SCCM Pod-522 PCCM: Early Adrenaline Infusion Versus Standard Fluid Resuscitation in Children With Septic Shock

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Host Elizabeth H. Mack, MD, MS, FCCM, is joined by Luregn J. Schlapbach, MD, PhD, FCICM, to discuss the Pediatric Critical Care Medicine article, “Resuscitation With Early Adrenaline Infusion for Children With Septic Shock: A Randomized Pilot Trial” (Harley A, et al. Pediatr Crit Care Med. 2024 Feb;25:106-117). The study found that a fluid-sparing algorithm for children presenting with septic shock using early adrenaline is feasible. Dr. Schlapbach is a professor and chief of intensive care and neonatology at the University Children's Hospital in Zurich, Switzerland.

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Transcript:

Dr. Mack: Hello and welcome to the Society of Critical Care Medicine Podcast. I’m your host, Dr. Elizabeth Mack. Today, I’ll be speaking with Dr. Luregn Schlapbach, MD, PhD, fellow of the College of Intensive Care Medicine, about the article, “Resuscitation With Early Adrenaline Infusion for Children With Septic Shock: A Randomized Pilot Trial,” published in the February 2024 issue of Pediatric Critical Care Medicine. To access the full article, please visit pccmjournal.org. Dr. Schlapbach is a professor and chief of intensive care and neonatology at the University Children’s Hospital in Zurich, Switzerland. Welcome.

Dr. Schlapbach: Hi, Dr. Mack. Thank you so much for the invitation. It is a pleasure to be here with SCCM, and I look forward to this podcast.

Dr. Mack: Wonderful. Before we start, do you have any disclosures to report?

Dr. Schlapbach: There’ve been a number of foundations who supported the paper we’re reporting on, which are cited in there, and I have no other disclosures to report.

Dr. Mack: Thank you so much for sharing. First, if you don’t mind, just tell us a little bit about the RESPOND ED study group. How was this collaborative formed? What have you been working on together? What sort of hospitals are represented in the group? We’d love to hear.

Dr. Schlapbach: The origins of these studies date back to discussions we had with clinicians in Queensland, Australia, when a sepsis quality improvement initiative was started. We realized that there was actually a certain discrepancy between the guidelines recommending to use 40 to 60 mL/kg of fluid before starting inotropes and an increasing concern by clinicians on how much fluid should be used.

This essentially led to some of the first discussions between clinicians and researchers, and we said, well, this is probably an important area for a trial. After over a year of preparation work, which included a lot of discussions with clinicians and stakeholders, we formulated a protocol for this pilot trial, which then in the end was conducted across four pediatric emergency departments in Queensland, Australia.

Dr. Mack: Okay, thank you. Sounds like a collaborative, mature work group, so I appreciate you sharing a bit more about that. Tell us a bit more about your primary end point and why your study group felt the need to challenge the status quo, i.e., the Surviving Sepsis Campaign guidelines.

Dr. Schlapbach: Maybe it’s worth it to just take a bit of a step back. Pretty much, 20 years ago when the early goal-directed therapy papers from Rivers were published, it was a strong belief that actually sepsis deaths as well happened because of delayed resuscitation. Of course, delayed resuscitation encompasses aspects such as treatment with antibiotics, with fluids, or with inotropes or with other aspects of management, such as transfusions.

This essentially led, in pediatrics, to relatively fluid-aggressive resuscitation in many children who then received actually well over 16 mL/kg of fluid in the first few hours. The original guidelines, this is if you go back to, for example, 2008 guidelines or, as well, more recent ones from ACCM, they recommend pushing fluid in very, very quickly, assuming that actually through pushing fluid that hemodynamic stability can be restored quicker. But there is actually no high-grade evidence to support that management.

There is strong observational evidence supporting, on one side, that delayed resuscitation with a focus on delayed antibiotics increases mortality in sepsis, but there is as well an increasing observational body of evidence that indicates a strong association of fluid overload with increased mortality, even if you correct for severity. So we’re currently a bit left in limbo in terms of the data, in terms of what should we do when it comes to fluids and inotropes for children with sepsis.

The only high-quality recommendation in the Surviving Sepsis Campaign published in 2020 specific for kids, the only high-grade evidence in the whole over-70 recommendations, pertains to the amount of fluids used, and this is based on the FEAST study. The FEAST study was conducted over 10 years ago in a setting in Africa where no intensive care could be provided, for example, no ventilation. Over 3000 children were randomized to no fluid or normal saline as opposed to an albumin fluid bolus.

The mortality in all study groups increased already with the first fluid bolus. So, based on the FEAST study, actually increasing caution with administering fluids would be justified. However, we do not know to this date if this evidence is transferable to a setting where we can provide intensive care. So the question was, how would a trial need to look that essentially addresses strategies to use a more restrictive amount of fluids during early resuscitation for sepsis? There are a number of adult studies recently published that have looked at this, such as the CLOVERS study or the CLASSIC trial.

So our question was actually, what type of design is needed to look at this for kids, because there were concerns about the feasibility of such. First of all, would there be enough patients? Then as well, would clinicians adhere to such recommendations? The third question was, would it be feasible actually to develop inotropes within such a quick time frame?

We thought it was absolutely essential to first properly design a pilot study. For the pilot study, in terms of the primary end points, what we said actually, we need some feasibility end points, but we need as well patient-centered end points as well as some proxy of efficacy. So we have defined as the primary feasibility end points essentially compliance with the study protocol and with a particular focus on recruiting rates but, as well, time to initiation of inotropes between the control and the early inotrope arm and, as well, we were keen to see if we would find a separation in terms of the amount of fluid delivered during the first 24 hours between the arms.

In terms of clinical outcome, the hypothesis was that if we would use earlier inotropes and less fluid, we would have less side effects associated with fluid overload so that essentially the patients would recover quicker. We operationalized this by a measure of organ dysfunction-free survival censored at 28 days of randomization. In addition, we had a number of secondary outcomes to explore associations with clinical outcomes such as survival free of inotrope support, free of multiorgan dysfunction, mortality, PICU length of stay, and hospital length of stay.

In addition, we captured at 28 days the functional status score as well as the modified pediatric overall performance category. Finally, as well, we obtained measures on proxies of the intervention efficacy. We assessed the amount of fluid delivered as well as the proportion of patients with a low lactate, less than two mmol/L, as well as time to reversal of tachycardia and time to shock reversal, which we defined as the cessation of inotropes for at least four hours, again censored at 28 days.

Dr. Mack: Wonderful. Thank you for that background and really how you got to this study design. I’m very impressed by the quick times to randomization and intervention, and particularly the fact that you had 100% of your families of those approached consented. If you don’t mind, just tell us a bit about the consent process. Maybe not all of us are familiar with the concept of consent to continue versus written informed consent.

Dr. Schlapbach: Because this is a randomized controlled trial, the ethics board considered it necessary to have consent from parents, given as well that children in the age group studied, of course, are a particularly vulnerable group. However, the ethics board in Australia agreed that there could be two ways of obtaining consent, which is something that is becoming more and more standard in many critical care or acute care studies.

One is the traditional, what we call prospective consent, so that essentially clinicians or study teams talk to parents and ask for permission to randomize them and will randomize them actually with that permission. The other approach is so-called consent to continue, which is where actually clinicians are allowed to include the patient in the trial already before having consent from the parents, then afterwards actually need to go explain the study to the parents and ask for permission to include these data. Parents then are given the opportunity actually to withdraw essentially from the study.

What we talk about here is an extremely time-critical disease. We talk about children presenting with septic shock, where clinicians consider it an urgent need of the patients to receive some type of cardiovascular resuscitation. We know that the dynamics of these diseases are very, very quick, so this is a truly time-critical aspect. In addition to this, we do know that parents are extremely stressed at such times. They present to the emergency department often with very substantial concerns for the life of their children, so this is not a good time for parents usually to be approached about consent.

There’s evidence actually or data from focus groups, in particular from the UK but as well from the U.S. that show that it may not be family centered to ask parents for consent in that setting immediately and that actually consumers have stated often that they prefer to be asked for consent after. However, this approach is only possible if both interventions are considered acceptable and safe.

What we were able to argue towards ethics is that this discrepancy between guidelines in high-income countries and at the same time what the SSC recommends for settings where no intensive care can be provided based on the FEAST evidence that, given this discrepancy, actually both the early inotrope intervention arm, as well as the standard resuscitation arm with 40 to 60 mL/kg of fluid first, actually would be acceptable and compatible with current evidence. So this was the approach we applied.

In total, we randomized 43 children. We missed 15 patients because they were not approached for consent. So essentially, if you want, this is almost like a screening failure. But of the 43 who were actually randomized, most of these were included in consent to continue. So, specifically speaking, these were 36 patients. In five cases, we attempted prospective consent. In one case, this was not feasible to be finalized. In no case did parents withdraw from the study, which gives essentially the high consent rates. Again, this to us indicates that there is a strong wish from parents, at least in the setting where we did this study, for such studies to be conducted and a very broad willingness for families to be part of such studies.

Dr. Mack: Wonderful. Thank you for that. I think there’s a lot to be learned there. You mentioned screening. What was the screening process like? I noted that you had coordinators screening 24/7. How did that work? And how did you resource this with an average of one to two patients per month being recruited among all the sites?

Dr. Schlapbach: First of all, I would really like to extend my gratitude to all the clinicians, doctors, and nurses in the participating EDs who made this possible. Because it was not feasible, of course, to have research staff 24/7. But we had research staff having a strong presence, in particular during daytime at nursing handovers to really make sure that the study was on everyone’s mind. But in the end it was in particular after hours, as many of these kids present, it was the clinical teams who actually had to think of the study and then actually call the study team. So I think this was one aspect.

The second aspect was that, as in many parts of the world, there were strong initiatives for quality improvement around sepsis happening at that stage. Certainly this was a time when the awareness of sepsis was strong and where actually the use of sepsis pathways to sort of say, could this be sepsis? Think this could be sepsis? That message was part of a lot of education to clinical staff.

The third aspect was that we spent a lot of time with the clinicians thinking through, what can we do to make this study as easy as possible to perform, to avoid that a child is eligible but then does not get randomized because someone doesn’t remember how to randomize and things like this.

So we ended up having packages with all study materials in the EDs. We had posters and they were made in a way that actually clinicians could very quickly grab the package. There was a booklet with clear-cut instructions. They had to open an envelope and so on. With this as well, what we realized was that as soon as a clinician thought, could this be sepsis, they were prompted to think of the study, and if they started giving a first fluid bolus to a patient, we recommended that already they draw up adrenaline, but that the randomization only happened once the first fluid bolus was given.

By this, what we achieved was that actually the adrenaline was given fairly quickly in those who were allocated to that arm. This had been one of our major feasibility concerns before we did the trial because we thought, from the time that someone decides to use adrenaline until it’s actually prescribed and drawn up and in the end administered to a patient, in particular in kids, we were concerned that too much time may elapse. And we’re concerned that, in the worst case, this potentially could result in a disadvantage to the kids.

So maybe one of the hidden success stories of this pilot was as well that, in the beginning, in particular ED nurses and ED doctors said, well, inotropes in pediatric EDs is an intervention that intensivists have much more experience with rather than ED physicians. And a bit similar to the reverse trial, which sort of tried to take early resuscitation out from the ICU into the ED to really enable early resuscitation, we tried to have a similar approach in the education of staff to explain to them that inotropes are drugs, in particular adrenaline, that clinicians can fairly quickly become familiar with, that there are not that many risks really with starting an inotrope in particular for a few hours or in particular in kids.

Concerns on inotropes such as hypertension, arrhythmia, and so on are much less relevant in kids. Concerns pediatric physicians have much more are things like extravasation. We were able to show, using the protocol, the way we diluted adrenaline, that actually this was very safe and we did not have episodes of extravasation leading to tissue necrosis and so on.

I think this is important because, in my life as an intensivist, I’ve seen probably most treatments used way too much in EDs or in other pre-ICU settings. Take fluids, for example, take antibiotics, take steroids, take salbutamol, and so on. Many, many treatments are used very generously that often actually we stop them when patients come to the ICU.

But I’ve never seen this happen with inotropes. When a child comes to the ICU on inotropes, they usually need it. This probably indicates that we don’t use it enough pre-ICU, that thresholds to start inotropes are too high. One of the actually not-scientific aspects of this work was really to get the team familiar with how to use inotropes and lose maybe some of the fears around using inotropes.

Dr. Mack: Wonderful. I really appreciate your, as a quality and safety person, referencing the extravasation concerns and also what you saw in terms of it being a very safe intervention. Can you share a bit about how the intervention occurred? For example, would it be typical for septic children to stay in the ED for four to six hours on one hand? I think it’s really interesting to triage and see who responds and wean them off and send them to the floor earlier if they’re able. On the other hand, it seems like a burden on the ED. Interesting to hear a bit about how this happened.

Dr. Schlapbach: As you can see in the paper, actually we had two study arms and we had a one-to-one allocation to standard care, which was defined as giving 40 to 60 mL/kg of fluid before starting inotropes, as opposed to the intervention arm, where we said that inotropes should be started after 20 mL/kg, maximum 40 mL/kg of fluid. Essentially the study protocol mandated the use of adrenaline for such.

This may be something we can discuss later on, but was adrenaline the right drug or what’s the justification to use adrenaline? Now, in patients in the standard arm, we anticipate that essentially clinicians will do what they were used to do, so that their thresholds as to when to admit the patient to the ICU would be guided by their current practice.

But in the early inotrope arm, we actually said, okay, what happens if a patient now is being put on inotropes who usually would not be on inotropes and then the patient is in the ED? Do all these patients automatically go to the ICU? So what we said in the protocol was that these patients should be assessed closely in order to make a call as to whether they were actually dependent on the inotropes or deteriorating or whether inotropes could potentially be stopped. For this, Queensland has a standard operating procedure that essentially kids should not stay in the ED for longer than four hours. There are a few actually who stay longer than four hours, but that’s sort of the threshold. Most kids who are treated for sepsis, treatment started very, very quickly, within often an hour or two of presentation.

In the early inotrope arm, this specifically meant that we foresaw that there may be a small proportion where actually the ED staff may start inotropes but then, after some time of observation, decide again to stop it. Indeed, there were actually very, very few patients where this happened. Most kids actually, when inotropes were started, they were transferred from the ED to the ICU. Overall interesting actually, the study was not felt as a burden by the ED and we did not observe prolonged length of stay in the ED nor prolonged length of stay in the ICU.

Dr. Mack: Thank you so much. Could you share just a bit about your findings and results?

Dr. Schlapbach: We had in total, as mentioned, we were able to analyze 40 randomized episodes where we obtained consent, of which 23 were allocated to standard care and 17 were allocated to the intervention arm. The reason for the slight imbalance between the arms is that we used block randomization, which then of course for a relatively small sample size, which this pilot was, can lead to these slight imbalances.

The characteristics, maybe just briefly speaking of patients, are what are fairly common. We had an age group, in the standard care, of an average age of about six years and two years in the early inotrope arm with a roughly 50-50 split in terms of sex. Most patients actually were previously healthy. Just less than a third of patients had some type of chronic disease. This was really a community-acquired sepsis cohort. At presentation, actually, they were moderately unwell. In terms of pediatric SOFA score, they had an average score of two in the standard care arm and median score of four in the early inotrope arm.

When it comes to the results and when it comes to feasibility outcomes, we said the time from randomization to any inotrope infusion commencement was one of the key feasibility aspects. This was 49 minutes in the standard care arm and 60 minutes in the early inotrope arm, so a difference of over half an hour.

When it comes to the difference between time from randomization to the initiation of adrenaline infusion, this went from 42 minutes in the standard care arm to 16 minutes in the early inotrope arm so, again, a difference of almost half an hour. If you look at the proportion of patients who received inotropes within the first hour, this increased from 39% in the standard arm to almost double to 76% in the early inotrope arm. And if you look at the number of patients who received any inotrope within the first 24 hours, this increased from 57% in the standard arm to 76%, so this was coupled with a reduced amount of fluid, and the difference was 20 mL.

Children allocated to the early inotrope arm received a median of 20 mL/kg of fluid less. Most of this difference actually came from the amount of fluid received in the first hour. In terms of feasibility, what we could say is that actually the protocol was relatively well adhered to, that it was feasible actually to use adrenaline over half an hour earlier on average and that this was associated as well with a reduced use of fluid of about 20 mL/kg difference.

Interestingly, this effect size, actually, if you say you have a 52- to 100-kg adult, this would translate into a difference in terms of the amount of fluid received between one and two liters per patient, which is very similar to the difference observed in fluids in the CLASSIC or the CLOVERS adult RCTs, right? So, again, this sort of shows that we can deploy a different design but with some similarities to CLASSIC or CLOVERS to pediatric patients.

However, what the feasibility aspects show as well is that, in the 17 kids randomized to early inotropes, only 13 of them actually received any fluids. So there was roughly one in four kids randomized to early inotropes who did not end up getting any inotropes or any fluids, right? This means, as well, that the average acuity in this course in some patients was relatively low and that some patients even improved actually without receiving further fluid.

This of course is an important consideration for thinking then about a large study, right? Now, if we think about clinical outcomes, first of all, remember this is a pilot trial, so this was not powered for clinical outcomes, but the primary outcome of survival free of organ dysfunction censored at 28 days was a median of 26 in the standard care arm and one day more, so 27, in the early inotrope arm.

If you look at secondary outcomes, for example, survival free of inotrope support at seven days, that was the same, 6.8, in both arms. Or if you look at survival free of the PICU, this was 26.4 in the standard care arm and 27.2 in the early inotrope arm. When you look at time to shock reversal, this was 5.1 hours in the standard care arm and 4.8 hours in the early inotrope arm. None of these exploratory clinical outcomes suggests that the children who received early inotropes with less fluids did worse.

Again, this is not powered, this is purely exploratory but, if at all, the effect size points to at least equal performance or potentially even benefits of early inotropes and less fluids. So we thought this was an important safety signal from this pilot, which in principle would justify doing larger trials.

Dr. Mack: Wonderful. Thank you. Very promising results. In a little over two years at four children’s hospitals, it sounded like you screened about 628 children and 69% of the eligible children were enrolled. It sounds like some were screening failures. Any thoughts on the others?

Dr. Schlapbach: In the EDs included in this study, remember this is a metropolitan pediatric specialized ED in a high-income setting in Australia during a time when there were a lot of education activities on sepsis. What we realized was that there are many, many children evaluated for sepsis, but most of these actually are not considered to be in shock or most of these actually are not considered by clinicians to receive more than one fluid bolus, right?

Because the inclusion criterion was that kids had to have received at least 20 mL/kg of fluid, no more than 40 mL/kg of fluid in the past four hours, and that clinicians thought that ongoing treatment for shock was required. What essentially Figure 1 in the paper shows you is that, out of all kids assessed for eligibility with suspected sepsis, most of these kids are actually not receiving fluid resuscitation or doctors decide to stop resuscitation after one fluid bolus because the patient looks much better, right?

So this is this huge funnel actually from thinking about sepsis to then actually children who are in septic shock refractory to a first fluid bolus. This of course is not translatable in the same way to other healthcare settings. If you go, for example, to South America, where the average acuity may be much higher, actually numbers may look very, very different.

We realized as well that this was a major feasibility challenge for us, that, although adherence to the protocol was actually reasonably good, the number of eligible patients per site actually was too low. This is an interesting parallel to the FISH study, which David Inwald ran in the UK, where as well they showed they were able actually to conduct the study protocol with fairly good adherence, but that actually the number of eligible patients was low. The other aspect and, again, this is very similar to the FISH trial in the UK, was that the average acuity was quite low.

I already mentioned the Pediatric Sequential Organ Failure Assessment score, which was between 2 and 4 in most patients, but mortality as well in the kids we’ve included here actually was zero. So of course this means as well that, while we’re able to show in this setting here that the protocol in principle actually is feasible, this is not a setting where conducting a fully powered trial for clinical end points probably would make sense because the acuity overall seems to be too low and, as well, the number of patients may be too low.

Dr. Mack: Thank you. That makes a lot of sense. I appreciate you walking through that. Just as a little bit of a plug for the Children’s Hospital Association, the Improving Pediatric Sepsis Outcomes Collaborative has seen a reduction in mortality with a very large sample across many U.S. hospitals. The final analysis is not yet complete, but I’m curious, can you share a bit about the statewide sepsis QI collaborative prior to this study and how it may have primed your teams for this work? You mentioned there was a lot of ongoing education in this space.

Dr. Schlapbach: Yes, we’ve published some of the findings in Critical Care Explorations and we’re able to show, similar to the U.S., that actually process measures such as time to antibiotics, for example, were dramatically reduced for kids included on the sepsis pathway during the campaign, but the population included there was just slightly over two million in terms of total population. The amount of sick children presenting to these was not sufficient to be powered to look at mortality outcomes. Of course, the IPSO collaborative in the U.S. is probably currently what I would consider sort of the gold standard for pediatric sepsis quality improvement initiatives and they’ve done really very impressive results, not only in relation to process outcomes, but as well in terms of patient-centered outcomes.

Dr. Mack: I appreciate all the work that you all are doing on that side of the pond. Tell us, what’s next? Is your team managing sepsis in children differently now after this pilot study?

Dr. Schlapbach: First of all, this was a pilot study, so certainly not powered to change guidelines. What it certainly changed with the people involved is that they realized, in particular our colleagues in the ED and nurses, that it’s feasible to use inotropes earlier. We do think we’ve seen a benefit overall in the way inotropes are used. We’ve seen less children coming in with septic shock where there are big delays until inotropes are started. And I think the whole topic about fluid versus inotropes actually now has stirred a very interesting debate, right? But I think the next point now really is that there is a need for proper evidence.

On the one side, we’re eagerly awaiting the results of the SQUEEZE trial. The SQUEEZE trial is led by the Canadian group and actually compared children receiving 40 mL/kg to those receiving 60 mL/kg of fluid. I hear that the trial has completed recruitment. We really hope to see these data. However, this is already, when you think of the FEAST data, starting at 40 mL/kg of fluid, that’s already quite a lot of fluid actually. There are even some recent Indian data that showed in a randomized setting that giving less fluid slower as opposed to giving more fluid faster already makes a difference, for example, in the amount of children who end up on a ventilator or in terms of their oxygenation index, right?

From this perspective, we do think it’s important to explore further where and which settings would fluid-sparing approaches during early sepsis resuscitation in kids be promising to be studied more in detail. We’re currently working with colleagues in Latin America to essentially repeat the RESPOND ED study in their setting, first of all, to test the feasibility there but as well to see actually now if that could be used as a stepping-stone towards the next larger trial.

In this context, I think you may have seen there was a viewpoint in the launch of Child Adolescent Health last year where we discussed with colleagues from low- and middle-income settings how some of these controversies around fluids and inotropes could be put into context. That viewpoint, led by Suchitra Ranjit from India, is by no means a guideline. It’s actually intended more to stimulate clinicians to think around the concepts.

But essentially what we try and highlight there is that, as clinicians, we have to think not only of pressure outcome markers but, as well, feeling and flow of the patient and the dimensions we can use in addition to fluids or inotropes or, as well, vasoconstrictors. Many of our colleagues from less-resourced settings have shared their view with us that, subsequent to the FEAST study, even if you’re able to use inotropes or to use ventilation, many of them actually say, in septic states, excluding dengue, that they’ve become more cautious around fluids. So maybe it is time in the next years to conduct a properly powered trial with a similar design to RESPOND ED but maybe more focused for less-resourced settings.

Dr. Mack: Very exciting. Anything else you’d like to share that we haven’t discussed?

Dr. Schlapbach: Well, I’d just again like to thank all the colleagues from the trial group who made this study feasible but as well the parents and children who consented to being in this trial and of course the many, many clinicians, nurses, doctors, pharmacists who helped us actually conduct this study.

Dr. Mack: Well, thank you so much for all of the work that you and your colleagues did to get this study off the ground and to bring it to fruition. I look forward to seeing the next steps that come from this. This concludes another episode of the Society of Critical Care Medicine Podcast. If you’re listening on your favorite podcast app, and you liked what you heard, consider rating and leaving a review. For the Society of Critical Care Medicine Podcast, I am Dr. Elizabeth Mack. Thank you.

Announcer: Elizabeth H. Mack, MD, MS, FCCM, is a professor of pediatrics and chief of pediatric critical care at Medical University of South Carolina Children’s Health in Charleston, South Carolina.

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