Impact of climate change in emergency medicine: a narrative review
Review Article

Impact of climate change in emergency medicine: a narrative review

Claudio Dalla Vecchia1 ORCID logo, Abdi Sadik2, Lelegite Jonah3

1Emergency Department, Connolly Hospital Blanchardstown, Dublin, Ireland; 2Emergency Department, Beaumont Hospital, Dublin, Ireland; 3Emergency Department, Mater Misericordiae University Hospital, Dublin, Ireland

Contributions: (I) Conception and design: C Dalla Vecchia, A Sadik; (II) Administrative support: None; (III) Provision of study materials or patients: C Dalla Vecchia, A Sadik; (IV) Collection and assembly of data: C Dalla Vecchia, A Sadik; (V) Data analysis and interpretation: C Dalla Vecchia, A Sadik; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

Correspondence to: Claudio Dalla Vecchia, MD. Emergency Department, Connolly Hospital Blanchardstown, Mill Road, Dublin 15, Ireland. Email: claudiovecchia@rcsi.com.

Background and Objective: Climate change is an unprecedented global phenomenon with far-reaching implications for every sector, including healthcare. Emergency medicine is uniquely susceptible to the impacts of climate change, and emergency physicians will be increasingly challenged by the increase in attendances and the variation of disease patterns directly due to climate change. This narrative review aims to summarize how climate change is affecting emergency medicine practise through amplification of climate-related disease patterns and epidemiological shifts for conditions treated in the emergency department (ED) and what potential solutions have been explored to address this issue such as clinical practise improvements, disaster preparedness, public health engagement, mitigation and adaptive solutions.

Methods: This narrative review was conducted by the two lead authors through an independent literature review on Scopus, Embase, and PubMed in March 2023. All studies relevant to emergency medicine were included with limitations to English language.

Key Content and Findings: The key themes found were: the association between increase in average temperatures and ED attendances; the impact of increase in pollution and ED attendances for various conditions; the impact of climate-related disasters and adverse weather events to the ED; commentaries and reviews of how ED can be affected by climate change and how potential mitigation strategies can be applied. Increased in daily average temperatures, pollution and frequency of extreme weather events has led to a rise in climate-related health emergencies, for various conditions. Multiple commentaries and reviews called for action on emergency physicians and leaders to become more involved in climate change and look at potential solutions.

Conclusions: Climate change will inevitably play a vital part in provision of emergency care to patients in the coming future. Knowledge of its impact and the potential solutions to this problem can be of help for future clinicians.

Keywords: Emergency department (ED); climate change; emergency medicine; climate crisis


Received: 16 November 2023; Accepted: 14 June 2024; Published online: 16 July 2024.

doi: 10.21037/jphe-23-87


Introduction

Climate change represents a worldwide health emergency, primarily attributed to human activities such as the combustion of fossil fuels and deforestation. The World Health Organisation (WHO) estimates that between 2030 and 2050, the effects of climate change are projected to cause approximately 250,000 additional deaths each year from heat stress, malnutrition, malaria and diarrhoea (1).

The healthcare industry’s average 4% of worldwide net greenhouse gas emissions is a substantial contributor to the global climate crisis; this is equivalent to the annual emissions of 514 coal-fired power plants (2).

Emergency physicians are facing an increasing number of patients with conditions directly attributable to global warming (3,4). Factors such as wildfires, flooding, and heat-related illnesses contribute to the rise in medical emergencies (5). Climate change is anticipated to increase the prevalence of conditions already encountered in emergency departments (EDs), such as cardiovascular diseases (CVDs), respiratory conditions, and gastrointestinal disorders (3).

The implications of climate change for emergency care have been emphasised by medical organisations globally. In 2018, the policy statement issued by the American College of Emergency Physicians (ACEP) underscored the significance of fostering collaboration between emergency medicine and public health in the realm of climate change research (6). The Royal College of Emergency Medicine (RCEM) in the United Kingdom officially declared a climate emergency in 2019, leading to the establishment of Green ED as a means to incorporate environmental sustainability into routine medical procedures (7). The Australasian College of Emergency Medicine (ACEM) has advised governments to pledge to attain a carbon-neutral economy by 2050 and dedicate resources towards renewable energy sources (8).

The WHO has highlighted five global research priorities for protecting human health from the effects of climate change. This includes risk assessment, finding cost-effective solutions, assisting with decisions about adaptation and mitigation that promote health, and improving decision support and cost estimation (9).

Previous studies have looked at the impact of healthcare on greenhouse effect. A systematic review showed how healthcare services impact greenhouse effect by 15% to 50% through direct and indirect carbon emissions and suggested that disposable equipment and pharmaceuticals represented the highest percentage (10). Similar review has also found that, even though the rate of energy consumption and environmental impact per hospital bed is relatively low compared to other industries, it still compounds to a significant figure (11). Both sources agree that the use of energy saving initiatives like the use of renewable energy, thermal insulation for buildings and low-consumption equipment for electricity and rainwater harvesting and wastewater recycling could help significantly reduce the overall carbon footprint of healthcare (11).

A few studies specifically looked at the impact of climate change to emergency medicine (3,12). Hess et al. described how climate change could impact the delivery of emergency service in the USA within the next years (3). They argue that climate change will be highly likely to increase the incidence of conditions regularly seen in ED because of the impact of temperature rises, pollutions, pollens and extreme weather events. Also, it is likely that patients living in marginalised area and more socially vulnerable would be more likely to attend as a consequence of heat-related illnesses. They also predict that climate change will likely introduce unfamiliar zoonotic and vector-borne diseases into new geographic areas, as seen in some areas of the USA. Finally, they describe how climate change is due to impact disaster response and management from both a prehospital and intradepartmental point of view and reflect on priorities needed to be addressed to prepare emergency physicians in their role as future leaders.

The only scoping review that could be found on the impact of climate change on emergency care was from Theron et al. (12) although they limited their scope to the African continent. They identified three key themes in their review: surges in demands related to climate change, opportunities for health sector engagement and proposed solutions to improve preparedness. In particular, floodings were noted to be the major single hazard for infectious disease spread, but also injuries from mudslides and other extreme weather events and heat-related illnesses due to the rising average temperatures accounted for high emergency care requirement. Challenges specific to the African continent were also mentioned to be the need for a strengthened healthcare infostructure capable of dealing with these weather events and potential solutions identified were action plans aimed at improving capacity during adverse weather events and disaster tools to promote health care facility flood preparedness. In their article they also conclude with various recommendations for leaders to address climate-related health threats in the near future.

The purpose of this narrative review is to provide a concise overview of the impact of climate change on emergency medicine at an international level. Additionally, it highlights responses undertaken by certain countries to address the impact of climate change on ED presentations. This article is written in accordance with the Narrative Review reporting checklist (available at https://jphe.amegroups.com/article/view/10.21037/jphe-23-87/rc).


Methods

C.D.V. and A.S. performed an independent literature review through Embase, Scopus and PubMed in March 2023. The detailed research strategy is outlined in Appendix 1. A 5-year time limit was applied to focus on recent literature updates (Table 1).

Table 1

Research methods

Items Specification
Date of search Literature search: 11 March 2023
Manual search up until April 2024
Database PubMed, Embase, Scopus
Search items used (“climate change” OR “global warming” OR “heatwave” OR “heat wave” OR “greenhouse effect” OR “wildfire” OR “natural disaster”) AND (“Emergency department” OR “emergency medicine” OR “emergency department*” OR “emergency room” OR “emergency physician” OR “emergency physicians”) AND (y_5[Filter])
Timeframe From January 2018 to March 2023
Exclusion criteria Commentaries, letters, repeated published articles and case reports
Selection process Independent selection process by two authors C.D.V. and A.S. Discrepancies in study selection were resolved through mutual discussion

This search strategy yielded a total of 1,957 studies. Upon removing duplicates, the authors screened titles for relevance to emergency medicine. Irrelevant studies were excluded based on the authors’ judgment. Priority was given to international studies offering diverse perspectives from various countries. Discrepancies in study selection were resolved through mutual discussion.

All studies relevant to emergency medicine were included, with limitation to the English language. Additionally, we also consulted the website of major international emergency medicine colleges to identify policies, reports, and position statements relevant to climate change.

A further ad hoc literature review was performed by the authors to complement some sections of the article in April 2023.


Results

A total of 70 studies were obtained from the literature review (Table 2). These have been categorized by year, country of origin, and relevant results. The majority of the studies were observational, comprising three systematic reviews (13-15); two scoping reviews (12,16) and nine consisting of commentary and review articles (17-25).

Table 2

List of studies included

Topic Authors Year Country/region Methodology Results
Cardiovascular Bo Wen et al. 2022 Australia Observational study 10% increase in ED attendances for cardiovascular conditions during bushfires (95% CI: 5–15%)
Paolo Contiero et al. 2019 Italy Observational study Increase in presentation to ED during hot days for cardiovascular-related conditions (OR =1.34, 95% CI: 1.05–1.75) and increase in PM (OR =1.23, 95% CI: 1.09–1.37)
Kendra R. Cicci et al. 2022 Scoping review Increase in ED attendance due to cardiovascular disease, HTN, IHD, ischemic stroke with high temperatures
Wenzhi Zhu et al. 2021 China’s mainland Observational study 1% increase in diurnal temperature associated with increase ED attendance for CVD of 1.3% (95% CI: 0.99–1.62%)
Yuxia Ma et al. 2019 China’s mainland Observational study Increase in CVD attendances to ED associated with extreme temperature changes (both low and high temperatures) (RR =3, 95% CI: 1.6–4.4)
Joan A. Casey et al. 2021 USA Observational study High wildfire PM2.5 non-significantly associated with an increase in CVD-related ED visits or mortality
Respiratory Bo Wen et al. 2022 Australia Observational study 6% increase in ED attendances for cardiovascular conditions during bushfires (95% CI: 1.9–10%)
Yuxia Ma et al. 2019 China’s mainland Observational study Increase in ED attendances for respiratory condition with increase in temperature (OR =1.36, 95% CI: 0.96–1.92)
Larry W. Figgs et al. 2019 USA Observational study Non-significant increase of asthma ED diagnosis 1.23 (95% CI: 0.96–1.57) times higher during heat wave compared to previous year
Colleen E. Reid et al. 2016 USA Observational study Increase ED visits for asthma (RR =1.05, 95% CI: 1.02–1.07). Non-significant for hospitalizations
Nicholas J. Nassikas et al. 2021 USA Observational study Average excess asthma-related ED visits of 3.2 (95% CI: 1.52–4.75) per 10,000 population due to ozone attributable asthma attacks
Daniel Kiser et al. 2020 USA Observational study Daily increase in PM2.5 associated with increase in asthma visits to ED to 6.1% (95% CI: 2.1–10.3%). Presence of wildfire smoke increased ED asthma visit by 5.5% (95% CI: 2.5–8.6%)
Firdian Makrufardi et al. 2023 Systematic review Increase ED asthma visits 1.25 folds (95% CI: 1.14–1.27), hospital admissions 1.10 (95% CI: 1.04–1.17) and mortality 2.10 (95% CI: 1.35–3.27) with extreme weather
Ryan W Gan et al. 2020 USA Observational study Increase in PM2.5 associated with increase in asthma ED diagnosis (OR =1.08, 95% CI: 1.04–1.13)
Nicholas Nassikas et al. 2020 USA Observational study Comparison of climate warming mitigation scenario vs. “business as usual scenario” to project asthma admissions and healthcare spending. Projected annual average of 3,100 averted asthma ozone-related ED visits translating to 1.7 million USD averted costing
Francis Thien 2018 Australia Commentary Epidemic thunderstorm asthma leading to 3,365 excess asthma-related presentation to ED in Melbourne in one day with 10-fold increase in ICU admissions
Yuxia Ma et al. 2019 China’s mainland Observational study Association between ED visits for respiratory conditions and extreme temperatures. RR =1.36 (95% CI: 0.96–1.92) with high temperatures; RR =1.96 (95% CI: 1.7–2.26) with extreme cold
Xuping Song et al. 2021 China’s mainland Observational study Association between ED visits for respiratory conditions and air pollution index associated with moderate cold days (RR =1.006, 95% CI: 1.002–1.009)
Joan A. Casey et al. 2021 USA Observational study High wildfire PM2.5 associated with a 14.6% (95% CI: 4.2–24.9%) increase in same-week respiratory disease-related ED visits
Bowen Cheng et al. 2021 China’s mainland Observational study Increase in ED visits for respiratory conditions associated with increase in PM2.5 and PM10. RR for PM2.5 1.042 (95% CI: 1.036–1.047) and for PM10 1.01 (95% CI: 1.01–1.02)
Mental health Xinye Qiu et al. 2022 USA Observational Relative increase in admission for a psychiatric disorder with 5-degree increase in atmospheric temperature. Depression: RR 3.66 (95% CI: 3.06–4.25); schizophrenia: 3.03 (95% CI: 2.04–4.02); bipolar disorder: 3.52 (95% CI: 2.38–4.68)
Eric Lavigne et al. 2023 Canada Observational study Cumulative exposure to extreme heat associated with increase attendance to ED for mental and behavioural disorders (personality disorder, schizophrenia, dementia and substance misuse) (OR =0.98, 95% CI: 0.97–0.98)
Jamie T. Mullins et al. 2019 USA Observational study For every additional day with temperature >80 ℉, there is a 0.3% increase in ED attendances for mental health and a 0.24% increase in suicide rate
Eun-Hye Yoo et al. 2021 USA Observational study Positive association between short extreme weather bursts and ED attendances for mental health conditions (RR =1.28, 95% CI: 1.23–1.33)
Julia Feriato Corvetto et al. 2023 Systematic review Suicide (completed or attempted), substance misuse, schizophrenia, mood, organic and neurotic disorders, and mortality were strongly affected by climate change
Eun-Hye Yoo et al. 2021 USA Observational study Positive associations between short-term exposure to extreme ambient temperatures and increased ED visits for mental disorders (RR =1.16, 95% CI: 1.06–1.27)
Li Niu et al. 2023 USA Elevated temperature days were associated with higher risk of mental health-related ED for the 6- to 11-year-olds (OR =1.28, 95% CI: 1.13–1.46), for the 12- to 17-year-olds (OR =1.17, 95% CI: 1.09–1.25) and for the 18- to 25-year-olds (OR =1.09, 95% CI: 1.04–1.15)
Gastrointestinal Arbor J. L. Quist et al. 2022 USA Observational study Increase in acute gastrointestinal disease after hurricanes (RR =1.1, 95% CI: 1.0–1.23)
Jacob E. Simmering et al. 2022 USA Observational study Increase in incidence of appendicitis with higher-than-expected temperatures vs. normal temperatures (3.3% increase incidence, 95% CI: 1–5.7%)
Neurology Seonjeong Byun et al. 2020 South Korea Observational study Short-term exposure to wide diurnal temperature ranges immediately increased the risk of ED visits for MS (OR =8.81%, 95% CI: 3.46–14.4%)
Hyewon Lee et al. 2018 South Korea Observational study Higher air pollution levels associated with increased ED attendances for migraine (OR =1.031, 95% CI: 1.01–1.05)
Holly Elser et al. 2021 USA Observational study Anomalously warm weather was associated with increased risk for ED visits (RR =1.043, 95% CI: 1.025–1.063)
Endocrine Donghong Gao et al. 2022 Systematic review Increase in diabetes-related ED visits with exposures to extreme daily ambient maximum temperature (RR =1.03, 95% CI: 1.01–1.06)
Dermatology Dharshani Pearson et al. 2020 USA Observational study Risk of ED visits for HFMD per 1 °F increase in mean temperature during the same week increased 2.00% (95% CI: 1.15–2.86%) and 2.35% (95% CI: 1.38–3.33%) during the warm and cold seasons
Nai-Tzu Chen et al. 2021 Taiwan Observational study Increase in attendance to ED from patients with atopic dermatitis during floods (OR =1.14, 95% CI: 1.01–1.128)
Nephrology Zhiwei Xu et al. 2020 Australia Observational study Increase in AKI presentation in ED with hourly increase in temperature degree (OR =1.37, 95% CI: 1.10–1.71)
Satbyul Estella Kim et al. 2019 South Korea Observational study Increase in AKI presentation to ED with 1-degree increase of temperature (OR =1.01, 95% CI: 1.00–1.02)
Yanji Qu et al. 2023 USA Observational study Increase in kidney disease-related conditions (kidney stones, AKI, and urinary tract infections) with extreme heat exposure. 1.7% to 3.5% increased risk of attendance to ED with renal-related conditions
Disaster Kate R. Weinberger et al. 2021 USA Hurricane Sandy associated with a higher rate of ED visits due to injuries and poisoning (RR =1.19, 95% CI: 1.10–1.28), respiratory disease (RR =1.35, 95% CI: 1.21–1.49), cardiovascular disease (RR =1.10, 95% CI: 1.02–1.19), renal disease (RR =1.44, 95% CI: 1.22–1.72), and skin and soft tissue infections (RR =1.20, 95% CI: 1.03–1.39)
Chitta Ranjan Mohanty et al. 2020 India Observational study Retrospective study of patients attending ED during a cyclone. Injury primary cause for attendance
Verónica M. Frasqueri-Quintana et al. 2020 Puerto Rico Observational study Retrospective study of patients attending ED during a hurricane. Injury primary cause of presentation
Kevin C. Heslin et al. 2021 USA Observational study ED utilization rates for weeks during and after hurricanes were compared with pre-hurricane rates. Respiratory disorders exhibited the largest post hurricane increase, particularly 2–3 weeks following the hurricane
Rachel S.C. Friedman et al. 2022 USA Observational study Role of telemedicine to reduce attendance to ED in private healthcare during wildfires. Telemedicine familiarity associated with decreased absolute risk in pre- to post-fire inpatient and emergency department utilization
General Elzarie Theron et al. 2022 South Africa Scoping review Key themes that were identified: climate-related health impacts that contribute to surges in demand and resource utilization, opportunities for health sector engagement, and solutions to improve emergency preparedness
Cecilia J. Sorensen et al. 2020 USA Commentary Key opportunities for emergency medicine to lead the medical response to climate change through 7 key areas: clinical practice improvements, building resilient EDs and health care systems, adaptation and public health engagement, disaster preparedness, mitigation, research, and education
Mitigation strategies Hanna Linstadt et al. 2020 USA Commentary To educate and motivate emergency providers to action by providing a guide to sustainable health care and an approach to creating a climate-smart ED
Nadeem Ullah Khan et al. 2023 Pakistan Quasi-experimental study The diagnosis rate of heat-related conditions improved from 3% (n=125/4,181) to 7.5% (n=302/4,022) (P value <0.001)
Patrice K. Nicholas et al. 2021 USA Commentary Application of a clinical tool mnemonic to identify climate-related emergencies in ED
Katelyn Moretti et al. 2021 USA Commentary Argument to include climate change-related conditions in emergency medicine curriculum
Amy Dryden et al. 2019 Australia Commentary Argument that emergency departments cannot make a meaningful impact on climate change
Joseph Ting et al. 2019 Australia Commentary Counterargument that ED can make a meaningful impact on climate change
Daniel Aiham Ghazali et al. 2018 France Review article Climate change increase demand to ED generally and causes increase in disasters. Mitigation strategies entail capability development, enhance surge capacity, increase in resources and reduction of carbon footprint
Caitlin Rublee et al. 2021 South Africa Commentary Commentary on workshop aimed at improving emergency care in Africa with regard to climate change
Heatwaves Dimpalben Patel et al. 2019 Australia Observational study Increase in ED attendances due to air pollution during heatwaves compared (77.8/100,000/day) to non-heatwaves days (73.9/100,000/day) in Perth
Yu Wang et al. 2020 China’s mainland Observational study Increase in ED attendances for each degree of average temperature increase across 18 sites in China. Subgroup analysis showing increase in attendances for injury, digestive, respiratory and endocrine conditions
Berhanu Yazew Wondmagegn et al. 2022 Australia Observational study Increase in heat attributable ED attendances with estimated cost of 4.7 million Australian dollars. Expected to grow by 3.5% ED presentations and 5% costs by 2050
Shahan Waheed et al. 2019 Pakistan Short report Description of patient presentation during a heatwave in a tertiary hospital. Higher mortality in elderly patients
Hannah Mason et al. 2022 Australia Systematic review Increase in hospital admission for CVD, respiratory, renal, mental conditions during heatwaves. Increase in mortality during heatwaves. Most vulnerable children and elderly
Aaron S. Bernstein et al. 2022 USA Observational study Increase in ED attendance of children in 47 US children hospital (RR =1.83, 95% CI: 1.12–1.12). Subgroup analysis increase in heat-related illnesses (RR =1.83, 95% CI: 1.31–2.57), gastroenteritis (RR =1.35, 95% CI: 1.02–1.79) and otitis (RR =1.30, 95% CI: 1.11–1.52)
Robert E. Davis et al. 2018 USA Observational study Increase hospital admission during heatwaves compared to non-heatwaves periods
Sharon L. Campbell et al. 2019 Australia Observational study Increase of ED presentation of 5% (OR =1.05, 95% CI: 1.01–1.09) and 19% for children <5 years old (OR =1.19, 95% CI: 1.04–1.36)
Ines Corcuera Hotz et al. 2020 UK Observational study Increase in ED attendances of 1% (95% CI: 0.8–1.4%) and 1.4% (95% CI: 1.2–1.5%) for children <15 years old. Increase in fracture-related attendances 1.1% (95% CI: 0.7–1.5%) per 1-degree increase
Jessie Adams et al. 2022 Australia Observational study Decrease in ED presentation during heat days in rural south-west Victoria compared to non-heat days
Penelope Dring et al. 2022 USA Observational study Increase in ED heat-related conditions throughout the years
Fraser Kegel et al. 2021 Canada Observational study Increase in ED attendances and patients’ length of stay during days with higher average daily temperature
Nese Colak Oray et al. 2018 Turkey Observational study Higher ED attendance rate of patients during period of heatwave compared to previous years. Higher in hospital mortality rate. Same ED admission rate. No able to describe direct correlation
Paul J. Schramm et al. 2021 USA Report Description of patient presentations during heatwave. Increase in heat-related attendances. Elderly most affected
Kate R. Weinberger et al. 2021 USA Observational Estimation of attendances to ED with two projected greenhouse emission scenarios. Results are increase in ED attendances but reduce overall mortality annually
Piotr Wilk et al. 2020 USA Observational study Increase in ED attendance of 22% with extreme heat compared to normal temperature days. Subgroup analysis showed increase attendances for infectious diseases (35%) and most pronounced in children
Richard Skinner et al. 2022 Systematic review Mostly studies from Australia and USA. PM considered the primary cause for increase in ED attendances. Increase in attendance of respiratory and CVD during wildfires. Increase risk for children, elderly and patient with comorbidities

ED, emergency department; CI, confidence interval; OR, odds ratio; HTN, hypertension; IHD, ischemic heart disease; CVD, cardiovascular disease; RR, relative risk; PM, particulate matter; USD, US dollar; ICU, intensive care unit; MS, multiple sclerosis; HFMD, hand foot mouth disease; AKI, acute kidney injury.

Most studies come from high-income countries such as the USA (24), Australia (6) and China (6). Studies from the Asia continent excluding China’s mainland were from South Korea (3), India (1), Pakistan (1) and Taiwan region (1). Two studies from the American continent excluding the USA were from Canada and Puerto Rico and the only two European studies were from Italy and France. One study was from South Africa and was a scoping review of the impact of climate change on emergency care in the African continent. The key themes found were: the association between increase in average temperatures and ED attendances; the impact of increase in pollution and ED attendances for various conditions; the impact of climate-related disasters to the ED; commentaries and reviews of how ED can be affected by climate change and how potential mitigation strategies can be applied (19-26).

Most studies examined rates of ED attendance for specific medical conditions in association with increases in average temperatures and specifically cardiovascular diseases (16,27,28), respiratory diseases (13,29), renal diseases (30-32), mental health conditions (33-36), neurological disorders (37,38), diabetes (15), and dermatological conditions (39). Most studies found an association between ED attendances and increasing average daily temperatures. During heatwaves in particular, children and in the elderly were shown to be proportionally more affected (40). Only one study showed a decrease in ED attendances associated with elevated temperatures in regional Victoria, Australia (41).

Additionally, some studies compared ED attendances to concerning increases in particulate matter (PM) levels (27,42-44). Most found a positive association between attendance rate and increase in PM (43). Cheng et al. found a positive correlation between patients with respiratory conditions visiting ED and PM levels in a city in northwest China (45). They noted that children under 15 years, elderly and male patients were mainly affected with higher attendance recorded in the winter season. Kiser et al. looked at the association between asthma visits and PM in Nevada, USA (42). They found that wildfire smokes increase the association between PM levels and asthma visits especially in the immediate phase. They argue that PM from wildfire is more harmful to asthma patients than PM from non-wildfire causes and they hypothesise this to be due to the combination of a different PM composition, elevated temperature and patient behaviour during wildfire. Ozone was also an important factor in asthma attendances with two studies quoting specifically ozone-related asthma attacks (46,47). Nassikas et al. estimated the burden of ozone-related asthma attack in New England (47). They estimated an average rate of 3.2 (95% confidence interval: 1.52–4.75) per 10,000 population excess ozone-related asthma ED visits.

Some studies looked at mitigation strategies and tools to aid clinicians in detecting climate change-related conditions. One study from Friedman et al. explored a potential mitigation strategy through the use of telemedicine in the aftermath of a disaster to reduce ED attendances in a private hospital in the USA (48). This was a quasi-experimental study on the impact of a wildfire in California on ED admission of patients with conditions that would have been suitable for ambulatory care. They hypothesised on whether pre-existing familiarity with telemedicine could reduce ED attendance and hospital use compared with no familiarity. The study showed an overall reduced ED and hospital utilization. They argue that telemedicine access could keep patients from experiencing ill health and preventable hospitalization following a disaster. An important limitation is patient access to telemedicine and difficult generalisability to other countries where infostructures might be less developed.

Other studies explored clinical tools and mnemonic aids to help clinicians to diagnose and address heat-related emergencies arguing that these could be subtle and becoming more prevalent (20,26). Nicholas et al. developed a tool to help triage nurses in ED to identify climate-related conditions. In particular they stressed the importance of considering climate-related conditions such as heat strokes and educating on possible regional variations of extreme weather events to try anticipate ED demand (20). Khan et al. similarly did a quasi-experimental study on whether education on heat-related emergencies presenting to an ED in Pakistan could improve diagnosis and management of these conditions. In this study they claimed improvement of diagnosis from 3% to 7% and use of specific management such as external cooling methods from 1.3% to 3.4%, although it suffers from significant risk of bias from lack of blinding and the likely Hawthorne effect of pre- and post-implementation studies (26).

Two studies looked at the economic impact of climate-related conditions presenting to ED. The first from Nassikas et al. compared the cost of ED attendances of patients with ozone-related asthma in a scenario where the US government would have lowered their in-house gas emission compared to usual practice. In their study, the projected reduction of asthma cases prevented by reducing the ozone level would save the healthcare up to 1.7 million US dollars annually (46). The second from Wondmagegn et al. estimated the healthcare cost of projected increase in attendances due to heat-related conditions to EDs in Adelaide, Australia. It predicted a total spend of 4.5 million Australian dollars with an expected increase of 5% by 2050 (49).

Five studies looked at the aftermath of extreme weather events such as hurricanes (50-52), cyclones (53) and earthquakes (54) to the ED and the service demand that they required. In particular, a study from Mohanty et al. described the challenges faced by a tertiary ED in India following cyclone Fani (53). They described how the challenge of dealing with incoming trauma patients was also compounded by the hospital infostructure damage. Electricity blackout following the cyclone caused inability to utilise equipment, laboratory and imaging services, oxygen pipeline malfunction required massive relocation of patients from critical care areas and collapsed ceilings caused physical barriers to mobility within the hospital.

Some studies found in the literature search were categorised as studies that offered mitigation strategies or proposals for solutions. In some cases, these were commentaries made as a call for action required from all emergency physicians to become aware of climate change as a new challenge (19,25) with one commentary from Moretti et al. arguing that climate change should be added to the emergency medicine curriculum for residency in the USA (21). Two commentaries respectively from Ting et al. and Dryden et al. were an argument/counterargument on whether emergency physicians can make a meaningful impact on climate change (22,23). Suggestion on improvement were sustainable energy use, urban planning to facilitate public transport and healthier sustainable food, while the counterargument was that small adjustments from single individuals would be unlikely to bring to a significant reduction to the carbon footprint that the hospital generates.


Discussion

The narrative review highlighted the impact of specific disease burden due to either temperature increase or pollution and effect of extreme weather events on ED attendances. It also revealed studies focusing on potential solutions and strategies that could be adopted. To the best of our knowledge, this is the only review that analyzes studies on the association between emergency medicine and climate change, which highlights an important gap in the literature that needs to be filled. Not surprisingly, most studies pertained to high-income countries and only a few studies were from developing countries, reducing generalisability of the findings and suggesting the need for further research. Further will be discussed diseases specific effects of climate change and how they affect the provision of emergency medicine care.

Cardiovascular risk

Cardiac diseases are the biggest cause of death in the Western world and a major reason why people seek medical attention in the ED (16). Multiple studies have examined the increased susceptibility to CVD and morbidity linked to extreme heat conditions (16,55,56) with the main causal factor postulated to be the elevated heart rates, blood pressure, blood viscosity, and plasma cholesterol levels, which in turn trigger cardiovascular symptoms (56). Heatwaves have been associated with increase in cardiovascular mortality (55,57), ED attendances (16), and hospital admissions (58). A study from Wen et al. demonstrated a 10% increase in attendances to ED following a bushfire season in New South Wales in Australia. They suggest the health effect of bushfire seasons being related to oxidative stress at cellular level, platelet activation, thrombosis, and inflammation of vascular endothelia (58).

In a systematic review from Cicci et al., multiple studies reported statistically significant increase in ischaemic heart disease attendance to ED during heatwaves, an association between patients with myocardial infarction presenting to ED and increase daily temperatures and increase in ED attendance for arrythmia during heatwaves (16). Interestingly, there seem to be no association between heatwaves and increase in patients presenting to ED with decompensated heart failure, although a study found that pre-existing heart failure was a risk factor for patient to present to ED with a heat-related illness (16). Findings were more inconclusive for stroke attendances to ED. A major limitation of the review was the inclusion of only studies from US and Europe.

Pollution-induced rise in PM has also been recognised as a direct factor in the onset of cardiovascular disease (27,44). Short-term exposure to pollution triggers acute exacerbations, while long-term exposure results in decreased life expectancy (27). A study from Rahman et al. described how biomass burning in Bangladesh has been responsible for most PM air pollution but fossil fuel combustion PM affected CVD primarily (59). It showed a statistically significant increase in ED visits, hospitalisation, and mortality for seasons with increase in PM concentrations, although lower to effect sizes found in similar studies in developed countries. They argued that the cause of this finding is the lower prevalence of fossil fuel combustion in Bangladesh compared to high-income countries but it could also be explained by the different prevalence of CVD in the respective countries.

Country-specific responses to the crisis differ. Several countries are developing strategies to reduce the impact of climate change on cardiac health emergencies (60). While some countries place a high priority on public health campaigns that aim to educate the public about the dangers of CVD associated with heat and promote preventative measures, others invest in urban planning and put in place early warning systems for heatwaves to lessen the effects of heat islands. For instance, initiatives in the Netherlands emphasize early warning systems for heatwaves and community education (60). In France, the Plan Canicule reduces ED visits for heat-related CVDs by providing targeted interventions during heatwaves to protect vulnerable populations (61). Similarly, in Australia interventions include improving air quality and increasing access to cardiac care in bushfire-affected communities (61).

Despite efforts, many significant challenges still need to be overcome, such as unequal access to care, a lack of resources, and an inadequate healthcare infrastructure. It is recommended that future interventions prioritise interdisciplinary collaboration, policy advocacy, and public awareness campaigns to effectively address the intricate relationship between cardiac health and climate change (62).

Respiratory risk

Three major aspects of climate change have a significant impact on human respiratory health: the progressive global warming resulting from the greenhouse effect, the increased variability of weather patterns (63) and the increase in pollution (46). Respiratory diseases can be triggered directly or indirectly through the increased exposure to risk factors, the increased amount of allergens and the worsening air quality (63).

PM, ozone, and black carbon are three known air pollutants that are especially harmful to respiratory health (64). Higher pollen concentrations are thought to be caused by increased CO2 levels, and rising average temperatures have been shown to increase the allergenicity of existing pollens (65). As a result, more people are visiting ED and using healthcare services for allergic diseases. A large study from Liu et al. with data from over 600 cities around the world found an independent link between short-term PM exposure and all causes of respiratory mortality (66). Higher temperatures are associated with a greater ozone burden, which in turn increases the prevalence of hospitalisations for chronic obstructive pulmonary disease (67) and asthma exacerbations (68).

Wildfires are also linked to an increase in ED visits for acute dyspnoea caused by airway irritation from fumes and combusted particles in both patients with and without pre-existing respiratory diseases (69). In the USA, areas like California and the Pacific Northwest have been particularly hit by wildfires and various studies have been published on the subject (44). Direct exposure to smoke from wildfires is the main cause for reparatory deterioration (5). In Australia, extreme heat events and bushfires have raised respiratory health concerns, prompting EDs to deploy specialised respiratory care units and community outreach programmes (70). In China, where levels of air pollution are already elevated (71), there has been a number of studies showing increase ED attendance for respiratory conditions (29).

Asthma in particular has been a subject of interest given its direct link with climate-related changes. Seven studies looked at the increase in attendance rate, rate of diagnosis of asthma in ED (13,17,42,43,46,69,72). The increase in ozone levels seems to be a major contributor, with one study showing how a decrease in greenhouse production in the USA would allow for 3,100 averted attendances per year, together with a significant reduction in healthcare spending (46). As extreme weather events become more common with global warming, the risk of asthma epidemics, so called thunderstorm asthma, become more prevalent. In 2016, Melbourne in Australia has seen one of these events where an excess of 3,365 asthma attack in a single day during a storm, leading to overwhelm the major ED, a ten-fold increase in asthma admission and 10 deaths (17).

Governments and healthcare systems are progressively allocating resources towards climate adaptation initiatives, such as the establishment of air quality monitoring networks, implementation of public awareness campaigns, and improvement of respiratory care services in ED. However, to lessen the increasing strain that respiratory illnesses brought on by climate change are placing on emergency medical systems, coordinated worldwide action is required (73).

Gastrointestinal health

Elevated temperatures, extreme weather events, and changes in precipitation patterns all have direct and indirect effects on water quality, food safety, and the spread of infectious agents, exacerbating gastrointestinal illnesses (74). Diarrheal diseases are a leading cause of death worldwide, particularly in low-income countries and among people of extreme ages (75).

Hurricanes and flooding events have been associated with increased pathogen transmission, leading to illnesses when contaminated water is ingested (76). As ocean temperatures rise as a result of the greenhouse effect, the probability of extreme weather events such as storms and hurricanes is anticipated to increase (77). Arbour J. L. Quist conducted a study on the link between acute gastrointestinal illnesses (AGI) and two hurricanes that hit the country in 2016 and 2018. A 15% and 9% rise in AGI-related ED visit rates was documented in the flooded regions throughout the corresponding hurricane periods (76).

A scoping review by Theron et al. looking at the impact of climate change on emergency care in the African continent has identified flooding as a significant risk factor for outbreaks of infectious diseases, including cholera, malaria, leptospirosis, hepatitis A and E, schistosomiasis, and typhoid fever (12). Furthermore, elevated sea temperatures have contributed to a proliferation of waterborne pathogens, including Vibrio parahaemolyticus and ciguatera poisoning, both of which are prevalent contributors to seafood-associated AGI (18).

Another good example can be seen in Bangladesh where climate change has resulted in a heightened frequency of flooding which subsequently compromises the safety of drinking water sources and contributes to an outbreak of waterborne illnesses, including cholera and gastroenteritis (78). Similarly, rising temperatures in Australia promote the spread of foodborne pathogens such as Salmonella and Campylobacter, resulting in an increase in ED visits for gastrointestinal infections (79).

Three studies were found in our review regarding gastrointestinal pathologies. One study showed an association of gastrointestinal diseases after hurricanes (76), while another described an increase in the presentation to ED of patients with acute appendicitis (80). The third study from multiple paediatric hospitals in the USA showed an increase in gastroenteritis-related attendances (81).

Different nations have implemented diverse strategies in response to these challenges. Bangladesh has undertaken initiatives to develop community education on safe water practices in addition to infrastructure improvements related to water and sanitation (82). Australia has prioritised the improvement of surveillance systems and food safety regulations to reduce the incidence of foodborne illnesses (83).

Vector borne diseases

Infectious disease transmission is dependent on the interaction of host, agent, and environment, all of which are influenced by climate change (18,84).

The proliferation of vectors such as mosquitoes and ticks is facilitated by rising temperatures and altered precipitation patterns. As a result, the transmission of diseases including malaria, dengue fever, Zika virus, and Lyme disease has significantly increased (84).

Climate change has the potential to expose populations to a greater risk of mosquito and tick-borne diseases, leading to the emergence of novel diseases not typically endemic to specific regions (18). According to the Intergovernmental Panel on Climate Change, over the next 80 years, it is projected to be a rise in the prevalence of diseases such as malaria, Lyme disease, West Nile virus, and dengue fever (85). For instance, Aedes mosquitoes are increasingly being found in temperate regions such as North America and Europe, while Lyme disease and other tick-borne illnesses are rising in Canada (86).

Malaria, one of the most lethal and well-studied vector-borne diseases sensitive to climate, accounted for over 600,000 deaths in 2020 (87). Its spread has been observed to increase with rising temperatures, even reaching higher altitudes in regions like Ethiopia where it was not previously common (87).

Heatwaves have been associated with the proliferation of West Nile virus infections, as seen during an extreme summer heatwave in Europe in 2010, which led to a notable surge in cases (88). The nonspecific clinical manifestations of some vector-borne diseases pose challenges for diagnosis, underscoring the importance of emergency medicine physicians being cognizant of local shifts in disease rates driven by climate change.

A coordinated efforts from healthcare systems and governments to adapt and respond effectively to the evolving threat of vector-borne diseases is urgently needed. In Brazil, for example, the government took proactive steps to reduce mosquito breeding sites and increase public awareness about disease prevention due to the rising incidence of dengue fever (89). These measures included intensified mosquito control programmes and community engagement campaigns. Similar efforts have been made by the Indian government to distribute insecticide-treated bed nets to vulnerable populations and promote early detection and treatment of malaria, which is endemic there (90).

Healthcare professionals in the USA are increasing surveillance efforts due to the spread of Lyme disease and educating the public about preventive measures like donning protective gear and applying insect repellents (18). Additionally, research into innovative vector control methods, such as genetically modified mosquitoes, is underway in various countries to combat the spread of diseases (18).

Disaster management

Catastrophic events such as cyclones, storms, hurricanes, flooding, earthquakes, and landslides are predicted to increase as a direct effect of global warming (91). EDs are at the forefront of reception, management, and treatment of patients affected by natural disasters, and preparedness for these events will become increasingly important over time. The WHO projects that between 2030 and 2050, these phenomena will be accountable for over 250,000 annual fatalities in Europe alone (75). Consequently, ED are likely to witness a surge in patients with minor or serious injuries. The massive influx of patients in a short period during a major incident disrupts the regular service in EDs. Therefore, hospitals worldwide need to be prepared for major incidents by planning and simulating the response to these critical events (24). Natural disasters can also lead to infrastructural collapse, causing damage to electrical systems, mobile network breakdowns, and water supply failures that can impact both patients and hospitals (53).

In the aftermath of Hurricane Katrina, the USA experienced overcrowded EDs, impeding the timely delivery of medical care (92). Similar to this, Bangladesh faces increased flooding and cyclone risks, which increases the need for emergency medical care as well as for evacuation activities (78).

We found five studies in our review with the key theme being the cause of attendance to ED following hurricanes (50-52) and cyclones (53) with most studies describing trauma and orthopaedic injuries being the most common reasons.

In response to disasters, countries worldwide are implementing various strategies to enhance disaster preparedness and response in emergency medicine (93). For example, the Netherlands has invested in flood prevention infrastructure and early warning systems to reduce the health risks associated with flooding (94).

Mental health

Climate change has a profound impact on mental health, manifesting through various direct and indirect ways, which in turn escalate the demand for emergency mental health services. Direct pathways encompass exposure to traumatic events such as bushfires, flooding, droughts, and other extreme weather occurrences. Indirect pathways involve climate-related disasters like forced displacements and loss of livelihoods, culminating in poverty, unemployment, and housing instability (95). Moreover, climate change exacerbates the vulnerabilities of marginalized populations, including those grappling with pre-existing mental health conditions and economic hardships, thus heightening the risk of mental health disorders (96).

The spectrum of mental health effects spans from mild stress and distress symptoms to clinical disorders, encompassing anxiety, sleep disturbances, depression, post-traumatic stress disorder (PTSD), and suicidal ideation. Particularly vulnerable are individuals and communities in low-income countries, expected to bear the brunt of climate change impacts. Responses to extreme events involving disruption of life, such as loss of life, property, social support, or extensive relocation, often lead to PTSD, depression, and anxiety, contributing to increased substance abuse, higher rates of sexual assault, and domestic violence (97,98).

Seven studies were found in our review that investigated the impact of climate change on mental health illnesses in the ED. The majority of these studies showed a direct relationship between rising climate temperatures and increase in ED attendances for conditions such as schizophrenia, depression, bipolar disorder, substance misuse and personality disorders (33,36). Additionally, a study done in the USA showed a direct correlation between pollutants (ozone and PM) and increased hospital admission for psychiatric disorders (99). Furthermore, a systematic review reported an elevated rate of suicide (both completed or attempted) as a direct consequence of climate change (14).

Trauma and environmental diseases

Rising temperatures and extreme weather events may lead to an increase in ED trauma admissions. Traumatic injuries comprise a significant portion of direct mortality during extreme weather occurrences, notably in incidents such as car and motorcycle accidents (98).

The increase in average temperatures has been associated with the increase in attendances to ED related to fractures and injuries in the UK (40) and a large study from 18 sites in China had a similar result (93).

Environmental shifts, including alterations in temperature, humidity, sun exposure, and land surface temperature, are linked to heightened heat vulnerability, particularly in urban locales. A recent study conducted in China utilized land surface temperatures to gauge exposure, severity, and adaptability, thereby determining heat vulnerability among the population (100). Heat-related illnesses disproportionately affect individuals affected by homelessness due to their social circumstances, reduced access to care, and the intricate interplay of substance misuse and mental health disorders (101).

Renal and urological disorders

Heat has been linked to increased ED visits for patients with acute kidney injuries (30,31). Elevated temperatures can result in dehydration, blood hyperosmolality, and rhabdomyolysis. Moreover, chronic kidney disease is speculated to be more prevalent in regions with extreme heat exposure, primarily among workers (102). Kidney stone incidence demonstrates a correlation with ambient temperature, with higher temperatures in geographical areas associated with increased kidney stone formation, indicating an expected rise in patient admissions for urolithiasis (103).

Neurological conditions

Rising temperatures have been associated with heightened ED attendance among patients with multiple sclerosis (MS), attributed to relapse and acute exacerbation of their condition (37,38). The increase in body temperature, whether due to pyrexia from infection or from environmental factors is known to cause relapse in MS patients, condition called Uhthoff phenomenon. One study correlated increase pollution with additional ED attendances for patients with migraines (104). Experimental studies have linked air pollution with neurological damage and the combination of increase in temperatures and PM have been associated with migraines but the exact causation is still not clear (104).

Endocrine and dermatological disorders

A study investigated the correlation between an increase in daily high temperatures and a rise in ED attendance among patients with diabetes-related complications (15). Patients with DM are particularly prone to complications related to heatwaves because of their impaired autonomous nervous system response and also because of the overall increase in risk for CVD and renal diseases associated with pollution and increase in average daily temperatures. Two separate studies looked at dermatological conditions. A study from Pearson et al. observed the association of rising daily temperatures and increased ED visits due to hands foot and mouth disease in California (39) likely explained by coxsackie and enteroviruses thriving in humid and warm temperatures. They saw a 2% increase in ED attendances during the warm season per 1 ℉ increase in daily temperatures (39). A study from Chen et al. looked at the impact of flooding on ED attendances for atopic dermatitis flareup in children in the Taiwan region (105) with an odds ratio of 1.14 comparing case weeks with typhoons and control weeks. This is explained by an average rise in relative humidity, increasing the environmental dampness, an important risk factor for atopic dermatitis.

Mitigation strategies

Various options have been proposed to address the climate crisis in EDs worldwide. In the UK and Ireland, the RCEM has introduced the Green ED initiative to measure and reduce the environmental impact of EDs and to develop sustainable practices within the specialty (106). Their framework outlines different actions divided into bronze, silver, and gold levels that each ED should achieve to improve sustainability. Examples of actions include exclusive use of recycled paper, reduced use of Entonox, effective waste recycling, provision of reusable sharp bins, and minimization of electricity usage.

The concept of climate-smart healthcare was defined in 2017 by the World Bank Group and Health Care Without Harm as strategies to reduce carbon footprint and increase the resilience of healthcare systems (107). In the USA, the Climate Smart ED initiative suggests three major approaches to minimize contributions to climate change: addressing hospital operations, implementing departmental initiatives, and encouraging individual actions (19). Hospital operations may involve tracking wastage and implementing waste reduction or environmentally preferred purchasing options. At the departmental level, efforts may focus on increasing energy and water efficiency, reducing wastage, and minimizing the use of non-recyclable products. On an individual level, actions may include advocating for low-emission transportation and making lifestyle changes.

In Australia, a study on the impact of climate-related disasters on the health and well-being of healthcare workers (HCWs) has led to the development of the ‘HCWs Resilience Toolkit’. This toolkit, developed through interviews with staff affected by natural disasters at work, encourages policymakers to support HCW needs such as wellness, education, resources, and communication (108).

In our review of the literature, we also found initiatives to raise awareness and inform emergency physicians about climate-related emergency conditions. In Karachi, Pakistan, an educational intervention focused on heat emergency awareness and treatment improved the approach to heat-related emergencies in four hospitals, leading to increased rates of diagnosis and accurate treatment post-intervention (26). Another tool developed in Boston, known as A CLIMATE, helped providers recognize, diagnose, and treat conditions commonly associated with climate change (20).

Historically, the climate crisis has been framed as an environmental challenge, with health impacts often receiving little attention. As the climate crisis threatens to disrupt healthcare delivery, emergency medicine has the opportunity to mitigate exposures and improve health outcomes by applying climate-aware clinical decisions and behavioural interventions to care plans (109). Physicians continue to serve as trusted public health communicators and policy drivers. However, a workforce of clinicians with specific skills to address the climate crisis remains absent, despite the intersecting roles of climate and health policy. This gap is influenced by factors beyond healthcare, necessitating a broad, cross-sectoral approach to health policy (110).

The US Department of Health and Climate Resilient Health Services developed the Sustainable and Resilient Climate Healthcare Facilities Toolkit, in response to hospitals being forced to close and evacuate during hurricane disasters, resulting in devastating losses in infrastructure assets. Building resilient EDs and healthcare systems can minimize morbidity and mortality during such critical times (111).

Limitations and need for further research

There are various limitations inherent in this study. The search strategy was limited to publications written in the English language, which may have resulted in the exclusion of studies conducted in low-income or non-English speaking countries that lacked access to English publications.

In addition, we limited the study’s scope to the last five years as we wanted to highlight current research and we believed that recent studies would be more specific to the current climate situation.

We noticed a gap in research pertaining to climate change and its impact to emergency medicine as most studies would have looked at single conditions and not how attendances and patterns of presentations are changing in view of the global warming. Some published studies called for action for physicians to become aware of climate change but there were no systematic reviews or metanalysis on the subject. We hope that this article adds to the growing literature on the effect of climate change on emergency medicine and encourages further research on the topic.


Conclusions

Climate change will inevitably play a vital part in provision of emergency care to patients in the coming future. Knowledge of its impact and the potential solutions to this problem can be of help for future clinicians. By recognising the challenges, emergency physicians can continue provide care to individuals affected by climate-related emergencies, while also contributing to the broader effort of building a resilient and sustainable healthcare system.


Acknowledgments

Funding: None.


Footnote

Reporting Checklist: The authors have completed the Narrative Review reporting checklist. Available at https://jphe.amegroups.com/article/view/10.21037/jphe-23-87/rc

Peer Review File: Available at https://jphe.amegroups.com/article/view/10.21037/jphe-23-87/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jphe.amegroups.com/article/view/10.21037/jphe-23-87/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.


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doi: 10.21037/jphe-23-87
Cite this article as: Dalla Vecchia C, Sadik A, Jonah L. Impact of climate change in emergency medicine: a narrative review. J Public Health Emerg 2024;8:27.

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