Journal of Critical Care 48 (2018) 357–371
Contents lists available at ScienceDirect
Journal of Critical Care journal homepage: www.journals.elsevier.com/journal-of-critical-care
Highly visible sepsis publications from 2012 to 2017: Analysis and comparison of altmetrics and bibliometrics Craig S. Jabaley, MD, Assistant Professor of Anesthesiology a,b,⁎, Robert F. Groff IV, MD, Assistant Professor of Anesthesiology a,b, Michael J. Stentz, MD, MS, Assistant Professor of Anesthesiology a, Vanessa Moll, PhD, DESA, Assistant Professor of Anesthesiology a, Grant C. Lynde, MD, MBA, Associate Professor of Anesthesiology a, James M. Blum, MD, FCCM, Assistant Professor of Anesthesiology a,b,c, Vikas N. O'Reilly-Shah, MD, PhD, Assistant Professor of Anesthesiology a,d a
Department of Anesthesiology, Emory University, 1750 Gambrell Dr, Atlanta, GA 30322, USA Anesthesiology Service Line, Division of Critical Care Medicine, Atlanta Veterans Affairs Medical Center, 1670 Clairmont Rd, Decatur, GA 30033, USA c Department of Biomedical Informatics, Emory University School of Medicine, 201 Bowman Dr, Atlanta, GA 30322, USA d Department of Anesthesiology, Children's Healthcare of Atlanta, 1405 Clifton Rd, Atlanta, GA 30329, USA b
a r t i c l e
i n f o
Available online xxxx Keywords: Critical care Sepsis Information dissemination Bibliometrics Information science Scholarly communication
a b s t r a c t Purpose: We sought to delineate highly visible publications related to sepsis. Within these subsets, elements of altmetrics performance, including mentions on Twitter, and the correlation between altmetrics and conventional citation counts were ascertained. Materials and Methods: Three subsets of sepsis publications from 2012 to 2017 were synthesized by the overall Altmetric.com attention score, number of mentions by unique Twitter users, and conventional citation counts. For these subsets, geolocated Twitter activity was plotted on a choropleth, the lag between publication date and altmetrics mentions was characterized, and correlations were examined between altmetrics performance and normalized conventional citation counts. Results: Of 57,152 PubMed query results, Altmetric.com data was available for 28,344 (49.6%). The top 50 publications by Altmetric.com attention score and Twitter attention represented a mix of original research and other types of work, garnering attention from Twitter users in 143 countries that was highly contemporaneous with publication. Altmetrics performance and conventional citation counts were poorly correlated. Conclusions: While unreliable to gauge impact or future citation potential, altmetrics may be valuable for parties who wish to detect and drive public awareness of research findings and may enable researchers to dynamically explore the reach of their work in novel dimensions. Published by Elsevier Inc.
1. Introduction Sepsis is a prevalent disease with significant morbidity and mortality that has accordingly been named a global health priority by the World Health Organization [1-3]. Prompt intervention is critical to mitigate shock resulting from the pathophysiologic immune response to
⁎ Corresponding author at: Emory University, Department of Anesthesiology, 1750 Gambrell Dr, T5L27, Atlanta, GA 30322. E-mail addresses:
[email protected] (C.S. Jabaley),
[email protected] (R.F. Groff),
[email protected] (M.J. Stentz),
[email protected] (V. Moll),
[email protected] (G.C. Lynde),
[email protected] (J.M. Blum),
[email protected] (V.N. O'Reilly-Shah).
https://doi.org/10.1016/j.jcrc.2018.09.033 0883-9441/Published by Elsevier Inc.
infection and preserve end-organ function [4-10]. Efforts within the medical community to hasten the diagnosis and standardize the treatment of sepsis have improved mortality over time in high-income countries; however, available evidence suggests a disproportionate degree of mortality among low and middle-income countries [1,11-18]. Awareness campaigns, such as World Sepsis Day and the Surviving Sepsis Campaign, have similarly aimed to improve the historically poor public awareness of sepsis [18-22]. Examining the dissemination of editorials, guidelines, research findings, and other publications is integral to improving the reach and impact of all such efforts in driving advancements in clinical care and sepsis awareness. Measuring the dissemination and broader visibility of publications geared toward clinicians and researchers presents numerous challenges.
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The burgeoning field of altmetrics has sought to develop nontraditional means of assessing publication visibility and discussion, such as citations by the lay media, mentions on Twitter and other social media outlets, and other forms of online attention and interaction [23-26]. While altmetrics have been rightly criticized as poor surrogates for scientific validity, research quality, and future citation potential, such data can highlight publications that rise to high levels of visibility [27,28]. Twitter in particular, with approximately 335 million active monthly users globally, has emerged as a popular forum for discussion of biomedical publications, interaction with authors, promotion of research efforts, and the conduct post-publication peer review. Engagement with social media is therefore increasingly championed for clinicians and researchers alike [29-31]. There are several providers of altmetrics data that attempt to ascertain and catalogue the performance of publications in these domains, and biomedical publishers now frequently display elements of altmetrics performance online. The adoption and display of altmetrics has largely outpaced the scientific community's understanding of their meaning and utility, which offers an important opportunity for critical examination in specific content areas. We sought to use altmetrics data provided by Altmetric.com (Altmetric; Digital Science, a subsidiary of Holtzbrinck Publishing Group, Stuttgart, Germany), the most ubiquitous provider of altmetrics data, and conventional citation counts to identify and describe a subset of highly cited clinical and mechanistic investigations about sepsis from 2012 to 2017 to elucidate their reach beyond the peer-reviewed scientific literature. This was motivated by the potential value offered by an exploratory, descriptive analysis in highlighting the complementary
roles that both conventional citations in the peer-reviewed literature and altmetrics can play in the evaluation of individual publications. We also hypothesized that there may be differences in the media coverage of publications with implications for daily clinical practice in sepsis management versus those seeking to explore underlying mechanisms, and that these differences would be reflected in altmetrics to a greater extent than in citation count. 2. Materials and methods An exemption from review was granted by the Emory University Institutional Review Board. Reporting follows the Strengthening the Reporting of Observational Studies in Epidemiology statement guidelines where applicable [32]. The general methodologic approach is summarized in Fig. 1 and was as follows: (1) identify all publications potentially related to sepsis during the dates of interest via a PubMed query, (2) extract altmetrics and conventional citation data for all identified publications, (3) synthesize the data by sorting and manual filtering to identify three subsets of high-performing publications, (4) extract additional altmetrics data for these subsets, and (5) conduct comparative analyses within tese subsets. 2.1. Altmetric.com data overview Altmetric.com, referred to herein as Altmetric, is one of several commercial providers offering nontraditional publication mention, social media discussion, and general online interaction metrics, which are
Fig. 1. Title: Approach to data extraction, synthesis, and analysis. API: application programming interface; HAI: healthcare-associated infection.
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commonly referred to as altmetrics. Further background discussion about altmetrics and technical details about Altmetric's methodologic approach are offered in an online supplement [Additional file 1, eMethods]. Altmetric terms these outlets attention sources. Tracking began in October 2011, and since that time the total number of tracked sources has grown [33]. Altmetric provides a weighted, arbitrary “attention score” incorporating mentions in mainstream and social media outlets, which at the time of data extraction was heavily weighted to favor mentions in mainstream media sources as the number thereof is multiplied by 8 when calculating the overall attention score [34]. Altmetric has an open application programming interface (API), which is a common means by which to access large databases online. Altmetric grants unrestricted access to its full database via keyed API calls upon reasonable investigator-initiated request, as was the case for this investigation. Twitter (Twitter Inc., San Francisco, CA USA) activity is cataloged by Altmetric in the open API as the number of unique users mentioning a publication at least once, as opposed to the total number of tweets, as one user may generate multiple tweets about the same publication. The overall attention score is weighted to de-emphasize the impact of certain types of Twitter accounts, such as those of publishers; however, raw unique user, tweet counts, and other Twitter data are available via the full API [35]. 2.1.1. Identification of publications potentially concerning sepsis With the ultimate aim of identifying a subset of highly-cited sepsis publications, PubMed was first queried on March 2, 2018 to broadly identify all publications that could concern sepsis using the following search query: ("sepsis"[MeSH Terms] OR "sepsis"[All Fields]) OR septic[All Fields] OR ("septicaemia"[All Fields] OR "septicemia"[All Fields]) OR OR ("bacteraemia"[All Fields] OR "bacteremia"[MeSH Terms] OR "bacteremia"[All Fields]) OR bacteremic[All Fields] OR bacteraemic [All Fields] OR SIRS[All Fields] OR systemic inflammatory response [All Fields] OR ("systemic inflammatory response syndrome"[MeSH Terms] OR ("systemic"[All Fields] AND "inflammatory"[All Fields] AND "response"[All Fields] AND "syndrome"[All Fields]) OR "systemic inflammatory response syndrome"[All Fields]) AND ("2012/ 01/01"[PDAT] : "2017/12/31"[PDAT]). The data extraction date was selected to allow for 60 full days following 12/31/2017. Previous investigations have demonstrated that mentions in nontraditional outlets are highly contemporaneous with publication, and that a 60-day window is sufficient to capture the majority of contributors to Altmetric score for a given publication [36]. PubMed identifiers (PMIDs) from search results were extracted for further analysis as described below. 2.1.2. Preliminary altmetrics and conventional citation data extraction Using R version 3.4.1 (R Core Team, Vienna, Austria) in RStudio version 1.0.143 (RStudio Inc., Boston, MA, ISA), altmetrics data from Altmetric for all PMIDs were extracted via the open API and parsed with the rAltmetric package for R. For those PMIDs with any Altmetric data, corresponding conventional citation data were manually batch extracted from Web of Science (Clarivate Analytics, Philadelphia, PA, USA) and Scopus (Elservier, Amsterdam, Netherlands). 2.1.3. Data synthesis and identification of publication subsets At the time of data extraction, the overall Altmetric attention score was heavily weighted to favor mainstream media mentions [Additional file 1, eMethods] [34]. Moreover, the sources tracked by Altmetric have changed over time such that publications prior to December 2015 are likely to have fewer associated news media mentions and thus potentially lower overall scores [33]. Accordingly, the Altmetric data were sorted to identify the top 50 publications by overall Altmetric attention
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scores and top 50 publications by Twitter user activity as the latter is more likely to be consistent over the studied timeframe. These lists were independently reviewed by two authors (CSJ and RFG) to exclude those primarily concerning antimicrobial resistance, antimicrobial stewardship, those confined to specifics of a single pathogens (i.e. dengue, Ebola, HIV/AIDS, malaria, typhoid, Zika, and “other”), healthcare-acquired infections, and those generally unrelated to sepsis. Clinical and mechanistic publications about sepsis, systemic inflammatory response syndrome, or other investigations primarily involving critically ill septic patients were considered relevant. A list of all highperforming but excluded publications is available online as a supplement [see Additional file 2]. Mechanistic publications are those seeking to describe biochemical and other such mechanisms underlying systemic inflammation and the dysregulated host response to infection associated with sepsis. Any discordant determinations were refereed by a third author (VORS). Publications sorted by conventional citation count were similarly filtered to generate a top 50 list. Conventional citation counts from Web of Science were used for ranking, and the Scopus citation count was used to resolve ties. Although citation counts from Web of Science have been historically considered authoritative, alternative databases, such as Scopus, capture a larger number of peer-reviewed outlets, and results from both sources are presented to facilitate comparisons [37]. 2.1.4. Additional altmetrics data extraction for publication subsets For the subset of 50 publications with the greatest number of unique Twitter users mentioning the publication at least once (referred to as Twitter user activity subsequently), complete Altmetric data were fetched via the full API and parsed to extract all associated Twitter data of interest, including tweet timestamps, username, ID, geolocation, and number of followers. For the subset of 50 publications representing those with the highest associated overall Altmetric attention score (described below), complete Altmetric data were similarly extracted to determine the timestamp of each mention in mainstream media sources. For the subset of 51 publications with the highest conventional citation counts, journal impact factors (IFs) were extracted on 8/24/2018 from Journal Citation Reports (Clarivate Analytics, Philadelphia, PA, USA) for a post-hoc analysis. Publications from all top 50 lists were compared against annual data provided by Altmetric describing the top 100 articles by overall attention score, which were available for 2013–2017 at the time of data extraction [38]. 2.1.5. Comparative analyses of publication subsets Figures were generated in R using the ggplot2, ggpmisc, and rworldmap packages [39-41]. Means are presented as ± standard deviation. 2.1.5.1. Unique twitter user activity by geographic region. Counts of geolocation (two-character ISO 3166-1 alpha-2 code) for each unique user having tweeted about any publication on the Twitter top 50 list was plotted on a choropleth with a log-adjusted scale to depict Twitter activity related to sepsis by geographic region. As Altmetric data is provided on a per-publication basis, duplicate entries for a single user were present when users tweeted about more than one of the studied publications within the dates of interest. These duplicate entries were removed, using the entry with the largest follower count to define the geolocation for that Twitter user. Follower counts typically increase over time, and larger values are likely reflective of more recent geolocation data. 2.1.5.2. Publication to altmetrics mention lag. Density plots with associated rug plots were generated to depict the lag between publication and (a) Twitter mentions of the top 50 publications by Twitter user activity and (b) mainstream media mentions of the top 50 publications by overall Altmetric attention score. Due to low
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3.2. Unique twitter user activity by geographic region incidence, mentions 30 days before the recorded date of publication or 365 days after were excluded. Data used for figure generation are available in an online supplement [see Additional file 4].
2.1.5.3. Altmetrics versus conventional citation correlation. The correlation between (a) overall Altmetric attention score and (b) Twitter user activity with conventional citation counts was determined by linear modeling for the top 50 publications by conventional citation count. This converse analysis using top 50 publications by Altmetric attention score was not performed as publications with high altmetrics performance may be too recent to demonstrate a meaningful number of citations in the peer-reviewed literature. These relationships were also visually examined through two-dimensional density estimate plots. Publications that were either guidelines, consensus definitions, or editorial in nature as judged by abstract review were initially examined and excluded from analysis as related citation counts were widely outlying thus unduly influencing the regression and measures of its fit [Additional file 1, Supplemental Fig. 1] [42]. For example, practice guidelines garnered many citations but lower altmetrics performance as they are likely less buzz-worthy while editorials garnered few citations but better altmetrics performance [43]. Data used for figure generation are available in supplemental online files with excluded publications denoted accordingly [Additional file 5]. A post-hoc analysis was conducted similarly examining altmetrics performance and conventional citations per year multiplied by the associated journal IF for the year of publication.
3. Results 3.1. Data extraction and synthesis Results of data extraction, synthesis, and analysis are outlined in Fig. 1. Of 57,152 PubMed query results, Altmetric attention score data was available for 28,344 (49.6%), which reflects that about half of these publications had an identified degree of visibility beyond the peer-reviewed literature. Post-hoc analysis of citation counts for publications with and without Altmetric data demonstrated more favorable performance of the former [Additional file 1, Supplemental Fig. 2]. The top 50 publications by overall Altmetric attention score and Twitter user activity are presented in Tables 1 and 2 and represent a mix of editorials, reviews, consensus definitions, treatment guidelines, clinical investigations, and mechanistic investigations. Unusual case reports and publications with a humorous slant were also identified, suggesting that altmetrics performance may partially reflect the extent to which a publication is interesting or engaging but not necessarily longitudinally impactful [44-47]. Twenty nine publications overlapped among those included in Tables 1 and 2. Of the non-overlapping publications, those on the Altmetric attention score top 50 list had more mainstream media mentions (mean = 49 ± 17.3) than did those on the Twitter user activity top 50 list (mean = 2.1 ± 2.9), confirming that the Altmetric attention score is driven in part by heavy weighting of mainstream media mentions. Notably, one sepsis-related publication, the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3), appeared on the available annual Altmetric Top 100 lists (#19/100 in 2016) [48]. The top 49 of 50 publications by conventional citation count as reported by Web of Science and Scopus overlapped but with discordant rankings (Table 3). Reflecting the dynamic and immediate nature of altmetrics versus conventional citations, top publications by overall attention score, unique Twitter user activity, and conventional citations varied in their mean duration from publication to data extraction (691 ± 473, 643 ± 493, and 1611 ± 457 days respectively).
For the top 50 publications by Twitter user activity, 13,542 unique users made 25,108 tweets citing at least one of the publications. Geolocation data was available for 8,349 of the unique users, which spanned 143 geographic regions as depicted in Fig. 2 [Additional file 3]. A logarithmic scale was employed for plotting as a disproportionate number of users were located in the United States, Great Britain, Spain, Canada, Australia, Japan, Mexico, and India. 3.3. Publication to altmetrics mention lag For mainstream media mentions of top 50 publications by overall Altmetric attention score, and tweets mentioning the top 50 publications by Twitter user activity, mentions were most common close to the time of publication (Fig. 3). Mentions via Twitter were evident before the cataloged date of publication, which likely reflects discussion of publications released electronically ahead of print. This analysis suggests that discussion about publication in dimensions captured by altmetrics data aggregators is highly contemporaneous with publication. 3.4. Altmetrics versus conventional citation correlation For the subset of 51 publications with the highest traditional citation counts, 5 publications met exclusion criteria as outlined in the methods (Fig. 1) [see also Additional file 5]. For the remaining 46, both the overall Altmetric attention score and Twitter user activity were both poorly correlated with the Web of Science citation count (expressed as citations per year) as depicted with linear modeling and two-dimensional density estimates in Fig. 4 [49]. Publications concerning the mechanisms of sepsis and systemic inflammation had lower overall altmetrics performance, and correlations between these and conventional citation counts were lower than those for clinically oriented publications. Factoring journal IF against conventional citations per year modestly improved the strength of this correlation for mechanistic publications but worsened the correlation for clinical publications [Additional file 1, Supplemental Fig. 3]. 4. Discussion Using a replicable methodology, we were able to delineate subsets of highly visible publications about sepsis as assessed by altmetrics and conventional bibliometrics. When examining these subsets, we found that altmetrics correlate poorly with later citations in the peerreviewed literature, which is consistent with previous investigations [27,50-52]. Similarly, the relatively poor performance of mechanistic basic science research in altmetrics dimensions compared to more clinically-oriented publications, including editorials, is also consistent with previous large-scale altmetrics investigations [43,53]. This likely reflects the extent to which certain publications provoke discussion or reflection but do not ultimately demonstrate a continued impact on further scientific investigation [54]. Although altmetrics were poorly correlated with eventual citations in the peer-reviewed literature for the studied subsets of publications, online discussions at the time of publication offer an opportunity to raise public awareness about health and disease and of research findings within the scientific community. On Twitter, for example, discussion about the studied sepsis publications was a global phenomenon. We found that mentions or discussions in mainstream media outlets and Twitter were highly contemporaneous relative to the time of publication and tapered rapidly, which is again consistent with previous findings, and highlights the relatively narrow window for promotion efforts [55]. Practically speaking, this highlights the need for a more dynamic method for altmetrics assessment such that researchers, public agencies, or other interested parties can ascertain where and when these
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Table 1 Title – Top 50 Publications by Overall Altmetric.com Attention Score. Altmetric Attention Rank (Score)
Title
Journal
Year Published (Days Until Extraction)
Mainstream Media Mentions
Twitter Rank of 50 (User Count)
Web of Scopus Full Science Citations Reference Citations Number
1 (2629)
The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3) Time to treatment and mortality during mandated emergency care for sepsis Recognizing sepsis as a global health priority — a WHO resolution A randomized synbiotic trial to prevent sepsis among infants in rural India Hydrocortisone, vitamin C and thiamine for the treatment of severe sepsis and septic shock: a retrospective before-after study Vibrio vulnificus septic shock due to a contaminated tattoo Hospital deaths in patients with sepsis from 2 independent cohorts Opposing effects of fasting metabolism on tissue tolerance in bacterial and viral inflammation How bacterial pathogens colonize their hosts and invade deeper tissues Genomic responses in mouse models poorly mimic human inflammatory diseases Prehospital antibiotics in the ambulance for sepsis: a multicentre, open label, randomised trial Management of sepsis and septic shock Early, goal-directed therapy for septic shock — a patient-level meta-analysis State sepsis mandates — a new era for regulation of hospital quality Evaluating the impact of a computerized surveillance algorithm and decision support system on sepsis mortality Benchmarking the incidence and mortality of severe sepsis in the United States Effect of hydrocortisone on development of shock among patients with severe sepsis: the HYPRESS randomized clinical trial Vitamin C revisited Genomic responses in mouse models greatly mimic human inflammatory diseases Surviving Sepsis Campaign: international guidelines for management of sepsis and septic shock: 2016 Diagnostic accuracy of a host gene expression signature that discriminates clinical severe sepsis syndrome and infection-negative systemic inflammation among critically ill children Serial procalcitonin predicts mortality in severe sepsis patients Treating the host response to emerging virus diseases: lessons learned from sepsis, pneumonia, influenza and Ebola Robust classification of bacterial and viral infections via integrated host gene expression diagnostics Trends in the epidemiology of pediatric severe sepsis
JAMA
2016 (710)
77
1 (2248)
1272
1373
[15]
N Engl J Med
2017 (255)
123
2 (1132)
41
41
[71]
N Engl J Med
2017 (218)
60
4 (850)
10
11
[2]
Nature
2017 (170)
68
10 (663)
17
15
[72]
CHEST
2016 (428)
70
16 (427)
35
33
[73]
BMJ Case Rep JAMA
2017 (248) 2014 (1356)
98 75
(33) (155)
0 124
2 135
[44] [74]
Cell
2016 (512)
55
33 (247)
40
46
[75]
Microbes Infect Proc Natl Acad Sci USA Lancet Respir Med JAMA N Engl J Med
2015 (1100)
0
3 (943)
73
80
[76]
2013 (1817)
17
17 (399)
1220
1229
[77]
2017 (93)
0
5 (751)
0
0
[78]
2017 (379) 2017 (316)
2 5
6 (747) 7 (722)
15 30
15 39
[9] [10]
N Engl J Med
2017 (255)
44
32 (249)
4
4
[79]
J Am Med Inform Assoc Crit Care Med
2016 (618)
65
(20)
3
3
[80]
2013 (1803)
57
(25)
393
411
[81]
JAMA
2016 (487)
3
11 (619)
37
43
[82]
Crit Care Proc Natl Acad Sci USA Intensive Care Med Crit Care Med
2014 (1276) 2014 (1278)
59 6
(13) 8 (698)
30 166
39 156
[83] [84]
2017 (380)
2
12 (547)
189
198
[22]
2016 (500)
59
(2)
2
2
[85]
Crit Care Med 2017 (338) Ann Transl 2016 (458) Med Sci Transl Med 2016 (576)
54 55
(38) (0)
15 6
13 6
[86] [87]
44
(101)
32
32
[88]
Pediatr Crit Care Med J Artif Organs
2013 (1652)
50
(10)
127
131
[89]
2017 (241)
51
(6)
1
1
[90]
JAMA
2016 (710)
7
15 (444)
325
343
[91]
Pediatr Crit Care Med
2013 (1554)
49
(2)
33
30
[92]
eLife Br Med J Front Endocrinol N Engl J Med JAMA BMJ Case Rep
2017 (388) 2016 (620) 2016 (592)
34 0 44
(111) 9 (665) (5)
0 43 6
1 51 0
[45] [93] [94]
2013 (1618) 2015 (899) 2016 (582)
2 3 41
18 (390) 13 (480) (11)
910 76 0
967 42 3
[95] [96] [47]
Nat Med N Engl J Med Eur J Prev Cardiol JAMA
2014 (1237) 2014 (1417) 2017 (397)
26 5 42
(74) 30 (253) (14)
72 719 2
83 982 3
[97] [98] [99]
2017 (318)
18
26 (299)
5
7
[100]
2 (1811) 3 (1086) 4 (1012) 5 (998)
6 (825) 7 (729) 8 (669) 9 (652) 10 (648) 11 (575) 12 (552) 13 (530) 14 (528) 15 (523) 16 (482) 17 (482)
18 (477) 19 (475) 20 (459) 21 (458)
22 (454) 23 (434) 24 (415) 25 (407) 26 (405) 27 (400)
28 (391)
29 (388) 30 (386) 31 (373) 32 (371) 33 (366) 34 (359) 35 (350) 36 (337) 37 (329) 38 (329)
Extracorporeal cytokine elimination as rescue therapy in refractory septic shock: a prospective single-center study Assessment of clinical criteria for sepsis: for the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3) Functional outcomes in pediatric severe sepsis: further analysis of the researching severe sepsis and organ dysfunction in children: a global perspective trial A molecular portrait of maternal sepsis from Byzantine Troy Sepsis: pathophysiology and clinical management The role of ACTH and corticosteroids for sepsis and septic shock: an update Severe sepsis and septic shock Septic shock: advances in diagnosis and treatment Lick of death: Capnocytophaga canimorsus is an important cause of sepsis in the elderly An extracorporeal blood-cleansing device for sepsis therapy A randomized trial of protocol-based care for early septic shock Severe infections and subsequent delayed cardiovascular disease Association between US norepinephrine shortage and mortality
(continued on next page)
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Table 1 (continued) Altmetric Attention Rank (Score) 39 (326) 40 (324) 41 (321) 42 (314) 43 (310) 44 (305)
45 (278) 46 (278) 47 (266) 48 (263)
49 (244) 50 (241)
Title
among patients with septic shock Early identification of sepsis in hospital inpatients by ward nurses increases 30-day survival A point-of-care microfluidic biochip for quantification of CD64 expression from whole blood for sepsis stratification Surviving Sepsis Campaign: international guidelines for management of sepsis and septic shock 2016 Proportion and cost of unplanned 30-day readmissions after sepsis compared with other medical conditions Histidine-rich glycoprotein prevents septic lethality through regulation of immunothrombosis and inflammation Effect of an early resuscitation protocol on in-hospital mortality among adults with sepsis and hypotension: a randomized clinical trial Gone fishing in a fluid trial The biomarker GlycA is associated with chronic inflammation and predicts long-term risk of severe infection qSOFA does not replace SIRS in the definition of sepsis Developing a new definition and assessing new clinical criteria for septic shock: for the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3) Levosimendan for the prevention of acute organ dysfunction in sepsis Engineered liposomes sequester bacterial exotoxins and protect from severe invasive infections in mice
Journal
Year Published (Days Until Extraction)
Mainstream Media Mentions
Twitter Rank of 50 (User Count)
Scopus Full Web of Citations Reference Science Number Citations
Crit Care
2016 (546)
10
22 (345)
9
8
[101]
Nat Commun
2017 (214)
36
(31)
0
0
[102]
Crit Care Med
2017 (381)
3
21 (348)
159
174
[18]
JAMA
2017 (376)
12
24 (316)
7
7
[103]
EBioMedicine
2016 (609)
39
(11)
1
1
[104]
JAMA
2017 (128)
1
14 (453)
7
6
[105]
Crit Care Resusc Cell Systems
2016 (703)
2
20 (361)
0
2
[46]
2015 (855)
31
(78)
32
27
[106]
Cell Syst JAMA
2016 (565) 2016 (710)
0 13
19 (363) 42 (187)
22 237
31 246
[107] [108]
N Engl J Med
2016 (484)
6
29 (283)
39
47
[109]
Nat Biotechnol
2014 (1188)
20
(55)
34
32
[110]
opportunities are occurring. Concurrently, altmetrics can help the scientific and medical community better understand retrospectively how and why certain publications garner more attention and discussion than do others [56]. Similar investigations will be critical to furthering our understanding of knowledge dissemination in the public, including engagement and information use, as it pertains to both sepsis and other important aspects of critical care medicine. Sepsis research has been previously shown to be heavily cited compared to other topics within the critical care literature [57,58]. Similar to previous findings from a bibliometric analysis concerning sepsis literature published from 1974 to 2008, many highly-cited publications as measured by both alternative and conventional metrics were published in high IF journals targeted toward a broad medical readership [59]. However, the present work demonstrates that publications can rise to high levels of visibility even from subspecialty journals. Again highlighting the potential value of this methodology, further examination of publications outside high-impact outlets with high levels of attention may help researchers better understand how to promote their work and help to delineate the differential role of content versus promotion as it relates to altmetrics performance [60-62]. Moreover, engagement with sources reflected in altmetrics may evolve as a necessary skill set in the researcher's armamentarium should grant funders begin to consider them despite accepted limitations [63,64]. Familiarity with Twitter is similarly becoming an increasingly important skillset for researchers given its utilization as a nearimmediate post-publication peer review medium [65]. The geographic distribution of Twitter users tweeting about sepsis was relatively consistent with the overall distribution of the Twitter user base [66]. As noted by other investigators, content analysis will be an important next step to better delineate when and how Twitter is used for meaningful discussion given the potential impact of automated “bot” accounts and recent observation that less than 10% of tweets about scientific publications contain meaningful content [67-69]. The present work has several strengths. We utilized a broad approach to the identification of clinical and mechanistic publications
relevant to sepsis that may not have been otherwise elucidated by a more focused approach. By comparing publications with high conventional citation counts against those with high levels of attention as measured by altmetrics, a more complete picture of the overall body of highly-visible sepsis literature can be developed. Within the critical care literature, we selected sepsis as an altmetrics test case as this body of work is likely familiar to a diverse group of clinicians and researchers in the field. We do not know the relative roles played by knowledge creation versus information dissemination in driving welldemonstrated improvements in sepsis outcomes, and the approach used here may help to delineate these roles moving forward. Our investigation has certain limitations. Analyses were limited to small subsets of highly visible sepsis publications given the challenges of identifying publications truly related to sepsis with standard Boolean search queries alone. We utilized data provided by Altmetric as the only source of altmetrics performance as its data are used in part by other providers of altmetrics and have been widely adopted by publishers, therefore rendering it familiar to researchers and clinicians alike [26]. Methods used for data gathering by altmetrics providers are heterogeneous and sometimes obfuscated to protect intellectual property, and these considerations complicate comparisons across providers [26,70]. We have offered additional discussion of the methodology underlying Altmetric data gathering in Additional file 1, eMethods and present all analyzed data in the supplemental files. While comparison of data across altmetrics providers was beyond the scope of the present investigation, our findings presented in the supplemental analyses are consistent with those of recent investigations [50-52]. The overall Altmetric attention score is influenced by variable go-live dates of elements used in its calculation, arbitrary weighting for attention sources, and changing approaches to score calculation [Additional file 1, eMethods]. Although limited by these considerations, we included the attention score in our analyses owing to its frequent display by biomedical publishers and the need for critical examination. By examining Twitter user mentions, we sought to explore a more consistent dimension of altmetrics [27]. Both altmetrics and conventional citations are
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Table 2 Title – Top 50 Publications by Unique Twitter User Activity. Twitter User Rank (Num Users)
Title
Journal
Year Published (Days Until Extraction)
Mainstream Media Mentions
Altmetric Attention Score Rank (Raw Sore)
Web of Scopus Full Science Citations Reference Citations Number
1 (2248)
The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3) Time to treatment and mortality during mandated emergency care for sepsis How bacterial pathogens colonize their hosts and invade deeper tissues Recognizing sepsis as a global health priority — a WHO resolution Prehospital antibiotics in the ambulance for sepsis: a multicentre, open label, randomised trial
JAMA
2016 (710)
77
1 (2629)
1272
1373
[15]
N Engl J Med Microbes Infect N Engl J Med Lancet Respir Med JAMA N Engl J Med Proc Natl Acad Sci USA Br Med J Nature
2017 (255)
123
2 (1811)
41
41
[71]
2015 (1100)
0
9 (652)
73
80
[76]
2017 (218)
60
3 (1086)
10
11
[2]
2017 (93)
0
11 (575)
0
0
[78]
2017 (379) 2017 (316)
2 5
12 (552) 13 (530)
15 30
15 39
[9] [10]
2014 (1278)
6
19 (475)
166
156
[84]
2016 (620) 2017 (170)
0 68
30 (386) 4 (1012)
43 17
51 15
[93] [72]
JAMA
2016 (487)
3
17 (482)
37
43
[82]
Intensive Care Med JAMA JAMA
2017 (380)
2
20 (459)
189
198
[22]
2015 (899) 2017 (128)
3 1
33 (366) 44 (305)
76 7
42 6
[96] [105]
JAMA
2016 (710)
7
27 (400)
325
343
[91]
CHEST
2016 (428)
70
5 (998)
35
33
[73]
Proc Natl Acad Sci USA N Engl J Med Crit Care Crit Care Resusc Crit Care Med Crit Care
2013 (1817)
17
10 (648)
1220
1229
[77]
2013 (1618)
2
32 (371)
910
967
[95]
2016 (565) 2016 (703)
0 2
47 (266) 45 (278)
22 0
31 2
[107] [46]
2017 (381)
3
41 (321)
159
174
[18]
2016 (546)
10
39 (326)
9
8
[101]
Crit Care
2015 (963)
0
(222)
61
63
[111]
JAMA
2017 (376)
12
42 (314)
7
7
[103]
Intensive Care Med
2017 (60)
0
(219)
0
0
[112]
JAMA
2017 (318)
18
38 (329)
5
7
[100]
JAMA N Engl J Med N Engl J Med N Engl J Med JAMA
2017 (198) 2017 (239)
0 1
(196) (196)
0 3
0 4
[113] [8]
2016 (484)
6
49 (244)
39
47
[109]
2014 (1417)
5
36 (337)
719
982
[98]
2013 (1549)
2
(215)
216
264
[114]
2017 (255)
44
14 (528)
4
4
[79]
2016 (512)
55
8 (669)
40
46
[75]
2 (1132) 3 (943) 4 (850) 5 (751)
6 (747) 7 (722) 8 (698)
9 (665) 10 (663) 11 (619)
12 (547) 13 (480) 14 (453)
15 (444)
16 (427)
17 (399)
Management of sepsis and septic shock Early, goal-directed therapy for septic shock — a patient-level meta-analysis Genomic responses in mouse models greatly mimic human inflammatory diseases Sepsis: pathophysiology and clinical management A randomized synbiotic trial to prevent sepsis among infants in rural India Effect of hydrocortisone on development of shock among patients with severe sepsis: the HYPRESS randomized clinical trial Surviving Sepsis Campaign: international guidelines for management of sepsis and septic shock: 2016 Septic shock: advances in diagnosis and treatment Effect of an early resuscitation protocol on in-hospital mortality among adults with sepsis and hypotension: a randomized clinical trial Assessment of clinical criteria for sepsis: for the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3) Hydrocortisone, vitamin c and thiamine for the treatment of severe sepsis and septic shock: a retrospective before-after study Genomic responses in mouse models poorly mimic human inflammatory diseases
18 (390)
Severe sepsis and septic shock
19 (363) 20 (361)
qSOFA does not replace SIRS in the definition of sepsis Gone fishing in a fluid trial
21 (348)
Surviving Sepsis Campaign: international guidelines for management of sepsis and septic shock 2016 Early identification of sepsis in hospital inpatients by ward nurses increases 30-day survival A positive fluid balance is an independent prognostic factor in patients with sepsis Proportion and cost of unplanned 30-day readmissions after sepsis compared with other medical conditions Polymyxin B-immobilized hemoperfusion and mortality in critically ill adult patients with sepsis/septic shock: a systematic review with meta-analysis and trial sequential analysis Association between US norepinephrine shortage and mortality among patients with septic shock In treating sepsis, questions about timing and mandates Management of septic shock
22 (345) 23 (320) 24 (316) 25 (310)
26 (299) 27 (286) 28 (284) 29 (283) 30 (253) 31 (250)
32 (249) 33 (247)
Levosimendan for the prevention of acute organ dysfunction in sepsis A randomized trial of protocol-based care for early septic shock Effects of fluid resuscitation with colloids vs crystalloids on mortality in critically ill patients presenting with hypovolemic shock: the CRISTAL randomized trial State sepsis mandates — a new era for regulation of hospital N Engl J quality Med Opposing effects of fasting metabolism on tissue tolerance in Cell bacterial and viral inflammation
(continued on next page)
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C.S. Jabaley et al. / Journal of Critical Care 48 (2018) 357–371
Table 2 (continued) Twitter User Rank (Num Users)
Title
Journal
Year Published (Days Until Extraction)
Mainstream Media Mentions
Altmetric Attention Score Rank (Raw Sore)
Scopus Full Web of Citations Reference Science Number Citations
34 (245)
Effect of dexmedetomidine on mortality and ventilator-free days in patients requiring mechanical ventilation with sepsis: a randomized clinical trial High versus low blood-pressure target in patients with septic shock Albumin replacement in patients with severe sepsis or septic shock Early goal-directed resuscitation of patients with septic shock: current evidence and future directions Trial of short-course antimicrobial therapy for intraabdominal infection. Effect of early vasopressin vs norepinephrine on kidney failure in patients with septic shock: the VANISH randomized clinical trial The timing of early antibiotics and hospital mortality in sepsis
JAMA
2017 (318)
3
(183)
5
5
[115]
N Engl J Med N Engl J Med Critical Care N Engl J Med JAMA
2014 (1417)
2
(236)
274
306
[116]
2014 (1417)
3
(222)
268
303
[117]
2015 (889)
0
(165)
23
23
[118]
2015 (988)
6
(220)
124
127
[119]
2016 (549)
8
(210)
43
44
[120]
35 (241) 36 (238) 37 (232) 38 (199) 39 (198)
40 (191)
41 (189) 42 (187)
43 (176) 44 (176) 45 (175)
46 (168)
47 (164) 48 (163)
49 (161) 50 (159)
Corticosteroids in septic shock: a systematic review and network meta-analysis Developing a new definition and assessing new clinical criteria for septic shock: for the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3) Hydroxyethyl starch 130/0.4 versus ringer's acetate in severe sepsis Adequate antibiotic therapy prior to ICU admission in patients with severe sepsis and septic shock reduces hospital mortality The impact of timing of antibiotics on outcomes in severe sepsis and septic shock: a systematic review and meta-analysis Prognostic accuracy of Sepsis-3 criteria for in-hospital mortality among patients with suspected infection presenting to the emergency department Incidence and trends of sepsis in US hospitals using clinical vs claims data, 2009–2014 American College of Critical Care Medicine clinical practice parameters for hemodynamic support of pediatric and neonatal septic shock Identifying paediatric sepsis: the difficulties in following recommended practice and the creation of our own pathway The value of blood lactate kinetics in critically ill patients: a systematic review
Am J Respir Crit Care Med Crit Care
2017 (310)
1
(147)
0
5
[121]
2017 (63)
0
(129)
9
7
[122]
JAMA
2016 (710)
13
48 (263)
237
246
[108]
N Engl J Med Crit Care
2012 (2046)
4
(223)
798
930
[123]
2015 (890)
0
(117)
15
16
[124]
Crit Care Med
2015 (952)
1
(148)
70
81
[125]
JAMA
2017 (381)
4
(176)
51
49
[126]
JAMA
2017 (142)
10
(185)
7
6
[127]
Crit Care Med
2017 (246)
0
(121)
17
13
[128]
Arch Dis Child Crit Care
2017 (153)
0
(120)
0
0
[129]
2016 (538)
0
(101)
14
22
[130]
Table 2 Caption – Unique Twitter user activity is defined as the number of unique users having mentioned a publication at least once.
dynamic, which can confound unplanned analyses. We attempted to mitigate this problem through a predefined analysis plan and bulk extraction of data on a single date.
Consent for publication
5. Conclusions
Availability of data and materials
While altmetrics data are now routinely displayed by many biomedical publishers, the rise of such data has largely outpaced their defined utility and the collective conception their limitations [70]. Although dubious surrogates of eventual research impact, altmetrics are an easily accessible and dynamic means by which to ascertain attention to publications such that discussion, promotion, awareness efforts can be deployed in a timely and effective manner. Additionally, altmetrics may enable researchers to better understand the reach of their work sooner than would otherwise be reflected by citations in the peerreviewed literature, including publications promoting sepsis awareness.
Dr. Jabaley had full access to all of the data subsets extracted for use in the study and takes responsibility for the integrity of the extracted data subsets and the accuracy of their analysis. The full dataset used under license to conduct this study is available from Altmetric.com, but restrictions apply to the availability of these data given their commercial nature. The aggregate data subsets generated and/or analyzed during the current study are included in this published article and its supplementary information files with permission from Altmetric.com.
Ethics approval and consent to participate
The authors declare that they have no competing interests. Altmetric.com granted Dr. Jabaley unrestricted access to their database via an application programming interface in response to an investigator-initiated request but provided no conceptual or material support. Dr. Blum reported an equity stake in Intensix (Netanya, Israel).
A written exemption from review was granted by the Emory University Institutional Review Board as the present investigation does not constitute research with human subjects.
Not applicable.
Competing interests
C.S. Jabaley et al. / Journal of Critical Care 48 (2018) 357–371
365
Table 3 – Top 50 Publications by Conventional Citation Counts. Web of Science Rank (Citations)
Scopus Title Rank (Citations)
Journal
Year Published (Days Until Extraction)
Overall Altmetric Score Rank of 50 (Raw Score)
Mainstream Media Mentions
Twitter Rank of 50 (User Count)
Classification Full Reference Number
1 (2522)
2 (2007)
Crit Care Med
2013 (1827)
(94)
0
(59)
Clinical
[131]
2 (1711)
1 (2968)
Intensive Care Med
2013 (1829)
(44)
0
(28)
Clinical
[132]
3 (1272)
3 (1373)
JAMA
2016 (710)
1 (2629)
77
1 (2248)
Clinical
[15]
4 (1220)
4 (1229)
2013 (1817)
10 (648)
17
17 (399)
Mechanistic
[77]
5 (910)
6 (967)
2013 (1618)
32 (371)
2
18 (390)
Clinical
[95]
6 (798)
7 (930)
2012 (2046)
(223)
4
43 (176)
Clinical
[123]
7 (754)
8 (844)
2012 (2120)
(1)
0
(1)
Mechanistic
[133]
8 (719)
5 (982)
2014 (1417)
36 (337)
5
30 (253)
Clinical
[98]
9 (597)
10 (626)
2012 (2120)
(1)
0
(2)
Mechanistic
[134]
10 (542)
9 (712)
2014 (1220)
(96)
1
(28)
Clinical
[135]
11 (530)
11 (596)
2012 (2073)
(114)
0
(102)
Clinical
[136]
12 (460)
13 (510)
2015 (1053)
(115)
1
(75)
Clinical
[137]
13 (423)
14 (439)
2013 (1540)
(24)
0
(38)
Mechanistic
[138]
14 (393)
16 (411)
2013 (1803)
16 (482)
57
(25)
Clinical
[81]
15 (388)
15 (415)
2013 (1799)
(15)
0
(19)
Mechanistic
[139]
16 (357)
17 (361)
2013 (1858)
(4)
0
(1)
Mechanistic
[140]
17 (345)
18 (357)
2013 (1653)
(24)
0
(37)
Mechanistic
[141]
18 (325)
19 (343)
2016 (710)
27 (400)
7
15 (444)
Clinical
[91]
19 (319)
12 (523)
2014 (1402)
(184)
11
(126)
Clinical
[11]
20 (303)
20 (343)
2013 (1828)
(47)
0
(47)
Clinical
[142]
21 (279)
25 (291)
2012 (2023)
(2)
0
(2)
Mechanistic
[143]
22 (278)
27 (287)
2015 (870)
(94)
8
(35)
Mechanistic
[144]
23 (277)
23 (297)
2013 (1780)
(26)
0
(4)
Clinical
[145]
24 (274)
21 (306)
2014 (1417)
(236)
2
35 (241)
Clinical
[116]
25 (270)
30 (279)
2013 (1603)
(81)
9
(24)
Mechanistic
[146]
26 (268)
24 (292)
2012 (2276)
(0)
0
(2)
Clinical
[147]
Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2012 Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock, 2012 The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3) Genomic responses in mouse models poorly mimic human inflammatory diseases Severe sepsis and septic shock
Proc Natl Acad Sci USA N Engl J Med Hydroxyethyl starch 130/0.4 versus N Engl J ringer's acetate in severe sepsis Med Nitric oxide synthases: regulation and Eur Heart function J A randomized trial of protocol-based care N Engl J for early septic shock Med Physiol Physiological implications of hydrogen Rev sulfide: a whiff exploration that blossomed Goal-directed resuscitation for patients N Engl J with early septic shock Med Drotrecogin alfa (activated) in adults N Engl J with septic shock Med Trial of early, goal-directed resuscitation N Engl J for septic shock Med Nat Rev. Sepsis-induced immunosuppression: Immunol from cellular dysfunctions to immunotherapy Crit Care Benchmarking the incidence and Med mortality of severe sepsis in the United States Lancet Immunosuppression in sepsis: a novel understanding of the disorder and a new Infect Dis therapeutic approach Immunity Necroptosis: the release of damage-associated molecular patterns and its physiological relevance Noncanonical inflammasome activation Science by intracellular LPS independent of TLR4 Assessment of clinical criteria for sepsis: JAMA for the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3) JAMA Mortality related to severe sepsis and septic shock among critically ill patients in Australia and New Zealand, 2000–2012 Lancet Procalcitonin as a diagnostic marker for Infect Dis sepsis: a systematic review and meta-analysis Cell TRIF Licenses Caspase-11-Dependent NLRP3 Inflammasome Activation by Gram-Negative Bacteria Caspase-11 cleaves gasdermin D for Nature non-canonical inflammasome signalling JAMA Effect of eritoran, an antagonist of MD2-TLR4, on mortality in patients with severe sepsis: the ACCESS randomized trial High versus low blood-pressure target in N Engl J patients with septic shock Med Science Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock Crit Care Hospitalizations, costs, and outcomes of severe sepsis in the United States 2003 to Med 2007
(continued on next page)
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Table 3 (continued) Web of Science Rank (Citations)
Title Scopus Rank (Citations)
Journal
Year Published (Days Until Extraction)
Overall Altmetric Score Rank of 50 (Raw Score)
Mainstream Media Mentions
Twitter Rank of 50 (User Count)
Classification Full Reference Number
27 (268)
22 (303)
2014 (1417)
(222)
3
36 (238)
Clinical
[117]
28 (262)
29 (280)
N Engl J Med Crit Care Med
2014 (1379)
(83)
0
(92)
Clinical
[148]
29 (261)
(176)
Science
2014 (1225)
(93)
7
(45)
Mechanistic
[149]
30 (249)
28 (283)
N Engl J Med
2015 (1053)
(181)
9
(120)
Clinical
[150]
31 (237)
26 (291)
2014 (1220)
(139)
3
(97)
Clinical
[151]
32 (237)
35 (246)
N Engl J Med JAMA
2016 (710)
48 (263)
13
42 (187)
Clinical
[108]
33 (235)
33 (247)
J Clin Invest
2012 (2241)
(3)
0
(5)
Mechanistic
[152]
34 (228)
37 (238)
2012 (1966)
(0)
0
(0)
Mechanistic
[153]
35 (227)
32 (260)
J Immunol Intensive Care Med
2014 (1177)
(64)
0
(68)
Clinical
[154]
36 (220) 37 (219)
34 (247) 38 (238)
Lancet JAMA
2013 (1798) 2013 (1563)
(14) (149)
0 2
(23) (150)
Clinical Clinical
[155] [156]
38 (219) 39 (216)
40 (235) 31 (264)
Virulence JAMA
2014 (1493) 2013 (1549)
(46) (215)
5 2
(3) 31 (250)
Clinical Clinical
[157] [114]
40 (212)
36 (243)
Crit Care
2012 (2080)
(9)
0
(3)
Clinical
[158]
41 (210)
39 (237)
Lancet Infect Dis
2012 (2224)
(18)
0
(18)
Clinical
[159]
42 (206)
43 (216)
Cell Host Microbe
2012 (2224)
(19)
0
(11)
Mechanistic
[160]
43 (200)
44 (212)
2015 (1124)
(69)
5
(39)
Clinical
[161]
44 (199)
42 (217)
Lancet Infect Dis J Clin Invest
2012 (2078)
(1)
0
(2)
Mechanistic
[162]
45 (199)
46 (210)
Crit Rev. Biochem Mol Biol
2013 (1767)
(3)
0
(2)
Mechanistic
[163]
46 (194)
41 (223)
Pediatrics
2012 (2224)
(34)
0
(28)
Clinical
[164]
47 (192)
47 (208)
Crit Care Med
2013 (1549)
(99)
9
(25)
Clinical
[12]
48 (192) 49 (189)
49 (197) 48 (198)
Blood Intensive Care Med
2013 (1858) 2017 (380)
(7) 20 (459)
0 2
(1) 12 (547)
Mechanistic Clinical
[165] [22]
50 (187)
45 (211)
Expert Rev. Anti Infect
2012 (2044)
(24)
2
(3)
Clinical
[166]
Albumin replacement in patients with severe sepsis or septic shock Empiric antibiotic treatment reduces mortality in severe sepsis and septic shock from the first hour: results from a guideline-based performance improvement program mTOR- and HIF-1a-mediated aerobic glycolysis as metabolic basis for trained immunity Systemic inflammatory response syndrome criteria in defining severe sepsis Lower versus higher hemoglobin threshold for transfusion in septic shock Developing a new definition and assessing new clinical criteria for septic shock: for the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3) A subset of neutrophils in human systemic inflammation inhibits T cell responses through Mac-1 Neutrophil extracellular traps: double-edged swords of innate immunity Consensus on circulatory shock and hemodynamic monitoring. Task force of the European Society of Intensive Care Medicine Sepsis definitions: time for change Effect of heart rate control with esmolol on hemodynamic and clinical outcomes in patients with septic shock: a randomized clinical trial Epidemiology of severe sepsis Effects of fluid resuscitation with colloids vs crystalloids on mortality in critically ill patients presenting with hypovolemic shock: the CRISTAL randomized trial Assessment of hemodynamic efficacy and safety of 6% hydroxyethylstarch 130/0.4 vs. 0.9% NaCl fluid replacement in patients with severe sepsis: The CRYSTMAS study Outcomes of the Surviving Sepsis Campaign in intensive care units in the USA and Europe: a prospective cohort study Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis Sepsis: a roadmap for future research MicroRNA-181b regulates NF-kappaB-mediated vascular inflammation Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9): The next decade Management of neonates with suspected or proven early-onset bacterial sepsis Two decades of mortality trends among patients with severe sepsis: a comparative meta-analysis NETosis: how vital is it? Surviving Sepsis Campaign: international guidelines for management of sepsis and septic shock: 2016 Sepsis, severe sepsis and septic shock: changes in incidence, pathogens and outcomes
C.S. Jabaley et al. / Journal of Critical Care 48 (2018) 357–371
367
Table 3 (continued) Web of Science Rank (Citations)
Title Scopus Rank (Citations)
(187)
50 (193)
Signaling by IL-6 promotes alternative activation of macrophages to limit endotoxemia and obesity-associated resistance to insulin
Journal
Ther Nat Immunol
Year Published (Days Until Extraction)
Overall Altmetric Score Rank of 50 (Raw Score)
Mainstream Media Mentions
Twitter Rank of 50 (User Count)
Classification Full Reference Number
2014 (1405)
(8)
0
(2)
Mechanistic
[167]
Fig. 2. Title: Unique Twitter users mentioning at least one selected sepsis publication by geographic region. Counts of unique Twitter users having cited any publication on the Twitter user activity top 50 list (Table 2) are depicted by geographic region on a choropleth with a log-adjusted scale.
Fig. 3. Title: Density plot depicting time from publication to mentions in alternative metric sources. Publication to mention lag time for mainstream media sources was derived from the 51 publications with the highest overall Altmetric.com attention score (Table 1). Lag time for mentions by Twitter users was derived from the 50 publications with the highest overall Twitter user activity (Table 2). Mentions not occurring between 30 days before publication and 365 days after publication are not depicted (see Fig. 1).
368
C.S. Jabaley et al. / Journal of Critical Care 48 (2018) 357–371
Linear Modeling
R 2 = 0.4 R 2 = 0.11
Overall Altmetric Attention Score
150
100
50
Publication Category 200
Clinical Mechanistic
2
R = 0.41 R 2 = 0.18
Twitter User Citation Count
Conventional Citations Per Year (Per Web of Science)
200
2D Density Estimate
150
100
50
0
100
200
300
400
500
0
100
200
300
400
500
Altmetric Subset Score Fig. 4. Title: Correlation between overall Altmetric.com attention score and Twitter user activity with conventional citations. Those publications with the highest overall conventional citation counts as derived from Web of Science (Table 3) were used for the analysis. Five publications with outlying values as delineated in the Methods were excluded from the analysis and are not depicted (see Fig. 1).
Funding Internal departmental funds were used to support the authors' time to conduct the current study. Authors' contributions All authors met criteria for authorship under ICMJE criteria. CSJ conceived the study with critical input from VORS and JMB. CSJ developed and implemented the data acquisition approach. CSJ developed and implemented the analysis plan with critical input and assistance from VORS. All authors interpreted the data and critically reviewed the analysis. CSJ authored the manuscript with critical revisions and conceptual advice from RFG, MJS, VM, GCL, JMB, and VORS. All authors approved the final manuscript. Acknowledgements The authors wish to thank Altmetric.com for access to their database. Appendix A. Supplementary data Supplementary data to this article can be found online at https://doi. org/10.1016/j.jcrc.2018.09.033. References [1] Fleischmann C, Scherag A, Adhikari NK, Hartog CS, Tsaganos T, Schlattmann P, et al. Assessment of global incidence and mortality of hospital-treated sepsis. Current estimates and limitations. Am J Respir Crit Care Med 2016;193(3):259–72.
[2] Reinhart K, Daniels R, Kissoon N, Machado FR, Schachter RD, Finfer S. Recognizing sepsis as a global health priority - a WHO resolution. N Engl J Med 2017;377(5): 414–7. [3] World Health Organization. Resolution WHA 70.7: improving the prevention, diagnosis and clinica management of sepsis. http://apps.who.int/gb/ebwha/pdf_files/ WHA70/A70_R7-en.pdf; 2017. Accessed 6/30/2017. [4] Ferrer R, Artigas A, Levy MM, Blanco J, Gonzalez-Diaz G, Garnacho-Montero J, et al. Improvement in process of care and outcome after a multicenter severe sepsis educational program in Spain. JAMA 2008;299(19):2294–303. [5] Barochia AV, Cui X, Vitberg D, Suffredini AF, O'Grady NP, Banks SM, et al. Bundled care for septic shock: an analysis of clinical trials. Crit Care Med 2010;38(2): 668–78. [6] Gaieski DF, Mikkelsen ME, Band RA, Pines JM, Massone R, Furia FF, et al. Impact of time to antibiotics on survival in patients with severe sepsis or septic shock in whom early goal-directed therapy was initiated in the emergency department. Crit Care Med 2010;38(4):1045–53. [7] Kumar A, Roberts D, Wood KE, Light B, Parrillo JE, Sharma S, et al. Duration of hypotension before initiation of effective antimicrobial therapy is the critical determinant of survival in human septic shock. Crit Care Med 2006;34(6):1589–96. [8] Berger RE, Rivers E, Levy MM. Management of septic shock. N Engl J Med 2017;376 (23):2282–5. [9] Howell MD, Davis AM. Management of sepsis and septic shock. JAMA 2017;317(8): 847–8. [10] Rowan KM, Angus DC, Bailey M, Barnato AE, Bellomo R, Canter RR, et al. Early, goaldirected therapy for septic shock - a patient-level meta-analysis. N Engl J Med 2017;376(23):2223–34. [11] Kaukonen KM, Bailey M, Suzuki S, Pilcher D, Bellomo R. Mortality related to severe sepsis and septic shock among critically ill patients in Australia and New Zealand, 2000-2012. JAMA 2014;311(13):1308–16. [12] Stevenson EK, Rubenstein AR, Radin GT, Wiener RS, Walkey AJ. Two decades of mortality trends among patients with severe sepsis: a comparative metaanalysis. Crit Care Med 2014;42(3):625–31. [13] Levy MM, Rhodes A, Phillips GS, Townsend SR, Schorr CA, Beale R, et al. Surviving Sepsis Campaign: association between performance metrics and outcomes in a 7.5-year study. Crit Care Med 2015;43(1):3–12. [14] Rhodes A, Phillips G, Beale R, Cecconi M, Chiche JD, De Backer D, et al. The surviving sepsis campaign bundles and outcome: results from the international multicentre prevalence study on sepsis (the IMPreSS study). Intensive Care Med 2015;41(9): 1620–8.
C.S. Jabaley et al. / Journal of Critical Care 48 (2018) 357–371 [15] Singer M, Deutschman CS, Seymour CW, Shankar-Hari M, Annane D, Bauer M, et al. The third international consensus definitions for sepsis and septic shock (sepsis-3). JAMA 2016;315(8):801–10. [16] Gobatto AL, Besen BA, Azevedo LC. How can we estimate sepsis incidence and mortality? Shock 2017;47(1S Suppl. 1):6–11. [17] Herran-Monge R, Muriel-Bombin A, Garcia-Garcia MM, Merino-Garcia PA, Martinez-Barrios M, Andaluz D, et al. Epidemiology and changes in mortality of sepsis after the implementation of surviving Sepsis Campaign guidelines. J Intensive Care Med 2017http://journals.sagepub.com/doi/abs/10.1177/ 0885066617711882. 885066617711882. [18] Rhodes A, Evans LE, Alhazzani W, Levy MM, Antonelli M, Ferrer R, et al. Surviving Sepsis Campaign: international guidelines for management of sepsis and septic shock: 2016. Crit Care Med 2017;45(3):486–552. [19] Rubulotta FM, Ramsay G, Parker MM, Dellinger RP, Levy MM, Poeze M. An international survey: public awareness and perception of sepsis. Crit Care Med 2009;37 (1):167–70. [20] Stehr SN, Reinhart K. Sepsis as a global health problem-why we need a global sepsis alliance. Shock 2013;39(Suppl. 1):3–4. [21] Vincent JL. Increasing awareness of sepsis: World Sepsis Day. Crit Care 2012;16(5): 152. [22] Rhodes A, Evans LE, Alhazzani W, Levy MM, Antonelli M, Ferrer R, et al. Surviving Sepsis Campaign: international guidelines for management of sepsis and septic shock: 2016. Intensive Care Med 2017;43(3):304–77. [23] Warren HR, Raison N, Dasgupta P. The rise of altmetrics. JAMA 2017;317(2):131–2. [24] Bornmann L. Do altmetrics point to the broader impact of research? An overview of benefits and disadvantages of altmetrics. J Informet 2014;8(4):895–903. [25] Sugimoto CR, Work S, Larivière V, Haustein S. Scholarly use of social media and altmetrics: a review of the literature. J Assoc Inf Sci Technol 2017;68(9):2037–62. [26] Erdt M, Nagarajan A, Sin S-CJ, Theng Y-L. Altmetrics: an analysis of the state-of-theart in measuring research impact on social media. Scientometrics 2016;109(2): 1117–66. [27] Thelwall M, Haustein S, Larivière V, Sugimoto CR. Do Altmetrics work? Twitter and ten other social web services. PLoS One 2013;8(5):e64841. [28] Costas R, Zahedi Z, Wouters P. Do “altmetrics” correlate with citations? Extensive comparison of altmetric indicators with citations from a multidisciplinary perspective. J Assoc Inf Sci Technol 2015;66(10):2003–19. [29] Wong A, Wilkinson J. Malbrain M. Free open access medical education (FOAM): the new way to keep up-to-date. On Medicine, 2018. ; 2018 BioMed Central. [30] Wong A, Wilkinson J, Malbrain M. Using social media in medicine to your advantage, with care! On Medicine. BioMed Central; 2018. [31] Wong A, Wilkinson J, Malbrain M. Social media in critical care: what's all the fuss about? On Medicine. BioMed Central; 2018. [32] von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP. Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. BMJ 2007;335(7624): 806–8. [33] Altmetric Staff. When did altmetric start tracking attention to each attention source? https://goo.gl/EkGKeK; 2018. Accessed March 2, 2018. [34] Altmetric Staff. How is the altmetric attention score calculated? https://goo.gl/ aKKjR6; 2017. Accessed March 2, 2018. [35] Altmetric Staff. Altmetric API reference & getting started. http://api.altmetric.com/; 2017. Accessed March 2, 2018. [36] Wang X, Cui Y, Li Q, Guo X. Social media attention increases article visits: an investigation on article-level referral data of PeerJ. Front Res Metr Anal 2017;2(11). [37] Meho LI, Yang K. Impact of data sources on citation counts and rankings of LIS faculty: web of science versus scopus and google scholar. J Am Soc Inf Sci Technol 2007;58(13):2105–25. [38] Altmetric Engineering. Altmetric Engineering on Figshare. https://figshare.com/ authors/Altmetric_Engineering/831115; 2008. February 2, 2018. [39] Wickham H. ggplot2: elegant graphics for data analysis. New York: SpringerVerlag; 2009. [40] Aphalo PJ. Learn R ...as you learnt your mother tongue. Leanpub; 2016. [41] South A. Rworldmap: a new R package for mapping global data. R I Dent J 2011;3 (1):35–43. [42] Altman N, Krzywinski M. Analyzing outliers: influential or nuisance? Nat Methods 2016;13:281. [43] Haustein S, Costas R, Larivière V. Characterizing social media metrics of scholarly papers: the effect of document properties and collaboration patterns. PLoS One 2015;10(3):e0120495. [44] Hendren N, Sukumar S, Glazer CS. Vibrio vulnificus septic shock due to a contaminated tattoo. BMJ Case Rep 2017;2017. [45] Devault AM, Mortimer TD, Kitchen A, Kiesewetter H, Enk JM, Golding GB, et al. A molecular portrait of maternal sepsis from byzantine Troy. Elife 2017;6. [46] Hjortrup PB, Haase N, Wetterslev J, Perner A. Gone fishing in a fluid trial. Crit Care Resusc 2016;18(1):55–8. [47] Wilson JP, Kafetz K, Fink D. Lick of death: Capnocytophaga canimorsus is an important cause of sepsis in the elderly. BMJ Case Rep 2016;2016. [48] Altmetric Engineering. Top 100 2016 - article data. https://figshare.com/articles/ Top_100_2016_-_article_data/4294073/1; 2016. February 2, 2016. [49] Fraley C, Raftery AE. Model-based clustering, discriminant analysis, and density estimation. J Am Stat Assoc 2002;97(458):611–31. [50] Ortega JL. Reliability and accuracy of altmetric providers: a comparison among Altmetric.com, PlumX and Crossref Event Data. Scientometrics 2018;116(3): 2123–38. [51] Meschede C, Siebenlist T. Cross-metric compatability and inconsistencies of altmetrics. Scientometrics 2018;115(1):283–97.
369
[52] Zahedi Z, Costas R. General discussion of data quality challenges in social media metrics: Extensive comparison of four major altmetric data aggregators. PLoS One 2018;13(5):e0197326. [53] Rodrigo C, Zohreh Z, Paul W. The thematic orientation of publications mentioned on social media: large-scale disciplinary comparison of social media metrics with citations. Aslib J Inf Manag 2015;67(3):260–88. [54] Haustein S, Peters I, Sugimoto CR, Thelwall M, Larivière V. Tweeting biomedicine: an analysis of tweets and citations in the biomedical literature. J Assoc Inf Sci Technol 2014;65(4):656–69. [55] Haustein S, Bowman TD, Costas R. When is an article actually published? An analysis of online availability, publication, and indexation dates. arXiv preprint. arXiv 2015 150500796. [56] Konkiel S. Altmetrics: diversifying the understanding of influential scholarship. Palgrave Commun 2016;2:16057. [57] Zhang Z, Poucke SV, Goyal H, Rowley DD, Zhong M, Liu N. The top 2,000 cited articles in critical care medicine: a bibliometric analysis. J Thorac Dis 2018;10(4): 2437–47. [58] Rosenberg AL, Tripathi RS, Blum J. The most influential articles in critical care medicine. J Crit Care 2010;25(1):157–70. [59] Tao T, Zhao X, Lou J, Bo L, Wang F, Li J, et al. The top cited clinical research articles on sepsis: a bibliometric analysis. Crit Care 2012;16(3):R110. [60] Priem J. Scholarship: beyond the paper. Nature 2013;495(7442):437–40. [61] Erdt M, Aung HH, Aw AS, Rapple C, Theng Y-L. Analysing researchers' outreach efforts and the association with publication metrics: a case study of Kudos. PLoS One 2017;12(8):e0183217. [62] Holmberg K, Vainio J. Why do some research articles receive more online attention and higher altmetrics? Scientometrics: Reasons for online success according to the authors; 2018. [63] Dinsmore A, Allen L, Dolby K. Alternative perspectives on impact: the potential of ALMs and altmetrics to inform funders about research impact. PLoS Biol 2014;12 (11):e1002003. [64] Gordon G, Lin J, Cave R, Dandrea R. The question of data integrity in article-level metrics. PLoS Biol 2015;13(8):e1002161. [65] Mandavilli A. Peer review: trial by Twitter. Nature 2011;469(7330):286–7. [66] Mocanu D, Baronchelli A, Perra N, Gonçalves B, Zhang Q, Vespignani A. The Twitter of babel: mapping world languages through microblogging platforms. PLoS One 2013;8(4):e61981. [67] Bornmann L. What do altmetrics counts mean? A plea for content analyses. J Assoc Inf Sci Technol 2016;67(4):1016–7. [68] Haustein S, Bowman TD, Holmberg K, Tsou A, Sugimoto CR, Larivière V. Tweets as impact indicators: examining the implications of automated “bot” accounts on Twitter. J Assoc Inf Sci Technol 2016;67(1):232–8. [69] Robinson-Garcia N, Costas R, Isett K, Melkers J, Hicks D. The unbearable emptiness of tweeting—about journal articles. PLoS One 2017;12(8):e0183551. [70] Haustein S. Grand challenges in altmetrics: heterogeneity, data quality and dependencies. Scientometrics 2016;108(1):413–23. [71] Seymour CW, Gesten F, Prescott HC, Friedrich ME, Iwashyna TJ, Phillips GS, et al. Time to treatment and mortality during mandated emergency care for sepsis. N Engl J Med 2017;376(23):2235–44. [72] Panigrahi P, Parida S, Nanda NC, Satpathy R, Pradhan L, Chandel DS, et al. A randomized synbiotic trial to prevent sepsis among infants in rural India. Nature 2017;548(7668):407–12. [73] Marik PE, Khangoora V, Rivera R, Hooper MH, Catravas J. Hydrocortisone, vitamin C, and thiamine for the treatment of severe sepsis and septic shock: a retrospective before-after study. Chest 2017;151(6):1229–38. [74] Liu V, Escobar GJ, Greene JD, Soule J, Whippy A, Angus DC, et al. Hospital deaths in patients with sepsis from 2 independent cohorts. JAMA 2014;312(1):90–2. [75] Wang A, Huen SC, Luan HH, Yu S, Zhang C, Gallezot JD, et al. Opposing effects of fasting metabolism on tissue tolerance in bacterial and viral inflammation. Cell 2016;166(6) 1512-25.e12. [76] Ribet D, Cossart P. How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect 2015;17(3):173–83. [77] Seok J, Warren HS, Cuenca AG, Mindrinos MN, Baker HV, Xu W, et al. Genomic responses in mouse models poorly mimic human inflammatory diseases. Proc Natl Acad Sci U S A 2013;110(9):3507–12. [78] Alam N, Oskam E, Stassen PM, Exter PV, van de Ven PM, Haak HR, et al. Prehospital antibiotics in the ambulance for sepsis: a multicentre, open label, randomised trial. Lancet Respir Med 2018;6(1):40–50. [79] Hershey TB, Kahn JM. State sepsis mandates - a new era for regulation of hospital quality. N Engl J Med 2017;376(24):2311–3. [80] Manaktala S, Claypool SR. Evaluating the impact of a computerized surveillance algorithm and decision support system on sepsis mortality. J Am Med Inform Assoc 2017;24(1):88–95. [81] Gaieski DF, Edwards JM, Kallan MJ, Carr BG. Benchmarking the incidence and mortality of severe sepsis in the United States. Crit Care Med 2013;41(5):1167–74. [82] Keh D, Trips E, Marx G, Wirtz SP, Abduljawwad E, Bercker S, et al. Effect of hydrocortisone on development of shock among patients with severe sepsis: the HYPRESS randomized clinical trial. JAMA 2016;316(17):1775–85. [83] Oudemans-Van Straaten HM, Spoelstra-De Man AM, de Waard MC. Vitamin C revisited. Crit Care 2014;18(4):460. [84] Takao K, Miyakawa T. Genomic responses in mouse models greatly mimic human inflammatory diseases. Proc Natl Acad Sci U S A 2015;112(4):1167–72. [85] Zimmerman JJ, Sullivan E, Yager TD, Cheng C, Permut L, Cermelli S, et al. Diagnostic accuracy of a host gene expression signature that discriminates clinical severe sepsis syndrome and infection-negative systemic inflammation among critically ill children. Crit Care Med 2017;45(4) e418-e25.
370
C.S. Jabaley et al. / Journal of Critical Care 48 (2018) 357–371
[86] Schuetz P, Birkhahn R, Sherwin R, Jones AE, Singer A, Kline JA, et al. Serial procalcitonin predicts mortality in severe sepsis patients: results from the Multicenter Procalcitonin MOnitoring SEpsis (MOSES) study. Crit Care Med 2017;45 (5):781–9. [87] Fedson DS. Treating the host response to emerging virus diseases: lessons learned from sepsis, pneumonia, influenza and Ebola. Ann Transl Med 2016;4(21):421. [88] Sweeney TE, Wong HR, Khatri P. Robust classification of bacterial and viral infections via integrated host gene expression diagnostics. Sci Transl Med 2016;8 (346):346ra91. [89] Hartman ME, Linde-Zwirble WT, Angus DC, Watson RS. Trends in the epidemiology of pediatric severe sepsis. Pediatr Crit Care Med 2013;14(7):686–93. [90] Friesecke S, Stecher SS, Gross S, Felix SB, Nierhaus A. Extracorporeal cytokine elimination as rescue therapy in refractory septic shock: a prospective single-center study. J Artif Organs 2017;20(3):252–9. [91] Seymour CW, Liu VX, Iwashyna TJ, Brunkhorst FM, Rea TD, Scherag A, et al. Assessment of clinical criteria for sepsis: for the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA 2016;315(8):762–74. [92] Farris RW, Weiss NS, Zimmerman JJ. Functional outcomes in pediatric severe sepsis: further analysis of the researching severe sepsis and organ dysfunction in children: a global perspective trial. Pediatr Crit Care Med 2013;14(9):835–42. [93] Gotts JE, Matthay MA. Sepsis: pathophysiology and clinical management. BMJ 2016;353:i1585. [94] Annane D. The role of ACTH and corticosteroids for sepsis and septic shock: an update. Front Endocrinol (Lausanne) 2016;7:70. [95] Angus DC, van der Poll T. Severe sepsis and septic shock. N Engl J Med 2013;369 (9):840–51. [96] Seymour CW, Rosengart MR. Septic shock: advances in diagnosis and treatment. JAMA 2015;314(7):708–17. [97] Kang JH, Super M, Yung CW, Cooper RM, Domansky K, Graveline AR, et al. An extracorporeal blood-cleansing device for sepsis therapy. Nat Med 2014;20(10): 1211–6. [98] Yealy DM, Kellum JA, Huang DT, Barnato AE, Weissfeld LA, Pike F, et al. A randomized trial of protocol-based care for early septic shock. N Engl J Med 2014;370(18): 1683–93. [99] Bergh C, Fall K, Udumyan R, Sjoqvist H, Frobert O, Montgomery S. Severe infections and subsequent delayed cardiovascular disease. Eur J Prev Cardiol 2017;24(18): 1958–66. [100] Vail E, Gershengorn HB, Hua M, Walkey AJ, Rubenfeld G, Wunsch H. Association between US norepinephrine shortage and mortality among patients with septic shock. JAMA 2017;317(14):1433–42. [101] Torsvik M, Gustad LT, Mehl A, Bangstad IL, Vinje LJ, Damas JK, et al. Early identification of sepsis in hospital inpatients by ward nurses increases 30-day survival. Crit Care 2016;20(1):244. [102] Hassan U, Ghonge T, Reddy Jr B, Patel M, Rappleye M, Taneja I, et al. A point-of-care microfluidic biochip for quantification of CD64 expression from whole blood for sepsis stratification. Nat Commun 2017;8:15949. [103] Mayr FB, Talisa VB, Balakumar V, Chang CH, Fine M, Yende S. Proportion and cost of unplanned 30-day readmissions after sepsis compared with other medical conditions. JAMA 2017;317(5):530–1. [104] Wake H, Mori S, Liu K, Morioka Y, Teshigawara K, Sakaguchi M, et al. Histidine-rich glycoprotein prevents septic lethality through regulation of immunothrombosis and inflammation. EBioMedicine 2016;9:180–94. [105] Andrews B, Semler MW, Muchemwa L, Kelly P, Lakhi S, Heimburger DC, et al. Effect of an early resuscitation protocol on in-hospital mortality among adults with sepsis and hypotension: a randomized clinical trial. JAMA 2017;318(13):1233–40. [106] Ritchie SC, Wurtz P, Nath AP, Abraham G, Havulinna AS, Fearnley LG, et al. The biomarker ClycA is associated with chronic inflammation and predicts long-term risk of severe infection. Cell Syst 2015;1(4):293–301. [107] Vincent JL, Martin GS, Levy MM. qSOFA does not replace SIRS in the definition of sepsis. Crit Care 2016;20(1):210. [108] Shankar-Hari M, Phillips GS, Levy ML, Seymour CW, Liu VX, Deutschman CS, et al. Developing a new definition and assessing new clinical criteria for septic shock: for the Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA 2016;315(8):775–87. [109] Gordon AC, Perkins GD, Singer M, McAuley DF, Orme RM, Santhakumaran S, et al. Levosimendan for the prevention of acute organ dysfunction in sepsis. N Engl J Med 2016;375(17):1638–48. [110] Henry BD, Neill DR, Becker KA, Gore S, Bricio-Moreno L, Ziobro R, et al. Engineered liposomes sequester bacterial exotoxins and protect from severe invasive infections in mice. Nat Biotechnol 2015;33(1):81–8. [111] Acheampong A, Vincent JL. A positive fluid balance is an independent prognostic factor in patients with sepsis. Crit Care 2015;19:251. [112] Fujii T, Ganeko R, Kataoka Y, Furukawa TA, Featherstone R, Doi K, et al. Polymyxin B-immobilized hemoperfusion and mortality in critically ill adult patients with sepsis/septic shock: a systematic review with meta-analysis and trial sequential analysis. Intensive Care Med 2018;44(2):167–78. [113] Abbasi J. In treating sepsis, questions about timing and mandates. JAMA 2017;318 (6):506–8. [114] Annane D, Siami S, Jaber S, Martin C, Elatrous S, Declere AD, et al. Effects of fluid resuscitation with colloids vs crystalloids on mortality in critically ill patients presenting with hypovolemic shock: the CRISTAL randomized trial. JAMA 2013;310 (17):1809–17. [115] Kawazoe Y, Miyamoto K, Morimoto T, Yamamoto T, Fuke A, Hashimoto A, et al. Effect of dexmedetomidine on mortality and ventilator-free days in patients requiring mechanical ventilation with sepsis: a randomized clinical trial. JAMA 2017; 317(13):1321–8.
[116] Asfar P, Meziani F, Hamel JF, Grelon F, Megarbane B, Anguel N, et al. High versus low blood-pressure target in patients with septic shock. N Engl J Med 2014;370 (17):1583–93. [117] Caironi P, Tognoni G, Masson S, Fumagalli R, Pesenti A, Romero M, et al. Albumin replacement in patients with severe sepsis or septic shock. N Engl J Med 2014; 370(15):1412–21. [118] Gupta RG, Hartigan SM, Kashiouris MG, Sessler CN, Bearman GM. Early goaldirected resuscitation of patients with septic shock: current evidence and future directions. Crit Care 2015;19:286. [119] Sawyer RG, Claridge JA, Nathens AB, Rotstein OD, Duane TM, Evans HL, et al. Trial of short-course antimicrobial therapy for intraabdominal infection. N Engl J Med 2015;372(21):1996–2005. [120] Gordon AC, Mason AJ, Thirunavukkarasu N, Perkins GD, Cecconi M, Cepkova M, et al. Effect of early vasopressin vs norepinephrine on kidney failure in patients with septic shock: the VANISH randomized clinical trial. JAMA 2016;316(5): 509–18. [121] Liu VX, Fielding-Singh V, Greene JD, Baker JM, Iwashyna TJ, Bhattacharya J, et al. The timing of early antibiotics and hospital mortality in sepsis. Am J Respir Crit Care Med 2017;196(7):856–63. [122] Gibbison B, Lopez-Lopez JA, Higgins JP, Miller T, Angelini GD, Lightman SL, et al. Corticosteroids in septic shock: a systematic review and network meta-analysis. Crit Care 2017;21(1):78. [123] Perner A, Haase N, Guttormsen AB, Tenhunen J, Klemenzson G, Aneman A, et al. Hydroxyethyl starch 130/0.42 versus Ringer's acetate in severe sepsis. N Engl J Med 2012;367(2):124–34. [124] Garnacho-Montero J, Gutierrez-Pizarraya A, Escoresca-Ortega A, FernandezDelgado E, Lopez-Sanchez JM. Adequate antibiotic therapy prior to ICU admission in patients with severe sepsis and septic shock reduces hospital mortality. Crit Care 2015;19:302. [125] Sterling SA, Miller WR, Pryor J, Puskarich MA, Jones AE. The impact of timing of antibiotics on outcomes in severe sepsis and septic shock: a systematic review and meta-analysis. Crit Care Med 2015;43(9):1907–15. [126] Freund Y, Lemachatti N, Krastinova E, Van Laer M, Claessens YE, Avondo A, et al. Prognostic accuracy of Sepsis-3 criteria for in-hospital mortality among patients with suspected infection presenting to the emergency department. JAMA 2017; 317(3):301–8. [127] Rhee C, Dantes R, Epstein L, Murphy DJ, Seymour CW, Iwashyna TJ, et al. Incidence and trends of sepsis in US hospitals using clinical vs claims data, 2009-2014. JAMA 2017;318(13):1241–9. [128] Davis AL, Carcillo JA, Aneja RK, Deymann AJ, Lin JC, Nguyen TC, et al. American College of Critical Care Medicine clinical practice parameters for hemodynamic support of pediatric and neonatal septic shock. Crit Care Med 2017;45(6):1061–93. [129] Powell R, Jeavons K. Identifying paediatric sepsis: the difficulties in following recommended practice and the creation of our own pathway. Arch Dis Child 2018; 103(1):114. [130] Vincent JL, Quintairos ESA, Couto Jr L, Taccone FS. The value of blood lactate kinetics in critically ill patients: a systematic review. Crit Care 2016;20(1):257. [131] Dellinger RP, Levy MM, Rhodes A, Annane D, Gerlach H, Opal SM, et al. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock: 2012. Crit Care Med 2013;41(2):580–637. [132] Dellinger RP, Levy MM, Rhodes A, Annane D, Gerlach H, Opal SM, et al. Surviving Sepsis Campaign: international guidelines for management of severe sepsis and septic shock, 2012. Intensive Care Med 2013;39(2):165–228. [133] Forstermann U, Sessa WC. Nitric oxide synthases: regulation and function. Eur Heart J 2012;33(7):829–37 37a-37d. [134] Wang R. Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 2012;92(2):791–896. [135] Peake SL, Delaney A, Bailey M, Bellomo R, Cameron PA, Cooper DJ, et al. Goaldirected resuscitation for patients with early septic shock. N Engl J Med 2014; 371(16):1496–506. [136] Ranieri VM, Thompson BT, Barie PS, Dhainaut JF, Douglas IS, Finfer S, et al. Drotrecogin alfa (activated) in adults with septic shock. N Engl J Med 2012;366 (22):2055–64. [137] Mouncey PR, Osborn TM, Power GS, Harrison DA, Sadique MZ, Grieve RD, et al. Trial of early, goal-directed resuscitation for septic shock. N Engl J Med 2015;372(14): 1301–11. [138] Hotchkiss RS, Monneret G, Payen D. Sepsis-induced immunosuppression: from cellular dysfunctions to immunotherapy. Nat Rev Immunol 2013;13(12):862–74. [139] Hotchkiss RS, Monneret G, Payen D. Immunosuppression in sepsis: a novel understanding of the disorder and a new therapeutic approach. Lancet Infect Dis 2013;13 (3):260–8. [140] Kaczmarek A, Vandenabeele P, Krysko DV. Necroptosis: the release of damageassociated molecular patterns and its physiological relevance. Immunity 2013;38 (2):209–23. [141] Kayagaki N, Wong MT, Stowe IB, Ramani SR, Gonzalez LC, Akashi-Takamura S, et al. Noncanonical inflammasome activation by intracellular LPS independent of TLR4. Science 2013;341(6151):1246–9. [142] Wacker C, Prkno A, Brunkhorst FM, Schlattmann P. Procalcitonin as a diagnostic marker for sepsis: a systematic review and meta-analysis. Lancet Infect Dis 2013; 13(5):426–35. [143] Rathinam VA, Vanaja SK, Waggoner L, Sokolovska A, Becker C, Stuart LM, et al. TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by gram-negative bacteria. Cell 2012;150(3):606–19. [144] Kayagaki N, Stowe IB, Lee BL, O'Rourke K, Anderson K, Warming S, et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature 2015;526 (7575):666–71.
C.S. Jabaley et al. / Journal of Critical Care 48 (2018) 357–371 [145] Opal SM, Laterre PF, Francois B, Larosa SP, Angus DC, Mira JP, et al. Effect of eritoran, an antagonist of MD2-TLR4, on mortality in patients with severe sepsis: the ACCESS randomized trial. JAMA 2013;309(11):1154–62. [146] Hagar JA, Powell DA, Aachoui Y, Ernst RK, Miao EA. Cytoplasmic LPS activates caspase-11: implications in TLR4-independent endotoxic shock. Science 2013; 341(6151):1250–3. [147] Lagu T, Rothberg MB, Shieh MS, Pekow PS, Steingrub JS, Lindenauer PK. Hospitalizations, costs, and outcomes of severe sepsis in the United States 2003 to 2007. Crit Care Med 2012;40(3):754–61. [148] Ferrer R, Martin-Loeches I, Phillips G, Osborn TM, Townsend S, Dellinger RP, et al. Empiric antibiotic treatment reduces mortality in severe sepsis and septic shock from the first hour: results from a guideline-based performance improvement program. Crit Care Med 2014;42(8):1749–55. [149] Cheng SC, Quintin J, Cramer RA, Shepardson KM, Saeed S, Kumar V, et al. mTORand HIF-1alpha-mediated aerobic glycolysis as metabolic basis for trained immunity. Science 2014;345(6204):1250684. [150] Kaukonen KM, Bailey M, Pilcher D, Cooper DJ, Bellomo R. Systemic inflammatory response syndrome criteria in defining severe sepsis. N Engl J Med 2015;372 (17):1629–38. [151] Holst LB, Haase N, Wetterslev J, Wernerman J, Guttormsen AB, Karlsson S, et al. Lower versus higher hemoglobin threshold for transfusion in septic shock. N Engl J Med 2014;371(15):1381–91. [152] Pillay J, Kamp VM, van Hoffen E, Visser T, Tak T, Lammers JW, et al. A subset of neutrophils in human systemic inflammation inhibits T cell responses through Mac-1. J Clin Invest 2012;122(1):327–36. [153] Kaplan MJ, Radic M. Neutrophil extracellular traps: double-edged swords of innate immunity. J Immunol 2012;189(6):2689–95. [154] Cecconi M, De Backer D, Antonelli M, Beale R, Bakker J, Hofer C, et al. Consensus on circulatory shock and hemodynamic monitoring. Task force of the European Society of Intensive Care Medicine. Intensive Care Med 2014;40(12):1795–815. [155] Vincent JL, Opal SM, Marshall JC, Tracey KJ. Sepsis definitions: time for change. Lancet 2013;381(9868):774–5.
371
[156] Morelli A, Ertmer C, Westphal M, Rehberg S, Kampmeier T, Ligges S, et al. Effect of heart rate control with esmolol on hemodynamic and clinical outcomes in patients with septic shock: a randomized clinical trial. JAMA 2013;310(16): 1683–91. [157] Mayr FB, Yende S, Angus DC. Epidemiology of severe sepsis. Virulence 2014;5(1): 4–11. [158] Guidet B, Martinet O, Boulain T, Philippart F, Poussel JF, Maizel J, et al. Assessment of hemodynamic efficacy and safety of 6% hydroxyethylstarch 130/0.4 vs. 0.9% NaCl fluid replacement in patients with severe sepsis: the CRYSTMAS study. Crit Care 2012;16(3):R94. [159] Levy MM, Artigas A, Phillips GS, Rhodes A, Beale R, Osborn T, et al. Outcomes of the surviving sepsis campaign in intensive care units in the USA and Europe: a prospective cohort study. Lancet Infect Dis 2012;12(12):919–24. [160] McDonald B, Urrutia R, Yipp BG, Jenne CN, Kubes P. Intravascular neutrophil extracellular traps capture bacteria from the bloodstream during sepsis. Cell Host Microbe 2012;12(3):324–33. [161] Cohen J, Vincent JL, Adhikari NK, Machado FR, Angus DC, Calandra T, et al. Sepsis: a roadmap for future research. Lancet Infect Dis 2015;15(5):581–614. [162] Sun X, Icli B, Wara AK, Belkin N, He S, Kobzik L, et al. MicroRNA-181b regulates NF-kappaB-mediated vascular inflammation. J Clin Invest 2012;122(6): 1973–90. [163] Vandooren J, Van den Steen PE, Opdenakker G. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9): the next decade. Crit Rev Biochem Mol Biol 2013;48(3):222–72. [164] Polin RA. Management of neonates with suspected or proven early-onset bacterial sepsis. Pediatrics 2012;129(5):1006–15. [165] Yipp BG, Kubes P. NETosis: how vital is it? Blood 2013;122(16):2784–94. [166] Martin GS. Sepsis, severe sepsis and septic shock: changes in incidence, pathogens and outcomes. Expert Rev Anti Infect Ther 2012;10(6):701–6. [167] Mauer J, Chaurasia B, Goldau J, Vogt MC, Ruud J, Nguyen KD, et al. Signaling by IL-6 promotes alternative activation of macrophages to limit endotoxemia and obesityassociated resistance to insulin. Nat Immunol 2014;15(5):423–30.