An Updated History of Antimicrobial Agents and Chemotherapy: 2000–2020

Since its inaugural issue nearly half a century ago, Antimicrobial Agents and Chemotherapy has served as a premier source for reports on scientific and clinical advances in the field of antimicrobial chemotherapy. As a follow-up to the previous “History of Antimicrobial Agents and Chemotherapy from 1972 to 1998” written by George A. Jacoby (Antimicrob Agents Chemother 43:999–1002, 1999, https://doi.org/10.1128/AAC.43.5.999), we herein highlight the further evolution of this comprehensive and authoritative journal in response to changing science, demographics, and information technology.

ABSTRACT

Since its inaugural issue nearly half a century ago, Antimicrobial Agents and Chemotherapy has served as a premier source for reports on scientific and clinical advances in the field of antimicrobial chemotherapy. As a follow-up to the previous “History of Antimicrobial Agents and Chemotherapy from 1972 to 1998” written by George A. Jacoby (Antimicrob Agents Chemother 43:999–1002, 1999, https://doi.org/10.1128/AAC.43.5.999), we herein highlight the further evolution of this comprehensive and authoritative journal in response to changing science, demographics, and information technology.

TEXT

In May 1999, George A. Jacoby, then the editor-in-chief of Antimicrobial Agents and Chemotherapy (AAC), published a minireview entitled “History of Antimicrobial Agents and Chemotherapy from 1972 to 1998” (1). In this article, George Jacoby recounted the early history of how AAC evolved into a monthly periodical, how it found its specific niche among ASM journals, and acknowledged the editors who had served the journal over those years. The subsequent 2 decades have seen AAC maintain and solidify its reputation as a premier journal for high-quality scientific articles on antibacterial, antifungal, antiviral, and antiparasitic mechanisms of action and resistance. As the field has evolved, the journal has evolved as well, both in its scientific content and its editorial practices. As such, we think it is a reasonable time to provide another update on the progress of the journal over the past 2 decades.

A major source of AAC’s strength over the years has been its outstanding editorial board. There have been three editors-in-chief (EICs) and 42 editors of AAC since 2000. EICs serve 5-year terms with an option to renew for a second 5 years. George M. Eliopoulos served as EIC from 2000 to 2010. He trained in internal medicine at Columbia Presbyterian Medical Center and in infectious diseases at Massachusetts General Hospital and the Beth Israel Deaconess Medical Center and serves on the infectious diseases faculty at the latter institution. He has special interests in antimicrobial development and antimicrobial resistance. Louis B. Rice served as EIC from 2010 to 2020. He trained in internal medicine at New York University-Bellevue Hospital Center and in infectious diseases at the New England Deaconess Hospital. His career began on the infectious diseases faculty at Case Western Reserve University, and for the past 10 years. he has served as chair of the Department of Medicine at the Warren Alpert Medical School of Brown University. His research interests include mechanisms and epidemiology of antimicrobial resistance, particularly in resistance to beta-lactam antibiotics.

The process for selecting EICs has recently undergone a significant change for all ASM journals, with AAC among the first two journals to engage in the process. The prior process had been unstructured, resulting in most cases in a current or retired editor rising to the position after discussion between the outgoing EIC and the chair of the Journals Board. The new process is an open one that invites applications from the scientific community, with no requirement of prior service as an AAC editor. Those applications are evaluated by a search committee composed of the chair of the Journals Board, the director of Journals, the outgoing AAC EIC, and EICs from two other ASM journals, followed by live interviews with selected candidates. Cesar A. Arias was selected through this process and began serving as AAC EIC in July 2020. He received his M.D. from Universidad El Bosque, School of Medicine in Colombia and his Ph.D. in molecular biology and microbial biochemistry from the University of Cambridge. He did his internal medicine and infectious disease training at the University of Texas McGovern Medical School at Houston and MD Anderson Cancer Center. His research interests are in the molecular mechanisms and clinical implications of resistance in Gram-positive bacteria, particularly in daptomycin resistance in enterococci.

In the year 2000, there were nine editors of AAC, including the editor-in-chief. By July 2010, that number had increased to 12, and by 2019, there were 14. In 2000, there were two female editors, and no editors hailed from outside the United States. In 2019, there were 5 female editors and four of the 14 were located outside the United States. The names and terms of the editors are listed in Table 1. The list includes some of the most prolific and respected investigators in a variety of fields related to antimicrobial chemotherapy. The AAC editorial board, which consisted of 120 members in 2000, had expanded to 149 by 2020. The editorial board is also populated by some of the foremost investigators in the field.

TABLE 1.

Editors of AAC during the 2000–2020 period

Editora	Term	EIC term
Barbara E. Murray	1992−2002
Karen Bush	1994−2004
Michael N. Dudley	1995−2003
George M. Eliopoulos*	1995−2000	2000−2010
Spotswood L. Spruance	1995−2005
Lowell S. Young	1996−2006, 2007−2012
William A. Craig	1998−2007
Louis B. Rice*	2000−2009	2010−2020
John H. Rex	2001−2010
Patricia A. Bradford	2002−2011
Johan W. Mouton	2003−2008
Gian M. Rossolini	2004−2014
Barry I. Eisenstein	2005−2014
Robert L. LaFemina	2005−2015
Paul G. Ambrose	2007−2017
Thomas D. Edlind	2007−2012
John D. Turnidge	2008−2012
Henry F. Chambers	2009−2019
David M. Shlaes	2010−2020
Sevtap Arikan-Akdagli	2010−2020
Robert A. Bonomo	2011−2016
David R. Andes	2012−
Eric Nuermberger	2013−2017
Wilbur K. Milhous	2013−
Helen Boucher	2014−
Yohei Doi	2014−2019
Cesar A. Arias*	2015−2020	2020−
Miguel Angel Martinez	2015−
Jared A. Silverman	2016−
Laurent Poirel	2016−
James E. Leggett	2017−
Kelly E. Dooley	2017−
Pranita D. Tamma	2019−
Alessandra Carattoli	2019−
Boudewijn L. M. DeJonge	2020−
Andreas H. Groll	2020−
Benjamin Howden	2020−
Ryan K. Shields	2020−
Anne-Catrin Uhlemann	2020−

^aEditors-in-chief are indicated by an asterisk.

The number of manuscripts published in AAC peaked at 1,061 in 2015. At the time, the acceptance rate for manuscripts submitted to AAC was 50%. In subsequent years, the editors of AAC have made a concerted effort to be more selective in the manuscripts that are accepted, resulting in acceptance rates that range between 40 and 45%. There were 805 papers published in 2019. Over the past 2 decades, AAC has seen a gradual reduction in the percentage of articles it publishes that originate from the United States. In 1998, 44% of articles published in AAC were from the United States. In 2019, that number had decreased to 36%.

The categories of articles in AAC have evolved with the field (Table 2). Two new categories were added between 2000 and 2020: the Epidemiology and Surveillance category was first added in February 2011, reflecting the increased resources devoted to tracking the growth and evolution of antimicrobial resistance around the globe. Sixty-one such manuscripts were published in 2018 to 2019. In 2015, Challenging Clinical Cases in Antimicrobial Resistance was introduced at the suggestion of Cesar Arias, who came on as an editor to manage the section and is now AAC’s editor-in-chief. Other sections have seen an increase or diminution in their numbers, again reflecting movement in the field. The percentage of manuscripts comprising the Susceptibility section published between 2000−2001 and 2018−2019 decreased from 20% to 11%, perhaps reflecting the reduced number of early phase new agents introduced during the intervening period. On the other hand, the percentage of Clinical Therapeutics manuscripts increased from 3% to 13%.

TABLE 2.

Number of articles published in AAC categories and percentage of the total for each 2-year period

AAC category	2000–2001		2018–2019
	No. of articles published	% of total	No. of articles published	% of total
Minireviews	12	1	18	1
Challenging Clinical Cases			5	<1
Epidemiology and Surveillance			121	7
Mechanisms of Resistance	363	28	349	21
Analytical Procedures	4	<1	18	1
Antiviral Agents	124	9	105	6
Biologic Response Modifiers	17	1	9	<1
Experimental Therapeutics	172	13	269	16
Clinical Therapeutics	38	3	205	12
Susceptibility	249	19	169	10
Mechanisms of Action	129	10	99	6
Pharmacology	142	11	218	13
Chemistry/Biosynthesis	12	<1	8	<1
Letters to the Editor	49	4	81	5

One measure of a journal’s influence is the impact factor. There has been much discussion over the past 5 years among the editors-in-chief of ASM journals of the pernicious effects of the impact factor on academic publishing, leading to a statement from the ASM that it would no longer use the impact factor in its journal advertising (2). Still, impact factor is often mentioned as a consideration in author decisions regarding where to submit their manuscripts. During the period of 1977 to 1997, the AAC impact factor ranged between 3 and 4. Since 2001, the AAC impact factor has ranged between 4 and 5, with the 2019 impact factor being 4.904, which ranked it 28th worldwide among journals both in the Microbiology category and the Pharmacology & Pharmacy category (3). AAC was the most cited journal in the Pharmacology & Toxicology category in 2019, maintaining its top position for several years running (3).

The process of publishing papers in AAC has evolved markedly over the past 2 decades. In 1999, AAC introduced online publication for the first time. In 2000, AAC was still receiving submissions via snail mail in hard copy and floppy disks. Editors mailed copies of manuscripts to reviewers. Staff copy edited papers by hand, with pencils, pens, correction tape, and rulers. Figures were submitted on regular or photo paper and were photographed to prepare them for publication. Online submission began in 2003, with review through the Rapid Review system. Most editors felt that the Rapid Review system, while being a significant improvement over paper, was limited in the ease with which reviewers could be identified and lacked convenient mechanisms for following the progress of manuscripts. As a result, the review system was switched to eJournalPress (eJP) in 2011, with significant improvements that led, perhaps not surprisingly, to reductions in several metrics around time to first response and time to publication. AAC continues to use eJP today.

Several other advanced features have been added to improve author experience, publication efficiency, and access over the past 2 decades. The first online AAC publication occurred in 1999. ASM hosting of supplemental material was introduced in 2005. Publish-ahead-of-print papers (“AAC Accepts”) were introduced in 2007. An open-access option for papers published in AAC was introduced in 2010, and in January 2015, online only publication began. In all cases, these evolutions were expertly managed by ASM publications staff, in particular directors of Journals Linda M. Illig (1982−2007), Barbara M. Goldman (2008−2018), and Melissa Junior (2018−present) and, for AAC specifically, Senior Production Editor Noel Lin (2003−present).

Two problems that frequently present themselves to scientific journals are reviewer fatigue and slow turnaround times for articles that are ultimately rejected (and therefore could have been submitted elsewhere if decisions were made earlier). One solution to this problem is to encourage editors to reject manuscripts they deem to be unacceptable to AAC for a variety of reasons (quality of science, scope, lack of novelty, etc.) without sending them for outside review. For understandable reasons, editors are frequently hesitant to make such decisions alone. The move to the eJP system facilitated a solution to this problem through its consultation function. Through eJP, any editor can easily consult a second editor regarding a “Reject without outside review” decision. The second editor has complete access to the paper and offers a response, allowing the managing editor to either reconsider the reject decision or to truthfully write to the author that a second editor concurred with the decision to reject without outside review. It would be an exaggeration to state that most authors are satisfied with these decisions, but at least they have saved a month or more in their ability to submit the papers elsewhere.

Concerns over terrorism elevated after the attacks of 9/11, and these concerns became particularly relevant to AAC after the subsequent anthrax attacks. In December 2001, all ASM journals began screening papers for anything deemed to have potential for bioterrorism. In 2007, the Journal of Virology added a question on the reviewer form asking reviewers to provide an assessment about dual use research of concern (DURC), a question later expanded to all journals. In 2014, ASM adopted a formal process for vetting manuscripts containing possible DURC before making a decision whether or not to publish the manuscript in its original form. The responsibility for making these determinations for AAC falls to the editor-in-chief of AAC.

A comparison of the “Scope” sections of the Instructions to Authors between 2000 and 2020 reveals much about how the journal has endeavored to sharpen its focus and relevance to its audience over those years. In 2000, the journal still considered (reluctantly) articles addressing cancer chemotherapy agents as within its scope. In 2020, such articles are not considered within AAC’s scope, nor are articles addressing immune modulating agents. Consideration for AAC publication now excludes unpurified natural products where the observed activity cannot be directly attributed to a specific component. On the pathogen side, AAC’s scope now specifically excludes microorganisms that are primarily pathogens for nonhuman species.

To focus AAC’s papers on compounds that had a chance to become actual drugs, AAC adopted what have been referred to as the “Rex rules” after John Rex, the editor who suggested them. These rules essentially state that if a compound is to be considered for an AAC manuscript, the authors must show some evidence that the compound could actually become a drug. Such evidence could include a combination of pharmacokinetic/pharmocodynamic studies and/or toxicity studies. These rules effectively distinguish between what is most appropriate for AAC and what is appropriate for a medicinal chemistry journal. They have subsequently been extended regarding peptide antimicrobials to require that a new peptide demonstrate a profile that is distinct from previously reported similar molecules and that it demonstrates reasonable pharmacokinetics and credible efficacy in an in vivo model.

Advances in science and the availability of large databases of nucleotide and protein sequences have also prompted evolution. In 2000, a manuscript describing a complete plasmid sequence would be readily publishable. In 2020, plasmid sequences require additional clinical, epidemiological, or molecular characterization that represents an advance in the field. Studies on enzymes such as β-lactamases will be considered only if the kinetic analysis is done on an enzyme in its native form (without any leader sequences or fusions used for purification)—reflecting concerns regarding an alteration of enzyme activity by the presence of His tags, etc. As an extension of AAC’s firm requirement that structures of compounds be revealed, it now also requires that quality control data for any in-house compounds used as comparators be presented to guarantee the quality of the comparator.

One change in scope that reflects the evolution in AAC more than most is the current policy on susceptibility studies. In the early years of AAC, susceptibility studies were in many respects its hallmark, at least in part because the 1970s and 1980s were periods of broad and active antimicrobial development by the pharmaceutical industry. The present scope section states that “Susceptibility studies describing novel findings or testing new agents, those with broad geographic reach, detailed mechanistic analysis and important epidemiological implications, will be given higher priority than those testing isolates from local regions, with limited analysis or with modest numbers of tested species or microorganisms.” In general, single center studies are no longer appropriate for AAC. AAC editors struggled over these decisions, especially since they tend to exclude studies from underresourced areas of the world where we want to encourage scientific investigation. The availability of another ASM journal (mSphere) that is appropriate for such studies made these decisions more palatable.

The past 2 decades have witnessed significant changes in many aspects of AAC. We hope that these changes have made the journal more relevant to the readership and augmented the acknowledged strengths of the journal historically. Without doubt, the journal will continue to evolve in response to changes in science and to the needs of our readers.

The views expressed in this article do not necessarily reflect the views of the journal or of ASM.