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Original research
Assessment of adherence to the 2020 Surviving Sepsis Campaign guidelines for fluid resuscitation in children with suspected septic shock in paediatric emergency departments: a prospective multicentre study
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  1. Julian San Geroteo1,
  2. Michael Levy1,
  3. Marion Bailhache2,
  4. Claire De Jorna3,
  5. Elodie Privat3,
  6. Oussama Gasmi4,
  7. Maria Fuentes-Lopez5,
  8. Yacine Laoudi6,
  9. Mustapha Mazeghrane7,
  10. Aline Malterre8,
  11. Pauline Bories9,
  12. Khaled Abdel Aal10,
  13. Iozefina Arjoca11,
  14. Jean Gaschignard12,
  15. Davy Tanchaleune13,
  16. Philippe Minodier14,
  17. Fabien Audren15,
  18. Tifanny Mazetier16,
  19. Pauline Quagliaro17,
  20. Florence Raimond18,
  21. Soria Sieng19,
  22. Blandine Robert20,
  23. Delphine Wohrer21,
  24. Nathalie De Suremain22,
  25. Stéphane Dauger1
  1. 1 Pediatric Intensive Care Unit, Robert-Debré Mother-Child University Hospital, Paris, France
  2. 2 Pediatric Emergency Department, University Hospital Centre Bordeaux Pellegrin Hospital Group Children's Hospital, Bordeaux, France
  3. 3 Pediatric Emergency Department, Lille University Hospital Center, Lille, France
  4. 4 Pediatric Emergency Department, University Hospital Centre Nantes, Nantes, France
  5. 5 Pediatric Emergency Department, University Hospital Necker for Sick Children, Paris, France
  6. 6 Pediatric Emergency Department, Intermunicipal Hospital Centre Robert Ballanger, Aulnay sous Bois, France
  7. 7 Pediatric Emergency Department, Centre Hospitalier Intercommunal André Grégoire, Montreuil, France
  8. 8 Pediatric Emergency Department, Centre Hospitalier Intercommunal de Créteil, Creteil, France
  9. 9 Pediatric Emergency Department, Hospital Louis-Mourier, Colombes, France
  10. 10 Pediatric Emergency Department, Hospital Centre Gonesse, Gonesse, France
  11. 11 Pediatric Emergency Department, Centre Hospitalier François Quesnay, Mantes-la-Jolie, France
  12. 12 Pediatric Emergency Department, Groupement Hospitalier Nord Essonne, Longjumeau, France
  13. 13 Pediatric Emergency Department, Hospital Bicetre, Le Kremlin-Bicetre, France
  14. 14 Pediatric Emergency Department, Public Assistance–Hospitals of Marseille, Marseille, France
  15. 15 Pediatric Emergency Department, Intermunicipal Hospital Centre Villeneuve Saint Georges, Villeneuve Saint Georges, France
  16. 16 Pediatric Emergency Department, Hospital Centre Victor Dupouy Argenteuil, Argenteuil, France
  17. 17 Pediatric Emergency Department, Hospital Jean Verdier, Bondy, France
  18. 18 Pediatric Emergency Department, Hospital Antoine-Beclere, Clamart, France
  19. 19 Pediatric Emergency Department, Grand Hopital de l'Est Francilien, Jossigny, France
  20. 20 Pediatric Emergency Department, Centre Hospitalier de Pontoise, Pontoise, France
  21. 21 Pediatric Emergency Department, Robert-Debré Mother-Child University Hospital, Paris, France
  22. 22 Pediatric Emergency Department, Armand-Trousseau Children's Hospital, Paris, France
  1. Correspondence to Dr Julian San Geroteo; julian.san-geroteo{at}aphp.fr

Abstract

Background Paediatric sepsis is the leading cause of death in children under 5 years. No studies have evaluated the application of the Surviving Sepsis Campaign 2020 (SSC-2020) guidelines in paediatric emergency departments (PEDs).

Objective To assess physician adherence to the SSC-2020 fluid resuscitation guidelines in children with suspected septic shock in PEDs.

Methods This was a prospective multicentre observational study conducted in 21 French hospitals over 5 sequential weeks, between November 2021 and March 2022. Children with suspected septic shock and who received antimicrobial therapy within 72 hours were included. Primary outcome was SSC-2020 fluid resuscitation guidelines adherence (low 0–24%; moderate 25–74%; high 75–100%) according to: bolus volume of 10–20 mL/kg each, exclusive administration of balanced crystalloids at 1 and 24 hours of management, and initiation of fluid resuscitation within 1 hour of septic shock recognition.

Results 63 children were included. 10 (16%) children had severe sepsis and 2 (3%) met the definition of septic shock. Compared with the SSC-2020 guidelines, 43 (68%) patients received boluses of 10–20 mL/kg; fluid resuscitation was initiated within 1 hour of septic shock recognition in 42 (76%) cases; balanced crystalloids were the only fluids administrated in 35 (56%) and 34 (55%) children at 1 and 24 hours of management, respectively. Main barriers reported by physicians were difficult intravenous access (43%), lack of team training (29%), workload constraints (28%), and absence or out-of-date protocols (24%).

Conclusions This study found high adherence for fluid resuscitation initiation but moderate adherence for bolus volume and fluid choice.

Trial registration number NCT05066464.

  • Sepsis
  • Paediatric Emergency Medicine
  • Paediatrics
  • Intensive Care Units, Paediatric
  • Emergency Care

Data availability statement

Data are available upon reasonable request.

https://doi.org/10.1136/archdischild-2023-325837

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    WHAT IS ALREADY KNOWN ON THIS TOPIC

    • Paediatric sepsis is the leading cause of death in children under 5 years.

    • Adherence to fluid resuscitation guidelines has been shown to reduce mortality in paediatric intensive care setting.

    • To date, no studies have evaluated their application in children with suspected septic shock in emergency departments.

    WHAT THIS STUDY ADDS

    • Compared with the latest Surviving Sepsis Campaign 2020 (SSC-2020) guidelines, we found high adherence for fluid resuscitation initiation but moderate adherence for bolus volume and fluid choice.

    • The main barriers reported by physicians were difficult intravenous access, lack of team training, workload constraint, and absence or out-of-date protocols.

    HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE OR POLICY

    • A better definition of suspected septic shock is needed in paediatric emergency departments.

    • SSC-2020-based care protocols and teaching programmes emphasising early antimicrobial therapy and intraosseous access training should be implemented.

    • Future studies could investigate compliance with these guidelines and children’s outcomes after such programmes.

    Introduction

    Paediatric sepsis has been defined as proven or suspected infection in presence of systemic inflammatory response syndrome and septic shock as sepsis plus cardiovascular organ dysfunction.1 This long-standing definition from the 2005 International Pediatric Sepsis Consensus Conference (IPSCC) has been updated very recently, based on the new Phoenix criteria, but has not yet been translated into guidelines.2 3 25 million cases and 3.4 million deaths related to paediatric sepsis were reported in 2017 in a large international retrospective study where sepsis was identified according to medical diagnosis codes from death databases (‘sepsis’ or ‘infection’ and ‘organ failure’). Thus, sepsis remains the world’s leading cause of mortality in children under-5 years.4 Although fluid resuscitation was found to increase mortality in the only randomised clinical trial to date to assess it in children with severe febrile illness and impaired perfusion,5 it is one of the cornerstones of current paediatric septic shock management, in addition to early antimicrobial therapy.6 7 In 2020, the international guidelines of the Surviving Sepsis Campaign (SSC-2020) revised the management of septic shock and sepsis-associated organ dysfunction in children, with a particular attention to fluid resuscitation. In healthcare systems with availability of paediatric intensive care unit (PICU), fluid bolus of 10–20 mL/kg in case of abnormal perfusion or hypotension, up to 40–60 mL/kg over the first hour of septic shock recognition and preferably with balanced crystalloids were recommended.8 Despite the importance of these guidelines, to our knowledge, there is no study to date evaluating their application in paediatric emergency departments (PEDs).

    We conducted the Fluid Resuscitation for Suspected Septic shock in Paediatric Emergency Departments (FRESSPED) Study to assess physician adherence to the SSC-2020 fluid resuscitation guidelines in children with suspected septic shock in French PEDs.

    Methods

    FRESSPED was a prospective observational study conducted in 21 French PEDs during 5 sequential weeks between November 2021 and March 2022. The methodology was consistent with ethical standards, and this report follows the guidelines of the Strengthening the Reporting of Observational studies in Epidemiology statement.9 A registration on ClinicalTrials.gov database was performed prior to inclusion (NCT05066464).

    Population

    All children (<18 years) with suspected septic shock who received fluid resuscitation (at least 5 mL/kg within 1 hour) in participating PEDs during the 5-week inclusion period were eligible. Septic shock suspicion was defined according to the prescription of antimicrobial therapy within 72 hours and the presence of at least three of the eight criteria of the American Academy of Pediatrics (AAP) septic shock trigger tool (temperature abnormality, hypotension, tachycardia, tachypnoea, capillary refill abnormality, mental status abnormality, pulse abnormality, skin abnormality). Only two of these criteria were required in case of a high-risk condition (malignancy, asplenia including sickle cell disease, bone marrow or solid organ transplant, central or indwelling line/catheter, severe mental retardation or cerebral palsy, immunodeficiency or immunosuppression).10 Exclusion criteria were preterm infants under 39 weeks’ corrected age at screening time and children whose parents (or legal guardians) have expressed their objection to data collection.

    Children with ‘severe sepsis’ and ‘septic shock’ were in retrospect defined as meeting the 2005 IPSCC criteria.1 Septic shock recognition was defined as the moment when fluid resuscitation was prescribed at the end of the clinical examination that led to it.

    Outcomes

    Primary outcome was SSC-2020 fluid resuscitation guidelines adherence (low 0–24%; moderate 25–74%; high 75–100%) according to: (1) volume of 10–20 mL/kg for each bolus; (2) exclusive administration of balanced crystalloids at 1 hour and 24 hours of management; and (3) initiation of fluid resuscitation within 1 hour of septic shock recognition. Primary outcome was assessed independently for each of its three individual components and for each bolus (including within the same patient). SSC-2020 fluid resuscitation guidelines for healthcare systems with availability of intensive care were used as reference.

    Secondary outcome included: other key elements of fluid resuscitation (time to fluid resuscitation, volume of each bolus, prescribed and real bolus duration, number of bolus received at 1 hour, and total fluid bolus volume received at 1 hour and 24 hours); non-fluid management (time to clinical examination, time to antimicrobial therapy start, blood culture collection, oxygen therapy, lactate measurement, and peripheral venous and intraosseous accesses); and barriers to SSC-2020 fluid resuscitation guidelines adherence reported by physicians.

    Study protocol

    An invitation to participate in the study was sent by email to 26 French PEDs’ heads. FRESSPED was carried out in three successive stages. First, usual fluid resuscitation practices were assessed through the completion of paper case report forms (less than 5 min), within 72 hours of inclusion, by physicians of the participating centres caring for an eligible patient during the 5-week inclusion period. Second, patients were followed up during 1 month after inclusion (extending the study period to 28 April 2022) to investigate their outcomes by data collected in routine care (patient chart) by the principal investigator. Third, from May to June 2022, participating physicians responded to a short, anonymised online survey, blinded of centre outcomes, to explore the barriers to SSC-2020 fluid resuscitation guidelines adherence as well as their attitudes and knowledge.

    Data and statistics

    Paper case report forms were scanned and deposed on a secure online platform (HCP Anywhere) by local coordinating investigators. Then, data were collected, anonymised and entered in an electronic database (Microsoft Excel; Microsoft Corp) by the principal investigator. Data were analysed using descriptive statistics to evaluate the study population. Each score was calculated using the worst values observed during the period of interest. Qualitative variables are reported as numbers and percentages. Quantitative variables are reported as median with IQR and Agostino-Pearson test was used to assess distribution. Statistical analyses were performed using GraphPad Prism V.9.4.0 (GraphPad Software, California, USA).

    Results

    Patients’ characteristics

    Five centres rejected participation in the study either because of the workload involved or because of the rarity of septic shock in their centres. During the 5-week study period, 78 492 patients visited the 21 participating PEDs, of whom 86 (0.1%) were screened. 63 patients were included (figure 1) after exclusion of children who did not meet the AAP criteria (n=3) or who had not received antimicrobial therapy within 72 hours (n=16) or both (n=4). Characteristics of patients included are shown in table 1. 10 (16%) children had severe sepsis and 2 (3%) met the definition of septic shock (online supplemental table 1). An infectious organism was isolated in 47 (75%) patients. All viruses were isolated from nasopharyngeal swabs, while bacterial isolates came from various sources (urine cultures for n=13; peritoneal fluid samples for n=2; blood culture for n=1; urine and blood culture for n=1; tracheal aspirate for n=1; cerebrospinal fluid culture for n=1; stool culture for n=1) (table 2).

    Figure 1
    Figure 1

    Flow chart. AAP, American Academy of Pediatrics; PICU, paediatric intensive care unit.

    View this table:
    Table 1

    Baseline characteristics of children (n=63)

    View this table:
    Table 2

    Microbiological documentation (n=47*)

    Primary outcome

    Compared with the SSC-2020 guidelines, 43 (68%) patients received boluses of 10–20 mL/kg; fluid resuscitation was initiated within 1 hour of septic shock recognition in 42 (76%) cases; balanced crystalloids were the only fluid administrated in 35 (56%) and 34 (55%) children at 1 hour and 24 hours of management, respectively (table 3).

    View this table:
    Table 3

    Primary outcome and other key elements of septic shock management

    Secondary outcomes

    Other key elements of fluid resuscitation and non-fluid management are summarised in table 3. Median time to fluid resuscitation was 34 (12.3–61.5) min after septic shock recognition. Interestingly, antimicrobial therapy was initiated after fluid resuscitation with a median of 73 (40.0–145.0) min. No patient required renal replacement therapy, had persistent renal dysfunction at 28 days or died (table 3). 125 attending physicians from the 21 participating centres completed the online survey. Remarkably, only 65 (52%) reported being aware of the SSC-2020 guidelines. Reported barriers to SSC-2020 fluid resuscitation guidelines adherence are presented in figure 2.

    Figure 2
    Figure 2

    Barriers reported to Surviving Sepsis Campaign 2020 fluid resuscitation guidelines adherence.

    Discussion

    We sought to assess physician adherence to SSC-2020 fluid resuscitation guidelines in children with suspected septic shock in PEDs. Such adherence was high for fluid resuscitation initiation and moderate for bolus volume and fluid choice. Main barriers reported were difficult intravenous access, lack of team training, workload constraints and absence or out-of-date protocols. Despite these discrepancies, no patient died among the few cases of severe sepsis.

    The implementation of guidelines is an essential part of quality improvement process. One of the challenges facing emergency departments is whether guidelines should be implemented when a condition is suspected but not proven.11 Thus, this work focused on children with suspected septic shock, regardless of whether they had it. This population was selected because the problem of concern was the initial management in PEDs, where the clinician is not certain of septic shock. This initial management has a major prognostic impact, as recently highlighted in 259 French children.12 In addition, given the short inclusion period of the study (5 weeks), this population of interest allowed the inclusion of more patients (n=63) than only severe sepsis cases (n=10).

    Characteristics of patients included in the study differ from the literature, with a median age of 7.9 months (2.8–35.9), as well as a fewer rate of comorbid conditions (30%) and undocumented infections (23%).13 One explanation for this may be the winter inclusion period, where influenza outbreaks (22%) occurred in mostly healthy infants who frequently presented poorly tolerated fever and signs of abnormal perfusion but no septic shock. In addition, it is striking that only two children had positive blood cultures. Moreover, it is striking that bacteria were isolated from blood cultures in only two patients. In addition, imputability of viruses, identified in 44% of cases, is difficult to establish given their prevalence in healthy children and their frequent association with bacteria that are themselves responsible for septic shock.14 In addition, the included patients were not critically ill, with a total fluid resuscitation volume of 19.7 mL/kg (10.4–28.0) and a peak serum lactate of 2.8 mmol/L (2.0–4.0), as well as a median length of hospital stay of 5 (3–7) days.

    The FRESSPED Study is, to our knowledge, the first prospective multicentre study evaluating adherence to the SSC-2020 fluid resuscitation guidelines for suspected septic shock in PEDs. The 21 participating centres represent 24% of French PEDs of which 17% of academic medical centres in France. First, this adherence could be improved by implementing SSC-2020-based care protocols, especially as only 52% of physicians were aware of these guidelines in our study. Indeed, such protocols, including ‘bundles’ completion, have been associated with shorter time to recognition of septic shock, initiation of fluid resuscitation and antimicrobial therapy, as well as reduced organ dysfunction, length of hospital stay and mortality.15–17 Second, the creation of a teaching programme for health professionals would be of interest, as it has proven effective in increasing compliance with guidelines, especially as the lack of team training was reported by 29% of physicians.18 Time to antimicrobial therapy from septic shock recognition which was 73 min (40–145) in our study was not consistent with the 1-hour threshold of the SSC-2020 guidelines. Some authors have reported higher mortality with delayed antibiotic therapy beyond 1 hour in this setting19 and therefore such a teaching programme should emphasise early initiation of antimicrobial therapy. Finally, training in the placement of intraosseous catheters would reduce the difficulties of intravascular access that were reported in 43% of cases. Only 3% of children included benefited from an intraosseous line, which is yet recommended in case of peripheral venous cannulation failure and has shown a decrease in insertion time, length of hospital stay and mortality in relation to the latter.20 This can be explained by the low severity of the patients and by the large proportion (38%) of responding physicians who considered themselves not competent to perform it.

    The FRESSPED Study has several limitations. First, the SSC-2020 fluid resuscitation guidelines specifically apply to children with septic shock, as defined in the 2005 IPSCC,1 and other sepsis-associated acute organ dysfunction.8 In retrospect, most of the patients included did not fulfil these criteria, as only 10 (16%) and 2 (3%) of whom met the definition of severe sepsis and septic shock, respectively. Although inevitable if one is identifying children at risk of septic shock at an early stage of the condition, this major discrepancy between the population addressed by the SSC-2020 guidelines and that included in our study highlights the inaccuracy of the suspicion of septic shock according to the prescription of antimicrobial therapy within 72 hours and the AAP septic shock trigger tool.10 We can thus assume that the pressure to identify sepsis early in the illness led to fluid resuscitation in children who had not cardiovascular dysfunction requiring it. This is a serious issue since such an intervention can be harmful to children, as shown by the FEAST Study, even though the patients included in our study were different from those in the latter.5 Furthermore, this may explain the relatively low rate of adherence to the SSC-2020 guidelines, which may have been skewed by the low probability of septic shock in the least severe children, leading some physicians to deliberately not follow these recommendations. This finding is consistent with an observational study by Nijman et al in which, among children at risk of sepsis at PEDs, only 0.6% of whom developed a serious bacterial infection or were admitted to a PICU and only 0.2% complied with the 1-hour sepsis bundle of care. The authors conclude that early escalation of care for children with suspected sepsis at the PEDs could have adverse effects on the overall management.21 It is therefore necessary to better define the criteria for suspicion of septic shock in PEDs. Second, in the absence of consultation of local registries, some patients meeting the inclusion criteria may not have been included, although this risk was largely reduced by: (1) the short sequential inclusion period; (2) the multiple reminders sent to local investigators preceding the weeks of data collection; (3) a monthly newsletter; (4) the systematic check of all patients who received a fluid resuscitation at the end of each week of inclusions by the local investigator. Third, as physicians were not blinded, there is an inherent bias related to practice observation, limited by the unawareness of the SSC-2020 guidelines reported by half of them.22 Finally, although there were no missing data on the primary outcome, the small sample of the study (n=63) did not allow for comparative statistical analyses, particularly concerning the children outcomes according to compliance with guidelines.

    Conclusions

    FRESSPED Study aimed to assess physician adherence to the SSC-2020 fluid resuscitation guidelines in infants and children with suspected septic shock in PEDs. Such adherence was high for fluid resuscitation initiation and moderate for bolus volume and fluid choice. Our study highlights the need for a better definition of the suspicion of septic shock in PEDs, as well as the importance of both implementing SSC-2020-based care protocols and teaching programmes emphasising early antimicrobial therapy and intraosseous access training. Future studies could investigate compliance with these guidelines and children’s outcomes after such programmes.

    Data availability statement

    Data are available upon reasonable request.

    Ethics statements

    Patient consent for publication

    Ethics approval

    This study involves human participants and was approved by Robert-Debré University Hospital Ethical Review Board (no: 2021-545). Legal guardians' consent was obtained after individual oral and written information as the study involves critically ill children who are unable to give consent because of their age or the severity of their illness.

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    Supplementary materials

    • Supplementary Data

      This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

    Footnotes

    • Presented at This work was presented at the 2023 French Intensive Care Society International Congress.

    • Contributors JSG and SD conceptualised and designed the study and drafted the initial manuscript. JSG designed the data collection instruments and carried out the initial analyses. ML reviewed all medical files of children admitted to PICU and revised the manuscript. All authors collected data, critically reviewed the manuscript and gave their approval of the final version. JSG is the guarantor and accepts full responsibility for the conduct of the study, had access to the data, and controlled the decision to publish.

    • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

    • Competing interests None declared.

    • Provenance and peer review Not commissioned; externally peer reviewed.

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