad antibacterial spectrum including P. aertrginosa; good antibacterial activity against Enterobacteriaceae isolates producing type 1 p-lactamases such E. cloacae, S. rnarcescens or Citrobacterfreundii. They have to fulfil the definition of group I11 [14,16]. NOVELTIES IN ANTIBACTERIAL ACTIVITIES All the C-3' quaternary compounds introduced for clinical use or under development possess the same antibacterial activity as cefotaxime, but they differ by adding antipseudomonal activity [17,18]. There are differences, however, among these compounds: cefclidin is twice as active as ceftazidime against P. aeruginosa, but cefepime and cefpirome are two-fold less active than ceftazidime against P. aeruginosa (Figure 4). Compared to ceftazidime these compounds are more active against Enterobacteriaceae producing type 1 p-lactamases such as S. rnarcescens, C.freundii, E. cloacae, E. coli, Providencia and M. rnovganii (MIC,, 5 8 mg/l) which are resistant to ceftazidime (Table 1) [18]. Studies have shown that ceeirome generates significant p-lactamase induction less frequently than ceftazidime against E. cloacae. Cefpirome has been shown to select derepressed mutants in vitro and in vivo to a lesser extent than ceftazidime [ 171. Against S. pneurnoniae, the most active compound within the C-3' quaternary ammonium cephems was cefpirome, whatever the resistance phenotype to Quaternary ammonium c-3 c-7 2-amino-5-thiazolyl I 5-amino-2-thiadiazolyl Cefpirome Cefclidin L Cefepime Cefozopran L Cefquinone Cefluprenam L Cefoselis ME FK 518 CP 6679 ME-1220 YM CS-46 1 ME-1228 DN9550 MT520 DQ2556 MT382 DW-751 TOC-39 ICI TOC-50 ICI YM I Figure 3 Structure of C-3' and C-7 quaternary ammonium cephems. Figure 4 Activity of C-3' quaternary ammonium cephems against P. aeuuginosa. From Le Noc et al. (181.
5 Bryskier: C-3' quaternary ammonium cephems penicillin G of the pneumococci isolates [ZY]. Against penicillin-resistant isolates, cefepime and cefozopran exhibit equivalent activity to cefotaxime. Cefluprenam was weakly active and cefclidin is inactive (Figure 5). Against S. awecis isolates susceptible to oxacillin, cefpirome was the most active compound. It was three times more active than cefozopran and cefluprenam and eight-times more active than cefepime. Ceftazidime was poorly active and cefclidin was inactive (Figure 6). CONCLUSION C-3' quaternary ammonium cephalosporins belong to group IV of the niicrobiologcal classification. Their chemical structure is innovative and the azolium part as well as the 2-amino-5-thiazolyl ring and the oxime residue, constitute the backbone of all novel series of cephalosporin derivatives. Due to the C-3' azolium part they have an orignal mecharllsni of actioii. Furthermore, they have overcome bacterial resistance by stability to and low affinity for cephalosporinases. Among the available C-3' quaternary ammonium cephalosporins, cefpirome followed by cefozopran have a well-balanced antibacterial spectrum including Grarnpositive cocci and Gram-negative bacilli. The activity against enterococci is more controversial. Cefpirorne exhibits in vitro activity against E.faecalis but not against E. faecitrm. Cefepime exerts an overall higher activity than cefluprenam except against S. aweu-. Cefclidin is the most active derivative against Gram-negative bacilli, but it is ineffective against Gram-positive cocci. Cefoselis shares the same antibacterial activity as cefozopran. The main aim of the preparation of these molecules was for microbiological advantages. All of them show approximately the same pharmac-okinetic profile. They have an apparent elimination half-life of two hours and are mainly eliminated unchanged in urine. s5 Table 1 In vitro activity of C-3' quaternary ammonium cephalosporin against Enterobacteriaceae Cefpirome Cefepime Cefozopran Cefclidiiie Cefluprenani Ccftazidinie Susceptible s Class IV P-lactamases V 0.1s Class 111 P-lactaiiiases Clasc I hyperproduced so oo Extended-spectrum ) P-lactaniascs Adapted from Le Noc et al. [ls]. I Figure 5 Activity of C-3' quaternary ammonium cephems against S. pneumoniae. From FrCmaux et al. [19]. Figure 6 Activity of C-3' quaternary ammonium cephems against 5'. uurcus. From Le Noc et al. [lxj.
6 S6 Clinical Microbiology and Infection, Volume 3 Supplement 1, April 1997 References 1, Sanders CC, Sanders WE, JR. Microbial resistance to newer generation p-lactam antibiotics: clinical and laboratory implications. J Infect Dis 1985; 151: Bucoua R, Heymks R, Lutz A, Pknasse L, Perronet J. Propriktts antibiotiques inattendues dans le domaine des ckphalosporines. CR Acad Sci - Paris - Sine D- 1977; 284: Reinert R, Weiss U, Brombacher U, et al. Ro /001, a novel potent long acting parenteral cephalosporin. J Antibiot 1992; 45: Watanabe NA, Sugiyama I. Role of the aminothiadiazolyl group in the antipseudomonal activity of cefclidm. J Antibiot 1992; 45: Jacoby GA, Cameras I. Activities of 0-lactam antibiotics against Escherichia coli strains providmg extended-spectrum p- lactamases. Antimicrob Agents Chemother 1990; Aszodi J, Humbea D, Bonnefoy A, Collette P, Mauvais P, Chantot JF. RU 59863, a novel catechol substituted vinylogous cephalosporin: in vitro antibacterial activity. Program and Abstracts of 35th Intersci Conf Antimicrob Agents Chemother San Francisco 1995, F Nikaido H, Liu W, Rosenberg EY. Outer membrane permeabhty and p-lactamases stability of dipolar ionic cephalosporins containing methoxyimino substituents. Antimicrob Agents Chemother 1990; 34: Yoshimura H, Nikaido H. Diffusion of B-lactam antibiotics through the porin chanel of Escherichia coli K-12. Antimicrob Agent Chemother 1985; 27: Livermore DM. Kinetics and significance of the activity of the Sabath and Abraham s p-lactamase of P. aeruginora against cefotaxime and cefsulodin. J Antimicrob Chemother 1983; 11: Inoue E, Mitushuhashi S. Interaction of E-1040 with cephalosporinase from Citrobacter freundii GN 739. Antimicrob Agents Chemother 1989; 33: Satakes S, Hiraoka M, Mitshuhashi S. Interaction of cefpirome and a cephalosporinase from C. freundii GN Antimicrob Agents Chemother 1989; 33: Pucci MJ, Sowek JB, Kessler RE, Dougherty TJ. Comparison of cefpirome, cefepime, and cefclidine binding affinities for penicillin binding proteins in E. coli K-12 and P. aenrginosa SC Antimicrob Agents Chemother 1991; 35: Bryskier A. Classification des ckphalosporines et relation structure activitt. des mkthoxyiminoaminothiazolyl ctphalosporines. Lyon Pharm 1983; 34: Bryskier A, Procyk T, Labro MT. Cefodzime, a new 2-aminothiazolyl cephalosporin:physicochemical properties, toxicology and structure activity realionship. J Antimicrob Chemother 1990; 26: (suppl C) O Callaghan CH. Classification of cephalosporins by their antibacterial activity and pharmacokinetic properties. J Antimicrob Chemother 1975; 1: (suppl) Bryskier A, Aszod~ J, Chantot JF. Parenteral cephalosporin classification. Exp Opin Invest Drug 1994; 3: Pkchkre JC, Wilson W, Neu H. Laboratory assessment of antibacterial activity of zwitterionic 7-methoxyimino cephalosporins. J Antimicrob Chemother 1995; 36: Le Noc P, Bryskier A, Champevollier D. Comparative antibacterial activity of RU 59863, a new catechol cephalosporin Program and Abstracts of 35th Intersci conf Antimicrob Agent Chemother San Francisco 1995; F Frkmaux A, Sissia G, Bryskier A, Geslin P. In vitro activity of cefpirome and six other parented p-lactam agents, penicillin-susceptible and penicillin-resistant pneumococci. 6th Eur Cong Clin Microb Infect Dis, Vienna 1995.
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