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The Consequences for Antibiotic Resistance antibiotics Review Antibiotics in Food Chain: The Consequences for Antibiotic Resistance Shashi B. Kumar, Shanvanth R. Arnipalli and Ouliana Ziouzenkova * Department of Human Sciences, The Ohio State University, Columbus, OH 43210, USA; [email protected] (S.B.K.); [email protected] (S.R.A.) * Correspondence: [email protected] Received: 19 August 2020; Accepted: 8 October 2020; Published: 13 October 2020 Abstract: Antibiotics have been used as essential therapeutics for nearly 100 years and, increasingly, as a preventive agent in the agricultural and animal industry. Continuous use and misuse of antibiotics have provoked the development of antibiotic resistant bacteria that progressively increased mortality from multidrug-resistant bacterial infections, thereby posing a tremendous threat to public health. The goal of our review is to advance the understanding of mechanisms of dissemination and the development of antibiotic resistance genes in the context of nutrition and related clinical, agricultural, veterinary, and environmental settings. We conclude with an overview of alternative strategies, including probiotics, essential oils, vaccines, and antibodies, as primary or adjunct preventive antimicrobial measures or therapies against multidrug-resistant bacterial infections. The solution for antibiotic resistance will require comprehensive and incessant efforts of policymakers in agriculture along with the development of alternative therapeutics by experts in diverse fields of microbiology, biochemistry, clinical research, genetic, and computational engineering. Keywords: microbiome; resistome; horizontal evolution; quorum-sensing 1. Introduction and Background In 1928 Alexander Fleming serendipitously discovered penicillin [1] (Figure1). Its utility as medicine became clear following the extraction of a small amount of penicillin from a fungus Penicillium chrysogenum, by Howard Florey and Ernst Chain in 1941, at the Radcliffe Infirmary. This extract was initially used for treating a policeman in Oxford, England who contracted a likely infection of Staphylococcus aureus with an admixture of various Streptococci. The condition of the policeman was initially improved; however, the amount and quality of penicillin synthesis were inadequate at the time. Eventually, sepsis relapsed and the policeman died. Presently, penicillin and other antibiotics are produced in copious amounts. The term antibiotic is defined as a natural or synthetic chemical inhibiting both the growth and survival of microorganisms. Among these antibiotics, methicillin is considered to be one of the most effective. However, studies revealed that sepsis cases increased from 621,000 to 1,141,000 between the years of 2000 and 2008 [2]. The death toll from sepsis rose from 154,000 to 207,000 cases. The extent of this rise is attributed to the emergence of methicillin resistant S. aureus (MRSA). MRSA marks the beginning of the development of antibiotic–resistant microbes (also called ESKAPE pathogens, standing for Enterococcus faecium, S. aureus, Klebsiella pneumoniae, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacteriaceae)[3]. It is reported that in the United States, India, Thailand, and European Union, antibiotic resistance causes more than 23,000, 58,000, 38,000 and 25,000 deaths per year, respectively [4–7]. The predicted deaths from drug-resistant microbial pathogens could rise from approximately 700,000 per year to 10 million deaths per year by 2050 and threaten global health [8]. Antibiotics 2020, 9, 688; doi:10.3390/antibiotics9100688 www.mdpi.com/journal/antibiotics Antibiotics 2020, 9, 688 2 of 26 Antibiotics 2020, 9, x FOR PEER REVIEW 2 of 26 FigureFigure 1. Timeline 1. Timeline of antibiotic of antibiotic discovery discovery and itsand onset its onset of resistance. of resistance. The antibiotic The antibiotic paradigm paradigm emerges emerges out of theout followed of the followed discovery discovery of penicillin. of penicillin. Between theBetween 1960s andthe 1960s the 1980s and there the 1980s was a surgethere was in the a discoverysurge in the of antibiotics,discovery of but antibiotics, this development but this declineddevelopm betweenent declined the 1980s between and thethe 1990s. 1980s Theand identificationthe 1990s. The of newidentification antibiotic of classes new byantibiotic pharmaceutical classes by companies pharmaceutical has stagnated companies since has 1987 stagnated and coincided since 1987 with and progressivelycoincided with increased progressively antibiotic resistanceincreased andantibiotic mortality resistance related toand antibiotic-resistant mortality related infections. to antibiotic- resistant infections. Microorganisms are able to develop antibiotic-resistant genes to enhance their survival, thus minimizingMicroorganisms the treatment are able options to develop for microbial antibiotic-res infectionsistant andgenes increasing to enhanc mortalitye their survival, in human thus populations.minimizing Antibiotic the treatment resistance options is classified for microbial into three infections categories basedand increasing on the threat: mortality urgent, in serious, human andpopulations. concerning Antibiotic (Table1). Theresistance global is threat classified of resistance into three to imipenemcategories antibioticsbased on inthe A.threat: baumannii urgent, infectionsserious, has and been concerning reported in(Table both Organization1). The global for Economicthreat of resistance Co-operation to andimipenem Development antibiotics (OECD) in A. andbaumannii non-OECD infections countries has across been the reported globe [9]. in Several both reasonsOrganization are responsible for Economic for the developmentCo-operation ofand antibioticDevelopment resistance (OECD) globally and andnon-OECD in developing countries countries, across the such globe as India[9]. Several [10,11 ].reasons Poor public are responsible health conditionsfor the development and health care of systems, antibiotic availability resistance of antibioticsglobally and over in the developing counter, lack countries, of public such knowledge as India of appropriate[10,11]. Poor dosage public of health antibiotics conditions and their and haphazard health care use, systems, as well availability as a high incidence of antibiotics of infectious over the diseasescounter, have lack been of proposedpublic knowledge as the major of factorsappropriate augmenting dosage the of problem.antibiotics This and continuum their haphazard of antibiotic use, as resistancewell as a concept high incidence was proposed of infectious to describe diseases the ha progressiveve been proposed interconnecting as the major influence factors of augmenting human, industrial,the problem. agricultural, This continuum and wild environments of antibiotic [ 12resi]. Thestance crude concept mortality was dueproposed to infectious to describe diseases the in Indiaprogressive is 416.75 interconnecting per 100,000 persons, influence which of human, is twice indu thestrial, rate agricultural, in the United and States wild (roughly environments 200 per [12]. 100,000The crude persons) mortality [13]. The due problem to infectious is aggravated diseases further in India by is the 416.75 void inper the 100,000 development persons, of which new classes is twice of antibioticsthe rate in the since United 1990 States (Figure (roughly1)[14–17 200]. per 100,000 persons) [13]. The problem is aggravated further by the void in the development of new classes of antibiotics since 1990 (Figure 1) [14–17]. Table 1. Classification of antibiotic resistance threats. UrgentTable 1. Classification of Serious antibiotic resistance threats. Concerning 1. A. baumannii, P.Urgent aeruginosa , 1. Streptococcus pneumonia, penicillin-non-susceptibleSerious Concerning carbapenem-resistant 2. Haemophilus1.Streptococcus influenzae, pneumoniaampicillin-resistant, penicillin-non- 2. Clostridium1. A. baumannii, difficile P.(CDIFF) aeruginosa, 3. Shigella spp., fluoroquinolone-resistant 1. Group B susceptible 1. Group B 3. N.carbapenem-resistant gonorrhoeae-3rd generation 4. Enterococcus spp., vancomycin resistant Streptococcus Streptococcus (GBS), cephalosporin-resistant, 5. Multidrug-resistant2. Haemophilus influenzae,Acinetobacter ampicillin-resistant 2.Clostridium difficile (CDIFF) clindamycin(GBS), resistant fluoroquinolone-resistant 6. Drug3. resistant Shigella Campylobacterspp., fluoroquinolone-resistant 3. N. gonorrhoeae-3rd generation 2. Groupclindamycin A 4. Carbapenem- and 3rd 7.Extended-spectrum4. Enterococcusβ spp.,-lactamase vancomycin producing resistant cephalosporin-resistant, Streptococcusresistant(GAS), generation cephalosporin Enterobacteriae (ESBLs) 5. Multidrug-resistant Acinetobacter erythromycin resistant resistantfluoroquinolone-resistantEnterobacteriaceae: 8. Multidrug-resistant P. aeruginosa 2. Group A 6. Drug resistant Campylobacter 3. S. aureus, K. pneumonia4. Carbapenem-, E. coli, and 3rd 9. Drug-resistant non-typhoidal Salmonella Streptococcus 7.Extended-spectrum β-lactamase producing vancomycin resistant Enterobactergenerationspp., cephalosporinSerratia spp., 10. Drug-resistant Salmonella serotype Typhi (GAS), Enterobacteriae (ESBLs) Proteusresistantspp. andEnterobacteriaceaeProvidencia spp.,: K. 11. Drug resistant M. tuberculosis erythromycin 8. Multidrug-resistant P. aeruginosa Morganellapneumonia,spp. E. coli, Enterobacter 12. Methicillin-resistant S. aureus (MRSA) resistant 9. Drug-resistant non-typhoidal Salmonella spp., Serratia spp., Proteus spp., 3. S. aureus,
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