Perspectives of South American physicians hosting foreign rotators in emergency medicine

Steve O'donnell
David H Adler
PholaphatCharles Inboriboon
Hermenegildo Alvarado
Raul Acosta
Daniel Godoy-Monzon
Perspectives of South American physicians hosting foreign rotators in emergency medicine
O R I G I N A L R E S E A R C H Open Access
Background: Emergency Medicine (EM) is increasingly becoming an international field. The number of fellowships in International EM in the USA is growing along with opportunities to complete international health electives (IHEs) during residency training. The impact on host institutions, however, has not been adequately investigated. The objective of this study is to assess the experience of several South American hospitals hosting foreign EM residents completing IHEs. Methods: Anonymous, semi-structured one-on-one interviews were conducted with physicians working in Emergency Departments in three hospitals in Lima, Peru and one hospital in Buenos Aires, Argentina. All participants reported previously working with EM foreign rotators. Interviews were analyzed qualitatively and coded for common themes. Results: Three department chairs, six residents, and 15 attending physicians were interviewed (total = 24). After qualitative analysis of interviews, two broad theme categories emerged: Benefits and Challenges. Most commonly reported benefits were knowledge sharing about emergency medical systems (78%), medical knowledge transfer (58%), and long-term relationship formation (42%). Top challenges included rotator Spanish language proficiency (70%) lack of reciprocity (58%), and level of training and rotation length (25%). Spanish proficiency related directly to how involved rotators became in patient care (e.g., taking a history, participating in rounds) but was not completely prohibitive, as a majority of physicians interviewed felt comfortable speaking in English. Lack of reciprocity refers to the difficulty of sending host physicians abroad as well as failed attempts at building long-lasting relationships with foreign institutions. Lastly, 25% preferred rotators to stay for at least 1 month and rotate in the last year of EM residency. This latter preference increased knowledge transfer from rotator to host. Conclusions: Our research identified benefits and challenges of IHEs in Emergency Medicine from the perspective of physician hosts in several hospitals in South America. Our results suggest that IHEs function best when EM residents rotate later in residency training and when relationships are maintained and deepened among those involved including host physicians, rotators, and institutions. This leads to future rotators, project collaboration, research, and publications which not only benefit individuals involved but also the wider field of Emergency Medicine.

Background

Every year, physicians enrolled in residency training programs from the USA fan out across the globe to complete International Health Electives (IHEs) in a myriad of institutions that include urban academic medical centers, rural hospitals, and smaller clinics. The manner in which these opportunities are found varies. Some residents independently contact international institutions, others utilize extant electives offered by their home residency programs, and some choose to work with nongovernmental organizations operating in a particular area of the world.

Emergency Medicine (EM), in particular, is becoming an increasingly international field. In the USA, 24% of EM residency training programs offer fellowships in global health and, according to a 2011 study, 71% have global health partnerships and International Health Electives [1,2].

Effects of IHEs on the education and possible career trajectories of medical students and internal medicine resident physicians have been reported. Previous research revealed IHEs increased interest in primary care among medical students, made students more likely to select a residency training program with international opportunities, and created positive attitudinal changes towards public health and cross-cultural communication [3].

A study of resident physicians from a number of different specialties at the Mayo Clinic found educational and personal benefits of IHEs. Educationally, residents encountered a wider variety of pathology than at home institutions, learned to work with limited resources, and saw patients with a wide scope of pathologies and illness that often were not common in the USA. Personally, resident physicians enjoyed experiencing new people and cultures, appreciated the gratitude of the patients they saw, and were exposed to a different level of poverty and suffering since most experiences took place in the developing world [4]. Such research, however, has focused only on the effects on the resident physicians, or rotator, and not the physicians who play host. In addition, the studies above have not been specific to the field of Emergency Medicine.

What do institutions and physicians hosting residents completing an International Health Elective gain from the experience? What are the benefits, to host physicians particularly, of engaging in such activities? What are the challenges? To our knowledge, no study has sought to answer these questions.

Methods

Study design

This qualitative research project was created with the objective of evaluating the experience of physicians working in Emergency Departments that host foreign rotating Emergency Medicine residents completing International Health Electives. Our hypothesis was that institutions and physicians electing to act as hosts must experience benefits from participating in IHEs since the number of IHEs continues to grow. We also imagined that there were inherent problems and barriers. Thus, our research question became: What are the specific benefits and challenges to physician hosts participating in International Health Electives in Emergency Medicine?

An initial literature search was conducted on PubMed looking for previous research on the topic. Search terms included 'International Educational Exchanges', 'International Medical Education', 'International Emergency Medicine', 'International Health Elective', 'Global Health Elective', 'Global Health', AND Emergency Medicine.' The search yielded no articles that focused particularly on host institution and physician experiences with IHEs in Emergency Medicine.

The next question became how best to acquire qualitative data for the study. An e-mail survey was contemplated but the authors were concerned over low response rates and lack of in-depth answers. Using a Qualitative Research Methods reference, the authors decided the methodology that would yield the most in-depth qualitative data would be face-to-face interviews with physician hosts using a survey that would act as a data guide during stakeholder interviews [5]. A qualitative survey was designed to evaluate the experience of physician hosts involved in EM IHEs and was translated into Spanish by a professional translator (Tables 1 and 2).

South American physicians known to be active in the International Section of the American College of Emergency Physicians (ACEP) were contacted by e-mail and asked if they would be willing to collaborate in such an investigation. A physician in Peru and one in Argentina agreed to host the lead author and facilitate one-on-one physician interviews. The lead author traveled to South America to conduct stakeholder interviews from January to April of 2012.

Hospitals

Interviews were conducted at Cayetano Heredia, Dos De Mayo, and Maria Auxiliadora hospitals in Lima, Peru and Hospital Italiano in Buenos Aires, Argentina. The majority of interviews occurred at two sites: Cayetano Heredia and Hospital Italiano.

Cayetano Heredia is a leading academic teaching hospital in Peru. It has an associated medical school and residency training programs in all major medical specialties including one in Emergency Medicine. It also hosts the internationally renowned Gorgas in Tropical Medicine Course that attracts physicians from around the world. Cayetano's EM residency program trains one to two residents per year. Emergency Medicine is a relatively new specialty in Peru, in existence for only 10 to 15 years. Given this fact, most physicians caring for patients in the Emergency Department (ED) have training in either internal medicine or surgery. Because of Cayetano's robust international connections, physicians in the ED frequently have worked with foreign rotators that include Emergency Medicine residents from the USA. In addition, Cayetano hosts medical students, resident physicians, and physicians from North America and Europe in specialties that range from Emergency Medicine, Internal Medicine, Infectious Disease, and Pediatrics among others.

Hospital Italiano is an academic private hospital in Buenos Aires, Argentina that mostly serves patients with some form of private health insurance who tend to be employed and among the more affluent members of the society. It has a medical school and residency training programs in all medical specialties, including one in Emergency Medicine, and is associated with the Universidad Nacional de Buenos Aires. The Emergency Department has hosted EM resident physicians from the USA and Canada. It also hosts physicians-in-training from other South American countries and Western Europe in Emergence Medicine, Pediatrics, and Internal Medicine. The trauma surgery service, which works closely with the Emergency Department, hosts Orthopedic Surgery residents from around the world including Western Europe and North America. In addition, faculty and residents in all specialties are encouraged to travel internationally for conferences, electives, and fellowship opportunities.

Dos de Mayo and Maria Auxiliadora are public hospitals in Lima, Peru.

Interviews

Residents, attending physicians, and department chairs in each Emergency Department visited were asked if they would be willing to be interviewed. An information letter about the study in English and Spanish was provided and a time for the interview agreed upon. Two potential interviewees could not participate because of scheduling conflicts. Otherwise, all those approached to participate did so.

One-on-one interviews were performed with an interview guide (Tables 1 and 2). Follow-up questions were posed on individual topics that arose during the conversations. The majority of interviews were in English as most physicians felt comfortable speaking the language. A minority of interviews were conducted in Spanish. Notes taken during each interview were transcribed and saved electronically on the same day.

Then the 'snowball sampling method' -also known as the chain referral sampling -was utilized to identify study participants. In this method, initial contacts made 'use their social networks to refer the researcher to other people who could potentially participate in or contribute to the study' [5]. Two of the co-authors, Dr. Hermenegildo Alvarado and Dr. Godoy-Monzon, who work in the Emergency Departments in Peru and Argentina, respectively, initially referred the lead author to several physicians to interview. Each study participant was asked if he or she knew of other physicians that might want to take part and this led to additional interviews.  At the investigation's conclusion, all interview transcripts were reviewed, analyzed qualitatively, and coded for common themes according to qualitative research principles [5]. The qualitative survey that acted as an interview guide ensured discussion of specific topics (Tables 1 and 2). The authors had no pre-conceived themes in mind and specifically made survey questions broad and open-ended. For example, question 8 from Table 1 asks, what are the barriers/difficulties of hosting international residents? A repeated answer was that rotators with limited Spanish fluency faced increased challenges engaging in direct patient care. The authors reviewed all interview transcripts and counted the number of participants who specifically mentioned language as a challenge and this topic then became a qualitative theme reported in the results section below.

The study received Institutional Review Board approval from the University of Rochester IRB.

Results

Three department chairs, 6 residents, and 15 attending physicians were interviewed. All had worked with Emergency Medicine residents from North America completing an International Health Elective. Two broad theme categories, benefits and challenges, emerged to describe hosts' experiences of international educational exchanges. Quotations from themed categories are listed in Tables 3  and 4 while Figures 1 and 2 are graphs of the percentage of respondents who mentioned a particular theme.

Benefits of international educational exchanges to hosts

Knowledge sharing about emergency medical systems and practice This was the most common perceived benefit, identified by 78% of those interviewed. Hosts enjoy comparing the medical systems of host and rotator countries, particularly variances in the delivery of pre-hospital care in response to an emergency, methods of triage when a patient arrives to the ED, and the utilization and implementation of guidelines for different clinical situations. Distinct patient populations and antibiotic availability in South America and in Peru especially, compared to the 'developed world', necessitated different clinical approaches. Often a combination of guidelines from the USA, Europe, and World Health Organization was used to develop institutional practice. Hosts liked sharing with rotators how their hospitals' clinical practices evolved and were curious to compare these clinical practices with those in the USA and Europe.

Medical knowledge transfer

Fifty-eight percent reported medical knowledge transfer in the form of discussions, lectures, or skills demonstrations given by visiting residents as a benefit. For example, at one hospital an EM resident from the USA taught the placement of central lines with ultrasound guidance. After the resident departed the practice was continued and maintained.

The faculty at another hospital had collaborated with an EM physician from the University of Arizona to help create an online EM curriculum in Spanish geared towards residents and physicians wishing to engage in continuing medical education. The website, www.reeme. arizona.edu, is particularly popular in Latin America where access to continuing medical education is not as abundant as in the USA or Europe.

Overall, interviewees said education was bidirectional, flowing from rotator to host and host to rotator. Hosts repeatedly relayed that they enjoyed teaching rotators about infectious disease processes uncommon in the

Lack of reciprocity

'It would be invaluable for our residents to visit the U.S. to understand where we are, where we could be, where we have to go, and how we have to improve but to do so requires finding a residency program to work with and the necessary finances'.

Length of stay

'They should stay more than a few weeks to better know the hospital, the people, the culture, the city'.

Level of training

'Rotators should come later in residency. When you travel abroad you should not seek to learn how to practice medicine, but instead learn how medicine is practiced in another country'. developed world as well as procedures and clinical practices utilized in the host hospital.

Long-term relationship formation

Long-term relationship formation can be viewed both as a benefit and a challenge: a benefit when a relationship was solidified and maintained and a challenge when it was not. Discussions in interviews often touched upon the development of relationships. Forty-two percent of the participants mentioned that a successful international educational exchange occurred when a long-term relationship was formed, which could be with an individual, institution, or both. When asked why this was a positive, participants responded that it could lead to other rotators in the future, project creation and collaboration, and research.

Often, foreigners brought expertise and experience in research while the host provided a different clinical setting and patient population. For example, one site was conducting a clinical trial of an anti-coagulant drug that had completed phased clinical trials in the USA, and early results showed different rates of drug efficacy in a South American cohort.

Challenges of international educational exchanges to hosts Rotator Spanish language proficiency

This was the most common challenge, mentioned by 70% of interviewees. The issue of language related specifically to the realm of direct patient care. Spanish fluency is certainly not a requirement for completing an IHE in South America, and a majority of physicians interviewed spoke English with comfort, especially since most must pass an English language proficiency exam in order to graduate from medical school. But when rotators want to participate in the care of patients, as they understandably do during an elective, language can become a barrier. If a rotator has little to no Spanish proficiency, it becomes necessary to pair the rotator with a bilingual physician or to provide a translator. It is much easier to have rotators see patients and integrate them into the medical team if they possess intermediate to advanced mastery of Spanish. It was intrinsically understood by most South American physicians in the survey that part of the reason that some rotators came to South America was to work on language skills. One ED chair explicitly encouraged concomitant clinical rotations and language classes during electives.

Lack of reciprocity

Fifty-eight percent of host physicians mentioned something that was placed into this themed category. For example, one department chair wished his EM residents were able to do a rotation in the USA. This, however, was prohibitively difficult due to the high cost and bureaucratic barriers of entrance to the USA as well as reluctance on the part of some US hospitals to host foreign physicians.

As mentioned in the benefits section above, the hosts desired the creation of long-lasting relationships. Many interviewees, however, stated that some rotators came and were never heard from again and contacts with outside institutions broke down. When these things occurred, it was a source of frustration and viewed as a loss of investment of time and effort.

Level of training and rotation length

Twenty-five percent said they wanted a rotator to stay for at least a month. This allowed time for the hosts and rotator to adapt to one another and for the rotator to learn about, and be integrated into, the host's medical system.

In addition, the same percentage of hosts preferred when residents came in the later stages of training or to have an attending accompanying residents. This relieved the host from having to teach basic skills to residents and facilitated increased knowledge transfer from rotator to host. One institution asked every resident to prepare a talk on a topic of their choice to present during grand rounds or similar didactic conference.

Discussion

We believe this qualitative research study is one of the first to report on benefits and challenges experienced by physicians who host Emergency Medicine residents completing International Health Electives. From 24 interviews with physician hosts, themed benefits and challenges of IHEs emerged. Benefits included knowledge sharing about Emergency Medical Systems and practice, bidirectional knowledge acquisition and education, and long-term relationship formation. Reported challenges included language proficiency, lack of reciprocity, level of training of the resident, and length of stay by the resident. Four Emergency Departments in South America, specifically in Peru and Argentina, were the sites for this investigation.

Collectively, the benefits listed above may aid in the better delivery of emergency medical care throughout the world in different resource settings. A systematic review of existing research is the hallmark of advancing medical practice. It is the basis upon which clinical guidelines are created. But as Arnold and colleagues point out, the majority of studies underpinning reviews are performed in countries with sophisticated health care systems, 'thus not necessarily reflecting the burden of disease or resources available in developing economies' [6]. Our research suggests that participants in IHEs, both hosts and rotators, gain broader knowledge of the diversity of Emergency Medical Systems. Long-term relationships also lead to local research projects that have more relevance to host populations. Hence, IHEs represent one important mechanism of adapting existing EM guidelines and protocols to varying local realities throughout the world and for building a broader evidence base upon which general, widely implementable emergency medical care principles can be created.

We believe that the identified challenges are not prohibitive to the continued expansion of these experiences. The Council of Emergency Medicine Resident Directors (CORD), during their 2011 Academic Assembly, developed consensus recommendations to enhance the global health education of Emergency Medicine residents. They recommended standardizing global health application materials, standardizing resident evaluations during global health rotations, creating a global health site database, and incorporating a method to evaluate global health sites [2]. We support standardization, evaluation, and transparency, and believe they will only improve IHEs in the future. Implicit in CORD's recommendations, and necessary for success in our opinion, is the continual input and feedback from those who host EM trainees. A thorough understanding of the IHE experience -from the perspectives of both host and rotator -will ultimately lead to the design of electives that yield the highest educational benefit.

Additionally, we would recommend that US EM professional organizations continue to offer, and increase when possible, scholarships and grants for foreign physicians to rotate in US hospitals.

Limitations

This qualitative research project investigates physician host experiences of IHEs offered to foreign EM residents in four hospitals in Peru and Argentina. It is uncertain how generalizable and applicable these results are to other places in the world where IHEs occur. In addition, only large, urban hospitals were visited and thus the results might not be germane to smaller hospitals or more rural health facilities.

As mentioned in the Methods section, participants in the study were identified utilizing the snowball method whereby initial in-country contacts refer the investigator to potential additional contacts. Snowball sampling will always have selection bias because of purposive sampling. This is mitigated by the wide variety of subjects identified and by having a mixed team of researchers from several countries.

The number of interviews obtained was constrained by the finite amount of time the lead author had at each site and the availability of participants in that time frame. Therefore, the data is susceptible to some convenience sampling. However, in three out of four sites, an interview with the Emergency Department Chair was obtained which provided consistent viewpoints from those in leadership positions. In addition, out of all interviews attempted, only two could not be performed due to scheduling conflicts.

Finally, this qualitative research study does not comprehensively assess EM IHEs. As identified by the 2011 CORD Academic Assembly, a helpful step would be to collect and analyze evaluation data from residents who completed global health rotations throughout the world. Furthermore, a future investigation that tracked EM residents after they completed global health rotations to understand how these experiences impacted future career trajectories would be helpful to better comprehend the impact of IHEs.

Conclusions

Our research identified benefits and challenges of international educational exchanges in Emergency Medicine from the perspective of physician hosts in several hospitals in South America. Our results suggest that International Health Electives function best when relationships are maintained and deepened among those involved including host physicians, rotators, and institutions. This leads to the expression of clear expectations from all parties of what the international health elective should entail. Relationship maintenance creates opportunities for more rotators in the future, maximal educational benefits for rotator and host, and the possibility to collaborate on new projects and research. Thus, IHEs have the potential to expand the EM knowledge base, to adapt existing EM guidelines and protocols to local realities, and to identify broadly applicable principles of emergency medical care in multiple resource settings.

Interest among US EM trainees in participating in international electives is on the rise. Almost threequarters of US EM residencies report having opportunities in global health and about one-quarter offer a fellowship specifically in the field [1,2]. As participation in global health by US trainees continues to increase, future work should strive to ensure the optimization of global health opportunities. The Council of Emergency Medicine Residency Directors' recommendations would help standardize the global health elective process for residents. Additional feedback from residents when they return from abroad as well as tracking their future career trajectories would lead to better understanding of the impact of global health experiences. Finally, it is vital to consistently elicit input and perspective from those who graciously agree to serve as host.

'
Challenges' theme quotations from in-person interviews with South American physicians working in Emergency Departments hosting Emergency Medicine residents and other foreign rotators (total interviews = 24).

Figure 1
1Percentages of South American physician interviewees mentioning specific benefits while hosting foreign rotators in ED.

Figure 2
2Percentages of South American physician interviewees mentioning specific challenges while hosting foreign rotators in ED.

Table 1
1Guiding questions, in English, for semi-structured interviewsQuestions for Latin American staff 1 Describe your experience working with physicians from the U.S. What do you believe to be the importance of international educational experiences in EM residency training today?10 What are your plans for future international educational exchanges?11 With whom else should I talk to about these issues?2 What are the benefits of having U.S. physicians work in your
hospital? Detriments?

3 Do you plan to train in another country in the future? If so,
please describe these plans.

4 How does your residency program support international
educational opportunities for residents?

5 Does your program host residents/physicians from foreign countries?
If so, please describe these programs.

6 Describe what international residents do at your institution.
What are their responsibilities?

7 What are the benefits from hosting international residents?

8 What are the barriers/difficulties?

9

Table 2
2Guiding questions, in Spanish, for semistructured interviews Preguntas para el Personal Latino Americano 1 Describa su experiencia trabajando con los médicos de los Estados Unidos. 2 ¿Cuáles son los beneficios de tener médicos de los Estados Unidos que trabajan en su hospital? ¿Desventajas? 3 ¿Tiene usted planes para capacitarse en otro país en el futuro? Si este es el caso, por favor describa estos planes. 4 ¿Cómo apoya su programa de residencia las oportunidades educativas internacionales para los residentes? 5 ¿Acepta su programa residentes/médicos de países extranjeros? Si este es el caso, por favor describa estos programas. 6 Describa lo que los residentes internacionales hacen en su institución. ¿Cuáles son sus responsabilidades? 7 ¿Cuáles son las experiencias beneficiosas de aceptar residentes internacionales 8 ¿Cuáles son las barreras/dificultades? 9 ¿Qué cree usted es la importancia de experiencias educativas internacionales en la capacitación en la residencia para Médicos de Emergencia hoy día? 10 ¿Cuáles son sus planes para intercambios educativos internacionales en el futuro?

Table 3
3Benefits to hosts participating in international educational exchangesBenefit
Quotations from interviews

Knowledge sharing about
EM systems and practice

'Learning about how another system works
in different countries is great and it makes
you think about your own system, its
administration, and what advantages
new technology can bring'.

Medical knowledge
transfer

'A visiting resident taught us how to start
central lines with ultrasound guidance.
Now several of us use ultrasound whenever
possible to start our central lines'.

Long-term relationship
formation

'My department maintains contact with the
physicians who have worked here from
around the world. Over time we have built a
network that produces research projects and
future exchanges'.

'Benefits' theme quotations from in-person interviews with South American
physicians working in Emergency Departments hosting Emergency Medicine
residents and other foreign rotators (total interviews = 24).

Table 4
4Challenges to hosts participating in international educational exchangesChallenge Quotations from interviews

Language
proficiency

'The more you can speak Spanish, the more you can
participate with interviewing patients and the medical team'.

http://www.intjem.com/content/7/1/24
AcknowledgementsThis study was funded by a research fellowship award from the University of Rochester School of Medicine and Dentistry granted to the lead author while he was a medical student.Competing interestsThe authors declare that they have no competing interests.Authors' contributions SO traveled to the hospitals mentioned in the study and conducted one-on-one stakeholder interviews. SO, DA, and PI collaborated on study design, surveys used for interviews, and qualitative data analysis. HA, RA, and DM helped identify the sites visited in the study and provided feedback and advice for study implementation. All authors read and approved the final manuscript.Submit your manuscript to a journal and benefi t from:7 Convenient online submission 7 Rigorous peer review 7 Immediate publication on acceptance 7 Open access: articles freely available online 7 High visibility within the fi eld 7 Retaining the copyright to your article Submit your next manuscript at 7 springeropen.com
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Optimizing global health experiences in emergency medicine residency programs: a consensus statement from the Council of Emergency Medicine Residency Directors 2011 Academic Assembly global health specialty track. J P Tupesis, C Babcock, D Char, K Alagappan, B Hexom, G B Kapur, Int J Emerg Med. 20121Tupesis JP, Babcock C, Char D, Alagappan K, Hexom B, Kapur GB: Optimizing global health experiences in emergency medicine residency programs: a consensus statement from the Council of Emergency Medicine Residency Directors 2011 Academic Assembly global health specialty track. Int J Emerg Med 2012, 5(1):5-43.

Educational effects of international health electives on U.S. and Canadian medical students and residents: a literature review. M J Thompson, M K Huntington, D D Hunt, L E Pinsky, J J Brodie, Acad Med. 783Thompson MJ, Huntington MK, Hunt DD, Pinsky LE, Brodie JJ: Educational effects of international health electives on U.S. and Canadian medical students and residents: a literature review. Acad Med 2003, 78(3):342-347.

Eight years of the Mayo International Health Program: what an international elective adds to resident education. A P Sawatsky, D J Rosenman, S P Merry, F S Mcdonald, Mayo Clin Proc. 858Sawatsky AP, Rosenman DJ, Merry SP, McDonald FS: Eight years of the Mayo International Health Program: what an international elective adds to resident education. Mayo Clin Proc 2010, 85(8):734-741.

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Knowledge translation in international emergency medical care. L K Arnold, H Alomran, V Anantharaman, P Halpern, M Hauswald, P Malmquist, E Molyneux, B Rajapakse, M Ranney, J Razzak, 10.1186/s12245-014-0024-5Acad Emerg Med. 1411Arnold LK, Alomran H, Anantharaman V, Halpern P, Hauswald M, Malmquist P, Molyneux E, Rajapakse B, Ranney M, Razzak J: Knowledge translation in international emergency medical care. Acad Emerg Med 2007, 14(11):1047-1051. doi:10.1186/s12245-014-0024-5

Perspectives of South American physicians hosting foreign rotators in emergency medicine. O'donnell, International Journal of Emergency Medicine. 24Cite this article asCite this article as: O'Donnell et al.: Perspectives of South American physicians hosting foreign rotators in emergency medicine. International Journal of Emergency Medicine 2014 7:24.


Open Access
2017-2019.

Ming Tat firstname.lastname@example.com
Ng
Department of Pharmacy
Tan Tock Seng Hospital
SingaporeSingapore

Department of Pharmacy
Tan Tock Seng Hospital
Singapore, Singapore

Hoon Sock
Tan
Department of Pharmacy
Tan Tock Seng Hospital
SingaporeSingapore

Department of Pharmacy
Tan Tock Seng Hospital
Singapore, Singapore

Shi Thong Heng
Department of Pharmacy
Tan Tock Seng Hospital
SingaporeSingapore

Department of Pharmacy
Tan Tock Seng Hospital
Singapore, Singapore

Hui Lin Tay
Department of Pharmacy
Tan Tock Seng Hospital
SingaporeSingapore

Department of Pharmacy
Tan Tock Seng Hospital
Singapore, Singapore

Min Yi Yap
Department of Pharmacy
Tan Tock Seng Hospital
SingaporeSingapore

Department of Pharmacy
Tan Tock Seng Hospital
Singapore, Singapore

Boon Hou Chua
Department of Pharmacy
Tan Tock Seng Hospital
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Department of Pharmacy
Tan Tock Seng Hospital
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Christine B Teng
Department of Pharmacy
Tan Tock Seng Hospital
SingaporeSingapore

Department of Pharmacy
Tan Tock Seng Hospital
Singapore, Singapore

Department of Pharmacy
Faculty of Science
National University of Singa-pore
Singapore, Singapore

David C Lye
Department of Infectious Diseases
National Centre for Infectious Diseases
Singapore, Singapore

Department of Infec-tious Diseases
Tan Tock Seng Hospital
Singapore, Singapore

Lee Kong Chian School of Medicine
Nanyang Technological University
Singapore, Singapore

Yong Loo Lin School of Medicine
National University of Singapore
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Tau Hong Lee
Department of Infectious Diseases
National Centre for Infectious Diseases
Singapore, Singapore

Department of Infec-tious Diseases
Tan Tock Seng Hospital
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Lee Kong Chian School of Medicine
Nanyang Technological University
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Yong Loo Lin School of Medicine
National University of Singapore
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Open Access
2017-2019.10.1186/s13756-021-00898-8Received: 23 October 2020 Accepted: 21 January 2021Ng et al. Antimicrob Resist Infect Control (2021) 10:28 RESEARCH Effects of coronavirus disease 2019 (COVID-19) pandemic on antimicrobial prevalence and prescribing in a tertiary hospital in Singapore Results: The prevalence of antimicrobial prescribing (55% in 2015 to 49% in 2019 and 47% in 2020, p = 0.02) and antibacterials (54% in 2015 to 45% in 2019 and 42% in 2020, p < 0.01) have been reducing despite the pandemic. Antimicrobial prescribing in infectious disease wards with suspected or confirmed COVID-19 cases was 29% in 2020. Overall, antimicrobial prescribing quality indicators continued to improve (e.g. reasons in notes, 91% in 2015 to 94% in 2019 and 97% in 2020, p < 0.01) or remained stable (compliance to guideline, 71% in 2015 to 62% in 2019 and 73% in 2020, p = 0.08). Conclusion: During the COVID-19 pandemic, there was no increase in antimicrobial prescribing and no significant differences in antimicrobial prescribing quality indicators. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article' s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article' s to the data made available in this article, unless otherwise stated in a credit line to the data. *Correspondence: Full list of author information is available at the end of the articleCOVID-19Antimicrobial prevalenceSingaporeResourcesAntimicrobial stewardshipPandemic
Background: The deployment of antimicrobial stewardship (AMS) teams to deal with the COVID-19 pandemic can lead to a loss of developed frameworks, best practices and leadership resulting in adverse impact on antimicrobial prescribing and resistance. We aim to investigate effects of reduction in AMS resources during the COVID-19 pandemic on antimicrobial prescribing.Methods:One of 5 full-time equivalent AMS pharmacists was deployed to support pandemic work and AMS rounds with infectious disease physicians were reduced from 5 to 2 times a week. A survey in acute inpatients was conducted using the Global Point Prevalence Survey methodology in July 2020 and compared with those in 2015 and

Background

The global response to the coronavirus disease 2019 (COVID-19) pandemic has focused on controlling the spread of infection and development of treatment and vaccines [1]. The typical symptoms of patients with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection are fever, sore throat, fatigue, cough or dyspnea [2]. These symptoms may prompt clinicians to start antibiotics to treat community-acquired pneumonia or COVID-19 with secondary bacterial infection. In a review of patients with coronavirus infections, 62/806(8%) of patients with COVID-19 were reported to have bacterial or fungal co-infections. However, among COVID-19 patients, 1450 of 2010 (72%) received antibiotics. These agents tended to be broad-spectrum and empiric [3]. As the pandemic continues, treatment of patients with respiratory symptoms can drive increasing rates of empiric antimicrobial therapy.

Antimicrobial stewardship (AMS) teams generally comprise infectious disease physicians, AMS pharmacists or pharmacists with special interest in infectious diseases. Many of these individuals are re-deployed to focus on patient care and other areas directly related to COVID-19 during the pandemic. This can lead to loss of established AMS frameworks, best practices, and leadership in healthcare institutions, resulting in adverse impact on antimicrobial resistance in the long term [4]. It is important that healthcare systems keep AMS in consideration as they channel resources to control COVID-19 [5].

The Global Point Prevalence Survey (Global-PPS) first conducted in 2015 provides a rapid way to understand the quantity and quality of antimicrobial prescribing [6]. Using a standardised methodology over the years, the surveys allow comparisons to be made between time periods [7]. Information from these surveys can be used for tailor made surveillance and help develop prescribing guidelines and educational initiatives to improve antimicrobial use. The antimicrobial stewardship team at Tan Tock Seng Hospital (TTSH) and the National Centre for Infectious Diseases (NCID), Singapore, comprise a team of 5 full-time equivalent (FTE) pharmacists who provided daily prospective review and feedback (PRF) on piperacillin-tazobactam, carbapenem and ciprofloxacin use. They work closely with a team of 5 Infectious diseases (ID) physicians who take turns to perform PRF on complex cases. Since the start of the pandemic in January 2020, 1 full-time equivalent of AMS pharmacist was deployed to support COVID-19 clinical trials and only 1-2 ID physicians continued with PRF once to twice a week. The other ID physicians were deployed to duties related to the pandemic.

In this study, we aimed to compare the prevalence of antimicrobial use and quality indicators in hospitalised patients using the Global-PPS methodology from 2015 and 2017-2020 to investigate the effects of the deployment of AMS manpower resources to support the ongoing COVID-19 efforts.

Methods

Study design and setting

This was a retrospective study comparing 5 cross-sectional surveys conducted in years 2015, 2017, 2018, 2019 and 2020. The survey methodology was in accordance with Global-PPS study protocol in 2015 and 2017 -2020. They were conducted in acute care wards of TTSH, a 1500-bed university teaching adult hospital in Singapore, in the 5 years. The new 330-bed NCID, located in the same campus, was included in years 2019 and 2020. NCID, is a purpose-built infectious disease management facility. During the COVID-19 pandemic, high risk suspect cases were admitted, isolated and tested for SARS-CoV-2. Low risk suspect cases were tested and discharged to self-isolate at home. Phone surveillance for symptom progression was performed and patients with persistent symptoms or positive swab results were recalled for further evaluation or isolation. Close contacts of confirmed COVID-19 patients were identified and place in quarantine either at home or government quarantine facilities while casual contacts were placed o phone surveillance [8]. The Global-PPS was conducted on any day except weekends and public holidays by the AMS pharmacists. The 5 surveys were conducted in March 2015, November 2017, October 2018, April 2019 and July 2020. All inpatients were included for audit at 0800 h of the chosen survey day and the survey was completed over several days. Following the Global-PPS annual protocols, antimicrobials for topical use were excluded.

Data

Data collection was completed using Global-PPS methodology specified forms. The ward form included the total number of admitted inpatients at 0800 h on survey day and the total number of available inpatient beds in the surveyed wards. The patient form was only completed if patient included in the survey was on at least 1 systemic antimicrobial at 0800 h on survey day. Patient data was collected using electronic medical records. No patient identifier was collected. The survey was completed without questioning the diagnoses indicated by medical teams. The type of data collected were described previously (https ://www.globa l-pps.com/) [6]. Specifically, age, ward type, type of antimicrobial, diagnosis, type of indication (i.e. whether prophylactic use, or for community-onset or healthcare-associated infections), whether treatment was empiric or targeted, and quality indicators of antimicrobial prescribing were collected. Compliance to institutional guidelines was only reported for empiric use and surgical prophylaxis. Quality indicators of antimicrobial use considered documented reason for antimicrobial treatment, and presence of stop/ review dates. Hospital antimicrobial utilization was also collected for the period before and during COVID-19 pandemic for changes in antimicrobial prescribing behaviours. Utilization data was extracted from pharmacy dispensing records between January 2019 and September 2020, including April 2020, which was the peak of the COVID-19 pandemic in Singapore [9]. All antimicrobials excluding antituberculosis drugs, antiretrovirals and antimalarials were monitored. Daily defined dose (DDD) was used as the measurement unit for antimicrobial utilization, which was adjusted for every 1000 patient days per month.

The Global-PPS protocol remained consistent over the years with minor changes. In 2018, antivirals other than neuraminidase inhibitors were added. The other changes were described in the Additional file 1. The study was approved by local institutional review board (DSRB reference: 2015/00015, 2017/01012, 2019/00768, 2020/01045).

Statistical analysis

Comparisons of proportions for binary variables were performed using chi-squared test for trend in proportions where appropriate. The median of continuous variables was compared using the Kruskal-Wallis test. A P-value of < 0.05 was used as the level of significance. The statistical tests were performed using R software version 3.5.0. Segmented regression analysis was performed to describe the utilization trends before and after the peak of the pandemic. The Stata package ITSA was used and the statistics were estimated using ordinary least squares regression and Newey-West regression was specified to account for an error structure that is assumed to be heteroskedastic and autocorrelated at lag 0. The autocorrelation of each model was tested using Cumby-Huizinga general test and visual inspection of autocorrelation and partial autocorrelation plots.

Results

The first COVID-19 case was cared for in our facility on 2 nd February 2020. On 15 July 2020, there were 65 inpatients with confirmed COVID-19 and 64 new admissions for suspected COVID-19. A cumulative total of 8952 COVID-19 patients had been admitted to our facility, of which 16 had died. Another 6105 admissions had been investigated for suspected COVID-19. In terms of antimicrobial utilization, there was a significant reduction of 361.46 DDD/1000 patient days/month (p < 0.01) before and after the peak of the COVID-19 pandemic in Singapore in April 2020 [9]. At the point of PPS survey (July 2020), the total antimicrobial utilization was 1849.71 DDD/1000 patient days/month. (Fig. 1).

The Global-PPS dataset from 2015 and 2017-2020 included all acute inpatient wards. The median number of available beds on survey day annually was 1357 (range 1135-1375). The median number of patients admitted was 1173 (range 1150-1214). The median number of adult wards surveyed annually was 44 (range 35-50). On the survey day in July 2020, 4 surgical and 2 medical wards were closed due to COVID-19; 2 intensive care wards (ICU) and 9 infectious disease wards (AMW-ID) catered to 199 suspected and confirmed COVID-19 patients. Among these patients, 15   were similar but the proportion of surgical patients were lower in 2020 (19%) compared to previous years (range 22-27%).

There was a median of 780 (range 755-839) antimicrobial prescriptions on the survey day. Antibacterials for systemic use, corresponding to World Health Organization anatomical therapeutic chemical (WHO ATC) code J01, accounted for 84% of total prescriptions with a median of 665 (range 615-727) on survey day. Antimycotic (ATC code J02) prescriptions accounted for 2% of total prescriptions with a median of 18 (range 11-20) prescriptions, antimycobacterials (ATC code J04) accounted for 6% of total prescriptions with a median of 50 (range 21-52) on survey day. Intestinal anti-infectives (ATC code A07A) and antivirals for systemic use (ATC code J05) accounted for 1% and 7% of total prescriptions and median of 6 (range 1-14) and 70 (range 8-83) prescriptions on survey day. Overall, the mean prevalence of patients on antimicrobials was 49% (range, 45-55%) and varied significantly over the years. It has reduced from 55% in 2015 to 49% in 2019 and 47% in 2020 (p-value of test for trend in proportions = 0.02). Similar trends were observed in terms of antibacterials for systemic use (ATC code J01) from 54% in 2015 to 45% in 2019 and 42% in 2020 (p-value of test for trend in proportions < 0.01) ( Table 1).

Overall, the prevalence of patients on antimicrobials was reducing but not significantly different in the medical (56% in 2015 to 47% in 2020) and haematology-oncology wards (73%, 2015 to 66%, 2020) (p-value of test for trend in proportions > 0.05). The proportion of patients on antimicrobials increased significantly in the surgical wards (49%, 2015 to 58%, 2020) (p-value of test for trend in proportions = 0.03). In intensive care wards, proportion of patients on antimicrobials decreased from 2015 to 2018 but increased to a high of 81% in 2019 (p-value of test for trend in proportions = 0.18). In 2020, antimicrobial use in the infectious disease wards which housed suspected or confirmed COVID-19 cases was 29%. (Table 2).

Over the years, common indications for antimicrobial use were community acquired infections (47-63%) and healthcare-associated infections (26-39%). The top reasons for starting antibiotics were pneumonia or lower respiratory tract infections (26-34%), skin and soft tissue infections (11-15%), intra-abdominal infections (9-10%), lower urinary tract infections (4-12%), and upper urinary tract infections (3-13%) ( Table 3).

Forty-seven different systemic antibacterials were used in patients admitted to adult wards on the survey days. The penicillins were the most prescribed class (1562/3346 antibacterial prescriptions, 47%), comprising mainly amoxicillin with beta-lactamase inhibitor (1125/3346, 34%) and piperacillin with betalactamase inhibitor (300/3346, 9%). The second and third most prescribed antibacterials were cephalosporins (462/3346,14%)-mainly cefazolin, ceftriaxone, and fluoroquinolones (355/3346, 11%)-mainly ciprofloxacin and levofloxacin. The overall antibacterial utilisation trends  For quality indicators, there was an overall improvement in terms of documented reasons for giving antimicrobials in the medical records: 91% in 2015 to 94% in 2019 and 97% in 2020 (p-value of test for trend in proportions < 0.01); this trend was similarly observed in surgical patients (Additional file 1: Table 2). The documentation of stop/review date improved from 53% in 2015 to 56% in 2019 and 61% in 2020 (p-value of test

Table 3 Indications of antimicrobials use and top 10 reasons to treat inpatients with at least one antibiotic for systemic use (J01), year 2015-2020

Patients recorded with more than one diagnosis were counted by number of diagnoses

Patients not treated with antibiotics for systemic use, but who were treated with other antimicrobials (e.g., antimalarials) were not included † Includes cellulitis, wound infections (including surgical site infections), deep soft tissue infections not involving bone (e.g., infected pressure or diabetic ulcers, abscesses). ‡Includes intra-abdominal sepsis and hepatobiliary and intra-abdominal abscesses. §Includes catheter-related urinary tract infections and pyelonephritis **Includes septic arthritis (including prosthetic joints) and osteomyelitis † † Includes sepsis syndrome or septic shock with no clear anatomical site for trend in proportions < 0.01). Overall compliance to guideline did not change significantly from 71% in 2015 to 62% in 2019 and 73% in 2020 (p-value of test for trend in proportions = 0.08); the compliance rate did not significantly change over the years among surgical patients (p-value of test for trend in proportions = 0.493), medical patients (p-value of test for trend in proportions = 0.435), and intensive care patients (p-value of test for trend in proportions = 0.056) respectively (Additional file 1: Tables 1-3). The proportion of surgical antimicrobial prophylaxis prescriptions being ordered for more than 1 day did not significantly decrease over time: 56% in 2015 to 69% in 2019 and 52% in 2020 (p-value of test for trend in proportions = 0.76) ( Table 4). The number of courses of carbapenems, piperacillintazobactam and ciprofloxacin reduced by 17% from 7046 during the 6-month period from July to December 2019 to 5852 during the next 6-month period from January to June 2020. However, the proportion of courses reviewed by AMS team were maintained at 4834/7046 (69%) compared to 4141/5853 (71%). The number of recommendations made and accepted were also maintained during both periods, 1151/1440 (80%) vs. 1204/1537 (78%).

Discussion

Despite the re-deployment of our AMS manpower, the prevalence of antimicrobial and antibacterial use did not increase despite the COVID-19 pandemic. Antimicrobial utilization was very much lower at the peak of the COVID-19 pandemic as hospital resources pivoted to taking care of COVID-19 patients. In 2020, about a quarter of patients in the infectious disease wards were on antimicrobials. There were fewer surgical patients but there was a higher proportion of antibiotic use among them in 2020 due to the cancellation of elective and postponement of non-urgent procedures. Therefore, surgical inpatients could have been sicker and more often required antibiotics.  Among the antibacterials audited via prospective review and feedback, only meropenem prevalence showed an increase. However, this trend started before the pandemic. Overall, antimicrobial prescribing quality indicators continued to improve or remained stable. We found that only 29% of patients with suspected or confirmed COVID-19 were on antibacterial agents. This is in stark contrast to 71.9%, reported by Langford et al. in a recently published meta-analysis and 71% reported by Nori et al. during the March to May pandemic surge period in New York [10,11]. This may be accounted by rapid confirmatory diagnosis of SARS-CoV-2 infection as the cause of pneumonia in our setting, and the vast majority of patients having non-severe infections [12]. To prepare for the pandemic, the AMS team was requested by the hospital management to work with hospital pharmacy to provide recommendations on alternative antimicrobial use in anticipation of possible drug shortfall. In addition, the team briefed the hospital senior management on the possibilities of antibiotic supply disruption and shared best practices and common inappropriate antibiotic use previously observed during audit and feedback. These case vignettes were shared with all doctors and pharmacists via monthly email messages. It is possible that these activities reminded the prescribers on the ground to be more judicious in antimicrobial use.

The sustainable culture of judicious antimicrobial use was developed over the years at our institutions. This could have contributed to continued practice of appropriate prescribing. Since 2009, our multi-disciplinary AMS programme introduced guidelines and performed prospective review and feedback. These measures were augmented by computerised clinical decision support systems (introduced in 2011) and educational efforts to engage healthcare providers and the public on appropriate use of antimicrobials. [13][14][15] Results of the PPS were shared with the hospital management and senior doctors to raise awareness on the high prevalence of antimicrobial prescribing. These activities may have driven the improvement in some antimicrobial prescribing quality indicators and reduced the prevalence of antimicrobials among acute inpatients. Collectively, the AMS efforts over the years could have paid dividends during the time of COVID-19 pandemic. The maturity of antimicrobial prescribing habits may have sustained the practices even when AMS resources were substantially reduced.

While the AMS team reduced in size, the team continued prospective review and feedback during the pandemic, focussing on meropenem, piperacillin-tazobactam and oral ciprofloxacin use. The smaller team of pharmacists and physicians maintained the review rate of these antibiotics and provided comparable number of recommendations with similar acceptance rate. Although these constituted a small proportion of the total antimicrobials used, the continued presence of the AMS team and the recommended interventions may have encouraged prescribers to maintain judicious use of antibiotics.

As these were point prevalence studies, variation within and between survey periods may not be sufficiently accounted for. The appropriateness of antimicrobial duration and the impact of duration of therapy on antimicrobial utilisation were not reported. The compliance to guidelines was assessed solely based on the prescribing doctor's documented diagnosis or reasons of use. Other opportunities for improved antimicrobial prescribing such as dose, route and duration were not assessed.

Conclusion

As COVID-19 diverted resources from AMS teams, there was no significant deterioration in trends of antimicrobial use or reduction in quality of antimicrobial prescribing at our institutions. Despite a smaller AMS team, the presence of an established multi-disciplinary AMS programme prior to the COVID-19 pandemic managed to keep antimicrobial prevalence and quality of antimicrobial prescribing stable in our institutions. As the pandemic continues, attention must be given to control the amount and appropriateness of antimicrobial use. AMS resources and efforts should be enhanced especially in areas where AMS practices are still in early stages of development. As the global momentum of controlling antimicrobial resistance accumulate in last few years, careful and deliberate actions must be taken now so that the COVID-19 pandemic does not derail this process.

Supplementary Information

The online version contains supplementary material available at https ://doi. org/10.1186/s1375 6-021-00898 -8.

Fig. 1
1Segmented regression analysis of monthly total antimicrobial utilization in the hospital from January 2019 till September 2020, in daily defined dose (DDD) per 1000 patient days (April 2020 was observed as the peak of COVID-19 pandemic in Singapore)

were stable since 2015 (
2015Fig. 2). Amoxicillin with betalactamase inhibitor proportion increased from 28.2% in 2015 to 37.0% in 2017, then decreased to 36.1% in 2019 and 34.8% in 2020. Piperacillin with beta-lactamase inhibitor proportion was on downward trend from 10.7% in 2015 to 9.2% in 2019 and 7.0% in 2020. Carbapenem use increased from 5.1% in 2015 to 9.3% in 2017, then decreased to 5.9% in 2019 and 8.8% in 2020, this change was mainly driven by Meropenem (3.9% in 2015 to 5.1% in 2019 and 7.6% in 2020). Ciprofloxacin proportion changed from 8.3% in 2015 to 9.3% in 2019 and 5.0% in 2020.

Fig. 2
2Anti-bacterial use from 2015 to 2020

Additional file 1 .
1Percentage of Empiric antimicrobial use and prescribing quality indicators for medical, surgical and intensive care patients respectively from 2015 to 2020. Abbreviations COVID-19: Coronavirus disease 2019; AMS: Antimicrobial stewardship; TTSH: Tan Tock Seng Hospital; NCID: National Centre for Infectious Diseases; FTE: Fulltime equivalent; ID: Infectious diseases; Global-PPS: Global Point Prevalence Survey.

were admitted to ICU and 184 were managed as medical patients in the infectious disease wards. Overall number of admitted patientsValue (in DDD/1000 patient days)
95% confidence interval
p-value
Intercept at time zero
1906.89
1822.19,1991.59
< 0.01
Trend
+8.38
-0.91,17.67
0.07
Level change
-361.46
-534.80, -188.11
<0.01
Trend change
+32.95
-2.93,68,83
0.07

Table 1
1Antimicrobial use in inpatients from 2015 to 2019 P = test for trends in proportions and test for differences in median using the Kruskal-Wallis test as appropriate * Introduction of the surveillance of the complete list of antivirals for systemic use (J05) as opposed to surveillance of neuraminidase inhibitors (J05AH) alone in 2015 and 2017Year
2015
2017
2018
2019
2020
P

No. of available beds (No. of surveyed wards)
1135 (35)
1345 (40)
1359 (44)
1375 (46)
1357 (50)
-

No. of patients admitted
1018
1150
1173
1214
1182
NA

No. of patients on antimicrobials
558 (55%)
519 (45%)
592 (50%)
589 (49%)
558 (47%)
0.02

No. of patients on antibacterials for systemic use (J01)
550 (54%)
504 (44%)
562 (48%)
550 (45%)
501 (42%)
< 0.01

Age, median years (range)
73 (16-99)
69 (17-100)
71 (17-100)
72 (15-99)
71 (16-101)
-

Male
290 (53%)
281 (54%)
340 (57%)
345 (59%)
330 (59%)
-

Medical patients
704 (69%)
802 (70%)
849 (72%)
914 (75%)
912 (77%)
< 0.01

Surgical patients
278 (27%)
297 (26%)
290 (25%)
273 (22%)
226 (19%)
< 0.01

Intensive care patients
36 (4%)
51 (4%)
34 (3%)
27 (2%)
44 (4%)
0.27

No. of antimicrobials
768
755
839
821
780
-

Antibacterials for systemic use (J01)
727 (95%)
647 (86%)
692 (82%)
665 (81%)
615 (79%)
-

Antimalarials (P01BA)
0
2 (0.2%)
0
10 (1%)
4 (0.5%)
-

Antimycobacterials (J04)
21 (3%)
51 (7%)
50 (6%)
44 (5%)
52 (7%)
-

Antimycotics for systemic use (J02)
11 (1%)
19 (3%)
13 (2%)
18 (2%)
20 (3%)
-

Antivirals for systemic use (J05)
8 (1%)
26 (3%)
80 (10%)*
70 (9%)
83 (11%)
-

Intestinal anti-infectives (A07A)
1 (< 1%)
10 (1%)
4 (< 1%)
14 (2%)
6 (< 1%)
-

Table 2
2Patients on antimicrobials divided by ward types from 2015 to 2020 P = test for trends in proportionsYear
2015
2017
2018
2019
2020
P

Overall
558/1018 (55%)
519/1150 (45%)
592/1173 (50%)
589/1214 (49%)
558/1182 (47%)
0.02

Medical ward
331/596 (56%)
335/780 (43%)
404/852 (47%)
395/860 (46%)
372/789 (47%)
0.08

Surgical ward
168/341 (49%)
133/281 (47%)
139/244 (57%)
151/285 (53%)
76/130 (58%)
0.03

Intensive care ward
32/44 (73%)
30/51 (59%)
23/41 (56%)
26/32 (81%)
34/44 (75%)
0.18

Haematology and oncology ward
27/37 (73%)
21/38 (55%)
26/36 (72%)
17/37 (46%)
23/35 (66%)
0.34

Infectious disease ward
-
-
-
-
53/184 (29%)
-

Table 4
4Empiric antimicrobial use and prescribing quality indicators from 2015 to 2020a The number of antimicrobial prescriptions for which guidelines were available was used as the denominator to calculate percentages. Only includes empiric and surgical prophylaxis use. P = test for trends in proportionsYear
2015
2017
2018
2019
2020
P

No. of anti-microbials
768
755
839
821
780
-

Empiric treatment
608 (79%)
538 (71%)
660 (79%)
577 (70%)
532 (68%)
-

Reasons in notes
697 (91%)
733 (97%)
746 (89%)
772 (94%)
755 (97%)
< 0.01

Stop/review date
404 (53%)
323 (43%)
450 (54%)
458 (56%)
476 (61%)
< 0.01

Guideline compliant a
340/479 (71%)
291/375 (78%)
286/403 (71%)
235/377 (62%)
248/344 (73%)
0.08

No guideline available
96/589 (16%)
66/480 (14%)
138/560 (25%)
108/507 (21%)
110/463 (24%)
-

Surgical prophylaxis > 24 h
20/36 (56%)
20/34 (59%)
11/26 (42%)
18/26 (69%)
15/27 (52%)
0.76

AcknowledgementsWe would like to thank all doctors, pharmacists and nurses at Tan Tock Seng Hospital and National Centre for Infectious Diseases for their support of the Antimicrobial Stewardship Programme throughout the years and especially during this pandemic. We would like to thank Prof. Herman Goossens and Ann Versporten for reviewing the manuscript. The Global Point Prevalence Survey is coordinated at the University of Antwerp, Belgium and sponsored through an unrestricted grant given to them annually by bioMérieux.• fast, convenient online submissionFundingThis study was conducted as part of our routine work.Availability of data and materialsThe datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.Ethics approval and consent to participateThe study was approved by local institutional review board (DSRB reference: 2015/00015, 2017/01012, 2019/00768, 2020/01045).Consent for publicationsNot applicable.Competing interestsThe authors declare that they have no competing interests.Author details
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The ambition of the European Respiratory Journal continues: chapter 5

Marc Humbert firstname.lastname@example.com
Univ. Paris-Sud
Université Paris-Saclay
Le Kremlin-BicêtreFrance

Service de Pneumologie
Hôpital Bicêtre
Assistance Publique Hôpitaux de Paris
Le Kremlin-BicêtreFrance

INSERM UMR_S 999
Hôpital Marie Lannelongue
Le Plessis RobinsonFrance

Anh Tuan Dinh-Xuan
Service de Physiologie
Marc Humbert, Service de Pneumologie, Hôpitaux Universitaires Paris-Sud, Assistance Publique Hôpitaux de Paris
Paris Descartes University EA
78 rue du Général Leclerc94270Le Kremlin-BicêtreFrance

Elin L Reeves
Matthew G Broadhead
Neil J Bullen
The ambition of the European Respiratory Journal continues: chapter 5
10.1183/13993003.02393-2016Received: Dec 06 2016 | Accepted: Dec 06 20162511, Hôpital Cochin, Assistance Publique Hôpitaux de Paris, Paris, France. 5 European Respiratory Society Publications Office, Sheffield, UK. Correspondence: @ERSpublications A look back at the highlights from the ERJ in 2016, and forward to new developments that will arrive in 2017 Cite this article as: Humbert M, Dinh-Xuan AT, Reeves EL, et al. The ambition of the European Respiratory Journal continues: chapter 5. Eur Respir J 2017; 49: 1602393 [https:// Conflict of interest: E.L. Reeves, M.G. Broadhead and N.J. Bullen are employees of the European Respiratory Society. Further disclosures can be found alongside this article at
Happy New Year! As 2017 begins, so too does the final year of the current editorial board's mandate. Welcome to our annual look back at some of the highlights of our past 12 months of publishing, and forward to some of the new developments 2017 will see for the European Respiratory Journal.As many of you will already know, 2017 marks a transition to continuous publication for the European Respiratory Journal and its sister publication, the European Respiratory Review. The most important motivation behind this decision was improving the service we provide to our authors and readers. In the continuous publication model, the final version of an article is published directly into an "open" issue of the journal; the issue "grows" over time as content is added, until it is considered "closed". In effect, continuous publication will allow us to publish a "version of record" of every article as quickly as possible after it has been through our production processes. This version of record is the final publication of an article, and includes permanent citation details that are immediately indexed and available through platforms such as Web of Knowledge and Medline/PubMed. Previously, articles would be published "in press" initially, and would only have attained a final, permanent citation when they were eventually republished in one of our monthly issues. You may notice that we've made some small changes to our article PDFs, giving more prominence to a "cite this article as" section, to make it clear that page numbers won't be used in article citations any more. Under continuous publication, authors and readers can be assured that whenever we publish an article, its citation details will not change.Those receiving our printed journal will notice that instead of being distributed at the beginning of the month stated on the front cover, the print edition will be compiled later in the month, at the point when the online issue is "closed" and new content will not be added. (At that time, the following month's online issue is effectively "opened", and available for publication of new content immediately.) Having said this, it should also be recognised that many articles will appear in the printed issue more quickly than they would have under the previous publication model, owing to the reduced time to "final" publication of an article in a journal issue.

As many of you will already know, 2017 marks a transition to continuous publication for the European Respiratory Journal and its sister publication, the European Respiratory Review. The most important motivation behind this decision was improving the service we provide to our authors and readers. In the continuous publication model, the final version of an article is published directly into an "open" issue of the journal; the issue "grows" over time as content is added, until it is considered "closed". In effect, continuous publication will allow us to publish a "version of record" of every article as quickly as possible after it has been through our production processes. This version of record is the final publication of an article, and includes permanent citation details that are immediately indexed and available through platforms such as Web of Knowledge and Medline/PubMed. Previously, articles would be published "in press" initially, and would only have attained a final, permanent citation when they were eventually republished in one of our monthly issues. You may notice that we've made some small changes to our article PDFs, giving more prominence to a "cite this article as" section, to make it clear that page numbers won't be used in article citations any more. Under continuous publication, authors and readers can be assured that whenever we publish an article, its citation details will not change.

Those receiving our printed journal will notice that instead of being distributed at the beginning of the month stated on the front cover, the print edition will be compiled later in the month, at the point when the online issue is "closed" and new content will not be added. (At that time, the following month's online issue is effectively "opened", and available for publication of new content immediately.) Having said this, it should also be recognised that many articles will appear in the printed issue more quickly than they would have under the previous publication model, owing to the reduced time to "final" publication of an article in a journal issue.

Another recent development for the journal has been the introduction of support for authors who wish to share their datasets via the online repository Dryad (datadryad.org). This was our response to the increasing trend toward transparency and data sharing; many authors are now being mandated by their funding bodies to make the raw data that forms the basis for their published results and analyses publicly available for examination by readers and other researchers. Although some of the major general medical journals have started to mandate data sharing for the clinical trials they publish, as a more specialised journal, we have not decided to adopt this approach; however, if any of our authors should wish to, or have been instructed to, publicly archive their datasets, our collaboration with Dryad should facilitate this. A more detailed explainer is available via our manuscript submissions page (erj.ersjournals.com/authors/ms-preparation).

In another response to author and funding body requests, we have also recently introduced new options for those authors and funders who wish to publish their work open access in the European Respiratory Journal. Until recently, open access in the journal meant publishing with a CC BY-NC (creativecommons.org/licenses/by-nc/4. 0) licence only, which restricts re-use to non-commercial purposes. However, over the past couple of years, we have increasingly seen that authors are being mandated by their funding bodies to publish their work open access without this distinction between non-commercial and commercial re-use. As a result, eligible authors can request open access publication with the less restrictive CC BY licence (creativecommons.org/licenses/by/4.0). More details can be found through our "instructions for authors" page (erj.ersjournals.com/authors/instructions). Finally, another change we have made over the past few months is that we have integrated a tool for electronic transfer of copyright via the ScholarOne Manuscripts submission platform (mc.manuscriptcentral.com/erj). This new functionality should help authors to reduce the time spent completing paperwork for this task, while still fulfilling the requirements of the journal for this important element of article publication.

Leaving aside these new developments in how we publish, of course the single, most important aspect for the continuing success of the European Respiratory Journal is what we publish. This past year, we have once again been privileged to receive some of the best research emerging from the field of respiratory medicine. Indeed, 2016 was a recording-breaking year for submissions to the journal, with well in excess of 2500 manuscripts received. As a single journal could not possibly publish such a number of articles, the chief editor, deputy chief editor and all of the associate editors work exceptionally hard all year in order to select the best of these submissions for publication -with tremendous support from our many hundreds of peer reviewers (erj.ersjournals.com/journal/editorial-board). We also work closely with the editors of our companion journals, the European Respiratory Review and ERJ Open Research, to make sure the European Respiratory Society (ERS) journals can offer authors a place for their best articles.

In 2016, we published around 220 original research articles, supplemented by two or three comprehensive review articles in each monthly issue. Of course, we cannot mention here each and every one of the papers that passed our rigorous reviewing process, even if we do feel that all have made a great contribution to the journal. However, some particular highlights from the past year include an analysis of three multinational phase 3 trials of pirfenidone, demonstrating a positive effect on disease progression in patients with idiopathic pulmonary fibrosis [1]; a study elaborating on how identification of four clinical phenotypes in bronchiectasis could enable future dedicated treatment options to be established [2]; a contribution from the ISOLDE study group with new results indicating that blood eosinophil levels may have use as a marker of a COPD patient's response to inhaled corticosteroids [3]; and the results of a phase 2 trial examining the safety and efficacy of bedaquiline when added to existing treatment regimens for multidrug-resistant tuberculosis [4].

In addition to original research articles such as the few mentioned above, the contributions of task force groups continue to comprise an important portion of our selection of published articles, as the official statements and guidelines generated by these expert groups provide essential reading and a "go-to" reference for practising clinicians and researchers. A joint task force established by the ERS and the European Society for Clinical Microbiology and Infectious Diseases published guidelines for the diagnosis and management of chronic pulmonary aspergillosis [5]; another joint venture of the ERS, this time with the European Cystic Fibrosis Society, produced a task force report on the care of adults with cystic fibrosis [6]. Through the year, official ERS statements have been published on the following: the standardisation of lung sound nomenclature [7], diagnosis and management of obstructive sleep disordered breathing in children [8], tele-monitoring for ventilator-dependent patients [9], and exercise testing for the evaluation of intervention efficacy [10]. Later in the year, another important document was published by EMBARC (the European Multicentre Bronchiectasis Audit and Research Collaboration), a clinical research collaboration supported by both the Inhaled Antibiotics in Bronchiectasis and Cystic Fibrosis consortium, a project of the European Union Innovative Medicines Initiative, and ERS. The article identified new priorities for research in bronchiectasis, aiming to set out a roadmap for improving the understanding of bronchiectasis and the quality of care for patients [11].

The quality of the articles published in the journal over the past years was once again underscored by another healthy increase in Impact Factor. Impact Factors for 2015 are calculated from the number of citations made in 2015 to articles published in 2013 and 2014, and were released in June of this year. We were delighted to find that the Impact Factor of the European Respiratory Journal continues to rise, from 7.636 in 2014 to 8.332 this year (figure 1). This was also borne out in the levels of readership achieved by the journal. At the time of writing, the number of visits to the website (erj.ersjournals.com) in 2016 is already more than a quarter higher than in 2015, and the number of article downloads has increased by 55%.

We briefly mentioned our peer reviewers earlier on, but as this conscientious army of experts provides such a crucial foundation to our journals (and, indeed, to all others) they deserve a further comment here. In 2016, we repeated our initiative that commenced the previous year, and asked our board of associate editors to nominate a select few peer reviewers for special recognition of their outstanding contribution to the journal. Congratulations to Christophe Guignabert (Inserm and Université Paris-Sud, France), Luis Puente-Maestu (Hospital Universitario Gregorio Marañón, Madrid, Spain), Nicolas Roche (Université Paris Descartes, France) and Sanja Stanojevic (Hospital for Sick Children, Toronto, Canada), who were awarded for their achievements at the International Congress in London. As always, we will publish the full list of 2016 peer reviewers online early in 2017many thanks to all of them. In addition to the peer reviewer awards, we have also over the past year introduced a new associate editor mentoring scheme. The brainchild of associate editor Ramon Farré, this initiative aims to foster the next generation of journal editors; as an internationally recognised journal, we strongly believe in developing these relationships and skills for the future of our community. Briefly, a number of European Respiratory Journal associate editors have each agreed to act as mentors, so that "junior" associate editors can gain experience in coordinating the external peer review process and be party to the decision-making required when selecting manuscripts for publication. We will aim to produce a more detailed report on this venture later in the year.
 https://doi.org/10.1183/13993003.02393-2016
We hope that you appreciate and enjoy the changes we have brought to the European Respiratory Journal for 2017, whether you are a reader, an author, or both. Thank you to all of you for each playing your part in the achievements we have been able to report to you in this editorial, which will be the last "new year" bulletin from the present editorial team. All the best to you for 2017!
Pirfenidone for idiopathic pulmonary fibrosis: analysis of pooled data from three multinational phase 3 trials. P W Noble, C Albera, W Z Bradford, Eur Respir J. 47Noble PW, Albera C, Bradford WZ, et al. Pirfenidone for idiopathic pulmonary fibrosis: analysis of pooled data from three multinational phase 3 trials. Eur Respir J 2016; 47: 243-253.

Clinical phenotypes in adult patients with bronchiectasis. S Aliberti, S Lonni, S Dore, Eur Respir J. 47Aliberti S, Lonni S, Dore S, et al. Clinical phenotypes in adult patients with bronchiectasis. Eur Respir J 2016; 47: 1113-1122.

Blood eosinophils as a marker of response to inhaled corticosteroids in COPD. N C Barnes, R Sharma, S Lettis, Eur Respir J. 47Barnes NC, Sharma R, Lettis S, et al. Blood eosinophils as a marker of response to inhaled corticosteroids in COPD. Eur Respir J 2016; 47: 1374-1382.

Bedaquiline in the treatment of multidrug-and extensively drug-resistant tuberculosis. A S Pym, A H Diacon, S-J Tang, Eur Respir J. 47Pym AS, Diacon AH, Tang S-J, et al. Bedaquiline in the treatment of multidrug-and extensively drug-resistant tuberculosis. Eur Respir J 2016; 47: 564-574.

Chronic pulmonary aspergillosis: rationale and clinical guidelines for diagnosis and management. D W Denning, J Cadranel, C Beigelman-Aubry, Eur Respir J. 47Denning DW, Cadranel J, Beigelman-Aubry C, et al. Chronic pulmonary aspergillosis: rationale and clinical guidelines for diagnosis and management. Eur Respir J 2016; 47: 45-68.

Report of the European Respiratory Society/European Cystic Fibrosis Society task force on the care of adults with cystic fibrosis. J S Elborn, S C Bell, S L Madge, Eur Respir J. 47Elborn JS, Bell SC, Madge SL, et al. Report of the European Respiratory Society/European Cystic Fibrosis Society task force on the care of adults with cystic fibrosis. Eur Respir J 2016; 47: 420-428.

Towards the standardisation of lung sound nomenclature. H Pasterkamp, Plp Brand, M Everard, Eur Respir J. 47Pasterkamp H, Brand PLP, Everard M, et al. Towards the standardisation of lung sound nomenclature. Eur Respir J 2016; 47: 724-732.

Obstructive sleep disordered breathing in 2-to 18-year-old children: diagnosis and management. A G Kaditis, Alonso Alvarez, M L Boudewyns, A , Eur Respir J. 47Kaditis AG, Alonso Alvarez ML, Boudewyns A, et al. Obstructive sleep disordered breathing in 2-to 18-year-old children: diagnosis and management. Eur Respir J 2016; 47: 69-94.

Tele-monitoring of ventilator-dependent patients: a European Respiratory Society Statement. N Ambrosino, M Vitacca, M Dreher, Eur Respir J. 48Ambrosino N, Vitacca M, Dreher M, et al. Tele-monitoring of ventilator-dependent patients: a European Respiratory Society Statement. Eur Respir J 2016; 48: 648-663.

Use of exercise testing in the evaluation of interventional efficacy: an official ERS statement. L Puente-Maestu, P Palange, R Casaburi, Eur Respir J. 47Puente-Maestu L, Palange P, Casaburi R, et al. Use of exercise testing in the evaluation of interventional efficacy: an official ERS statement. Eur Respir J 2016; 47: 429-460.

Research priorities in bronchiectasis: a consensus statement from the EMBARC Clinical Research Collaboration. S Aliberti, S Masefield, E Polverino, Eur Respir J. 48Aliberti S, Masefield S, Polverino E, et al. Research priorities in bronchiectasis: a consensus statement from the EMBARC Clinical Research Collaboration. Eur Respir J 2016; 48: 632-647.