The Global Alliance for Infections in Surgery: defining a model for antimicrobial stewardship—results from an international cross-sectional survey

Background

Antimicrobial Stewardship Programs (ASPs) have been promoted to optimize antimicrobial usage and patient outcomes, and to reduce the emergence of antimicrobial-resistant organisms. However, the best strategies for an ASP are not definitively established and are likely to vary based on local culture, policy, and routine clinical practice, and probably limited resources in middle-income countries. The aim of this study is to evaluate structures and resources of antimicrobial stewardship teams (ASTs) in surgical departments from different regions of the world.

Methods

A cross-sectional web-based survey was conducted in 2016 on 173 physicians who participated in the AGORA (Antimicrobials: A Global Alliance for Optimizing their Rational Use in Intra-Abdominal Infections) project and on 658 international experts in the fields of ASPs, infection control, and infections in surgery.

Results

The response rate was 19.4%. One hundred fifty-six (98.7%) participants stated their hospital had a multidisciplinary AST. The median number of physicians working inside the team was five [interquartile range 4–6]. An infectious disease specialist, a microbiologist and an infection control specialist were, respectively, present in 80.1, 76.3, and 67.9% of the ASTs. A surgeon was a component in 59.0% of cases and was significantly more likely to be present in university hospitals (89.5%, p < 0.05) compared to community teaching (83.3%) and community hospitals (66.7%). Protocols for pre-operative prophylaxis and for antimicrobial treatment of surgical infections were respectively implemented in 96.2 and 82.3% of the hospitals. The majority of the surgical departments implemented both persuasive and restrictive interventions (72.8%). The most common types of interventions in surgical departments were dissemination of educational materials (62.5%), expert approval (61.0%), audit and feedback (55.1%), educational outreach (53.7%), and compulsory order forms (51.5%).

Conclusion

The survey showed a heterogeneous organization of ASPs worldwide, demonstrating the necessity of a multidisciplinary and collaborative approach in the battle against antimicrobial resistance in surgical infections, and the importance of educational efforts towards this goal.

Antimicrobial Stewardship Programs (ASPs) have been promoted to optimize antimicrobial usage and patient outcomes and reduce the emergence of antimicrobial-resistant organisms. However, the best strategies for an ASP are not definitively established and are likely to vary based on local culture, policy and routine clinical practice, and probably limited resources in middle-income countries [1, 2]. Many hospitals remain without formal programs and those that do continue to struggle with gaining acceptance across service lines [3]. Moreover, identifying optimal efforts to impact system change has been challenging [4].

Restriction strategies may be effective at controlling use but raise issues of prescriber autonomy and require a large personnel commitment. Encouraging multidisciplinary collaboration within health systems to ensure that prophylactic, empirical, and targeted use of antimicrobial agents results in optimal patient outcomes is mandatory in the current era of antimicrobial resistance.

A panel of experts from the Surgical Infection Society (SIS) and World Society of Emergency Surgery (WSES) has recently published a review with the aim of defining the role of surgeons within the ASPs. The panel proposed that the best means of improving antimicrobial stewardship in surgical units worldwide should involve collaboration among various specialties within institutions including prescribing clinicians and pharmacists [5].

In 2016, a multidisciplinary task force from 79 different countries joined a global project to develop a consensus on the rational use of antimicrobials for patients with intra-abdominal infections (IAIs). The project has been termed AGORA (Antimicrobials: A Global Alliance for Optimizing their Rational Use in Intra-Abdominal Infections) [1].

Recently the Global Alliance for Infections in Surgery was founded and experts from 87 countries worldwide joined the highly diverse and skilled International Advisory Board. This alliance, promoted by the WSES, includes an interdisciplinary group of hospital administrators, epidemiologists, infection control specialists, infectious disease specialists, microbiologists, clinical pharmacologists and hospital pharmacists, surgeons, and intensivists. The mission of this alliance is to educate healthcare providers promoting the standards of care in managing infections in surgery worldwide [6]. Therefore, this study was conducted to evaluate the structure and resources of antimicrobial stewardship teams (ASTs) in surgical departments from different regions of the world.

We conducted a cross-sectional electronic survey evaluating the structure and resources of ASTs in surgical departments. The survey was designed by a multidisciplinary team of investigators including an epidemiologist, a surgeon, an infectious diseases physician, a pharmacologist, and a microbiologist. The questionnaire was piloted among five physicians for face and content validity.

The 24-item self-administered questionnaire collected information from multidisciplinary experts—mostly physicians—about characteristics and composition of the hospital team, implementation of local procedures, availability of antimicrobial use monitoring and surveillance systems, presence of an ASP, and related interventions (Additional file 1). An electronic invitation with a link to the survey was sent to 831 physicians: 173 physicians who participated in the AGORA project [1], and a large number (658) of international experts in the fields of antimicrobial stewardship, infection control, and infections in surgery identified after a thorough investigation using the PubMed database. The survey was Internet-based (using http://www.docs.google.com). Participation was voluntary but not anonymous; however, the confidentiality of respondents and their choices was ensured. No incentives were provided to the respondents. The study was open for 6 weeks between September 30 and November 11, 2016. Reminders were sent to all those who had not replied after 1 and 3 weeks. Due to the characteristics of the survey, a response rate ranging between 15 and 25% was expected.

Data were entered in an Excel database (Microsoft Corporation, Redmond, Washington, USA) and analyzed using Stata 11.0 software package (StataCorp, College Station, TX). Descriptive analyses included medians and interquartile ranges (IQR) for continuous variables or frequency (%) for categorical variables The two-sided chi-square or Fisher’s exact test was used for categorical variables, as appropriate. All tests were two-sided, and p values of 0.05 or lower were considered statistically significant.

Baseline data: coverage, response rate, working setting, and professional profile

A total of 161 (19.4%) of the 831 experts who were contacted by email completed the survey after two reminders. One incomplete survey was excluded from the study. In two cases the participants were from the same institution and only one survey was considered. One hundred fifty-eight responses were included in our analysis. Participants work settings and professional profiles are summarized in Table 1.

The response rate was similar to that of previous studies promoted by WSES [1, 7, 8].

As in the other WSES studies [1, 7, 8], participants were not homogeneously distributed across all geographic regions of the world due to the difficulty in recruiting participants in some areas of the world. However all geographic regions were represented in the survey.

Characteristics of the team

One hundred fifty-six (98.7%) participants stated their hospital had a multidisciplinary AST. Ninety participants (90/156, 57.7%) declared they were currently members of the team, with no difference in frequency between different WHO regions. The median number of physicians working inside the team was five [IQR 4–6]. Characteristics of the team are in Table 2.

One hundred thirty-five (135/158, 85.4%) participants had at least one surgeon with an interest or skills in surgical infections within the surgical department of their hospital; a surgeon was significantly more likely to be present in university hospitals (89.5%, two-sided chi-square test p < 0.05) compared to community teaching hospitals (83.3%) and community hospitals (66.7%).

Implementation of protocols and monitoring systems

Implementation of protocols and monitoring systems in 158 hospitals are reported in Table 3.

The vast majority of respondents (152/158, 96.2%) stated that their hospitals have a protocol for pre-operative prophylaxis. The protocol covered all surgical wards in 124 (78.5%) cases. A protocol for antimicrobial treatment of surgical infections was available in 130 (82.3%) hospitals; however, only 70 (44.3%) had it available in every surgical ward. One hundred twenty-eight (81.0%) hospitals had both a protocol for peri-operative prophylaxis and for antimicrobial treatment of surgical infections available, while four (4/158, 2.5%) hospitals lacked both.

Among 130 surgical wards implementing a protocol for antimicrobial treatment of surgical infections, 97 (74.6%) participants stated it included interventions to reduce the duration of therapy, 88 (67.7%) interventions to switch selected antimicrobials from intravenous-to-oral therapy, 78 (60.0%) interventions for alternative dosing strategies based on pharmacokinetics and pharmacodynamics, with significant difference between community hospitals (11.1%, two-sided Fischer’s exact test p < 0.05) compared to university (57.0%) and community teaching (60.0%) hospitals. Thirty-five (26.9%) participants reported the use of biological markers - such as procalcitonin to decrease antimicrobial use in critically ill patients.

Implementations of ASPs and related interventions

One hundred fifty-five (155/158, 98.1%) participants declared their hospital had an ASP running.

Our survey showed that 30 (19.4%) hospitals have developed persuasive interventions, 17 (11.0%) restrictive interventions and 108 (69.7%) both of them.

Twenty-three surgical departments (23/136, 16.9%) have developed persuasive interventions, 14 (10.3%) restrictive interventions and 99 (72.8%) both of them.

The most common types of interventions in surgical departments were dissemination of educational materials (62.5%), expert approval (61.0%), audit and feedback (55.1%), educational outreach (53.7%), and compulsory order forms (51.5%).

Types of ASPs and related interventions in surgical departments and in all hospital wards are described in detail in Table 4.

Six (6/41, 14.6%) surgical departments implementing a formulary restriction do not perform any monitoring system of used antimicrobials, and 4 (4/41, 9.8%) do not carry out any systematic reports about resistance data. Furthermore, 6 (7/70, 10.0%) surgical departments using a compulsory order form do not perform any monitoring system of used antimicrobials, and 11 (11/70, 15.7%) do not carry out any systematic reports about resistance data.

One hundred twenty-five (125/158, 79.1%) participants stated their hospital had carried out structural interventions to improve ASPs in the last 5 years. Sixty-nine (43.7%) changed from paper to computerized records, 74 (46.8%) implemented rapid laboratory testing, 32 (20.3%) introduced computerized decision support systems, 69 (43.7%) introduced organization of quality monitoring mechanisms and 29 (18.4%) implemented other structural interventions.

Characteristics of the implementation of protocols, monitoring systems, and ASPs interventions in surgical departments are detailed in Table 5.

Antimicrobial stewardship programs (ASP) are a key strategy to curb the spread of antibiotic resistance [3, 9]. The best strategies for an ASP are not definitively established and are likely to vary based on local routine clinical practice [7], despite several guidelines on the topic [9, 10].

Successful ASPs should focus on collaboration between healthcare professionals in order to share knowledge and best practices. It is essential for an ASP to have at least one member who is an infectious diseases specialist. Pharmacists with advanced training or longstanding clinical experience in infectious diseases are also key actors for the design and implementation of the stewardship program interventions [11]. Infection control specialists and hospital epidemiologists should coordinate efforts on monitoring and preventing healthcare-associated infections and in analyzing and reporting “real-time” data to prevent infections, improve antimicrobial use, and minimize secondary spread of resistance. Microbiologists should actively guide the proper use of tests and the flow of laboratory results. Being involved in providing surveillance data on antimicrobial resistance, they should provide periodic reports on antimicrobial resistance data allowing the multidisciplinary team to determine the ongoing burden of antimicrobial resistance in the hospital. Moreover, timely and accurate reporting of microbiology susceptibility test results allows selection of more appropriate targeted therapy, and may help reduce broad-spectrum antimicrobial use.

Surgeons with adequate knowledge in surgical infections and surgical anatomy when involved in ASPs may audit antibiotic prescriptions, provide feedback to the prescribers and integrate best practices of antimicrobial use among surgeons, and act as champions among colleagues. Although many surgeons are aware of the problem of antimicrobial resistance, most underestimate it in their own hospital [1]. Very few studies have been published on the role of ASPs in general surgical departments. In 2015, Cakmakci [12] suggested that the engagement of surgeons in ASPs might be crucial to their success. In 2013, however, Duane et al. showed poor compliance of surgical services with ASP recommendations [13]. Surgeons need to take part in addressing the global issue of antimicrobial resistance. Failure to do so will be catastrophic to patients and programs [3].

Infections are the main factors contributing to mortality in intensive care units (ICU) [14].

Intensivists have a critical role in treating multidrug resistant organisms in ICUs in critically ill patients. They have a crucial role in prescribing antimicrobial agents for our most challenging patients and are at the forefront of a successful ASP [15].

Finally, without adequate support from hospital administration, the ASP will be inadequate or inconsistent since the programs do not generate revenue [16]. Engagement of hospital administration has been confirmed as a key factor for both developing and sustaining an ASP [17].

In most cases, our survey demonstrated that ASPs do not involve a true multi-disciplinary approach.

An infectious diseases specialist and a hospital pharmacist were part of the team in 125 (80.1%) and in 95 (60.9%) cases, respectively. Only 87 (55.8%) teams included both an infectious diseases specialist and a hospital pharmacist. An infection control specialist and a hospital epidemiologist were part of the team in 106 (67.9%) and in 64 (41.0%) cases, respectively. It is possible that in some hospitals, AMS and infection prevention and control team are two separate entities, which collaborate. A microbiologist was part of the team in 119 (76.3%) cases. A surgeon was part of the team in 92 (59.0%) cases and an intensivist in 76 (48.6%) cases. A hospital administrator was part of the team only in 73 (46.8%) cases. Interestingly a surgeon was significantly more likely to be part of the team in university hospitals (89.5%, two-sided chi-square test p < 0.05) compared to community teaching (83.3%) and community non-teaching hospital (66.7%).

Strategies of ASPs should be tailored based on individual hospital characteristics and personnel and resources available. The Infectious Diseases Society of America/Society for Healthcare Epidemiology of America (IDSA/SHEA) guidelines identified two core proactive evidence-based strategies and several supplemental strategies for promoting antimicrobial stewardship [7, 8]: first, a restrictive strategy based on a proactive strategy of either formulary restriction or a requirement for pre-approval for specific drugs or both, and second, a persuasive strategy of performing prospective audit with intervention and feedback to the prescriber.

Our survey showed that 23 (16.9%) surgical departments have developed persuasive interventions, 14 (10.3%) restrictive interventions and 99 (72.8%) both of them. ASP policies should be based on both international/national antibiotic guidelines, and tailored to local microbiology and resistance patterns. Local clinical practice guidelines and algorithms can be an effective way to standardize prescribing practices based on the country’s epidemiology. Standardizing a shared protocol of antimicrobial prophylaxis should represent the first step of any Antimicrobial Stewardship program.

One hundred fifty-two (96.2%) participants stated their hospitals have a protocol for surgical antibiotic prophylaxis. Among the 158 hospitals, a protocol for antibiotic prophylaxis is present in all surgical wards in 124 (78.5%) of hospitals while only in some surgical wards in 28 (17.7%) hospitals.

A protocol for antibiotic treatment was present in all surgical wards in 70 (44.3%) hospitals, while only in some surgical wards in 60 (38.0%) hospitals. Among 130 hospitals implementing a protocol for antimicrobial treatment of surgical infections, 97 (74.6%) participants stated that it included interventions to reduce the duration of therapy, 88 (67.7%) interventions to switch select antimicrobials from intravenous-to-oral therapy, 78 (60.0%) interventions for alternative dosing strategies based on pharmacokinetic and pharmacodynamic principles, with substantial difference between community hospitals (11.1%, two-sided Fischer’s exact test p < 0.05), university (57.0%) and community teaching (60.0%) ones. Thirty-five (26.9%) participants admitted to the use of biological markers - such as procalcitonin - to decrease antimicrobial use in critically ill patients.

In any healthcare setting, a significant amount of time and energy should be spent on infection control. Surveillance studies can help clinicians to identify trends in pathogens incidence and antimicrobial resistance, including identification of emerging pathogens at local level. The survey showed that 130 (83.3%) surgical departments had systematic reports about resistance data.

Hospital pharmacists inside the multidisciplinary team should negotiate with hospital administration to obtain adequate and necessary infrastructure to measure antimicrobial use. Regular feedback about antimicrobial consumption can be an important determinant for change for healthcare professionals and policy makers to expedite progress towards prudent use of antimicrobials. The survey showed that 129 (81.6%) surgical departments had an antimicrobial monitoring system.

Interestingly, 6 (6/41, 14.6%) surgical departments implementing a formulary restriction do not perform any monitoring system of used antimicrobials, and 4 (4/41, 9.8%) do not carry out any systematic reports about resistance data. Furthermore, 6 (7/70, 10.0%) surgical departments using a compulsory order form do not perform any monitoring system of used antimicrobials, and 11 (11/70, 15.7%) do not carry out any systematic reports about resistance data. In institutions that use restrictive interventions, monitoring overall trends in antimicrobial use and systematic reports about resistance data should be necessary to assess and respond to such shifts in use.

The ultimate goal of any stewardship program should be to stimulate a behavioral change in prescribing practices. In this context, education of prescribers is crucial to convince clinicians to use antibiotics judiciously. However, without concurrent interventions education alone is of little value. In this regard, various stewardship interventions have been implemented with the aim of improving adherence to guidelines. Where these interventions have been clinician focused, accumulating evidence suggests that educational interventions are mostly ineffective and result in insignificant changes to overall compliance [17]. It is possible that this might relate to cognitive dissonance, a process in which clinician-focused education fails to engage prescribers effectively, allowing them to ignore the evidence and to continue with their regular habits and practices. Alternative strategies of improving antibiotic management of surgical patients are needed and these may include guidance of clinicians in the institutional process of improvement, which has not as yet been addressed in guidelines [17]. The answer may lie within the principles and imperatives contained with the change of processes in hospitals.

It is highly important that faculty in academic medical centers and teaching hospitals focus on fundamental antibiotic stewardship principles in their preclinical and clinical curricula [18].

The survey found that dissemination of educational materials and educational outreach were developed respectively in 85 cases (62.5%) and 73 (53.7%) surgical departments.

This study has several limitations: with a response rate of just 19.4% we have to consider a response bias, and it is possible that non-participating physicians may have been less interested in ASPs than the participants and therefore it is possible that results are biased towards a better picture than it actually is. Furthermore, the study was conducted in a sample of physicians who participated in the AGORA project, and selecting international experts in the field again potentially resulting in an overrepresentation of hospitals with a considerably active ASP. No stratification or sampling according to medical specialty were pre-planned to ensure that all stakeholders were adequately represented, and finally our questionnaire was self-reported, has not been externally validated, and was evaluated in a single institution. The major strength of the study is its multinational (global) and multidisciplinary approach, to our best knowledge the first in this setting. Thus, our survey provides a benchmark to all interested stakeholders; it can be repeated over time to explore if better uniformity on a global platform of healthcare environments would develop in the future, and may be used to build consensus around the best practices in the field of prevention of surgical infections and rational use of antibiotics in a future project.

The results of the survey showed a heterogeneous organization of ASPs worldwide and demonstrated the need for a cohesive approach in order limit the emergence of antimicrobial resistance in surgical infections. Successful ASPs should focus on collaboration between all healthcare professionals in order to gain the wider-possible acceptance, share knowledge and spread best clinical practices. The main bias of the survey is the low response rate.

ASP:

Antimicrobial stewardship program

Not applicable.

Funding

None.

Availability of data and materials

Not applicable.

Affiliations

1. Department of Surgery, Macerata Hospital, Macerata, Italy
   • Massimo Sartelli
2. Department of Biomedical Sciences and Public Health, Unit of Hygiene, Preventive Medicine and Public Health, Università Politecnica delle Marche, Ancona, Italy
   • Francesco M. Labricciosa
   •  & Pamela Barbadoro
3. Infectious Diseases Unit, Bolzano Central Hospital, Bolzano, Italy
   • Leonardo Pagani
4. General Surgery Department, Papa Giovanni XXIII Hospital, Bergamo, Italy
   • Luca Ansaloni
5. Department of Clinical microbiology, Ampath National Laboratory Services, Milpark Hospital, Johannesburg, South Africa
   • Adrian J. Brink
6. Division of Infectious Diseases and HIV Medicine, Department of Medicine, University of Cape Town, Cape town, South Africa
   • Adrian J. Brink
7. World Alliance against Antibiotics Resistance, Rome, Italy
   • Jean Carlet
8. Center for Critical Care, Anaesthesiology Institute and Department of Outcomes Research, Cleveland Clinic, Cleveland, OH, USA
   • Ashish Khanna
9. Department of Surgery and Obstetrics/Gynaecology, Regional Hospital, Limbe, Cameroon
   • Alain Chichom-Mefire
10. Department of Surgery, Infermi Hospital, Rimini, Italy
    • Federico Coccolini
11. Department of Surgery, Maggiore Hospital, Bologna, Italy
    • Salomone Di Saverio
12. Department of Surgery, Vanderbilt University Medical Center, Nashville, Tennessee, USA
    • Addison K. May
13. Infectious Diseases Unit, Department of Medical and Surgical Sciences, Sant’Orsola Hospital, University of Bologna, Bologna, Italy
    • Pierluigi Viale
14. Division of Infectious Diseases, Cleveland Clinic Akron General, Akron, OH, USA
    • Richard R. Watkins
15. Department of Medicine, Northeast Ohio Medical University, Rootstown, OH, USA
    • Richard R. Watkins
16. Clinical Epidemiology Unit, IRCCS Policlinico San Matteo Foundation, Pavia, Italy
    • Luigia Scudeller
17. Division of Infectious Diseases, Jackson Health System, University of Miami Miller School of Medicine, Miami, FL, USA
    • Lilian M. Abbo
18. Department of Surgery, College of Medicine and Health Sciences, UAE University, Al-Ain, United Arab Emirates
    • Fikri M. Abu-Zidan
19. Department of Surgery, College of Health Sciences, Obafemi Awolowo University, Ile-Ife, Nigeria
    • Abdulrashid K. Adesunkanmi
20. Division of Clinical and Administrative Sciences, College of Pharmacy, Xavier University of Louisiana, New Orleans, LA, USA
    • Sara Al-Dahir
21. Department of Medicine, Division of Infectious Diseases, University of South Carolina School of Medicine, Columbia, SC, USA
    • Majdi N. Al-Hasan
22. General Surgery Department, Bakirkoy Dr Sadi Konuk Training and Research Hospital, Instanbul, Turkey
    • Halil Alis
23. Unit of Prevention and Infection Control, Center of Hospital Epidemiology, São João Hospital Centre, Porto, Portugal
    • Carlos Alves
    •  & Nuno Rocha Pereira
24. Infection Control Committee, Prontobaby Hospital da Criança, Rio de Janeiro, Brazil
    • André R. Araujo da Silva
25. Department of Surgery, University Hospital Center, Zagreb, Croatia
    • Goran Augustin
26. Trauma and Acute Care Surgery Unit, Hadassah Hebrew University Medical Center, Jerusalem, Israel
    • Miklosh Bala
27. Department of Surgery, Weill Cornell Medicine, New York, NY, USA
    • Philip S. Barie
28. Department of General Surgery, Hospital San Juan de Dios de La Serena, La Serena, Chile
    • Marcelo A. Beltrán
29. Academic Department of Surgery, Queen Elizabeth Hospital, Birmingham, UK
    • Aneel Bhangu
30. Department of Microbiology National Reference Laboratory Cheikh Khalifa Ibn Zaid Hospital, Mohammed 6th University of Health Sciences, Casablanca, Morocco
    • Belefquih Bouchra
31. Department of Pathology and Laboratory Medicine, VA Boston HealthCare System, Boston, MA, USA
    • Stephen M. Brecher
32. Department of Pathology and Laboratory Medicine, Boston University School of Medicine, Boston, MA, USA
    • Stephen M. Brecher
33. Department of Surgery, Hospital Clínico Universitario, Santiago de Compostela, Spain
    • Miguel A. Caínzos
34. Hospital Epidemiology and Infectious Diseases, Hospital Universitario Dr Jose Eleuterio Gonzalez, Monterrey, Mexico
    • Adrian Camacho-Ortiz
35. Department of Emergency, Umberto I Hospital, Rome, Italy
    • Marco Catani
36. Department of Pharmacology, Pushpagiri Institute of Medical Sciences and Research Centre, Thiruvalla, Kerala, India
    • Sujith J. Chandy
37. Department of General Surgery, Kuala Krai Hospital, Kuala Krai, Kelantan, Malaysia
    • Asri Che Jusoh
38. Division of Acute Care Surgery, Department of Surgery, University of Michigan, Ann Arbor, MI, USA
    • Jill R. Cherry-Bukowiec
39. Niguarda Hospital, Milano, Italy
    • Osvaldo Chiara
40. Department of General Surgery, Health Sciences University, Samsun Training and Research Hospital, Samsun, Turkey
    • Elif Colak
41. Department of Internal Medicine and Infectious Diseases, University of Cologne, Cologne, Germany
    • Oliver A. Cornely
42. Department of Surgery, Tianjin Nankai Hospital, Nankai Clinical School of Medicine, Tianjin Medical University, Tianjin, China
    • Yunfeng Cui
43. Department General Surgery, Kipshidze Central University Hospital, Tbilisi, Georgia
    • Zaza Demetrashvili
44. Department of Digestive Surgery, Cannes Hospital, Cannes, France
    • Belinda De Simone
45. Department of Critical Care Medicine, Ghent University Hospital, Ghent, Belgium
    • Jan J. De Waele
46. School of Pharmacy, Faculty of Medical Sciences, The University of the West Indies, St. Augustine, Trinidad and Tobago
    • Sameer Dhingra
47. Eric Williams Medical Sciences Complex, Uriah Butler Highway, Champ Fleurs, Trinidad and Tobago
    • Sameer Dhingra
48. Department of Surgery, Versilia Hospita, Lido di Camaiore, Italy
    • Francesco Di Marzo
49. Department of Surgery, University Hospital of Trauma, Tirana, Albania
    • Agron Dogjani
50. School of Pharmacy and Biomedicine, Mongolian National University of Medical Sciences, Ulaanbaatar, Mongolia
    • Gereltuya Dorj
51. Department of Microbiology, Bicêtre Hospital, Paris-Sud University, La Kremlin-Bicêtre, France
    • Laurent Dortet
52. Department of Surgery, John Peter Smith Health Network, Fort Worth, Texas, USA
    • Therese M. Duane
53. Sudan National Public Health Laboratory, Federal Ministry of Health, Khartoum, Sudan
    • Mutasim M. Elmangory
54. Department of Medicine, Infectious Disease Division, King Fahad Medical City, Riyadh, Saudi Arabia
    • Mushira A. Enani
55. Department of Surgery, Virginia Commonwealth University, Richmond, VA, USA
    • Paula Ferrada
56. Department of Surgery, Clinica Foianini, Santa Cruz, Bolivia
    • J. Esteban Foianini
57. Department of Abdominal Surgery, Vladimir City Clinical Hospital of Emergency Medicine, Vladimir, Russia
    • Mahir Gachabayov
58. Department of Surgery, Bharati Vidyapeeth Deemed University Medical College and Hospital, Sangli, Maharashtra, India
    • Chinmay Gandhi
59. Department of General Surgery, Mansoura Faculty of Medicine, Mansoura University, Mansoura, Egypt
    • Wagih Mommtaz Ghnnam
60. Sixth Department of Internal Medicine, Hygeia General Hospital, Athens, Greece
    • Helen Giamarellou
61. Second Department of Surgery, Aretaieion University Hospital, National and Kapodistrian University of Athens, Athens, Greece
    • Georgios Gkiokas
62. Center for Global Health, Mito Kyodo General Hospital, University of Tsukuba, Mito, Ibaraki, Japan
    • Harumi Gomi
63. University Department for Tumours, Sestre Milosrrdnice UHC, Zagreb, Croatia
    • Tatjana Goranovic
64. General and Upper GI Surgery, Queen Elizabeth Hospital, Birmingham, UK
    • Ewen A. Griffiths
65. Peruvian Navy Medical Center, Lima, Peru
    • Rosio I. Guerra Gronerth
66. Department of Gastrointestinal Surgery, Santa Casa Hospital, Campo Grande, Brazil
    • Julio C. Haidamus Monteiro
67. Trauma and Trauma ICU, Inkosi Albert Luthuli Central Hospital and Department of Surgery, University of KwaZulu-Natal, Durban, South Africa
    • Timothy C. Hardcastle
68. Department of General and Thoracic Surgery, University Hospital Giessen, Giessen, Germany
    • Andreas Hecker
69. Department of Surgery, Faculty of Medicine, University of Parakou, BP 123, Parakou, Benin
    • Adrien M. Hodonou
70. Fourth Surgical Department, General Hospital G. Papanikolaou, Medical School, Aristotle University of Thessaloniki, Thessaloniki, Greece
    • Orestis Ioannidis
71. Department of General Surgery, Erzincan University, Faculty of Medicine, Erzincan, Turkey
    • Arda Isik
72. Department of Pharmacy, Lebanese, International University, Beirut, Lebanon
    • Katia A. Iskandar
73. Drug Applied Research Center, Tabriz University of Medical Sciences, Tabriz, Iran
    • Hossein S. Kafil
74. Division of Infectious Diseases, American University of Beirut, Beirut, Lebanon
    • Souha S. Kanj
75. Department of Surgery Philadelphia VA Medical Center, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA
    • Lewis J. Kaplan
76. Department of Microbiology, Gandhi Medical College, Bhopal, India
    • Garima Kapoor
77. Clinic for Emergency Surgery, Medical Faculty University of Belgrade, Belgrade, Serbia
    • Aleksandar R. Karamarkovic
78. Third Department of General Surgery, Jagiellonian University Medical College, Krakow, Poland
    • Jakub Kenig
79. Department of Abdominal Surgery, Regional Hospital of Tienen, Tienen, Belgium
    • Ivan Kerschaever
80. Department of Internal Medicine, Royal Hospital, Muscat, Oman
    • Faryal Khamis
81. Department of Emergency Surgery, City Hospital, Mozyr, Belarus
    • Vladimir Khokha
82. Department of Pharmacology and Therapeutics, College of Health Sciences, Makerere University, Kampala, Uganda
    • Ronald Kiguba
83. Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Republic of Korea
    • Hong B. Kim
84. Department of Internal Medicine, National Cheng Kung University Hospital, Tainan, Taiwan
    • Wen-Chien Ko
85. Department of Primary Care and Emergency Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan
    • Kaoru Koike
86. Department of Surgery n. 2, Higher educational institutions of Ukraine Bukovina State Medical University, Chernivtci City, Ukraine
    • Iryna Kozlovska
87. Section of Critical Care Medicine and Section of Infectious Diseases, Department of Medicine, Medical Microbiology and Pharmacology/Therapeutics, University of Manitoba, Winnipeg, MB, Canada
    • Anand Kumar
88. Hospital Central Dr Ignacio Morones Prieto, San Luis Potosi, Mexico
    • Leonel Lagunes
89. Department of Surgery, Division of Trauma, University of Arizona, Tucson, AZ, USA
    • Rifat Latifi
90. Department of Surgery, Yonsei University College of Medicine, Seoul, South Korea
    • Jae G. Lee
91. Texas Tech University, Health Sciences Center School of Pharmacy, Abilene, TX, USA
    • Young R. Lee
92. Abdominal Center, University Hospital Meilahti, Helsinki, Finland
    • Ari Leppäniemi
93. Department of Surgery, Inling Hospital, Nanjing University School of Medicine, Nanjing, China
    • Yousheng Li
94. Division of Infectious Diseases, Division of Emergency Medicine, Washington University School of Medicine, St. Louis, MO, USA
    • Stephen Y. Liang
95. Clinical Microbiology and Infectious Diseases, School of Pathology, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa
    • Warren Lowman
96. Department of Surgery, Universidad Nacional de Asuncion, Asuncion, Paraguay
    • Gustavo M. Machain
97. Department for Traumatology and Orthopedic Surgery, Cologne Merheim Medical Center (CMMC), University of Witten/Herdecke (UW/H), Cologne, Germany
    • Marc Maegele
98. Second Department of General Surgery, Jagiellonian University Medical College, Krakow, Poland
    • Piotr Major
99. Health Research Program, Institute of Economic and Social Research, University of Zambia, Lusaka, Zambia
    • Sydney Malama
100. Clinical Research Center, Fundacion Valle del Lili, Cali, Colombia
     • Ramiro Manzano-Nunez
101. First Department of Surgery, Tzaneion General Hospital, Piraeus, Greece
     • Athanasios Marinis
102. Service of General Surgery, Hospital Complex of Jaén, Jaén, Spain
     • Isidro Martinez Casas
103. Department of Surgery, Post-Graduate Institute of Medical Sciences, Rohtak, India
     • Sanjay Marwah
104. Servicio de Anestesia y Reanimación, Hospital Universitario La Paz Madrid, Madrid, Spain
     • Emilio Maseda
105. Department of Surgery, Radiology, University Hospital of the West Indies, Kingston, Jamaica
     • Michael E. McFarlane
106. Infectious Diseases Division, Department of Medicine, Prince Mohamed Bin Abdulaziz Hospital, Ministry of Health, Riyadh, Saudi Arabia
     • Ziad Memish
107. Departments of Medicine, Clinical Epidemiology and Biostatistics, and Pathology and Molecular Medicine, McMaster University, Hamilton, ON, Canada
     • Dominik Mertz
108. Second Surgical Clinic, Emergency Hospital of Craiova, Craiova, Romania
     • Cristian Mesina
109. Department of Microbiology, Tribhuvan University Teaching Hospital, Institute of Medicine, Kathmandu, Nepal
     • Shyam K. Mishra
110. Department of Surgery, University of Colorado, Denver Health Medical Center, Denver, CO, USA
     • Ernest E. Moore
111. Department of Surgery, Onandjokwe Hospital, Ondangwa, Namibia
     • Akutu Munyika
112. Infectious Diseases Division, Warren Alpert Medical School of Brown University, Rhode Island Hospital, Providence, RI, USA
     • Eleftherios Mylonakis
113. Department of Surgery, University of Michigan, Ann Arbor, MI, USA
     • Lena Napolitano
114. Department of Surgery, Emergency Hospital of Bucharest, Bucharest, Romania
     • Ionut Negoi
115. Clinic for General Surgery, Clinical Centre, Nis, Serbia
     • Milica D. Nestorovic
116. Center of Anti-Infective Research and Development, Hartford, CT, USA
     • David P. Nicolau
117. Department of Surgery, King Abdullah University Hospital, Irbid, Jordan
     • Abdelkarim H. Omari
118. Department of Surgery and Critical Care, Universidad del Valle, Fundación Valle del Lili, Cali, Colombia
     • Carlos A. Ordonez
119. Intensive Care Medicine Department, Centro Hospitalar São João, University of Porto, Porto, Portugal
     • José-Artur Paiva
120. Department of Microbiology, Grande International Hospital, Dhapasi, Kathmandu, Nepal
     • Narayan D. Pant
121. Department of Surgery, Santa Casa de Sao Paulo School of Medical Sciences, São Paulo, Brazil
     • Jose G. Parreira
122. Department of General and Emergency Surgery, University Hospital Kraków, Kraków, Poland
     • Michal Pędziwiatr
123. Department of Surgery, University of Campinas, Campinas, Brazil
     • Bruno M. Pereira
124. Laboratory of Clinical Microbiology, Department of Infectious Diseases, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
     • Alfredo Ponce-de-Leon
125. Fourth Department of Internal Medicine and Infectious Diseases Unit, National and Kapodstrian University-Medical School, Attikon University General Hospital, Athens, Greece
     • Garyphallia Poulakou
126. John Farman Intensive Care Unit, University Hospitals, NHS Foundation Trust, Cambridge, UK
     • Jacobus Preller
127. Infectious and Tropical Diseases Department, University Hospital of Nancy, and EA 4360 APEMAC, Lorraine University, Nancy, France
     • Céline Pulcini
128. Department of General and Emergency Surgery, Riga East University Hospital ‘Gailezers’, Riga, Latvia
     • Guntars Pupelis
129. Department of Trauma, Hospital Santo Tomas, Panama, Panama
     • Martha Quiodettis
130. National Institute for Health Research, Health Protection Research Unit in Healthcare Associated Infections and Antimicrobial Resistance, Imperial College London, Hammersmith Campus, London, UK
     • Timothy M. Rawson
131. Emergency Post-operative Department, Otavio de Freitas Hospital and Hosvaldo Cruz Hospital, Recife, Brazil
     • Tarcisio Reis
132. Department of General Surgery, Jesenice General Hospital, Jesenice, Slovenia
     • Miran Rems
133. Trauma and Acute Care Service, St Michael’s Hospital, University of Toronto, Toronto, Canada
     • Sandro Rizoli
134. Burns, Trauma and Critical Care Research Centre, The University of Queensland, Brisbane, Queensland, Australia
     • Jason Roberts
135. Unidad Clínica Intercentros de Enfermedades Infecciosas, Microbiología y Medicina Preventiva, Hospitales Universitarios Virgen Macarena y Virgen del Rocío-IBiS and Departamento de Medicina, Universidad de Sevilla, Seville, Spain
     • Jesús Rodríguez-Baño
136. General Surgery Department, Medical University, University Hospital St George, Plovdiv, Bulgaria
     • Boris Sakakushev
137. JPS Health Network, Texas, TX, USA
     • James Sanders
138. Hospital Center Tondela Viseu, Tondela, Portugal
     • Natalia Santos
139. Department of Aeromedical Services for Emergency and Trauma Care, Ehime University Graduate School of Medicine, Ehime, Japan
     • Norio Sato
140. Department of Surgery, University of Virginia Health System, Charlottesville, VA, USA
     • Robert G. Sawyer
141. Department of Surgery, University of Sao Paulo, Ribeirao Preto, Brazil
     • Sandro Scarpelini
142. Unit of Hospital Pharmacy, Macerata Hospital, Macerata, Italy
     • Loredana Scoccia
143. Department of Pharmacology, Postgraduate Institute of Medical Education and Research, Chandigarh, India
     • Nusrat Shafiq
144. Department of General Surgery, Tan Tock Seng Hospital, Tan Tock Seng, Singapore
     • Vishalkumar Shelat
145. Office of Hospital Epidemiology/Infection Prevention and Control, University of Virginia Health System, Charlottesville, VA, USA
     • Costi D. Sifri
146. Department of Surgery, Faculty of Medicine, Thammasat University Hospital, Thammasat University, Pathum Thani, Thailand
     • Boonying Siribumrungwong
147. Department of Gastrointestinal Surgery, Stavanger University Hospital, Stavanger, Norway
     • Kjetil Søreide
148. Department of Clinical Medicine, University of Bergen, Bergen, Norway
     • Kjetil Søreide
149. Department of Emergency Surgery and Critical Care, Centro Medico Imbanaco, Cali, Colombia
     • Rodolfo Soto
150. Department of Surgery, School of Medicine, Pontifícia Universidade Católica do Rio Grande do Sul (PUCRS), Porto Alegre, Brazil
     • Hamilton P. de Souza
151. Department of Surgery, North Estonia Medical Center, Tallinn, Estonia
     • Peep Talving
152. Department of Molecular Biology, Tran Hung Dao Hospital, No 1, Tran Hung Dao Street, Hai Ba Trung Dist, Hanoi, Vietnam
     • Ngo Tat Trung
153. Department of Infectious Diseases, John Peter Smith Health Network, Fort Worth, Texas, USA
     • Jeffrey M. Tessier
154. Institute of Infectious Diseases, Catholic University, Rome, Italy
     • Mario Tumbarello
155. First Department of Surgery—Department of Abdominal, Thoracic Surgery and Traumatology, General University Hospital, Prague, Czech Republic
     • Jan Ulrych
156. Department of Surgery, Medical University of Graz, Graz, Austria
     • Selman Uranues
157. Department of Surgery, Radboud University Nijmegen Medical Center, Nijmegen, The Netherlands
     • Harry Van Goor
158. Department of Surgery, Medical School University of Pécs, Pécs, Hungary
     • Andras Vereczkei
159. Department of Urology, Pediatric Urology and Andrology, Medical Faculty of the Justus Liebig University Giessen, Giessen, Germany
     • Florian Wagenlehner
160. State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affilliated Hospital, Zhejiang University, Zhejiang, China
     • Yonghong Xiao
161. Trauma and Emergency Surgery Department, Chang Gung Memorial Hospital, Taoyuan City, Taiwan
     • Kuo-Ching Yuan
162. Department of Antibiotics and Infection Control, Rudolfstiftung Hospital, Vienna, Austria
     • Agnes Wechsler-Fördös
163. Infection Control Unit, Angers University, CHU d’Angers, Angers, France
     • Jean-Ralph Zahar
164. Division of Trauma and Surgical Critical Care, DeWitt Daughtry Family Department of Surgery, University of Miami, Miami, FL, USA
     • Tanya L. Zakrison
165. Department of Surgery, University of Pittsburgh, Pittsburgh, PA, USA
     • Brian Zuckerbraun
166. VU University Medical Center, Amsterdam, The Netherlands
     • Wietse P. Zuidema
167. Department of General Surgery, Maggiore Hospital, Parma, Italy
     • Fausto Catena

Contributions

MS wrote the first draft of the manuscript. All the authors reviewed the manuscript and approved the final draft.

Corresponding author

Correspondence to Massimo Sartelli.

Ethics approval and consent to participate

Not applicable.

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Not applicable.

Competing interests

The authors declare that they have no competing interests.

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