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Avoparcin and virginiamycin as animal growth promoters: a plea for science in decision-making
- Clement Summers
- 3 months ago
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1 IN SEARCH OF OPINION Avoparcin and virginiamycin as animal growth promoters: a plea for science in decision-making J. Acar 1, M. Casewell 2, J. Freeman 3, C. Friis 4 and H. Goossens 5 1 University of Pierre et Marie Curie, Paris, France; 2 King's College School of Medicine, London, UK; 3 Harvard School of Public Health, Boston, MA, USA; 4 RoyalVeterinary and Agricultural University, Copenhagen, Denmark; 5 University of Antwerp, Antwerp, Belgium INTRODUCTION In the past few years there have been renewed calls to phase out or even ban antibiotics given to animals as growth promoters. For example, these were made at a WHO conference in Berlin in 1997, at a European meeting in Copenhagen in September 1998, and in recent reports from the House of Lords and from Directorate General XXIV of the European Commission. However, an interdisciplinary conference was held at Georgetown University in spring 1999 and included physicians, congressional sta, and regulatory agencies, including the Food and Drug Administration and Centers for Disease Control and Prevention (CDC). It was agreed that a rigorous risk assessment should be undertaken before conclusions were reached on the future of feed additives in livestock production, and, indeed, it has recently been announced by the FDA that a quantitative risk assessment will be carried out of the impact of growth promoters on enterococcal resistance. Used as growth promoters from the 1950s, various antibiotics were found to increase growth in young animals by up to 8% [1]. The possible actions in the gut include altering the ora, increasing nutrient absorption, and diminishing toxin production. Initially, a wide range of antibiotics was used, but because resistant organisms emerged, various countries introduced restrictions. Thus, in 1969, the Swann Report recommended that therapeutic antibiotics should not be used as growth promoters. Later, the European Union (EU) banned certain antibiotics as growth promoters, but the USA did not introduce similar restrictions. In April 1997, avoparcin was banned in the EU, as were virginiamycin, bacitracin, spiramycin, and tylosin in July The EU directive (70/524) stipulates that not only must additives favorably a ect livestock production, but that they should not endanger human health. Corresponding author and reprint requests: H. Goossens, Department of Microbiology, Universitair Ziekenhuis Antwerpen, Wilrijkstraat 10, B-2650 Edegem, Belgium Tel: Fax: Clearly, any decision to ban or phase out should be based on scienti c studies. The EU avoparcin ban was implemented despite scienti c advice from the EU's own Scienti c Committee on Animal Nutrition (SCAN) that there were insu cient data to support it. Moreover, SCAN reviewed the evidence for the unilateral Danish ban on virginiamycin in 1998, also concluding that this was insu cient. A major problem is the non-rigorous literature: so many of the data are recent and not peer-reviewed that drawing rm conclusions is di cult. In particular, there are few wellplanned and conducted studies, as pointed out by Phillips [2]. Nevertheless, we review here publications and recent communications for two key antibioticsöavoparcin and virginiamycinöbut not for the others, given the paucity of the data. AVOPARCIN Avoparcin is a glycopeptide structurally related to vancomycin and teicoplanin, and was widely used in Europe as a growth promoter from the early 1970s until banned. Vancomycinresistant enterococci (VRE) in Europe were rst reported in the mid-1980s [3,4], and are now an important cause of hospital-acquired infection, almost exclusively in the USA [5]. Their acquired resistance mechanisms to glycopeptides are complex, and three phenotypes (vana, vanb and vand)canbe distinguished [6]. The vana resistance phenotype consists of high-level vancomycin and teicoplanin resistance. The genes are often found on a transposon that in vitro is easily transferred to other enterococci [6]. In the laboratory, the vana gene cluster has also been successfully transferred from Enterococcus faecalis to Staphylococcus aureus [7].The vanb resistance phenotype consists of variable levels of vancomycin resistance and susceptibility to teicoplanin. The genes encoding the vanb resistance phenotype are more commonly chromosomal but can also be transferred. VanD is very rare. The van gene clusters confer resistance to glycopeptides through similar mechanisms. In the USA, avoparcin was never used in animals, whereas in Europe it was widely used until banned [8]. In the USA, only vancomycin is used for human disease, whereas in Europe, both vancomycin and teicoplanin are used. So, despite = 2000 Copyright by the European Society of Clinical Microbiology and Infectious Diseases
2 ãæð Clinical Microbiology and Infection, Volume 6 Number 9, September 2000 the very low incidence of VRE infections in Europe [9], was there enough evidence to justify the ban? To answer this, it is useful to compare the di erences in the occurrence and spread of VRE in both continents, in humans and animals [10].The prevalence of VRE in isolates in US hospitals, both inside and outside intensive care units, has been rapidly increasing [5]. About 70% of isolates exhibit the vana phenotype and about 25% the vanb phenotype [11,12]. Strategies to eradicate VRE from US hospitals have generally failed. Moreover, most VRE have high-level resistance to ampicillin and the aminoglycosides, leaving few options for treatment [12]. As opposed to hospitalized patients,vre have not been found in community-based volunteers in the USA [13,14]. Likewise, VRE have not been found in American food-producing animals and pet animals [13,15,16]. These studies suggest that VRE are not present in the gut of humans and animals in the USA. However, only two studies have been performed in humans [13,14] and three studies in animals [13,15,16]; the microbiological methods were inadequate and only a few samples were studied. Clearly, better-designed studies should be performed in the USA to con rm the absence of VRE in the community and animals. In particular, a broth enrichment step in the culture of feces almost doubles the rate of detection of VRE carriage [17]. In Europe, VRE have spread only in high-risk units such as intensive care, transplant, hematology and renal units. The outbreaks were mostly caused by clonal dissemination of single strains of vana-containing E. faecium, although several strains have been involved in hospital units in the UK. In contrast to the USA, the outbreaks have been successfully contained in Europe through infection control and/or reduction of antibiotic selective pressure.thus,vre infection is not persistent in European hospitals. On the other hand,vre can be isolated from the feces of as many as 12% of healthy volunteers [18]. Several studies have shown that VRE can be found in farm and pet animals in Europe [18,19]. These VRE have always been of the vana phenotype. In contrast to the VRE isolated in US hospitals, those from humans and animals in Europe, e.g. in Belgium [20], remain generally susceptible to ampicillin and to the aminoglycosides. In addition, the susceptibility pro les of the vana phenotype of E. faecium from food animals are comparable with those from community fecal samples. On the other hand, where the vanb phenotype occurs in human feces [21], this cannot be derived from animals, as it is not found in the latter. In Australia it appears that vanb is the predominant phenotype found in humanvre cases, which contrasts with the situation in Europe, despite the fact that avoparcin has been widely used on both continents [22]. In European hospitals with a VRE problem, multiply resistant strains are reported that are similar to those in the USA, rather than those in European animals, with resistance to ampicillin, to high-level gentamicin, and to virtually all antimicrobials [23,24]. VRE may spread clonally from one host to another, or there may be horizontal transfer of vancomycin resistance genes between E. faecium of human and animal origins, and/or from a common reservoir of glycopeptide resistance. Thus the vana resistance genes may have been introduced into the community via the food chain [25]. Although the experimental ingestion by a single subject of 10 7 CFU of chicken-derived VRE resulted in the excretion of VRE for about 3 weeks [26], the interpretation of these ndings has been questioned with regard to the microbiological detection and identi cation methodology, and the lack of con rmation that the ingested and excreted strains were identical [27]. In addition, it has proved remarkably di cult to nd indistinguishable clone pairs of vana phenotypes of E. faecium in fecal samples from humans and animals, although this has been shown for a turkey farmer and his ock [28], and in two instances for epidemiologically unrelated pig and human fecal isolates by Descheemaeker et al [20]. Any generalized deduction from these observations about the unidirectional spread of VRE from animals to humans would be highly speculative. Such observations may simply indicate the wide distribution of VRE clones or the existence of a common reservoir [20]. An alternative suggestion is that the glycopeptide-resistant genetic elements spread horizontally and contribute to vancomycin resistance in humans [29,30]. The transposon originally identi ed as conferring resistance, Tn1546, displays striking diversity due to point mutations, insertion of IS elements, and deletions in the intergenic regions. These variations provide potential markers to type and trace the spread of transposonmediated glycopeptide resistance [30,31]. However, the stability of the elements must be established before they can be used as epidemiologic markers and the true signi cance of their heterogeneity can be resolved [30]. Some have found that elements of vana are shared between organisms of human and animal origins [20,29^31] and others have not [32]. For example, in a collection of 132 vancomycin-resistant E. faecium strains from Belgium, eight transposon RFLP types were found [20].The two predominant types, one indistinguishable fromtn1546 (`type 1') and a more common close variant (`type 2'), were found invre from both animal and human feces. A statistically signi cant association was found between this type 2 and pig VRE isolates. These ndings are in agreement with results reported by Jensen et al [29],Woodford et al [30], and Willems et al [31]. Thus, VRE isolates from human and farm animals may share a common vancomycin resistance gene pool. These results would suggest that genetic diversity in Tn1546 can be successfully exploited for tracing the routes of transmission of vancomycin resistance genes. Further studies are therefore needed, and, for example,vre from di erent origins should be exchanged among research groups in
3 Acar et al Avoparcin and virginiamycin as animal growth promoters ãæñ several countries to compare glycopeptide-resistant clones and transposon types. In The Netherlands, the use of avoparcin in turkey ocks has been correlated with a high frequency of VRE compared with ocks not fed avoparcin, although details are scant [28]. More evidence of the role of avoparcin in the emergence of VRE in food animals was provided recently. Bager et al [33] showed a statistically signi cant decline of VRE isolated from broilers after the ban of avoparcin in 1995 in Denmark. Kruse et al [34] also demonstrated a strong and statistically signi cant association between the use of avoparcin in Norwegian poultry production and the occurrence of VRE. Pantosti et al [35] demonstrated, 18 months after the banning of avoparcin, a decline in the percentage of poultry meat samples containing vana gene-positive VRE from 14.6% to 8%. Thus, avoparcin consumption data correlate well with the prevalence of vana VRE in animals. Several US studies have correlated the acquisition of VRE by humans with the intensity and duration of antimicrobial therapy. Clonal dissemination has been associated with oral as well as intravenous vancomycin [36]. Consumption data in the USA compared with those of major European countries from 1984 to 1996 show an acceleration of vancomycin use in the early 1980s, and further acceleration when oral formulations became available in the mid-1980s. During 1996, for example, kg of vancomycin was used in the USA, compared with 60 kg for the whole of The Netherlands [8,37]. Its intravenous use may have increased because of the emergence of multiresistant coagulase-negative or - positive staphylococci, enterococci, and Streptococcus pneumoniae. The increase in oral use in the USA is possibly a result of its widespread prescription for antibiotic-associated colitis. The vancomycin consumption data correlate well with the greater prevalence of VRE in US hospitals compared with Europe. Moreover, its spread in the former in the 1990s may have been preceded by increased resistance of E. faecium to ampicillin and aminoglycosides. Indeed, high-level resistance to ampicillin and gentamicin among E. faecium isolated in one institution signi cantly increased over the 22 years from 1968 [38]. Given the mobility of the vana and vanb resistance genes, transfer of these genes to ampicillin- and gentamicin-resistant E. faecium may have occurred subsequently. Multiresistant vancomycin-resistant E. faecium strains may have been further selected by the use of b-lactam antibiotics and aminoglycosides. E. faecium is less susceptible to b-lactam antibiotics than E. faecalis because of low a nity or the overproduction of penicillin-binding proteins [39].This might partly explain the greater spread of E. faecium compared to other enterococci.the vana gene has been linked with gentamicin resistance [40] and the vanb gene with ampicillin resistance in enterococci [41]. Thus, the emergence of ampicillin and aminoglycoside resistance may be a prerequisite for the emergence and nosocomial spread of VRE. VIRGINIAMYCIN Used extensively as a growth promoter for 30 years, virginiamycin consists of a synergistic mixture of type A and type B streptogramins. In humans, oral pristinamycin, also a mixture of streptogramin A and B, has been used for 30 years for staphylococcal infections, particularly in France, where topical virginiamycin was also used. Recently, dalfopristin/quinupristin (Synercid), a mixture of type A and B semisynthetic streptogramins, has been developed for human intravenous use [42]. Synercid has promising activity against methicillinresistant Staphylococcus aureus (MRSA), and against VRE, excluding E. faecalis [43]. The recent controversy has arisen because animal-derived virginiamycin-resistant organisms (or their genetic determinants) are cross-resistant with Synercid and might cause human infections. There is anecdotal evidence of clinical infection with streptogramin-resistant enterococci in humans, but the emergence of resistance was associated with therapeutic use of Synercid. Resistance to streptogramin A, but not streptogramin B, confers resistance to the combination. The mechanism of streptogramin resistance in one strain of human E. faecium is inactivation of the streptogramin A component by an acetyltransferase encoded by the sata gene [44] and the satg gene [45]. In human staphylococcal isolates, type A streptogramins are resisted by acetyltransferase enzymes (encoded by vat, vatb, vatc) or active e ux (encoded by vga, vgab). All these mechanisms are reported to be plasmid-mediated. Little is known about the genetic mechanisms in animal isolates. After 30 years' use of virginiamycin in animals, streptogramin-resistant staphylococcal or streptogramin-resistant enterococcal infections in humans are still rare, as con rmed by Jones et al [46]. Of clinical isolates of Gram-positive cocci from 200 centers in the USA and Canada, 99.8% of 1011 E. faecium isolates were sensitive to Synercid, as were 99.8% of 519 VRE isolates. More than 99% of the isolates of Staphylococcus aureus were sensitive to Synercid. Even in France, with the additional selective pressure of pristinamycin, there is no evidence of increasing streptogramin resistance. Of 895 isolates of MRSA from 95 non-university hospitals, 98.5% were sensitive to both pristinamycin and Synercid. In 1997, van den Bogaard found pristinamycin-resistant enterococci in the feces of Dutch pigs [47]. However, these were not speciated, which is important, as E. faecalis is intrinsically resistant to streptogramins. The Danish monitoring program also reported virginiamycin resistance in about half of the isolates of E. faecium from pigs and broilers [48,49]. Although a control group was not included, Welton et al showed the emergence of streptogramin-resistant E. faecium from cloacal cultures of turkeys fed virginiamycin [16].
4 ãðò Clinical Microbiology and Infection, Volume 6 Number 9, September 2000 From The Netherlands, a letter reported enterococci (again, non-speciated) resistant to pristinamycin in 30% of healthy suburban residents [47]. Nevertheless, confusingly, the 1997 Danish Danmap Report found [50] only 2% of healthy humans with stool samples containing streptogramin-resistant E. faecium. Hence, rigorous studies are needed to determine the prevalence of streptogramin-resistant enterococci and to determine whether these organisms re ect transitory excretion or colonization or represent a threat to human health. DISCUSSION Understandable anxieties about antibiotic resistance, with its overtones of human health impairment, can engender evangelical calls for premature action. Nevertheless, the importance of therapeutic use in humans to the development of such resistance should not be underestimated. Our review of the data provides no rigorous evidence that the two growth promoters avoparcin and virginiamycin used in animals create antibiotic-resistant bacterial strains in humans that cause clinical infections, and there are insu cient data for the other antibiotics used in this way. However, for avoparcin there are recent studies suggesting that vana-positive VRE in feces of healthy humans may be derived from animals. Fortunately, these VRE have not been associated with an emergence of VRE infections in humans in Europe. Direct evidence for such a link will be di cult to demonstrate, given the molecular complexity of the problem. Such a sequence might comprise: presence of vana genes in enterococci in animals; selection of thesevre in animals following the use of avoparcin or other antibiotics and horizontal gene transfer; ingestion of food contaminated with vana-positive VRE by humans; selection of thesevre in humans following the use of glycopeptides or other antibiotics and horizontal gene transfer; clinical infection with vana-positivevre in humans. Our understanding is supported by a recent comprehensive review of the literature by the Heidelberg Appeal Nederland (HAN) Foundationöan independent alliance of almost 200 senior academicsöwhich also concluded [51] that `documented in-vivo cases showing spread of antimicrobial resistant Gram-positive bacteria from livestock to humans are in essence non-existent'. CONCLUSIONS We need to clarify the issue of gene transfer and bacterial population dynamics. Speci cally, the following questions need to be answered: To what extent do growth promoters select for resistant organisms in animals? What is the prevalence of resistant enterococci in human populations? If they are in the gut transitorily, can they transfer resistance to other organisms? If so, to what extent? Do animal enterococci colonize humans? If so, do they cause disease? Answers to these questions need well-designed studies and would take years of research, but would enable a proper risk analysis. Banning antibiotics as growth promoters in animals will not solve the problem of antibiotic resistance in hospitals. ACKNOWLEDGMENT We thank Dr Stephen Lock CBE for his invaluable help in the preparation of this manuscript. REFERENCES 1. Friis C. Consumption of antimicrobials by food animals and the resistance of pathogens in food animals. J Hosp Infect 1999; in press. 2. Phillips I. Assessing the evidence that antibiotic growth promoters in uence human infections. J Hosp Infect1999; 43: 173^8. 3. Leclercq R, Derlot E, Duval J, Courvalin P. Plasmid-mediated resistance to vancomycin and teicoplanin in Enterococcus faecium. N EnglJ Med1988; 319: 157^ Uttley AHC, Collins CH, Naidoo J, George RC. Vancomycinresistant enterococci. Lancet1988; 1: 57^8. 5. Anonymous. Nosocomial enterococci resistant to vancomycin in the United States, 1989^1993. MMWR1993; 42: 597^9. 6. Leclercq R, Courvalin P. Resistance to glycopeptides in enterococci. Clin Infect Dis1997; 24: 545^ Noble WC,Virani Z, Cree RGA. Co-transfer of vancomycin and other resistance genes from Enterococcus faecalis NCTC12201to Staphylococcus aureus. FEMS Microbiol Lett1992; 93: 195^8. 8. Wegener HC. Historical yearly usage of glycopeptides for animals and humans: the American^European paradox revisited. Antimicrob Agents Chemother1998; 42: Vandamme P,Vercauteren E, Lammens C et al. A survey of enterococcal susceptibility patterns in Belgium. J Clin Microbiol 1996; 34: 2572^ Goossens H. Spread of vancomycin-resistant enterococci: di erences between the United States and Europe. Infect Control Hosp Epidemiol1998; 19: 546^ Clark NC, Cooksey RC, Hill BC, Swenson JM, Tenover FC. Characterization of glycopeptide-resistant enterococci from US hospitals. Antimicrob Agents Chemother1993; 37: 2311^ Eliopoulos GM,Wennersten CB, Gold HS et al. Characterization of vancomycin-resistant Enterococcus faecium isolates from the United States and their susceptibility in vitro to dalfopristin^quinupristin. Antimicrob Agents Chemother1998; 42: 1088^ Coque TM, Tomayko JF, Ricke SC, Okhyusen PC, Murray BE. Vancomycin-resistant enterococci from nosocomial, community and animal sources in the United States. Antimicrob Agents Chermother1996; 40: 2605^ Silverman J,Thal LA, Perri MB, Bostic G, Zervos MJ. Epidemiologic evaluation of antimicrobial resistance in communityacquired enterococci. J Clin Microbiol1998; 36: 830^ Thal LA, Chow JW, Mahayni R et al. Characterization of antimicrobial resistance in enterococci of animal origin. Antimicrob Agents Chemother1995; 39: 2112^15.
5 Acar et al Avoparcin and virginiamycin as animal growth promoters ãð" 16. Welton LA, Thal LA, Perri MB et al. Antimicrobial resistance in enterococci isolated from turkey ocks fed virginiamycin. Antimicrob Agents Chemother1998; 42: 705^ Ieven M, Vercauteren E, van Descheemaker P, Laer F, Goossens H. Comparison of direct plating and broth enrichment culture for the detection of intestinal colonization by glycopeptide-resistant enterococci among hospitalized patients. J Clin Microb 1999; 37: 1436^ Bates J. Epidemiology of vancomycin-resistant enterococci in the community and the relevance of farm animals to human infection. J Hosp Infect1997; 37: 89^ Devriese LA, Ieven M, Goossens H et al. Presence of vancomycin-resistant enterococci in farm and pet animals. Antimicrob Agents Chemother1996; 40: 2285^ Descheemaeker PRM, Chapelle S, Devriese LA, Butaye P, Vandamme P, Goossens H. Comparison of glycopeptide resistant Enterococcus faecium isolates and glycopeptide resistance genes of human and animal origins. Antimicrob Agents Chemother 1999; 43(8): 2032^ Wendt C, Krause C, Xander LU, Lo er D, Floss H. Prevalence of colonization with vancomycin-resistant enterococci in various population groups in Germany. J Hosp Infect1999; 42: 193^ Commonwealth Department of Health and Aged Care, Commonwealth Department of Agriculture, Fisheries and Forestry. The use of antibiotics in food-producing animals: antibiotic resistant bacteria in animals and humans. Report of thejoint ExpertTechnical Advisory Committee on antibiotic resistance (JETACAR). Commonwealth Department of Health and Aged Care, Commonwealth Department of Agriculture, Fisheries and Forestry, Wade JJ, Rolando N, Williams R, Casewell MW. Serious infections caused by multiply-resistant Enterococcus faecium. Microb Drug Res1995; 1(3): 241^ Wade JJ. The emergence of Enterococcus faecium resistant to glycopeptides and other standard agentsöa preliminary report. J Hosp Infect1995; 30: 483^ Chadwick PR, Woodford N, Kaczmarski EB, Gray S, Barrell RA, Oppenheim BA. Glycopeptide-resistant enterococci isolated from uncooked meat. JAntimicrob Chemother1996; 38: 908^ Berchieri Jr A. Intestinal colonization of a human subject by vancomycin-resistant Enterococcus faecium. Clin Microb Infect 1999; 5: 97^ Goossens H. Vancomycin-resistant Enterococcus faecium derived from animals colonizing the human gut: the missing evidence? Clin Microbiol Infect1999; 5: 64^ Van den Bogaard AE, Jensen LB, Stobberingh EF. Vancomycinresistant enterococci in turkeys and farmers. N Engl J Med 1997; 337: 1558^ Jensen LB, Ahrens P, Dons L, Jones RN, Hammerum AM, Aarestrup FM. Molecular analysis of Tn1546 in Enterococcus faecium isolated from animals and humans. J Clin Microbiol 1998; 36: 437^ Woodford N, Adebiyl A-MA, Palepou M-FI, Cookson BD. Diversity of vana glycopeptide resistance elements in enterococci from human and nonhuman sources. Antimicrob Agents Chemother 1998; 42: 502^ Willems RJL, Top J, van den Braak N et al. Molecular diversity and evolutionary relationships of Tn1546-like elements in enterococci from humans and animals. Antimicrob Agents Chemother 1999; 43: 483^ Van den Braak N, Belkum A, Keulen M,Vliegenthart J,Verbrugh HA, Endtz HP. Molecular characterization of vancomycinresistant enterococci from hospitalized patients and poultry products inthe Netherlands. J Clin Microbiol1998; 36: 1927^ Bager F, Aarestrup FM, Madsen M, Wegener F. Glycopeptide resistance in Enterococcus faecium from broilers and pigs following discontinued use of avoparcin. Microb Drug Res1999; 5: 53^ Kruse H, Johansen BK, Rorvik LM, Schaller G. The use of avoparcin as a growth promotor and the occurrence of vancomycinresistant Enterococcus species in Norwegian poultry and swine production. Microb Drug Res1999; 5: 135^ Pantosti A, Del Grosso M, Tagliabue S, Macri A, Caprioli A. Decrease of vancomycin-resistant enterococci in poultry meat after avoparcin ban. Lancet1999; 354: 741^ RaoGG,OjoF,KolokithasD.Vancomycin-resistantGram-positive cocci:riskfactorsforfecalcarriage.jhospinfect1997;35: 63^ Kirst HA,Thompson DG, NicasTI. Historical yearly usage of vancomycin. Antimicrob Agents Chemother1998; 42: 1303^ Grayson ML, Eliopoulos GM, Wennersten CB et al. Increasing resistance to beta-lactam antibiotics among clinical isolates of Enterococcus faecium: a 22-year review at one institution. Antimicrob Agents Chemother1991; 35: 2180^ Fontana R, Aldegheri M, Ligozzi M, Lopez H, Sucari A, Satta G. Overproduction of a low-a nity penicillin-binding protein and high-level ampicillin resistance in Enterococcus faecium. J Clin Microbiol1984; 38: 1980^ Cercenado E, Unal S, Eliopoulos CT et al. Characterization of vancomycin-resistance in Enterococcus durans. JAntimicrob Chemother 1995; 36: 821^ Rice LB, Carias LL, Rudin SB, Donskey CJ. Plasmid-mediated vanb-type resistance in Enterococcus faecium. In 37th Interscience Conference on Antimicrobial Agents and Chemotherapy [abstract C-157] Zervos MJ. Vancomycin-resistant Enteroccocus faecium infection in the ICU. New Horizons1996; 4: 385^ Solh N, Allignet J. Staphylococcal resistance to streptogramins and related antibiotics. Drug Res Updates1998; 1: 169^ Ronde-Fournier R, LeClercq R, Galimand M, Duval J, Courvalin P. Identi cation of the sata gene encoding a streptogramin A acetyltransferase in Enterococcus faecium BM4145. Antimicrob Agents Chemother1993; 37: Werner G, Witte W. Characterization of a new enterococcal gene satg, encoding a putitive acetyltransferase conferring resistance to streptogramin A compound. Antimicrob Agents Chemother 1999; 43: 1813^ Jones RN, Ballow CH, Biedenbach DJ, Deinhart JA, Schentag JJ. Antimicrobial activity of quinupristin^dalupristin (RP 59500, Synercid) tested against over 2800 recent clinical isolates from 200 medical centers in the United States and Canada. Diagn Microbiol Infect Dis1998; 30: 437^ Van den Bogaard AE, Mertens P, London NH, Stobberingh EE. High prevalence of colonization with vancomycin- and pristinamycin-resistant enterococci in healthy humans and pigs in The Netherlands: is the addition of antibiotics to animal feeds to blame? JAntimicrob Chemother1997; 40: 454^ Aarestrup FM, Bager F, Jensen NE, Madsen M, Meyling A, Wegener HC. Surveillance of antimicrobial resistance in bacteria isolated from food animals to antimicrobial growth promoters and related therapeutic agents in Denmark. APMIS 1998; 105: 606^ DANMAP98. Consumptionofantimicrobialagentsandoccurrenceof antibiotic resistance in bacteria, food and humans in Denmark. Copenhagen: Statens Veterinaere Serumlaboratorium, Statens Serum Institut, 1999.
6 ãðá Clinical Microbiology and Infection, Volume 6 Number 9, September DANMAP 97. Consumption of antimicrobial agents and occurrence of antibiotic resistance in bacteria, food and humans in Denmark. Copenhagen: StatensVeterinaere Serumlaboratorium, Statens Serum Institut, Bezoen A, Haren W, Hanekamp JC. Emergence of a debate: AGPs and public health. Human health and growth promoters (AGPs): Re-assessing the risk. Amsterdam: Heidelberg Appeal Nederland Foundation, 1999.


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Man, I love marinating chicken. I really really do. Once I get a good marinade going I know my meal is going to be a winner. Plus I feel like mom of the year because there's something about marinading something that just tells me I'm a boss. Like an organized "yeah, I have dinner planned and I know what I'll be cooking in an hour" boss. Just me? Stay with me, friend.
When I was in college I cooked two things. (1) Corn from a can that I poured into a bowl, heated in the microwave, and drowned in salt and butter. (2) Chicken marinated in store bought Italian dressing and baked in the oven.
Also brownies from a box of brownie mix. I was a beast at brownie making.
Now I'm a little older (ahem, thirty-six), wiser, and my food tastes have most definitely changed. But I still crave me some Italian Marinated Chicken. These days I use my own Easy Homemade Italian Dressing. It contains no sugar or junk of any kind. (Those sneaky salad dressing makers are not scared to throw in a crazy sounding ingredient.) My dressing is completely Whole30 compliant, gluten free, and dairy free. I can personally attest that it's also dang tasty on a salad or as a marinade.
I like to let the chicken marinade for at least an hour. From there it's up to you how you want to prepare it. It's awesome on the grill or in a saute pan on the stove with a little olive oil. Give it a try and let me know what you think!
Italian Marinated ChickenPrint Recipe Pin Recipe
- 6 chicken breasts trimmed
Easy Homemade Italian Dressing
- 3/4 cup olive oil
- 1/4 cup red or white wine vinegar
- 1 teaspoon garlic powder
- 1 teaspoon dried oregano
- 1 teaspoon dried basil
- 1/2 teaspoon onion powder
- 1/2 teaspoon crushed red pepper
- 3/4 teaspoon salt
- 1/2 teaspoon pepper
- 1 teaspoon lemon juice
- Add all your Easy Homemade Italian Dressing Ingredients to a jar. Shake until combined.
- Place your chicken breasts in a gallon Ziploc bag. Pour the dressing over them. Seal the bag.
- Let your chicken marinade for at least one hour.
- Grill or saute your chicken depending on your preference. I'm providing instructions for both below.
To Grill
- Remove each chicken breast from the bag and place on a hot grill over medium heat. Grill 5 to 7 minutes on each side or until done. (Juices should run clear.)
To Saute
- Add 2 tablespoons of olive oil to a skillet on the stove. Heat the oil over medium high heat. (You'll know it's ready when the chicken sizzles as you place it in the pan.) Add each chicken breast to the skillet in a single layer. Cook for about 5 minutes. Flip your chicken. Cook for an additional 5 minutes. (Chicken should be firm to the touch when done and juices should run clear.)

subset: commoncrawl


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Lisbeth Salander, the cult figure and title character of the acclaimed Millennium book series created by Stieg Larsson, will return to the screen in The Girl in the Spider's Web, a first-time adaptation of the recent global bestseller. Golden Globe winner Claire Foy, the star of The Crown, will play the outcast vigilante defender under the direction of Fede Alvarez, the director of 2016's breakout thriller Don't Breathe; the screenplay adaptation is by Steven Knight and Fede Alvarez & Jay Basu.
Official Site: www.girlinthespidersweb.movie/site
Director: Fede Alvarez
Writer: Steven Knight and Fede Alvarez & Jay Basu
Cast: Claire Foy, Sverrir Gudnason, Lakeith Stanfield, Sylvia Hoeks, Stephen Merchant, Claes Bang, Christopher Convery, Synnøve Macody Lund and Vicky Krieps
Sorry there are no upcoming showtimes for The Girl in the Spider's Web


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Just coming to write this update has done me good. Until I read what I wrote nearly a month ago I had forgotten how far I have come, and how much things have changed. I have had a lot of ups and downs in the last few weeks, the worst stage being a few days of really bad rectal pain, so bad that I was taking pain killers and Valium just to be able to sleep, and really felt rough. I suspect that may have been a flare up of radiation proctitis caused partly by having home made tomato soup- too acidic for my poor old bum, at least just yet.
My bowel is gradually starting to settle down, and I have also discovered a really good trick which seems definitely to help. I've only started this today, but it really has made a difference to me, so I'll pass it on; As you get better organized, there gets to be a certain time of day when your bowels decide it is OPEN time. For me this is after lunch, but everyone is different, and for some people it is after every meal. The problem for me was that I would start going to the loo after lunch and be in and out maybe 10 times or more until everything calmed down for another day, usually after 4-5 hours. This is draining, bad for your ass and very restricting, you can't go anywhere during this time, even trying to cook or do basically anything is difficult. I was taking Imodium with little effect. SO....the big secret is this- take one Imodium half an hour to an hour before the meal which gives you grief. It doesn't mean you won't go at all, (I was worried about this, weirdly!) but it does slow things down and make it all come together. Eureka! I have only been three times to the loo today! No-one who hasn't been in this situation can understand how much this means; I was getting so depressed and angry, I didn't know what to do with myself. One little tablet and everything is better.
I am back on the Metamucil by the way, I gradually built up from a teaspoon once a day up to three spoons and the gas is better. I am still not eating much fresh vegetables or fruit, except bananas, but I did have some cabbage salad and a few beans on Saturday, both considered potential trouble makers, with no bad effects. I would try to introduce more veggies, but it isn't really a good time now, because tomorrow we go on a big trip. Yes, back to dear old Chasamba, waiting for us in Puerto Princesa. It's a 36 hour journey, which means that my Imodium discovery is just in time. We leave here tomorrow afternoon and travel to Jordan by road, get on a plane to Bangkok, then Hong Kong, then Manila, then Puerto Princesa. Four flights, but thank goodness not much waiting in airports, which I hate the most, and the long flight is a night flight, so we can sleep. I hope. I have chosen seats near the loo, just in case.
I am so happy to be going home at last, even though this is my home too, and Oren's relatives have been very good to us. But Chasamba needs us, her keel plates need changing and her engine needs to be fixed, she needs to sail again, and so do we!
I will have regular check ups in whatever country we are in; my next one is CEA in May. So far my levels are; 0.8, 1.37. May will be the third since finishing treatment, and I'm obviously hoping for a low one, fingers crossed.


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Play a play
This is the only two possibilities.
The first kind of possibility, as Jiang Chen speculated, Scarlet Cauldron Region basic impossible exists in such a Formation Grandmaster. Celestial level Other Formation Grandmaster, Divine Abyss Continent may have, but decided not to be in the Scarlet Cauldron Region. Even the entire Human Territory may not exist.
Therefore, this possibility can be ruled out.
Then the remaining possibility is the second plant.
For a time, Jiang Chen's mood was complicated. The powerful Earth Attribute treasure has always been what Jiang Chen is looking for.
In the Five Elements attribute of Metal, Wood, Water, Fire, Earth, there is no perfect supplement in the section of Earth Attribute. This is why Jiang Chen has not impacted Emperor Realm.
is waiting, waiting for the treasure of the Earth Attribute to appear.
If this place really has the Earth Attribute treasure, it can produce the power of the big earth veins, and this treasure is absolutely extraordinary.
Even if Jiang Chen previous generation is well-informed, at this moment it is also unavoable and some hearts are hot.
Perhaps the previous generation he has seen more powerful ten times hundr than this treasure, but it is something that belongs to the previous generation. For him, it is just a decoration.
Because he has no cultivation talent, it is not used at all.
This world is different, what he lacks now is such a treasure. You wear out iron shoes in hunting round!
Originally tracking the Greenwood Villa, in order to save Wei Xing'er. If there is an accidental discovery, it is undoubtedly an unexpected surprise. it is the big surprise of Tianda.
Jiang Chen's brain was a little hot for a moment, and quickly calmed down. Suddenly sitting cross-legged, seriously meditation deduction.
To ensure accuracy, Jiang Chen sent a Gold Biting Rat King to let it scout again. Determine if it is really big earth veins moving.
As a Gold Biting Rat Race, Gold Biting Rat King, even close to the formation edge, will not attract the special attention of those Emperor Realm.
After all, in the depths of this mountain, some powerful beasts are also very normal matter.
Gold Biting Rat King is timid, but the task that Jiang Chen confesses will be executed in every sense of the term.
About a hour later, Gold Biting Rat King returned again, telling Jiang Chen very surely, that is the big earth veins, there is absolutely nothing wrong with it.
After confirming Gold Biting Rat King, Jiang Chen is more and more sure that there is definitely a powerful Earth Attribute treasure around this area.
However, what a treasure is, Jiang Chen is not known.
However, one thing is affirmed. This treasure must have been bred here for a long time. Otherwise, it is impossible to make this land, so that this land will form a terrible pulsating terrain.
This kind of pulsation topography, a little understanding of the formation of the formation, can easily build a terrible formation based on this pulsating terrain.
Once this form is activated, it will force the big earth veins to move. There is no need for the forformable attack to be launched by the formation itself. Just by stimulating the big earth veins, it is enough to make the Emperor Realm strong on the spot.
Have to say that people who found this place are very lucky.
This lucky person, maybe the Greenwood Villa Lord!
Although it is only speculation, Jiang Chen can basically confirm that the Greenwood Villa main choice impacts the Emperor Realm seventh level, and it must be his reason.
The dynamic terrain of this big earth veins is perhaps the reason for the Greenwood Villa main choice.
Greenwood Villa main discovery here, afraid there is already a very long time. Otherwise, he will not construct a form here, nor will there be such a layout.
Although this layout is not perfect, it is definitely not a year and a half. Without a ten-year-old layout, it can't be done.
Seeing is believing, Jiang Chen is finished. Immediately summon Ice and Fire Monster Lotus, slowly approaching the formation edge from the depths of the ground.
Coming to the formation edge, Jiang Chen used his life to learn and began to study the formation.
Formation itself is not really esoteric. But the place where formation is in the eye, but it is a powerful force vortex.
Therefore, the big earth veins move from the area to the surrounding area. Form a powerful large earth veins to move aura.
This formation, just the aura guidance of the big earth veins to surround, forming a perfect defense, so that all people who want to pass through here, can not circumvent the formation.
Jiang Chen sees it really, looked at it for a long time, looked at it from all angles, wants to find the loophole of this form, and find a region that can pass.
However, what disappoints Jiang Chen is that although this form is simple, there is no loophole at all.
To be precise, after the formation of the aura of this big earth veins, there is no loophole at all.
Unless this formation stops, the big earth veins are not guided. Otherwise, if you want to pass through here, even the Great Emperor rank is strong, you may not be able to do so.
But what makes Jiang Chen happy is that the formation is too simple and does not guide the aura of the big earth veins.
Otherwise, this area will become a dead zone. Anyone close this area will be involved in this pulsating trend.
This large veins of the Pulsation region, like a giant big disc, produces a terrible amount of grinding power, strangling everything, killing everything!
Everything that enters this pulsating core will be crushed into fly ash.
In this way, there is almost no possibility to get into the gap. Unless the guards come out by themselves, it is impossible for outsiders to enter the control area.
Gold Biting Rat King sighed:
Gold Biting Rat King's Inheritance Memories has a certain understanding of the big earth veins.
Jiang Chen sighed:
Jiang Chen has been looking for flaws, but sadly found that there is no flaw in the dynamic area of this big earth veins.
Gold Biting Rat King can't live nod:
Gold Biting Rat King's words gave Jiang Chen some inspiration.
These four guards are not common characters, one of the Emperor Realm six, one Emperor Realm five, and two are also Emperor Realm fourth level peak, close to the existence of Emperor Realm.
Such characters, in the Upper Eight Regions may not be the most top rank. But in the Scarlet Cauldron Region, it is definitely a top rank figure.
This kind of character, the common thing, really can't attract them.
But Jiang Chen has a bunch of good things, and there is no shortage of good things at all.
Gold Biting Rat King screams frantically, carrying 12 Heaven level Spirit Medicines in his mouth. Facial expression, rushing toward the formation edge.
There was a burst of sound behind the scenes:
This swearing person is not the other one, it is Jiang Chen.
At the moment, he and Gold Biting Rat King are performing a ruse of inflicting an injury on oneself.
The color of the Emperor on the Gold Biting Rat King face is not pretending. Because the Gold Biting Rat Race inborn courage is small, the closer it is to the edge of the formation, the greater the psychological pressure of the Gold Biting Rat.
This formation has four orientations, four orientations are independent and echo each other.
At this moment, the defender of this position is a senior elder of the Scarlet Cauldron Region third rank sect Scarlet Separation Sect, under the Greenwood Villa main invitation, here is the Greenwood Villa Master Protector.
This old surname is high, Emperor Realm five-fold peak, close to Emperor Realm's six-fold cultivation base, and the position of Scarlet Separation Sect is extremely high. Because of his age, has basically asked about mortal.
This time, Greenwood Villa was able to invite him, and it was unexpected from the many person.
This old is very alert, heard Jiang Chen's screaming, immediately applied eye technique, and looked around.
In this old sight, a big old mouse with an entire height of golden hair rushed toward him.
Behind this Great Golden Rat, but the distance of 3-5 miles, a martial artist is catching up crazy.
Old Gao brow-wrinkle, he never imagined, there would be human cultivator in this place. did not expect that this person and a beast came to the defensive area of He.
Seeing the two levels of Heaven level Spirit Medicine in Gold Biting Rat King's mouth, Old Gao's first thought was to rush out to kill the golden mouse, and then take that Heaven level Spirit Medicine as his own.
However, reason tells him that this matter cannot be reckless.
The most important person at the moment is the guarding formation. In the formation region, he is absolutely absolute safety. Once you leave the formation, you are outside and everything is unknown.
Although Old Gao doesn't think the big mouse and the cultivator behind it can pose any threat to him. But to live to a big age, the most basic care is still there.
Therefore, although this Old Gao has a heart movement, it has no impulse. Instead, the battle is at the formation edge, examining the situation and watching the scene that happened under his nose.
Gold Biting Rat King quickly hit the edge of the formation, a flaw, pushed directly by the strength of the formation edge, and the figure flew directly.
This form itself has a rejection of the strength of the outside, which is a warning.
If you have to be hard-hitting, it will completely ignite the big earth veins and be involved in the pulsation of the might. Once caught by the force of the big earth veins, it must be ground into fly ash.
Just before the Gold Biting Rat King hit, Jiang Chen had arrived.
Coldly smiled:


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bringing 2 U events & happenings in and around Ipoh … & beyond…
If you have been following my social media platforms, you would know that I was in Taiwan (Republic of China) in mid-January. I visited the island country for 6D/5N at the invitation of Golden Century Tour & Travel, with the support of and in collaboration with the Tourism Bureau of the Republic of China (Taiwan). I have ... continue reading »
Having spent only about five days in Jordan, I do not claim to know everything about The Hashemite Kingdom. The following are just my perceptions and I wish to share them with anyone who is planning a trip to this fascinating country. Limestone boxes Almost 99% of the buildings in the places that we visited in Amman ... continue reading »
Much has been written and documented in videos about Petra, the world heritage site in southern Jordan, also listed as one of the New 7 Wonders of the World. However, nothing beats experiencing the Red Rose City personally. When I returned from my trip, a friend enquired if I was disappointed with Petra. Why should I ... continue reading »


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Amsterdam the capital of the Netherlands is one of the greatest tourist magnets in Europe. A relaxed cosmopolitan atmosphere, exciting museums and the picturesque canal district with its tiny bridges, cafes and townhouses makes Amsterdam a popular destination. Beautiful, sloping architecture, cosy bars and canal lined streets are all central to Amsterdam's enduring appeal. Historic buildings and arched bridges over striking canals adorn the beautiful city of Amsterdam. Known as one of the greatest small cities in the world, Amsterdam charms visitors with its cool and cosy atmosphere. This capital city of Neth... More
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As the capital of Gelderland, Arnhem has a rich and interesting history, part of which can be discovered in a number of monumental buildings. Arnhem is surrounded by green landscapes with the Veluwe on one side and the water meadows on the other. Arnhem has been among the top 10 best shopping cities in Holland for years now. A visit to Arnhem is easily combined with one of the many top attractions. Arnhem is known mostly for its John Frost Bridge, which the British tried to secure during World War II. Arnhem is probably best known for the battle conducted here in 1944 and immortalised in the film 'A Bridge ... More
Breda is a wonderful fun loving city in the southern part of Netherlands. Breda is it the main city of Nassau in Holland, boasting many imposing monuments. Between 1403 and 1568, the ancestors of royal family converted Breda to a beautiful city with richly decorated buildings. Even today these architectural pearls still manage to impress. Breda is a city in the west of the province North Brabant of the Netherlands and has over 170000 inhabitants. It is a very cosy and social city, partly due to the large number of students that live in the city. In the historical city centre tourists will find lots of interesting... More
Leiden was Holland's first University City and today offers an unbeatable combination of character full architecture, high quality museums and picturesque canals. The events are as diverse as a Rembrandt ice sculpture exhibition and a musical of his life. Leiden is known as the City of Refugees. Throughout history Leiden has given shelter to people who were no longer welcome elsewhere. In the 17th century the population of Leiden grew from just over 20000 to 70000 in a short amount of time. Even in the 20th century no less than three out of four Leiden inhabitants descended from a refugee. The Pilgrims too fo... More
The city of Rotterdam is located in the South Holland province. It is a welcoming city with a plethora of museums, bars and restaurants to entertain visitors and residents. Rotterdam is a vibrant city known for its architecture, art and edginess and is fast becoming a must see European destination. Rotterdam makes a great alternative for visitors wanting to avoid the more tourist trodden Amsterdam and although this is true, Rotterdam is a truly exciting destination in its own right. Rotterdam is the second largest city in the Netherlands and forms the southern part of the Randstad, the 6th largest metropolitan ar... More
With its 30 kms of sandy beaches Texel Island is a paradise for beach lovers. Texel has much more to offer, however seven villages each one pretty as a picture and unique natural scenery and is within easy and quick reach. On Texel there's room enough for large nature areas a significant farming culture and seven small villages. In an area roughly the same size as the capital, there are less than 14000 inhabitants not including the sheep. Den Burg the biggest of the villages is both charming and vibrant boasting plenty of interesting local shops and even a cute little cinema. The island is renowned for its bi... More


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@leboudoirselectif wearing YBD's Simeon Farrar Attention Tote at London Fashion Week.
@jodieldun wearing YBD's Kelly Love Lost Innocence Blouse at London Fashion Week.
Good evening guys! Tonight I'm sharing with you my new outfit and a new café!
Ksu and I have recently discovered a lovely restaurant in Residence hotel called 'Davydov'. This place is decorated in a historic style. There are many pictures, baroque curtains and columns.
During the week I often go downtown and sometimes I have time to stop and drink a cup of coffee or tea in one of my fave cafés. Now I can include Davydov to my list of favourite places.
I should keep this office style often, because we don't have free style at school and in the evening I usually have meetings with clients. This weekend I have two creative projects with different models so keep your eyes on my blog for more photos and details!
Today's look consists of a nude basic top, black shorts, amazing shoes in black nude tones and watches (I can't imagine life without them!). I really like shoes, especially those which can be mixed in with different looks and styles. That's why I have these new shoes.
They are perfect and classy! The best thing about them is that they have zippers at the back, so they fit my legs perfectly and don't fly away!
I hope you're having a wonderful end to the week!


text: New Session Starts Oct. 15 Posted on October 8, 2018 by ATABlackBeltAcademyOur new session begins the week of October 15. Contact us today and try your first class.Communication – the link between the world and me. We welcome good communication between potential students parents and our instructors. How can help you?


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About the continuation of the anime "Bleach" fans do not even dream, but about the restart/reload they are seriously thinking. Kubo, why not give your child a new life? New breath? To revive him from the ashes of last arch? The last arch, unfortunately, was not adequately appreciated by the public. Many people do not like the canon in terms of patterns. The main character and the girl, who loving him... Fans would like more reciprocity and harmonious pairs. But this is not the most important thing. Originally you wanted to make shinigami with guns or scythe of death. Japanese traditions are also good. But what if you combine firearms and samurai swords? All this will look very impressive, new styles of battles! As for the love lines ... Here we should rely on reality, socionics, kindred souls. In the manga and anime as such, there was no romance, would like to see this, even with a rating of 18+ ) The audience grew and the new generation is already fed up with the stereotypes of the past great shonens (少年). We do not ask you to make a completely new story. We want to see old, but in a new interpretation, and alternative development of the canon, where the heroes will be happy with those who were intended for them by fate. And would like a more large-scale battle with Yahweh, where not only Ichigo. He and his whole team, by common efforts, fights the enemy and that each of them contributed to the victory over the enemy, but not royal one-short.
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